Proton-coupled electron transfer in biology: Results from synergistic studies in natural and model systems

Annual Review of Biochemistry

Volumn 78, Issue , 2009, Pages 673-699

  Reece, Steven Y ^a   Nocera, Daniel G ^a  

^a MASSACHUSETTS INSTITUTE OF TECHNOLOGY   (United States)

Author keywords

Amino acid radical; Lipoxygenase; Photosystem II; Ribonucleotide reductase; Tyrosine

Indexed keywords

ALCOHOL DEHYDROGENASE; AZURIN; IRON COMPLEX; LIPOXYGENASE; PROTON; RHENIUM COMPLEX; RIBONUCLEOTIDE REDUCTASE; RUTHENIUM COMPLEX;

BIOLOGY; ELECTRON; ELECTRON TRANSPORT; HUMAN; HYDROGEN BOND; NONHUMAN; PHOTOSYSTEM II; PRIORITY JOURNAL; PROTON TRANSPORT; REVIEW;

ANIMALS; ELECTRON TRANSPORT; HYDROGEN BONDING; MODELS, BIOLOGICAL; PLANTS; PROTONS;

GLYCINE MAX;

EID: 67649586806     PISSN: 00664154     EISSN: 00664154     Source Type: Book Series    
DOI: 10.1146/annurev.biochem.78.080207.092132     Document Type: Review

References (134)

