Chance and design-Proton transfer in water, channels and bioenergetic proteins

Biochimica et Biophysica Acta - Bioenergetics

Volumn 1757, Issue 8, 2006, Pages 886-912

  Wraight, Colin A ^a  

^a UNIVERSITY OF ILLINOIS AT URBANA CHAMPAIGN   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ADENOSINE TRIPHOSPHATASE; AMINO ACID; AQUAPORIN; BACTERIORHODOPSIN; CYTOCHROME C OXIDASE; GRAMICIDIN; ION CHANNEL; PROTEIN; WATER;

DEVICE; ELECTRON TRANSPORT; HYDROGEN BOND; NONHUMAN; PRIORITY JOURNAL; PROTON TRANSPORT; REVIEW; WATER TRANSPORT;

ANTI-BACTERIAL AGENTS; AQUAPORINS; BIOLOGICAL TRANSPORT; ION CHANNELS; KINETICS; MODELS, BIOLOGICAL; MODELS, MOLECULAR; PROTEIN CONFORMATION; PROTONS; WATER;

EID: 33749052047     PISSN: 00052728     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.bbabio.2006.06.017     Document Type: Review

References (278)

1. Moser C.C., Page C.C., Cogdell R.J., Barber J., Wraight C.A., and Dutton P.L. Length, time and energy scales of photosystems. Adv. Protein Chem. 63 (2003) 71-109
2. Page C.C., Moser C.C., Chen X., and Dutton P.L. Natural engineering principles of electron tunnelling in biological oxidation-reduction. Nature 402 (1999) 47-52
3. Winkler J.R., and Gray H.B. Electron tunneling in proteins: role of the intervening medium. J. Biol. Inorg. Chem. 2 (1997) 399-404
4. Gray H.B., and Winkler J.R. Electron transfer in proteins. Annu. Rev. Biochem. 65 (1996) 537-561
5. Onuchic J.N., Beratan D.N., Winkler J.R., and Gray H.B. Pathway analysis of protein electron-transfer reactions. Ann. Rev. Biophys. Biomol. Struct. 21 (1992) 349-377
6. Moser C.C., Page C.C., Chen X., and Dutton P.L. Effects of intervening medium on long-range biological electron transfer. J. Biol. Inorg. Chem. (1997) 1-11
7. Krishtalik L.I. The mechanism of the proton transfer: an outline. Biochim. Biophys. Acta 1458 (2000) 6-27
8. Kohen A., Cannio R., Bartolucci S., and Klinman J.P. Enzyme dynamics and hydrogen tunnelling in a thermophilic alcohol dehydrogenase. Nature 399 (1999) 496-499
9. Garcia-Viloca M., Gao J., Karplus M., and Truhlar D.G. How enzymes work: analysis by modern rate theory and computer simulations. Science 303 (2004) 186-195
10. Masgrau L., Roujeinikova A., Johannissen L.O., Hothi P., Basran J., Ranaghan K.E., Mulholland A.J., Sutcliffe M.J., Scrutton N.S., and Leys D. Atomic description of an enzyme dominated by proton tunneling. Science 312 (2006) 237-241
11. Doll K.M., Bender B.R., and Finke R.G. The first experimental test of the hypothesis that enzymes have evolved to enhance hydrogen tunneling. J. Am. Chem. Soc. 125 (2003) 10877-10884
12. Siebr W., and Smedarchina Z. Temperature dependence of kinetic isotope effects for enzymatic carbon-hydrogen bond cleavage. J. Phys. Chem., B 108 (2004) 4185-4195
13. Olsson M.H.M., Siegbahn P.E.M., and Warshel A. Simulations of the large kinetic isotope effect and the temperature dependence of the hydrogen atom transfer in lipoxygenase. J. Am. Chem. Soc. 126 (2004) 2820-2828
14. Kohen A., and Klinman J.P. Enzyme catalysis: beyond classical paradigms. Acc. Chem. Res. 31 (1998) 397-404
15. Hwang J.-K., and Warshel A. How important are quantum mechanical nuclear motions in enzyme catalysis?. J. Am. Chem. Soc. 118 (1996) 11745-11751
16. Benkovic S.J., and Hammes-Schiffer S. A perspective on enzyme catalysis. Science 301 (2003) 1196-1201
17. Eigen M. Proton transfer, acid-base catalysis, and enzymatic hydrolysis. Angew. Chem., Int. Ed. 3 (1964) 1-19
18. Tuckerman M.E., Marx D., Klein M.L., and Parrinello M. On the quantum nature of the shared proton in hydrogen bonds. Science 275 (1997) 817-820
19. Marx D., Tuckerman M.E., Hutter J., and Parrinello M. The nature of the hydrated excess proton in water. Nature 397 (1999) 601-603
20. Kiefer P.M., and Hynes J.T. Nonlinear free energy relations for adiabatic proton transfer reactions in a polar environment: II. Inclusion of the hydrogen bond vibration. J. Phys. Chem., A 106 (2002) 1850-1861
21. Vuillemier R., and Borgis D. Molecular dynamics of an excess proton in water using a non-additive valence bond force field. J. Mol. Struct. 437 (1998) 555-565
22. Kornyshev A.A., Kuznetsov A.M., Spohr E., and Ulstrup J. Kinetics of proton transport in water. J. Phys. Chem., B 107 (2003) 3351-3366
23. Robinson R.A., and Stokes R.H. Electrolyte Solutions. 2nd ed. (1970), Butterworths, London
24. Eisenberg D., and Kauzmann W. The Structure and Properties of Water (1969), Oxford Univ. Press
25. 18 as tracers. J. Am. Chem. Soc. 75 (1953) 466-470
26. Grotthuss C.J.T.V. Sur la decomposition de l'eau et des corps qu'elle tient en dissolution a l'aide de l'electricite galvanique (Theory of decomposition of liquids by electric currents). Ann. Chim. 58 (1806) 54-74
27. Dalton J. A New System of Chemical Philosophy, Part I (1808), R. Bickerstaff, London
28. Danneel H. Notiz über Ionengeschwindigkeiten, Zeitschrift für Elektrochemie und angewandte physikalische. Chemie 11 (1905) 249-252
29. Bernal J.D., and Fowler R.H. A theory of water and ionic solution, with particular reference to hydrogen and hydroxyl ions. J. Chem. Phys. 1 (1933) 515-548
30. + ion. J. Chem. Phys. 24 (1956) 834-850
31. Agmon N. Hydrogen bonds, water rotation and proton mobility. J. Chem. Phys. 93 (1996) 1714-1736
