Steps of the coupled charge translocation in the catalytic cycle of cytochrome c oxidase

Frontiers in Bioscience

Volumn 18, Issue 1, 2013, Pages 36-57

  Siletsky, Sergey A ^a  

^a MOSCOW STATE UNIVERSITY   (Russian Federation)

Author keywords

Channels; Cytochrome; Electrogenic; Electron injection; Membrane potential; Oxidase; Protons; Review; Voltage

Indexed keywords

CYTOCHROME C OXIDASE; PROTON; PROTON PUMP;

ANIMAL; CATALYSIS; CHEMICAL STRUCTURE; ELECTRON; METABOLISM; OXIDATION REDUCTION REACTION; REVIEW;

ANIMALS; CATALYSIS; ELECTRON TRANSPORT COMPLEX IV; ELECTRONS; MODELS, MOLECULAR; OXIDATION-REDUCTION; PROTON PUMPS; PROTONS;

MLCS; MLOWN;

EID: 84878796508     PISSN: 27686701     EISSN: 27686698     Source Type: Journal    
DOI: 10.2741/4086     Document Type: Review

References (174)

1. Anraku, Y.: Bacterial electron transport chains. Ann Rev Biochem, 57, 101-132 (1988)
2. Garcia-Horsman, J. A., B. Barquera, J. Rumbley, J. Ma & R. B. Gennis: The superfamily of heme-copper respiratory oxidases. J Bacteriol, 176, 5587-5600 (1994)
3. Ferguson-Miller, S. & G. T. Babcock: Heme/copper terminal oxidases. Chem Rev, 7, 2889-2907 (1996)
4. Belevich, I. & M. I. Verkhovsky: Molecular mechanism of proton translocation by cytochrome c oxidase. Antioxidants and Redox Signaling, 10, 1-29 (2008)
5. Pereira, M. M., M. Santana & M. Teixeira: A novel scenario for the evolution of haem-copper oxygen reductases. Biochim Biophys Acta, 1505, 185-208 (2001)
6. Brzezinski, P. & R. B. Gennis: Cytochrome c oxidase: exciting progress and remaining mysteries. J Bioenerg Biomembr, 40, 521-531 (2008)
7. Brzezinski, P. & A. L. Johansson: Variable proton-pumping stoichiometry in structural variants of cytochrome c oxidase. Biochim Biophys Acta, 1797, 710-23 (2010)
8. Hosler, J. P., S. Ferguson-Miller & D. A. Mills: Energy transduction: proton transfer through the respiratory complexes. Annu Rev Biochem, 75, 165-187 (2006)
9. Yoshikawa, S., K. Muramoto & K. Shinzawa-Itoh: Proton-pumping mechanism of cytochrome c oxidase. Annu Rev Biophys, 40, 205-23 (2011)
10. Rich, P. R. & A. Marechal: The mitochondrial respiratory chain. Essays Biochem, 47, 1-23 (2010)
11. Wikstrom, M. & M. I. Verkhovsky: Mechanism and energetics of proton translocation by the respiratory hemecopper oxidases. Biochim Biophys Acta, 1767, 1200-1214 (2007)
12. Zimmermann, B. H., C. I. Nitsche, J. A. Fee, F. Rusnak & E. Munck: Properties of a copper-containing cytochrome ba3: a second terminal oxidase from the extreme thermophile Thermus Thermophilus. Proc Natl Acad Sci USA, 85, 5779-5783 (1988)
13. Soulimane, T., G. Buse, G. B. Bourenkov, H. D. Bartunik, R. Huber & M. E. Than: Structure and mechanism of the aberrant ba3-cytochrome c oxidase from Thermus thermophilus . EMBO J, 19, 1766-1776 (2000)
14. Chang, H. Y., J. Hemp, Y. Chen, J. A. Fee & R. B. Gennis: The cytochrome ba3 oxygen reductase from Thermus thermophilus uses a single input channel for proton delivery to the active site and for proton pumping. Proc Natl Acad Sci U S A, 106, 16169-73 (2009)
15. Pitcher, R. S. & N. J. Watmough: The bacterial cytochrome cbb3 oxidases. Biochim Biophys Acta, 1655, 388-99 (2004)
16. Rauhamaki, V., D. A. Bloch, M. I. Verkhovsky & M. Wikstrom: Active site of cytochrome cbb3. J. Biol. Chem., 284, 11301-11308 (2009)
17. Buschmann, S., E. Warkentin, H. Xie, J. D. Langer, U. Ermler & H. Michel: The structure of cbb3 cytochrome oxidase provides insights into proton pumping. Science, 329, 327-30 (2010)
