Calculated proton uptake on anaerobic reduction of cytochrome c oxidase: Is the reaction electroneutral?

Biochemistry

Volumn 45, Issue 26, 2006, Pages 7959-7975

  Song, Yifan ^a   Michonova Alexova, Ekaterina ^a   Gunner, M R ^a  

^a CITY COLLEGE OF NEW YORK   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ANAEROBIC DIGESTION; BACTERIA; CARBOXYLIC ACIDS; CONTINUUM MECHANICS; ENZYME KINETICS; IONIZATION; PROTONS; REDOX REACTIONS; REDUCTION;

ANAEROBIC REDUCTION; BINUCLEAR CENTER (BNC); ELECTROCHEMICAL GRADIENT; MULTI-CONFORMATION CONTINUUM ELECTROSTATICS (MCCE);

ENZYMES;

COPPER; CYTOCHROME C OXIDASE; GLUTAMINE; HEME; HEME A3; HYDROXIDE; HYDROXYL GROUP; PROPIONIC ACID; PROTON; PROTON PUMP; TYROSINE; UNCLASSIFIED DRUG;

ANAEROBIC METABOLISM; ARTICLE; CALCULATION; ELECTRICITY; ELECTRON; ENZYME ACTIVE SITE; ENZYME BINUCLEAR CENTER; EVALUATION; MULTI CONFORMATION CONTINUUM ELECTROSTATICS; NONHUMAN; OXIDATION REDUCTION STATE; PKA; PRIORITY JOURNAL; PROTON TRANSPORT; REACTION ANALYSIS; REDUCTION; RHODOBACTER SPHAEROIDES;

ANAEROBIOSIS; BACTERIAL PROTEINS; ELECTRON TRANSPORT COMPLEX IV; ELECTROSTATICS; HYDROGEN-ION CONCENTRATION; KINETICS; METALS; MODELS, MOLECULAR; OXIDATION-REDUCTION; PROTEIN CONFORMATION; PROTONS; RHODOBACTER SPHAEROIDES; THERMODYNAMICS;

RHODOBACTER SPHAEROIDES;

EID: 33745605230     PISSN: 00062960     EISSN: None     Source Type: Journal    
DOI: 10.1021/bi052183d     Document Type: Article

References (117)