32. Agmon N. The Grötthuss mechanism. Chem. Phys. Lett. 244 (1995) 456-462
33. Lapid H., Agmon N., Petersen M.K., and Voth G.A. A bond-order analysis of the mechanism for hydrated proton mobility in liquid water. J. Chem. Phys. 122 (2005)
34. Day T.J.F., Schmitt U.W., and Voth G.A. The mechanism of hydrated proton transport in water. J. Am. Chem. Soc. 122 (2000) 12027-12028
35. Ohmine I., and Saito S. Water dynamics: Fluctuation, relaxation, and chemical reactions in hydrogen bond network rearrangement. Acc. Chem. Res. 32 (1999) 741-749
36. Luz Z., and Meiboom S. The activation energies of proton transfer reactions in water. J. Am. Chem. Soc. 86 (1964) 4768
37. Pines E., Huppert D., and Agmon N. Geminate recombination in excited-state proton-transfer reactions-numerical-solution of the Debye-Smoluchowski equation with backreaction and comparison with experimental results. J. Chem. Phys. 88 (1988) 5620-5630
38. Schmitt U.W., and Voth G.A. The computer simulation of proton transport in water. J. Chem. Phys. 111 (1999) 9361-9381
39. Onsager L. Ion passages in lipid bilayers. Science 156 (1967) 541-543
40. Nagle J.F., and Morowitz H.J. Molecular mechanisms for proton transport in membranes. Proc. Natl. Acad. Sci. U. S. A. 75 (1978) 298-302
41. Nagle J.F., and Tristram-Nagle S. Hydrogen bonded chain mechanisms for proton conduction and proton pumping. J. Membr. Biol. 74 (1983) 1-14
42. Zundel G., and Schwab G.-M. Foils of polystyrenesulfonic acid and its salts. Continuous absorption spectrum of aqueous acid solutions. J. Phys. Chem. 67 (1963) 771-773
43. Zundel G. Hydrogen bonds with large polarizability and proton transfer processes in electrochemistry and biology. In: Prigogine I., and Rice S.A. (Eds). Advances in Chemical Physics (2000), John Wiley and Sons, New York 1-217
44. Rousseau R., Kleinschmidt V., Schmitt U.W., and Marx D. Assigning protonation patterns in water networks in bacteriorhodopsin based on computed IR spectra. Angew. Chem., Int. Ed. 43 (2004) 4804-4807
45. Garczarek F., Brown L.S., Lanyi J., and Gerwert K. Proton binding with a membrane protein by a protonated water cluster. Proc. Natl. Acad. Sci. U. S. A. 102 (2005) 3633-3638
46. Asmis K.R., Pivonka N.L., Santambrogio G., Brümmer M., Kaposta C., Neumark D.M., and Wöste L. Gas-phase infrared spectrum of the protonated water dimer. Science 299 (2003) 1375-1377
47. n (n = 6 to 27) clusters. Science 304 (2004) 1137-1140
48. Headrick J.M., Diken E.G., Walters R.S., Hammer N.I., Christie R.A., Cui J., Myshakin E.M., Duncan M.A., Johnson M.A., and Jordan K.D. Spectral signatures of hydrated proton vibrations in water clusters. Science 308 (2005) 1765-1769
49. Nagle J.F., Mille M., and Morowitz H.J. Theory of hydrogen bonded chains in bioenergetics. J. Chem. Phys. 72 (1980) 3959-3971
50. Hodgkin A.L., and Keynes R.D. The potassium permeability of a giant nerve fibre. J. Physiol. 128 (1955) 61-88
51. + conduction and selectivity. Science 280 (1998) 69-77
52. + channel-Fab complex at 2.0 Å resolution. Nature 414 (2001) 43-48
53. Finkelstein A., and Andersen O.S. The gramicidin A channel. A review of its permeability characteristics with special reference to the single-file aspect oftransport. J. Membr. Biol. 59 (1981) 155-171
54. Andersen O.S., and Koeppe R.E. Molecular determinants of channel function. Physiol. Rev. 72 (1992) S89-S158
55. Cukierman S. The transfer of protons in water wires inside proteins. Front. Biosci. 8 (2003) s1118-s1139
56. (L, D) helices. Proc. Natl. Acad. Sci. U. S. A. 68 (1971) 672-676
57. Bamberg E., and Janko K. The action of carbonsuboxide dimerized gramicidin A on lipid bilayer membranes. Biochim. Biophys. Acta 465 (1977) 486-499
58. Stankovic C.J., Heinemann S.H., Delfino J.M., Sigworth F.J., and Schreiber S.L. Transmembrane channels based on tartaric acid-dimer gramicidin A hybrids. Science 244 (1989) 813-817
59. Cukierman S., Quigley E.P., and Crumrine D.S. Proton conduction in gramicidin A and its dioxolane-linked dimer in different lipid bilayers. Biophys. J. 73 (1997) 2489-2502
60. Cukierman S. Proton mobilities in water and in different stereoisomers of covalently linked gramicidin A channels. Biophys. J. 78 (2000) 1825-1834
61. Bamberg E., Noda K., Gross E., and Lauger P. Single-channel parameters of gramicidin A, B and C. Biochim. Biophys. Acta 419 (1976) 223-238
62. Becker M.D., Greathouse D.V., Koeppe II R.E., and Andersen O.S. Amino acid sequence modulation of gramicidin channel function: Effects of tryptophan-to-phenylalanine substitutions on the single channel conductance and duration. Biochemistry 30 (1991) 8830-8839
63. Andersen O.S., Greathouse D.V., Providence L.L., Becker M.D., and Koeppe I.R.E. Importance of tryptophan dipoles for protein function: 5-fluorination of tryptophans in gramicidin A channels. J. Am. Chem. Soc. 120 (1998) 5142-5146
64. Gowen J.A., Markham J.C., Morrison S.E., Cross T.A., Busath D.D., Mapes E.J., and Schumaker M.F. The role of Trp Side chains in tuning single proton conduction through gramicidin channels. Biophys. J. 83 (2002) 880-898
65. Andersen O.S. Ion movement through gramicidin A channels. Single-channel measurements at very high potentials. Biophys. J. 41 (1983) 119-133
66. Andersen O.S. Ion movement through gramicidin A channels. Interfacial polarization effects on single-channel measurements. Biophys. J. 41 (1983) 135-146
