AR NCMLS - Radboudumc

Annual Report 2013

NCMLSNijmegen Centre for Molecular Life Sciences (NCMLS)

Postal address259 RIMLSP.O. Box 91016500 HB NijmegenThe Netherlands

Visiting addressGeert Grooteplein 286525 GA Nijmegen

T: +31 (0)24 361 07 07E: [email protected]: www.rimls.nl

Design: Final Design

Nijm

egen Centre for Molecular Life Sciences

Annual Report 2013N

CMLS

The NCMLS seeks to achieve greater insightsinto the complexity of living cells with thepurpose of obtaining a multifaceted know-ledge of both normal and pathologicalprocesses. The NCMLS will pursue its goalsin the interests of curiosity driven researchand education. The NCMLS aims to advanceinnovation in translational research based onthe integration of diverse scientific exper-tise in molecular and medical sciences.

Nijmegen Centre for Molecular Life Sciences

Annual Report 2013 NCMLS

RIMLS

Postal address

259 RIMLS

P.O. Box 9101

6500 HB Nijmegen

The Netherlands

Visiting address

Geert Grooteplein 28

6525 GA Nijmegen

T: +31 (0)24 361 07 07

E: [email protected]

I: www.rimls.nl

Editing: René Bindels, Judith Burgers, Adrian Cohen


Front cover: The cover image depicts an artistic collection of photos of molecular life sciences

Photography: Theo Hafmans, Eric Scholten

Printed by: Rikken Print

2

It has been an extremelysuccessful year for NCMLSscientists. NCMLS resear-chers have acquired sub-stantial personal grantsfrom national (e.g. NWOVeni, Vidi, Vici), European(e.g. ERC Starting, Consoli-

3Annual Report 2013 Adrian Cohen and René Bindels Foreword

It has been an extremely successful year for NCMLS scientists. NCMLS researchers have acquired substantial personalgrants from national (e.g. NWO Veni, Vidi, Vici), European (e.g. ERC Starting, Consolidator, Advanced) and international(e.g. Bill & Melinda Gates Foundation) sources. Furthermore, numerous researchers have been effective in obtainingEuropean multi-partner subsidies either as co-ordinator or participant. This impressive success rate is thanks to theambition of our researchers, as well as the personal coaches that dedicate their time and energy into improving appli-cations and interview techniques. Our excellence was further illustrated by prestigious awards including royal acco-lades, KNAW and Academia Europaea memberships and various advisory board positions. Selected highlights as wellas top publications from our young researchers are presented in this report.

Training the new generation of researchers is one of our core tasks, and one that we do with pride. It takes substantialeffort to keep curricula up-to-date, implement new teaching methodologies and redesign old lectures. To all those thathelp teach and/or supervise students a deserving special thanks, especially the various members of NCMLS have beenawarded prizes for their teaching qualities.

The Executive Board of the Radboud university medical center recently took the decision to bundle all current UMCresearch into 19 research themes and to ‘house’ these themes in three institutes, namely: Radboud Institute forMolecular Life Sciences (RIMLS), Radboud Institute for Health Sciences and Donders Centre for Neuroscience (part of thelarger Donders Institute). The decision is based on the Radboudumc’s strategic vision to “have a significant impact onhealthcare” and to form high quality focused research lines from molecule-to-man-to-population (M-M-P).

Consequently, from early 2014 we will begin the exciting transition to new clinical- and methodological themes andimproved synergy with other local institutes. Our website will be amended accordingly and as usual will be kept up-to-date with all relevant news and events. An exciting year lies ahead.

For now, a look back to a successful 2013.

Prof. René BindelsScientific Director NCMLS

Dr. Adrian CohenScientific Manager NCMLS

Foreword

NCMLS4

Page

Foreword 3

Nijmegen Centre for Molecular Life Sciences 7-26Nijmegen Centre for Molecular Life Sciences 7-8

Mission 7Introduction 7Research and management organisation 8

NCMLS Research Themes 9-12Themes 1 and 2 9Themes 3 and 4 10Themes 5 and 6 11Theme 7 12

Facts & Figures 13NCMLS & Selected Awards 14-17NCMLS New Frontiers Symposium in Synthetic Life 18NCMLS Activities 2013-2014 20-21

Scientific Activities 22PhD retreat 22The Radboudumc Postdoc Initiative 22

Technology Platforms: from Molecule-2-Man 23

The NCMLS as Graduate School 24-26Introduction 24MSc Molecular Mechanisms of Disease 25International PhD programme 26

NCMLS Committees 27

Selected Research Highlights NCMLS 2013 29-48Theme 1: Infection & Inflammation 30-31Theme 2: Immune Regulation 32-34Theme 3: Regenerative Medicine & Microenvironment 35-36Theme 4: Energy & Redox Metabolism 37-39Theme 5: Membrane Transport & Cell Dynamics 40-42Theme 6: Genetic & Epigenetic Pathways of Disease 43-45Theme 7: Chemical & Physical Biology 46-48

NCMLS Members 49-52NCMLS Members Themes 1-3 50NCMLS Members Themes 4-6 51NCMLS Members Themes 7 52

Scientific publications 2013 53-96

5Annual Report 2013 Table of contents

Table of contents

NCMLS6

7Annual Report 2013 Nijmegen Centre for Molecular Life Sciences

Mission

Understanding the cellular basis of disease

The NCMLS seeks to achieve greater insights into the complexity of liv-ing cells with the purpose of obtaining a multifaceted knowledge ofboth normal and pathological processes. The NCMLS will pursue itsgoals in the interests of curiosity driven research and education. TheNCMLS aims to advance innovation in translational research based onthe integration of diverse scientific expertise in molecular and medicalsciences.

Introduction

The NCMLS was first established in 1994 under the name ‘Institute ofCellular Signalling (ICS)’, and subsequently in 1995 and again in 2000recognised by the Royal Netherlands Academy of Arts and Sciences(KNAW) as a research school. In 2000 the name Nijmegen Centre forMolecular Life Science (NCMLS) was coined, the NCMLS and ICS organi-sations were merged and placed under a collegial board of directors toreflect a further integration of Nijmegen research themes and the multi-disciplinary and translational research approach of the organisation.Approval for the new name and organisation was obtained during the2004 recognition-round by the KNAW and more recently in 2011. Theresearch school continues to represent a growing research staff, bothfrom the Radboud University Nijmegen Medical Centre (RUNMC) and theFaculty of Science, Mathematics and Computing Sciences (FNWI) at theRadboud University Nijmegen (RU).

The NCMLS is a leading multidisciplinary research school within thedomain of molecular mechanisms of disease and particularly in thefields of molecular medicine, cell biology and translational research.NCMLS aims to develop as a unique centre of excellence with innovativeapproaches to research and education. In order for the NCMLS to rank asone of the top European research institutes/Graduate school, a compet-itive research environment should be created where quality and excel-lence are foremost considerations. By offering researchers a stimulatingand challenging environment, NCMLS aims to foster talent and furtherincrease international visibility.

The major goal of the NCMLS is to generate basic knowledge in molecu-lar medical research and to translate this knowledge into clinical appli-cations, into the development of diagnostics and into the treatment ofpatients through translational research programmes. The multi-discipli-nary approach to research in molecular life science is reflected both inits research themes and in the Master’s and PhD programmes offered.As such, NCMLS provides a stimulating and challenging environment foryoung scientists to learn the vital skills necessary for an independentand productive career in science.

The NCMLS Graduate School operates a two-year Research Masters M.Scprogramme, ‘Molecular Mechanisms of Disease’, accredited by NVAO,the Dutch-Flemish accreditation organisation, which is a member of theEuropean Consortium for Accreditation (ECA). The NCMLS also runs anationally approved PhD research training programme which attracts anincreasing number of foreign students to the institute.

NCMLS researchers collaborate at local, national and international lev-els. The research school is allied with the Institute for Molecules andMaterials (IMM) and the Donders Institute for Brain, Cognition andBehaviour (DI-BCB), providing a solid platform for integrating the chem-ical synthesis, nanoscience and neuroscience with molecular life sci-ences. Furthermore, incorporating the Centre for Molecular andBiomolecular Informatics (CMBI) within the NCMLS has strengthenedthe multidisciplinary approach to solving biomedical research prob-lems. The NCMLS houses The Netherlands Bioinformatics Centre (NBIC)which aims to stimulate the development of bioinformatics in theNetherlands, further strengthening NCMLS links in bioinformatics. TheNCMLS also has associations with the Dutch Programme for TissueEngineering (DPTE) and the Netherlands Proteomics Centre. The NCMLScontributes to the Top-Institute Pharma and has several academic andindustrial partners in this context. In addition, the NCMLS is activelyinvolved in national programmes, such as the BioMedical Materials pro-gram (BMM), Centre for Societal Genomics (CSG), Center forTranslational and Molecular Medicine, Netherlands Genomics Initiative(NGI), and international multipartner programmes such as EU FP7.

The NCMLS seeks to achieve greater insights into the complexity of livingcells with the purpose of obtaining a multifaceted knowledge of both nor-mal and pathological processes. The NCMLS will pursue its goals in theinterests of curiosity driven research and education. The NCMLS aims toadvance innovation in translational research based on the integration ofdiverse scientific expertise in molecular and medical sciences.


8 Nijmegen Centre for Molecular Life Sciences NCMLS

Research and management organisation

Research and education are focused along seven research themes inkeeping with our mission towards ‘Understanding the cellular basis ofdisease’. NCMLS Principal Investigators are organised within thesethemes providing critical mass of expertise and a visible structure forthe institute on which to base science research and education policy.

The Scientific Director of the NCMLS institute, Prof. René Bindels, con-sults with the Dean of the Medical Faculty (Prof. Paul Smits) and theDean of the Science Faculty (Prof. Stan Gielen) during regular meetingsin which research and education policy is discussed in relation toRadboud University and its Medical Centre research strategies.

René Bindels is Professor of Physiology and Head of the Department ofPhysiology. He has won great accolades in the field of biomedicalresearch and education. In 2009 he received three international awards

for his ground-breaking research on calcium and magnesium ion trans-port mechanisms in the kidneys and intestines. In addition to being anexcellent researcher, René Bindels is an inspiring lecturer and super-visor. He is executive editor of the European Journal of Physiology and a member of the Academia Europaea. He represents the UniversityMedical Center in ZonMW TOP and NWO ALW-project committees and iswithin the University Medical Center chairman of various committees.

The NCMLS Management Team (MT) meets bi-weekly and is involvedwith all decisions and policy-making with respect to NCMLS researchand education activities. A number of committees are active in diverseareas such as supporting and guiding young researchers through grantapplications and organizing seminars from international top speakers.All committees report to the MT, directly or via the Scientific Manager.

The NCMLS seeks to achieve greater insights into the complexity of li-ving cells with the purpose of obtaining a multifaceted knowledge ofboth normal and pathological processes. The NCMLS will pursue itsgoals in the interests of curiosity driven research and education. TheNCMLS aims to advance innovation in translational research basedon the integration of diverse scientific expertise in molecular andmedical sciences.


Organogram of the NCMLS highlighting the NCMLS Management, the 2 year research Master’s program (MMD) and 4 year PhD training program. The various NCMLS supporting committees are not shown (see page 27).

Within the NCMLS institute, allresearch and education is linkedto the study of molecular life scien-ces in relation to disease. NCMLSfocuses on seven thematicresearch areas, each of which isheaded by a prominent NCMLS

9Annual Report 2013 NCMLS Research Themes

Research themes

Theme 1: Infection & Inflammation(Anna Simon)

Mission Statement: Our mission is to elucidate molecular mechanismsof infections, (auto)inflammatory and autoimmune diseases, and todevelop innovative tools for diagnostics, treatment, and prevention.

Keywords: Antimicrobial agents, autoimmunity, biomarkers, immuno-deficiencies, immunogenetics, infection, inflammation, innate immu-nity, microbial pathogenesis, vaccinology, vector biology.

This theme covers two important areas of biomedical research:■ Infectious diseases: The focus lies on the role of the innate immune

system in pathogen recognition and host defence (fungal, bacterialand viral infections), on pathogen-host interactions, vector biology,anti-microbial drugs and development of drug-resistance, vaccinedevelopment and the role of pathogens in the development of(chronic) inflammatory diseases.

■ Inflammatory diseases: The aim is to identify disease mechanismsthat encompass both the innate and adaptive immune system andthe identification of modifier genes and post-translational modifica-tions, including autoantigens, to explain tissue specificity of theseconditions such as rheumatoid arthritis, systemic sclerosis, goutyarthritis, psoriasis, and systemic lupus erythematosus.

Theme 2: Immune Regulation (Gosse Adema)

Mission Statement: Our mission is to increase the understanding ofthe molecules and regulatory circuits active in immune cells in healthand disease. We strive to translate fundamental findings to the bene-fit of patients suffering from cancer and immune related disordersthrough preclinical models and experimental immunotherapy in pa-tients.

Keywords: Cell adhesion and migration, dendritic cells, hemato-poiesis, imaging immune responses, immunotherapy, leukemia, mole-cular imaging, therapy resistance, transplantation, tumor microenvi-ronment, vaccination.

This theme covers immunological and haematological research in threemajor biomedical fields:■ Molecular and functional analysis of normal and malignant blood cell

development and immune control: The theme includes analysis ofdendritic cells, regulatory T-cells and natural killer cells and aims atdefining regulatory circuits effective in tolerance and immunity.

■ Immunotherapy of cancer: Development and clinical application ofvaccination and imaging strategies for solid and haematopoieticmalignancies and their microenvironment.

■ Organ transplantation: Development and clinical application of novelimmune monitoring and intervention approaches in kidney trans-plantation.

NCMLS Research Themes

Within the NCMLS institute, all research and education is linked to the study of molecular life sciences in relation to disease. NCMLS focuses on seventhematic research areas, each of which is headed by a prominent NCMLS Principal Investigator.

10 NCMLS Research Themes NCMLS

Theme 3: Regenerative Medicine & Microenvironment(Wout Feitz)

Mission Statement: To improve the quality of life of patients by under-standing cell-matrix interactions (microenvironment), and to apply theobtained knowledge for the regeneration of tissues/organs.

Keywords: Animal models, bioceramics, biocompatibility, biomaterials,bone, cancer invasion, cartilage, stem cells, chemokines, collagen,cytokines, devices, drug delivery, dynamic imaging, ethics, extracellularmatrix, fibrosis, glycans, glycobiology, glycosaminoglycans, growth fac-tors, kidney, microspheres, oral biology, polymers, regenerative medi-cine, scaffolds, skin, tissue engineering, urogenital organs, urology,wound healing.

This theme addresses two main topics:■ Regenerative medicine: In this theme tissue-engineered constructs,

based on extracellular matrix molecules, polymers and effector mole-cules, are designed and fabricated, and analysed in vitro and in vivo.Smart organ-specific bioscaffolds are prepared in such a way thatthey provide appropriate signals to the cells to proliferate, migrate ofdifferentiate. Focus is on ceramics, calcium phosphates, collagens,glycosaminoglycans and effector molecules (e.g. growth factors andcytokines). Emphasis is on a selected number of tissues, viz. carti-lage/bone, skin, kidney and blood vessels and urogenital organs.

■ Microenvironment in health and disease: In the subtheme focus is on collagens, glycosaminoglycans, matrix metalloproteinases and anumber of effector molecules (e.g. BMPs, TGF beta). The role of thesecomponents in cancers, nephropathies and degenerative cartilagediseases is studied in vitro as well as in vivo. Strategies to restorehomeostasis in deranged and disease-associated microenviron-ments are pursued, including the use of glycomimetics.

Theme 4: Energy & Redox Metabolism (Martijn Huijnen)

Mission Statement: We investigate biomolecular pathways of NADH andATP conversion in human health and disease. We study the systems rele-vant for mitochondrial medicine and apply newly acquired knowledgefor diagnosis and treatment.

Keywords: ATP, glycolysis, mitochondrial biogenesis, NAD(P)(H), oxida-tive phosphorylation, ROS.

This theme aims to improve our understanding of the principles of (bio-chemical) adaptation to energy and redox stress, in order to betterdefine 'healthy responses within the normal physiological range' andthe 'pathophysiological thresholds' for diseases whereby mitochondrialfunction or energy transfer pathways are compromised. As such thissubtheme strives to make a substantial contribution to the well-beingand treatment of mitochondrial disease patients and other conditions inwhich energy metabolism is compromised. Research is focused in threeareas.■ ‘Imaging’ of ATP/ADP/AMP and NAD(P)H concentration and fate with

existing and novel biosensor reporters;■ ‘Imaging’ of metabolite fate with MRS and MRI;■ The use of new strategies to follow mitochondrial shape and activity

as well as cellular metabolic state and viability. The integration of“4-D” imaging and simultaneous recording of the behaviour of smallmolecules and macromolecular assemblies and cellular organelles isan important challenge.





11Annual Report 2013 NCMLS Research Themes

Theme 5: Membrane Transport & Cell Dynamics(Joost Hoenderop)

Mission Statement: Our mission is to understand the molecular mecha-nisms of transport of water, solutes, drugs and metabolites in healthand disease to apply newly acquired knowledge for diagnosis and thera-pies of kidney diseases and beyond.

Keywords: ABC transporters, kidney, liver cysts, salt and water transport,transport physiology, TRP channels.

Membrane transporters are involved in a whole range of diseases inorgans such as brain, muscles, kidney, intestine, liver and bone. Theultimate aim of our subtheme is to provide a molecular basis to under-stand, diagnose and ultimately cure inherited and acquired diseases oftransport proteins, such as channelopathies. Transport proteins current-ly studied within this theme are sodium (or hydrogen) and potassiumATPases, aquaporin water channels, transient receptor potential chan-nels, organic anion and cation transporters, ATP-binding cassette (ABC)transporters and sodium cotransporters. Research integrates funda-mental and clinical studies conducted at the genetic (gene defects, poly-morphisms), molecular (transport and associated proteins), cellular(established model systems, isolated and transfected cells) and organ-ism (conditional) knockout models) level. In addition, our theme willdevelop and implement new tools to tackle the outlined scientific goalsincluding real-time imaging, large scale screening assays at the mRNAand protein level, application of small interference RNA libraries, condi-tional knockout models, bioinformatics and functional analysis at themolecular level.

Theme 6: Genetic & Epigenetic Pathways of Disease (Hans van Bokhoven)

Mission Statement: Our mission is to unravel the molecular basis of cellbehaviour that emanates from the genetic and epigenetic code con-tained in the nucleus in the context of health and disease. We combinefundamental and clinical research to unravel the molecular pathwaysand cellular processes in specific (hereditary) tumorgenic pathways andin normal and pathological conditions of development, in particular ofthe nervous system.

Keywords: Acute myeoloid leukemia, blindness, breast cancer, ChIP-seq, chromatin, cilia, ciliopathy, colorectal cancer, deafness, epigenetic,epigenome, exome, genetic, genome, genomic disorders, intellectualdisability, iPS, neurodevelopment, neurogenetic, next generationsequencing (NGS), oncogenetics, oncology, pluripotency, prostate can-cer, RNA-seq, sensory disorders, transcription regulation, Xenopus, X-inactivation.

