Structure and duplication of the centrosome

8/13/2019 Structure and duplication of the centrosome

1/4

Structure andduplication of thecentrosome

Juliette Azimzadeh1,* and MichelBornens2

1Department of Biochemistry and Biophysics,University of California, San Francisco, CA 94143,USA2Institut Curie, CNRS/UMR144, 75248 Paris,France

*Author for correspondence(e-mail: [email protected])

Journal of Cell Science 120, 2139-2142

Published by The Company of Biologists 2007

doi:10.1242/jcs.005231

The centrosome has evolved inmulticellular organisms from the basalbody/axoneme of the unicellularancestor (Azimzadeh and Bornens,

2004). It plays a major role in organizingthe microtubule cytoskeleton in animal

cells. During interphase, the centrosomeorganizes an astral array of microtubules(MTs) that participate in fundamentalcellular functions such as intracellulartrafficking, cell motility, cell adhesionand cell polarity. In proliferating cells,the centrosome starts duplicating just

before, or at, the onset of S phase and thetwo newly formed centrosomesparticipate in the assembly andorganization of the mitotic spindle, itsorientation with respect to cortical cues,and the late events of cytokinesis.

The animal centrosome consists of a pairof centrioles linked together throughtheir proximal regions by a matrixconsisting in part of large coiled-coilproteins of the pericentrin family, whichanchor other matrix components. Thecentrioles contain cylindrical arrays of

triplet MTs organized with nine-foldradial symmetry and the proximal region

is structurally similar to the basal bodiesof cilia and flagella. In animals,centrioles retain the ability to act as basalbodies by templating the assembly attheir distal end (the plus ends of thecentriole MTs) either of a primary ciliumor of beating cilia during ciliogenesis in

specialized cells. Recent discoverieshave revealed that cilia have crucial rolesin an increasing number of cellular anddevelopmental processes, establishing alink between dysfunctional cilia andseveral genetic diseases (for reviews, seeDavis et al., 2006; Bisgrove and Yost,2006; Dawe et al., 2007).

In post-mitotic cells, the centrosomecontains a mature centriole called themother centriole and an immaturecentriole assembled during the previouscell cycle, the daughter centriole, which

is about 80% the length of the mothercentriole (Chretien et al., 1997). Mother

2139Cell Science at a Glance

(See poster insert)

Structure and Duplication of the CentrosomeJuliette Azimzadeh and Michel Bornens

S

G2Mitosis

C. elegans

DrosophilaD-TACC

Asp

SAS-6/

SAS-5

SAS-4

G1/G0

Primaryciliumassembly

The centrosome cycle in mammalian cells

Spindle pole 1 Spindle pole 2

Cytokinesis

C-Nap1Nek2PP1

Rootletin

Distal appendages(dockingat the plasmamembrane)

Sub-distal appendages(Microtubule anchoring)

ODF2/CenexinNineinCep170Centriolin-Tubulin

+ Centrin

Mothercentriole

Daughtercentriole

Nudel, NudE, Lis1

Dynactin/p150glued

EB1

SatellitesPCM1/BBS4PericentrinNineinCentrin

MatrixPericentrin/kendrinAKAP450/CG-Nap

Microtubule anchoring

-TuRC

Microtubule release

DyneinDynactin

Polyglutamylated-tubulin

Cartwheel

CP110

Appendagesform

NuMaTPX2

CAP350-FOP-EB1 complex

ChlamydomonasBLD-10

hSAS-6 ?

DrosophilaSAS-4 ?

HumanCPAP ?

Chlamydomonas

-Tubulin

Chlamydomonas-Tubulin

CentrinhSAS6?

Centrobin?Nlp

Separase

Centriole

disorientation/disengagement

Licencing for duplication?

G1

DistalAppendages

Proximalsection ofboth centrioles

(Mother Centriole)

(Daughter Centriole)

Sub-distalAppendages

Matrix

0.2 m

jcs.biologists.org

Centrosome maturation

Centrosome separation

Procentriole elongation

Nek2(inducesC-Nap1

dissociation)

Recruitment ofspindle polecomponents

Plk1

Aurora A

Appendagesare no longer visible

Recruitment of -TuRC, matrixand appendage components

Initiation ofprocentriole

assembly

CDK2cyclin-A/E

Mps1

Plk4/SAK

Recruitment atprocentriole

assembly sites

ZYG-1

Central tubeformation

SPD-2

Initiation of

duplication

Assembly ofcentriole MTs

Cartwheelformation

Assembly of

centriole MTs

-TubulinGCP2GCP3

GCP4GCP5GCP6

GCP-WD/NEDD1 ?