67. Andersen O.S. Ion movement through gramicidin A channels. Studies on the diffusion-controlled association step. Biophys. J. 41 (1983) 147-165
68. Levitt D.G., Elias S.R., and Hautman J.M. Number of water molecules coupled to the transport of sodium, potassium and hydrogen ions via gramicidin, nonactin and valinomycin. Biochim. Biophys. Acta 512 (1978) 436-451
69. Rosenberg P.A., and Finkelstein A. Interaction of ions and water in gramicidin A channels. Streaming potentials across lipid bilayer membranes. J. Gen. Physiol. 72 (1978) 327-340
70. Rosenberg P.A., and Finkelstein A. Water permeability of gramicidin A treated lipid bilayer membranes. J. Gen. Physiol. 72 (1978) 341-350
71. Dani J.A., and Levitt D.G. Water transport and ion-water interactions in the gramicidin channel. Biophys. J. 35 (1981) 501-508
72. + in the gramicidin channel determined from water permeability measurements. Biophys. J. 35 (1981) 485-499
73. Neher E., Sandblom J., and Eisenman G. Ionic selectivity, saturation, and block in gramicidin A channels: II. Saturation behavior of single channel conductances and evidence for the existence of multiple binding sites in the channel. J. Membr. Biol. 40 (1978) 97-116
74. Owen B.B., and Sweeton F.H. The conductance of hydrochloric acid in aqueous solutions from 5° to 65°. J. Am. Chem. Soc. 63 (1941) 2811-2817
75. Lown D.A., and Thirsk H.R. Proton transfer conductance in aqueous solution: Part 2.-Effect of pressure on the electrical conductivity of concentrated orthophosphoric acid in water at 25°C. Trans. Faraday Soc. 67 (1971) 149-152
76. Chiu S.-W., Subramaniam S., and Jakobsson E. Simulation study of a gramicidin/lipid bilayer system in excess water and lipid: II. Rates and mechanism of water transport. Biophys. J. 76 (1999) 1939-1950
77. Levitt D.G. Kinetics of movement in narrow channels. Curr. Top. Membr. Trans. 21 (1984) 181-197
78. +, and effects of anion binding. Biophys. J. 22 (1978) 307-340
79. Hinton J.F., Whaley W.L., Shungu D., Koeppe R.E., and Millett F.S. Equilibrium binding constants for the group I metal cations with gramicidin A determined by competition studies and Tl-205 nuclear magnetic resonance spectroscopy. Biophys. J. 50 (1986) 539-544
80. Tian F., and Cross T.A. Cation transport: An example of structural based selectivity. J. Mol. Biol. 285 (1999) 1993-2003
81. + translocation along the single-file water chain in the gramicidin A channel. Biophys. J. 71 (1996) 19-39
82. + conduction along hydrogen-bonded chains of water molecules. Biophys. J. 75 (1998) 33-40
83. + conductance through a gramicidin channel. Biophys. J. 53 (1988) 25-32
84. Phillips L.R., Cole C.D., Hendershot R.J., Cotten M., Cross T.A., and Busath D.D. Noncontact dipole effects on channel permeation: III. Anomalous proton conductance effects in gramicidin. Biophys. J. 77 (1999) 2492-2501
85. + conduction in the single-file water chain of the gramicidin channel. Biophys. J. 82 (2002) 2304-2316
86. Schumaker M.F. Numerical framework models of single proton conduction through gramicidin. Front. Biosci. 8 (2003) s982-s991
87. Braun-Sand S., Burykin A., Chu Z.T., and Warshel A. Realistic simulations of proton transport along the gramicidin channel: demonstrating the importance of solvation effects. J. Phys. Chem., B 109 (2005) 583-592
88. de Godoy C.M.G., and Cukierman S. Modulation of proton transfer in the water wire of dioxolane-linked gramicidin channels by lipid membranes. Biophys. J. 81 (2001) 1430-1438
89. Burykin A., and Warshel A. What really prevents proton transport through aquaporin? Charge self-energy versus proton wire proposals. Biophys. J. 85 (2003) 3696-3706
90. Olsson M.H.M., Sharma P.K., and Warshel A. Simulating redox coupled proton transfer in cytochrome c oxidase: Looking for the proton bottleneck. FEBS Lett. 579 (2005) 2026-2034
91. Warshel A. Molecular dynamics simulations of biological reactions. Acc. Chem. Res. 35 (2002) 385-395
92. Hummer G., Rasaiah J.C., and Noworyta J.P. Water conduction through the hydrophobic channel of a carbon nanotube. Nature 414 (2001) 188-190
93. Beckstein O., Biggin P.C., Bond P., Bright J.N., Domene C., Grottesi A., Holyoake J., and Sansom M.S. Ion channel gating: insights via molecular simulations. FEBS Lett. 555 (2003) 85-90
94. Beckstein O., and Sansom M.S.P. Liquid-vapor oscillations in hydrophobic nanopores. Proc. Natl. Acad. Sci. U. S. A. 100 (2003) 7063-7068
95. Beckstein O., Tai K., and Sansom M.S.P. Not ions alone: barriers to ion permeation in nanopores and channels. J. Am. Chem. Soc. 126 (2004) 14694-14695
96. Beckstein O., and Sansom M.S. The influence of geometry, surface character, and flexibility on the permeation of ions and water through biological pores. Phys. Biol. 1 (2004) 42-52
97. Corry B. Theoretical conformation of the closed and open states of the acetylcholine receptor channel. Biochim. Biophys. Acta 1663 (2004) 2-5
98. Sotomayor M., and Schulten K. Molecular dynamics study of gating in the mechanosensitive channel of small conductance MscS. Biophys. J. 87 (2004) 3050-3065
99. Spronk S.A., Elmore D.E., and Dougherty D.A. Voltage-dependent hydration and conduction properties of the hydrophobic pore of the mechanosensitive channel of small conductance. Biophys. J. 90 (2006) 3555-3569
