The 2004 Benjamin Franklin Medal in Chemistry presented to Harry B. Gray

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<ul><li><p>Journal of the Franklin Institute 342 (2005) 586591</p><p>The 2004 Benjamin Franklin Medal in Chemistry</p><p>tunneling mediated by the molecules separating donor and acceptor. Tunneling timetables</p><p>ARTICLE IN PRESS</p><p>www.elsevier.com/locate/jfranklin</p><p>0016-0032/$30.00 r 2005 The Franklin Institute. Published by Elsevier Ltd. All rights reserved.</p><p>doi:10.1016/j.jfranklin.2005.04.015</p><p>Tel.: +1 302 831 1546; fax: +1 302 831 6335.</p><p>E-mail address: theopold@udel.edu.have been established for various intervening media. Important biological processes like</p><p>respiration and photosynthesis depend on facile electron transfer, and Grays contribution</p><p>serves as the fundamental basis for understanding these and many related reactions.</p><p>r 2005 The Franklin Institute. Published by Elsevier Ltd. All rights reserved.</p><p>Keywords: Electron transfer; Proteins; Franklin medalpresented to Harry B. Gray</p><p>Klaus H. Theopold</p><p>Department Chemistry and Biochemistry, University of Delaware, Newark, DE 19716, USA</p><p>Abstract</p><p>The Franklin Institute, Philadelphia, Pennsylvania, awarded the 2004 Benjamin Franklin</p><p>Medal in Chemistry to Harry B. Gray for his pioneering contributions in the eld of electron</p><p>transfer in metalloproteins. In a series of elegant and challenging experiments beginning in the</p><p>late 70s, Gray and his coworkers have shown that the transfer of electrons in metalloproteins</p><p>can proceed over long distances (~ 20 A) and at fast rates. These experiments have involved the</p><p>regiospecic functionalization of structurally characterized electron transfer proteins with</p><p>ruthenium complexes, coupled with laser excitation and transient spectroscopy. Probing the</p><p>effects of thermodynamic driving force, temperature, donoracceptor distance and electronic</p><p>coupling, Gray has shaped our detailed current understanding of the principles governing</p><p>biological electron ow. The mechanism of electron transfer has been identied as electron</p></li><li><p>ARTICLE IN PRESS</p><p>K.H. Theopold / Journal of the Franklin Institute 342 (2005) 586591 5871. Introduction and background</p><p>Redox reactions, i.e. reactions involving reduction (addition of electrons) andoxidation (removal of electrons), are among the most important and fundamentalchemical transformations. Beyond the obvious thermodynamic constraints, whichare readily understood in terms of the redox potentials of electron donors andacceptors, there also arise kinetic considerations. Rates of electron transfer reactionsspan a wide range, and the investigation of the mechanisms and rates of electrontransfer in particular between metal complexeshas been an active area ofresearch in the second half of the twentieth century [1].Two major classes of reactions have been identied, namely inner sphere and</p><p>outer sphere electron transfer processes. The former involve facilitation of theelectron transfer through bridging ligands; they are exemplied by the classicreaction of two coordination compounds in aqueous solution shown in Eq. (1) [2]:</p><p>CIIIo NH35Cl 2 CrIIOH26</p><p> 2 ! CoIIOH36 2 CrIIIOH25Cl</p><p> 2 5 NH3.(1)</p><p>Outer sphere electron transfer, on the other hand, merely relies on momentaryclose approach of the reactants by diffusion. Much effort has been expended on thedetermination of rates of degenerate self exchange reactions [3], such as the onegiven in Eq. (2), an acknowledged outer sphere electron transfer.