-TuSC

Cap

-TuRC :

Microtubule nucleation

Journal of Cell Science 2007 (120, pp. 2139-2142)


2/4

2140

centrioles are distinguished by two setsof nine appendages at their distal ends(Paintrand et al., 1992), which arethought to be required for anchoringmicrotubules at the centriole and fordocking of centrioles at the plasmamembrane during ciliogenesis.

Centrosome functionsThe architecture of the microtubule arrayin differentiated cell types results notonly from the dynamic behaviour ofMTs but also from a balance betweenMT nucleation and MT-anchoringactivities at the centrosome. Duringinterphase, MTs are nucleated in thematrix associated with both mother anddaughter centrioles, but only the mothercentriole is able to anchor them on itsassociated sub-distal appendages (Piel et

al., 2000). Microtubules are nucleated bythe -tubulin ring complex (-TuRC). -Tubulin is present throughout the cellcycle in the matrix, close to the proximalwalls of centrioles. Its levels increasedramatically prior to mitosis,concomitantly with the recruitment ofMT-associated proteins required formitotic spindle formation. This process,centrosome maturation, is under thecontrol of the Polo-like and Aurora Akinases (for a review, see Blagden andGlover, 2003).

Following their nucleation by the -TuRC, MTs are either released into thecytoplasm or recaptured and anchored atthe centrosome. Several different MT-anchoring mechanisms have beenproposed. The subdistal appendages ofthe mother centriole are thought to be amajor site for MT anchoring, and thisactivity requires ninein, a component ofsub-distal appendages (Mogensen et al.,2000). In addition, ninein has beenshown to interact with the -TuRC andthus also ensures a link with MTnucleation (Delgehyr et al., 2005). OtherMT anchoring complexes are seeminglyalso present in the matrix, althoughpreferentially associate with the mothercentriole. Among them, the p150glued

subunit of the dynactin complex seemsto play an important role in collaborationwith the MT-associated protein EB1(Askham et al., 2002).

A recently described complex containingthe centrosome proteins CAP350 andFOP, and EB1, has also been proposed to

play a role in anchoring MTs at thecentrosome (Yan et al., 2006). Inaddition, centrosome anchoring capacityrequires pericentrosomal satellites. Thesatellites are non-membranous granulesof 70-100 nm composed of PCM1protein, which binds to centrosome

proteins such as centrin, ninein andpericentrin. The pericentrosomallocalization of the satellites is MT- anddynein/dynactin-dependent (Kubo et al.,1999; Dammermann and Merdes, 2002).The BBS4 protein, one of the proteinsinvolved in the Bardet-Biedl syndrome,a heterogeneous disease that results inpart from defective ciliogenesis, hasbeen shown to act as an adaptor proteinbetween PCM1 and p150glued (Kim et al.,2004).

In addition to its function in MT

organization, the centrosome could playa crucial role in cytokinesis. Anincreasing number of centrosomalproteins have been reported to participatein cytokinesis, such as centriolin, Cep55,CP110 and BBS6 (Gromley et al., 2005;Fabbro et al., 2005; Tsang et al., 2006;Kim et al., 2005). Other major transitionswhere centrosome activity couldimpinge on the cell division cycle are theG1-S and G2-M transitions (Jackman etal., 2003; Mikule et al., 2007; Uetake etal., 2007) (for a review, see Doxsey et al.,2005).

Centrosome duplicationDistinct phases of the centrosome cyclehave been identified. Disorientation, ordisengagement, corresponds to the lossof the duplicative orthogonal tightassociation between mother anddaughter centrioles. Disengagementoccurs during early G1 phase beforecompletion of cytokinesis (Piel et al.,2001) and requires the activity ofseparase, a protease that also drives theseparation of sister chromatids prior toanaphase (Tsou and Stearns, 2006).Whether separase acts directly orindirectly on the linkers betweenorthogonal centriole pairs, and the natureof those linkers, remains unknown.