We use state of the art biological and ‘omics approaches to elucidatemolecular pathways and cellular processes in normal and pathologicalconditions. To achieve our mission, we are engaged in technology devel-opment in fundamental research as well as in a diagnostic setting.Important lines of research focus on the molecular and cellular aspectsof tumorgenic pathways, development and function of the nervous sys-tem, and the basic mechanisms of transcription regulation, includingepigenetics. Molecular and cellular mechanisms are studied in the con-text of mammalian (stem) cells, yeast, parasites (plasmodium) and ver-tebrates: Xenopus, zebrafish, Drosophila, mouse and rat. Our geneticand epigenetic research has an immediate impact on diagnosis andprognosis of pathological conditions. Moreover, our fundamentalresearch uncovers new mechanisms and common pathways in thedevelopment of specific cellular structures (e.g. ciliogenesis, synaptoge-nesis) or cellular pathology (tumorgenesis, nerve cell degeneration).Such knowledge will provide new targets for therapeutic interventionthat can be studied in vitro, in animal models and ultimately in patients.

12 NCMLS Research Themes NCMLS

Theme 7: Chemical & Physical Biology(Jan van Hest)

Mission Statement: Theme 7 aims at exploiting molecular approaches tounderstand, follow and modulate biological processes in cells and organ-isms. This translates to new therapeutic and diagnostic approaches.

Keywords: Bio (chem)informatics/homology modeling, chemical modifi-cation and bioconjugation, complex molecular systems, microsystems/single molecule studies, post-translational modification, probes for ima-ging and targeting, signal transduction.

Structure and function of proteins and their complexes play crucial rolesin virtually all NCMLS research projects. ■ At the molecular level this subtheme aims at optimally exploiting the

potential of (bio)molecular chemistry to modify, design and mimicproteins and their building blocks with the purpose to modulate andanalyse their activities and properties in the (sub)cellular environ-ment. This is best illustrated by the following examples: (i) novel bio-orthogonal conjugation methods to study and interfere with biologi-cal processes; (ii) stimulus-responsive cell penetrating peptides; (iii)use of non-proteinogenic amino acids in diagnosis and treatment ofdisease; (iv) mimicking cellular synthetic processes in microenviron-ments; and (v) hybrid cell systems: incorporation of synthetic com-ponents into living cells.

■ At the cellular and multicellular level theme 7 deals with elucidation of protein structure and protein-protein interactions. Research topicsare: (i) post-transcriptional events in gene expression; (ii) cellularsignaling pathways; (iii) (de)activation mechanisms of tyrosinekinases and tyrosine phosphatases; (iv) external control of cellularproliferation and differentiation; and (v) molecular probing of vas-cular pathology and angiogenesis.

Within the NCMLS, all researchand education is linked to thestudy of molecular life sciences inrelation to disease. The centrefocuses on three thematic re-search areas, which are furtherdivided into sub-themes.


The scientific output of an insti-tute, measured in publications,prestigious awards, patent appli-cations etc, is an important meas-ure of the growth and perform-ance of the principal investigatorsforming the institute. Further-

Facts & Figures www.NCMLS.eu400,000 page-views70,000 unique visitors2 min average visit

13Annual Report 2013 Scientific Output

14 NCMLS & Selected Awards NCMLS

NCMLS Awards & grants

Best scientific report: Sarah Weischer (Dept. of Tumor Immunology),Blocking Aberrant Sialylation in Cancer Cells -A Sweet Way to AugmentAnti-Tumor Immunity.Best thesis: Jurjen Tel (Dept. of Tumor Immunology), Plasmacytoid den-dritic cells & immunotherapy of cancer.Breakthrough paper of the year: Ehsan Habibi (Dept. of Mol. Biology),Whole-Genome Bisulfite Sequencing of Two Distinct InterconvertibleDNA Methylomes of Mouse Embryonic Stem Cells. Cell Stem Cell, 13: 360-369, 2013.Best lecturers (PhD retreat): Joep de Ligt (Dept. of Human Genetics),Detecting de novo mutations in intellectual disability, and SabineKlischies (PhD student from IRB, Barcelona), The role of the γTuRC sub-unit GCP8 in cytoskeleton organization.Best poster (PhD retreat): Jorn Havinga (Dept. of Paediatrics): Functio-nal characterization of the role of IKZF family members in modulatingtherapy response in pediatric precursor B-all.

New Frontiers symposium poster awards: Ruud Peters (IMM, Nijmegen),Enzymatic cascade reactions in multicompartmentalised polymer-somes; Xin Huang (Univ. of Bristol), Interfacial assembly ofprotein–polymer nano-conjugates into stimulus-responsive biomimeticprotocells; Henrike Niederholtmeyer (EPF Lausanne), Implementationof cell-free biological networks at steady state.

Travel grant: Rocio Acuna (Dept. of Human Genetics), Jeroen de Baaij(Dept. of Physiology), Ellen van Bogaard (Dept. of Dermatology), ArthurKuiper (Dept. of Pediatrics) and Wieteke Hoeijmakers (Dept. of Mol.Biology).

Best PhD project proposals (4): Peter Friedl (Dept. of Cell Biology),P120 catenin as master regulator of microenvironment-dependentplasticity of cancer cell dissemination and metastasis; JoostHoenderop (Dept. of Physiology), The renal cell's antenna to regulateCa2+ transport; Joop Jansen (Dept. of Laboratory Medicine), GFI1B inmegakaryocyte and platelet biology; Jack Schalken (Dept. of Urology),Elongated primary transcription in prostate cancer.

NWO Graduate School PhD positions: Of the four positions available,one position was awarded in 2012 to Maria Victoria Luna Velez (Dept.of Urology). The remaining three positions were awarded to JakobGoldman (Dept. of Human Genetics), Three-dimensional genome archi-tecture and regulatory gene network during epidermal keratinocytedifferentiation; Anoek van Rijn (Dept. of Tumor Immunology), Deciphe-ring dendritic cell lymph node homing; Susan Schuster (Dept. ofMedical Microbiology), The role of RNAi in Dengue virus infections inmammals.

The Veni, Vidi and Vici grants areawarded by the NWO as part of the‘Vernieuwingsimpuls’ (Renewalimpulse) and is supported by theMinistry of Science, Educationand Culture (OCW), and the RoyalAcademy of Sciences and the Arts

NCMLS & Selected Awards



15Annual Report 2013 NCMLS & Selected Awards

Selected Coordination grants 2013

■ A consortium led by Jack Neefjes (NKI, Amsterdam) involving CarlFigdor (Dept. of Tumor Immunology) has been awarded € 27.6Million NWO ‘Gravitation’ Grant to initiate the Institute for ChemicalImmunology (ICI). The 10-year project allows internationally topexperts in chemistry and immunology to join forces to define a novelfield of chemistry-driven immune intervention. Specifically they willtrain a novel generation of multidisciplinary scientists to create newsolutions for human healthcare interventions.

■ Gert-Jan Veenstra (Dept. of Molecular Developmental Biology) toge-ther with computational biologist Simon van Heeringen, from thesame department, and international colleagues received a € 4Million European grant to set-up a training network on Develop-mental and Computational Biology (DevCom). DevCom aims to elu-cidate embryonic gene regulatory and developmental networks,including those associated with disease, by integrating molecular-,developmental-, statistical- and computational approaches.

■ Egbert Oosterwijk (Dept. of Urology), has been awarded a Marie CurieInitial Training Network (ITN) grant of € 3.6 Million to develop novelmaterials for tissue engineering and regenerative medicine. Thenetwork aims to develop new materials and implants for the bio-engineering of soft tissue (skin, urogenital) and hard (bone) tissueas well as state-of-the-art novel multimodality visualization proce-dures to monitor the behaviour of implants.

■ The Dutch Kidney Foundation awarded € 1.25 Million to the Dutchconsortium PROCARE. The project, coordinated by H. Otten (UU) in-volves two scientists from Radboud, namely Irma Joosten and LuukHilbrands. PROCARE is an unique cooperation between laboratoryspecialists and nephrologists from all Dutch transplantation cen-tres. The joint effort will produce innovative insights by linking theclinical outcome of 5,400 transplantations to the results of moderntechniques to measure the allo-response.

European Research Council (ERC) Awards

■ Henk Stunnenberg (Dept. of Molecular Biology) has been awardedan ERC Advanced Grant of € 2.5 Million for his project SysStemCell.SysStemCell aims to dissect regulatory transcriptional networksorchestrating mouse pluripotent embryonic stem cells (ESC). State-of-the-art functional (epi)genomics and proteomics techniques willbe used to yield invaluable insights into pluripotency and self-renewal of ESCs, but also into the molecular mechanisms drivingmouse early embryonic development.

■ Peter Friedl (Dept. of Cell Biology) has been awarded an ERC Consoli-dator Grant of € 2 Million to study tumor biology in live animal mo-dels using the novel technology of multiphoton microendoscopy.Together with project partners LaVision Biotec/Bielefeld andGintech/Jena, he will develop new tools to allow "optical biopsy" oftumors. This device will then be used to map cancer progression,metastatic evasion and therapy response.

■ Ronald van Rij (Dept. of Medical Microbiology) has been awarded an ERC Consolidator Grant of € 2 Million. Mosquitoes transmit impor-tant viruses, such as Dengue virus and West Nile virus. The antiviralimmune system of the mosquito is a critical determinant for virustransmission. In this project, the biogenesis, mechanism and func-tion of small RNA-mediated antiviral defense will be analyzed.

■ Geert van den Bogaart, (Dept. of Tumor Immunology), was success-ful in obtaining an ERC starting grant of € 1.5 Million to uncover newmechanisms of membrane organization.

■ Mangala Srinivas, (Dept. of Tumor Immunology), was successful in obtaining an ERC starting grant of € 1.2 Million to develop novelimaging agents for multimodal clinical and preclinical and clinicalimaging, with a focus on in vivo cell tracking

16 NCMLS & Selected Awards NCMLS

Veni, Vidi & Vici Awards

■ Jolanda de Vries (Dept. of Tumor Immunology) has been awarded aNWO Vici grant of 1,5 M Euro for the development of natural dendrit-ic cell vaccines to combat and prevent cancer.

■ Four experienced researchers have been awarded prestigious NWO-Vidi grants, each € 800.000, to develop their own innovative linesof research: (1) Leonie Kamminga, Epigenetic regulation of cellularidentity (Dept. of Molecular Biology), (2) Dirk Lefeber, Unraveling aunique sugar layer in human brain and muscle (Dept. of Neurology),(3) Hendrik Marks, Understanding embryonic stem cells (Dept. ofMolecular Biology) and (4) Klaas Mulder, Understanding how geneswork together (Dept. of Molecular Developmental Biology).

■ Five young researchers have each received a Veni grant of 250,000Euro from the Netherlands Organization for Scientific Research(NWO): (1) Nina Hubner, The railway network of our cells (Dept. ofMolecular Biology), (2) Christian Gilissen, Understanding diffe-rences in DNA (Dept. of Human Genetics), (3) Jurjen Tel, Systemsimmunology at the single cell level (Dept. of Tumor Immunology), (4)Cindy Dieteren, Features of an immunological serial killer (Dept. ofCell Biology), and (5) Jenny van der Wijst, An ion channel andenzyme inextricably linked (Dept. of Physiology).

Selected personal grants 2013

■ Robert Sauerwein (Dept. of Medical Microbiology) has received apersonal grant of $ 3.4 Million from the Bill & Melinda GatesFoundation to further the development of a malaria vaccine. Theaward is to continue clinical investigation of the vaccine based onresults published in top journals such as the New England Journal ofMedicine, The Lancet and PNAS.

■ Bé Wieringa and Rick Wansink (Dept. of Cell Biology) have been awarded a € 675,000 NWO-ZONMW TOP Grant for their proposalentitled Myotonic dystrophy: Disease of imbalance in proteostasisand cell stasis?

■ Bert de Vries, Joris Veltman and Annette Schenck (Dept. HumanGenetics) have been awarded a € 675,000 NWO-ZONMW TOP Grantto provide novel insights into genetic control of cognition andimprove diagnosis, personalized patient support and treatment.

■ Stanleyson Hato (Dept. of Tumor Immunology) received the BasMulder Award of € 620,000 to perform research to improve tumorimmune-therapy.

■ Gosse Adema en Martijn den Brok (Dept. of Tumor Immunology)have been awarded a € 560,000 KWF Grant for their projectSaponin-based adjuvants in anti-tumor immunity: a role for lipidbodies in adjuvanticity?

■ Jack Schalken and Gerald Verhaegh (Dept. of Urology) have receiveda € 500,000 STW subsidy for the development of a new therapyagainst prostate cancer.





17Annual Report 2013 NCMLS & Selected Awards

■ Roland Brock (Dept. of Biochemistry) and Peter Friedl (Dept. of CellBiology), together with international colleagues, received a €448,000 instrument grant (NWO middelgroot) for a new state-of-the-art confocal microscope.

■ A grant of € 437,000 was awarded by KiKa (Kinderen Kankervrij) toLaurens van der Meer (Dept. of Pediatrics) and colleagues to studythe molecular pathways involved in the clearance of the proteindrug Asparaginase (ASNase), a key component of the multi-drugtherapy regimen that is used to treat acute lymphoblastic leukemiain children.

■ Gosse Adema, Michiel Kroesen (Dept. of Tumor Immunology) andPeter Hoogerbrugge (Dept. of Paediatrics) were awarded a €430,000 Villa Joep Grant to study and improve immunotherapy aspart of multimodal therapy using a novel pre-clinical MYCN-neurob-lastoma tumor model in mice.

■ William Leenders (Dept. of Pathology) received a grant of €330,000 as a partner in the FP7 project COSMOPhos nano: Novel nano-technology-enabled system for endovascular in vivo near-infraredfluorescence molecular imaging and endovascular near-infrared targeted photodynamic therapy of atherosclerotic heart disease.

■ Theun de Groot (Dept. of Physiology) has been awarded with a MarieCurie grant (€ 270,000) and a Niels Stensen Fellowship to identifynovel susceptibility genes for the development of lithium-inducednephrogenic diabetes insipidus, hypercalcaemia and chronic kid-ney disease.

■ Marjolijn Ligtenberg, Marjolijn Jongmans and Richarda de Voer(Dept. of Human Genetics) have received a MLDS Focus project grant(€ 240,000) from the Dutch Maag Lever Darm Stichting. Their pro-ject is entitled: Unraveling the Genetic Background of ColorectalCancer in Adolescents and Young Adults.

■ Frans Cremers (Dept. of Human Genetics) has received a prestigiousresearch grant ($ 300,000) for 3 years from the Macula VisionResearch Foundation (MVRF).

■ Dirk Lefeber (Dept. of Neurology) and Ewa Swiezewska (Institute ofBiochemistry and Biophysics, Polish Academy of Sciences) havereceived a cooperative framework grant of the Polish Academy ofSciences of € 240,000 to investigate novel metabolic steps in thisprotein N-glycosylation

■ Merel Adjobo-Hermans from the Department of Biochemistry hasbeen awarded an E-Rare-2 grant (€ 250,000) to dissecting themolecular pathophysiology of Chorea-Acanthocytosis.

■ Sonja Buschow and Carl Figdor from the department of Tumor Immunology have received a NWO open programme grant (€250,000) for their research project entitled: Galectin-9: a novelmembrane organizer that regulates phagocytic receptors.

■ Leonie Kamminga (Dept. of Molecular Biology) has been awarded an NWO MEERVOUD Grant (€ 224,567) for her work on epigenetic con-trol of fertility. MEERVOUD is the Dutch acronym for More WomenResearchers as University Lecturers. The aim of this programme is toencourage the appointment of more women to assistant professor-ships.

18 NCMLS

Selected Awards & Honours 2013

■ To acknowledge their efforts for medical research, Her Majesty ho-nored René Bindels (Dept. of Physiology) and Han Brunner (Dept. ofHuman Genetics) with the highly prestigious Knight of the Order ofthe Dutch Lion.

■ The Royal Netherlands Academy for Arts and Sciences (KNAW) haselected new members, including Han Brunner (Dept. of HumanGenetics).

■ Jan Smeitink, (Dept. of Pediatrics) is elected as a member of the prestigious Academia Europaea.

■ Frances Ashcroft, professor at the University of Oxford and interna-tionally renowned researcher in Physiology, received an honorarydoctorate from Radboud University Nijmegen on the occasion of theninetieth anniversary of the university.

■ Frans Russel (Dept. of Pharmacology and Toxicology) has beenappointed by the Minister for Health, Welfare and Sport as memberof the Dutch Medicines Evaluation Board (MEB) for a four-year term.

■ Joost Drenth (Dept. of Gastroenterology) has been elected as thenew chairman of the National Society Committee of the UnitedEuropean Gastroenterology Federation (UEG).

■ Bé Wieringa (Dept. of Cell Biology) received two prestigious awardsfor his scientific achievements and lifetime commitment forMyotonic Dystroph (DM), a severe neuromuscular repeat expansiondisease.

■ Mihai Netea (Dept. of Internal Medicine) received the 2013 Awardfor Excellence in Clinical Research of the European Society forClinical Investigation.

■ Hans van Bokhoven and Arjan de Brouwer (Dept. of Human Gene-tics), received the Radboud Science Award 2013. The award hasbeen created by "het Wetenschapsknooppunt" Radboud Universityto allow researchers to translate their research into learning andteaching materials suitable for primary school pupils.

■ Jan van Hest (IMM) won the Radboud senior lecturer award andIneke van der Zee (Dept. of Cell Biology) was nominated for Teacherof the Year.

■ Prof. Joris Veltman (Dept. of Human Genetics) received the ZonMw‘Parel’ (pearl) for his outstanding research on human genomic disor-ders and genomic architecture.

Appointments

■ Joris Veltman (Dept. of Human Genetics) has been appointed fullprofessor.



The New Frontiers in Nobel Chan-nels symposium, held on the 14thand 15th of November 2011,focused on ion channels and theirimportance in biology and medi-cine. In the highly regulated envi-ronment of a cell, 'ion channels'

NCMLS New Frontiers Symposium in Synthetic Life

19Annual Report 2013 NCMLS New Frontiers Symposium in Synthetic Life

Bridging the subjects of chemistry and biology, the 7th NCMLS NewFrontiers symposium, entitled Synthetic Life, explored the use of chem-ical technologies to understand complex biological systems, in particu-lar evolution, synthetic genetic and cellular systems.

The first session, aptly named, 'Evolution of life' explored efforts tounderstand the chemistry that led to the emergence of the first livingsystem. Philipp Holliger (UK) presented recent progress on the develop-ment and application of strategies to enable the enzymatic synthesisand reverse transcription (and thus replication and evolution) of novelsynthetic genetic polymers, termed XNA's. Strikingly information stor-age is not limited to just DNA and RNA. What was the first genetic poly-mer of life? and how did proteins evolve function? were the main ques-tions explored by John Chaput (USA). William Shih (USA) continued bydiscussing customized 3D DNA nanostructures and their potential med-ical applications. Cees Dekker (NL) closed the session with his insightsinto bacterial shape and cellular division. Alexander van Oudenaarden(NL) opened the second session focusing on how microRNA's conferrobustness in biological processes. Joachim Spatz (DE) discussed thecollective migration dynamics of epithelial cells and the implicationsduring wound healing, embryonic development and oncogenesis. Thefirst day of the symposium ended with inspiring keynote lecture byCarolyn Bertozzi (USA) focusing on bio-orthogonal chemistries.

