Modification of quinone electrochemistry by the proteins in the biological electron transfer chains: Examples from photosynthetic reaction centers

Journal of Bioenergetics and Biomembranes

Volumn 40, Issue 5, 2008, Pages 509-519

  Gunner, M R ^a   Madeo, Jennifer ^a   Zhu, Zhenyu ^a  

^a CITY COLLEGE OF NEW YORK   (United States)

Author keywords

Continuum electrostatics; Em; Electrochemistry; Ligand; Photosynthesis; Quinone; Ubiquinone

Indexed keywords

PROTON; QUINONE DERIVATIVE; UBIQUINONE;

AQUEOUS SOLUTION; BINDING AFFINITY; BINDING SITE; CONFORMATIONAL TRANSITION; ELECTRICITY; ELECTROCHEMISTRY; ELECTRON TRANSPORT; KINETICS; OXIDATION REDUCTION REACTION; PHOTOSYNTHESIS; PROTEIN BINDING; PROTON TRANSPORT; REVIEW; THERMODYNAMICS;

ELECTROCHEMISTRY; ELECTRON TRANSPORT CHAIN COMPLEX PROTEINS; KINETICS; MODELS, BIOLOGICAL; OXIDATION-REDUCTION; PHOTOSYNTHETIC REACTION CENTER COMPLEX PROTEINS; QUINONES; THERMODYNAMICS;

BACTERIA (MICROORGANISMS);

EID: 57049149598     PISSN: 0145479X     EISSN: 15736881     Source Type: Journal    
DOI: 10.1007/s10863-008-9179-1     Document Type: Review

References (93)

