Quantum chemical studies of proton-coupled electron transfer in metalloenzymes

Chemical Reviews

Volumn 110, Issue 12, 2010, Pages 7040-7061

  Siegbahn, Per E M ^a   Blomberg, Margareta R A ^a  

^a ALBANOVA UNIVERSITY CENTER   (Sweden)

Author keywords

[No Author keywords available]

Indexed keywords

CYTOCHROME C OXIDASE; DONOR AND ACCEPTOR; ELECTROSTATIC EFFECT; EXTENDED MODEL; HYDROGEN-ATOM TRANSFER; LOCAL MINIMA PROBLEMS; LOCAL MINIMUMS; METALLOENZYMES; PHOTOSYSTEM II; PRESENT STAGE; PROTON-COUPLED ELECTRON TRANSFER; QUANTUM CHEMICAL; QUANTUM CHEMICAL CALCULATIONS; QUANTUM CHEMICAL STUDIES; QUANTUM-CHEMICAL METHODS; REDOX POTENTIALS; RELATIVE ENERGIES; RELIABLE ENERGY; REVERSE REACTIONS; RIBONUCLEOTIDE REDUCTASE; STRUCTURAL CHANGE; WATER OXIDATION;

AMINO ACIDS; ATOMS; CATALYSTS; ENZYMES; FREE RADICAL REACTIONS; MOLECULAR OXYGEN; PROTON TRANSFER; QUANTUM CHEMISTRY; REDOX REACTIONS;

ELECTRONS;

ENZYME; METALLOPROTEIN; PROTON;

ARTICLE; CHEMISTRY; ELECTRON TRANSPORT; OXIDATION REDUCTION REACTION; QUANTUM THEORY;

ELECTRON TRANSPORT; ENZYMES; METALLOPROTEINS; OXIDATION-REDUCTION; PROTONS; QUANTUM THEORY;

EID: 78650084194     PISSN: 00092665     EISSN: 15206890     Source Type: Journal    
DOI: 10.1021/cr100070p     Document Type: Article

References (158)