1. Brzezinski, P. (2004) Redox-driven membrane-bound proton pumps, Trends Biochem. Sci. 29, 380-387.
2. Gennis, R. B. (2003) Some recent contributions of FTIR difference spectroscopy to the study of cytochrome oxidas, FEBS Lett. 555, 2-7.
3. Ferguson-Miller, S., and Babcock, G. T. (1996) Heme/copper terminal oxidases, Chem. Rev. 96, 2889-2907.
4. Wikström, M. (2004) Cytochrome c oxidase: 25 years of the elusive proton pump, Biochim. Biophys. Acta 1655, 241-247.
5. Babcock, G. T., and Wikström, M. (1992) Oxygen activation and the conservation of energy in cell respirations, Nature 356, 301-308.
6. Junemann, S., Meunier, B., Fisher, N., and Rich, P. R. (1999) Effects of mutation of the conserved glutamic acid-286 in subunit I of cytochrome c oxidase from Rhodobacter sphaeroides, Biochemistry 38, 5248-5255.
7. Wikström, M., Jasaitis, A., Backgren, C., Puustinen, A., and Verkhovsky, M. I. (2000) The role of the D- and K-pathways of proton transfer in the function of the haem-copper oxidases, Biochim. Biophys. Acta 1459, 514-520.
8. Ådelroth, P., Karpeforsa, M., Gildersona, G., Tomsonc, F. L., Gennis, R. B., and Brzezinski, P. (2000) Proton transfer from glutamate 286 determines the transition rates between oxygen intermediates in cytochrome c oxidase, Biochim. Biophys. Acta 1459, 533-539.
9. Branden, M., Tomson, F., Gennis, R. B., and Brzezinski, P. (2002) The entry point of the K-proton-transfer pathway in cytochrome c oxidase, Biochemistry 41, 10794-10798.
10. Tomson, F. L., Morgan, J. E., Gu, G., Barquera, B., Vygodina, T. V., and Gennis, R. B. (2003) Substitutions for glutamate 101 in subunit 11 of cytochrome c oxidase from Rhodobacter sphaeroides result in blocking the proton-conducting K-channel, Biochemistry 42, 1711-1717.
11. Junemann, S., Meunier, B., Gennis, R. B., and Rich, P. R. (1997) Effects of mutation of the conserved lysine-362 in cytochrome c oxidase from Rhodobacter sphaeroides, Biochemistry 36, 14456-14464.
12. Wikström, M., Verkhovsky, M. I., and Hummer, G. (2003) Water-gated mechanism of proton translocation by cytochrome c oxidase, Biochim. Biophys. Acta 1604, 61-65.
13. Zheng, X., Medvedev, D. M., Swanson, J., and Stuchebrukhov, A. A. (2003) Computer simulation of water in cytochrome c oxidase, Biochim. Biophys. Acta 1557, 99-107.
14. Olkhova, E., Hutter, M. C., Lill, M. A., Helms, V., and Michel, H. (2004) Dynamic water networks in cytochrome c oxidase from Paracoccus denitrificans investigated by molecular dynamics simulations, Biophys. J. 86, 1873-1889.
15. Ruitenberg, M., Kannt, A., Bamberg, E., Ludwig, B., Michel, H., and Pendler, K. (2000) Single electron reducton of the oxidized state is coupled to proton uptake via the K pathway in Paracoccus denitrificans cytochrome c oxidase, Proc. Natl. Acad. Sci. U.S.A. 97, 4632-4636.
16. Verkhovsky, M. I., Tuukkanen, A., Backgren, C., Puustinen, A., and Wikström, M. (2001) Charge translocation coupled to electron injection into oxidized cytochrome c oxidase from Paracoccus denitrificans, Biochemistry 40, 7077-7083.
17. Giuffre, A., Barone, M. C., Brunori, M., D'Itri, E., Ludwig, B., Malatesta, F., Muller, H. W., and Sarti, P. (2002) Nitric oxide reacts with the single-electron reduced active site of cytochrome c oxidase, J. Biol. Chem. 277, 22402-22406.
18. Forte, E., Scandurra, F. M., Richter, O. M. H., D'Itri, E., Sarti, P., Brunori, M., Ludwig, B., and Giuffre, A. (2004) Proton uptake upon anaerobic reduction of the Paracoccus denitrificans cytochrome c oxidase: A kinetic investigation of the K354M and D124N mutants, Biochemistry 43, 2957-2963.