18. Hemp, J. & R. B. Gennis: Diversity of the heme-copper superfamily in archaea: insights from genomics and structural modeling. Results Probl Cell Differ, 45, 1-31 (2008)
19. Mitchell, P.: Chemiosmotic coupling and energy transduction. Glynn Research Ltd., Bodmin (1968)
20. Wikstrom, M.: Proton pump coupled to cytochrome c oxidase in mitochondria. Nature, 266, 271-273 (1977)
21. Wikstrom, M.: Cytochrome c oxidase: 25 years of the elusive proton pump. Biochim Biophys Acta, 1655, 241-247 (2004)
22. Tsukihara, T., H. Aoyama, E. Yamashita, T. Takashi, H. Yamaguichi, K. Shinzawa-Itoh, R. Nakashima, R. Yaono & S. Yoshikawa: The whole structure of the 13-subunit oxidized cytochrome c oxidase at 2.8 A. Science, 272, 1136-1144 (1996)
23. Yoshikawa, S., K. Shinzawa-Itoh, R. Nakashima, R. Yaono, N. Inoue, M. Yao, M. J. Fei, C. P. Libeu, T. Mizushima, H. Yamaguchi, T. Tomizaki & T. Tsukihara: Redox-coupled crystal structural changes in bovine heart cytochrome c oxidase. Science, 280, 1723-1729 (1998)
24. Tsukihara, T., K. Shimokata, Y. Katayama, H. Shimada, K. Muramoto, H. Aoyama, M. Mochizuki, K. Shinzawa-Itoh, E. Yamashita, M. Yao, Y. Ishimura & S. Yoshikawa: The low-spin heme of cytochrome c oxidase as the driving element of the proton-pumping process. Proc Natl Acad Sci USA, 100, 15304-15309 (2003)
25. Muramoto, K., K. Hirata, K. Shinzawa-Itoh, S. Yoko-o, E. Yamashita, H. Aoyama, T. Tsukihara & S. Yoshikawa: A histidine residue acting as a controlling site for dioxygen reduction and proton pumping by cytochrome c oxidase. Proc Natl Acad Sci USA, 104, 7881-7886 (2007)
26. Iwata, S., C. Ostermeier, B. Ludwig & H. Michel: Structure at 2.8 A resolution of cytochrome c oxidase from Paracoccus denitrificans . Nature, 376, 660-669 (1995)
27. Ostermeier, C., S. Iwata, B. Ludwig & H. Michel: FV fragment-mediated crystallization of the membrane protein bacterial cytochrome c oxidase. Nat Struct Biol, 2, 842 (1995)
28. Koepke, J., E. Olkhova, H. Angerer, H. Muller, G. Peng & H. Michel: High resolution crystal structure of Paracoccus denitrificans cytochrome c oxidase: New insights into the active site and the proton transfer pathways. Biochim Biophys Acta, 1787, 635-645 (2009)
29. Svensson-Ek, M., J. Abramson, G. Larsson, S. Tornroth, P. Brzezinski & S. Iwata: 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 (2002)
30. Qin, L., J. Liu, D. A. Mills, D. A. Proshlyakov, C. Hiser & S. Ferguson-Miller: Redox dependent conformational changes in cytochrome c oxidase suggest a gating mechanism for proton uptake. BIochemistry, 48, 5121-5130 (2009)
31. Abramson, J., S. Riistama, G. Larsson, A. Jasaitis, M. Svensson-Ek, L. Laakkonen, A. Puuustinen, S. Iwata & Wikstrom: The structure of the ubiquinol oxidase from Escherichia coli and its ubiquinone binding site. Nat Struct Biol, 7, 910-917 (2000)
32. Luna, V. M., Y. Chen, J. A. Fee & C. D. Stout: Crystallographic studies of Xe and Kr binding within the large internal cavity of cytochrome ba 3 from Thermus thermophilus : Structural analysis and role of oxygen transport channels in the heme-Cu oxidases. Biochemistry, 47, 4657-4665 (2008)
33. Pilet, E., A. Jasaitis, U. Liebl & M. H. Vos: Electron transfer between hemes in mammalian cytochrome c oxidase. Proc Natl Acad Sci USA, 101, 16196-16203 (2004)
34. Buse, G., T. Soulimane, M. Dewor, H. E. Meyer & M. Bloggel: Evidence for a copper coordinated histidine-tyrosine crosslink in the active site of cytochrome oxidase. Protein Sci, 8, 985-990 (1999)