1. Huynh, M. H. V. and Meyer, T. J. Chem. Rev. 2007, 107, 5004
2. Stubbe, J. and van der Donk, W. A. Chem. Rev. 1998, 98, 705
3. Himo, F. and Siegbahn, P. E. M. Chem. Rev. 2003, 103, 2421
4. Himo, F. Biochim. Biophys. Acta 2005, 1707, 24
5. Siegbahn, P. E. M., Eriksson, L., Himo, F., and Pavlov, M. J. Phys. Chem. 1998, 102, 10622
6. Babcock, G. T. The oxygen-evolving complex in photosystem II as a metallo-radical enzyme. In Photosynthesis from Light to Biosphere; Mathis, P., Ed.; Kluwer: Dordrecht, The Netherlands, 1995; Vol. 2, p 209.
7. Meyer, J. M., Hrovat, D. A., Thomas, J. L., and Borden, W. T. J. Am. Chem. Soc. 2002, 124, 11142
8. Siegbahn, P. E. M. Q. Rev. Biophys. 2003, 36, 91
9. Stubbe, J., Nocera, D. G., Yee, C. S., and Chang, M. C. Y. Chem. Rev. 2003, 98, 2167
10. Seyedsayamdost, M. R., Xie, J., Chan, C. T. Y., Schultz, P. G., and Stubbe, J. J. Am. Chem. Soc. 2007, 129, 15060
11. Hammes-Schiffer, S. and Soudackov, A. V. J. Phys. Chem. B 2008, 112, 14108
12. Georgievskii, Y. and Stuchebrukhov, A. A. J. Chem. Phys. 2000, 113, 10438
13. Cukier, R. I. J. Phys. Chem. 1994, 98, 2377
14. Marcus, R. A. Annu. Rev. Phys. Chem. 1964, 15, 155
15. Liu, H. and Warshel, A. J. Phys. Chem. B 2007, 111, 7852
16. Hay, S., Johannissen, L. O., Sutcliffe, M. J., and Scrutton, N. S. Biophys. J. 2010, 98, 121
17. Kamerlin, S. C. L. and Warshel, A. J. Phys. Org. Chem. 2010, DOI 10.1002/poc.1620.
18. Page, C. C., Moser, C. C., Chen, X. X., and Dutton, P. L. Nature 1999, 402, 47
19. Gray, H. B. and Winkler, J. R. Q. Rev. Biophys. 2003, 36, 341
20. Moser, C. C., Anderson, J. L. R., and Dutton, P. L. Biochim. Biophys. Acta 2010, 1797, 1573
21. Becke, A. D. J. Chem. Phys. 1993, 98, 5648
22. Siegbahn, P. E. M. J. Biol. Inorg. Chem. 2006, 11, 695
23. Warshel, A. and Levitt, M. J. Mol. Biol. 1976, 103, 227
24. Senn, H. M. and Thiel, W. Top. Curr. Chem. 2007, 268
25. Siegbahn, P. E. M. and Himo, F. J. Biol. Inorg. Chem. 2009, 14, 643
26. Siegbahn, P. E. M., Blomberg, M. R. A., and Blomberg, M. L. J. Phys. Chem. B 2003, 107, 10946
27. Blomberg, M. R. A. and Siegbahn, P. E. M. J. Comput. Chem. 2006, 27, 1373
28. Siegbahn, P. E. M. and Blomberg, M. R. A. In Computational Modeling for Homogeneous Catalysis and Biocatalysis; Morokuma, K. and Musaev, J., Eds.; Wiley-VCH: Germany, 2008; p 57.
29. Siegbahn, P. E. M. and Blomberg, M. R. A. Dalton Trans. 2009, 5832
30. Blomberg, M. R. A. and Siegbahn, P. E. M. Biochim. Biophys. Acta 2010, 1797, 129
31. Siegbahn, P. E. M. Proc. R. Soc. 2008, 363, 1221
32. Siegbahn, P. E. M. and Blomberg, M. R. A. J. Phys. Chem A 2008, 112, 12772
33. Morgan, J. E., Verkhovsky, M. I., and Wikström, M. J. Bioenerg. Biomembr. 1994, 26, 599
34. Wikström, M., Morgan, J. E., and Verkhovsky, M. I. J. Bioenerg. Biomembr. 1998, 30, 139
35. Wikström, M. Biochim. Biophys. Acta 2000, 44827, 1