19. Bockris, J. O. M., and Reddy, A. K. N. (1973) Modem Electrochemistry, Vol. 1, Plenum, New York.
20. Kassner, R. J. (1973) A theoretical model for the effects of local nonpolar heme environments on the redox potentials in cytochromes, J. Am. Chem. Soc. 95, 2674-2676.
21. Warshel, A., and Russell, S. T. (1984) Calculations of electrostatic interactions in biological systems and in solutions, Q. Rev. Biophys. 17, 283-422.
22. Rashin, A. A., and Honig, B. (1985) Reevaluation of the Born model of ion hydration, J. Phys. Chem. 89, 5588-5593.
23. Kim, J., Mao, J., and Gunner, M. R. (2005) Are acidic and basic groups in buried proteins predicted to be ionized?, J. Mol. Biol. 348, 1283-1298.
24. Churg, A. K., and Warshel, A. (1986) Control of the redox potential of cytochrome c and microscopic dielectric effects in proteins, Biochemistry 25, 1675-1681.
25. Gunner, M. R., and Honig, B. (1991) Electrostatic control of midpoint potentials in the cytochrome subunit of the Rhodopseudomonas viridis reaction center, Proc. Natl. Acad. Sci. U.S.A. 88, 9151-9155.
26. Voigt, P., and Knapp, E. W. (2003) Tuning heme redox potentials in me cytochrome c subunit of photosynthetic reaction centers, J. Biol. Chem. 278, 51993-52001.
27. Mao, J., Hauser, K., and Gunner, M. R. (2003) How cytochrpmes with different folds control heme redox potentials, Biochemistry 42, 9829-9840.
28. Reedy, C. J., and Gibney, B. R. (2004) Heme protein assemblies, Chem. Rev. 104, 617-649.
29. Michel, H. (1998) The mechanism of proton pumping by cytochrome c oxidase, Proc. Natl. Acad. Sci. U.S.A. 95, 12819-12824.
30. Michel, H. (1999) Cytochrome c oxidase: catalytic cycle and mechanisms of proton pumping-a discussion, Biochemistry 38, 15129-15140.
31. Moody, A. J., and Rich, P. R. (1990) The effect of pH on redox titrations of heme a in cyanide liganded cytochrome c oxidase-Experimental and modeling studies, Biochim. Biophys. Acta 1015, 205-215.
32. 3-type quinol oxidase from Bacillus subtilis: an ENDOR and EXAFS study, Biochemistry 34, 10245-10255.
33. Kannt, A., Lancaster, C. R. D., and Michel, H. (1998) The coupling of electron transfer and proton translocation: electrostatic calculations on Paracoccus denitrificans, cytochrome c oxidase, Biophys. J. 74, 708-721.
34. Branden, M., Namslauer, A., Hansson, O., Aasa, R., and Brzezinski, P. (2003) Water-hydroxide exchange reactions at the catalytic site of heme-copper oxidases, Biochemistry 42, 13178-13184.
35. Puustinen, A., and Wikström, M. (1999) Proton exit from the heme-copper oxidase of Escherichia coli, Proc. Natl. Acad. Sci. U.S.A. 96, 35-37.
36. Mills, D. A., and Ferguson-Miller, S. (2002) Influence of structure, pH and membrane potential on proton movement in cytochrome oxidase, Biochim. Biophys. Acta 1555, 96-100.
37. Behr, J., Michel, H., Mantele, W., and Hellwig, P. (2000) Functional properties of the heme propionates in cytochrome c oxidase from Paracoccus denitrificans. Evidence from FTIR difference spectroscopy and site directed mutagenesis, Biochemistry 39, 1356-1363.
38. Wikström, M., Bogachev, A., Finel, M., Morgan, J. E., Puustinen, A., Raitio, M., Verkhovskaya, M., and Verkhovsky, M. I. (1994) Mechanism of proton translocation by the respiratory oxidases. The histidine cycle, Biochim. Biophys. Acta 1187, 106-111.
39. Popovic, D. M., and Stuchebrukhov, A. A. (2004) Electrostatic study of the proton pumping mechanism in bovine heart cytochrome c oxidase, J. Am. Chem. Soc. 126, 1858-1871.
40. a of CUB histidine ligand in cytochrome c oxidase, J. Phys. Chem. B 108, 18383-18389.
