Mechanism for electron transfer within and between proteins

Current Opinion in Chemical Biology

Volumn 7, Issue 5, 2003, Pages 551-556

  Page, Christopher C ^a   Moser, Christopher C ^a   Dutton, P Leslie ^a  

^a UNIVERSITY OF PENNSYLVANIA   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

AMINO ACID; PEPTIDE; PROTEIN; SUCCINATE DEHYDROGENASE;

CATALYSIS; DIFFUSION; ELECTRON TRANSPORT; GENE MUTATION; OXIDATION REDUCTION REACTION; PROTEIN ENGINEERING; REVIEW;

EID: 0142231009     PISSN: 13675931     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.cbpa.2003.08.005     Document Type: Review

References (37)

1. Gould S.J., Lewontin R.C. The spandrels of San Marco and the Panglossian paradigm: a critique of the adaptationist programme. Proc R Soc Lond B Biol Sci. 205:1979;581-598.
2. Pigliucci M., Kaplan J. The fall and rise of Dr Pangloss: adaptationism and the Spandrels paper 20 years later. Trends Ecol Evol. 15:2000;66-70.
3. Weiss M.A., Nakagawa S.H., Jia W.H., Xu B., Hua Q.X., Chu Y.C., Wang R.Y., Katsoyannis P.G. Protein structure and the Spandrels of San Marco: insulin's receptor-binding surface is buttressed by an invariant leucine essential for its stability. Biochemistry. 41:2002;809-819 The lively debate on how to remove the bias of the scientist lover's eye when it comes to understanding how living systems are designed is illustrated in a strictly biochemical context.
4. Darwin C: Origin of Species by Means of Natural Selection. New York: Earlton House; 1872.
5. Page C.C., Moser C.C., Chen X.X., Dutton P.L. Natural engineering principles of electron tunnelling in biological oxidation-reduction. Nature. 402:1999;47-52.
6. Moser C.C., Keske J.M., Warncke K., Farid R.S., Dutton P.L. Nature of biological electron-transfer. Nature. 355:1992;796.
7. Marcus R.A., Sutin N. Electron transfers in chemistry and biology. Biochim Biophys Acta. 811:1985;265-322.
8. Feng C.J., Kedia R.V., Hazzard J.T., Hurley J.K., Tollin G., Enemark J.H. Effect of solution viscosity on intramolecular electron transfer in sulfite oxidase. Biochemistry. 41:2002;5816-5821.
9. Crane B.R., Di Bilio A.J., Winkler J.R., Gray H.B. Electron tunneling in single crystals of Pseudomonas aeruginosa azurins. J Am Chem Soc. 123:2001;11623-11631.
10. Tezcan F.A., Crane B.R., Winkler J.R., Gray H.B. Electron tunneling in protein crystals. Proc Natl Acad Sci USA. 98:2001;5002-5006 Laying to rest the idea that a tunneling electron should somehow sense that it is moving between proteins rather than within a single protein.
11. Johansson M.P., Blomberg M.R.A., Sundholm D., Wikstrom M. Change in electron and spin density upon electron transfer to haem. Biochim Biophys Acta. 1553:2002;183-187.
12. Stuchebrukhov A.A. Tunneling currents in long-distance electron transfer reactions. V. Effective one electron approximation. J Chem Phys. 118:2003;7898-7906.
13. Kawatsu T., Kakitani T., Yamato T. Worm model for electron tunneling in proteins: consolidation of the pathway model and the Dutton plot. J Phys Chem B. 105:2001;4424-4435 An explicit connection between sophisticated tunneling current descriptions and simplified packing density descriptions of electron tunneling in protein.
14. Beratan D.N., Onuchic J.N., Hopfield J.J. Electron tunneling through covalent and noncovalent pathways in proteins. J Chem Phys. 86:1987;4488-4498.
15. Beratan D.N., Betts J.N., Onuchic J.N. Protein electron-transfer rates set by the bridging secondary and tertiary structure. Science. 252:1991;1285-1288.
16. Winkler J.R. Electron tunneling pathways in proteins. Curr Opin Chem Biol. 4:2000;192-198.
17. Jones M.L., Kurnikov I.V., Beratan D.N. The nature of tunneling pathway and average packing density models for protein-mediated electron transfer. J Phys Chem A. 106:2002;2002-2006 A theoretical comparison of the similarities and the few differences in expected packing and pathway rate deviations in a survey of intraprotein electron transfer with resolved structures.
18. van Amsterdam I.M.C., Ubbink M., Einsle O., Messerschmidt A., Merli A., Cavazzini D., Rossi G.L., Canters G.W. Dramatic modulation of electron transfer in protein complexes by crosslinking. Nat Struct Biol. 9:2002;48-52.
19. Huppman P., Arlt T., Penzkofer H., Schmidt S., Bibikova M., Dohse B., Oesterhelt D., Wachtveit J., Zinth W. Kinetics, energetics, and electronic coupling of the primary electron transfer reactions in mutated reaction centers of Blastochloris viridis. Biophys J. 82:2002;3186-3197 A thoughtful and thorough examination of how mutations in photosynthetic reaction centers affect the various basic parameters that determine electron tunneling rates, cautioning that any mutation close to redox centers can be expected to vary multiple parameters at once.