1. EG Alexov MR Gunner 1997 Incorporating protein conformational flexibility into the calculation of pH-dependent protein properties Biophys J 72 2075 2093
2. B in bacterial photosynthetic reaction centers Biochemistry 38 8253 8270
3. B in photosynthetic reaction centers Biochemistry 39 5940 5952
4. NA Baker 2005 Improving implicit solvent simulations: a Poisson-centric view Cur Opin Struct Biol 15 137 143
5. as of ionizable groups in proteins: atomic detail from a continuum electrostatic model Biochemistry 29 10219 10225
6. P Beroza D Case 1996 Including side chain flexibility in continuum electrostatic calculations of protein titration J Phys Chem 100 20156 20163
7. P Beroza DR Fredkin MY Okamura G Feher 1991 Protonation of interacting residues in a protein by a Monte Carlo method: application to Lysozyme and the photosynthetic reaction center of Rhodobacter sphaeroides Proc Natl Acad Sci USA 88 5804 5808
8. -, in the reaction center Biophys J 68 2233 2250
9. Bockris JOM, Reddy AKN (1973) Modern electrochemistry, vol. 1. Plenum, New York
10. B in bacterial photosynthetic reaction centers Biochemistry 43 3318 3326
11. B binding site at the proximal position in wild-type reaction centers and in the Pro-L209 → Tyr mutant from Rhodobacter sphaeroides Biochemistry 41 12921 12927
12. 1 complex: mechanistic and physiological implications J Biol Chem 280 34654 34660
13. JL Cape MK Bowman DM Kramer 2006 Computation of the redox and protonation properties of quinones: towards the prediction of redox cycling natural products Phytochemistry 67 1781 1788
14. JL Cape MK Bowman DM Kramer 2006 Understanding the cytochrome bc complexes by what they don't do. The Q-cycle at 30 Trends Plant Sci 11 46 55
15. 1 complex: importance for the Q-cycle and superoxide production Proc Natl Acad Sci USA 104 7887 7892
16. AK Churg A Warshel 1986 Control of the redox potential of cytochrome c and microscopic dielectric effects in proteins Biochemistry 25 1675 1681
17. AK Churg RM Weiss A Warshel T Takano 1983 On the action of cytochrome c: correlating geometry changes upon oxidation with activation energies of electron transfer J Phys Chem 87 1683 1694
18. BA Diner CC Schenck C DeVitry 1984 Effect of inhibitors, redox state and isoprenoid chain length on the affinity of ubiquinone for the secondary acceptor binding site in the reaction centers of photosynthetic bacteria Biochim Biophys Acta 766 9 20
19. PL Dutton JS Leigh CA Wraight 1973 Direct measurement of the midpoint potential of the primary electron acceptor in Rhodopseudomonas spheroides in situ and in the isolated state: some relationships with pH and o-phenanthroline FEBS Lett 36 169 173
20. G Feher JP Allen MY Okamura DC Rees 1989 Primary processes in bacterial photosynthesis: structure and function of bacterial photosynthetic reaction centres Nature 339 111 116
21. 1 complex J Biol Chem 281 38459 38465
22. as in proteins Biophys J 83 1731 1748
23. B) reduction in reaction centers of R. sphaeroides J Am Chem Soc 118 9005 9016
24. - in bacterial reaction centers of Rhodobacter sphaeroides determined by a driving force assay Proc Natl Acad Sci USA 95 11679 11684
25. MS Graige ML Paddock G Feher MY Okamura 1999 Observation of the protonated semiquinone intermediate in isolated reaction centers from Rhodobacter sphaeroides: implications for the mechanism of electron and proton transfer in proteins Biochemistry 38 11465 11473
26. MR Gunner 1991 The reaction center protein from purple bacteria: structure and function Curr Top Bioenerg 16 319 367
27. MR Gunner E Alexov 2000 A pragmatic approach to structure based calculation of coupled proton and electron transfer in proteins Biochim Biophys Acta 1458 63 87
28. A J Am Chem Soc 111 3400 3412
29. MR Gunner B Honig 1991 Electrostatic control of midpoint potentials in the cytochrome subunit of the Rhodopseudomonas viridis reaction center Proc Natl Acad Sci USA 88 9151 9155
30. MR Gunner A Nicholls B Honig 1996 Electrostatic potentials in Rhodopseudomonas viridis reaction center: implications for the driving force and directionality of electron transfer J Phys Chem 100 4277 4291
31. MR Gunner E Alexov E Torres S Lipovaca 1997 The importance of the protein in controlling the electrochemistry of heme metalloproteins: methods of calculation and analysis J Biol Inorg Chem 2 126 134