41. a values in cytochrome c oxidase, J. Phys. Chem. B 109, 3616-3626.
42. Popovic, D. M., and Stuchebrukhov, A. A. (2005) Proton exit channels in bovine cytochrome c oxidase, J. Phys. Chem. B 109, 1999-2006.
43. Blomberg, M., Siegbahn, P. E. M., Babcock, G., and Wikström, M. (2000) O-O bond splitting mechanism in cytochrome oxidase, J. Inorg. Biochem. 80, 261-269.
44. Siegbahn, P. E. (2003) The catalytic cycle of tyrosinase: peroxide attack on the phenolate ring followed by O-O cleavage, J. Biol. Inorg. Chem. 8, 567-576.
45. Siegbahn, P. E. M., Blomberg, M. R. A., and Blomberg, M. L. (2003) Theoretical study of the energetics of proton pumping and oxygen reduction in cytochrome oxidase, J. Phys. Chem. B 107, 10946-10955.
46. Xu, J., and Voth, G. A. (2005) Computer simulation of explicit proton translocation in cytochrome c oxidase: The D-pathway, Proc. Natl. Acad. Sci. U.S.A. 102, 6795-6800.
47. Pomes, R., Hummer, G., and Wikström, M. (1999) Structure and dynamics of a proton shuttle in cytochrome c oxidase, Biochim. Biophys. Acta 1365, 255-260.
48. Seibold, S. A., Mills, D. A., Ferguson-Miller, S., and Cukier, R. I. (2005) Water chain formation and possible proton pumping routes in Rhodobacter sphaeroides cytochrome c oxidase: A molecular dynamics comparison of the wild type and R481K mutant, Biochemistry 44, 10475-10485.
49. Cukier, R. I. (2005) A molecular dynamics study of water chain formation in the proton-conducting K channel of cytochrome c oxidase, Biochim. Biophys. Acta 1706, 134-146.
50. Alexov, E. G., and Gunner, M. R. (1997) Incorporating protein conformational flexibility into the calculation of pH-dependent protein properties, Biophys. J. 72, 2075-2093.
51. as in proteins, Biophys. J. 83, 1731-1748.
52. Zhu, Z., and Gunner, M. R. (2005) Energetics of quinone-dependent electron and proton transfers in Rhodobacter sphaeroides photosynthetic reaction centers, Biochemistry 44, 82-96.
53. as of hydroxyl ligands, Biochemistry 45, 7949-7958.
54. Gunner, M. R., Nicholls, A., and Honig, B. (1996) Electrostatic potentials in Rhodopseudomonas viridis reaction center: Implications for the driving force and directionality of electron transfer, J. Phys. Chem. 100, 4277-4291.
55. - to QB in bacterial photosynthetic reaction centers, Biochemistry 38, 8253-8270.
56. Song, Y., Mao, J., and Gunner, M. R. (2003) Calculation of proton transfers in bacteriorhodopsin bR and M intermediates, Biochemistry 42, 9875-9888.
57. Haas, A. H., and Lancaster, C. R. (2004) Calculated coupling of transmembrane electron and proton transfer in dihemic quinol: fumarate reductase, Biophys. J. 87, 4298-4315.
58. Mitchell, R., and Rich, P. R. (1994) Proton uptake by cytochrome c oxidase on reduction and on ligand binding, Biochim. Biophys. Acta 1186, 19-26.
59. B, Biochemistry 41, 13046-13052.
60. 3 contributions and assignment of vibrational modes, Biochemistry 38, 1685-1694.
61. Babcock, G. T., Vickery, L. E., and Palmer, G. (1978) The electronic state of heme in cytochrome oxidase II. Oxidation-reduction potential interactions and heme iron spin state behavior observed in reductive titrations, J. Biol. Chem. 253, 2400-2411.
62. Carithers, R. P., and Palmer, G. (1981) Characterization of the potentiometric behavior of soluble cytochrome oxidase by magnetic circular dichroism. Evidence in support of heme-heme interaction, J. Biol. Chem. 256, 7967-7976.
63. Verkhovsky, M. I., Belevich, N., Morgan, J. E., and Wikström, M. (1999) Proton linkage of cytochrome a oxidoreduction in carbon monoxide-treated cytochrome c oxidase, Biochim. Biophys. Acta 1412, 184-189.