The initiation of procentriole assemblyappears to take place before or at theonset of S phase. This idea is supportedby the early recruitment of centrin in theimmediate vicinity of parental centriolesin human cells. Centrin proteins are

ancient proteins that are associated withcentriole/basal bodies in most eukaryoticspecies, sometimes forming a veryintricate network for example, inChlamydomonas reinhardtii. Therequirement for centrin proteins in thecentrosome duplication process is not

mechanistically understood, becausedifferent conclusions have been drawnfrom studies of different species. It is notabsolute either, because the sequenceand functions of centrin appear to havegreatly diverged in the nematodeCaenorhabditis elegans (Azimzadeh andBornens, 2004).

In yeasts, centrin participates in thehalf-bridge characteristic of thecentrosome/SPB and is clearly requiredfor SPB duplication in both buddingand fission yeasts. Remarkably,

characterization of a centrin interactorcalled Sfi1p shows that the half-bridge-to-bridge transition that precedes theformation of the new SPB in buddingyeast corresponds with the assembly of anew half-bridge that has a mirror imagestructure with respect to the other half-bridge (Kilmartin, 2003; Li et al., 2006).Thus the first event in the SPB duplicationevent is the duplication of the half-bridge,which connects the SPB to the nucleus.This early duplication could reflect theneed to ensure that the daughtercentrosome/SPB maintains or re-

establishes an association with thedividing nucleus during cell division (seealso Jaspersen et al., 2006). This could bea general feature in most species in whichthe nucleusbasal-body connection iscrucial for cell polarity. Accordingly, alink between the centrosome and thenucleus has been conserved in manydivergent organisms and the continuity ofthis link must be preserved duringcentrosome reproduction (Bornens andAzimzadeh, 2007).

The molecular mechanisms underlyingcentriole assembly have been beststudied in C. elegans, in which fiveproteins essential for centrioleduplication have been identified. Afterfertilization of the C. elegans embryo,SPD-2 is first recruited to the parentalcentriole and allows the recruitment ofthe kinase ZYG-1, which in turns allowsthe recruitment of the SAS-6SAS-5complex (Pelletier et al., 2006; Delattreet al., 2006). Recruitment of SAS-5 andSAS-6 is required for the formation of

Journal of Cell Science 120 (13)


3/4

2141

the central tube, a structure onto whichsinglet microtubules are subsequentlyassembled in an SAS-4-dependentmanner (Pelletier et al., 2006). Althoughthe centriolar structure is noticeablydivergent in nematodes, this pathway ismost likely to be conserved in other

eukaryotes, because SAS-6 and SAS-4have orthologs in other species. Inparticular, human SAS-6 andDrosophilaSAS-4 and SAS-6 orthologs have beenshown to be essential for centrioleduplication (Leidel et al., 2005; Basto etal., 2006; Rodrigues-Martins et al.,2007). Human SAS-6 localizes to thecentrosome and its overexpressiontriggers centrosome amplification, whichsuggests a crucial role in centrioleassembly. In human cells, centrioleduplication has also been shown torequire centrobin, a centriole-associated

protein that localizes asymmetrically toprocentrioles and daughter centrioles(Zou et al., 2005).

The kinase Plk4/SAK is essential forcentriole duplication in both human andDrosophila (Habedanck et al., 2005;Bettencourt-Dias et al., 2005) and hasthus been proposed to be the functionalequivalent of C. elegans ZYG-1.Plk4/SAK could be an assembly-limitingfactor because overexpression ofPlk4/SAK leads to centrosomeamplification in both human and

Drosophila (Habedanck et al., 2005;Rodrigues-Martins et al., 2007).Plk4/SAK appears to act directlyupstream of the centriole assemblypathway. Indeed centriole amplificationinduced by SAK overexpression inDrosophila is suppressed when DSAS-4or DSAS-6 are lacking (Rodrigues-Martins et al., 2007). SAK, DSAS-4 andDSAS-6 are required not only forcanonical centriole duplication but alsofor de novo centriole assembly. A denovo assembly pathway for centrioleassembly that is turned off whencentrioles are present has beencharacterized in human cells and in thegreen algae Chlamydomonas(Khodjakov et al., 2000; Marshall et al.,2001; La Terra et al., 2005; Uetake et al.,2007). The fact that the same regulator(i.e. SAK) and the same downstreameffectors are required for both thecanonical and de novo pathwayssuggests that centriole biogenesis is atemplate-free process. The mothercentriole in canonical duplication could

thus be seen as a platform used toconcentrate the components required forprocentriole assembly (Rodrigues-Martins et al., 2007).