100. Martí J., and Gordillo M.C. Temperature effects on the static and dynamic properties of liquid water inside nanotubes. Phys. Rev., E 64 (2001) 1-6 (021504)
101. Holt J.K., Park H.G., Wang Y., Stadermann M., Artyukhin A.B., Grigoropoulos C.P., Noy A., and Bakajin O. Fast mass transport through sub-2-nanometer carbon nanotubes. Science 312 (2006) 1034-1037
102. Brewer M.L., Schmitt U.W., and Voth G.A. The formation and dynamics of proton wires in channel environments. Biophys. J. 80 (2001) 1691-1702
103. Dellago C., Naor M., and Hummer G. Proton transport through water-filled nanotubes. Phys. Rev. Lett. 90 (2003) 1-4 (105902)
104. Lynden-Bell R.M., and Rasaiah J.C. Mobility and solvation of ions in channels. J. Chem. Phys. 105 (1996) 9266-9280
105. Wu Y., and Voth G.A. A computer simulation study of the hydrated proton in a synthetic proton channel. Biophys. J. 85 (2003) 864-875
106. Lear J.D., Wasserman Z.R., and DeGrado W.F. Synthetic amphiphilic peptide models for protein ion channels. Science 240 (1988) 1177-1181
107. Sarkar N., and Paulus H. Function of peptide antibiotics in sporulation. Nat. New Biol. 239 (1972) 228-230
108. Paulus H., Sarkar N., Mukherjee P.K., Langley D., Ivanov V.T., Shepel E.N., and Veatch W. Comparison of the effect of linear gramicidin analogues on bacterial sporulation, membrane permeability, and ribonucleic acid polymerase. Biochemistry 18 (1979) 4532-4536
109. Fisher R., and Blumenthal T. An Interaction between Gramicidin and the Subunit of RNA Polymerase. Proc. Natl. Acad. Sci. U. S. A. 79 (1982) 1045-1048
110. Sui H., Han B.G., Lee J.K., Walian P., and Jap B.K. Structural basis of water-specific transport through the AQP1 water channel. Nature 414 (2001) 872-878
111. Tajkhorshid E., Nollert P., Jensen M.Ø., Miercke L.J.W., O'Connell J., Stroud R.M., and Schulten K. Control of the selectivity of the aquaporin water channel family by global orientational tuning. Science 296 (2002) 525-530
112. Jensen M.Ø., Tajkhorshid E., and Schulten K. Electrostatic tuning of permeation and selectivity in aquaporin water channels. Biophys. J. 85 (2003) 2884-2899
113. Chakrabarti N., Tajkhorshid E., Roux B., and Pomès R. Molecular basis of proton blockage in aquaporins. Structure 12 (2004) 65-74
114. Ilan B., Tajkhorshid E., Schulten K., and Voth G.A. The mechanism of proton exclusion in aquaporin channels. Proteins 55 (2004) 223-228
115. Chakrabarti N., Roux B., and Pomès R. Structural determinants of proton blockage in aquaporins. J. Mol. Biol. 343 (2004) 493-510
116. Chen H., Wu Y., and Voth G.A. Origins of proton transport behavior from selectivity domain mutations of the aquaporin-1 channel. Biophys. J. 90 (2006) L73-L75
117. H. Chen, B. Ilan, Y. Wu, C.J. Burnham, F. Zhu, E. Tajkhorshid, K. Schulten, and G.A. Voth, Electrostatics and charge delocalization in proton channels: the aquaporin channels and proton blockage, J. Mol. Biol. (in press).
118. Burykin A., and Warshel A. On the origin of the electrostatic barrier for proton transport in aquaporin. FEBS Lett. 570 (2004) 41-46
119. Beitz E., Wu B., Holm L.M., Schultz J.E., and Zeuthen T. Point mutations in the aromatic arginine region in aquaporin 1 allow passage of urea, glycerol, ammonia, and protons. Proc. Natl. Acad. Sci. U. S. A. 103 (2006) 269-274
120. Liu K., Kozono D., Kato Y., Agre P., Hazama A., and Yasui M. Conversion of aquaporin 6 from an anion channel to a water-selective channel by a single amino acid substitution. Proc. Natl. Acad. Sci. U. S. A. 102 (2005) 2192-2197
121. Warshel A. Inverting the selectivity of aquaporin 6: Gating versus direct electrostatic interaction. Proc. Natl. Acad. Sci. U. S. A. 102 (2005) 1813-1814
122. Chernyshev A., and Cukierman S. Thermodynamic view of activation energies of proton transfer in various gramicidin A channels. Biophys. J. 82 (2002) 182-192
123. Xu J., and Voth G.A. Computer simulation of explicit proton translocation in cytochrome c oxidase: The D-pathway. Proc. Natl. Acad. Sci. U. S. A. 102 (2005) 6795-6800
124. Junge W., and McLaughlin S. The role of fixed and mobile buffers in the kinetics of proton movement. Biochim. Biophys. Acta 890 (1987) 1-5
125. Junge W., and Polle A. Theory of proton flow along appressed thylakoid membranes under instationary and under stationary conditions. Biochim. Biophys. Acta 848 (1986) 265-273
126. Gutman M., and Nachliel E. The dynamics of proton exchange between bulk and surface groups. Biochim. Biophys. Acta 1231 (1995) 123-138
127. Gutman M., and Nachliel E. Time-resolved dynamics of proton transfer in proteinous systems. Annu. Rev. Phys. Chem. 48 (1997) 329-356
128. Ädelroth P., and Brzezinski P. Surface-mediated proton-transfer reactions in membrane-bound proteins. Biochim. Biophys. Acta 1655 (2004) 102-115
129. Feniouk B.A., Kozlova M.A., Knorre D.A., Cherepanov D.A., Mulkidjanian A.Y., and Junge W. The proton-driven rotor of ATP synthase: ohmic conductance (10 fS), and absence of voltage gating. Biophys. J. 86 (2004) 4094-4109
130. Lauger P. Diffusion-limited ion flow through channels. Biochim. Biophys. Acta 455 (1976) 493-509
131. M. Smoluchowski, Drei Vorträge über Diffusion, Brownsche Molekularbewegung und Koagulation von Kolloidteilchen, Phys. Z. 17 (1916) 557-571 and 585-599.
