Proton-coupled electron transfer: The mechanistic underpinning for radical transport and catalysis in biology

Philosophical Transactions of the Royal Society B: Biological Sciences

Volumn 361, Issue 1472, 2006, Pages 1351-1364

  Reece, Steven Y ^a   Hodgkiss, Justin M ^a   Stubbe, JoAnne ^a   Nocera, Daniel G ^a  

^a MASSACHUSETTS INSTITUTE OF TECHNOLOGY   (United States)

Author keywords

Amino acid radicals; Catalysis; Proton coupled electron transfer; Ribonucleotide reductase; Tunnelling; Tyrosine

Indexed keywords

AMINO ACID; CATALYSIS; ELECTRON; ENZYME ACTIVITY; FECAL COLIFORM; RADICAL;

ESCHERICHIA COLI;

EID: 33748376918     PISSN: 09628436     EISSN: None     Source Type: Journal    
DOI: 10.1098/rstb.2006.1874     Document Type: Conference Paper

References (104)

1. Aubert, C., Vos, M. H., Mathis, P., Eker, A. P. M. & Brettel, K. 2000 Intraprotein radical transfer during photoactivation of DNA photolyase. Nature 405, 586-590. (doi:10. 1038/35014644)
2. Baldwin, J., Krebs, C., Ley, B. A., Edmondson, D. E., Huynh, B. H. & Bollinger Jr, J. M. 2000 Mechanism of rapid electron transfer during oxygen activation in the R2 subunit of Escherichia coli ribonucleotide reductase. 1. Evidence for a transient tryptophan radical. J. Am. Chem. Soc. 122, 12 195-12 206. (doi:10.1021/ja001278u)
3. Barber, J., Ferreira, K., Maghlaoui, K. & Iwata, S. 2004 Structural model of the oxygen-evolving center of photosystem II with mechanistic implications. Phys. Chem. Chem. Phys. 6, 4737-4742. (doi:10.1039/b407981g)
4. Barry, B. & Babcock, G. T. 1987 Tyrosine radicals are involved in the photosynthetic oxygen-evolving system. Proc. Natl Acad. Sci. USA 84, 7099-7103. (doi:10.1073/pnas.84.20.7099)
5. Beratan, D. N., Onuchic, J. N. & Hopfield, J. J. 1987 Electron tunneling through covalent and noncovalent pathways in proteins. J. Chem. Phys. 86, 4488-4498. (doi:10.1063/1.452723)
6. Beratan, D. N., Onuchic, J. N., Betts, J. N., Bowler, B. E. & Gray, H. B. 1990 Electron-tunneling pathways in ruthenated proteins. J. Am. Chem. Soc. 112, 7915-7921. (doi:10.1021/ja00178a011)
7. Beratan, D. N., Betts, J. N. & Onuchic, J. N. 1991 Protein ET rates set by the bridging secondary and tertiary structure. Science 252, 1285-1288.
8. Bollinger Jr, J. M., Edmonson, D. E., Huynh, B. H., Filley, J., Norton, J. R. & Stubbe, J. 1991 Mechanism of assembly of the tyrosyl radical-dinuclear iron cluster cofactor of ribonucleotide reductase. Science 253, 292-298.
9. 2+ reaction by optical, EPR, and Mössbauer spectroscopies. J. Am. Chem. Soc. 116, 8024-8032. (doi:10.1021/ja00097a009)
10. Chang, C. J., Brown, J. D. K., Chang, M. C. Y., Baker, E. A. & Nocera, D. G. 2001 Electron transfer in hydrogen-bonded donor-acceptor supramolecules. In Electron transfer in chemistry, vol. 3.2.4 (ed. V. Balzani), pp. 409-461. Weinheim, Germany: Wiley-VCH.