Canonical centrioles observed in mosteukaryotic species are thought to

assemble onto the cartwheel, a structurein the proximal region of the centriolethat is the first nine-fold-symmetricalstructure to appear during assembly. Amutation in BLD-10, the onlycomponent of the cartwheel identified todate, inhibits centriole assembly inChlamydomonas (Matsuura et al., 2004).Whether BLD-10 has true orthologs inother eukaryotes remains to beelucidated. Whereas the cartwheelpersists in mature basal bodies of ciliatedprotozoa, it is only transient in vertebrateproliferating cells, but the precise timing

of cartwheel disassembly during G2-Mis not known (Lemullois et al., 1988).

Procentriole elongation starts during lateS phase; the centriole reaches full lengthduring the following cell cycle. Themechanisms triggering centrioleelongation are poorly understood butappear to require -tubulin inChlamydomonas, because the -tubulinmutant BLD-2 forms short centriolesmade of singlet MTs instead of triplets.-tubulin is conserved in mammals andhas been proposed to be required for

centriole duplication, although itsprecise function remains unclear(Dutcher, 2003).

During late G2 phase, centrosomeseparation allows the formation of abipolar spindle. Centrosome separationis thought to require the disassembly ofa fibrous linker that mediates centrosomecohesion by connecting the two centriolepairs (but not the two centrioles within apair see above). C-Nap1 is found at theproximal end of parental centrioles andis proposed to serve as a docking site forthis linker. C-Nap1 interacts withrootletin, a conserved component of theciliary rootlet. The ciliary rootlet is acytoskeletal structure found in manyciliated cells that originates from thebasal body and extends proximallytoward the nucleus, providing structuralsupport for the cilium (Yang et al., 2005).Rootletin is, however, also found in cellsdevoid of a ciliary rootlet, forming fibersthat emanate from the proximal ends ofcentrioles. Centrosome cohesion is

regulated during the cell cycle byphosphorylation of C-Nap1 androotletin, which depends on the balancebetween NIMA-related kinase (Nek2)and protein phosphatase 1 (PP1)activities (Fry et al., 1998; Helps et al.,2000; Bahe et al., 2005; Yang et al.,

2006). C-Nap1 and rootletin do not seemto form a continuous linker between theparental centrioles, and it is thus believedthat other proteins are required forcentrosome cohesion.

The complete maturation of theprocentrioles into mother centriolesextends over one and a half cell cycles:it is completed only after two successivemitoses, culminating with the acquisitionof distal and sub-distal appendages.

Centrosome duplication is tightlycoupled to the cell cycle. In particular, ithas been shown that the activity of thecell cycle kinase CDK2, in complex withcyclin E or cyclin A, is required for theinitiation of centrosome duplication(Hinchcliffe et al., 1999; Meraldi et al.,1999). Intriguingly, cyclin E has acentrosome-binding domain essential forpromoting S-phase entry in a CDK2-independent manner (Matsumoto andMaller, 2004).

In addition to the above-mentioned

regulators, which must be activated in acell-cycle-dependent manner to triggercentriole duplication, a mechanism thatprecludes centriole re-duplication hasrecently been characterized. In thislicensing model, Tsou and Stearns (Tsouand Stearns, 2006) propose that centriolere-duplication is prevented by temporalseparation of licencing during anaphase,which would correspond to separase-dependent centriole disengagement, fromcentriole growth that requires S-phase-specific kinase activities.

How centrosome reproduction and celldivision cycle are precisely coupled is stilla matter of active research and has not yetled to a comprehensive picture that wouldfulfill Boveris vision of the centrosomeas the division organ coordinatingkaryokinesis and cytokinesis.

ReferencesAskham, J. M., Vaughan, K. T., Goodson, H. V. and

Morrison, E. E. (2002). Evidence that an interaction

between EB1 and p150Glued is required for the formation



4/4

2142

and maintenance of a radial microtubule array anchored at

the centrosome.Mol. Biol. Cell 13, 3627-3645.