The opening session on day 2, 'Bioengineering', focused on the excitingemerging area of microfluidic tools for single cell genomics (StephenQuake, USA). Continuing the nanotechnology theme, Donald Ingber(USA) presented an awe-inspiring lecture on his work developing'organs on a chip' and the ongoing efforts to combine 10 different organchips to create a 'human body on a chip'. Frank Baaijens (NL) and CarlFigdor (NL) presented their work on cardiovascular tissue engineeringand the development of synthetic dendritic cells, respectively. The finalsession, 'Synthetic life' was opened by Albert Libchaber (USA) on theminimum genetic requirements for a self-reproducing cell. This was fol-lowed by Daniel Gibson (USA) who described the recent promisingefforts in the Craig Venter Institute for building a synthetic cell capableof self-reproducing. Finally, Wilhelm Huck (NL) and Sven Vogel (DE) pre-sented their work on the creation of artificial cell-like environments inpicolitre droplets for studying the basic physical chemistry of the celland the intelligent design of minimal in vitro systems for studying actin-myosin-membrane interactions, respectively.

The symposium was a huge success and paves the way for our eighth'New Frontiers' symposium on regenerative medicine (page 21).

Bloemendal medal 2013

The Hans Bloemendal Medal for 2013 is awarded to Professor CarolynBertozzi, in recognition of her groundbreaking studies spanning the dis-ciplines of chemistry and biology. Carolyn Bertozzi is an internationallywell-respected expert in glycans, and one of the pioneering scientists inthe area of chemical biology. Her lab focuses on profiling changes in cellsurface glycosylation associated with disease, and exploiting this infor-mation for development of diagnostic and therapeutic approaches. In alandmark paper in PNAS (2007) she developed copper-free click chem-istry for dynamic imaging and then went on to further develop the tech-nique for in vivo imaging of glycosylation in zebrafish (Science, 2008)and in mice (PNAS, 2010). This innovative approach uses bio-orthogonallaboratory-developed reagents that do not react with the normal mole-cules in the body, and thus do not interfere with the sugars' ability tocarry out their normal signaling functions. Her work suggests that thistechnique could potentially be used to attach tracers to diseased cells. Inaddition to the diagnosis and treatment of disease, the techniques devel-oped by Bertozzi also are being used in her laboratory to construct bio-compatible materials, such as artificial bone and cartilage, with applica-tions in medicine and in materials science. These findings hold greatpromise for the future of medicine and personalized healthcare.

Carolyn Bertozzi's enthusiasm for her research is matched by her talentfor communicating science. She is an elected member of the NationalAcademy of Sciences, the American Academy of Arts and Sciences andthe Institute of Medicine. Including the Lemelson-MIT Prize, dubbed the'Oscar for inventors', she has nearly 50 accolades to her name. She haspublished more than 450 papers, which have been cited nearly than20,000 times (current H-index 70).

20 NCMLS Activities 2013 NCMLS

The NCMLS seeks to achieve grea-ter insights into the complexity ofliving cells with the purpose ofobtaining a multifaceted know-ledge of both normal and patho-logical processes. The NCMLS willpursue its goals in the interests of

NCMLS Activities 2013

The NCMLS seeks to achieve grea-ter insights into the complexity ofliving cells with the purpose ofobtaining a multifaceted know-ledge of both normal and patho-logical processes. The NCMLS willpursue its goals in the interests of

RIMLS Activities 2014

21Annual Report 2013 RIMLS Activities 2014

22 Scientific Activities NCMLS

PhD retreat

On Thursday 16th and Friday 17th of May, the 19th annual PhD retreatwas organized at the Hof van Wageningen, not just for the NCMLS stu-dents, but in a boost to our institute internationalisation, together withselected students from the Institute for Research in Biomedicine(Barcelona, Spain).Bert van der Reijden, chairman of the PhD Program Committee, openedthe program on Thursday with an update on the current status of the pro-gram. During the retreat, fourth-year students from the NCMLS present-ed their data in oral presentations, interspersed with presentations fromsome of the IRB students, highlighting the great diversity in the projectswe work on. All other participants were able to show their work in organ-ized poster-walks, which resulted in great discussions. Thursday lateafternoon arrived and it was time for some relaxation with a well-attended Pubquiz in café 'De Dokter' in the centre of Wageningen anddinner at the Hof van Wageningen afterwards. Hans Clevers, president ofthe Koninklijke Nederlandse Academie voor de Wetenschappen (KNAW),was the invited key-note speaker for the evening program, which wasalso attended by Prof. René Bindels, Scientific Director NCMLS. HansClevers treated us with a fantastic presentation on stem cells in thecrypts of the intestinal tract and their work on the formation oforganoids to regenerate intestinal tissue, followed by a lively discus-sion. During the closing session, the best oral presentation and posterpresentation were awarded. The PhD retreat was highly rated by its par-ticipants and the organization is looking forward to the 20th in May2014.

As part of an exchange between the NCMLS and the Institute forResearch in Biomedicine (IRB) in Barcelona, seven NCMLS PhD students

went to Barcelona to participate in their PhD Student Symposium, 'Theclock of life', focusing on the molecular mechanisms of aging. The sym-posium, held on the 14th and 15th of November, brought together 200young scientists from 17 countries. Senior guest speakers from top uni-versities such as Princeton, Oxford, and Cambridge presented theirinspiring work. In between, young scientists had the opportunity topresent their work to the international audience. By means of oral pre-sentations and posters also the NCMLS' research was promoted. Thecombination of the fundamental research performed at the IRB and themore clinically orientated research performed at NCMLS led to fruitfuldiscussions. The great science on offer and Catalan hospitality madethis exchange a great success.

The Radboudumc Postdoc Initiative

How can I get in contact with coworkers in- and outside my field? Howcan I improve my chances at being successful at the Radboudumc andbeyond? The Radboudumc Postdoc Initiative (RPI) provides a platformfor these issues for final year PhD students, postdocs, and clinicians,and actively lobbies to develop a postdoc career policy within theRadboudumc. The RPI hosts a website(www.radboudpostdocinitiative.nl) disseminating funding opportunitiesand provides a newsletter for updates on events. One such event is theRPI postdoc retreat, last organized in 2012 and entitled “A survival kitfor UMC Postdocs”. In addition the RPI organizes a series of lunch sem-inars, which feature invited speakers on various topics important to apostdoctoral career such as communication, career development, trans-ferable skills, and postdoc policy. In 2013 the RPI organized 4 seminars,with topics “Sell yourself” (Carl Figdor and Didi Braat), “(Social) Mediause in research and patient care” (Mariska Boshoven, Maroeska Rovers,Hanneke Kalf), “Perspectives on the future of personalized healthcare”(Paul Smits, Joris Veltman, Lia Fluit), and “Science and Society: thequest for the missing link” (Simone van der Burg). Stay posted for newRPI lunch seminars and the next retreat athttp://www.radboudpostdocinitiative.nl, and join us at LinkedIn.

The annual NCMLS PhD Retreatwas held at Hof van Wageningen,Wageningen on Thursday 14thand Friday 15th of April. This 17thedition of the retreat was a greatsuccess. Traditionally, all the lastyear PhD students give an oral

Scientific Activities

The unique research setting of theNCMLS - access to an extensiveknowledge infrastructure all with-in walking distance - allowsNCMLS to integrate diverseexpertise in the medical domainwith the ultimate goal of under-

Technology Platforms: from Molecule-2-Man

23Annual Report 2013 Technology Platforms: from Molecule-2-Man

Technology platforms: from molecule-2-man

Animal modelsThe NCMLS has excellent links to the Central Animal Facility (CDL) forexpert advice and access to facilities for animal testing. NCMLS has sev-eral disease-related animal models available, for example, for arthritis,cancer, kidney disease, tissue engineering, heart transplantation, neu-ral disorders, metabolic disorders, osteoporosis, haematopoiesis, fun-gal and bacterial septicaemia and malaria (P. falciparum).

BiobankThe Radboud Biobank, launched in 2012, aims to create an infrastructurefor the collection, storage and delivery of biomaterial and associated cli-nical data. The String of Pearls Institute (PSI) standards were used for thispurpose. It is expected that this infrastructure will facilitate biomedicalresearch enormously, and will ultimately result in better care and betterhealth for patients. With the continuation of existing collections and thecreation of new collections, the Radboud Biobank establishes a profes-sional and sustainable collation of a wide variety of biomaterialsobtained from well characterized patient groups.

BioinformaticsThe CMBI is the Dutch national centre for computational molecular scien-ces and is housed on the groundfloor of the NCMLS research tower. Theinstitute pursues a rigorous research programme with topics rangingfrom computational smallmolecule chemistry to protein function predic-tion and the complete metabolism of a cell. The Centre's facilities, data-bases and software packages are available to external scientists andthere is a helpdesk for scientists who use the service facility. Currently,the CMBI is primarily involved in bioinformatics research and in main-taining a data and software infrastructure to help scientists improvebioinformatics and/or computational small-molecule research.

Flow CytometryThe flow cytometry facility is part of the Laboratory of Hematology, Dept.of Laboratory Medicine at the RUNMC. Flow cytometry is a sophisticatedtechnique of single cell analysis simultaneously measuring andanalysing multiple physical characteristics of cells. State-of-the-artequipment available include 2 Beckman-Coulter analyzers, a BeckmanCoulter and a Becton Dickinson sorter.

GenomicsDNA sequencing and micro-array technology for gene expression profil-ing are rapidly becoming standard everyday laboratory tools. TheMicroarray Facility Nijmegen is one of the core facilities of the RUNMC.

The Dept. of Human Genetics also harbours a sequencing facility and agenotyping facility. The facility focuses on multiple applications such asexpression profiling, genomic copy number profiling (array CGH) andhigh density SNP profiling. Next-generation Genome Sequencers (Roche 454 FLX Titanium and Solexa) are operational in the Depts. of HumanGenetics and Molecular Biology.

GlycobiologyThe Nijmegen Glycobiology Platform (NGP) covers a diverse range ofglycobiological research from chemistry, biology to genetics and patientcare. The NGP serves as a platform to facilitate access to relevant re-search infrastructure and knowledge with a focus on human pathology.

Molecular imagingImaging at the cellular and subcellular level is an essential tool formolecular life scientists. The Microscopic Imaging Centre (MIC) at theNCMLS is a state-of-the-art facility for imaging of biological specimensutilizing light microscopy (bright-field, confocal and fluorescence), con-ventional scanning and transmission electron microscopy, and sophisti-cated digital imaging. The facility is available for researchers within andoutside the NCMLS. NCMLS also offers access to other techniques suchas, Atomic Force Microscopy, Flow cytometry, FRET and FRAP.

PRIMEPrime is the Preclinical Imaging Centre of RUNMC. This centre has state-of-the-art equipment for small animal imaging: MRI (7 Tesla, 11.7 Tesla),PET/ CT, SPECT/CT, bioluminescence imaging and in vivo multi-photonmicroscopy.

ProteomicsThe growing availability of genomic sequence information, together withimprovements in protein characterization by mass spectrometry, greatlyfacilitates protein research. The Radboud Proteomics Centre (NPC) wasestablished in 2004 to exploit these opportunities. Equipment availableincludes 2D-electrophoresis, SELDI-TOF and Mass spectrometry (MALDI-TOF, MALDI-LTQ and nano-LC LTQ-FT MS).

Translational research and cellular therapyA Good Manufacturing Practice (GMP) facility with clean rooms is usedfor translational research e.g. immunotherapeutic cell therapy and stemcell transplantation.

24 The NCMLS as Graduate School NCMLS

Introduction

NCMLS is a leading graduate school where students follow a tailor-maderesearch programmes shoulder to shoulder with professionals. NCMLSgraduate school offers career possibilities at all levels, from Masters’students to PhD and beyond in the form of post-doctoral research posi-tions and tenure-track positions.

The regulation of cellular processes is crucial for human development,and maintenance of health throughout life. It is clear that cellular mal-function affects common multi-factorial diseases such as diabetes,immune and inflammatory disorders, renal disease, cardiovascular,metabolic and neurodegenerative diseases as well as obesity and cer-tain forms of cancer. In the fight against such diseases, the NCMLSGraduate School – which is part of Radboud University Nijmegen andRadboud University Nijmegen Medical Centre – plays a key role. A majorgoal of the NCMLS is to translate basic knowledge generated from bio-medical research into clinical application, in order to improve diagnos-tics and develop new treatments.

All MSc and PhD students are registered junior members of the researchschool and have the corresponding responsibilities and privileges.

Excellent career prospectsThere is considerable demand for specialists in fundamental molecularbiology and cell biology as well as in its application to the treatment ofdiseases such as cancer, autoimmune and inflammatory disorders, andmetabolic and neurodegenerative disorders.

Our Research Master’s MSc training enables students to move rapidlyinto an international PhD programme, giving them a more mature per-spective and a broader range of experimental approaches than is possi-ble within standard MSc programmes. They are also prepared for furthertraining as a PhD-level researcher. Graduates are exempted from certainelements of the NCMLS PhD programme. For example, the graduatecourse is taught during the MSc phase and the main practical projectcan be incorporated into a PhD project.

Education is focussed is on the domain of molecular life sciences relat-ed to disease and in particular in three main fields related to molecularmedicine, cell biology and translational research. Programmes arealigned along the seven research themes.

Tailor-made tuition Students are guided throughout the practical training period by a super-visor and throughout the entire programme by a mentor, who stimulatesthem to explore your abilities and develop general research competen-cies, including reflection. Together with these coaches, students drawup a personal training and supervision plan. Such a broad and interdis-ciplinary approach to research is particularly important in the interna-tional scientific arena.

The Nijmegen Centre for Molecu-lar Life Science (NCMLS) is theleading graduate school wherestudents follow a tailor-maderesearch programmes shoulder toshoulder with professionals.NCMLS graduate school offers

The NCMLS as Graduate School

Figure showing the career development from Bachelor to senior researcher level.Highlighted is the role of the NCMLS Graduate School. Throughout their career progres-sion, students are encouraged to write and obtain subsides as well as gain experiencein other (inter)national research laboratories (latter not shown).



25Annual Report 2013 The NCMLS as Graduate School

MSc Molecular Mechanisms of Disease

The NCMLS offers a high quality Masters programme in MolecularMechanisms of Disease (MMD), which is taught by top researchers andclinicians.

A unique and challenging programmeThis groundbreaking programme translates disease related basicresearch in cellular and molecular biology into clinical experimentalresearch in patients. Designed to meet the needs of talented studentswith the drive, motivation and ambition to push forward their scientificcareers, it represents a unique opportunity to develop a research projectand build up an international research network.

This competitive programme provides a sound balance of theory andpractice. We enroll just 24 students per year, each of whom is allocateda personal mentor. The selection of top students from all over the worldresults in an ambitious, highly motivated group of students in an inter-national atmosphere. The programme is intensive, but stimulating, withplenty of room for discussion and interaction. This selective approachguarantees excellence, especially during the research training periods.The programme offers a focused combination of didactic and practicalcomponents suited to optimally synthesize current discoveries, concep-tual breakthroughs and technological advancement – mandatory for theeffective education of the new vanguard of multidisciplinary investiga-tors. Currently, 40 students from 15 countries are enrolled in the pro-gramme.

The MSc programmeThe 2-year Master’s programme, which starts each September, is modu-lar in structure and organised along three educational themes whichbundle the areas of research of the NCMLS:■ Infection, immunity and regenerative medicine ■ Metabolism, transport and motion■ Cell growth and differentiation

Theoretical CoursesFor each theme, one 4-week long module focuses on the core fundamen-tal and translational research aspects of the field. These courses providea solid basis of theoretical knowledge and expose students to transla-tional research, which links basic science and the treatment of disease.

One of the highlights of the programme is a series of Master classes,which are given by leading authorities from renowned internationalinstitutes. These offer valuable insights both within and beyond the spe-cific educational themes, explaining the current state of the art in impor-tant scientific areas.

The programme trains students not only in theoretical knowledge, but isalso focused on important scientific skills such as academic writing, giv-ing scientific presentations and writing grant applications. These skillsoffer our students head start in their scientific career.

Research training periodsThe practical research skills are further developed in the two researchtraining periods. The first research training is performed in the NCMLS.In the second year, students perform an international internship atrenowned institutes which is concluded with a thesis.

Table 1: Courses and study load of the Master’s programme Molecular Mecha-

nisms of Disease (1 EC = 28 hours of study, total programme is 120 EC) Year 1

Year 1 Year 2

Introductory course (2.5 EC) Genomics and Statistics (4 EC)

Excellence in communication (1.5 EC) International Master class (1.5 EC)

Science and society (1.5 EC) Elective courses (9.5 EC)

Infection immunity and

regenerative medicine (5.5 EC)

Metabolism, transport and motion (5.5 EC)

Cell growth and differentiation (5.5 EC)

International Master classes (3 EC)

Elective courses (2 EC)

Research internship (33 EC) Research internship (45 EC)

Career opportunitiesThe MMD Master’s programme provides students with the qualificationsto enter an international PhD programme. Our graduate students distin-guish themselves through their high knowledge level and independentworking attitude. About 85% of them enter a PhD programme inNijmegen or elsewhere in the world. PhD scholarships are available forthe best MMD students who can apply for their selfwritten researchpro-ject within the NCMLS, thereby allowing them to actively shape theirown career and future. In 2012 five MMD students who are expected tograduate in 2013 obtained such a PhD scholarship. Twelve studentsgraduated in 2012, two of which cum laude and one summa cum laude.Four of these students have started their PhD studies in the NijmegenCentre for Molecular Life Sciences institute and four students have start-ed their PhD in other (inter)national institutes (Amsterdam, Dresden,Barcelona and Stockholm).



26 The NCMLS as Graduate School NCMLS

International PhD programme

The aim of the NCMLS PhD training programme is to provide PhD studentswith a multifaceted education in the field of Molecular Life Sciences.NCMLS PhD students are offered an interdisciplinary training program-me, containing both general and elective components. The general com-ponents are followed by all students, whereas the elective componentsallow a section of the NCMLS training programme to be tailormade tocomplement the specific specialisation of the individual student. Thetraining programme encourages both practical and theoretical participa-tion in several NCMLS activities.

Entrance requirementsThe training programme is accessible to PhD students from one of theresearch groups that are related to the graduate school. Students with aMSc degree, with a higher professional degree or with a similar degreefrom a foreign institute can enter the programme. Medicine, (Medical)Biology, Molecular Mechanisms of Disease, Chemistry, Physics,Mathematics, Computer Science and (Bio) Engineering are suitablepreparatory fields of study. Because of the heterogeneity of the know-ledge and interest of the students, a diverse education programme, inwhich many subjects will be taught, is provided.

The NCMLS certificate Alongside practical training, PhD students are given the opportunity tobroaden their skills through participation in specialised knowledgetransfer courses. A certain number of courses are thought to be necessaryin the development and education of each PhD student as independentresearchers. Students that complete a full programme of NCMLS cour-ses will be awarded with the NCMLS certificate.

The NCMLS Management team isinvolved in all decisions withrespect to research and educationactivities within the NCMLS. Thecommittee meets on a bi-weeklybasis and contains members rep-resenting the seven research

NCMLS Committees

27Annual Report 2013 NCMLS Committees

NCMLS management team

The NCMLS Management team is involved in all decisions with respectto research and education activities within the NCMLS. The committeemeets on a bi-weekly basis and contains members representing theseven research themes and/or play an active role in various NCMLScommittees.Chairman: René Bindels.