64. Capitanio, N., Capitanio, G., Minuto, M., DeNitto, E., Palese, L. L., Nicholls, P., and Papa, S. (2000) Coupling of electron transfer with proton transfer at heme a and CUA redox Bohr effects in cytochrome c oxidase, Biochemistry 39, 6373-6379.
65. Svensson-Ek, M., Abramson, J., Larsson, G., Tornroth, S., Brzezinski, P., and Iwata, S. (2002) The X-ray crystal structures of wild-type and EQ(I-286) mutant cytochrome c oxidases from Rhodobacter sphaeroides, J. Mol. Biol. 321, 329-339.
66. Nicholls, A., and Honig, B. (1991) A rapid finite difference algorithm utilizing successive over-relaxation to solve the Poisson-Boltzmann equation, J. Comput. Chem. 12, 435-445.
67. Bharadwaj, R., Windemuth, A., Sridharan, S., Honig, B., and Nicholls, A. (1995) The fast multipole boundary element method for molecular electrostatics: An optimal approach for large systems, J. Comput. Chem. 16, 898-913.
68. Rocchia, W., Alexov, E., and Honig, B. (2001) Extending the applicability of the nonlinear Poisson-Boltzmann equation: multiple dielectric constants and multivalent ions, J. Phys. Chem. B 105, 6507-6514.
69. Sitkoff, D., Sharp, K. A., and Honig, B. (1994) Accurate calculation of hydration free energies using macroscopic solvent models, J. Phys. Chem. 98, 1978-1988.
70. Gilson, M. K., and Honig, B. (1988) Calculation of the total electrostatic energy of a macromolecular system: solvation energies, binding energies, and conformational analysis, Proteins: Struct., Funct., Genet. 4, 7-18.
71. Cornell, W. D., Cieplak, P., Bayly, C. I., Gould, I. R., Merz, K. M., Ferguson, D. M., Spellmeyer, D. C., Fox, T., Caldwell, J. W., and Kollman, P. A. (1995) A second generation force field for the simulation of proteins, nucleic acids, and organic molecules, J. Am. Chem. Soc. 117, 5179-5197.
72. Beroza, P., Fredkin, D. R., Okamura, M. Y., and Feher, G. (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. U.S.A. 88, 5804-5808.
73. Richarz, R., and Wüthrich, K. (1975) Carbon-13 NMR chemical shifts of the common amino acid residues measured in aqueous solutions of the linear tetrapeptides H-Gly-Gly-X-L-Ala-OH, Biopolymers 17, 2133-2141.
74. Matthew, J. B., Gurd, F. R. N., Garcia-Moreno, B., Flanagan, M. A., March, K. L., and Shire, S. J. (1985) pH-dependent processes in proteins, CRC Crit. Rev. Biochem. 18, 91-197.
75. McCauley, K. M., Vrtis, J. M., Dupont, J., and van der Donk, W. A. (2000) Insights into the functional role of the tyrosine-histidine linkage in cytochrome c oxidase, J. Am. Chem. Soc. 122, 2403-2404.
76. Frisch, M. J., Trucks, G. W., Schlegel, H. B., Scuseria, G. E., Robb, M. A., Cheeseman, J. R., Zakrzewski, V. G., Montgomery, J., Stratmann, R. E., Burant, J. C., Dapprich, S., Millam, J. M., Daniels, A. D., Kudin, K. N., Strain, M. C., Farkas, O., Tomasi, J., Barone, V., Cossi, M., Cammi, R., Mennucci, B., Pomelli, C., Adamo, C., Clifford, S., Ochterski, J., Petersson, G. A., Ayala, P. Y., Cui, Q., Morokuma, K., Malick, D. K., Rabuck, A. D., Raghavachari, K., Foresman, J. B., Cioslowski, J., Ortiz, J. V., Baboul, A. G., Stefanov, B. B., Liu, G., Liashenko, A., Piskorz, P., Komaromi, I., Gomperts, R., Martin, R. L., Fox, D. J., Keith, T., Al-Laham, M. A., Peng, C. Y., Nanayakkara, A., Challacombe, M., Gill, P. M. W., Johnson, B., Chen, W., Wong, M. W., Andres, J. L., Gonzalez, C., Head-Gordon, M., Replogle, E. S., and Pople, J. A. (1998) Gaussian 98, Revision A.9, Gaussian, Inc., Pittsburgh, PA.
77. Becke, A. D. (1993) Density-functional thermochemistry. 3. The role of exact exchange, J. Chem. Phys. 98, 5648-5652.