Azimzadeh, J. and Bornens, M. (2004). The centrosome

in evolution. In Centrosomes in Development and Disease

(ed. E. A. Nigg), pp. 93-122. Weinheim: Wiley-VCH.

Bahe, S., Stierhof, Y. D., Wilkinson, C. J., Leiss, F. and

Nigg, E. A. (2005). Rootletin forms centriole-associated

filaments and functions in centrosome cohesion. J. Cell

Biol. 171, 27-33.

Basto, R., Lau, J., Vinogradova, T., Gardiol, A., Woods,

C. G., Khodjakov, A. and Raff, J. W. (2006). Flieswithout centrioles. Cell 125, 1375-1386.

Bettencourt-Dias, M., Rodrigues-Martins, A.,

Carpenter, L., Riparbelli, M., Lehmann, L., Gatt, M.,

Carmo, N., Balloux, F., Callaini, G. and Glover, D.

(2005). SAK/PLK4 is required for centriole duplication

and flagella development. Curr. Biol. 15, 2199-2207.

Bisgrove, B. W. and Yost, H. J. (2006). The roles of cilia

in developmental disorders and disease.Development133,

4131-4143.Blagden, S. P. and Glover, D. M. (2003). Polar

expeditions: provisioning the centrosome for mitosis.Nat.

Cell Biol. 5, 505-511.Bornens, M. and Azimzadeh, J. (2006). Origin andevolution of the centrosome. In Origins and Evolution of

Eukaryotic Endomembranes and Cytoskeleton (ed. G.

Jkely), http://www.Eurekah.com.

Chretien, D., Buendia, B., Fuller, S. D. and Karsenti,

E. (1997). Reconstruction of the centrosome cycle from

cryoelectron micrographs.J. Struct. Biol. 120, 117-133.Dammermann, A. and Merdes, A. (2002). Assembly of

centrosomal proteins and microtubule organization

depends on PCM-1.J. Cell Biol. 159, 255-266.

Davis, E. E., Brueckner, M. and Katsanis, N. (2006).

The emerging complexity of the vertebrate cilium: new

functional roles for an ancient organelle. Dev. Cell 11, 9-

19.

Dawe, H. R., Farr, H. and Gull, K. (2007).

Centriole/basal body morphogenesis and migration during

ciliogenesis in animal cells. J. Cell Sci. 120, 7-15.

Delattre, M., Canard, C. and Gonczy, P. (2006).

Sequential protein recruitment in C. elegans centriole

formation. Curr. Biol. 16, 1844-1849.

Delgehyr, N., Sillibourne, J. and Bornens, M. (2005).

Microtubule nucleation and anchoring at the centrosome

are independent processes linked by ninein function. J.

Cell Sci. 118, 1565-1575.Doxsey, S., McCollum, D. and Theurkauf, W. (2005).

Centrosomes in cellular regulation. Annu. Rev. Cell Dev.Biol. 21, 411-434.Dutcher, S. K. (2003). Long-lost relatives reappear:

identification of new members of the tubulin superfamily.

Curr. Opin. Microbiol. 6, 634-640.

Fabbro, M., Zhou, B., Takahashi, M., Sarcevic, B., Lal,

P., Graham, M. E., Gabrielli, B. G., Robinson, P. J.,

Nigg, E. A., Ono, Y. et al. (2005). Cdk1/Erk2- and Plk1-

dependent phosphorylation of a centrosome protein,

Cep55, is required for its recruitment to midbody and

cytokinesis developmental. Cell 9, 477-488.Fry, A. M., Mayor, T., Meraldi, P., Stierhof, Y. D.,

Tanaka, K. and Nigg, E. A. (1998). C-Nap1, a novel

centrosomal coiled-coil protein and candidate substrate of

the cell cycle-regulated protein kinase Nek2.J. Cell Biol.141, 1563-1574.Gromley, A., Yeaman, C., Rosa, J., Redick, S., Chen,

C., Mirabelle, S., Guha, M., Sillibourne, J. and Doxsey,

S. J. (2005). Centriolin anchoring of exocyst and SNARE

complexes at the midbody is required for secretory-vesicle-mediated abscission. Cell 123, 75-87.