MMD master’s educational management team

The Educational Management Team (‘Onderwijs management Team –OMT’) is involved in the main aspects of the MSc MMD, such as therecruitment of students, budget planning and monitoring, mentorshipassignments, initiation of new modules, selection of new Masterclasstopics, and the evaluation of the courses.Chairman: Roland Brock.

PhD programme committee

This committee’s primary role is the smooth running of the completePhD programme, including the lectures for the 1 week introductorycourse, and approval of the individual PhD training programmes. Thecommittee is responsible for the coordination of the student-mentorsystem, selects the lecturers for the graduate course, and regularly eval-uates their performance. Furthermore, the committee organises anannual PhD conference and supervises the organisation (by PhD stu-dents) of 4-5 PhD workshops per annum.Chairman: Bert van der Reijden.

Subsidy review committee

This committee advises applicants (Master’s, PhD students, post-docsetc) on grant applications provides concrete advice on how content andstyle may be improved to increase the likelihood of success. TheSubsidy review Committee critically reviews pre-proposals for Veni, Vidi,Vici applications and KWF grants, and also provides interview trainingfor students. Chairman: Johan van der Vlag.

28 NCMLS

29Annual Report 2013

Selected Research Highlights NCMLS 2013

30 NCMLS

Theme 1: Infection & Inflammation

Proc Natl Acad Sci USA 110:7862-7, 2013.

Giving antimalarial drugs to healthy volunteers, and exposing them atthe same time to the malaria sporozoites with bites from infected mos-quitoes, Chemoprophylaxis and Sporozoites immunization, turns out tobe a very efficient way to induce complete and long-lasting protectionagainst malaria. This article shows that after Chemoprophylaxis andSporozoites immunization, the parasite is attacked by the immune sys-tem at the earliest stage of the infection, before the parasites reach theblood and get the chance to cause symptoms. Malaria still causes655.000 deaths every year, mainly amongst young children in Africa.Because of increasing drug- and insecticide resistance, novel tools areurgently needed to fight this disease. This article establishesChemoprophylaxis and Sporozoites immunization as an efficient andreproducible method to protect healthy volunteers against malaria. Infuture studies, the model will be used to further unravel the immuneresponses underlying protection. Moreover, the findings support a con-tinued focus on vaccine development toward the sporozoite and liverstages of the malaria parasite.

Fighting the malaria parasite with an early attack

Else BijkerGuido Bastiaens

Nat Commun 4:1342, 2013.

Candida albicans is the most common fungal commensal microorganismfound in human skin and mucosa. Despite the availability of novel anti-fungal drugs, such as azoles and echinocandins, the mortality of sys-temic Candida sepsis remains high in immunocompromised patients.Therefore, understanding of the host defense pathway involved in can-didiasis is crucial for identifying novel targets for immunotherapy. In thecurrent study we applied the state-of-the-art functional genomicsapproaches, integrating the system biology and transcriptional analysisin an in-vitro Candida stimulation model in the peripheral mononuclearblood cells (PBMCs) and identified unexpectedly a novel role of type I IFNin Candida. We further validated that the type I IFN pathway is defectedin the patients with chronic mucocutaneous candidiasis (CMC) and alsodemonstrated that addition of type I IFN in peripheral mononuclearblood cells with Candida stimulation would skew the T cell differentia-tion from Th17 to Th1. It is expected that this knowledge will have animportant contribution in devising novel immunotherapeutic strategiesfor fungal infections, as well as influencing decision-making for vaccinedesign.

A novel role of type I IFN in Candida infection

Shih-Chin ChengSanne Smeekens

Figure: Transcriptional responses to Candida. (a) K-means clustering identifies shared and specific gene signatures in response to infection

or stimulation. Signal-to-noise ratio relative to untreated is shown in the heatmap. (b) Principal component analysis (PCA) of the Candida-

response signature. Stimulation color coded as follows: Candida albicans (2h: bright red; 24 hr: dark red),Borrelia burgdorferi (Green),

E.coli-derived LPS (Blue), Mycobacterium tuberculosis (M.tb) (Purple) and untreated (Yellow). (c) Enrichment analysisEnrichment analysis

(MetaCore pathways) of the 101-transcript feature set reveals a striking enrichment of the interferon (IFN) signaling pathway.

Figure: Anopheles mosquitoes after a bloodmeal.



J Clin Invest 123:917-27, 2013.

Atopic dermatitis (AD), also known as ‘eczema’, is an extremely commoninflammatory skin disease characterized by skin barrier defects. Eczemapatients experience intense itch and their affected skin is red, scaly andoften covered with blisters and crusts. The medical, psycho-social andeconomic impact is high. Topical application of coal tar is one of the oldest treatment of skin diseases, and is a cheap, safe and effectivetherapy. However, its use in dermatological practice is declining due tosafety concerns, cosmetic reasons, and the - until recently - unknownmechanism of action. We have elucidated the molecular mechanism andfound that coal tar activates the aryl hydrocarbon receptor (AhR) there-by restoring the skin barrier and reducing inflammatory signaling. Wenow aim to isolate coal tar fractions with more favorable properties(colorless, less smell) that retain the desired in vitro biological effects.This exciting first step in seeking alternatives for the classical coal tartherapy will aid in drug discovery for eczema.

Old drug, new hope for eczema patients

Ellen van den BogaardJoost Schalkwijk

Ann Rheum Dis 72: 1407-15, 2013.

Rheumatoid arthritis is an autoimmune disease which leads to destruc-tion of bone and cartilage causing impaired mobility and pain. Toll-Likereceptor 4 (TLR4) is a key receptor in innate immunity. It recognizesGram negative bacteria and degradation products (DAMPS) associatedwith inflammation.Therefore, the role of TLR4 was studied on both inflammatory cells andthe cells residing in the joint capsule (such as fibroblasts), bone, andcartilage. A reciprocal bone marrow transplantation was performed withTLR4 knock out animals in a spontaneous arthritis model.The animals were monitored over time for ankle joint swelling. TLR4+/+recipients with TLR4+/+ bone marrow showed increased swelling com-pared to animals that lack TLR4 on bone marrow, recipient cells, or both(Figure). In addition, absence of TLR4 resulted in decreased bone andcartilage destruction (not shown). These results show that in arthritis TLR4 on inflammatory cells and alsoon non-hematopoietic cells both contribute to inflammation and connec-tive tissue destruction. Moreover, this study contributes to the emergingevidence that DAMPS in the arthritic joint, play an active role in arthritis.

Toll-Like receptor 4 in arthritis

Ben van den BrandFons van de Loo

Figure: (A)Typical atopic dermatitis or eczema lesions on the flexural site of the

knees. (B) Restored protein expression of two major skin barrier proteins ‘filaggrin’

and ‘loricrin’ in lesional skin of atopic dermatitis patients after coal tar treatment.

Figure: Development of arthritis severity over time in bone marrow chimeras. Ankle

joint swelling was monitored over time to assess disease severity and represented

as mean per group. * p< 0.05; ** p< 0.01.

32 NCMLS

Theme 2: Immune Regulation

Blood 121:459-67, 2013.

Patients with metastatic disease are poorly served by current therapiesand therefore, novel strategies of treatment including immunotherapyare explored worldwide. One of the modern experimental therapies formelanoma is dendritic cell (DC)-based immunotherapy. DCs are the mostprofessional antigen presenting cells of our immune system with theunique capacity to attract and activate antigen specific killer T-cells. Thecross presentation of exogenous antigens by DCs on MHC class I isessential for the initiation of effective tumor specific killer T cellsresponses (Figure). Therefore over the past decade cross-presentationhas been extensively studied and the cell type and conditions best facil-itating cross-presentation has become the holy grail of (tumor)immunology. In human peripheral blood, three populations of DCs canbe distinguished, plasmacytoid DCs (pDCs) and, CD1c+ and BDCA-3+

myeloid DCs (mDCs), each with distinct functional characteristics.Although pDCs take up less Ags than CD1c+ and BDCA3+ mDCs, pDCsinduce potent Ag-specific CD4+ and CD8+ T cells responses. We showthat pDCs can preserve Ags for prolonged periods of time and upon stim-ulation show strong induction of both MHC class I and II, which explainstheir efficient activation of both CD4+ and CD8+ T cells. These findings,together with their potent IFN-I production, put human pDCsforward as potent activators of CD8+ T cells in anti-tumor responses.

Human plasmacytoid dendritic cells as potential targets for anti-cancer therapy

Jurjen Tel Jolanda de Vries

Nat Commun 4:1412, 2013.

While overwhelming information is available about cells undergoing fastmigration, little is known about the mechanisms regulating slow migra-tion of tissue-resident antigen-presenting dendritic cells (DCs). Usingactomyosin-based structures called podosomes, DCs probe and remodelthe extracellular matrix topography while patrolling for foreign intruders.Podosomes comprise an actin-rich protrusive core surrounded by anadhesive ring of integrins, cytoskeletal adaptor proteins and actin net-work filaments (Figure A). Here we revealed that the integrity and dynam-ics of protrusive cores and adhesive rings are coordinated by the acto-myosin apparatus (Figure B), providing novel mechanistic insights intohow actomyosin-based structures allow DCs to sense the extracellularenvironment. Podosomes enable osteoclasts to digest and remodel bonematrix and endothelial cells to promote arterial vessel remodelling.Moreover, podosomes are related to “invadopodia”, structures associa-ted with cancer cell migration. Fundamental research on the propertiesand function of these structures will contribute to understand patholo-gies such as vascular diseases, impaired bone resorption and tissueinvasion by cancer cells.

Understanding adhesion and migration of antigen-presenting cells

Koen van den DriesAlessandra Cambi

Figure: Decisive factors that determine the cross-presentation ability of DCs. Theability of DCs to cross-present antigens is not just an intrinsic property of the spe-cific DC subset, but is also determined by: (i) type of antigen; (ii) presence of DCstimulatory factors; and (iii) timing and phase of the immune response. Wedemonstrated that human pDCs have the capacity to take up and process exoge-nous antigens, and subsequently efficiently cross-present tumor antigens to killerT cells leading to antigen specific T cell proliferation and IFNγ secretion.

Figure: (A) Human adherent DCs fixed and labelled for actin (red) and vinculin

(green). Insets show one enlarged individual podosome and the separate fluorescent

signals of the core (middle) and the ring (bottom). (B) Actin intensity fluctuations in

three representative podosomes of a living DC. Blocking myosin contractility with

blebbistatin (Blebb) or the Rho kinase inhibitor Y27632 abrogates these fluctuations.



Blood 122:2213-23, 2013.

Regulatory T cells (Tregs) regulate immune responses and are essentialfor the maintenance of (self-) tolerance and homeostasis. Immunomodu-lating therapy with Treg is a promising strategy in autoimmunity andtransplantation. However, to achieve full clinical efficacy, a better under-standing of where and how Treg operate in humans is needed. We founda striking difference in the behavior of Treg in peripheral blood and bonemarrow versus those in lymph nodes and spleen. Whereas the firstshowed a resting phenotype, the majority of Tregs in secondary lymphoidorgans were activated cells with the capacity to proliferate and producecytokines, while revealing similar suppressive potential. Also, next tochemokine receptors important for a prolonged stay in lymphoid organs,a significant part of Tregs expressed peripheral tissue–associated ho-ming markers. These data suggest that human secondary lymphoidorgans aid in the maintenance and regulation of Treg function andhomeostasis. This knowledge may be exploited for further optimizationof Treg immunotherapy (Figure), for example, by ex vivo selection ofTregs with capacity to migrate to lymphoid organs providing an in vivoplatform for further Treg expansion.

Human lymphoid organs aid in the support of an immune regulatory network

Jorieke PetersIrma Joosten

Nat Genet 45:1226-31, 2013.

B-cell precursor acute lymphoblastic leukemia (B-ALL) is the most com-mon pediatric malignancy. In this study, we report the first inheritedgene mutation linked exclusively to ALL occurring in multiple relatives inindividual families. The heterozygous germline variant, c.547G>A(p.Gly183Ser), affecting the octapeptide domain of PAX5 was found tosegregate with disease in two unrelated kindreds with autosomal domi-nant B-ALL. Leukemic cells from all affected individuals in both familiesexhibited 9p deletion, with loss of heterozygosity and retention of themutant PAX5 allele at 9p13 (Figure). Two additional sporadic ALL caseswith 9p loss harbored somatic PAX5 substitutions affecting Gly183.Functional and gene expression analysis of the PAX5 mutation demon-strated that it had significantly reduced transcriptional activity. Somaticalterations of the lymphoid transcription factor gene PAX5 are a hall-mark of B-ALL, but inherited mutations of PAX5 have not previously beendescribed. These data extend the role of PAX5 alterations in the patho-genesis of B-ALL, and implicate PAX5 in a novel syndrome of susceptibi-lity to B-cell neoplasia. Using this strategy, we will study other kindredswith a history of ALL to improve our knowledge on cancer predispositionat childhood.

Rare, inherited PAX5 mutation leaves children susceptible to acute lymphoblastic leukemia

Esmé WaandersRoland Kuiper

Figure: Potential use of (differences in) key-

characteristics of human Treg in peripheral

blood and bone marrow versus Treg in lymph

nodes and spleen. (A) Similar suppressive

potential. (B) Selective proliferative and

cytokine producing potential: increased

numbers. (C) Targeted tissue homing for opti-

mal function.

Figure: Familial pre-B cell ALL associated with PAX5 p.Gly183Ser and somatic loss of

chromosome 9p

Chromosome 9 copy number heat map for SNP6.0 microarray data of germline and

tumor samples of three members of family 2. Deletions are shown in blue, gains are

depicted in red. G, germline; D, diagnosis and R, relapse sample.

34 NCMLS


Eur Urol 63:6, 1101–1106, 2013.

Due to the increased use of conventional imaging techniques such asultrasound and Computed Tomography, renal cell carcinoma (RCC) isdetected more frequently at an earlier stage of disease progression.However, a major drawback of these imaging techniques is that theycannot reliably distinguish between RCC malignant and benign solidlesions. For clinicians this results in a diagnostic dilemma. Adequatecharacterization of lesions based on imaging is essential to avoid inva-sive biopsies and superfluous surgery, and most importantly not to missa potentially lethal disease. Clear cell RCC is the most common renalmalignancy. This particular subtype shows very high and specificexpression of carbonic anhydrase IX, which can be targeted with mono-clonal antibody girentuximab. By labeling this antibody with gamma rayemitting radionuclides such as 111Indium, primary clear cell RCC tumorscan be detected with a gamma camera (Figure 1). 111Indium-girentuxi-mab imaging can be a helpful, non-invasive tool for clinical decisionmaking in patients with a history of clear cell RCC presenting withlesions suspect for metastases, particularly in cases with inconclusiveconventional imaging or biopsies (Figure 2).

Imaging renal cell carcinoma with radiolabeled antibodies

Stijn MuselaersPeter Mulders

Am J Transplant 13:1503-11, 2013.

Rituximab (RTX) is a chimeric anti-CD20 monoclonal antibody which trig-gers B-cell lysis. It is a very effective drug for patients with B-cell lym-phoma or various autoimmune disorders. In renal transplantation, RTX issuccessfully used in ABO-incompatible transplantation in order todecrease detrimental antibody production. Although RTX rapidlydepletes CD19+ B cells from peripheral blood, we and others found thatB cells are still present in secondary lymphoid organs of patients trea-ted with RTX.As B cells have additional functions beyond antibody production, thisraised the question of how these B cells were affected by RTX and whatthe functional consequences for the immune response would be. Wefound that the B cells remaining in lymph nodes at 4 weeks after rituxi-mab administration were mostly of the memory type (IgD-CD27+), andinduced altered responses in T cells with decreased production of inter-leukin-17. Consequently, we showed that the effect of rituximab on theimmune response will not only be determined by the extent of B celldepletion, but also by the functional properties of the remaining B cells.This has added to our understanding of the mechanism of action of RTX,which may guide in the design of future therapeutic regimens.

Transplant patients and rituximab treatment

Elena KamburovaLuuk Hilbrands

Figure 1: SPECT/CT of a 62 year old male

patient. Uptake of 111In-girentuximab

in a primary clear cell RCC lesion (white

arrow). No accumulation of the tracer is

observed in the benign cyst (blue arrow)

or in the normal renal tissue.

Figure 2: Sagittal view of SPECT/CT

of a patient with multiple lesions

suspect for local recurrence of

clear cell RCC (white arrows).

Figure: B cells remaining in lymphoid organs after rituximab treatment.

When tumor cells invade extracellular matrix (ECM), the membrane-teth-ered matrix metalloproteinase MT1-MMP focally degrades ECM barriersand greatly enhances invasion efficacy. However, a long-standing con-troversy remained; the relevance of MMP function for invasion andwhether therapeutic MMP inhibition results in arrested migration. Ourcover-story publication resolves opposing concepts from different labsby systematically analyzing different ECM conditions, cell types, andmolecular programs of proteolytic and non-proteolytic migration. WhenECM pores are smaller than 10% of the normal cell cross section, ECMdegradation by MMPs is indispensable for forward migration becausecell body and nucleus fail to deform and propel the cell forward (Figure).Conversely, larger ECM gaps enable cell migration by shape change, withMMPs dispensable. Thus molecular plasticity of cell migration in 3D tissue depends on the physics of ECM. This multi-parametric approach of3D tissue invasion provides the basis for understanding tissue-guidanceand remodeling in cancer metastasis, inflammation and regeneration.


Theme 3: Regenerative Medicine & Microenvironment

J Cell Biol 201:1069-1084, 2013. A cover-story publication.

Testing the limits of cell migration

Katarina WolfPeter Friedl

J Urol 190:341-9, 2013.

Current tissue engineering techniques in cell and tissue culturing makeit possible to keep organ tissues viable for longer periods outside of thebody in controlled laboratory conditions. This is called organotypic cul-turing and it has the potential to partially replace in vivo experiments.The urinary bladder is prone to disease, such as bladder cancer andoveractive bladder syndrome which both have a high prevalence and aconsiderable impact on a patients’ quality of life. The study describes anew and straightforward experimental model, which involves the organ-otypic culturing of abattoir-derived porcine bladder mucosa on type 1collagen scaffolds. Since both functional and morphological aspects ofthe urothelium are preserved for more than 1 week, the model has thepotential to become a practical and cost-efficient alternative for experi-ments that are now performed on laboratory animals. In this study, wesystematically evaluated different culturing protocols using ScanningElectron Microscopy and specific immunohistochemical stainings suchas proliferation and apoptosis assays. The model may be well suited toevaluate current and new treatment modalities, screen toxic compo-nents, and investigate regeneration processes.

A new, straightforward ex vivo bladder model for preclinical research

Dick JanssenJohn Heesakkers

Figure: Migration is deter-

mined by nuclear diameter in

the presence of MMP inhibitor

GM6001: (A) Migration rates at

indicated collagen sources and

concentrations. Non-proteoly-

tic migration in the presence of

GM6001 in bovine collagen

was equalized with 100%

migration rate. Migration rates

<10% were associated with

migration arrest. (B) The pre-

sence of GM6001 causes

nuclear deformation of 1-3 µm

(arrow) together with cell

arrest.

Figure: A & B) The organotypical culturing model where bladder mucosal tissue

is placed on a collagen type I scaffold and cultured in specific culturing medium.