</p><p>FeIIOH26 2 FeIIIOH26</p><p> 3 ! FeIIIOH26 3 FeIIOH26</p><p> 2,</p><p>ket22C 3:3M1s1;DGz 16:7 kcal=mol. 2Such thermoneutral reactions DG0 0 provide intrinsic activation barriers</p><p>unaffected by a thermodynamic driving force. In 1983 Henry Taube won the NobelPrize in Chemistry for his experimental work in the area of electron transferreactions [4].In parallel to the experiments, a theoretical treatment of outer sphere electron</p><p>transfer was developed by Marcus [5]. His theory, summarized in expressions such asEq. 3, allowed the calculation of activation barriers and absolute rate constants fromrst principles, taking into account reorganization energies (l), thermodynamicdriving forces DGo, and electronic coupling between donor and acceptor (HAB) [6]:</p><p>ket 4p3=h2lkBT 1=2</p><p>H2AB exp DGo l2=4lkBT </p><p>. (3)</p><p>Rudi Marcus won the 1992 Nobel Prize in Chemistry for the development of thetheory that carries his name [7].Electron transfer processes play a vital role in biology [8]. Life sustaining processes</p><p>such as respiration, photosynthesis, nitrogen xation, and many others rely on thetransfer of electrons between biomolecules. However, biological electron donors andacceptors typically metal complexes are often shrouded in proteins, preventingthem from attaining close contact. Based on the established notions about electrontransfer reactions, such long transfer distances should lead to extremely slow</p><p>electron transfer rates. And yet, electrons are apparently transferred, over distances</p></li><li><p>istry of transition metal complexes proved instrumental for carrying out thesestudies. While this experiment was only the rst of many to come, it has been called a</p><p>ARTICLE IN PRESS</p><p>K.H. Theopold / Journal of the Franklin Institute 342 (2005) 586591588milestone and having revolutionized the eld.The distance dependence of electron transfer rates was an obvious next issue, and</p><p>Gray designed and carried out experiments with various proteins (i.e. cytochrome c,azurin, plastocyanin, myoglobin, cytochrome b562, HiPIP) that had beenfunctionalized with ruthenium complexes in different locations, thus setting upcomparisons between electron transfer reaction equal in all respects except for thedonor acceptor distance [11]. A fundamental discovery emerging from theseexperiments was the observation that the matter intervening between the donor andacceptor had a profound effect on the electron transfer rates and moreimportantly their distance dependence. In the limit of innitely small directelectronic coupling (HAB) between the two redox partners, the electron transfer wasdescribed as tunneling through a barrier, the height and shape of which is determinedby accessible states of atoms along the electron transfer path [12]. This model leadsup to 20 A, and with rates on the millisecond time scale. In order to resolve thisapparent contradiction, Gray initiated a series of experiments in the 70s thatconrmed and ultimately explained the feasibility of rapid long-distance electrontransfer in proteins.A quote from a 1974 paper by Hopeld may serve to put Grays achievement into</p><p>the historical context [9]: Since electron-transfer proteins play a specic chemicalrole, one should be able to explain in quantitative physical terms how the observedfunctional properties are related to aspects of molecular structure. There are twomajor obstacles to attempting such an explanation at present. First, very little isknown about the relative geometry of the donor and acceptor during the electrontransfer process. Second, even when a geometry is known or surmised, themechanism of electron transfer is unsure. It will be shown that Grays work hassupplied the sought explanation in quantitative physical terms.