1. Reece SY, Hodgkiss JM, Stubbe J, Nocera DG. 2006. Proton-coupled electron transfer: The mechanistic underpinning for radical transport and catalysis in biology. Philos. Trans. R. Soc. Lond. Ser. B 361:1351-64
2. Cukier RI, Nocera DG. 1998. Proton-coupled electron transfer. Annu. Rev. Phys. Chem. 49:337-69
3. Mayer JM. 2004. Proton-coupled electron transfer: a reaction chemist's view. Annu. Rev. Phys. Chem. 55:363-90
4. Huynh MHV, Meyer TJ. 2007. Proton-coupled electron transfer. Chem. Rev. 107:5004-64
5. Pourbaix M. 1966. Atlas of Electrochemical Equilibria in Aqueous Solutions. Oxford: Pergamon
6. Westheimer FH. 1949. The mechanisms of chromic acid oxidations. Chem. Rev. 45:419-51
7. Wiberg KB. 1955. The deuterium isotope effect. Chem. Rev. 55:713-43
8. Chang CJ, Brown JDK, Chang MCY, Baker EA, Nocera DG. 2001. Electron transfer in hydrogenbonded donor-acceptor supramolecules. In Electron Transfer in Chemistry, ed. V Balzani, pp. 409-61. Weinheim, Ger.:Wiley-VCH
9. Cukier RI. 1994. Mechanism for proton-coupled electron-transfer reactions. J. Phys. Chem. 98:2377-81
10. Fang J-Y, Hammes-Schiffer S. 1997. Proton-coupled electron transfer reactions in solution: molecular dynamics with quantum transitions for model systems. J. Chem. Phys. 106:8442-54
11. Marcus RA, Sutin N. 1985. Electron transfers in chemistry and biology. Biochim. Biophys. Acta 811:265-322
12. Ando K, Hynes JT. 1999. Acid-base proton transfer and ion pair formation in solution. Adv. Chem. Phys. 110:381-430
13. Hammes-Schiffer S. 2006. Hydrogen tunneling and protein motion in enzyme reactions. Acc. Chem. Res. 39:93-100
14. Moser CC, Keske JM, Warncke K, Farid RS, Dutton PL. 1992. Nature of biological electron transfer. Nature 355:796-802
15. Gray HB,Winkler JR. 1996. Electron transfer in proteins. Annu. Rev. Biochem. 65:537-61
16. Marcus RA, Sutin N. 1985. Electron transfers in chemistry and biology. Biochim. Biophys. Acta 811:265-322
17. Gray HB,Winkler JR. 2003. Electron tunneling through proteins. Q. Rev. Biophys. 36:341-72
18. Moser CC, Page CC, Dutton CC. 2006. Darwin at the molecular scale: selection and variance in electron tunnelling proteins including cytochrome c oxidase. Philos. Trans. R. Soc. Lond. Ser. B 361:1295-305
19. Hopfield JJ. 1974. Electron transfer between biological molecules by thermally activated tunneling. Proc. Natl. Acad. Sci. USA 71:3640-44
20. Levich VG. 1966. Present state of the theory of oxidation-reduction in solution (bulk and electrode reactions). Adv. Electrochem. Electrochem. Eng. 4:249-371
21. Hush NS. 1967. Intervalence-transfer absorption. II. Theoretical considerations and spectroscopic data. Prog. Inorg. Chem. 8:391-444
22. Sutin N. 1983. Theory of electron transfer reactions: insights and hindsights. Prog. Inorg. Chem. 30:441-98
23. Cukier RI. 1996. Proton-coupled electron transfer reactions: evaluation of rate constants. J. Phys. Chem. 100:15428-43
24. Soudackov AV, Hammes-Schiffer S. 2000. Derivation of rate expressions for nonadiabatic protoncoupled electron transfer reactions in solution. J. Chem. Phys. 113:2385-96
25. Presśe S, Silbey R. 2006. Anomalous temperature-isotope dependence in proton-coupled electron transfer. J. Chem. Phys. 124:164504/1-7
26. Hammes-Schiffer S. 2001. Theoretical perspectives on proton-coupled electron transfer reactions. Acc. Chem. Res. 34:273-81
27. Costentin C, Robert M, Sav́eant JM. 2007. Adiabatic and non-adiabatic concerted proton-electron transfers. Temperature effects in the oxidation of intramolecularly hydrogen-bonded phenols. J. Am. Chem. Soc. 129:9953-63
28. Knapp MJ, Rickert K, Klinman JP. 2002. Temperature-dependent isotope effects in soybean lipoxygenase-1: correlating hydrogen tunneling with protein dynamics. J. Am. Chem. Soc. 124:3865-74