C) A electron microscopy (TEM) image of a bladder mucosa biopsy that has been

cultured on a collagen scaffold for 1 week. D) Histological evaluation (H&E) of a

bladder mucosal biopsy that has been cultured for 1 week.

36 NCMLS


Am J Pathol 182:1196-204, 2013.

End-stage renal disease (ESRD), necessitating dialysis or kidney trans-plantation, is a result of progressive renal function loss. Therefore, pre-venting or inhibiting renal injury is of highest priority. Increased activityand expression of the Transient Receptor Potential channel C6 (TRPC6) isinvolved in injury to the podocyte, a specialized cell in the renal filter,which can lead to ESRD. We demonstrated that vitamin D treatment low-ers TRPC6 expression and prevents kidney injury in rats. Vitamin D dose-dependently downregulated podocyte TRPC6 expression, at least in partby direct binding to vitamin D responsive elements in the TRPC6 promot-er, reducing its activity. Importantly, we were the first to show that vita-min D deficiency induces TRPC6 expression and kidney, particularlypodocyte, injury (Figure), which could be prevented by vitamin D supple-mentation. We concluded that vitamin D prevents TRPC6 upregulationand renal injury, while vitamin D deficiency conversely causes renalinjury. Because renal insufficiency itself also leads to vitamin D deficien-cy, our data underscore the need for early vitamin D supplementation inpatients with kidney disease.

Vitamin D, a crucial hormone for patients with kidney disease

Ramon SonneveldTom Nijenhuis

Biomaterials 34:3747-57, 2013.

Dental implants may not be an optimal approach for patients sufferingfrom osteoporosis, a disease of increasing importance in an aging popu-lation. This study was designed to address the performance of bioactive-coated implants in osteoporotic conditions with the use of the esta-blished osteoporotic rat model. The main finding in this study is that theosteogenicity of titanium implants can be significantly improved bydepositing a calcium phosphate (CaP) or collagen type-I coating for bothosteoporotic and healthy conditions (Figure). Interestingly, an increasedlevel of bone-to-implant contact could be obtained for either type ofcoated implant in osteoporotic conditions compared to non-coated tita-nium implants. The study confirmed that an osteoporotic condition hasa significant effect on the amount of bone present in close vicinity toimplants. Evidently, the use of osteogenic surface coatings has a favor-able effect on the bone-implant interface in both osteoporotic andhealthy conditions.

Osteogenicity of dental implants

Hamdan AlghamdiJohn Jansen

Figure: Electron microscopy images of renal filters from wildtype (WT), vitamin D

deficient 1α-hydroxylase knockout mice (KO), and vitamin D-treated KOs (KO + Vit

D). Normal podocyte foot processes are depicted in the WT mice (arrows), while a

significant part of the podocytes are injured in KOs, leading to loss of their charac-

teristic architecture (arrows). Vitamin D treatment (KO + Vit D) normalized podocyte

architecture (arrows).

Figure: Histological images present osteogenicity of coated implants.


Theme 4: Energy & Redox Metabolism


The intraflagellar transport (IFT) is an integral component of the cilium.Ciliary dysfunction leads to a class of genetic disorders called cilio-pathies with an estimated combined incidence of 1:1000. Componentsof the IFT have been implied to function as part of the coatomer vesicletransport machinery as well, but it is not clear exactly how. By investiga-ting the sequences of all 31 subunits we have been able to trace the origins of 12 subunits to an ancestral coatomer complex related to COPI,a complex involved in coated vesicle formation. The coatomer origin ofIFT therefore indicates that components of the IFT function similarly toCOPI components in coatomer vesicle transport. Additionally, the evolu-tionary patterns of the IFT subunits show that specific functions of the IFT,such as anterograde and retrograde transport, are separated into distinctmodules in a hierarchal manner within the IFT complex. The evolutionarystudy of the IFT has provided a compelling insight into its structural andfunctional aspects and will help us to understand its role in the cilium,vesicle transport and ultimately in its role in ciliopathies.

Evolution of ciliopathy-associated intraflagellar transport

John van DamMartijn Huijnen

Antioxid Redox Signal 18:129-38, 2013.

One of the main functions of mitochondria in the cell is the generation ofits fuel, ATP, and mitochondria are therewith often regarded as the cell’spowerhouses. Mitochondria use oxygen to produce ATP and one of theside effects of that is oxidative stress, implicated in aging and in a largearray of diseases such as Alzheimer’s, Parkinson’s and Diabetes. Toidentify new proteins involved in the protection against oxidative stresswe turned our attention to BOLA1, a protein that is highly expressedunder stress conditions in bacteria. We demonstrated that depletion ofBOLA1 increases the level of oxidative stress in mitochondria. Conver-sely, increasing the concentration of BOLA1 in mitochondria protectsthem from oxidative stress. Consistent with these results, BOLA1 inter-acts with GLRX5, another protein implicated in the defense againstoxidative stress. Furthermore, BOLA1 only occurs in species that live inaerobic, oxidating environments. By a combination of computationaland experimental approaches our results have thus identified a newplayer in protecting us from one of the dangers from using oxygen togenerate our energy supply.

A new player in the protection against oxidative stress

Peter WillemsMartijn Huijnen

Figure: BSO, an agent that causes oxidative

stress to mitochondria causes them to frag-

ment (left). Overexpressing BOLA1 in the

presence of BSO reduces the level of stress,

resulting in elongated, normal looking

mitochondria (right).

Figure: The order of branching in the phylogenetic tree of IFT and coatomer subunits

(left) is used to infer the order of emergence of the distinct sub complexes (right) as

the intraflagellar transport evolved.

38 NCMLS


Cell Mol Life Sci 70:2175-90, 2013.

Nicotinamide adenine dinucleotide (NAD+ or NADH when in its oxidizedor reduced form, respectively) is the main electron carrier in all livingcells. It is also the rate-determining factor for the production of cellularenergy, ATP, and an important regulator of protein (de)acetylation.Intracellular NAD(H) concentrations may vary between tissues, celltypes, and subcellular locations, depending on developmental state,nutrient conditions and the genetically determined capacity for de novoor salvage synthesis of NAD+. We used genetic knockdown and pharma-cological inhibition of nicotinamidephosphoribosyltransferase (Nampt)to modulate synthetic capacity and create brain tumor cells with gradedlevels of global NAD(H). We found that there is differential couplingbetween the NAD(H) level and a cell’s capacity to undergo morphologi-cal change and migrate or to grow and proliferate. Based on our findingswe propose that nutrient or drug-mediated modulation of NAD(H) levelsin vivo offers new opportunities for blocking the invasive behavior oftumor cells.

Differential control of cell dynamics and growth by NAD(H)

Remco van HorssenBé Wieringa

Brain 136: 1544-54, 2013.

Mitochondrial disorders are a heterogeneous group of diseases thatusually affects tissues with a high energy demand, such as muscle andbrain. Recent technological developments have made it possible toexamine all these genes in one experiment by using whole exomesequencing. In a study of two siblings with a fatal mitochondrial dis-ease, we have applied whole exome sequencing and identified a genet-ic defect in the ATP5A1 gene. This gene encodes a protein that is part ofthe mitochondrial complex V, an enzyme that synthesizes ATP.Functional studies using patient-derived fibroblasts proved that thepatients had an enzyme deficiency of complex V that could be attributedto the mutations in the ATP5A1 gene, causing destabilization of the pro-tein complex (Figure). This was one of the first studies in which wholeexome sequencing was successfully applied to diagnose mitochondrialdisease patients, providing important new insights into the role ofATP5A1 in the structure and function of complex V.

A fatal disease caused by a defect in ATP synthesis

Martijn HuijnenRichard Rodenburg

Figure: Different intracellular NAD((P)(H) levels (indicated by letter size) - produced by

genetic or drug inhibition of Nampt - differentially affect morphodynamic behavior or

growth and viability of cells.

Figure: Impact of the ATP5A1 p.Arg329Cys mutation at the protein structure level.

Left figure: The Arg-329 (indicated in purple) of the ATP5A1 protein (indicated in blue) is

predicted to interact with the Gly-323 residue of the ATP5B subunit (indicated in yellow).

Right figure: The p.Arg329Cys mutation in ATP5A1 disturbs the interaction with ATP5B, thus

interfering with the stability of complex V. (R: arginine; C: cysteine; G: glycine)

Mitochondrial complex III deficiency is a devastating disorder thatimpairs energy generation, resulting in wide range of symptoms and fre-quent death at a young age. At the time of birth our patient had severemetabolic acidosis, showed developmental delays and by nine years ofage a number of autistic features. The genetic basis of complex III defi-ciency is not yet fully understood, often precluding genetic diagnosis. Itis partly due to an incomplete understanding of the genes required forcomplex III assembly and function. Using complex III as a molecular sys-tem we pursued discovery of additional components, using among oth-ers the co-expression of genes.This search led to identification of two key proteins required for complexIII formation, UQCC1 and UQCC2. We have elucidated the role of thesenovel inter-dependent proteins in complex III biogenesis. Both associatewith mitochondria-encoded cytochrome b in the early steps of complexassembly (Figure). We have shown that mutations in UQCC2 causehuman complex III deficiency in our patient. This work contributes to animproved understanding of complex III biogenesis, and will aid futuremolecular diagnoses of complex III deficiency.



Nat Commun 4, 2124:1-10, 2013.

Recent advances in computational and experimental biology enable the identification of anti-cancer drug targets by characterizing cancer-specific essential genes. One strategy is to screen for negative geneticinteractions (GIs). Two genes have a negative GI when a loss-of-functionmutation of one gene has no effect on cell viability but a double muta-tion results in a severe growth defect. Therefore, a gene is identified asa target in cancer cells when its negative GI partner is mutated (e.g.,oncogene). Since most negative GIs in human cells are still unknown, weconstructed a computational model to predict negative GIs by systema-tically exploiting gene gain and loss patterns in genome evolution(Figure). We evaluated our model with yeast protein complexes andshowed that predicted protein pairs more frequently have a negative GIthan random proteins from the same complex. Furthermore, we appliedour model to human protein complexes and predicted a list of novelcancer drug targets with empirical support. Currently, we aim to predictpersonalized anti-cancer targets by applying our approach to patient-specific protein-protein interaction networks. This will pave the way forthe realization of effective cancer treatments at a personalized-level.

From genome evolution to personalized cancer treatment

Xiaowen LuRichard Notebaart

Plos Genetics 9:e1004034, 2013.

Integrative genomics for mitochondrial disease

Radek SzklarczykMartijn Huynen

Figure: Identifying negative genetic interactions via genome evolution

Figure: complex III assembly starts with stabilization of cytochrome b by UQCC1

and UQCC2

40 NCMLS

Theme 5: Membrane Transport & Cell Dynamics

Biochim Biophys Acta 1832:2173-9, 2013.

Familial Hemiplegic Migraine (FHM) is a rare subtype of migraine withaura, characterized by severe migraine attacks preceded by neurologicalsymptoms. Today, three genes are linked to this disease, including thegene encoding the alpha 2 subunit of the Na,K-ATPase, a membrane pro-tein transporting Na+ and K+ across the cellular membrane. Presence ofthis subunit in astrocytes is essential for effective signal transduction atneuronal synapses. In the development of a therapy for FHM, under-standing the effect of mutations at the protein level is paramount. Here,we performed an extensive biochemical characterization of eleven muta-tions found in the alpha 2 subunit. Five out of eleven mutations wereshown to decrease the enzyme’s transport activity by affecting intramo-lecular amino acid interactions, two affected enzyme activity via secon-dary effects, whereas the remaining four mutations could not be linkedto FHM. Based on these findings, we were able to gain fundamentalinsight into the exact molecular effects of seven alpha 2 mutations,whereas four mutations are not pathogenic but rather polymorphismsindicating that there may be more genes involved in FHM development.

Familial Hemiplegic Migraine affects Na,K-ATPase domain interactions

Karl WeigandJan Koenderink

J Clin Endocrinol Metab 98: 4089-96, 2013.

Parathyroid glands release parathyroid hormone (PTH) into the circula-tion to maintain normal extracellular calcium (Ca2+) and phosphate(PO4

3-) concentrations (Figure). PTH levels depend on PTH release fromsecretory granules and synthesis of new PTH molecules secondary toPTH gene transcription. In this study, we identified the transcription fac-tor HNF1β as a novel repressor of PTH gene transcription. HNF1β muta-tions or deletions result in a heterogeneous syndrome with renal andextra-renal manifestations (genitourinary abnormalities, renal cysts,diabetes, hypomagnesemia, gout). We observed early hyperparathy-roidism disproportionate to the renal function in patients with HNF1βabnormalities. We demonstrated HNF1β expression in PTH-positive cellsof human parathyroid gland. We showed that HNF1β directly binds tothe human PTH promoter. Wild-type HNF1β reduced PTH promoter acti-vity, while mutant HNF1β failed to do so. Our data suggest that loss ofPTH transcriptional inhibition by HNF1β contributes to the developmentof early hyperparathyroidism in patients with HNF1β abnormalities.

Unravelling the molecular basis of early hyperparathyroidism in patients with HNF1β mutations

Silvia FerrèTom Nijenhuis

Figure: Hormonal regulation of Ca2+ and Pi homeostasis. PTH, parathyroid hormone;

1,25(OH)2D3, active vitamin D; FGF23, fibroblast growth factor 23; Pi, inorganic phos-

phate.

Figure: Under normal conditions, Na,K-ATPase activity results in a favorable driving force

for re-uptake of glutamate from the synaptic cleft. Mutations in the Na,K-ATPase result in

an extended re-uptake time of glutamate which is associated with FHM attacks.



Biochim Biophys Acta 1832:142-50, 2013.

The main role of the kidney is recycling nutrients and removing wasteproducts. A key feature of chronic kidney disease (CKD) is the retentionand subsequent accumulation of a wide array of chemically diversemetabolites that are normally excreted by the healthy kidney. Anotherhallmark of CKD are changes in drug disposition, partially caused by areduction in glomerular filtration and active tubular secretion of xenobi-otics, as well as mediated by a direct effect of uremic toxins on theexpression level and activity of drug metabolism enzymes. Most studieson the role of drug metabolism in CKD have focused on hepaticcytochrome P450 (phase I) enzyme expression levels and their activity.We investigated the interaction between a multiplicity of uremic soluteswith an important class of phase II metabolism enzymes, namely UDP-glucuronosyltransferases (UGT), and mitochondrial function in renalproximal tubule cells. Our results demonstrated that a wide variety ofuremic toxins, including indole-3-acetic acid and p-cresyl sulfate,reduced UGT activity, without affecting protein expression. Furthermore,several uremic toxins inhibited mitochondrial succinate dehydrogenaseactivity in renal tubule cells, and indole-3-acetic acid reduced thereserve capacity of the energy-generating oxidative phosphorylationsystem. Thus, uremic solutes can affect diverse intracellular targetsthereby hampering the metabolic capacity of the kidney during CKD.

Deactivation of the renal metabolic machinery during chronic kidney disease

Rick MutsaersRoos Masereeuw

Pflugers Arch–Eur J Physiol 465: 1409-21, 2013.

Hypomagnesemia is diagnosed in a high percentage of hospitalizedpatients (26.1% and 3.5% in acute and chronic care patient populations,respectively). Hypomagnesemia manifests in a variety of clinical symp-toms including seizures, muscle cramps, and psychiatric and neurolo-gical disorders. Introduction of zebrafish as a model for human diseaseswith symptomatic hypomagnesemia first requires the identification ofregulatory transport genes involved in zebrafish Mg2+ physiology. Wehave provided molecular evidence for the magnesiotropic transcriptomeof zebrafish. Importantly, the genes involved in zebrafish Mg2+ physiolo-gy are the homologues of human genes which when mutated yield hypo-magnesemia. Moreover, tissue distribution and expression of thesegenes is similar to that in humans. When zebrafish Mg2+ homeostasiswas challenged by exposure to different Mg2+ concentrations in waterand by feeding different Mg2+ diets, the gene regulation patterns werein line with compensatory mechanisms to cope with Mg2+ deficiency orsurplus. Furthermore, regulation of Mg2+ is achieved through the con-certed action of the intestine and kidney (Figure). Our data paves theway to develop specific zebrafish models to elucidate the molecular(patho)mechanisms of hypomagnesemia.

Zebrafish as a model to study human magnesium physiology

Francisco Arjona MadueñoJoost Hoenderop

Figure: The regulation of Mg2+ balance in zebrafish is similar to that in humans. Human

proteins related to hypomagnesemia are TRPM6, CNNM2, EGF, NCC, Kv1.1 and Kir4.1.

Zebrafish homologues are expressed in intestine and kidney. Arrows indicate that expres-

sion of the gene encoding for its respective protein is up-regulated in low Mg2+ conditions,

therefore illustrating compensatory mechanisms.

Figure: Intracellular targets affected by uremic toxins. Schematic presentation of the

negative impact of uremic toxins on renal proximal tubule cells. Uremic solutes can

cause mitochondrial dysfunction, inhibit UGT-mediated metabolism as well as ham-

per transport activity.

42 NCMLS


Gastroenterol 145:357-65, 2013.

Polycystic liver disease (PLD) is an hereditary condition characterized bydevelopment of multiple fluid-filled cysts throughout the liver (Figure).The continuous growth of these cysts can lead to severe hepatomegaly(up to 10 times normal liver size), and as a consequence these patientsexperience abdominal distension, pain and early satiety. The medicaland psycho-social impact is high in these patients. Current surgicaltreatment options are aimed at reduction of liver volume. However,these procedures are partly effective, resulting in the need for livertransplantation in a subset of patients. New therapeutic options thatalter the course of PLD are needed. Three randomized controlled trials(RCT) showed that somatostatin analogues (SA) reverse polycystic livergrowth in PLD patients. We performed a pooled analysis using the RCTindividual patient data to identify subgroups with increased treatmentresponses. We discovered that young female PLD patients had most dis-ease progression and showed the best treatment response. Our resultshighlight the merits of SA therapy in PLD. Furthermore, our findingsfocus attention on mechanisms of cyst growth and potential pathways totarget for future therapies.

Treatment for patients with polycystic liver disease in sight?

Tom GeversJoost Drenth

Clin Chem 59:527-35, 2013.

Serum hepcidin is a promising biomarker in the diagnosis of iron disor-ders. Hepcidin concentrations have been shown to increase during theday in individuals who are following a regular diet. In this study weassessed the effect of dietary iron on hepcidin variations during the day.Our data show that serum hepcidin concentrations increase during aday of an iron-deficient diet, and that these concentrations are signifi-cantly higher in women but not in men following oral iron intake. Ourdata suggest that ferritin sets the basal concentrations and that trans-ferrin saturation in conjunction with the innate daily rhythm contributesto the daily variations in hepcidin concentrations. We concluded for thefirst time that an innate daily rhythm rather than dietary iron mediatesdaily hepcidin regulation, which will be useful for optimizing samplingprotocols and will facilitate interpretation of hepcidin as a novel iron bio-marker.

Effect of dietary iron on the regulatory hormone hepcidin

Charlotte SchaapDorine Swinkels

Figure: T2 MRI liver of patient with polycystic liver disease.

Figure: The estimated mean hepcidin profiles of women both on a day of

iron-deficient diet (thick broken line) and on a day of iron-enriched diet (thick

solid line). The thin dashed lines indicate the appropriate 95% confidence

bands. The vertical bars indicate 1 SD of the observed mean.