35. Rauhamaki, V., M. Baumann, R. Soliymani, A. Puustinen & M. Wikstrom: Identification of histidin-tyrosin cross-link in the active site of the cbb3-type cytochrome c oxidase from Rhodobacter sphaeroides. Proc Natl Acad Sci U S A, 103, 16135-16140 (2006)
36. Babcock, G. T.: How oxygen is activated and reduced in respiration. Proc Natl Acad Sci USA, 96, 12971-12973 (1999)
37. Proshlyakov, D. A., M. A. Pressler, C. DeMaso, J. F. Leykam, D. L. DeWitt & G. L. Babcock: Oxygen activation and reduction in respiration: involvement of redox-active tyrosine 244. Science, 290, 1588-1591 (2000)
38. Gennis, R. B.: Coupled proton and electron transfer reactions in cytochrome oxidase. Front Biosci, 9, 581-91 (2004)
39. Mills, D. A. & J. P. Hosler: Slow proton transfer through the pathways for pumped protons in cytochrome c oxidase induces suicide inactivation of the enzyme. Biochemistry, 44, 4556-4666 (2005)
40. Fetter, J. R., J. Qian, J. Shapleigh, J. W. Thomas, A. Garcia-Horsman, E. Schmidt, J. Hosler, G. T. Babcock, R. B. Gennis & S. Ferguson-Miller: Possible proton relay pathways in cytochrome c oxidase. Proc Natl Acad Sci USA, 92, 1604-1608 (1995)
41. Konstantinov, A. A., S. Siletsky, D. Mitchell, A. Kaulen & R. B. Gennis: 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 USA, 94, 9085-9090 (1997)
42. Gennis, R. B.: Multiple proton-conducting pathways in cytochrome oxidase and a proposed role for the active-site tyrosine. Biochim Biophys Acta, 1365, 241-248 (1998)
43. Qin, L., C. Hiser, A. Mulichak, R. M. Garavito & S. Ferguson-Miller: Identification of conserved lipid/detergent-binding sites in a high-resolution structure of the membrane protein cytochrome c oxidase. Proc Natl Acad Sci U S A, 103, 16117-16122 (2006)
44. Branden, M., F. Tomson, R. B. Gennis & P. Brzezinski: The entry point of the K-proton-transfer pathway in cytochrome c oxidase. Biochemistry, 41, 10794-10798 (2002)
45. Hofacker, I. & K. Schulten: Oxygen and proton pathways in cytochrome c oxidase. Proteins, 30, 100-107 (1998)
46. Shimokata, K., Y. Katayama, H. Murayama, M. Suematsu, T. Tsukihara, K. Muramoto, H. Aoyama, S. Yoshikawa & H. Shimada: The proton pumping pathway of bovine heart cytochrome c oxidase. Proc Natl Acad Sci U S A, 104, 4200-4205 (2007)
47. Pfitzner, U., A. Odenwald, O. T., L. Weingard, B. Ludwig & O. M. Richter: Cytochrome c oxidase (heme aa3) from Paracoccus denitrificans: analysis of mutations in putative proton channels of subunit I. J Bioenerg Biomembr, 30, 89-97 (1998)
48. Lee, H.M., T. K. Das, D. L. Rousseau, D. Mills, S. Fergusson-Miller & R. Gennis: Mutations in the putative H-channel in the cytochrome c oxidase from Rhodobacter sphaeroides show that this channel is not important for proton conduction but reveals modulation of the properties of heme a. Biochemistry, 39, 2989-2996 (2000)
49. Wikstrom, M., M. I. Verkhovsky & G. Hummer: Water-gated mechanism of proton translocation by cytochrome c oxidase. Biochim Biophys Acta, 45238, 1-5 (2003)
50. Cukier, R. I.: Quantum molecular dynamics simulation of proton transfer in cytochrome c oxidase. Biochim Biophys Acta, 1656, 189-202 (2004)
51. Tashiro, M. & A. A. Stuchebrukhov: Thermodynamic properties of internal water molecules in the hydrophobic cavity around the catalytic center of cytochrome c oxidase. J Phys Chem B, 109, 1015-22 (2005)
52. Zheng, X., D. M. Medvedev, J. Swanson & A. A. Stuchebrukhov: Computer simulation of water in cytochrome c oxidase. Biochim Biophys Acta, 1557, 99-107 (2003)