29. Klinman JP. 2006. The role of tunneling in enzyme catalysis of C-H activation. Biochim. Biophys. Acta 1757:981-87
30. Klinman JP. 2006. Linking protein structure and dynamics to catalysis: the role of hydrogen tunnelling. Philos. Trans. R. Soc. Lond. Ser. B 361:1323-31
31. Kuznetsov AM, Ulstrup J. 1999. Proton and hydrogen atom tunnelling in hydrolytic and redox enzyme catalysis. Can. J. Chem. 77:1085-96
32. Hatcher E, Soudackov AV, Hammes-Schiffer S. 2007. Proton-coupled electron transfer in soybean lipoxygenase: dynamical behavior and temperature dependence of kinetic isotope effects. J. Am. Chem. Soc. 129:187-96
33. Winkler JR, Nocera DG, Yocom KM, Bordignon E, Gray HB. 1982. Electron-transfer kinetics of pentaammineruthenium(III)(histidine-33)- ferricytochrome c. Measurement of the rate of intramolecular electron transfer between redox centers separated by 15 ̊A in a protein. J. Am. Chem. Soc. 104:5798-800
34. Nocera DG, Winkler JR, Yocom KM, Bordignon E, Gray HB. 1984. Kinetics of intermolecular and intramolecular electron transfer from ruthenium(II) complexes to ferricytochrome c. J. Am. Chem. Soc. 106:5145-50
35. Crane BR, Di Bilio AJ,Winkler JR, Gray HB. 2001. Electron tunneling in single crystals of Pseudomonas aeruginosa azurins. J. Am. Chem. Soc. 123:11623-31
36. Beratan DN, Onuchic JN, Hopfield JJ. 1987. Electron tunneling through covalent and noncovalent pathways in proteins. J. Chem. Phys. 86:4488-98
37. Onuchic JN, Beratan DN. 1990. A predictive theoretical model for electron tunneling pathways in proteins. J. Chem. Phys. 92:722-33
38. Beratan DN, Onuchic JN, Betts JN, Bowler BE, Gray HB. 1990. Electron tunneling pathways in ruthenated proteins. J. Am. Chem. Soc. 112:7915-21
39. Beratan DN, Betts JN, Onuchic JN. 1991. Protein electron transfer rates set by the bridging secondary and tertiary structure. Science 252:1285-88
40. Langen R, Chang IJ, Germanas JP, Richards JH, Winkler JR, Gray HB. 1995. Electron tunneling in proteins: coupling through a â strand. Science 268:1733-35
41. Turr ́o C, Chang CK, Leroi GE, Cukier RI, Nocera DG. 1992. Photoinduced electron transfer mediated by a hydrogen-bonded interface. J. Am. Chem. Soc. 114:4013-15
42. Cukier RI. 2002. A theory that connects proton-coupled electron-transfer and hydrogen-atom transfer reactions. J. Phys. Chem. B 106:1746-57
43. Zhao XG, Cukier RI. 1995. Molecular dynamics and quantum chemistry study of a proton-coupled electron transfer reaction. J. Phys. Chem. 99:945-54
44. Sessler JL,Wang B, Springs SL, Brown CT. 1996. Electron- and energy-transfer reactions in noncovalently linked supramolecular model systems. In Comprehensive Supramolecular Chemistry, ed. YMurakami, pp. 311-36. Oxford: Pergamon
45. Ward MD. 1997. Photoinduced electron and energy transfer in non-covalently bonded supramolecular assemblies. Chem. Soc. Rev. 26:365-76
46. Shafirovich VY, Courtney SH, Ya N, Geacintov NE. 1995. Proton-coupled photoinduced electron transfer, deuterium isotope effects, and fluorescence quenching in noncovalent benzo[a]pyrenetetraolnucleoside complexes in aqueous solutions. J. Am. Chem. Soc. 117:4920-29
47. GhaddarTH,CastnerEW,Isied SS. 2000. Molecular recognition and electron transfer across a hydrogen bonding interface. J. Am. Chem. Soc. 122:1233-34
48. Roberts JA, Kirby JP, Nocera DG. 1995. Photoinduced electron transfer within a donor-acceptor pair juxtaposed by a salt bridge. J. Am. Chem. Soc. 117:8051-52
49. Kirby JP, van Dantzig NA, Chang CK, Nocera DG. 1995. Formation of porphyrin donor-acceptor complexes via an amidinium-carboxylate salt bridge. Tetrahedron Lett. 36:3477-80
50. Kirby JP, Roberts JA, Nocera DG. 1997. Significant effect of salt bridges on electron transfer. J. Am. Chem. Soc. 119:9230-36