Theme 6: Genetic & Epigenetic Pathways of Disease

PLoS Genet 9(10):e1003911, 2013.

Intellectual Disability (ID) affects more than 2% of our population and isone of the biggest unsolved medical and socio-economic problems ofour society. So far genetic causes of ID disorders have only been inves-tigated at the single gene level. Consequently our understanding of theneuropathology of ID as a whole is still very limited. We have applied thepower of the fruit fly Drosophila as a model to overcome this bottleneckand provided the first study to systematically understand the commonmolecular basis of ID disorders. Characterization of 270 fly orthologs ofhuman ID genes contributed a large number of novel gene functions thatranged from neurodevelopmental to neurophysiological. Furthermore,we identified 26 functionally coherent modules that comprise 100 inter-connected ID genes. Two examples of these modules are shown in theFigure. Groups of ID genes with overlapping Drosophila phenotypes alsoshowed increased phenotypic similarity in humans and could be used tosuccessfully predict novel gene functions. The conserved functionalmodules identified here provide a basis for the development of thera-peutic strategies that can target genetically heterogeneous ID patientswith a common treatment.

Functional networks of Intellectual Disability genes

Merel OortveldAnnette Schenck

Cell Stem Cell 13:360-9, 2013.

Embryonic stem cells (ESCs) derived from mouse have the potential todifferentiate into all somatic cell lineages and into germ line cells,referred to as pluripotency. In the past decades, ESCs were grown onfeeder cells or in the presence of serum (‘serum ESCs’) and under theseconditions, specific traits have been attributed to mouse ESCs. Morerecently, so-called ground state or 2i pluripotent ESCs have beenderived in serum-free conditions supplemented with two kinaseinhibitors (2i): PD0325901 and CHIR99021 targeting mitogen-activatedprotein kinase (Mek) and glycogen synthase kinase-3 (Gsk3), respective-ly. In collaboration with the groups of Smith and Stewart we previouslyshowed that the transcriptomes and the epigenome of serum ESCs and2i ESCs are distinct hinting at biological/developmental differences. Inthe next step, using whole-genome bisulfite sequencing (WGBS), weshow that 2i ESCs are globally hypomethylated like the ICM cells theyare derived from as compared to conventional ESCs maintained in serumthat parallel the DNA methylation state of a later developmental stages.By converting serum to 2i, we provide a first glimpse at the mechanismand present a tractable system to study the dynamics and kinetics ofdemethylation during reprogramming from a hyper- to a hypomethylatedstate. Our data suggests that ESCs in serum represent a post-implanta-tion embryonic state, while the 2i condition stalls ESCs in a hypomethy-lated, ICM-like state.

Epigenomics (re)defines the developmental stage of cultured mouse embryonal stem cells

Ehsan HabibiHenk Stunnenberg

Figure: Functional modules in Intellectual Disability (ID) disorders, as identified by

integration of similar phenotypes in Drosophila and protein interactions. The figure

shows two of 26 ID modules that were identified in our study.

Figure: The Methylomes of ESCs in 2i and Serum Paralleling Pre- and

Post-implantation stages of mouse development.

Age-related macular degeneration (AMD) is the most common cause ofvisual impairment among the elderly, accounting for up to 50% of allcases of legal blindness in the Western world (Figure). Although agingrepresents a main determinant of AMD, it must be considered a multi-factorial disease caused by interactions between environmental andgenetic factors. Common genetic variants explain up to 50% of the heri-tability of AMD. A large proportion of the “missing heritability” of AMDmay be explained by rare variants which so far remain largely unex-plored. We identified a rare mutation in the complement factor I (CFI)-gene that confers a high risk of AMD (odds ratio 22), and leads to over-activation of the complement system. These data represent the firstdirect evidence that alterations in factor I, a main inhibitor of the com-plement system, confer high risk of developing AMD and increase sup-port for the hypothesis that rare variants contribute to the genetic bur-den of AMD. Our findings have major implications for both predictivetesting and for the development of personalized treatments tailored toeach patient's individual genetic makeup.

44 NCMLS



Familial exudative vitreoretinopathy (FEVR) is a disease characterized byabnormal development of the retinal vasculature, that can result insevere visual impairment. In our manuscript, we describe the identifi-cation of a ZNF408 mutation in a large Dutch FEVR family. This geneencodes the zinc-finger transcription factor ZNF408, and is the firsttranscription factor to be associated with retinal vasculature defects.Knock-down of znf408 in zebrafish also resulted in aberrant develop-ment of vasculature (Figure), thereby mimicking the phenotype obser-ved in FEVR patients. The identification of ZNF408 as a crucial regulatorof vasculogenesis has served as the basis for a new, recently grantedproject where we aim to identify the transcriptional targets of ZNF408 byChIP-SEQ, and assess their function in the zebrafish model system.Together, the outcome of this project may reveal detailed insight in themolecular mechanisms that regulate vasculogenesis, in the eye butpotentially also in other organs.

ZNF408 is crucial for the development of retinal vasculature

Rob CollinFrans Cremers

Nat Genet 45:813-7, 2013.

Rare variants contribute high risk of age-related macular degeneration

John van de VenAnneke den Hollander

Figure: Retinal vasculature defects in znf408 morphant zebrafish.

(A-C) Representative images of GFP-expression in the eyes of fli1:EGFP transgenic zebrafish larvae. Abnormal sprouting of the

vessels in class 1 embryos is indicated by white arrows (B). In class 2 (C), the nasal retinal vessel (nrv) is absent, the ventral

retinal vessel (vrv) is enlarged and both the vrv and the dorsal retinal vessel (drv) are directly attached to the lens (L).

(D) Phenotypic classification of zebrafish larvae injected with control MO or znf408 MO.

Figure: Representive fundus fotographs from a healthy subject (left) and a subject

with advanced AMD (right).




In cancer research, p53 is often mutated in many tumors, and manysmall molecules targeting mutant p53 have been tested. One of suchlow molecular weight compounds is APR246/PRIMA-1MET that was iden-tified as a compound targeting and reactivating p53 mutants, and it iscurrently tested in cancer treatment (clinical trial phase I/II). In our pu-blication in Proc Natl Acad Sci USA, ‘APR-246/PRIMA-1MET rescues epi-dermal differentiation in skin keratinocytes derived from EEC syndromepatients with p63 mutations’, we have reported that APR246/PRIMA-1MET can rescue differentiation defects caused by mutations in p63 thatbelongs to the p53 family and shares sequence and structural similaritywith p53 (Figure). This study was performed in skin keratinocytes esta-blished from EEC patients with p63 mutations who have skin, limb andorofacial defects. The success of this rational drug testing in our studysuggests an interesting possibility of developing targeted therapy forphenotypically distinct diseases that are caused by a similar underlyingmolecular mechanism.

A step closer towards therapies for p63-related disorders

Evelyn KouwenhovenJo Huiqing Zhou

Science 340:479-83, 2013.

Alpha-dystroglycan is a heavily glycosylated extracellular protein thatlinks the intracellular environment of muscle and brain cells with theextracellular matrix via beta-dystroglycan and laminin. A rare type of O-mannose glycan on alpha-dystroglycan is crucial for binding to laminin.Genetic defects in the O-mannosylation pathway lead to the dystrogly-canopathies. Clinically, patients are characterized by severe musculardystrophy, eye malformations and structural brain abnormalities. Inabout half of all dystroglycanopathy patients the genetic defect isunknown. Lassa virus, causing hemorrhagic fever uses the same O-man-nosyl glycan on alpha-dystroglycan to enter the cell. Together with ourcollaborators from the Netherlands Cancer Institute (Lucas Jae and ThijnBrummelkamp) a genome-wide haploid genetic screen was performed,in which muta-genized haploid cells were enriched for defective Lassavirus entry (Figure). The identified mutations in those enriched cellswere present in the already known dystroglycanopathy genes and, mostimportantly, in several new candidate genes. The newly identified candi-date genes were successfully tested in our patient cohort of dystrogly-canopathy patients. Mutations in TMEM5 and SGK196 were found to bethe underlying cause of disease in three families. Future work will befocused on elucidating the functional role of the new candidate genes inthe O-mannosylation pathway.

Identification of genetic defects underlying dystroglycanopathies

Moniek RiemersmaHans van Bokhoven

Figure: Epidermal differentiation defects

were restored by APR-246/PRIMA-1MET

in human skin equivalents established

from p63 patient keratinocytes (muta-

tions R204W and R304W). Epidermal dif-

ferentiation marker gene expression of

K10 and Involucrin was examined by

immunofluorescence staining of skin

equivalents generated from wild type

keratinocytes and R204W and R304W

keratinocytes which were treated with

APR-246. Nuclei were stained with DAPI

(blue). Bar = 50 µM.

Figure: Finding the missing dystroglycanopathy genes. Schematic overview of our

approach to identify genetic defects underlying dystroglycanopathies.

46 NCMLS

Theme 7: Chemical & Physical Biology

ACS Nano 7:3797-807, 2013.

Over the past years, various types of high-molecular weight molecules,including siRNA, other oligonucleotides and proteins, have been deve-loped that show great potential as drug candidates, in particular for indi-vidualized medicine. However, due to the size and charge of these mole-cules, delivery strategies are a prerequisite to exploit them for the deve-lopment of new, patient-directed therapies. Cell-penetrating peptides(CPPs) are among the most easy to use, versatile, non-immunogenic, andnon-toxic of such delivery vehicles. Depending on the cargo, these shortcationic peptides can be linked to, or electrostatically complexed with,the cargo into self-assembling nano-particles. It has been observed inthe past, that various CPPs differ greatly in their capacity to mediate thecellular import of therapeutic oligonucleotides. However, the molecularbasis for these differences has not been clear. In this publication, weprovide new insights into the dynamic association/dissociation beha-viour of CPP-based nano-particles in contact with serum and the cell-surface. In particular we found that stability towards serum and sensiti-vity towards decomplexation by negatively charged oligosaccharides isa characteristic of highly active CPPs. These insights are a significantstep towards the rational design of new, more powerful CPPs, which willaid in the development of innovative drugs and research tools.

Efficient cellular delivery of therapeutic oligonucleotides

Sander van AsbeckRoland Brock

Ann Neurol 73:397-407, 2013.

Dermatomyositis (DM), polymyositis (PM) and inclusion body myositis(IBM) are autoimmune diseases in which particularly skeletal musclesare affected. Previously, disease-specific autoantibodies have beenidentified in sera of patients with DM and PM, but were not found in IBMpatients. We identified an IBM-specific autoantibody, anti-Mup44, usinghuman skeletal muscle proteins as target molecules and determined theidentity of its target protein, cytosolic 5’ nucleotidase 1A (cN-1A). Highlevels of anti-Mup44/cN-1A antibodies are present in 33% of IBMpatients, whereas they are almost absent in DM and PM. The mostimportant regions of cN-1A that are targeted by anti-Mup44/cN-1Aautoantibodies were mapped (Figure). Our studies not only demonstratethat IBM is associated with disease-specific autoimmunity, but havealso identified the first molecular marker for this disease. The identifica-tion of the target protein allows the development of highly specific testsfor their detection in patients’ sera. A patent application has been filedand a license-agreement was closed with the German company EUROIM-MUN to develop a blood test for this IBM-biomarker.

Blood test for muscle disease Inclusion Body Myositis

Helma PlukGer Pruijn

Figure: Electrostatic complexation of anionic cargo (here siRNA) as one of the mechanisms

by which a CPP can interact with cargo. The resultant nano-particles then are taken up by

endocytosis and once released into the cytosol, the siRNA can direct in a highly specific

way the RISC complex to the target mRNA, effectively silencing the pathogenic gene. Also

indicated are the interaction with serum proteins and the requirement for partial disinte-

gration of the nano-particle by the glycocalyx.

Figure: Using synthetic cN-IA peptide microarrays three IBM-autoantibody epitope

regions were identified.




The interior of the living cell is crowded with proteins and other macro-molecules packed together. It is a question of paramount importance tounderstand how cells have adapted to the phenomenon of crowding,which has been preserved through evolution. Here we developed a method based on microdroplets via microfluidicsto produce droplets that can be used as individual pL reactors to studycomplex enzymatic reactions under controlled conditions. We followedtranscription/translation reactions inside of the droplets of cell lysatewith DNA encoding for GFP. By controlled evaporation of droplets weachieved the concentration of cell lysate in the range of 200-250 mg/ml.10-fold increase in concentration of the reaction components inducedphase separation, forming the coacervate. mRNA production rate wasincreased significantly in this artificial cell-like compartment. Fits to thedata showed a two orders of magnitude larger binding constant betweenDNA and RNA-polymerase, and five to six times larger rate constant fortranscription in crowded environments, strikingly similar to in vivo rates.Our results thus impact on our understanding of how biochemical net-works function, as rates of enzymatic reactions determined in dilutesolution do not necessarily reflect in vivo rates.

Gene expression in crowded coacervates

Ekaterina SokolovaWilhelm Huck

J Am Chem Soc 135:16308-11, 2013.

Polymersomes, vesicles made out of amphiphilic block copolymers,have been developed as artificial analogues to phospholipidicorganelles. The high level of design of the polymersome membraneenables a good control over the shape and stiffness of the vesicle. Acommon vesicular shape found in nature is the tubule. Not only mito-chondriae, but also many bacteria contain a membrane that has beenstretched in one dimension. So far, polymersomes with this morpholo-gy have proven to be difficult to realize. We have discovered an easysphere-to-tubule transformation of polymeric vesicles that is based onthe addition of a crosslinker 1 (Figure). This transition proved to be veryfast (<1 min) and afforded tubular polymersomes up to a length of 2 µm.Furthermore we showed that the elongation could be reversed throughthe incorporation of a cleavable disulfide bridge inside the crosslinker.Concerning the advantages of tubular shapes we foresee applicationsfor these vesicles as drug delivery vehicles or artificial organelles.

Tubular polymersomes: a cross-linker-induced shape transformation

Matthijs van OersJan van Hest

Figure: Schematic drawing of the microfluidic device in which two droplet populations

with identical contents coexist: nonshrunk, homogeneous droplets, and shrunk, phase-

separated droplets.

Figure: Schematic representation of the shape transformation of polymersomes.

Cells are very demanding about their environment. Besides the appro-priate biochemical signals, they need a matrix of the right mechanicalproperties to proliferate, move, divide, differentiate, etc. For tissue engi-neering and wound healing applications, a lot of effort has been direct-ed at developing new hydrogel-based cell matrices. Artificial matricescommonly lack the required complex mechanical behaviour, whilstbiopolymer-based gels remain difficult to manipulate and, in somecases, to apply in humans. We developed a new synthetic hydrogel thatprecisely mimics the structure and mechanical properties of gels ofintermediate filaments –a class of cytoskeletal proteins– including thestrain stiffening behaviour. In addition, our hydrogel is thermallyresponsive: a low viscosity solution turns into an elastic gel above a spe-cific temperature, which is readily tuned by the polymer’s structure.Cooling reverses the process completely. We related the macroscopicmechanical behaviour to the polymer structure, but also laid out designrules to optimise next generations of hydrogels. Filament formationproves extremely important to control. Our gels are readily function-alised with biochemical signals and these functionalised materials arecurrently investigated as matrices for cell growth as well as for woundhealing applications.

48 NCMLS


Nature 493:651-5, 2013.

A new environment for cells

Paul KouwerAlan Rowan

Chem Sci 4: 4168–4174, 2013.

Vaccination is one of the most successful and cost-effective health inter-ventions preventing several millions of deaths every year worldwide.Dendritic cells (DCs) vaccination has been extensively explored toinduce robust T-cell responses against cancer. Although clinical trialsproves their potential in cancer immunotherapy, generating DCs in-vitrois laborious, time consuming and expensive. Recent efforts to developthe next generation vaccines against infectious diseases and cancer areaimed at bypassing antigen presenting cells (APCs) for T-cell activation,by direct triggering of the TCR/CD3 complex (signal-1) and co-stimulato-ry molecules (signal-2) on T-cells. We developed a polymeric ‘syntheticDCs’ (sDCs) platform decorated with both anti-CD3 (signal-1) and anti-CD28 (signal-2) antibodies that mimic long dendrites of natural DCs(Figure). This provides robust expansion of cytotoxic T-cells (CTLs) whencompared to other artificial APCs structures, such as solid micros-pheres. Furthermore, sDCs are capable to inhibit the formation of regu-latory (FoxP3+) T-cells that suppress immune function, demonstratingits potency of sDC to drive sustained activation of CTL responses. Ourfindings demonstrate the potency of our approach to mimic immune cellfunctions by fully synthetic supramolecular complexes and to exploit thepotential of sDCs in cancer immunotherapy.

Polymer-based synthetic dendritic cells: tailoring robust and multifunctional T cellresponses for cancer immunotherapy

Subhra MandalAlan Rowan

Figure: sDCs functionally mimics long dendrites of the natural DCs. Confocal image show-

ing sDC binding (A) and their accumulation (B) on T-cell surface. sDCs induces robust T-cell

activation by triggering enhanced IFNγ production (C) and T-cell proliferation (D), compared

to bead based APCs or solution T-cell factors.

Figure: The dilute aqueous polyisocyanopeptide solution (0.1%) is a low-viscosity

liquid when retrieved from the fridge (left). It froms a hydrogel when heated above

room temperature (right). Cooling reverses the process.


NCMLS Members

50 NCMLS Members NCMLS


Berden, Jo*: Research interests are focused on clinical and fundamental aspects of both autoimmunity and glomerular diseases.Berg, van den, Wim: Chronicity of joint inflammation and mechanisms of cartilage and bone destruction.Bousema, Teun: Research focuses on the epidemiology and transmission of malaria, specifically on transmission-reducing interventions. Hermans, Peter: Pathogenesis, immunology and epidemiology of paediatric infectious diseases.Joosten, Leo: Host defence mechanisms triggered by pathogenic micro-organisms resulting in chronic inflammation. Kullberg, Bart-Jan: Cytokines and innate host defense in infection, immuno-therapy, and therapy of fungal infection. Loo, van de, Fons: Cytokine signalling and advanced gene therapies for rheumatoid arthritis.Melchers, Willem: Molecular microbiology, specifically molecular mechanisms of fungal resistance. Netea, Mihai: Mechanisms of pattern recognition of fungal pathogens and the immune-pathogeneticity of sepsis. Rij, van, Ronald: Dengue virus – host interactions, innate immunity and RNA interference in insects and mammals.Sauerwein, Robert: Development and clinical testing of Plasmodium falciparum malaria vaccines. Schalkwijk, Joost: My group studies epidermal biology in relation to skin diseases. Simon, Anna: Research interests include hereditary and acquired autoinflammatory diseases.Verweij, Paul: The main research interest is the management of invasive fungal diseases.Wagener, Frank: Research focuses on the anti-oxidative, anti-inflammatory, and cytoprotective effects and gasotransmitters.Zeeuwen, Patrick: Cellular differentiation programs that regulate the formation and homeostasis of the epidermis.