53. Michel, H.: Cytochrome c oxidase: catalytic cycle and mechanisms of proton pumping - a discussion. Biochemistry, 38, 15129-40 (1999)
54. Popovic, D. M. & A. A. Stuchebryukhov: Proton pumping mechanism and catalytic cycle of cytochrome c oxidase: Coulomb pump model with kinetic gating. FEBS Lett., 566, 126-130 (2004)
55. Sugitani, R., E. S. Medvedev & A. A. Stuchebrukhov: Theoretical and computational analysis of the membrane potential generated by cytochrome c oxidase upon single electron injection into the enzyme. Biochim Biophys Acta, 1777, 1129-39 (2008)
56. Kaila, V. R., V. Sharma & M. Wikstrom: The identity of the transient proton loading site of the proton-pumping mechanism of cytochrome c oxidase. Biochim Biophys Acta, 1807, 80-4 (2011)
57. Popovic, D. M. & A. A. Stuchebrukhov: Proton exit channels in bovine cytochrome c oxidase. J Phys Chem B, 109, 1999-2006 (2005)
58. Riistama, S., A. Puustinen, M. I. Verkhovsky, J. E. Morgan & M. Wikstrom: Binding of O2 and its reduction are both retarded by replacement of valine 279 by isoleucine in cytochrome c oxidase from Paracoccus denitrificans. Biochemistry, 39, 6365-72 (2000)
59. Salomonsson, L., A. Lee, R. B. Gennis & P. Brzezinski: A single-amino-acid lid renders a gas-tight compartment within a membrane-bound transporter. Proc Natl Acad Sci U S A, 101, 11617-21 (2004)
60. Sugitani, R. & A. A. Stuchebrukhov: Molecular dynamics simulation of water in cytochrome c oxidase reveals two water exit pathways and the mechanism of transport. Biochim Biophys Acta, 1787, 1140-1150 (2009)
61. Schmidt, B., J. McCracken & S. Ferguson-Miller: A discrete water exit pathway in the membrane protein cytochrome c oxidase. Proc Natl Acad Sci USA, 100, 15539-15542 (2003)
62. 2) in the reaction of mixed-valence cytochrome c oxidase with oxygen at room temperature. Biochem J, 215, 659-67 (1983)
63. 2 reduction with minimization of reactive oxygens and provide a proton-pumping gate. Proc Natl Acad Sci U S A, 107, 7740-5 (2010)
64. Kitagawa, T. & T. Ogura: Oxygen activation mechanism at the binuclear site of heme-copper oxidase superfamily as revealed by time-resolved resonance Raman spectroscopy. In: Progress in Inorganic Chemistry. Ed: K. D. Karlin. Wiley&Sons, Inc., (1997)
65. 4+=0 stretching Raman band for cytochrome oxidase compound B at ambient temperature. J Biol Chem, 265, 14721-14723 (1990)
66. Wiertz, F. G. M., O.M. H. Richter, A. V. Cherepanov, F. MacMillan, B. Ludwig & S. de Vries: An oxo-ferryl tryptophan radical catalytic intermediate in cytochrome c and quinol oxidases trapped by microsecond freeze-hyperquenching (MNQ) FEBS Lett, 575, 127-130 (2004)
67. Siegbahn, P. & M. R. A. Blomberg: Important roles of tyrosines in Photosystem II and cytochrome oxidase. Biochim Biophys Acta, 1655, 45-50 (2004)
68. MacMillan, F., K. Budiman, H. Angerer & H. Michel: The role of triptophan 272 in the Paracoccus denitrificans cytochrome c oxidase. FEBS Lett, 580, 1345-1349 (2006)
69. Wiertz, F. G. M., O.-M. H. Richter, B. Ludwig & S. de Vries: Kinetic resolution of a tryptophan-radical intermediate in the reaction cycle of Paracoccus denitrificans cytochrome c oxidase J Biol Chem, 282, 31580-31591 (2007)
70. Gorbikova, E. A., I. Belevich, M. Wikstrom & M. I. Verkhovsky: The proton donor for O-O bond scission by cytochrome c oxidase. Proc Natl Acad Sci USA, 105, 10733-10737 (2008)
71. Oliveberg, M., P. Brzezinski & B. G. Malmstrom: The effect of pH and temperature on the reaction of fully reduced and mixed-valence cytochrome c oxidase with dioxygen. Biochem Biophys Acta, 977, 322-328 (1989)