51. Roberts JA, Kirby JP,Wall ST, Nocera DG. 1997. Electron transfer within ruthenium(II) polypyridyl-(salt bridge)-dimethylaniline acceptor-donor complexes. Inorg. Chim. Acta 263:395-405
52. Deng Y, Roberts JA, Peng SM, Chang CK, Nocera DG. 1997. The amidinium-carboxylate salt bridge as a proton-coupled interface to electron transfer pathways. Angew. Chem. Int. Ed. 36:2124-27
53. Soudackov A, Hammes-Schiffer S. 1999. Theoretical study of photoinduced proton-coupled electron transfer through asymmetric salt bridges. J. Am. Chem. Soc. 121:10598-607
54. Damrauer NH, Hodgkiss JM, Rosenthal J, Nocera DG. 2004. Observation of proton-coupled electron transfer by transient absorption spectroscopy in a hydrogen-bonded, porphyrin donor-acceptor assembly. J. Phys. Chem. B 108:6315-21
55. Rosenthal J, Hodgkiss JM, Young ER, Nocera DG. 2006. Spectroscopic determination of proton position in the proton-coupled electron transfer pathways of donor-acceptor supramolecule assemblies. J. Am. Chem. Soc. 128:10474-83
56. Hodgkiss JM, DamrauerNH,Presśe S, Rosenthal J, NoceraDG.2006.Temperature-isotope dependence reveals electron-transfer driven by proton-fluctuations in a hydrogen-bonded donor-acceptor assembly. J. Phys. Chem. B 110:18853-58
57. Cape JL, Bowman MK, Kramer DM. 2005. Reaction intermediates of quinol oxidation in a photoactivatable system that mimics electron transfer in the cytochrome bc1 complex. J. Am. Chem. Soc. 127:4208-15
58. Cha Y, Murray CJ, Klinman JP. 1989. Hydrogen tunneling in enzyme reactions. Science 243:1325-30
59. Dutton PL, Munro AW, Scrutton NS, Sutcliffe MJ. 2006. Introduction. Quantum catalysis in enzymes: beyond the transition state theory paradigm. Philos. Trans. R. Soc. Lond. Ser. B 361:1293-94
60. Sutcliffe MJ, Masgrau L, Roujeinikova A, Johannissen LO, Hothi P, et al. 2006. Hydrogen tunnelling in enzyme-catalysed H-transfer reactions: flavoprotein and quinoprotein systems. Philos. Trans. R. Soc. Lond. Ser. B 361:1375-86
61. Klinman JP. 2006. Linking protein structure and dynamics to catalysis: the role of hydrogen tunneling. Philos. Trans. R. Soc. Lond. Ser. B 361:1323-31
62. Swain CG, Stivers EC, Reuwer JF, Schaad LJ. 1958. Use of hydrogen isotope effects to identify the attacking nucleophile in the enolization of ketones catalyzed by acetic acid. J. Am. Chem. Soc. 80:5885-93
63. Saunders WH. 1985. Calculations of isotope effects in elimination reactions. New experimental criteria for tunneling in slow proton transfers. J. Am. Chem. Soc. 107:164-69
64. Glickman MH, Wiseman JS, Klinman JP. 1994. Extremely large isotope effects in the soybean lipoxygenase-linoleic acid reaction. J. Am. Chem. Soc. 116:793-94
65. Glickman MH, Cliff S, Thiemens M, Klinman JP. 1997. Comparative study of 17O and 18O isotope effects as a probe for dioxygen activation: application to the soybean lipoxygenase reaction. J. Am. Chem. Soc. 119:11357-61
66. Rickert KW, Klinman JP. 1999. Nature of hydrogen transfer in soybean lipoxygenase 1: separation of primary and secondary isotope effects. Biochemistry 38:12218-28
67. Fischer E. 1894. Einfluss der Configuration auf dieWirkung der Enzyme. Ber. Deut. Chem. Ges. 27:2985-93
68. Koshland DE. 1958. Application of a theory of enzyme specificity to protein synthesis. Proc. Natl. Acad. Sci. USA 44:98-104
69. Roth JP, Mayer JM. 1999. Hydrogen transfer reactivity of a ferric bi-imidazoline complex that models the activity of lipoxygenase enzymes. Inorg. Chem. 38:2760-61
70. Roth JP, Lovell S, Mayer JM. 2000. Intrinsic barriers for electron and hydrogen atom transfer reactions of biomimetic iron complexes. J. Am. Chem. Soc. 122:5486-98
71. Hodgkiss JM, Rosenthal J, Nocera DG. 2006. The relation between hydrogen atom transfer and protoncoupled electron transfer in model systems. In Handbook of Hydrogen Transfer. Physical and Chemical Aspects of Hydrogen Transfer, ed. JT Hynes, JP Klinman, H-H Limbach, RL Schowen, pp. 503-62. Weinheim, Ger.:Wiley-VCH