132. Debye P. Reaction rates in ionic solutions. Trans. Electrochem. Soc. 82 (1942) 265-272
133. Friedman R., Nachliel E., and Gutman M. Application of classical molecular dynamics for evaluation of proton transfer mechanism on a protein. Biochim. Biophys. Acta 1710 (2005) 67-77
134. Eigen M. Diffusion control in biochemical reactions. In: Mintz S.L., and Widmayer S.M. (Eds). Quantum Statistical Mechanisms in Natural Sciences (1974), Plenum Press, New York 37-61
135. Zhang J., and Unwin P.R. Proton diffusion at phospholipid assemblies. J. Am. Chem. Soc. 124 (2002) 2379-2383
136. Serowy S., Saparov S.M., Antonenko Y.N., Kozlovsky W., Hagen V., and Pohl P. Structural proton diffusion along lipid bilayers. Biophys. J. 84 (2003) 1031-1037
137. Mulkidjanian A.Y., Heberle J., and Cherepanov D.A. Protons @ interfaces: Implications for biological energy conversion. Biochim. Biophys. Acta (2006) 10.1016/j.bbabio.2006.02.015 (this issue)
138. Sacks V., Marantz Y., Aagaard A., Checover S., Nachliel E., and Gutman M. The dynamic feature of the proton collecting antenna of a protein surface. Biochim. Biophys. Acta 1365 (1998) 232-240
139. Kasianowicz J., Benz R., and McLaughlin S. How do protons cross the membrane-solution interface? Kinetic studies on bilayer membranes exposed to the protonophore S-13 (5-chloro-3-tert-butyl-2′-chloro-4′-nitrosalicylanilide). J. Membr. Biol. 95 (1987) 73-89
140. B of the reaction center in chromatophores of Rhodobacter sphaeroides: Retarded conveyance by neutral water. Proc. Natl. Acad. Sci. U. S. A. 96 (1999) 13159-13164
141. - state of bacterial photosynthetic reaction centers: Rate limitation within the protein. Biophys. J. 73 (1997) 367-381
142. Brandsburg-Zabary S., Fried O., Marantz Y., Nachliel E., and Gutman M. Biophysical aspects of intra-protein proton transfer. Biochim. Biophys. Acta 1458 (2000) 120-134
143. DeCoursey T.E. Voltage-gated proton channels and other proton transfer pathways. Physiol. Rev. 83 (2003) 475-579
144. Aagaard A., Namslauer A., and Brzezinski P. Inhibition of proton transfer in cytochrome c oxidase by zinc ions: delayed proton uptake during oxygen reduction. Biochim. Biophys. Acta 1555 (2002) 133-139
145. 2+. Proc. Natl. Acad. Sci. U. S. A. 96 (1999) 6183-6188
146. 2+ and other divalent cations. J. Gen. Physiol. 114 (1999) 819-838
147. Sasaki M., Takagi M., and Okamura Y. A voltage sensor-domain protein is a voltage-gated proton channel. Science 312 (2006) 589-592
148. Ramsey I.S., Moran M.M., Chong J.A., and Clapha D.E. A voltage-gated proton-selective channel lacking the pore domain. Nature 440 (2006) 1213-1216
149. Wraight C.A. Proton and electron transfer in the acceptor quinone complex of bacterial photosynthetic reaction centers. Front. Biosci. 9 (2004) 309-327
150. o motor of the ATP synthase. Biochim. Biophys. Acta 1458 (2000) 374-386
151. +-transporting ATP synthase derived by solution NMR and intersubunit cross-linking in situ. Biochim. Biophys. Acta 1565 (2002) 232-245
152. Ferguson-Miller S., and Babcock G.T. Heme/copper terminal oxidases. Chem. Rev. 7 (1996) 2889-2907
153. Gennis R.B. Principles of molecular bioenergetics and the proton pump of cytochrome oxidase. In: Wikstrom M. (Ed). Biophysical and Structural Aspects of Bioenergetics (2005), Royal Society of Chemistry, Cambridge, UK 1-25
154. Brändén G., Gennis R.B., and Brzezinski P. Transmembrane proton translocation by cytochrome c oxidase. Biochim. Biophys. Acta (2006) 10.1016/j.bbabio.2006.05.020 (this issue)
155. Konstantinov A.A., Siletsky S., Mitchell D., Kaulen A., and Gennis R.B. The roles of the two proton input channels in cytochrome c oxidase from Rhodobacter sphaeroides probed by the effects of site-directed mutations on time-resolved electrogenic intraprotein proton transfer. Proc. Natl. Acad. Sci. U. S. A. 94 (1997) 9085-9090
156. Yoshikawa S. Structural chemical studies of the reaction mechanism of cytochrome c oxidase. In: Wikström M. (Ed). Biophysical and Structural Aspects of Bioenergetics (2005), Royal Society of Chemistry, Cambridge, UK 55-71
157. Sharp M.A., Qin L., and Ferguson-Miller S. Proton entry, exit and pathways in cytochrome oxidase: Insight from conserved water. In: Wikström M. (Ed). Biophysical and Structural Aspects of Bioenergetics (2005), Royal Society of Chemistry, Cambridge, UK 26-54
158. Tsukihara T., Shimokata K., Katayama Y., Shimada H., Muramoto K., Aoyama H., Mochizuki M., Shinzawa-Itoh K., Yamashita E., Yao M., Ishimura Y., and Yoshikawa S. The low-spin heme of cytochrome c oxidase as the driving element of the proton-pumping process. Proc. Natl. Acad. Sci. U. S. A. 100 (2003) 15304-15309
159. Pfitzner U., Hoffmeier K., Harrenga A., Kannt A., Michel H., Bamberg E., Richter O.-M.H., and Ludwig B. Tracing the D-pathway in reconstituted site-directed mutants of cytochrome c oxidase from Paracoccus denitrificans. Biochemistry 39 (2000) 6756-6762
160. Pomès R., Hummer G., and Wikström M. Structure and dynamics of a proton shuttle in cytochrome c oxidase. Biochim. Biophys. Acta 1365 (1998) 255-260
161. Hofacker I., and Schulten K. Oxygen and proton pathways in cytochrome c oxidase. Proteins 30 (1998) 100-107
162. Wikström M., Verkhovsky M.I., and Hummer G. Water-gated mechanism of proton translocation by cytochrome c oxidase. Biochim. Biophys. Acta 1604 (2003) 61-65
163. Olkhova E., Hutter M.C., Lill M.A., Helms V., and Michel H. Dynamic water networks in cytochrome c oxidase from Paracoccus denitrificans investigated by molecular dynamics simulations. Biophys. J. 86 (2004) 1873-1889
164. Wikström M., Ribacka C., Molin M., Laakkonen L., Verkhovsky M., and Puustinen A. Gating of proton and water transfer in the respiratory enzyme cytochrome c oxidase. Proc. Natl. Acad. Sci. U. S. A. 102 (2005) 10478-10481
165. Olsson M.H.M., and Warshel A. Monte Carlo simulations of proton pumps. on the working principles of the biological valve that controls proton pumping in cytochrome c oxidase. Proc. Natl. Acad. Sci. U. S. A. 103 (2006) 6500-6505
166. Kornblatt J.A. The water channel of cytochrome c oxidase: inferences from inhibitor studies. Biophys. J. 75 (1998) 3127-3134