</p><p>2. Rates of electron transfer in metalloproteins</p><p>To begin, Gray and his coworkers were the rst to show that electron transferfrom a ruthenium complex afxed to the outside of the iron containing proteincytochrome indeed proceeded with a rate constant of 20(75) s1 over a distance of15 A [10]. Several aspects of this experiment were groundbreaking and noteworthy.Thus, the regioselective functionalization of a protein of known molecular structure(determined by single crystal X-ray diffraction) with a redox active and substitutioninert metal complex created a situation in which the distance of the electron transferwas rigorously xed and known. It also simplied matters by making the electrontransfer an intramolecular event, removing any interference from bimolecularprotein protein binding steps. The experiment itself was carried out by acombination of photoinduced electron transfer, uorescence quenching, andtransient absorption spectroscopy; Grays extensive prior work in the photochem-to an exponential decrease of rate with distance, but with varying distance decay</p></li><li><p>constants (b</p><p>o</p><p>a</p><p>specic electron transfer path is unique. Indeed, Grays experiments with rutheniummodied wild-type and mutant cytochrome c showed that the measured electron</p><p>Harry Gray and his coworkers carried out the rst denitive experimentdemonstrating long-range electron transfer at rates consistent with metabolic</p><p>ARTICLE IN PRESS</p><p>K.H. Theopold / Journal of the Franklin Institute 342 (2005) 586591 589processes. Through an extended series of related measurements in which thermo-dynamic driving force, temperature, and donor/acceptor distance were system-atically varied and their effects probed, he has established our current detailedunderstanding of this class of reactions. While others have added to the developmentof the eld, Gray was the pioneer and the most prolic and consistent contributor.He is universally recognized as having made the greatest impact in the area ofbiological electron ow.</p><p>4. Medal legacy for the 2004 Benjamin Franklin Medal in Chemistry</p><p>1914 Edgar F. Smith (Cresson)Leading work in electrochemistry</p><p>1920 Svante A. Arrhenius (Franklin)Distinguished services to mankind in the eld of physical chemistry</p><p>1923 Joseph J. Thomson (Scott)For development of the physics of the electron and the identication of itas the atom of negative electricitytransfer rates did not correlate with the simple exponential distance decay model.They are better rationalized by a tunneling pathway model developed by Beratanand Onuchic [13]; this model accounts for the structural complexity of the protein byrecognizing different kinds of contacts along the tunneling path of the electron. Itallows searching for optimal coupling pathways between xed donor/acceptor pairs.The tunneling pathway model is now widely accepted as providing the bestdescription of long-distance electron transfer in proteins.</p><p>3. Conclusionsobvious consequences is that electrons can be transferred over much longer distancesin proteins than in water.Of course, proteins have complicated and varied structures, and consequently each1926(b-strands nd a-helices are common structural motifs of proteins). One of the</p><p>through a b-strand and b 1:3 (A1 for electron transfer through an a-helix</p><p>aforementi ned experiments are consistent with b 1:0 (A1 for electron tunneling</p><p>Whereas b is estimated as 3 4 A1 in vacuum and ca 1.7 A1 in water, theketH2AB exp bd do , (4)</p><p>, see Eq. (4)).Niels Bohr (Franklin)</p></li><li><p>1969 Henry Eyring (Cresson)</p><p>1979</p><p>1982</p><p>e</p><p>Harry B.f</p><p>1960. After,l</p><p>moved to t</p><p>7Medal of S</p><p>G</p><p>ARTICLE IN PRESS</p><p>K.H. Theopold / Journal of the Franklin Institute 342 (2005) 586591590(1994), the</p><p>the Nationcience (1986), the Linderstrm-Lang Prize (1991), the Basolo Medalibbs Medal (1994), the Chandler Medal (1999), the Harvey Prize (2000),Award (19 0), the Bailar Medal (1984), the Centenary Medal (1985), the National</p><p>Franklin Mhe California Institute of Technology. Grays honors include the E. C.emorial Award (1967), the Fresenius Award (1970), the Shoemakerconcurrent y held an adjunct appointment at Rockefeller University. In 1966 he</p><p>Universitya year as a postdoctoral fellow with Carl Ballhausen at Copenhagenhe joined the faculty of Columbia University in New