72. Stubbe J, van der DonkWA. 1998. Protein radicals in enzyme catalysis. Chem. Rev. 98:705-62
73. Whittaker JW. 2003. Free radical catalysis by galactose oxidase. Chem. Rev. 103:2347-64
74. Frey PA,Hegeman AD, Reed GH. 2006. Free radical mechanisms in enzymology. Chem. Rev. 106:3302-16
75. Stubbe J, Nocera DG, Yee CS, Chang MCY. 2003. Radical initiation in the class I ribonucleotide reductase: Long-range proton-coupled electron transfer? Chem. Rev. 103:2167-202
76. Meyer TJ, Huynh MHV, Thorp HH. 2007. The possible role of proton-coupled electron transfer (PCET) in water oxidation by photosystem II. Angew. Chem. Int. Ed. 46:5284-304
77. Sj ̈ odin M, Styring S,Wolpher H, Xu Y, Sun L, Hammarstr̈om L. 2005. Switching the redox mechanism: models for proton-coupled electron transfer from tyrosine and tryptophan. J. Am. Chem. Soc. 127:3855-63
78. Voet D, Voet JG. 1995. Biochemistry. New York:Wiley
79. Durrant JR, Klug DR, Kwa SLS, Grondelle RV, Porter G, Dekker JP. 1995. A multimer model for P680, the primary electron donor of photosystem II. Proc. Natl. Acad. Sci. USA 92:4798-802
80. Paddock ML, Feher G, Okamura MY. 2003. Proton transfer pathways and mechanism in bacterial reaction centers. FEBS Lett. 555:45-50
81. Kok B, Forbush B, McGloin M. 1970. Cooperation of charges in photosyntheticO2 evolution-I. A linear four step mechanism. Photochem. Photobiol. 11:457-75
82. Forbush B, Kok B, McGloin M. 1971. Cooperation of charges in photosynthetic oxygen evolution. II. Damping of flash yield oscillation, deactivation. Photochem. Photobiol. 14:307-21
83. McEvoy JP, Brudvig GW. 2006.Water-splitting chemistry of photosystem II. Chem. Rev. 106:4455-83
84. Haumann M, Liebisch P, Muller C, Barra M, Grabolle M, Dau H. 2005. Photosynthetic O2 formation tracked by time-resolved X-ray experiments. Science 310:1019-21
85. Barry BA, Babcock GT. 1987. Tyrosine radicals are involved in the photosynthetic oxygen-evolving system. Proc. Natl. Acad. Sci. USA 84:7099-103
86. Debus RJ, Barry BA, Babcock GT, McIntosh L. 1988. Site-directed mutagenesis identifies a tyrosine radical involved in the photosynthetic oxygen-evolving system. Proc. Natl. Acad. Sci. USA 85:427-30
87. Debus RJ, Barry BA, Sithole I, Babcock GT, McIntosh L. 1988. Directed mutagenesis indicates that the donor to P 680+ in photosystem II is tyrosine-161 of the D1 polypeptide. Biochemistry 27:9071-74
88. Diner BA, Nixon PJ, Farchaus JW. 1991. Site-directed mutagenesis of photosynthetic reaction centers. Curr. Opin. Struct. Biol. 1:546-54
89. Chu H-A, Nguyen AP, Debus RJ. 1995. Amino acid residues that influence the binding of manganese or calcium to photosystem II. 1. The lumenal interhelical domains of the D1 polypeptide. Biochemistry 34:5839-58
90. Hoganson CW, Babcock GT. 1997. A metalloradical mechanism for the generation of oxygen from water in photosynthesis. Science 277:1953-56
91. Hays AMA, Vassiliev IR, Golbeck JH, Debus RJ. 1998. Role of D1-His190 in proton-coupled electron transfer reactions in photosystem II: a chemical complementation study. Biochemistry 37:11352-65
92. Diner BA, Force DA, Randall DW, Britt RD. 1998. Hydrogen bonding, solvent exchange, and coupled proton and electron transfer in the oxidation and reduction of redox-active tyrosine YZ in Mn-depleted core complexes of photosystem II. Biochemistry 37:17931-43
93. Loll B, Kern J, Saenger W, Zouni A, Biesiadka J. 2005. Towards complete cofactor arrangement in the 3.0 ?A resolution structure of photosystem II. Nature 438:1040-44
94. Jordan A, Reichard P. 1998. Ribonucleotide reductases. Annu. Rev. Biochem. 67:71-98
95. Stubbe J. 2003. Radicals with a controlled lifestyle. Chem. Comm. Oct. (20):2511-13