20. Tosha T., Yoshioka S., Hori H., Takahashi S., Ishimori K., Morishima I. Molecular mechanism of the electron transfer reaction in cytochrome P450(cam)-putidaredoxin: roles of glutamine 360 at the heme proximal site. Biochemistry. 41:2002;13883-13893.
21. Dohse B., Mathis P., Wachtveitl J., Laussermair E., Iwata S., Michel H., Oesterhelt D. Electron-transfer from the tetraheme cytochrome to the special pair In the Rhodopseudomonas viridis reaction-center - effect of mutations of tyrosine L162. Biochemistry. 34:1995;11335-11343.
22. Tetreault M., Rongey S.H., Feher G., Okamura M.Y. Interaction between cytochrome c2 and the photosynthetic reaction center from Rhodobacter sphaeroides: effects of charge-modifying mutations on binding and electron transfer. Biochemistry. 40:2001;8452-8462.
23. Kyritsis P., Huber J.G., Quinkal I., Gaillard J., Moulis J.-M. Intramolecular electron transfer between [4Fe-4S] clusters studied by proton magnetic resonance spectroscopy. Biochemistry. 36:1997;7839-7846.
24. Hurley J.K., Morales R., Martinez-Julvez M., Brodie T.B., Medina M., Gomez-Moreno C., Tollin G. Structure-function relationships in Anabaena ferredoxin/ferredoxin: NADP(+) reductase electron transfer: insights from site-directed mutagenesis, transient absorption spectroscopy and X-ray crystallography. Biochim Biophys Acta. 1554:2002;5-21 An unusually wide-ranging and thorough investigation of which mutational changes matter, which don't and why in an interprotein electron transfer system.
25. Miyashita O., Okamura M.Y., Onuchic J.N. Theoretical understanding of the interprotein electron transfer between cytochrome c(2) and the photosynthetic reaction center. J Phys Chem B. 107:2003;1230-1241 A pathway based perspective of why mutations often have little effect on tunneling rates, despite lying on tunneling pathways.
26. Daizadeh I., Medvedev D.M., Stuchebrukhov A.A. Electron transfer in ferredoxin: Are tunneling pathways evolutionarily conserved? Mol Biol Evol. 19:2002;406-415 A defense of evolutionarily conserved tunneling pathways despite minor mutational effects; ignores Darwin's principle of multiple utility.
27. Moser C.C., Page C.C., Chen X., Dutton P.L. Biological electron tunneling through native protein media. J Biol Inorg Chem. 2:1997;393-398.
28. Denton M.J., Marshall C.J., Legge M. The protein folds as platonic forms: new support for the pre-Darwinian conception of evolution by natural law. J Theor Biol. 219:2002;325-342.
29. Taverna D.M., Goldstein R.A. Why are proteins marginally stable? Proteins Struct Funct Genet. 46:2002;105-109.
30. Chen I.P., Mathis P., Koepke J., Michel H. Uphill electron transfer in the tetraheme cytochrome subunit of the Rhodopseudomonas viridis photosynthetic reaction center: evidence from site-directed mutagenesis. Biochemistry. 39:2000;3592-3602.
31. Sun D.P., Davidson V.L. Effects of engineering uphill electron transfer into the methylamine dehydrogenase-amicyanin-cytochrome c-551i complex. Biochemistry. 42:2003;1772-1776 A nice example of how to test the practical effect of uphill electron tunneling, by re-engineering the free energy of electron tunneling in a natural protein.
32. Leys D., Basran J., Talfournier F., Sutcliffe M.J., Scrutton N.S. Extensive conformational sampling in a ternary electron transfer complex. Nat Struct Biol. 10:2003;219-225 An excellent description of the general design principle that uses restricted diffusion to foster robust interprotein electron transfer.
33. Gutierrez A., Paine M., Wolf C.R., Scrutton N.S., Roberts G.C.K. Relaxation kinetics of cytochrome P450 reductase: Internal electron transfer is limited by conformational change and regulated by coenzyme binding. Biochemistry. 41:2002;4626-4637.
34. Chohan K.K., Jones M., Grossmann J.G., Frerman F.E., Scrutton N.S., Sutcliffe M.J. Protein dynamics enhance electronic coupling in electron transfer complexes. J Biol Chem. 276:2001;34142-34147.
35. Liang Z.X., Nocek J.M., Huang K., Hayes R.T., Kurnikov I.V., Beratan D.N., Hoffman B.M. Dynamic docking and electron transfer between Zn-myoglobin and Cytochrome b(5). J Am Chem Soc. 124:2002;6849-6859 Another example in which nature deliberately avoids optimizing tunneling to assure robust operation of an interprotein electron transfer system.
36. Munro A.W., Leys D.G., McLean K.J., Marshall K.R., Ost T.W.B., Daff S., Miles C.S., Chapman S.K., Lysek D.A., Moser C.C.et al. P450BM3: the very model of a modern flavocytochrome. Trends Biochem Sci. 27:2002;250-257.
37. Moser C.C., Page C.C., Cogdell R.J., Barber J., Wraight C.A., Dutton P.L. Length, time, and energy scales of photosystems. Adv Protein Chem. 63:2003;71-109 A survey of protein design issues facing bioenergetic proteins working within the rules of physical chemistry.