36. Michel, H. Proc. Natl. Acad. Sci. U.S.A. 1998, 95, 12819
37. Michel, H. Biochemistry 1999, 38, 15129
38. Ruitenberg, M., Kannt, A., Bamberg, E., Fendler, K., and Michel, H. Nature 2002, 417, 99
39. Gennis, R. B. Proc. Natl. Acad. Sci. U.S.A. 1998, 95, 12747
40. Mitchell, R. and Rich, P. R. Biochim. Biophys. Acta 1994, 1186, 19
41. Capitanio, N., Vygodina, T. V., Capitanio, G., Konstantinov, A. A., Nicholls, P., and Papa, S. Biochim. Biophys. Acta 1997, 1318, 255
42. Blair, D. F., Ellis, J., Walther, R., Wang, H., Gray, H. B., and Chan, S. I. J. Biol. Chem. 1986, 261, 1524
43. Carithers, R. P. and Palmer, G. J. Biol. Chem. 1981, 256, 7967
44. Artzatbanov, V. Y., Konstantinov, A. A., and Skulachev, V. P. FEBS Lett. 1978, 87, 180
45. Brzezinski, P. and Larsson, G. Biochim. Biophys. Acta 2003, 1605, 1
46. Faxen, K., Gilderson, G., Adelroth, P., and Brzezinski, P. Nature 2005, 437, 286
47. Song, Y., Michonova-Alexova, E., and Gunner, M. R. Biochemistry 2006, 45, 7959
48. Popovic, D. M. and Stuchebrukhov, A. A. J. Am. Chem. Soc. 2004, 126, 1858
49. Popovic, D. M. and Stuchebrukhov, A. A. FEBS Lett. 2004, 566, 126
50. Medvevev, D. M., Medvevev, E. S., Kotelnikov, A. I., and Stuchebrukhov, A. A. Biochim. Biophys. Acta 2005, 1710, 47
51. Popovic, D. M. and Stuchebrukhov, A. A. J. Phys. Chem. B 2005, 109, 1999
52. Fadda, E., Yu, C.-H., and Pomes, R. Biochim. Biophys. Acta 2008, 1777, 277
53. Quenneville, J., Popovic, D. M., and Stuchebrukhov, A. A. J. Phys. Chem. B 2005, 108, 18383
54. Popovic, D. M., Quenneville, J., and Stuchebrukhov, A. A. J. Phys. Chem. B 2005, 109, 3616
55. Makhov, D. V., Popovic, D. M., and Stuchebrukhov, A. A. J. Phys. Chem. B 2006, 110, 12162
56. Stuchebrukhov, A. A. and Popovic, D. M. J. Phys. Chem. B 2006, 110, 17286
57. Quenneville, J., Popovic, D. M., and Stuchebrukhov, A. A. Biochim. Biophys. Acta 2006, 1757, 1035
58. Fadda, E., Chakrabarti, N., and Pomes, R. J. Phys. Chem. B 2005, 109, 22629
59. Fadda, E., Chakrabarti, N., and Pomes, R. J. Phys. Chem. B 2006, 110, 17288
60. Olsson, M. H., Sharma, P. K., and Warshel, A. FEBS Lett. 2005, 579, 2026
61. Olsson, M. H. and Warshel, A. Proc. Natl. Acad. Sci. U.S.A. 2006, 103, 6500
62. Olsson, M. H., Siegbahn, P. E. M., Blomberg, M. R. A., and Warshel, A. Biochim. Biophys. Acta 2007, 1767, 244
63. Henry, R. M., Yu, C.-H., Rodinger, T., and Pomes, R. J. Mol. Biol. 2009, 387, 1165
64. Siegbahn, P. E. M. and Blomberg, M. R. A. Biochim. Biophys. Acta 2007, 1767, 1143
65. Verkhovsky, M. I. and Wikström, M. Biochim. Biophys. Acta 2007, 1767, 1200
66. Kaila, V. R. I., Verkhovsky, M., Hummer, G., and Wikström, M. Biochim. Biophys. Acta 2009, 1787, 1205
67. Kaila, V. R. I., Verkhovsky, M., Hummer, G., and Wikström, M. Biochim. Biophys. Acta 2008, 1777, 890