96. Thelander L. 1973. Physicochemical characterization of ribonucleoside diphosphate reductase from Escherichia coli. J. Biol. Chem. 248:4591-601
97. Kashlan OB, Scott CP, Lear JD, Cooperman BS. 2002. A comprehensive model for the allosteric regulation of mammalian ribonucleotide reductase. Functional consequences of ATP- and dATP-induced oligomerization of the large subunit. Biochemistry 41:462-74
98. Kashlan OB, Cooperman BS. 2003. Comprehensive model for allosteric regulation of mammalian ribonucleotide reductase: refinements and consequences. Biochemistry 42:1696-706
99. Stubbe J, Riggs-Gelasco P. 1998. Harnessing free radicals: formation and function of the tyrosyl radical in ribonucleotide reductase. Trends Biochem. Sci. 23:438-43
100. Uhlin U, Eklund H. 1994. Structure of ribonucleotide reductase protein R1. Nature 370:533-39
101. Nordlund P, Sj ̈ oberg B-M, Eklund H. 1990. Three-dimensional structure of the free radical protein of ribonucleotide reductase. Nature 345:593-98
102. Ḧogbom M, Galander M, Andersson M, Kolberg M, Hofbauer W, et al. 2003. Displacement of the tyrosyl radical cofactor in ribonucleotide reductase obtained by single-crystal high-field EPR and 1.4- ?A X-ray data. Proc. Natl. Acad. Sci. USA 100:3209-14
103. Bennati M, Robblee JH, Mugnaini V, Stubbe J, Freed JH, Borbat P. 2005. EPR distance measurements support a model for long-range radical initiation in E. coli ribonucleotide reductase. J. Am. Chem. Soc. 127:15014-15
104. Ekberg M, Potsch S, Sandin E, Thunnissen M, Nordlund P, et al. 1998. Preserved catalytic activity in an engineered ribonucleotide reductase R2 protein with a nonphysiological radical transfer pathway. The importance of hydrogen bond connections between the participating residues. J. Biol. Chem. 273:21003-8
105. Ekberg M, Sahlin M, Eriksson M, Sj ̈ oberg B-M. 1996. Two conserved tyrosine residues in protein R1 participate in an intermolecular electron transfer in ribonucleotide reductase. J. Biol. Chem. 271:20655-59
106. Rova U, Goodtzova K, Ingemarson R, Behravan G, Graeslund A, Thelander L. 1995. Evidence by site-directed mutagenesis supports long-range electron transfer in mouse ribonucleotide reductase. Biochemistry 34:4267-75
107. Rova U, Adrait A, Potsch S, Graslund A, Thelander L. 1999. Evidence by mutagenesis that Tyr370 of the mouse ribonucleotide reductase R2 protein is the connecting link in the intersubunit radical transfer pathway. J. Biol. Chem. 274:23746-51
108. Ge J, Yu G, Ator MA, Stubbe J. 2003. Pre-steady-state and steady-state kinetic analysis of E. coli class I ribonucleotide reductase. Biochemistry 42:10071-83
109. Yee CS, Seyedsayamdost MR, Chang MCY, Nocera DG, Stubbe J. 2003. 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 42:14541-52
110. Yee CS, Chang MCY, Ge J, Nocera DG, Stubbe J. 2003. 2,3-Difluorotyrosine at position 356 of ribonucleotide reductase R2: a probe of long-range proton-coupled electron transfer. J. Am. Chem. Soc. 125:10506-7
111. Chang MCY, Yee CS, Nocera DG, Stubbe J. 2004. 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. 126:16702-3
112. Seyedsayamdost MR, Yee CS, Reece SY, Nocera DG, Stubbe J. 2006. pH rate profiles of FnY356-R2s (n = 2, 3, 4) in Escherichia coli ribonucleotide reductase: evidence that Y356 is a redox-active amino acid along the radical propagation pathway. J. Am. Chem. Soc. 128:1562-68
113. Seyedsayamdost MR, Reece SY, Nocera DG, Stubbe J. 2006. Mono-, di-, tri-, and tetra-substituted fluorotyrosines: new probes for enzymes that use tyrosyl radicals in catalysis. J. Am. Chem. Soc. 128:1569-79
114. Xie J, Schultz PG. 2006. A chemical toolkit for proteins-an expanded genetic code. Nat. Rev. Mol. CellBiol. 7:775-82
115. Seyedsayamdost MR, Xie J, Chan CTY, Schultz PG, Stubbe J. 2007. Site-specific insertion of 3-aminotyrosine into subunit á2 of E. coli ribonucleotide reductase: direct evidence for involvement of Y730 and Y731 in radical propagation. J. Am. Chem. Soc. 129:15060-71