Habedanck, R., Stierhof, Y., Wilkinson, C. J. and Nigg,

E. A. (2005). The Polo kinase Plk4 functions in centriole

duplication.Nat. Cell Biol. 7, 1140-1146.

Helps, N. R., Luo, X., Barker, H. M. and Cohen, P. T.

(2000). NIMA-related kinase 2 (Nek2), a cell-cycle-

regulated protein kinase localized to centrosomes, is

complexed to protein phosphatase 1.Biochem. J. 349, 509-

518.

Hinchcliffe, E. H., Li, C., Thompson, E. A., Maller, J.

L. and Sluder, G. (1999). Requirement of Cdk2-cyclin E

activity for repeated centrosome reproduction in Xenopus

egg extracts. Science 283, 851-854.

Jackman, M., Lindon, C., Nigg, E. A. and Pines, J.

(2003). Active cyclin B1-Cdk1 first appears oncentrosomes in prophase.Nat. Cell Biol. 5, 143-148.

Jaspersen, S. L., Martin, A. E., Glazko, G., Giddings,

T. H., Jr, Morgan, G., Mushegian, A. and Winey, M.

(2006). The Sad1-UNC-84 homology domain in Mps3

interacts with Mps2 to connect the spindle pole body with

the nuclear envelope.J. Cell Biol. 174, 665-675.

Khodjakov, A., Rieder, C. L., Sluder, G., Cassels, G.,Sibon, O. and Wang, C. L. (2002). De novo formation of

centrosomes in vertebrate cells arrested during S phase.J.

Cell Biol. 158, 1171-1181.Kilmartin, J. V. (2003). Sfi1p has conserved centrin-

binding sites and an essential function in budding yeast

spindle pole body duplication. J. Cell Biol. 162, 1211-1221.

Kim, J. C., Badano, J. L., Sibold, S., Esmail, M. A., Hill,

J., Hoskins, B. E., Leitch, C. C., Venner, K., Ansley, S.

J., Ross, A. J. et al. (2004). The Bardet-Biedl protein

BBS4 targets cargo to the pericentriolar region and is

required for microtubule anchoring and cell cycleprogression.Nat. Genet. 36, 462-470.

Kim, J. C., Ou, Y. Y., Badano, J. L., Esmail, M. A.,

Leitch, C. C., Fiedrich, E., Beales, P. L., Archibald, J.

M., Katsanis, N., Rattner, J. B. et al. (2005).

MKKS/BBS6, a divergent chaperonin-like protein linked

to the obesity disorder Bardet-Biedl syndrome, is a novel

centrosomal component required for cytokinesis. J. Cell

Sci. 118, 1007-1020.

Kubo, A., Sasaki, H., Yuba-Kubo, A., Tsukita, S. and

Shiina, N. (1999). Centriolar satellites: molecular

characterization, ATP-dependent movement toward

centrioles and possible involvement in ciliogenesis.J. Cell

Biol. 147, 969-980.

La Terra, S., English, C. N., Hergert, P., McEwen, B.F., Sluder, G. and Khodjakov, A. (2005). The de novo

centriole assembly pathway in HeLa cells: cell cycle

progression and centriole assembly/maturation. J. Cell

Biol. 168, 713-722.

Leidel, S., Delattre, M., Cerutti, L., Baumer, K. andGonczy, P. (2005). SAS-6 defines a protein familyrequired for centrosome duplication in C. elegans and in

human cells.Nat. Cell Biol. 7, 115-125.

Lemullois, M., Boisvieux-Ulrich, E., Laine, M. C.,

Chailley, B. and Sandoz, D. (1988). Development and

functions of the cytoskeleton during ciliogenesis in

metazoa.Biol. Cell 63, 195-208.

Li, S., Sandercock, A. M., Conduit, P., Robinson, C. V.,

Williams, R. L. and Kilmartin, J. V. (2006). Structural

role of Sfi1p-centrin filaments in budding yeast spindle

pole body duplicationJ. Cell Biol. 173, 867-877.

Marshall, W. F. and Rosenbaum, J. L. (2001).

Intraflagellar transport balances continuous turnover of

outer doublet microtubules: implications for flagellar

length control.J. Cell Biol. 155, 405-414.

Matsumoto, Y. and Maller, J. L. (2004). A centrosomal

localization signal in cyclin E required for Cdk2-

independent S phase entry. Science 306, 885-888.