167. Mitchell D.M., Fetter J.R., Mills D.A., Ädelroth P., Pressler M.A., Kim Y., Aasa R., Brzezinski P., Malmström B.G., Alben J.O., Babcock G.T., Ferguson-Miller S., and Gennis R.B. Site-directed mutagenesis of residues lining a putative proton transfer pathway in cytochrome c oxidase from Rhodobacter sphaeroides. Biochemistry 35 (1996) 13089-13093
168. Tu C., Qian M., Earnhardt J.N., Laipis P.J., and Silverman D.N. Properties of intramolecular proton transfer in carbonic anhydrase III. Biophys. J. 74 (1998) 3183-3189
169. Tu C., Rowlett R.S., Tripp B.C., Ferry J.G., and Silverman D.N. Chemical rescue of proton transfer in catalysis by carbonic anhydrases in the beta- and gamma-class. Biochemistry 41 (2002) 15429-15435
170. Lindskog S., and Silverman D.N. The catalytic mechanism of mammalian carbonic anhydrases. EXS 90 (2000) 175-195
171. Cui Q., and Karplus M. Is a "proton wire" concerted or stepwise? A model study of proton transfer in carbonic anhydrase. J. Phys. Chem., B 107 (2003) 1071-1078
172. Braun-Sand S., Strajbl M., and Warshel A. Studies of proton translocation in biological systems: simulating proton transport in carbonic anhydrase by EVB-based models. Biophys. J. 87 (2004) 2221-2239
173. Schutz C.N., and Warshel A. Analyzing free energy relationships for proton translocations in enzymes: carbonic anhydrase revisited. J. Phys. Chem., B 108 (2004) 2066-2075
174. Lanyi J.K. Crystallographic studies of the conformational changes that drive directional transmembrane ion movement in bacteriorhodopsin. Biochim. Biophys. Acta 1459 (2000) 339-345
175. Edmonds B.W., and Luecke H. Atomic resolution structures and the mechanism of ion pumping in bacteriorhodopsin. Front. Biosci. 9 (2004) 1556-1566
176. Lanyi J.K. A structural view of proton transport by bacteriorhodopsin. In: Wikström M. (Ed). Biophysical and Structural Aspects of Bioenergetics (2005), Royal Society of Chemistry, Cambridge, UK 227-248
177. Heberle J. The dynamics of proton transfer across bacteriorhodopsin explored by FT-IR spectroscopy. In: Wikstrom M. (Ed). Biophysical and Structural Aspects of Bioenergetics (2005), Royal Society of Chemistry, Cambridge, UK 249-272
178. a calculations suggest storage of an excess proton in a hydrogen-bonded water network in bacteriorhodopsin. J. Mol. Biol. 312 (2001) 203-219
179. Song Y., Mao J., and Gunner M.R. Calculation of proton transfers in Bacteriorhodopsin bR and M intermediates. Biochemistry 42 (2003) 9875-9888
180. Baudry J., Tajkhorshid E., Molnar F., Phillips J., and Schulten K. Molecular dynamics study of bacteriorhodopsin and the purple membrane. J. Phys. Chem., B 105 (2001) 905-918
181. Kandt C., Gerwert K., and Schlitter J. Water dynamics simulation as a tool for probing proton transfer pathways in a heptahelical membrane protein. Proteins 58 (2005) 528-537
182. Kandt C., Schlitter J., and Gerwert K. Dynamics of water molecules in the bacteriorhodopsin trimer in explicit lipid/water environment. Biophys. J. 86 (2004) 705-717
183. Rammelsberg R., Huhn G., Lübben M., and Gerwert K. Bacteriorhodopsin's intramolecular proton-release pathway consists of a hydrogen-bonded network. Biochemistry 37 (1998) 5001-5009
184. Hayashi S., and Ohmine I. Proton transfer in bacteriorhodopsin: structure, excitation, IR spectra, and potential energy surface analysis by an ab initio QM/MM method. J. Phys. Chem., B 104 (2000) 10678-10691
185. Heberle J., Riesle J., Thiedemann G., Oesterhelt D., and Dencher N. Proton migration along the membrane surface and retarded surface to bulk transfer. Nature 370 (1994) 379-382
186. Heberle J., and Dencher N. Surface-bound optical probes monitor proton translocation and surface potential changes during bacteriorhodopsin photocycle. Proc. Natl. Acad. Sci. U. S. A. 89 (1992) 5996-6000
187. Scherrer P., Alexiev U., Marti T., Khorana H.G., and Heyn M.P. Covalently bound pH-indicator dyes at selected extracellular or cytoplasmic sites in bacteriorhodopsin: 1. Proton migration along the surface of bacteriorhodopsin micelles and its delayed transfer from surface to bulk. Biochemistry 33 (1994) 13684-13692
188. Nachliel E., and Gutman M. Quantitative evaluation of the dynamics of proton transfer from photoactivated bacteriorhodopsin to the bulk. FEBS Lett. 393 (1996) 221-225
189. Kocher J.-P., Prévost M., Wodak S.J., and Lee B. Properties of the protein matrix revealed by the free energy of cavity formation. Structure 4 (1996) 1517-1529
190. Garczarek F., and Gerwert K. Functional waters in intraprotein proton transfer monitored by FTIR difference spectroscopy. Nature 439 (2006) 109-112
191. Mitchell P. Coupling of phosphorylation to electron and hydrogen transfer by a chemi-osmotic type of mechanism. Nature 191 (1961) 141-148
192. Mitchell P. Keilin's respiratory chain concept and its chemiosmotic consequences. Science 206 (1979) 1148-1159
193. Kaminskaya O.P., Drachev L.A., Konstantinov A.A., Semenov A.Y., and Skulachev V.P. Electrogenic reduction of the secondary quinone acceptor in chromatophores of Rhodospirillum rubum. FEBS Lett. 202 (1987) 224-228
194. - transition. FEBS Lett. 412 (1997) 490-494
195. - in bacterial wild-type and mutant reaction centers. Biochim. Biophys. Acta 1231 (1997) 149-156
196. Crofts A.R., and Wraight C.A. The electrochemical domain of photosynthesis. Biochim. Biophys. Acta 726 (1983) 149-185
197. Shinkarev V.P., and Wraight C.A. Electron and proton transfer in the acceptor quinone complex of reaction centers of phototrophic bacteria. In: Deisenhofer J., and Norris J.R. (Eds). The Photosynthetic Reaction Center (1993), Academic Press, San Diego 193-255
198. Okamura M.Y., Paddock M.L., Graige M.S., and Feher G. Proton and electron transfer in bacterial reaction centers. Biochim. Biophys. Acta 1458 (2000) 148-163
199. + binding by bacterial photosynthetic reaction centers: comparison of spectrophotometric and conductimetric methods. Biochim. Biophys. Acta 934 (1988) 314-328
200. + binding by bacterial reaction centers: Influences of the redox states of the acceptor quinones and primary donor. Biochim. Biophys. Acta 934 (1988) 329-347
201. -. Biochim. Biophys. Acta 934 (1988) 348-368
202. B in bacterial photosynthetic reaction centers. Biochemistry 38 (1999) 8254-8270