78. Hay, P. J., and Wadt, W. R. (1985) Ab initio effective core potentials for molecular calculations. Potentials for the transition metal atoms Sc to Hg, J. Chem. Phys. 82, 270-283.
79. Breneman, C. M., and Wiberg, K. B. (1990) Determining atom-centered monopoles from molecular electrostatic potentials-The need for high sampling density in formamide conformational-analysis, J. Comput. Chem. 11, 361-373.
80. Vanderkooi, G., and Stotz, E. (1965) Reductive alteration of heme a hemochromes, J. Biol. Chem. 240, 3418-3424.
81. Vanderkooi, G., and Stotz, E. (1966) Oxidation-reduction potentials of heme a hemochromes, J. Biol. Chem. 241, 3316-3323.
82. Battistuzzi, G., Borsari, M., Cowan, J. A., Ranieri, A., and Sola, M. (2002) Control of cytochrome c redox potential: axial ligation and protein environment effects, J. Am. Chem. Soc. 124, 5315-5324.
83. Wilson, G. S. (1974) Electrochemical studies of porphyrin redox reactions as cytochromes models, Bioelectrochem. Bioenerg. 1, 172-179.
84. Marques, H. M., Cukrowski, I., and Vashi, P. R. (2000) Coordination of weak field ligands by N-acetylmicroperoxidase-8 (NAcMP8), a ferric haempeptide from cytochrome c, and the influence of the axial ligand on the reduction potential of complexes of NAcMPS, J. Chem. Soc. 2000, 1335-1342.
85. Santucci, R., Reinhard, H., and Brunori, M. (1988) Direct electrochemistry of the undacapeptide from cytochrome c (microperoxidase) at a glassy carbon electrode, J. Am. Chem. Soc. 110, 8536-8357.
86. Munro, O. Q., and Marques, H. M. (1996) Heme-peptide models for hemoproteins. 1. Solution chemistry of N-acetylmicroperoxidase-8, Inorg. Chem. 35, 3752-3767.
87. IINAcMP8), J. Inorg. Biochem. 98, 1471-1482.
88. Anderegg, G., and Gramlich, V. (1994) Metal complexes of bivalent cobalt, nickel, copper, zinc, and cadmium with the tripodal ligand tris[2- (dimethylamino)ethyl]amine: their stabilities and the X-ray crystal structure of its copper(T1) complex sulfate, Helv. Chim. Acta 77, 685-690.
89. Thaler, F., Hubbard, C. D., Heinemann, F. W., Eldik, R. v., Schindler, S., Fabian, I., Dittler-Klingemann, A. M., Hahn, F. E., and Oryig, C. (1998) Structural, spectroscopic, thermodynamic and kinetic properties of copper(II) complexes with tripodal tetraamines, Inorg. Chem. 37, 4022-4029.
90. 3, Biochim. Biophys. Acta 1274, 109-111.
91. Sitter, A. J., Shifflett, J. R., and Terner, J. (1988) Resonance Raman spectroscopic evidence for heme iron-hydroxide ligation in peroxidase alkaline forms, J. Biol. Chem. 263, 13032-13038.
92. 2 concentration dependence, Biochemistry 35, 8580-8586.
93. MacMillan, F., Kannt, A., Behr, J., Prisner, T., and Michel, H. (1999) Direct evidence for a tyrosine radical in the reaction of cytochrome c oxidase with hydrogen peroxide, Biochemistry 38, 9179-9184.
94. Proshlyakov, D. A., Pressler, M. A., Demaso, C., Leykam, J. F., Dewitt, D. L., and Babcock, G. T. (2000) Oxygen activation and reduction in respiration involvement of redox-active tyrosine 244, Science 290, 1588-1591.
95. B, J. Am. Chem. Soc. 124, 11923-11935.
96. Cappuccio, J. A., Ayala, I., Elliott, G. I., Szundi, I., Lewis, J., Konopelski, J. P., Barry, B. A., and Einarsdottir, O. (2002) Modeling the active site of cytochrome oxidase: synthesis and characterization of a cross-linked histidine-phenol, J. Am. Chem. Soc. 124, 1750-1760.
97. Namslauer, A., Aagaard, A., Katsonouri, A., and Brzezinski, P. (2003) Intramolecular proton-transfer reactions in a membrane-bound proton pump: the effect of pH on the peroxy to ferryl transition in cytochrome c oxidase, Biochemistry 42, 1488-1498.