11. Chang, C. J., Chng, L. L. & Nocera, D. G. 2003 Proton-coupled O-O activation on a redox platform bearing a hydrogen-bonding scaffold. J. Am. Chem. Soc. 125, 1866-1876. (doi:10.1021/ja028548o)
12. Chang, C. J., Chang, M. C. Y., Damrauer, N. H. & Nocera, D. G. 2004a Proton-coupled electron transfer: a unifying mechanism for biological charge transport, amino acid radical initiation and propagation, and bond making/breaking reactions of water and oxygen. Biochim. Biophys. Acta 1655, 13-28. (doi:10.1016/j.bbabio.2003.08.010)
13. Chang, M. C. Y., Yee, C. S., Nocera, D. G. & Stubbe, J. 2004b Site-specific replacement of a conserved tyrosine in ribonucleotide reductase with an aniline amino acid: a mechanistic probe for a redox-active tyrosine. J. Am. Chem. Soc. 126, 16 702-16 703. (doi:10.1021/ja044124d)
14. Chang, M. C. Y., Yee, C. S., Stubbe, J. & Nocera, D. G. 2004c Turning on ribonucleotide reductase by light-initiated amino acid radical generation. Proc. Natl Acad. Sci. USA 101, 6882-6887. (doi:10.1073/pnas.0401718101)
15. Chng, L. L., Chang, C. J. & Nocera, D. G. 2003 Catalytic O-O activation chemistry mediated by iron Hangman porphyrins with a wide range of proton-donating abilities. Org. Lett. 5, 2421-2424. (doi:10.1021/ol034581j)
16. Climent, I., Sjöberg, B.-M. & Huang, C. Y. 1991 Carboxyl-terminal peptides as probes for Escherichia coli ribonucleotide reductase subunit interaction: kinetic analysis of inhibition studies. Biochemistry 30, 5164-5171. (doi:10. 1021/bi00235a008)
17. Climent, I., Sjöberg, B.-M. & Huang, C. Y. 1992 Site-directed mutagenesis and deletion of the carboxyl terminus of Escherichia coli ribonucleotide reductase protein R2. Effects on catalytic activity and subunit interaction. Biochemistry 31, 4801-4807. (doi:10.1021/bi00135a009)
18. Cukier, R. I. 1994 Mechanism for proton-coupled electron-transfer reactions. J. Phys. Chem. 98, 2377-2381. (doi:10.1021/jl00060a027)
19. Cukier, R. I. 1995 Proton-coupled electron transfer through an asymmetric hydrogen-bonded interface. J. Phys. Chem. 99, 16 101-16 115. (doi:10.1021/j100043a060)
20. Cukier, R. I. 1996 Proton-coupled electron transfer reactions: evaluation of rate constants. J. Phys. Chem. 100, 15 428-15 443. (doi:10.1021/jp961025g)
21. Cukier, R. I. 1999 A theory for the rate constant of a dissociative proton-coupled electron-transfer reaction. J. Phys. Chem. A 103, 5989-5995. (doi:10.1021/jp990329a)
22. Cukier, R. I. 2002 A theory that connects proton-coupled electron-transfer and hydrogen-atom transfer reactions. J. Phys. Chem. B 106, 1746-1757. (doi:10.1021/jp012396m)
23. Cukier, R. I. & Nocera, D. G. 1998 Proton-coupled electron transfer. Annu. Rev. Phys. Chem. 49, 337-369. (doi:10. 1146/annurev.physchem.49.1.337)
24. Cukier, R. I., Daniels, S., Vinson, E. & Cave, R. J. 2002 Are hydrogen bonds unique among weak interactions in their ability to mediate electronic coupling? J. Phys. Chem. A 106, 11 240-11 247. (doi:10.1021/ jp026230c)