203. Paddock M.L., Feher G., and Okamura M.Y. Proton transfer pathways and mechanism in bacterial reaction centers. FEBS Lett. 555 (2003) 45-50
204. - formation in the photosynthetic reaction center of Rhodobacter sphaeroides: Evidence from time-resolved infrared spectroscopy. Biochemistry 34 (1995) 2832-2843
205. Nabedryk E., Breton J., Hienerwadel R., Fogel C., Mäntele W., Paddock M.L., and Okamura M.Y. Fourier transform infrared difference spectroscopy of secondary quinone acceptor photoreduction in proton transfer mutants of Rhodobacter sphaeroides. Biochemistry 34 (1995) 14722-14732
206. Breton J., and Nabedryk E. Proton uptake upon quinone reduction in bacterial reaction centers: IR signature and possible participation of a highly polarizable hydrogen bond network. Photosynth. Res. 55 (1998) 307-310
207. Remy A., and Gerwert K. Coupling of light-induced electron transfer to proton uptake in photosynthesis. Nat. Struct. Biol. 10 (2003) 637-644
208. B photoreduction in Rhodobacter sphaeroides reaction center mutants at Asp-L213 and Glu-L212 sites. Biochemistry 43 (2004) 7236-7243
209. -) in the reaction center from Rhodobacter sphaeroides. Biochemistry 44 (2005) 14519-14527
210. Takahashi E., Maróti P., and Wraight C.A. Coupled proton and electron transfer pathways in the acceptor quinone complex of reaction centers from Rhodobacter sphaeroides. In: Diemann E., et al. (Ed). Electron and Proton Transfer in Chemistry and Biology (1992), Elsevier, Amsterdam 219-236
211. L213 in the proton transfer pathway to the secondary quinone of reaction centers from Rhodobacter sphaeroides. Biochim. Biophys. Acta 1020 (1990) 107-111
212. - binding site of Rhodobacter sphaeroides reaction centers. FEBS 283 (1991) 140-144
213. B). Biochemistry 40 (2001) 6893-6902
214. 2+. Proc. Natl. Acad. Sci. U. S. A. 97 (2000) 1548-1553
215. Paddock M.L., McPherson P.H., Feher G., and Okamura M.Y. Pathway of proton transfer in bacterial reaction centers: replacement of serine-L223 by alanine inhibits electron and proton transfers associated with reduction of quinone to dihydroquinone. Proc. Natl. Acad. Sci. U. S. A. 87 (1990) 6803-6807
216. Paddock M.L., Feher G., and Okamura M.Y. Pathway of proton transfer in bacterial reaction centers: further investigations on the role of Ser-L223 studied by site-directed mutagenesis. Biochemistry 34 (1995) 15742-15750
217. Paddock M.L., Rongey S.H., McPherson P.H., Juth A., Feher G., and Okamura M.Y. Pathway of proton transfer in bacterial reaction centers: role of aspartate-L213 in proton transfers associated with reduction of quinone to dihydroquinone. Biochemistry 33 (1994) 734-745
218. 2 share a common entry point. Proc. Natl. Acad. Sci. U. S. A. 97 (2000) 13086-13091
219. Ädelroth P., Paddock M.L., Tehrani A., Beatty J.T., Feher G., and Okamura M.Y. Identification of the proton pathway in bacterial reaction centers: Decrease of proton transfer rate by mutation of surface histidines at H126 and H128 and chemical rescue by imidazole identifies the initial proton donors. Biochemistry 40 (2001) 14538-14546
220. - is restored in bacterial reaction centers of Rhodobacter sphaeroides containing the Asp-L213→Asn lesion. Photosynth. Res. 55 (1998) 281-291
221. 2 is not released from L212EQ mutant reaction centers. Biochim. Biophys. Acta 1142 (1993) 214-216
222. 2 in native and Glu-L212→Gln mutant reaction centers from Rhodobacter sphaeroides. Biochemistry 33 (1994) 1181-1193
223. 2-. Biochim. Biophys. Acta 1144 (1993) 309-324
224. Mulkidjanian A.Y. Conformationally controlled pK-switching in membrane proteins: One more mechanism specific to the enzyme catalysis?. FEBS Lett. 463 (1999) 199-204
225. B) reduction in reaction centers of Rb. sphaeroides. J. Am. Chem. Soc. 118 (1996) 9005-9016
226. - in Asp-L213→Asn mutant RCs from Rb. sphaeroides. Biophys. J. 70 (1996) A11
227. Graige M.S., Paddock M.L., Feher G., and Okamura M.Y. 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 (1999) 11465-11473
228. B in photosynthetic reaction centers. Biochemistry 39 (2000) 5940-5952
229. Wraight C.A. Intraprotein proton transfer-Concepts and realities from the bacterial photosynthetic reaction center. In: Wikström M. (Ed). Biophysical and Structural Aspects of Bioenergetics (2005), Royal Society of Chemistry, Cambridge, UK 273-313
230. Takahashi E., and Wraight C.A. Potentiation of proton transfer function by electrostatic interactions in photosynthetic reaction centers from Rhodobacter sphaeroides: First results from site directed mutation of the H-subunit. Proc. Natl. Acad. Sci. U. S. A. 93 (1996) 2640-2645
231. B binding site of the photosynthetic reaction center. Proc. Natl. Acad. Sci. U. S. A. 90 (1993) 8929-8933
232. Rongey S.H., Paddock M.L., Feher G., and Okamura M.Y. Pathway of proton transfer in bacterial reaction centers: Second-site mutation Asn-M44→Asp restores electron and proton transfer in reaction centers from the photosynthetically deficient Asp-L213→Asn mutant of Rhodobacter sphaeroides. Proc. Natl. Acad. Sci. U. S. A. 90 (1993) 1325-1329
233. Maróti P., Hanson D.K., Baciou L., Schiffer M., and Sebban P. Proton conduction within the reaction centers of Rhodobacter capsulatus: The electrostatic role of the protein. Proc. Natl. Acac. Sci. U. S. A. 91 (1994) 5617-5621
234. Sebban P., Maróti P., Schiffer M., and Hanson D.K. Electrostatic dominoes: long distance propagation of mutational effects in photosynthetic reaction centers of Rhodobacter capsulatus. Biochemistry 34 (1995) 8390-8397
235. B can be achieved in the absence of L212Glu. Biochemistry 36 (1997) 12216-12226
236. Paddock M.L., Axelrod H.L., Abresch E.C., Yeh A.P., Rees D.C., Feher G., and Okamura M.Y. Crystal structure of a photosynthetic revertant from Rb. sphaeroides: Mechanism of action of a long distant suppressor mutation. Biophys. J. 76 (1999) A141
237. Pokkuluri P.R., Laible P.D., Deng Y.-L., Wong T.N., Hanson D.K., and Schiffer M. The structure of a mutant photosynthetic reaction center shows unexpected changes in main chain orientations and quinone position. Biochemistry 41 (2002) 5998-6007
238. Xu Q., Axelrod H.L., Abresch E.C., Paddock M.L., Okamura M.Y., and Feher G. X-ray structure determination of three mutants of the bacterial photosynthetic reaction centers from Rb. sphaeroides: altered proton transfer pathways. Structure 12 (2004) 703-715