32. MR Gunner J Mao Y Song J Kim 2006 Factors influencing energetics of electron and proton transfers in proteins. What can be learned from calculations Biochim Biophys Acta 1757 942 968
33. AH Haas CR Lancaster 2004 Calculated coupling of transmembrane electron and proton transfer in dihemic quinol:fumarate reductase Biophys J 87 4298 4315
34. J-y Hasegawa M Ishida H Nakatsuji Z Lu H Liu W Yang 2003 Energetics of the electron transfer from bacteriopheophytin to ubiquinone in the photosynthetic reaction center of Rhodopseudomonas viridis: theoretical study J Phys Chem B 107 838 847
35. P Heathcote 2002 Reaction centers: the structure and evolution of biological solar power Trends Biochem Sci 27 79 86
36. B Honig A Nicholls 1995 Classical electrostatics in biology and chemistry Science 268 1144 1149
37. B redox state in reaction centers from Rhodobacter sphaeroides J Am Chem Soc 126 8059 8064
38. H Ishikita G Morra EW Knapp 2003 Redox potential of quinones in photosynthetic reaction centers from Rhodobacter sphaeroides: dependence on protonation of Glu-L212 and Asp-L213 Biochemistry 42 3882 3892
39. RJ Kassner 1972 Effects of nonpolar environments on the redox potentials of heme complexes Proc Natl Acad Sci USA 69 2263 2267
40. J Kim J Mao MR Gunner 2005 Are acidic and basic groups in buried proteins predicted to be ionized? J Mol Biol 348 1283 1298
41. - Biochim Biophys Acta 766 126 140
42. D Kleinfeld MY Okamura G Feher 1984 Electron-transfer kinetics in photosynthetic reaction centers cooled to cryogenic temperatures in the charge separated state: evidence for light-induced structural changes Biochemistry 23 5780 5786
43. 1 identified by Poisson-Boltzmann electrostatics calculations Biochim Biophys Acta 1767 204 221
44. 1 (and related) complexes Methods Enzymol 382 21 45
45. CRD Lancaster 1998 Ubiquinone reduction and protonation in photosynthetic reaction centres from Rhodopseudomonas viridis: X-ray structures and their functional implications Biochim Biophys Acta 1365 143 150
46. CRD Lancaster H Michel B Honig MR Gunner 1996 Calculated coupling of electron and proton transfer in the photosynthetic reaction center of Rhodopseudomonas viridis Biophys J 70 2469 2492
47. - in Rhodobacter sphaeroides reaction centers Biochemistry 39 7445 7454
48. A site in bacterial reaction centers Biochemistry 44 10994 11004
49. B Mallik SN Datta 2004 Semiemprical quantum chemical treatment of the standard reduction potentials of quinone and plastoquinone in water Int J Quant Chem 52 629 649
50. - reaction in isolated reaction centers from the photosynthetic bacterium Rhodopseudomonas sphaeroides Biochim Biophys Acta 764 46 54
51. J Mao K Hauser MR Gunner 2003 How cytochromes with different folds control heme redox potentials Biochemistry 42 9829 9840
52. M Marchi JN Gehlen D Chandler M Newton 1993 Diabatic surfaces and the pathway for primary electron transfer in a photosynthetic reaction center J Am Chem Soc 115 4178 4190
53. 1 complex in the respiratory chain: proton motive ubiquinone cycle FEBS Lett 56 1 6
54. P Mitchell 1975 The proton motive Q cycle: a general formulation FEBS Lett 59 137 139
55. CC Moser CC Page RJ Cogdell J Barber CA Wraight PL Dutton 2003 Length, time, and energy scales of photosystems Adv Protein Chem 63 71 109
56. CC Moser TA Farid SE Chobot PL Dutton 2006 Electron tunneling chains of mitochondria Biochim Biophys Acta 1757 1096 1109
57. MY Okamura ML Paddock MS Graige G Feher 2000 Proton and electron transfer in bacterial reaction centers Biochim Biophys Acta 1458 148 163
58. A Osyczka CC Moser PL Dutton 2005 Fixing the Q cycle Trends Biochem Sci 30 176 182
59. WW Parson Z-T Chu A Warshel 1990 Electrostatic control of charge separation in bacterial photosynthesis Biochim Biophys Acta 1017 251 272
60. PR Pokkuluri PD Laible AE Crawford JF Mayfield MA Yousef SL Ginell DK Hanson M Schiffer 2004 Temperature and cryoprotectant influence secondary quinone binding position in bacterial reaction centers FEBS Let 43 9909 9917
61. RC Prince PL Dutton JM Bruce 1983 Electrochemistry of ubiquinones FEBS Lett 160 273 276
62. RC Prince P Lloyd-Williams JM Bruce PL Dutton 1986 Voltammetric measurements of quinines Methods Enzymol 125 109 119
63. B Rabenstein GM Ullmann E-W Knapp 1998 Energetics of electron-transfer and protonation reactions of the quinones in the photosynthetic reaction center of Rhodopseudomonas viridis Biochemistry 37 2488 2495