72. Verkhovsky, M. I., J. E. Morgan & M. Wikstrom: Oxygen binding and activation: early steps in the reaction of oxygen with cytochrome c oxidase. Biochemistry, 33, 3079-3086 (1994)
73. Siletsky, S. A., D. Han, S. Brand, J. E. Morgan, M. Fabian, L. Geren, F. Millett, B. Durham, A. A. Konstantinov & R. B. Gennis: Single-electron photoreduction of the PM intermediate of cytochrome c oxidase. Biochim Biophys Acta, 1757, 1122-1132 (2006)
74. Bloch, D., I. Belevich, A. Jasaitis, C. Ribacka, A. Puustinen, M. I. Verkhovsky & M. Wikstrom: The catalytic cycle of cytochrome c oxidase is not the sum of its two halves. Proc Natl Acad Sci USA, 101, 529-533 (2004)
75. Belevich, I., D. A. Bloch, M. Wikstrom & M. I. Verkhovsky: Exploring the proton pump mechanism of cytochrome c oxidase in real time. Proc Natl Acad Sci U S A, 104, 2685-2690 (2007)
76. H state of detergent-solubilized cytochrome oxidase. Biochemistry, 46, 14610-14618 (2007)
77. H transition of the aberrant ba3 oxidase from Thermus thermophilus . Biochim Biophys Acta, 1787, 201-5 (2009)
78. H state. Biochim Biophys Acta, 1807, 1162-1169 (2011)
79. Siletsky, S., A. D. Kaulen & A. A. Konstantinov: Resolution of electrogenic steps coupled to conversion of cytochrome c oxidase from the peroxy to the ferryl-oxo state. Biochemistry, 38, 4853-4861 (1999)
80. Verkhovsky, M. I., A. Tuukkanen, C. Backgren, A. Puustinen & M. Wikstrom: Charge translocation coupled to electron injection into oxidized cytochrome c oxidase from Paracoccus denitrificans. Biochemistry, 40, 7077-7083 (2001)
81. Jancura, D., V. Berka, M. Antalik, J. Bagelova, R. B. Gennis, G. Palmer & M. Fabian: Spectral and kinetic equivalence of oxidized cytochrome c oxidase as isolated and "activated" by reoxidation. J Biol Chem, 281, 30319-30325 (2006)
82. Gibson, Q. H. & C. Greenwood: Reactions of cytochrome oxidase with oxygen and carbon monoxide. Biochem J, 86, 541-554 (1963)
83. Blackmore, R. S., C. Greenwood & Q. H. Gibson: Studies of the primary oxygen intermediate in the reaction of fully reduced cytochrome oxidase. J Biol Chem, 266, 19245-19249 (1991)
84. Winkler, J. R., D. G. Nocera, K. M. Yocom, E. Bordignon & H. B. Gray: Electron-transfer kinetics of pentaammineruthenium(III)(histidine-33)- ferricytochrome c. Measurement of the rate of intramolecular electron transfer between redox centers separated by 15 A in a protein. J Am Chem Soc, 104, 5798-5800 (1982)
85. Pan, L. P., M. Frame, B. Durham, D. Davis & F. Millett: Photoinduced electron transfer within complexes between plastocyanin and ruthenium bisbipyridine dicarboxybipyridine cytochrome c derivatives. Biochemistry, 29, 3231-3236 (1990)
86. Pan, L. P., S. Hibdon, R.-Q. Liu, B. Durham & F. Millett: Intracomplex Electron Transfer Between Ruthenium-Cytochrome c Derivatives and Cytochrome c Oxidase. Biochemistry, 32, 8492-8498 (1993)
87. Nilsson, T.: Photoinduced electron transfer from tris(2,2'-bipyridyl) ruthenium to cytochrome c oxidase. Proc Natl Acad Sci USA, 89, 6497-6501 (1992)
88. Millett, F. & B. Durham: Photoinduced electron transfer reactions in metalloprotein complexes labeled with ruthenium polypyridine. In: Metal Ions in Biological Systems. Eds: H. Sigel&A. Siegel. Marcel Dekker, Inc., Basel, Switzerland (1991)
89. Geren, L., B. Durham & F. Millett: Use of ruthenium photoreduction techniques to study electron transfer in cytochrome oxidase. Methods Enzymol, 456, 507-520 (2009)