25. Damrauer, N. H., Hodgkiss, J. M., Rosenthal, J. & Nocera, D. G. 2004 Observation of proton-coupled electron transfer by transient absorption spectroscopy in a hydrogen-bonded, porphyrin donor-acceptor assembly. J. Phys. Chem. B 108, 6315-6321. (doi:10.1021/jp049296b)
26. z and the manganese cluster in the water oxidizing complex of photosystem II. Biochim. Biophys. Acta 1503, 164-186. (doi:10.1016/S0005- 2728(00)00221-8)
27. Debus, R. J., Barry, B. A., Sithole, I., Babcock, G. T. & McIntosh, L. 1988a Directed mutagenesis indicates that the donor to P680+ in photosystem II is tyrosine-161 of the D1 polypeptide. Biochemistry 27, 9071-9074. (doi:10. 1021/bi00426a001)
28. Debus, R. J., Barry, B. A., Babcock, G. T. & McIntosh, L. 1988b Site-directed mutagenesis identifies a tyrosine radical involved in the photosynthetic oxygen-evolving system. Proc. Natl Acad. Sci. USA 85, 427-430. (doi:10. 1073/pnas.85.2.427)
29. Decornez, H. & Hammes-Schiffer, S. 2000 Model proton-coupled electron transfer reactions in solution: predictions of rates, mechanisms, and kinetic isotope effects. J. Phys. Chem. A 104, 9370-9384. (doi:10.1021/jp001967s)
30. Dempsey, J. L., Esswein, A. J., Manke, D. R., Rosenthal, J., Soper, J. D. & Nocera, D. G. 2005 Molecular chemistry of consequence to renewable energy. Inorg. Chem. 44, 6879-6892. (doi:10.1021/ic0509276)
31. Deng, Y., Roberts, J. A., Peng, S. M., Chang, C. K. & Nocera, D. G. 1997 The amidinium-carboxylate salt bridge as a proton-coupled interface to electron transfer pathways. Angew. Chem. Int. Ed. Engl. 36, 2124-2127. (doi:10.1002/anie.199721241)
32. Ferreira, K. N., Iverson, T. M., Maghlaoui, K., Barber, J. & Iwata, S. 2004 Architecture of the photosynthetic oxygen-evolving center. Science 303, 1831-1838. (doi:10.1126/science.1093087)
33. Ge, J., Yu, G., Ator, M. A. & Stubbe, J. 2003 Pre-steady-state and steady-state kinetic analysis of E. coli class I ribonucleotide reductase. Biochemistry 42, 10071-10083. (doi:10.1021/bi034374r)
34. Ghaddar, T. H., Castner, E. W. & Isied, S. S. 2000 Molecular recognition and electron transfer across a hydrogen bonding interface. J. Am. Chem. Soc. 122, 1233-1234. (doi:10.1021/ja9930465)
35. Gray, H. B. & Winkler, J. R. 1996 Electron transfer in proteins. Annu. Rev. Biochem. 65, 537-561. (doi:10.1146/annurev.bi.65.070196.002541)
36. Hammes-Schiffer, S. 2001a Theoretical perspectives on proton-coupled electron transfer reactions. Acc. Chem. Res. 34, 273-281. (doi:10.1021/ ar9901117)
37. Hammes-Schiffer, S. 2001b Proton-coupled electron transfer. In Electron transfer in chemistry, vol. 1.1.5 (ed. V. Balzani), pp. 189-237. Weinheim, Germany: Wiley-VCH.
38. Hodgkiss, J. M., Damrauer, N. H., Pressé, S., Rosenthal, J. & Nocera, D. G. 2006. Temperature-isotope dependence reveals electron-transfer driven by proton-fluctuations in a hydrogen-bonded donor-acceptor assembly. J. Phys. Chem. B.