116. Reece SY, Nocera DG. 2009. Proton-coupled electron transfer: the engine that drives radical transport and catalysis in biology. In QuantumTunneling in Enzyme-Catalyzed Reactions, ed.NSScrutton,RAlleman, pp. 351-83. Cambridge, UK: R. Soc. Chem.
117. Climent I, Sj ̈ oberg BM, Huang CY. 1991. Carboxyl-terminal peptides as probes for Escherichia coli ribonucleotide reductase subunit interaction: kinetic analysis of inhibition studies. Biochemistry 30:5164-71
118. Climent I, Sj ̈ obergBM,Huang CY. 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 31:4801-7
119. Chang MCY,Yee CS, Stubbe J, Nocera DG. 2004.Turning on ribonucleotide reductase by light-initiated amino acid radical generation. Proc. Natl. Acad. Sci. USA 101:6882-87
120. Reece SY, Seyedsayamdost MR, Stubbe J, Nocera DG. 2007. Photoactive peptides for light-initiated tyrosyl radical generation and transport into ribonucleotide reductase. J. Am. Chem. Soc. 129:8500-9
121. Reece SY, Seyedsayamdost MR, Stubbe J, Nocera DG. 2007. Direct observation of a transient tyrosine radical competent for initiating turnover in a photochemical ribonucleotide reductase. J. Am. Chem. Soc. 129:13828-30
122. Sj ̈ odin M, Styring S, ̊Akermark B, Sun L, Hammarstr̈om L. 2000. Proton-coupled electron transfer from tyrosine in a tyrosine-ruthenium- tris-bipyridine complex: comparison with tyrosineZ oxidation in photosystem II. J. Am. Chem. Soc. 122:3932-36
123. Reece SY, Nocera DG. 2005. Direct tyrosine oxidation using the MLCT excited states of rhenium polypyridyl complexes. J. Am. Chem. Soc. 127:9448-58
124. Fecenko CJ, Meyer TJ, Thorp HH. 2006. Electrocatalytic oxidation of tyrosine by parallel rate-limiting proton transfer and multisite electron-proton transfer. J. Am. Chem. Soc. 128:11020-21
125. Costentin C, Robert M, Sav́eant JM. 2007. Concerted proton-electron transfer reactions in water. Are the driving force and rate constant depending on pH when water acts as proton donor or acceptor? J. Am. Chem. Soc. 129:5870-79
126. Irebo T, Reece SY, Sj ̈ odin M, Nocera DG, Hammarstr̈om L. 2007. Proton-coupled electron transfer of tyrosine oxidation: buffer dependence and parallel mechanisms. J. Am. Chem. Soc. 129:15462-64
127. Tommos C, Skalicky JJ, Pilloud DL,Wand AJ, Dutton PL. 1999. De novo proteins as models of radical enzymes. Biochemistry 38:9495-507
128. Ishikita H, Soudackov AV, Hammes-Schiffer S. 2007. Buffer-assisted proton-coupled electron transfer in a model rhenium-tyrosine complex. J. Am. Chem. Soc. 129:11146-52
129. Costentin C, Robert M, Sav́eant JM. 2006. Electrochemical and homogeneous proton-coupled electron transfers: concerted pathways in the one-electron oxidation of a phenol coupled with an intramolecular amine-driven proton transfer. J. Am. Chem. Soc. 128:4552-53
130. Rhile IJ, Mayer JM. 2004. One-electron oxidation of a hydrogen-bonded phenol occurs by concerted proton-coupled electron transfer. J. Am. Chem. Soc. 126:12718-19
131. Rhile IJ, Markle TF, Nagao H, DiPasquale AG, Lam OP, et al. 2006. Concerted proton-electron transfer in the oxidation of hydrogen-bonded phenols. J. Am. Chem. Soc. 128:6075-88
132. Suydam IT, Snow CD, Pande VS, Boxer SG. 2006. Electric fields at the active site of an enzyme: direct comparison of experiment with theory. Science 313:200-4
133. Sj ̈ odin M, Irebo T, Utas JE, Lind J, Meŕenyi G, et al. 2006. Kinetic effects of hydrogen bonds on proton-coupled electron transfer from phenols. J. Am. Chem. Soc. 128:13076-83
134. Costentin C, Evans DH, Robert M, Sav́eant JM, Singh PS. 2005. Electrochemical approach to concerted proton and electron transfers. Reduction of the water-superoxide ion complex. J. Am. Chem. Soc. 127:12490-91