Adema, Gosse: Molecular analysis & function of professional antigen presenting dendritic cells and T-reg cells.Boerman, Otto: Synthesis, optimization and characterization of radiotracers for molecularimaging and -medicine.Bogaart, van den, Geert: Exocytosis in immune cells.Cambi, Alessandra: Organisational dynamics of receptors & lipids at the plasma membrane using high res microscopy.Dolstra, Harry: Immune regulation and modulation of the graft-versus-tumor responses after stem cell transplantation.Figdor, Carl: Molecular mechanisms controlling antigen presenting cells, in particular dendritic cells.Friedl, Peter: Cell-matrix interactions & dynamic cell patterning during immune cell interactions and tumour invasion.Hilbrands, Luuk: Clinical research directed towards the induction of donor-specific tolerance after transplantation.Hoogerbrugge, Peter: Biology of childhood acute lymphoblastic leukemia (ALL) from both 'clinical' and ‘bench' perspectives. Jansen, Joop: Molecular mechanisms implicated in human leukemia and myelodysplastic syndromes.Joosten, Irma: Immunology and immunogenetics, in particular immunological tolerance in transplantation. Leeuwen, van, Frank: The mission our laboratory is to investigate the cell biology and genetics of childhood malignancies.Oosterwijk, Egbert: Targeted therapy of urologic malignancies, emphasis on antibodies as new therapeutic reagents.Reijden, van der, Bert: Molecular biology of leukemia, especially transcriptional regulation and protein ubiquitination.Spriel, van, Annemiek: Scientific interests include plasma membrane organization of antigen-presenting cells.Voort, van der, Robbert#: Immunotherapy of hematological malignancies with a focus on leukemia and multiple myeloma.Vries, de, Jolanda: Research interests include immunotherapy of cancer, in particular dendritic cell vaccination.Witte, de, Theo: Cellular immune responses after stem cell transplantation and cellular immunotherapy.


Buma, Pieter: Bioinspired scaffolds & tissue substitutes for regeneration of cartilage, bone & meniscus tissue.Feitz, Wout: Regenerative Medicine and paediatric urology.Hoff, Von den, Hans: Research focuses on wound healing and scarring after cleft palate repair.Jansen, John: Biomaterials, in particular the use of calcium phosphate ceramics as bone replacing materials.Kraan, van der, Peter: Research interests include the pathophysiology of osteoarthritis and cartilage biology. Kuppevelt, van, Toin: Role of extracellular matrix molecules, notably proteoglycans in health and disease. Leeuwenburg, Sander: Research interests include calcium phosphate ceramics, hydrogels, nanocomposites and biomolecule delivery.Meijer, Gert: Reconstructive medicine, especially intra- and extra-oral implants.Torensma, Ruurd: Role of immune regulating cells ovarian cancer & mesenchymal stem cells in wound repair.Vlag, van der, Johan: Research follows two main lines: (i) Glomerular diseases; (ii) Transplantation immunology.Walboomers, Frank: Biomaterials, in particular surface modification of (dental) implant materials.Wesseling, Pieter: Molecular and cellular dissection of tumour micro-environment interactions in brain tumours.Wolf, Katarina: Pericellular proteolysis in cancer invasion and metastasis: regulation and therapeutic targeting.


NCMLS members

51Annual Report 2013 NCMLS Members


Barentsz, Jelle: Functional and molecular imaging techniques in oncology.Heuvel, van den, Bert: Identification of novel biomarkers for OXPHOS disease.Heerschap, Arend: Research focuses on translational research, from in vitro NMR studies of tissues to MR of patients.Huynen, Martijn: Research interests revolve around comparative genomics and molecular biology.Koopman, Werner: Quantitative & mechanistic understanding of mitochondrial dynamics, function and regulation. Nijtmans, Leo: Biogenesis of mitochondria, in particular complexes involved in oxidative phosphorylation.Rodenburg, Richard: Biochemical and genetic characterization of mitochondrial energy metabolism in health and disease.Smeitink, Jan: Mitochondrial medicine, emphasis on defects underlying OXPHOS-system enzyme deficiencies.Spelbrink, Hans: Understanding & characterisation of mitochondrial DNA disorders.Wieringa, Bé: Research interests include cellular energy metabolism, cell dynamics and Myotonic Dystrophy Type 1.Willems, Peter: Metabolic disorders with special reference to genetic disorders of OXPHOS system.


Bindels, René: Regulation of ion transport processes in kidney and small intestine in health and disease. Deen, Peter: Molecular, cellular and structural biology of protein routing and regulation of water homeostasis.Drenth, Joost: Understanding of gastrointestinal disease, especially polycystic liver disorders.Fransen, Jack: Intracellular ultrastructural dynamics using immunoelectron microscopy and 3D & 4D confocal techniques.Hoenderop, Joost: Regulation of Ca2+ and Mg2+ transport, with a specific focus on transient receptor potential channels.Koenderink, Jan: Molecular interaction of membrane transport proteins and their ligands (substrates and inhibitors). Masereeuw, Roos: Regulation of drug transport under physiological and pathological conditions.Russel, Frans: Research interests include pharmacokinetics, drug transporters and toxicity.Swinkels, Dorine: Identification and characterization of factors affecting iron homeostasis and translation to the clinic.


Aschrifi, Armaz: Molecular neurobiology of synaptic development and plasticity.Bokhoven, van, Hans: Genetic and epigenetic networks that are disrupted in cognitive disorders.Brunner, Han: Research interests include the molecular basis of congenital malformations.Carels, Carine: Research interests include disrupted craniofacial and orofacial development. Collin, Rob: Research focuses on the development of novel therapeutic strategies for inherited retinal dystrophies.Coolen, Marcel: Research on the abnormal usage of genetic information in disease, especially epigenetics.Cremers, Frans: Identification and characterisation of novel genes implicated in inherited retinal disorders.Fischer, Simon: Molecular mechanisms underlying human speech and language development.Geurts van Kessel, Ad: Research interests include chromosome aberrations and cancer as well as technology development.Heesakkers, John: Investigate and test the (sub)urothelial barrier and signalling function on cellular and molecular level.Hollander, den, Anneke: The main research goal is to resolve the molecular basis of inherited blindness. Homberg, Judith: We focus on gene x envrionment interactions in psychiatric disorders.Hoogerbrugge, Nicoline: Research interests include the molecular basis of hereditary cancer and carcinogenesis.Huls, Gerwin: Translational hematology, MDS, AML.Kamminga, Leonie: Research aims to unravel epigenetic mechanisms regulating cellular identity during development.Kremer, Hannie: Research is focused on the unraveling of the molecular defects that underly hearing loss.Krieken, van, Han: Research interests focus on the understanding of the development of cancer.Kuiper, Roland: Identification of the genetic alterations associated with cancer predisposition and development.Lefeber, Dirk: Glycosylation defects and glycosylation disorders that result from defects in Golgi trafficking.Logie, Colin: Research interests include chromatin, chromatin structure and transcription.Marks, Hendrik: Research focuses on deciphering the regulatory mechanisms that maintain ESCs in the ground state. Martens, Gerard: Research interests include neurobiology- / -endocrinology, and cell and developmental biology.Martens, Joost: Transcriptional and epigenetic factors associated with oncofusion protein expression.Mulder, Klaas: Research on the mechanisms underlying human epidermal stem cell renewal & differentiation.Nadif Kasri, Nael: Research on the underlying molecular events involved in learning.Roepman, Ronald: Studying the protein connectivity in cilia and the severe consequences of its loss in ciliopathies.Schalken, Jack: Research interests include tumour cell biology, in particular prostate cancer. Schenck, Annette: Research aims to dissect the molecular networks & mechanisms underlying brain function.Stunnenberg, Henk: Our research aims at unravelling gene regulatory networks in human, mouse & malaria.Veenstra, Gert Jan: Research aims to elucidate gene regulation mechanisms during early vertebrate embryogenesis.Veltman, Joris: Research aims to uses genomics technologies to explain the causes of human disease (diagnostics).Wansink, Rick: Understanding the pathogenesis of myotonic dystrophy, in particular targets for molecular therapy.Zhou, Jo Huiqing: Elucidation of genetic and epigenetic mechanisms in developmental diseases.

52 NCMLS Members NCMLS


Brock, Roland: Our group is interested in: signal transduction in T cells and molecular targeting of cells. Buydens, Lutgarde: Research interests include chemometrics & the processing of (medical) multivariate images. Delft, van, Floris: Application of chemical tools to study biological phenomena, in particular bioorthogonal reactions.Hendriks, Wiljan: Research focuses on the signalling role of protein tyrosine phosphatases.Hest, van, Jan: The main research interest is the development of bio-inspired materials and processes.Huck, Wilhelm: The aim of our research is to exploit microdroplets technology to understand complex systems.Leenders, William: Research concentrates on the generation of novel cancer specific antibodies. Leeuwen, van, Jeroen: Research interests include cell biology with a primary interest in cell signalling and protein sorting.Pruijn, Ger: Biochemistry and molecular biology, with a specific focus on the molecular aspects of autoimmunity.Rowan, Alan: Design and synthesis of novel polymers, self-organizing molecules and ordered crystals.Rutjes, Floris: Synthesis of drug-like building blocks, i.e. small, highly functionalised enantiopure hetero-cycles.Vriend, Gert: Bioinformatics, macromolecular structure data, for answering biomedical questions. Zoelen, van, Joop: The role of polypeptide growth factors in cell proliferation, embryonic development and disease.

Names in blue: Our people from Radboud university medical center* retired in 2013# changed job in 2013

Names in red: Our people from Faculty of Science

Scientific publications 2013


54 Scientific publications 2013 NCMLS

Scientific publications 2013

Aarntzen, E.H.J.G., Srinivas, M., Figdor, C.G., Oyen, W.J.G. & Vries, I.J.M. de (2013). FLT-PET imaging for early identification of antigen-specificimmune responses in cancer patients. Journal of Nuclear Medicine, 54, 30-31.Aarntzen, E.H.J.G., Srinivas, M., Bonetto, F.J., Cruz, L.J., Verdijk, P., Schreibelt, G., Rakt, M.W.M.M. van de, Lesterhuis, W.J., Riel, M. van, Punt, C.J.A., Adema, G.J., Heerschap, A., Figdor, C.G., Oyen, W.J.G. & Vries, I.J.M. de (2013). Targeting of 111In-Labeled Dendritic Cell HumanVaccines Improved by Reducing Number of Cells. Clinical Cancer Research, 19(6), 1525-1533.Aarntzen, E.H.J.G., Srinivas, M., Radu, C.G., Punt, C.J.A., Boerman, O.C., Figdor, C.G., Oyen, W.J.G. & Vries, I.J.M. de (2013). In vivo imaging oftherapy-induced anti-cancer immune responses in humans. CELLULAR AND MOLECULAR LIFE SCIENCES, 70(13), 2237-57.Aarntzen, E.H.J.G., Srinivas, M., Schreibelt, G., Heerschap, A., Punt, C.J.A., Figdor, C.G., Oyen, W.J.G. & Vries, I.J.M. de (2013). Reducing cellnumber improves the homing of dendritic cells to lymph nodes upon intradermal vaccination. Oncoimmunology, 2(7), e24661.Aarntzen, E.H.J.G., Vries, I.J.M. de, Lesterhuis, W.J., Schuurhuis, D., Jacobs, J.F.M., Bol, K.F., Schreibelt, G., Mus, R.D.M., de Wilt, J.H., Haanen, J.B.,Schadendorf, D., Croockewit, A.J., Blokx, W.A.M., Rossum, M.M. van, Kwok, W.W., Adema, G.J., Punt, C.J.A. & Figdor, C.G. (2013). TargetingCD4(+) T-Helper Cells Improves the Induction of Antitumor Responses in Dendritic Cell-Based Vaccination. Cancer Research, 73(1), 19-29.Abaan, O.D., Hendriks, W.J., Uren, A., Toretsky, J.A. & Erkizan, H.V. (2013). Valosin containing protein (VCP/p97) is a novel substrate for the protein tyrosine phosphatase PTPL1. Experimental Cell Research, 319(1), 1-11.Abdollahi-Roodsaz, S., Koenders, M.I., Lent, P.L. van & Berg, W.B. van den (2013). Reply: To PMID 23860661. Arthritis and Rheumatism, 65(12),3314-6.Abdollahi-Roodsaz, S., Koenders, M.I., Walgreen, B., Bolscher, J., Helsen, M.M., Bersselaar, L.A. van den, Lent, P.L. van, Loo, F.A. van de & Berg, W.B. van den (2013). Toll-like receptor 2 controls acute immune complex-driven arthritis in mice by regulating the inhibitory Fcgammareceptor IIB. Arthritis and Rheumatism, 65(10), 2583-93.Abu-Amero, K.K., Jaeger, H.H.M., Plantinga, T.S., Netea, M.G. & Hassan, H.Y. (2013). Genetic variation of TLR2 and TLR4 among the Saudi Arabianpopulation: insight into the evolutionary dynamics of the Arabian Peninsula. Genetic Testing and Molecular Biomarkers, 17(2), 166-9.Adawy, A., Marks, K., Grip, W.J. de, Enckevort, J.P. van & Vlieg, E. (2013). The development of the depletion zone during ceiling crystallization:Phase shifting interferometry and simulation results. CRYSTENGCOMM, 15 (12), 2275-2286.Adawy, A., Rebuffet, E., Tornroth-Horsefield, S., Grip, W.J. de, Enckevort, J.P. van & Vlieg, E. (2013). High resolution protein crystals using an efficient convection-free geometry. Crystal Growth & Design, 13(2), 775-781.Adjobo-Hermans, M.J.W., Crosby, K.C., Putyrski, M., Bhageloe, A., Weeren, L. van, Schultz, C., Goedhart, J. & Gadella, T.W. (2013). PLCbeta isoforms differ in their subcellular location and their CT-domain dependent interaction with Galphaq. CELLULAR SIGNALLING, 25(1), 255-63.Aerts, D., Verhaeghe, T., Joosten, H.J., Vriend, G., Soetaert, W. & Desmet, T. (2013). Consensus engineering of sucrose phosphorylase: The outcome reflects the sequence input. BIOTECHNOLOGY AND BIOENGINEERING, 110(10), 2563-72.Aerts, D., Verhaeghe, T., Joosten, H.J., Vriend, G., Soetaert, W. & Desmet, T. (2013). Consensus engineering of sucrose phosphorylase: The outcome reflects the sequence input. BIOTECHNOLOGY AND BIOENGINEERING, 110(10), 2563-72.Agarwal, R., Chakrabarti, A, Shah, A., Gupta, D., Meis, J.F.G.M., Guleria, R., Moss, R. & Denning, D.W. (2013). Allergic bronchopulmonaryaspergillosis: review of literature and proposal of new diagnostic and classification criteria. Clinical and Experimental Allergy, 43(8), 850-73.Agha, Z., Iqbal, Z., Azam, M., Hoefsloot, L.H., Bokhoven, J.H.L.M. van & Qamar, R. (2013). A novel homozygous 10 nucleotide deletion in BBS10causes Bardet-Biedl syndrome in a Pakistani family. Gene, 519(1), 177-81.Ahmed Ali, U., Issa, Y., Bruno, M.J., Goor, H. van, Santvoort, H.C. van, Busch, O.R., Dejong, C.H., Nieuwenhuijs, V.B., Eijck, C.H. van, Dullemen, H.M. van, Fockens, P., Siersema, P.D., Gouma, D.J., Hooft, J.E. van, Keulemans, Y., Poley, J.W., Timmer, R., Besselink, M.G., Vleggaar, F.P.,Wilder-Smith, O.H.G., Gooszen, H.G., Dijkgraaf, M.G., Boermeester, M.A. & et. al., . (2013). Early surgery versus optimal current step-up practicefor chronic pancreatitis (ESCAPE): design and rationale of a randomized trial. BMC Gastroenterology, 13, 49.Ahout, I., Ferwerda, G. & Groot, R. de (2013). Elucidation and clinical role of emerging viral respiratory tract infections in children. Advances inExperimental Medicine and Biology, 764, 191-204.Ainsworth, S., Zomer, A.L., Jager, V.C.L. de, Bottacini, F., Hijum, S.A. van, Mahony, J. & Sinderen, D. van (2013). Complete Genome ofLactococcus lactis subsp. cremoris UC509.9, Host for a Model Lactococcal P335 Bacteriophage. Genome Announcements, 1(1), e00119-12.Ainsworth, S., Zomer, A.L., Mahony, J. & Sinderen, D. van (2013). Lytic Infection of Lactococcus lactis by Bacteriophages Tuc2009 and c2Triggers Alternative Transcriptional Host Responses. Applied and Environmental Microbiology, 79(16), 4786-98.Ajmal, M., Khan, M.I., Neveling, K., Tayyab, A., Jaffar, S., Sadeque, A., Ayub, H., Abbasi, N.M., Riaz, M., Micheal, S., Gilissen, C.F.H.A., Ali, S.H.,Azam, M., Collin, R.W.J., Cremers, F.P.M. & Qamar, R. (2013). Exome sequencing identifies a novel and a recurrent BBS1 mutation in Pakistanifamilies with Bardet-Biedl syndrome. Molecular Vision, 19, 644-53.Akkerman, O.W., Werf, T.S. van der, Boer, M. de, Beer, J.L. de, Rahim, Z., Rossen, J.W., Soolingen, D. van, Kerstjens, H.A. & Zanden, A.G. van der(2013). Comparison of 14 molecular assays for detection of Mycobacterium tuberculosis complex in bronchoalveolar lavage fluid. Journal ofClinical Microbiology, 51(11), 3505-11.Alexander, S., Weigelin, B., Winkler, F. & Friedl, P. (2013). Preclinical intravital microscopy of the tumour-stroma interface: invasion, metastasis,and therapy response. Current Opinion in Cell Biology, 25(5), 659-71.Alghamdi, H.S.A. & Jansen, J.A. (2013). Bone regeneration associated with nontherapeutic and therapeutic surface coatings for dental implantsin osteoporosis. Tissue Engineering Part B Reviews, 19(3), 233-53.Alghamdi, H.S.A., Bosco, R., Beucken, J.J. van den, Walboomers, X.F. & Jansen, J.A. (2013). Osteogenicity of titanium implants coated with calcium phosphate or collagen type-I in osteoporotic rats. Biomaterials, 34(15), 3747-57.Alghamdi, H.S.A., Cuijpers, V.M.J.I., Wolke, J.G.C., Beucken, J.J.J.P van den & Jansen, J.A. (2013). Calcium-phosphate-coated Oral ImplantsPromote Osseointegration in Osteoporosis. Journal of Dental Research, 92(11), 982-8.Alghamdi, H.S.A., Oirschot, B.A. van, Bosco, R., Beucken, J.J. van den, Aldosari, A.A., Anil, S. & Jansen, J.A. (2013). Biological response to titaniumimplants coated with nanocrystals calcium phosphate or type 1 collagen in a dog model. Clinical Oral Implants Research, 24(5), 475-83.Al-Hajoj, S., Varghese, B., Al-Habobe, F., Shoukri, M.M., Mulder, A. & Soolingen, D. van (2013). Current trends of Mycobacterium tuberculosismolecular epidemiology in Saudi Arabia and associated demographical factors. INFECTION GENETICS AND EVOLUTION, 16, 362-8.Al-Hajoj, S., Varghese, B., Ingen, J. van & Soolingen, D. van (2013). Mycobacterium riyadhense overlooked: we can only find what we are lookingfor. Journal of Infection In Developing Countries, 7(3), 293-4.Ali, S., Younis, M., Bangash, K. Sardar, Rauf, A., Anwar, K., Khurram, R., Khawaja, M. Athar, Qureshi, A., Akhter, S., Azam, M., Kiemeney, L.A.L.M.& Qamar, R. (2013). Common variants at 8q24 confer susceptibility to urothelial bladder cancer in the Pakistani population. Pakistan Journal OfZoology, 45(6), 1501-1509.Alken, A.P.B., Tan, E.C., Luursema, J.M., Fluit, C.R.M.G. & Goor, H. van (2013). Feedback activities of instructors during a trauma surgery course.American Journal of Surgery, 206(4), 599-604.