39. Hoganson, C. W. & Tommos, C. 2004 The function and characteristics of tyrosyl radical cofactors. Biochim. Biophys. Acta 1655, 116-122. (doi:10.1016/j.bbabio.2003.10.017)
40. Högbom, M., Galander, M., Andersson, M., Kolberg, M., Hofbauer, W., Lassmann, G., Nordlund, P. & Lendzian, F. 2003 Displacement of the tyrosyl radical cofactor in ribonucleotide reductase obtained by single-crystal high - field EPR and 1.4-Å X-ray data. Proc. Natl Acad. Sci. USA 100, 3209-3214. (doi:10.1073/pnas.0536684100)
41. Ito, N., Phillips, S. E. V., Yadav, K. D. S. & Knowles, P. F. 1994 Crystal structure of a free radical enzyme, galactose oxidase. J. Mol. Biol. 238, 794-814. (doi:10.1006/jmbi.1994.1335)
42. Jordan, A. & Reichard, P. 1998 Ribonucleotide reductases. Annu. Rev. Biochem. 67, 71-98. (doi:10.1146/annurev.biochem.67.1.71)
43. Kirby, J. P., van Dantzig, N. A., Chang, C. K. & Nocera, D. G. 1995 Formation of porphyrin donor-acceptor complexes via an amidinium-carboxylate salt bridge. Tetrahedron Lett. 36, 3477-3480. (doi:10.1016/00404039(95)00569-X)
44. Kirby, J. P., Roberts, J. A. & Nocera, D. G. 1997 Significant effect of salt bridges on electron transfer rate. J. Am. Chem. Soc. 119, 9230-9236. (doi:10.1021/ja970176+)
45. Kohen, A. & Klinman, J. P. 1998 Enzyme catalysis: beyond classical paradigms. Acc. Chem. Res. 31, 397-404. (doi:10.1021/ar9701225)
46. Krebs, C., Chen, S., Baldwin, J., Ley, B. A., Patel, U., Edmondson, D. E., Huynh, B. H. & Bollinger Jr, J. M. 2000 Mechanism of rapid electron transfer during oxygen activation in the R2 subunit of Escherichia coli ribonucleotide reductase. 2. Evidence for and consequences of blocked electron transfer in the W48F variant. J. Am. Chem. Soc. 122, 12 207-12 219. (doi:10.1021/ja001279m)
47. Liang, Z.-X. & Klinman, J. P. 2004 Structural bases of hydrogen tunneling in enzymes: progress and puzzles. Curr. Opin. Struct. Biol. 14, 648-655. (doi:10.1016/j.sbi.2004.10.008)
48. Lin, J., Balabin, I. A. & Beratan, D. N. 2005 The nature of aqueous tunneling pathways between electron-transfer proteins. Science 310, 1311-1313. (doi:10.1126/science.1118316)
49. Liu, S.-Y. & Nocera, D. G. 2005 Hangman salophens. J. Am. Chem. Soc. 127, 5278-5279. (doi:10.1021/ja042849b)
50. Loll, B., Kern, J., Saenger, W., Zouni, A. & Biesiadka, J. 2005 Towards complete cofactor arrangement in the 3.0 Å resolution structure of photosystem II. Nature 438, 1040-1044. (doi:10.1038/nature04224)
51. Maradufu, A., Cree, G. M. & Perlin, A. S. 1971 Stereochemistry of dehydrogenation by D-galactose oxidase. Can. J. Chem. 49, 3429-3437. (doi:10.1139/v71-575)
52. Marcus, R. A. & Sutin, N. 1985 Electron transfers in chemistry and biology. Biochim. Biophys. Acta 811, 265-322.
53. Mayer, J. M. 2004 Proton-coupled electron transfer: a reaction chemist's view. Annu. Rev. Phys. Chem. 55, 363-390. (doi:10.1146/annurev.physchem.55. 091602.094446)
54. Meunier, B., de Visser, S. P. & Shaik, S. 2004 Mechanism of oxidation reactions catalyzed by cytochrome P450 enzymes. Chem. Rev. 104, 3947-3980. (doi:10.1021/cr020443g)
55. Miller, M. A., Coletta, M., Mauro, J. M., Putnam, L. D., Farnum, M. F., Kraut, J. & Traylor, T. G. 1990 Carbon monoxide recombination in cytochrome c peroxidase: effect of the local heme environment on carbon monoxide binding explored through site-directed mutagenesis. Biochemistry 29, 1777-1791. (doi:10.1021/bi00459a017)
56. Moser, C. C., Keske, J. M., Warncke, K., Farid, R. S. & Dutton, P. L. 1992 Nature of biological electron transfer. Nature 355, 796-802. (doi:10.1038/355796a0)