68. Kaila, V. R. I., Verkhovsky, M., Hummer, G., and Wikström, M. Proc. Natl. Acad. Sci. U.S.A. 2008, 105, 6255
69. Wikström, M., Verkhovsky, M., and Hummer, G. Biochim. Biophys. Acta 2003, 1604, 61
70. Kim, Y. C., Wikström, M., and Hummer, G. Proc. Natl. Acad. Sci. U.S.A. 2009, 106, 13707
71. Blomberg, M. R. A. and Siegbahn, P. E. M. Mol. Phys., in press.
72. Belevich, I., Bloch, D. A., Belevich, N., Wikström, M., and Verkhovsky, M. I. Proc. Natl. Acad. Sci. U.S.A. 2007, 104, 2685
73. Moore, D. B. and Martinez, T. J. J. Phys. Chem. A 2000, 104, 2367
74. Kaukonen, M. J. Phys. Chem. B 2007, 111, 12543
75. Fee, J. A., Case, D. A., and Noodleman, L. J. Am. Chem. Soc. 2008, 130, 15002
76. Brzezinski, P. Trends Biochem. Sci. 2004, 29, 380
77. Wikström, M. Biochim. Biophys. Acta 2004, 1655, 241
78. Yoshioka, Y., Kawi, H., and Yamaguchi, K. Chem. Phys. Lett. 2003, 374, 45
79. Mitani, M., Inoue, M., and Yoshioka, Y. Chem. Phys. Lett. 2007, 440, 296
80. Yoshioka, Y., Satoh, H., and Mitani, M. J. Inorg. Biochem. 2007, 101, 1410
81. Ghosh, A. and Skancke, A. J. Phys. Chem. B 1998, 102, 10087
82. Daskalakis, V., Pinakoulaki, E., Stavrakis, S., and Varotsis, C. J. Phys. Chem. B 2007, 111, 10502
83. Daskalakis, V., Farantos, S. C., and Varotsis, C. J. Am. Chem. Soc. 2008, 130, 12385
84. Colbran, S. B. and Paddo-Row, M. N. J. Biol. Inorg. Chem. 2003, 8, 855
85. Kaila, V. R. I., Johansson, M. P., Sundholm, D., Laakkonen, L., and Wikström, M. Biochim. Biophys. Acta 2009, 1787, 221
86. Kamiya, K., Boero, M., Tateno, M., Shiraishi, K., and Oshiyama, A. J. Am. Chem. Soc. 2007, 129, 9663
87. Blomberg, M. R. A., Siegbahn, P. E. M., Babcock, G. T., and Wikström, M. J. Inorg. Biochem. 2000, 80, 261
88. Blomberg, M. R. A., Siegbahn, P. E. M., Babcock, G. T., and Wikström, M. J. Am. Chem. Soc. 2000, 122, 12848
89. Blomberg, M. R. A., Siegbahn, P. E. M., and Wikström, M. Inorg. Chem. 2003, 42, 5231
90. Hansson, Ö., Karlsson, B., Aasa, R., Vänng aard, T., and Malmsröm, B. G. EMBO J. 1992, 1, 1295
91. Proshlyakov, D. A., Pressler, M. A., and Babcock, G. T. Proc. Natl. Acad. Sci. U.S.A. 1998, 95, 8020
92. Karpefors, M.,Adelroth, P., Namslauer, A., Zhen, Y., and Brzezinski, P. Biochemistry 2000, 39, 14664
93. Kannt, A., Lancaster, R. D., and Michel, H. Biophys. J. 1998, 74, 708
94. Tuukkanen, A., Verkhovsky, M. I., Laakkonen, L., and Wikström, M. Biochim. Biophys. Acta 2006, 1757, 1117
95. Bränden, M., Sigurdson, H., Namslauer, A., Gennis, R., Aelroth, P., and Brzezinski, P. Proc. Natl. Acad. Sci. U.S.A. 2001, 98, 5013
96. Qin, L., Liu, J., Mills, D. A., Proshlyakov, D. A., Hiser, C., and Ferguson-Miller, S. Biochemistry 2009, 48, 5121
97. Ferreira, K. N., Iverson, T. M., Maghlaoui, K., Barber, J., and Iwata, S. Science 2004, 303, 1831
98. Loll, B., Kern, J., Saenger, W., Zouni, A., and Biesiadka, J. Nature 2005, 438, 1040