York in 1961, andUniversity in 1957 and his Ph.D. in Chemistry from Northwestern University in</p><p>Institute oGray is the Arnold O. Beckman Professor of Chemistry at the CaliforniaTechnology. He received his B.S. in Chemistry from Western Kentucky5. Laureat biographyhemoglobin, and the observation of structural changes in proteinsphases and biomolecules), including energy transfer in solids, reactionmechanisms in liquid solutions, the binding of small molecules onlevel understanding of the dynamics in complex systems (condensed</p><p>spectroscopies, and their applications to gain fundamental molecular-</p><p>Pioneering the development of ultrafast and multi-dimensional2003 Robin M. Hochstrasser (Franklin)Thermodynamics and kinetics of organic reactionsRichard G. Brewer (Michelson)Study of the interaction of laser light with moleculesE. Bright Wilson Jr. (Cresson)Contributions to the understanding of molecular structure and dynamicsQuantum mechanical calculations of activation energies1972 George B. Kistiakowsky (Franklin)Contribution to the mechanics of atomic structures and theory of theorigin of spectrum lines</p><p>1928 Walther Nernst (Franklin)Contributions to exact methods of thermodynamics to electro- andthermochemistry</p><p>1930 William H. Bragg (Franklin)Development of method of determining molecular and crystal structureby reection of X-rays</p><p>1937 Robert A. Millikan (Franklin)Measurement of the charge of an electron; and description of Plancksconstant and the study of cosmic radiation</p><p>1937 Peter J. W. Debye (Franklin)Theory that molecules possess permanent dipole momentsal Academy of Sciences Award in Chemical Sciences (2003), the</p></li><li><p>University of Delaware, where he is currently professor of chemistry and an</p><p>[5] R.A. Marcus, Ann. Rev. Phys. Chem. 15 (1964) 155.</p><p>ARTICLE IN PRESS</p><p>K.H. Theopold / Journal of the Franklin Institute 342 (2005) 586591 591[6] R.A. Marcus, N. Sutin, Biochim. Biophys. Acta 811 (1985) 265.</p><p>[7] R.A. Marcus, Angew, Chem. Int. Ed. Engl. 32 (1993) 1111.</p><p>[8] S.J. Lippard, J.M. Berg, Principles of Bioinorganic Chemistry, University Science Books, Mill Valley,</p><p>CA, 1994, p. 231.</p><p>[9] J.J. Hopeld, Proc. Nat. Acad. Sci. USA 71 (1974) 3640.</p><p>[10] J.R. Winkler, D.G. Nocera, K.M. Yocom, E. Bordignon, H.B. Gray, J. Am. Chem Soc. 104 (1982)</p><p>5798.</p><p>[11] H.B. Gray, J.R. Winkler, in: V. Balzani (Ed.), Electron Transfer in Chemistry, vol. III, WileyVCH,</p><p>Weinheim, 2001, p. 3.</p><p>[12] J.R. Winkler, A.J. Di Bilio, N.A. Farrow, J.H. Richards, H.B. Gray, Pure Appl. Chem. 71 (1999)</p><p>1753.</p><p>[13] J.N. Onuchic, D.N. Beratan, J. Chem. Phys. 92 (1990) 722.associate director of the Center for Catalytic Science and Technology. Theopold haspublished 90 papers and holds two patents. He was named a Presidential YoungInvestigator in 1985, an Alfred P. Sloan Research Fellow in 1992, and a Fellow ofthe American Association for the Advancement of Science in 1995.</p><p>References</p><p>[1] M.L. Tobe, J. Burgess, Inorganic Reaction Mechanisms, Addison Wesley, Longman, New York,</p><p>1999, p. 376.</p><p>[2] H. Taube, H. Myers, J. Am. Chem. Soc. 76 (1954) 2103.</p><p>[3] T.J. Meyer, H. Taube, in: G. Wilkinson (Ed.), Comprehensive Coordination Chemistry, vol. 1,</p><p>Pergamon Press, Oxford, 1987, p. 331.</p><p>[4] H. Taube, Angew. Chem. Int. Ed. Engl. 23 (1984) 329.Centennial Nichols Medal (2003), as well as several national awards of the AmericanChemical Society (most notably the Priestley Medal (1991). He is a member of theNational Academy of Sciences, the American Academy of Arts and Sciences, theAmerican Philosophical Society, the Royal Danish Academy of Sciences and Letters,the Royal Swedish Academy of Sciences and the Royal Society of Great Britain. Heholds honorary doctorates from Northwestern University, the University ofChicago, the University of Rochester, the University...</p></li></ul>