64. B Rabenstein GM Ullmann EW Knapp 2000 Electron transfer between the quinones in the photosynthetic reaction center and its coupling to conformational changes Biochemistry 39 10487 10496
65. AA Rashin B Honig 1985 Reevaluation of the born model of ion hydration J Phys Chem 89 5588 5593
66. CJ Reedy BR Gibney 2004 Heme protein assemblies Chem Rev 104 617 649
67. A Remy K Gerwert 2003 Coupling of light-induced electron transfer to proton uptake in photosynthesis Nat Struct Biol 10 637 644
68. PR Rich 2004 The quinone chemistry of bc complexes Biochem Biophys Acta 1658 165 171
69. PR Rich DS Bendall 1979 A mechanism for the reduction of cytochromes by quinols in solution and its relevance to biological electron transfer reactions FEBS Lett 105 189 194
70. AW Rutherford MCW Evans 1980 Direct measurement of the redox potential of the primary and secondary quinone electron acceptors in Rhodopseudomonas sphaeroides (wild-type) by EPR spectrometry FEBS Lett 110 257 261
71. M Saraste 1999 Oxidative phosphorylation at the fin de siecle Science 283 1488 1493
72. CN Schutz A Warshel 2001 What are the "dielectric constants" of proteins and how to validate electrostatic models? Proteins Struct Funct Genet 44 400 417
73. a's of ionizable residues in proteins: semi-microscopic and microscopic approaches J Phys Chem 101 4458 4472
74. Y Sham I Muegge A Warshel 1999 Simulating proton translocations in proteins: probing proton transfer pathways in the Rhodobacter sphaeroides reaction center Proteins Struct Funct Genet 36 484 500
75. A Shurki M Strajbl CN Schutz A Warshel 2004 Electrostatic basis for bioenergetics Methods Enzymol 380 52 84
76. T Simonson 2001 Macromolecular electrostatics: continuum models and their growing pains Curr Opin Struct Biol 11 243 252
77. MHB Stowell TM McPhillips DC Rees SM Soltis E Abresch G Feher 1997 Light-induced structural changes in photosynthetic reaction center: implications for mechanism of electron-proton transfer Science 276 812 816
78. Swallow AJ (1982) Physical chemistry of semiquinones. In: Trumpower BL (ed) Function of quinones in energy conserving systems. Academic, New York, pp 59-72
79. GM Ullmann EW Knapp 1999 Electrostatic models for computing protonation and redox equilibria in proteins Eur Biophys J 28 533 551
80. P Voigt EW Knapp 2003 Tuning heme redox potentials in the cytochrome c subunit of photosynthetic reaction centers J Biol Chem 278 51993 52001
81. A Warshel ST Russell 1984 Calculations of electrostatic interactions in biological systems and in solutions Q Rev Biophys 17 283 422
82. Woodbury NW, Allen JP (1995) The pathway, kinetics and thermodynamics of electron transfer in wild type and mutant reaction centers of purple nonsulfur bacteria. In: Blankenship RE, Madigan MT, Bauer CE (eds) Anoxygenic photosynthetic bacteria. Kluwer, Dordrecht
83. NW Woodbury WW Parson MR Gunner RC Prince PL Dutton 1986 Radical-pair energetics and decay mechanisms in reaction center containing anthraquinones or benzoquinones in place of ubiquinone Biochim Biophys Acta 851 6 22
84. + binding coupled to secondary electron transfer in the quinone acceptor complex Biochim Biophys Acta 548 309 327
85. CA Wraight 2004 Proton and electron transfer in the acceptor quinone complex of photosynthetic reaction centers from Rhodobacter sphaeroides Front Biosci 9 309 337
86. - charge recombination in photosynthetic reaction centers J Phys Chem B 104 8035 8043
87. Q Xu MR Gunner 2001 Trapping conformational intermediate states in the reaction center protein from photosynthetic bacteria Biochemistry 40 3232 3241
88. B electron transfer in bacterial photosynthetic reaction centers: effect of substrate position and tail length on the conformational gating step Biochemistry 41 10021 10025
89. a's in proteins Proteins Struct Funct Genet 15 252 265
90. TJ You D Bashford 1995 Conformation and hydrogen ion titration of proteins: a continuum electrostatic model with conformational flexibility Biophys J 69 1721 1733
91. o semiquinone radical Biochim Biophys Acta 1767 883 887
92. Z Zhu MR Gunner 2005 Energetics of quinone-dependent electron and proton transfers in Rhodobacter sphaeroides photosynthetic reaction centers Biochemistry 44 82 96
93. ms spanning 800 mV. Proteins (in press)