99. Guskov, A., Kern, J., Gabdulkhakov, A., Broser, M., Zouni, A., and Saenger, W. J. Nat. Struct. Biol. 2009, 16, 334
100. Siegbahn, P. E. M. Chem. - Eur. J. 2008, 27, 8290
101. Sproviero, E. M., Gascon, J. A., McEvoy, J. P., Brudvig, G. W., and Batista, V. S. J. Am. Chem. Soc. 2008, 130, 3428-3442
102. Sproviero, E. M., Gascon, J. A., McEvoy, J. P., Brudvig, G. W., and Batista, V. S. J. Am. Chem. Soc. 2008, 130, 6728
103. Pantazis, D. A., Orio, M., Petrenko, T., Zein, S., Lubitz, W., Messinger, J., and Neese, F. Phys. Chem. Chem. Phys. 2009, 11, 6788
104. Yano, J., Kern, J., Sauer, K., Latimer, M. J., Pushkar, Y., Biesiadka, J., Loll, B., Saenger, W., Messinger, J., Zouni, A., and Yachandra, V. K. Science 2006, 314, 821
105. Yano, J., Kern, J., Pushkar, Y., Sauer, K., Glatzel, P., Bergmann, U., Messinger, J., Zouni, A., and Yachandra, V. K. Philos. Trans. R. Soc. B 2008, 363, 1139
106. Siegbahn, P. E. M. J. Am. Chem. Soc. 2009, 131, 18238
107. Ishikita, H. and Knapp, E.-W. J. Biol. Chem. 2005, 280, 12446
108. Diner, B. A. Biochim. Biophys. Acta 2001, 1503, 147
109. Rappaport, F. and Lavergne, J. Biochim. Biophys. Acta 2001, 1503, 246
110. Ahlbrink, R., Haumann, M., Cherepanov, D., Bögershausen, O., Mulkidjanian, A., and Junge, W. Biochemistry 1998, 37, 1131
111. Curtiss, L. A., Raghavachari, K., Trucks, G. W., and Pople, J. A. J. Chem. Phys. 1991, 94, 7221
112. Kerr, J. A. Handbook of Chemistry and Physics, 77th ed.; Chemical Rubber Company: Cleveland, 1996; p 9.
113. Siegbahn, P. E. M. Acc. Chem. Res. 2009, 42, 1871
114. Siegbahn, P. E. M. In Molecular Solar Fuels; Wydrzynski, T. J. and Hillier, W., Eds.; RSC Publishing: Cambridge, England, in press.
115. Siegbahn, P. E. M. and Lundberg, M. Photochem. Photobiol. Sci. 2005, 4, 1035
116. Dau, H. and Haumann, M. Biochim. Biophys. Acta 2007, 1767, 472
117. Siegbahn, P. E. M. Chem. - Eur. J. 2006, 12, 9217
118. Renger, G. Physiol. Plant. 1997, 100, 828
119. Förster, V. and Junge, W. Photochem. Photobiol. 1985, 41, 183
120. Siegbahn, P. E. M. Dalton Trans. 2009, 10063
121. Eriksson, M., Uhlin, U., Ramaswamy, S., Ekberg, M., Regnström, K., Sjöberg, B.-M., and Eklund, H. Structure 1997, 5, 1077
122. Nordlund, P., Sjöberg, B.-M., and Eklund, H. Nature 1990, 345, 593
123. Ehrenberg, A. and Reichard, P. J. Biol. Chem. 1972, 247, 3485
124. Sjöberg, B.-M. In Nucleic Acids and Molecular Biology; Eckstein, F. and Lilley, D. M. J., Eds.; Springer Verlag: 1995; Vol. 9, p 192.
125. Han, W.-G., Liu, T., Lovell, T., and Noodleman, L. J. Inorg. Biochem. 2006, 100, 771
126. Aubert, C., Vos, M. H., Mathis, P., Eker, A. P., and Brettel, K. Nature 2000, 405, 586
127. Boon, E. M. and Barton, J. K. Curr. Opin. Struct. Biol. 2002, 12, 320
128. Giese, B. Annu. Rev. Biochem. 2002, 71, 51
129. Ekberg, M., Sahlin, M., Eriksson, M., and Sjöberg, B. M. J. Biol. Chem. 1996, 271, 20655