57. Muir, T. W. 2003 Semisynthesis of proteins by expressed protein ligation. Annu. Rev. Biochem. 72, 249-289. (doi:10.1146/annurev.biochem.72.121801.161900)
58. Newmyer, S. L. & Ortiz de Montellano, P. R. 1995 Horseradish peroxidase His-42→Ala, His-42→Val, and Phe-41→Ala mutants. Histidine catalysis and control of substrate access to the heme iron. J. Biol. Chem. 270, 19 430-19 438. (doi:10.1074/jbc.270.33.19430)
59. Nicolet, Y., Piras, C., Legrand, P., Hatchikian, C. E. & Fontecilla-Camps, J. C. 1999 Desulfovibrio desulfuricans iron hydrogenase: the structure shows unusual coordination to an active site Fe binuclear center. Structure 7, 13-23. (doi:10.1016/S0969-2126(99)80005-7)
60. Nordlund, P. & Eklund, H. 1993 Structure and function of the Escherichia coli ribonucleotide reductase protein R2. J. Mol. Biol. 232, 123-164. (doi:10.1006/jmbi.1993.1374)
61. Nordlund, P., Sjöberg, B.-M. & Eklund, H. 1990 Three-dimensional structure of the free radical protein of ribonucleotide reductase. Nature 345, 593-598. (doi:10. 1038/345593a0)
62. Okamura, M. Y., Paddock, M. L., Graige, M. S. & Feher, G. 2000 Proton and electron transfer in bacterial reaction centers. Biochim. Biophys. Acta 1458, 148-163. (doi:10. 1016/S0005-2728(00)00065-7)
63. Onuchic, J. N. & Beratan, D. N. 1990 A predictive theoretical model for electron tunneling pathways in proteins. J. Chem. Phys. 92, 722-733. (doi:10.1063/1.458426)
64. Osuka, A., Yoneshima, R., Shiratori, H., Okada, S., Taniguchi, S. & Mataga, N. 1998 Electron transfer in a hydrogen-bonded assembly consisting of porphyrin-diimide. Chem. Commun., 1567-1568. (doi:10.1039/a803541e)
65. Osyczka, A., Moser, C. C., Daldal, F. & Dutton, P. L. 2004 Reversible redox energy coupling in electron transfer chains. Nature 427, 607-612. (doi:10.1038/nature02242)
66. Peters, J. W., Lanzilotta, W. N., Lemon, B. J. & Seefeldt, L. C. 1998 X-ray crystal structure of the Fe-only hydrogenase (CpI) from Clostridium pasteurianum to 1.8 angstrom resolution. Science 282, 1853-1858. (doi:10.1126/science.282.5395.1853)
67. Pond, A. E., Ledbetter, A. P., Sono, M., Goodin, D. B. & Dawson, J. H. 2001 Redox enzymes: correlation of three-dimensional structure and mechanism for heme - containing oxygenases and peroxidases. In Electron transfer in chemistry, vol. 3.1.4 (ed. V. Balzani), pp. 56-104. Weinheim, Germany: Wiley-VCH.
68. Poulos, T. L., Finzel, B. C., Gunsalus, I. C., Wagner, G. C. & Kraut, J. 1985 The 2.6-Å crystal structure of Pseudomonas putida cytochrome P-450. J. Biol. Chem. 260, 16 122-16 130.
69. Poulos, T. L., Finzel, B. C. & Howard, A. J. 1986 Crystal structure of substrate-free Pseudomonas putida cytochrome P-450. Biochemistry 25, 5314-5322. (doi:10.1021/bi00366a049)
70. Poulos, T. L., Finzel, B. C. & Howard, A. J. 1987 High-resolution crystal structure of cytochrome P450cam. J. Mol. Biol. 195, 687-700. (doi:10.1016/0022-2836(87)90190-2)
71. Pressé, S. & Silbey, R. J. 2006 Anomalous temperature-isotope dependence in proton-coupled electron transfer. J. Chem. Phys. 124, 164504/1-7. (doi:10.1063/1.2188395)
72. Reece, S. Y. & Nocera, D. G. 2005 Direct tyrosine oxidation using the MLCT excited states of rhenium polypyridyl complexes. J. Am. Chem. Soc. 127, 9448-9458. (doi:10.1021/ja0510360)
73. Reece, S. Y., Stubbe, J. & Nocera, D. G. 2005 pH dependence of charge transfer between tryptophan and tyrosine in dipeptides. Biochim. Biophys. Acta 1706, 232-238. (doi:10.1016/j.bbabio.2004.11.011)