239. a shifts of key protonatable residues. Biochemistry 40 (2001) 1850-1860
240. 2+ on bacterial reaction center mutants: proton transfer uses interdependent pathways. Biochemistry 41 (2002) 9132-9138
241. A of functionally important histidine residues. Biochemistry 42 (2003) 9626-9632
242. B electron transfer. Biochemistry 37 (1998) 8278-8281
243. 2+ in bacterial reaction centers. Proc. Natl. Acad. Sci. U. S. A. 97 (2000) 1542-1547
244. 2+-substituted photosynthetic bacterial reaction centers: evidence for histidine ligation at the surface metal site. Biochemistry 39 (2000) 2961-2969
245. 2+ site in photosynthetic bacterial reaction centers from Rhodobacter sphaeroides, Rhodobacter capsulatus, and Rhodopseudomonas viridis. Biochemistry 40 (2001) 6132-6141
246. Paddock M.L., Ädelroth P., Feher G., Okamura M.Y., and Beatty J.T. Determination of proton transfer rates by chemical rescue: Application to bacterial reaction centers. Biochemistry 41 (2002) 14716-14725
247. M17. J. Biol. Chem. 281 (2006) 4413-4422
248. Nair H.K., Seravalli J., Arbuckle T., and Quinn D.M. Molecular recognition in acetylcholinesterase catalysis: Free-energy correlations for substrate turnover and inhibition by trifluoro ketone transition-state analogs. Biochemistry 33 (1994) 8566-8576
249. Zhou H.-X., Briggs J.M., and McCammon J.A. A 240-fold electrostatic rate-enhancements for acetylcholinesterase-substrate binding can be predicted by the potential within the active site. J. Am. Chem. Soc. 118 (1996) 13069-13070
250. Nicholls P., Fita I., and Loewen P.C. Enzymology and structure of catalases. Adv. Inorg. Chem. 51 (2001) 51-106
251. Chelikani P., Carpena X., Fita I., and Loewen P.C. An electrical potential in the access channel of catalases enhances catalysis. J. Biol. Chem. 278 (2003) 31290-31296
252. B by interchanging Asp and Glu at the L212 and L213 sites. Biochemistry 36 (1997) 14238-14249
253. Lancaster C.R.D. Ubiquinone reduction and protonation in photosynthetic reaction centres from Rhodopseudomonas viridis-X-ray structures and their functional implications. Biochim. Biophys. Acta 1365 (1998) 143-150
254. B reduction revealed by ENDOR spectroscopy in reaction centers from Rhodobacter sphaeroides. Biophys. J. 88 (2005) 204a
255. -, in the reaction center. Biophys. J. 68 (1995) 2233-2250
256. Lancaster C.R.D., Michel H., Honig B., and Gunner M.R. Calculated coupling of electron and proton transfer in the photosynthetic reaction center of Rhodopseudomonas viridis. Biophys. J. 70 (1996) 2469-2492
257. Zhu Z., and Gunner M.R. The energetics of quinone dependent electron and proton transfers in Rhodobacter sphaeroides photosynthetic reaction centers. Biochemistry 44 (2005) 82-96
258. Rabenstein B., Ullmann G.M., and Knapp E.-W. Calculation of protonation patterns in proteins with structural relaxation and molecular ensembles- application to the photosynthetic reaction center. Eur. Biophys. J. 27 (1998) 626-637
259. Rabenstein B., Ullmann G.M., and Knapp E.-W. Electron transfer between the quinones in the photosynthetic reaction center and its coupling to conformational changes. Biochemistry 39 (2000) 10487-10496
260. B) in bacterial reaction centers from Rhodobacter sphaeroides: FTIR studies on the effects of replacing Glu H173. Biochemistry 37 (1998) 14457-14462
261. B in the photosynthetic reaction center from Rhodobacter capsulatus. Biochemistry 39 (2000) 14654-14663
262. Aagaard A., and Brzezinski P. Zinc ions inhibit oxidation of cytochrome c oxidase by oxygen. FEBS Lett. 494 (2001) 157-160
263. Faxén K., Salomonsson L., Ädelroth P., and Brzezinski P. Inhibition of proton pumping by zinc ions during specific reaction steps in cytochrome c oxidase. Biochim. Biophys. Acta 1757 (2006) 388-394
264. Kolbe M., Besir H., Essen L.-O., and Oesterhelt D. Structure of the light-driven chloride pump halorhodopsin at 1.8 Å resolution. Science 288 (2000) 1390-1396
265. Shopes R.J., and Wraight C.A. Primary donor recovery kinetics in reaction centers from Rhodopseudomonas viridis. The influence of ferricyanide as a rapid oxidant of the acceptor quinones. Biochim. Biophys. Acta 848 (1986) 364-371
266. Horsefield R., Yankovskaya V., Sexton G., Whittingham W., Shiomi K., Omura S., Byrne B., Cecchini G., and Iwata S. Structural and computational analysis of the quinone-binding site of complex II (Succinate-Ubiquinone Oxidoreductase). A mechanism of electron transfer and proton conduction during ubiquinone reduction. J. Biol. Chem. 281 (2006) 7309-7316
267. 1 complex controls the rate of ubihydroquinone oxidation. Biochim. Biophys. Acta 1655 (2004) 77-92
268. 1 complex. Biochim. Biophys. Acta 1018 (1990) 138-141
269. 2 transport in CpI [FeFe]-hydrogenase and the role of packing defects. Structure 13 (2005) 1321-1329
270. Peters J.W., Lanzilotta W.N., Lemon B.J., and Seefeldt L.C. X-ray crystal structure of the Fe-only hydrogenase (CpI) from Clostridium pasteurianum to 1.8 Å resolution. Science 282 (1998) 1853-1858
271. Nicolet Y., Cavazza C., and Fontecilla-Camps J.C. Fe-only hydrogenases: structure, function and evolution. J. Inorg. Biochem. 91 (2002) 1-8
272. Marcus R.A., and Sutin N. Electron transfers in chemistry and biology. Biochim. Biophys. Acta 811 (1985) 265-322
273. Moser C.C., Keske J.M., Warncke K., Farid R.S., and Dutton P.L. Nature of biological electron transfer. Nature 355 (1992) 796-802
274. Marcus R.A. Chemical and electrochemical electron-transfer theory. Annu. Rev. Phys. Chem. 15 (1964) 155-196
275. Nagle J.F. Proton transport in condensed matter. In: Bountis T. (Ed). Proton Transfer in Hydrogen-Bonded Systems (1992), Plenum Press, New York 17-25
276. Subramaniam S., Gerstein M., Oesterhelt D., and Henderson R. Electron diffraction analysis of structural changes in the photocycle of bacteriorhodopsin. EMBO J. 12 (1993) 1-8
277. Humphrey W., Dalke A., and Schulten K. VMD: Visual molecular dynamics. J. Mol. Graph. 14 (1996) 33-38
278. Luecke H., Schobert B., Richter H.T., Cartailler J.P., and Lanyi J.K. Structure of bacteriorhodopsin at 1.55 Å resolution. J. Mol. Biol. 291 (1999) 899-911