98. Wikström, M., Ribacka, C., Molin, M., Laakkonen, L., Verkhovsky, M., and Puustien, A. (2005) Gating of proton and water transfer in the respiratory enzyme cytochrome c oxidase, Proc. Natl. Acad. Sci. U.S.A. 102, 10478-10481.
99. You, T. J., and Bashford, D. (1995) Conformation and hydrogen ion titration of proteins: a continuum electrostatic model with conformational flexibility, Biophys. J. 69, 1721-1733.
100. a values of ionizable groups in bacteriorhodopsin, J. Mol. Biol. 224, 473-486.
101. Bashford, D., and Karplus, M. (1991) Multiple-site titration curves of proteins: An analysis of exact and approximate methods for their calculation, J. Phys. Chem. 95, 9556-9561.
102. Antosiewicz, J., McCammon, J. A., and Gilson, M. K. (1994) Prediction of pH-dependent properties of proteins, J. Mol. Biol. 238, 415-436.
103. as in proteins, Biochemistry 35, 7819-7833.
104. Quenneville, J., Popovic, D. M., and Stuchebrukhov, A. A. (2006) Combined DFT and electrostatics study of the proton pumping mechanism in cytochrome c oxidase, Biochim Biophys Acta (in press).
105. Honig, B. H., and Hubble, W. L. (1984) Stability of "salt bridges" in membrane proteins, Proc. Natl. Acad. Sci. U.S.A. 81, 5412-5416.
106. Mills, D. A., Florens, L., Hiser, C., Qian, J., and Ferguson-Miller, S. (2000) Where is "outside" in cytochrome c oxidase and how and when do protons get there?, Biochim. Biophys. Acta 1458, 180-187.
107. Branden, M., Sigurdson, H., Namslauer, A., Gennis, R. B., Adelroth, P., and Brzezinski, P. (2001) On the role of the K-proton-transfer pathway in cytochrome c oxidase, Proc. Natl. Acad. Sci. U.S.A. 98, 5013-5018.
108. Kannt, A., Pfitzner, U., Ruitenberg, M., Hellwig, P., Ludwig, B., Mantele, W., Fendler, K., and Michel, H. (1999) Mutation of Arg-54 strongly influences heme composition and rate and directionality of electron transfer in Paracoccus dinitrificans cytochrome c oxidase, J. Biol. Chem. 274, 37974-37981.
109. Mitchell, R., Mitchell, P., and Rich, P. R. (1992) Protonation states of the catalytic intermediates of cytochrome c oxidase, Biochim. Biophys. Acta 1101, 188-191.
110. Wikström, M., and Verkhovsky, M. I. (2002) Proton translocation by cytochrome c oxidase in different phases of the catalytic cycle, Biochim. Biophys. Acta 1555, 128-132.
111. Brzezinski, P., and Larsson, G. (2003) Redox-driven proton pumping by heme-copper oxidases, Biochim. Biophys. Acta 1605, 1-13.
112. Bloch, D., Belevich, I., Jasaitis, A., Ribacka, C., Puustinen, A., Verkhovsky, M. I., and Wikström, M. (2004) The catalytic cycle of cytochrome c oxidase is not the sum of its two halves, Proc. Natl. Acad. Sci. U.S.A. 101, 529-533.
113. Zhao, X., Yeung, N., Wang, Z., Guo, Z., and Lu, Y. (2005) Effects of metal ions in the CUB on the redox properties of heme in heme-copper oxidases: spectroelectrochemical studies of an engineered heme-copper center in myoglobin, Biochemistry 44, 1210-1214.
114. Olsson, M. H., Sharma, P. K., and Warshel, A. (2005) Simulating redox coupled proton transfer in cytochrome c oxidase: looking for the proton bottleneck, FEBS Lett. 579, 2026-2034.
115. Onufriev, A., Smondyrev, A., and Bashford, D. (2003) Proton affinity changes driving unidirectional proton transport in the bacteriorhodopsin photocycle, J. Mol. Biol. 332, 1183-1193.
116. Balashov, S. P. (2000) Protonation reactions and their coupling in bacteriorhodopsin, Biochim. Biophys. Acta 1460, 75-94.
117. Hofacker, I., and Schulten, K. (1998) Oxygen and proton pathways in cytochrome c oxidase, Proteins: Struct., Funct., Genet. 30, 100-107.