74. Reece, S. Y., Seyedsayamdost, M. R., Stubbe, J. & Nocera, D. G. In preparation.
75. Roberts, J. A., Kirby, J. P. & Nocera, D. G. 1995 Photoinduced electron transfer within a donor-acceptor pair juxtaposed by a salt bridge. J. Am. Chem. Soc. 117, 8051-8052. (doi:10.1021/ja00135a038)
76. Roberts, J. A., Kirby, J. P., Wall, S. T. & Nocera, D. G. 1997 Electron transfer within ruthenium(II) polypyridyl-(salt bridge)-dimethylaniline acceptor-donor complexes. Inorg. Chim. Acta 263, 395-405. (doi:10.1016/S0020- 1693(97) 05668-5)
77. Rosenthal, J., Hodgkiss, J. M., Young, E. R. & Nocera, D. G. In press. Spectroscopic determination of proton position in PCET pathways of donor-acceptor supramolecular assemblies. J. Am. Chem. Soc.
78. Rova, U., Goodtzova, K., Ingemarson, R., Behravan, G., Gräslund, A. & Thelander, L. 1995 Evidence by site-directed mutagenesis supports long-range electron transfer in mouse ribonucleotide reductase. Biochemistry 34, 4267-4275. (doi:10.1021/bi00013a016)
79. Sessler, J. L., Wang, B., Springs, S. L. & Brown, C. T. 1996 Electron- and energy-transfer reactions in noncovalently linked supramolecular model systems. Comprehensive supramolecular chemistry, vol. 4, pp. 311-336. Oxford, UK: Pergamon Press.
80. Seyedsayamdost, M. R., Reece, S. Y., Nocera, D. G. & Stubbe, J. 2006a Mono-, di-, tri-, and tetra-substituted fluorotyrosines: new probes for enzymes that use tyrosyl radicals in catalysis. J. Am. Chem. Soc. 128, 1569-1579. (doi:10.1021/ja055926r)
81. nY356-R2s (n = 2 , 3, 4) in E. coli ribonucleotide reductase: evidence that Y356 is a redox active amino acid along the radical propagation pathway. J. Am. Chem. Soc. 128, 1562-1568. (doi:10.1021/ja055927j)
82. Shafirovich, V. Y., Courtney, S. H., Ya, N. & Geacintov, N. E. 1995 Proton-coupled photoinduced electron transfer, deuterium isotope effects, and fluorescence quenching in noncovalent benzo[a]pyrenetetraol-nucleoside complexes in aqueous solutions. J. Am. Chem. Soc. 117, 4920-4929. (doi:10.1021/ ja00122a024)
83. Soudackov, A. & Hammes-Schiffer, S. 1999 Multistate continuum theory for multiple charge transfer reactions in solution. J. Chem. Phys. 111, 4672-4687. (doi:10.1063/1.479229)
84. Soudackov, A. & Hammes-Schiffer, S. 2000 Derivation of rate expressions for nonadiabatic proton-coupled electron transfer reactions in solution. J. Chem. Phys. 113, 2385-2396. (doi:10.1063/1.482053)
85. Stubbe, J. & Riggs-Gelasco, P. 1998 Harnessing free radicals: formation and function of the tyrosyl radical in ribonucleotide reductase. Trends Biochem. Sci. 23, 438-443. (doi:10.1016/S0968-0004(98)01296-1)
86. Stubbe, J. & van der Donk, W. A. 1998 Protein radicals in enzyme catalysis. Chem. Rev. 98, 705-762. (doi:10.1021/cr9400875)
87. Stubbe, J., Ator, M. & Krenitsky, T. 1983 Mechanism of ribonucleoside diphosphate reductase from Escherichia coli. Evidence for 3′-C-H bond cleavage. J. Biol. Chem. 258, 1625-1631.