Matsuura, K., Lefebvre, P. A., Kamiya, R. and Hirono,M. (2004). Bld10p, a novel protein essential for basal body

assembly in Chlamydomonas: localization to thecartwheel, the first ninefold symmetrical structure

appearing during assembly.J. Cell Biol. 165, 663-671.

Meraldi, P., Lukas, J., Fry, A. M., Bartek, J. and Nigg,E. A. (1999). Centrosome duplication in mammalian

somatic cells requires E2F and Cdk2-cyclin A. Nat. Cell

Biol. 1, 88-93.Mikule, K., Delaval, B., Kaldis, P., Jurcyzk, A.,

Hergert, P. and Doxsey, S. (2007). Loss of centrosome

integrity induces p38-p53-p21-dependent G1-S arrest.Nat. Cell Biol. 9, 160-170.

Mogensen, M., Malik, A., Piel, M., Bouckson-Castaing,

V. and Bornens, M. (2000). Microtubule minus-end

anchorage at centrosomal and non-centrosomal sites: therole of ninein.J. Cell Sci. 113, 3013-3023.

Paintrand, M., Moudjou, M., Delacroix, H. and

Bornens, M. (1992). Centrosome organization and

centriole architecture: their sensitivity to divalent cations.J. Struct. Biol. 108, 107-128.

Pelletier, L., OToole, E., Schwager, A., Hyman, A. A.

and Muller-Reichert, T. (2006). Centriole assembly in

Caenorhabditis elegans.Nature 444, 619-623.

Piel, M., Meyer, P., Khodjakov, A., Rieder, C. L. and

Bornens, M. (2000). The respective contributions of the

mother and daughter centrioles to centrosome activity and

behavior in vertebrate cells. J. Cell Biol. 149, 317-329.

Piel, M., Nordberg, J., Euteneuer, U. and Bornens, M.

(2001). Centrosome-dependent exit of cytokinesis in

animal cells. Science 291, 1550-1553.

Rodrigues-Martins, A., Riparbelli, M., Callaini, G.,Glover, D. M. and Bettencourt-Dias, M. (2007).

Revisiting the role of the mother centriole in centriole

biogenesis. Science (in press).Tsang, W. Y., Spektor, A., Luciano, D. J., Indjeian, V.

B., Chen, Z., Salisbury, J. L., Sanchez, I. and Dynlacht,

B. D. (2006). CP110 cooperates with two calcium-bindingproteins to regulate cytokinesis and genome stability.Mol.

Biol. Cell 17, 3423-3434.

Tsou, M. B. and Stearns, T. (2006). Mechanism limiting

centrosome duplication to once per cell cycle.Nature 442,

947-951.

Uetake, Y., Loncarek, J., Nordberg, J. J., English, C.

N., La Terra, S., Khodjakov, A. and Sluder, G. V.

(2007). Cell cycle progression and de novo centriole

assembly after centrosomal removal in untransformed

human cells.J. Cell Biol. 176, 173-182.

Yan, X., Habedanck, R. and Nigg, E. A. (2006). A

complex of two centrosomal proteins, CAP350 and FOP,

cooperates with EB1 in microtubule anchoring.Mol. Biol.

Cell 17, 634-644.

Yang, J., Gao, J., Adamian, M., Wen, X. H., Pawlyk,

B., Zhang, L., Sanderson, M. J., Zuo, J., Makino, C. L.and Li, T. (2005). The ciliary rootlet maintains long-term

stability of sensory cilia. Mol. Cell. Biol. 25, 4129-4137.

Yang, J., Adamian, M. and Li, T. (2006). Rootletin

interacts with C-Nap1 and may function as a physical

linker between the pair of centrioles/basal bodies in cells.Mol. Biol. Cell 17, 1033-1040.Zou, C., Li, J., Bai, Y., Gunning, W. T., Wazer, D. E.,

Band, V. and Gao, Q. (2005). Centrobin: a novel daughter

centriole-associated protein that is required for centriole

duplication.J. Cell Biol. 171, 437-445.


Cell Science at a Glance on the Web

Electronic copies of the poster insert are

available in the online version of this ar ticleat jcs.biologists.org. The JPEG images canbe downloaded for printing or used asslides.

Documents

Structure and duplication of the centrosome