130. Lundberg, M. and Siegbahn, P. E. M. J. Chem. Phys. 2005, 122, 224103-1-9
131. Pelmenschikov, V., Cho, K.-B., and Siegbahn, P. E. M. J. Comput. Chem. 2004, 25, 311
132. Cho, K.-B., Pelmenschikov, V., Gräslund, A., and Siegbahn, P. E. M. J. Phys. Chem. B 2004, 108, 2056
133. Huang, Y., Reimann, J., Lepp, H., Drici, N., and Adelroth, P. Proc. Natl. Acad. Sci. U.S.A. 2008, 105, 20257
134. Blomberg, L. M., Blomberg, M. R. A., and Siegbahn, P. E. M. Biochim. Biophys. Acta 2006, 1757, 31
135. Blomberg, L. M., Blomberg, M. R. A., and Siegbahn, P. E. M. Biochim. Biophys. Acta 2006, 1757, 240
136. Blomberg, L. M., Blomberg, M. R. A., and Siegbahn, P. E. M. J. Biol. Inorg. Chem. 2007, 12, 79
137. Giuffre, A., Stubauer, G., Sarti, P., Brunori, M., Zumft, W. G., Buse, G., and Soulimane, T. Proc. Natl. Acad. Sci. U.S.A. 1999, 96, 14718
138. Przbyla, A. E., Robbins, J., Menon, N., and Peck, H. D., Jr. FEMS Microbiol. Rev. 1992, 88, 109
139. Nicolet, Y., Lemon, B. J., Fontecilla-Camps, J. C., and Peters, J. W. Trends Biochem. Sci. 2000, 25, 138
140. Lyon, E. J., Shima, S., Buurman, G., Chowdhuri, S., Batschauer, A., Steinbach, K., and Thauer, R. K. Eur. J. Biochem. 2004, 271, 195
141. Garcin, E., Vernede, X., Hatchikian, E. C., Volbeda, A., Frey, M., and Fontecilla-Camps, J. C. Structure 1999, 7, 557
142. Frey, M. and Fontecilla-Camps, J. C. In Handbook of Metalloproteins; Messerschmidt, A., Huber, R., Poulos, T., and Wieghardt, K., Eds.; John Wiley & Sons: Chichester, U.K., 2001; Vol. 2, p 880.
143. Pavlov, M., Siegbahn, P. E. M., Blomberg, M. R. A., and Crabtree, R. H. J. Am. Chem. Soc. 1998, 120, 548
144. Niu, S. Q., Thomson, L. M., and Hall, M. B. J. Am. Chem. Soc. 1999, 121, 4000
145. De Gioia, L., Fantucci, P., Guigliarelli, B., and Bertrand, P. Inorg. Chem. 1999, 38, 2658
146. Siegbahn, P. E. M. Adv. Inorg. Chem. 2004, 56, 101
147. Siegbahn, P. E. M., Tye, J. W., and Hall, M. B. Chem. Rev. 2007, 107, 4414
148. Nilsson Lill, S. O. and Siegbahn, P. E. M. Biochemistry 2009, 48, 1056
149. Baik, M.-H., Newcombe, M., Friesner, R. A., and Lippard, S. J. Chem. Rev. 2003, 103, 2385
150. Basch, H., Mogi, K., Musaev, D. G., and Morokuma, K. J. Am. Chem. Soc. 1999, 121, 7249
151. Siegbahn, P. E. M. J. Biol. Inorg. Chem. 2001, 6, 27
152. Bassan, A., Borowski, T., and Siegbahn, P. E. M. Dalton. Trans. 2004, 20, 3153
153. Shaik, S., Kumar, D., de Visser, S. P., Altun, A., and Thiel, W. Chem. Rev. 2005, 105, 2279
154. Knapp, M. J., Rickert, K. W., and Klinman, J. P. J. Am. Chem. Soc. 2002, 124, 3865
155. Olsson, M. H. M., Siegbahn, P. E. M., and Warshel, A. J. Am. Chem. Soc. 2004, 126, 2820-2828
156. J. Biol. Inorg. Chem. 2004, 9, 96.
157. Hatcher, E., Soudackov, A. V., and Hammes-Schiffer, S. J. Am. Chem. Soc. 2007, 129, 187
158. J. Am. Chem. Soc. 2004, 126, 5763.