88. Stubbe, J., Nocera, D. G., Yee, C. S. & Chang, M. C. Y. 2003 Radical initiation in the class I ribonucleotide reductase: long-range proton-coupled electron transfer? Chem. Rev. 103, 2167-2202. (doi:10.1021/cr020421u)
89. Tanaka, M., Ishimori, K., Mukai, M., Kitagawa, T. & Morishima, I. 1997 Catalytic activities and structural properties of horseradish peroxidase distal His42 → Glu or Gln mutant. Biochemistry 36, 9889-9898. (doi:10.1021/bi970906q)
90. Tommos, C. & Babcock, G. T. 1998 Oxygen production in nature: a light-driven metalloradical enzyme process. Acc. Chem. Res. 31, 18-25. (doi:10.1021/ar9600188)
91. Tommos, C. & Babcock, G. T. 2000 Proton and hydrogen currents in photosynthetic water oxidation. Biochim. Biophys. Acta 1458, 199-219. (doi:10.1016/S0005-2728(00)00069-4)
92. Turró, C., Chang, C. K., Leroi, G. E., Cukier, R. I. & Nocera, D. G. 1992 Photoinduced electron transfer mediated by a hydrogen-bonded interface. J. Am. Chem. Soc. 114, 4013-4015. (doi:10.1021/ja00036a081)
93. Uhlin, U. & Eklund, H. 1994 Structure of ribonucleotide reductase protein R1. Nature 370, 533-539. (doi:10.1038/370533a0)
94. Vidakovic, M., Sligar, S. G., Li, H. & Poulos, T. L. 1998 Understanding the role of the essential Asp251 in cytochrome p450cam using site-directed mutagenesis, crystallography, and kinetic solvent isotope effect. Biochemistry 37, 9211-9219. (doi:10.1021/bi980189f)
95. Volbeda, A. & Fontecilla-Camps, J. C. 2005 Structure-function relationships of nickel-iron sites in hydrogenase and a comparison with the active sites of other nickel-iron enzymes. Coord. Chem. Rev. 249, 1609-1619. (doi:10. 1016/j.ccr.2004.12.009)
96. Vrettos, J. S. & Brudvig, G. W. 2002 Water oxidation chemistry of photosystem II. Phil. Trans. R. Soc. B 357, 1395-1405. (doi:10.1098/rstb.2002. 1136)
97. Ward, M. D. 1997 Photoinduced electron and energy transfer in non-covalently bonded supramolecular assemblies. Chem. Soc. Rev. 26, 365-376. (doi:10.1039/cs9972600365)
98. Whittaker, J. W. 2005 The radical chemistry of galactose oxidase. Arch. Biochem. Biophys. 433, 227-239. (doi:10.1016/j.abb.2004.08.034)
99. Winkler, J. R. & Gray, H. B. 1992 Electron transfer in ruthenium-modified proteins. Chem. Rev. 92, 369-379. (doi:10.1021/cr00011a001)
100. Yee, C. S., Chang, M. C. Y., Ge, J., Nocera, D. G. & Stubbe, J. 2003a 2,3-Difluorotyrosine at position 356 of ribonucleotide reductase R2: a probe of long-range proton-coupled electron transfer. J. Am. Chem. Soc. 125, 10 506-10 507. (doi:10.1021/ja036242r)
101. Yee, C. S., Seyedsayamdost, M. R., Chang, M. C. Y., Nocera, D. G. & Stubbe, J. 2003b Generation of the R2 subunit of ribonucleotide reductase by intein chemistry: insertion of 3-nitrotyrosine at residue 356 as a probe of the radical initiation process. Biochemistry 42, 14 541-14 552. (doi:10.1021/ bi0352365)
102. Yeh, C. Y., Chang, C. J. & Nocera, D. G. 2001a "Hangman" porphyrins for the assembly of a model heme water channel. J. Am. Chem. Soc. 123, 1513-1514. (doi:10. 1021/ja003245k)
103. Yeh, C. Y., Miller, S. E., Carpenter, S. D. & Nocera, D. G. 2001b Structurally homologous β- and meso-amidinium porphyrins. Inorg. Chem. 40, 3643-3646. (doi:10.1021/ic001387+)
104. Zhao, X. G. & Cukier, R. I. 1995 Molecular dynamics and quantum chemistry study of a proton-coupled electron transfer reaction. J. Phys. Chem. 99, 945-954. (doi:10.1021/j100003a017)