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Alsaad, N., Altena, R. van, Pranger, A.D., Soolingen, D. van, Lange, W.C.M. de, Werf, T.S. van der, Kosterink, J.G.W. & Alffenaar, J.W.C. (2013).Evaluation of co-trimoxazole in the treatment of multidrug-resistant tuberculosis. European Respiratory Journal, 42(2), 504-12.Alsaad, N., Laan, T. van der, Altena, R. van, Wilting, K.R., Werf, T.S. van der, Stienstra, Y., Soolingen, D. van & Alffenaar, J.W.C. (2013).Trimethoprim/sulfamethoxazole susceptibility of Mycobacterium tuberculosis. International Journal of Antimicrobial Agents, 42(5), 472-4.Altena, A.M. van, Akker, P.A.J. van den, Hullu, J.A. de, Ottevanger, P.B., Aalders, A.L., Gerritse, R., Happel, M., Hoekstra, M.P., Janssen, M.J.,Samlal, R.A., Smeets, K.M., Snijders, M.P., Vasmel, M.J., Vollebergh, J.H.A., Kiemeney, L.A.L.M. & Massuger, L.F.A.G. (2013). Efficacy of aRegional Network for Ovarian Cancer Care. Obstetrics and Gynecology, 122(3), 668-675.Amadori, S., Suciu, S., Stasi, R., Salih, H.R., Selleslag, D., Muus, P., Fabritiis, P. De, Venditti, A., Ho, A.D., Lubbert, M., Thomas, X., Latagliata, R.,Halkes, C.J., Falzetti, F., Magro, D., Guimaraes, J.E., Berneman, Z., Specchia, G., Karrasch, M., Fazi, P., Vignetti, M., Willemze, R., Witte, T.J. de &Marie, J.P. (2013). Sequential Combination of Gemtuzumab Ozogamicin and Standard Chemotherapy in Older Patients With Newly DiagnosedAcute Myeloid Leukemia: Results of a Randomized Phase III Trial by the EORTC and GIMEMA Consortium (AML-17). Journal of Clinical Oncology,31(35), 4424-30.Ameling, S., Herda, L.R., Hammer, E., Steil, L., Teumer, A., Trimpert, C., Dorr, M., Kroemer, H.K., Klingel, K., Kandolf, R., Volker, U. & Felix, S.B.(2013). Myocardial gene expression profiles and cardiodepressant autoantibodies predict response of patients with dilated cardiomyopathy toimmunoadsorption therapy. European Heart Journal, 34(9), 666-75.Amiri, H., Bordonali, L., Lascialfari, A., Wan, S., Monopoli, M.P., Lynch, I., Laurent, S. & Mahmoudi, M. (2013). Protein corona affects the relaxivity and MRI contrast efficiency of magnetic nanoparticles. Nanoscale, 5(18), 8656-65.Amiri, H., Saeidi, K., Borhani, P., Manafirad, A., Ghavami, M. & Zerbi, V. (2013). Alzheimer’s disease: pathophysiology and applications ofmagnetic nanoparticles as MRI theranostic agents. ACS Chemical Neuroscience, 4(11), 1417-29.Andeweg, C.S., Bleichrodt, R.P. & Goor, H. van (2013). Reply to letter: “the role of abdominal imaging in cases with a high probability of acuteleft-sided colonic diverticulitis based on a clinical scoring system”. Annals of Surgery, 258(2), e15.Angelen, A.A. van, Glaudemans, B., Kemp, A. van der, Hoenderop, J.G.J. & Bindels, R.J.M. (2013). Cisplatin-induced injury of the renal distalconvoluted tubule is associated with hypomagnesaemia in mice. Nephrology Dialysis Transplantation, 28(4), 879-89.Angelen, A.A. van, San Cristobal, P., Pulskens, W.P., Hoenderop, J.G.J. & Bindels, R.J.M. (2013). The impact of dietary magnesium restriction onmagnesiotropic and calciotropic genes. Nephrology Dialysis Transplantation, 28(12), 2983-93.Angiari, S., Rossi, B., Piccio, L., Zinselmeyer, B.H., Budui, S., Zenaro, E., Bianca, V. Della, Bach, S.D., Scarpini, E., Bolomini-Vittori, M.,Piacentino, G., Dusi, S., Laudanna, C., Cross, A.H., Miller, M.J. & Constantin, G. (2013). Regulatory T cells suppress the late phase of the immuneresponse in lymph nodes through P-selectin glycoprotein ligand-1. Journal of Immunology, 191(11), 5489-500.Anil, S., Cuijpers, V.M.J.I., Preethanath, R.S., Aldosari, A.A. & Jansen, J.A. (2013). Osseointegration of oral implants after delayed placement inrabbits: a microcomputed tomography and histomorphometric study. International Journal of Oral & Maxillofacial Implants, 28(6), 1506-11.Anukam, K.C., Macklaim, J.M., Gloor, G.B., Reid, G., Boekhorst, J., Renckens, B.A.M., Hijum, S.A. van & Siezen, R.J. (2013). Genome Sequence ofLactobacillus pentosus KCA1: Vaginal Isolate from a Healthy Premenopausal Woman. PLoS ONE, 8(3), e59239.Ariani, F., Mari, F., Amitrano, S., Di Marco, C., Artuso, R., Scala, E., Meloni, I., Della Volpe, R., Rossi, A. de, Bokhoven, J.H.L.M. van & Renieri, A.(2013). Exome sequencing overrides formal genetics: ASPM mutations in a case study of apparent X-linked microcephalic intellectual deficit.Clinical Genetics, 83(3), 288-90.Arias-Mendoza, F., Payne, G.S., Zakian, K., Stubbs, M., O’Connor, O.A., Mojahed, H., Smith, M.R., Schwarz, A.J., Shukla-Dave, A., Howe, F.,Poptani, H., Lee, S.-C., Pettengel, R., Schuster, S.J., Cunningham, D., Heerschap, A., Glickson, J.D., Griffiths, J.R., Koutcher, J.A., Leach, M.O. &Brown, T.R. (2013). Noninvasive Phosphorus Magnetic Resonance Spectroscopic Imaging Predicts Outcome to First-line Chemotherapy in NewlyDiagnosed Patients with Diffuse Large B-Cell Lymphoma. Academic Radiology, 20, 1122-1129.Arif, M., Frank, W. & Khraiwesh, B. (2013). Role of RNA Interference (RNAi) in the Moss Physcomitrella patens. International Journal of MolecularSciences, 14(1), 1516-1540.Arjona, F.J., Chen, Y.X., Flik, G., Bindels, R.J.M. & Hoenderop, J.G.J. (2013). Tissue-specific expression and in vivo regulation of zebrafish orthologues of mammalian genes related to symptomatic hypomagnesemia. Pflugers Archiv-European Journal of Physiology, 465(10), 1409-21.Arts, R.J., Joosten, L.A.B., Meer, J.W. van der & Netea, M.G. (2013). TREM-1: intracellular signaling pathways and interaction with pattern recognition receptors. Journal of Leukocyte Biology, 93(2), 209-15.Asbeck, A.H. van, Beyerle, A., McNeill, H., Bovee-Geurts, P.H.M., Lindberg, S., Verdurmen, W.P.R., Hallbrink, M., Langel, U., Heidenreich, O. &Brock, R.E. (2013). Molecular Parameters of siRNA-Cell Penetrating Peptide Nanocomplexes for Efficient Cellular Delivery. ACS Nano, 7(5), 3797-807.Ascierto, P.A., Schadendorf, D., Berking, C., Agarwala, S.S., Herpen, C.M.L. van, Queirolo, P., Blank, C.U., Hauschild, A., Beck, J.T., St-Pierre, A.,Niazi, F., Wandel, S., Peters, M, Zubel, A. & Dummer, R. (2013). MEK162 for patients with advanced melanoma harbouring NRAS or Val600 BRAFmutations: a non-randomised, open-label phase 2 study. Lancet Oncology, 14(3), 249-56.Aslami, H., Pulskens, W.P., Kuipers, M.T., Bos, A.P., Kuilenburg, A.B.P. van, Wanders, R.J., Roelofsen, J., Roelofs, J.J., Kerindongo, R.P., Beurskens,C.J., Schultz, M.J., Kulik, W., Weber, N.C. & Juffermans, N.P. (2013). Hydrogen sulfide donor NaHS reduces organ injury in a rat model of pneumo-coccal pneumosepsis, associated with improved bio-energetic status. PLoS ONE, 8(5), e63497.Auner, H.W., Szydlo, R., Biezen, A. van, Iacobelli, S., Gahrton, G., Milpied, N., Volin, L., Janssen, J., Nguyen Quoc, S., Michallet, M., Schoemans, H.,Cheikh, J. El, Petersen, E., Guilhot, F., Schonland, S., Ahlberg, L., Morris, C., Garderet, L., Witte, T.J. de & Kroger, N. (2013). Reduced intensity-conditioned allogeneic stem cell transplantation for multiple myeloma relapsing or progressing after autologous transplantation: a study by theEuropean Group for Blood and Marrow Transplantation. Bone Marrow Transplantation, 48(11), 1395-400.Ba, W., Raadt, J. van der & Kasri, N. Nadif (2013). Rho GTPase signaling at the synapse: implications for intellectual disability. Experimental CellResearch, 319(15), 2368-74.Baaij, J.H.F. de, Groot Koerkamp, M.J., Lavrijsen, M., Zeeland, F. van, Meijer, H., Holstege, F.C., Bindels, R.J.M. & Hoenderop, J.G.J. (2013).Elucidation of the distal convoluted tubule transcriptome identifies new candidate genes involved in renal Mg2+ handling. American Journal ofPhysiology-Renal Physiology, 305(11), F1563-73.Baas, M.C., Besancon, A., Sawitzki, B., Mangez, C., Valette, F., Chatenoud, L. & You, S. (2013). Intragraft mechanisms associated with the immu-nosuppressive versus the tolerogenic effect of CD3 antibodies in a mouse model of islet allografts. Transplantation Proceedings, 45(5), 1895-8.Baas, M.C., Gerdes, V.E., Berge, I.J. Ten, Heutinck, K.M., Florquin, S., Meijers, J.C. & Bemelman, F.J. (2013). Treatment with everolimus is associa-ted with a procoagulant state. Thrombosis Research, 132(2), 307-11.Baas, M.C., Kers, J., Florquin, S., Fijter, J.W. de, Heide, J.J. van der, Weerman, M.A. van den Bergh, Berge, I.J. Ten & Bemelman, F.J. (2013).Cyclosporine versus everolimus: effects on the glomerulus. Clinical Transplantation, 27(4), 535-40.Badali, H., Fernández-González, M., Mousavi, B., Illnait-Zaragozi, M.T., González-Rodríguez, J.C., Hoog, G.S. de & Meis, J.F.G.M. (2013).Chromoblastomycosis due to Fonsecaea pedrosoi and F. monophora in Cuba. MYCOPATHOLOGIA, 175(5-6), 439-44.Badali, H., Vaezi, A., Haghani, I., Yazdanparast, S.A., Hedayati, M.T., Mousavi, B., Ansari, S., Hagen, F., Meis, J.F.G.M. & Chowdhary, A. (2013).Environmental study of azole-resistant Aspergillus fumigatus with TR34 /L98H mutations in the cyp51A gene in Iran. Mycoses, 56(6), 659-63.

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Badali, H., Yazdanparast, S.A., Bonifaz, A., Mousavi, B., Hoog, G.S. de, Klaassen, C.H. & Meis, J.F.G.M. (2013). Veronaea botryosa: molecularidentification with amplified fragment length polymorphism (AFLP) and in vitro antifungal susceptibility. MYCOPATHOLOGIA, 175(5-6), 505-13.Baerveldt, E.M., Onderdijk, A.J., Kurek, D., Kant, M., Florencia, E.F., Ijpma, A.S., Spek, P.J. van der, Bastiaans, J., Jansen, P.A.M., Kilsdonk, J.W.J.van, Laman, J.D. & Prens, E.P. (2013). Ustekinumab improves psoriasis-related gene expression in noninvolved psoriatic skin without inhibitionof the antimicrobial response. British Journal of Dermatology, 168(5), 990-8.Baidjoe, A., Stone, W., Ploemen, I., Shagari, S., Grignard, L., Osoti, V., Makori, E., Stevenson, J., Kariuki, S., Sutherland, C., Sauerwein, R., Cox, J.,Drakeley, C. & Bousema, T. (2013). Combined DNA extraction and antibody elution from filter papers for the assessment of malaria transmissionintensity in epidemiological studies. Malaria Journal, 12, 272.Bakdash, G., Schneider, L.P., Capel, T.M. van, Kapsenberg, M.L., Teunissen, M.B.M. & Jong, E.C. de (2013). Intradermal application of vitamin D3increases migration of CD14 (+) dermal dendritic cells and promotes the development of Foxp3 (+) regulatory T cells. Human Vaccines &Immunotherapeutics, 9(2), 250-8.Bakdash, G., Sittig, S.P., Dijk, T. van, Figdor, C.G. & Vries, I.J.M. de (2013). The nature of activatory and tolerogenic dendritic cell-derived signalII. Frontiers in Immunology, 4, 53.Baker, D.J., Dawlaty, M.M., Wijshake, T., Jeganathan, K.B., Malureanu, L., Ree, J.H. van, Crespo-Diaz, R., Reyes, S., Seaburg, L., Shapiro, V.,Behfar, A., Terzic, A., Sluis, B. van de & Deursen, J.M.A. van (2013). Increased expression of BubR1 protects against aneuploidy and cancer andextends healthy lifespan. Nature Cell Biology, 15(1), 96-102.Baker, D.J., Weaver, R.L. & Deursen, J.M.A. van (2013). p21 both attenuates and drives senescence and aging in BubR1 progeroid mice. CellReports (SCI), 3(4), 1164-74.Bakker, O.J., Santvoort, H. van, Besselink, M.G., Boermeester, M.A., Eijck, C. van, Dejong, K., Goor, H. van, Hofker, S., Ali, U. Ahmed, Gooszen, H.G., Bollen, T.L. & Study, G. (2013). Extrapancreatic necrosis without pancreatic parenchymal necrosis: a separate entity in necrotising pancreatitis? Gut, 62(10), 1475-80.Balemans, M.C.M., Kasri, N.N., Kopanitsa, M.V., Afinowi, N.O., Ramakers, G., Peters, T.A., Beynon, A.J., Janssen, S.M., Summeren, R.C. van,Eeftens, J.M., Eikelenboom, N., Benevento, M., Tachibana, M., Shinkai, Y., Kleefstra, T., Bokhoven, J.H.L.M. van & Zee, C.E. van der (2013).Hippocampal dysfunction in the Euchromatin histone methyltransferase 1 heterozygous knockout mouse model for Kleefstra syndrome. HumanMolecular Genetics, 22(5), 852-66.Ballak, D.B., Stienstra, R., Hijmans, A.G.M., Joosten, L.A.B., Netea, M.G. & Tack, C.J.J. (2013). Combined B- and T-cell deficiency does not protectagainst obesity-induced glucose intolerance and inflammation. Cytokine, 62(1), 96-103.Ballouz, S., Liu, J.Y., George, R.A., Bains, N., Liu, A., Oti, M.O., Gaeta, B., Fatkin, D. & Wouters, M.A. (2013). Gentrepid V2.0: a web server for candidate disease gene prediction. BMC Bioinformatics, 14, 249.Barandun, L.J., Immekus, F., Kohler, P.C., Ritschel, T., Heine, A., Orlando, P., Klebe, G. & Diederich, F. (2013). High-affinity inhibitors ofZymomonas mobilis tRNA-guanine transglycosylase through convergent optimization. ACTA Crystallographica Section D-BiologicalCrystallography, 69(Pt 9), 1798-807.Barentsz, J., Villers, A. & Schouten, M. (2013). Reply to Letter to the Editor re: ESUR prostate MR guidelines. European Radiology, 23, 2322-2323.Bartels, S.J.J. (2013, Januari 24). DNA methylation code : in search of novel DNA methylation readers. Radboud Universiteit Nijmegen (230 pag.)(S.l.: s.n.). Prom./coprom.: prof. dr. ir. H.G. Stunnenberg & dr. A.B. Brinkman.Bartolini, B., Thelin, M.A., Svensson, L., Ghiselli, G., Kuppevelt, T.H. van, Malmstrom, A. & Maccarana, M. (2013). Iduronic Acid inchondroitin/dermatan sulfate affects directional migration of aortic smooth muscle cells. PLoS ONE, 8(7), e66704.Bartzela, T.N., Carels, C.E.L., Bronkhorst, E.M. & Jagtman, A.M. (2013). Tooth agenesis patterns in unilateral cleft lip and palate in humans.Archives of Oral Biology, 58(6), 596-602.Basak, G.W., Wreede, L.C. de, Biezen, A. van, Wiktor-Jedrzejczak, W., Halaburda, K., Schmid, C., Schaap, N.P., Dazzi, F., Borne, P.A. von dem,Petersen, E., Beelen, D., Abayomi, A., Volin, L., Buzyn, A., Gurman, G., Bunjes, D., Guglielmi, C., Olavarria, E. & Witte, T.J.M. de (2013). Donorlymphocyte infusions for the treatment of chronic myeloid leukemia relapse following peripheral blood or bone marrow stem cell transplantation.Bone Marrow Transplantation, 48(6), 837-42.Bastings, L., Beerendonk, C.C.M., Westphal, J.R., Massuger, L.F.A.G., Kaal, S.E.J., Leeuwen, F.E. van, Braat, D.D.M. & Peek, R. (2013).Autotransplantation of cryopreserved ovarian tissue in cancer survivors and the risk of reintroducing malignancy: a systematic review. HumanReproduction Update, 19(5), 483-506.Bates, S., Hall, R.A., Cheetham, J., Netea, M.G., MacCallum, D.M., Brown, A.J., Odds, F.C. & Gow, N.A. (2013). Role of the Candida albicans MNN1gene family in cell wall structure and virulence. BMC research notes, 6, 294.Bayjanov, J., Starrenburg, M.J., Sijde, M.R. van der, Siezen, R.J. & Hijum, S.A.F.T. van (2013). Genotype-phenotype matching analysis of 38Lactococcus lactis strains using random forest methods. 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Annual Report 2013

NCMLSNijmegen Centre for Molecular Life Sciences (NCMLS)

Postal address259 RIMLSP.O. Box 91016500 HB NijmegenThe Netherlands

Visiting addressGeert Grooteplein 286525 GA Nijmegen

T: +31 (0)24 361 07 07E: [email protected]: www.rimls.nl


Nijm

egen Centre for Molecular Life Sciences

Annual Report 2013N

CMLS

The NCMLS seeks to achieve greater insightsinto the complexity of living cells with thepurpose of obtaining a multifaceted know-ledge of both normal and pathologicalprocesses. The NCMLS will pursue its goalsin the interests of curiosity driven researchand education. The NCMLS aims to advanceinnovation in translational research based onthe integration of diverse scientific exper-tise in molecular and medical sciences.


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