90. Kobayashi, K., H. Une & K. Hayashi: Electron transfer process in cytochrome oxidase after pulse radiolysis. J Biol Chem, 246, 7976-7980 (1989)
91. Farver, O., Y. Chen, J. A. Fee & I. Pecht: Electron transfer among the CuA-, heme b- and a3- centers of Thermus thermophilus cytochrome ba 3. FEBS Lett, 580, 3417-3421 (2006)
92. Drachev, L. A., A. A. Jasaitis, A. D. Kaulen, A. A. Kondrashin, E. A. Liberman, I. B. Nemecek, S. A. Ostroumov, A. Semenov & V. P. Skulachev: Direct measurement of electric current generation by cytochrome oxidase, H+-ATPase and bacteriorhodopsin. Nature, 249, 321-4 (1974)
93. Drachev, L. A., A. D. Kaulen, A. Y. Semenov, I. I. Severina & V. P. Skulachev: Lipid-impregnated filters as a tool for studying the electric current-generating proteins. Anal Biochem, 96, 250-262 (1979)
94. Zaslavsky, D., A. Kaulen, I. A. Smirnova, T. V. Vygodina & A. A. Konstantinov: Flash-induced membrane potential generation by cytochrome c oxidase. FEBS Lett, 336, 389-393 (1993)
95. Verkhovsky, M. I., J. E. Morgan, M. Verkhovskaya & M. Wikstrom: Translocation of electrical charge during a single turnover of cytochrome c oxidase. Biochim Biophys Acta, 1318, 6-10 (1997)
96. Zaslavsky, D. L., I. A. Smirnova, S. A. Siletsky, A. D. Kaulen, F. Millett & A. A. Konstantinov: Rapid kinetics of membrane potential generation by cytochrome c oxidase with the photoactive Ru(II)-tris-bipyridyl derivative of cytochrome c as electron donor. FEBS Lett, 359, 27-30 (1995)
97. Siletsky, S. A., A. D. Kaulen & A. A. Konstantinov: Electrogenic events associated with peroxy- to ferryl-oxo state transition in cytochrome c oxidase. Eur J Biophys, 26, 98 (1997)
98. Siletsky, S. A., A. D. Kaulen, D. Mitchell, R. B. Gennis & A. A. Konstantinov: Resolution of two proton conduction pathways in cytochrome c oxidase. EBEC Short Reports, 9, 90 (1996)
99. Siletsky, S. A., A. S. Pawate, K. Weiss, R. B. Gennis & A. A. Konstantinov: Transmembrane charge separation during the ferryl-oxo-> oxidized transition in a non-pumping mutant of cytochrome c oxidase. J Biol Chem, 279, 52558-52565 (2004)
100. Siletsky, S. A., J. Zhu, R. B. Gennis & A. A. Konstantinov: Partial steps of charge translocation in the nonpumping N139L mutant of Rhodobacter sphaeroides cytochrome c oxidase with a blocked D-channel. Biochemistry, 49, 3060-73 (2010)
101. Ruitenberg, M., A. Kannt, E. Bamberg, B. Ludwig, H. Michel & K. Fendler: Single-electron reduction of the oxidized state is coupled to proton uptake via the K pathway in Paracoccus denitrificans cytochrome c oxidase. Proc Natl Acad Sci USA, 97, 4632-4636 (2000)
102. Ruitenberg, M., A. Kannt, E. Bamberg, K. Fendler & H. Michel: Reduction of cytochrome c oxidase by a second electron leads to proton translocation. Nature, 417, 99-102 (2002)
103. Jasaitis, A., M. I. Verkhovsky, J. E. Morgan, M. L. Verkhovskaya & M. Wikstrom: Assignment and charge translocation stoichiometries of the electrogenic phases in the reaction of cytochrome c with dioxygen. Biochemistry, 38, 2697-2706 (1999)
104. Ribacka, C., M. I. Verkhovsky, I. Belevich, D. A. Bloch, A. Puustinen & M. Wikstrom: An elementary reaction step of the proton pump is revealed by mutation of tryptophan-164 to phenylalanine in cytochrome c oxidase from Paracoccus denitrificans. Biochemistry, 44, 16502-16512 (2005)
105. Lepp, H. & P. Brzezinski: Internal charge transfer in cytochrome c oxidase at a limited proton supply: Proton pumping ceases at high pH. Biochim Biophys Acta, 1790, 552-557 (2009)
106. Chance, B., C. Saronio & J. S. Leigh, Jr.: Functional intermediates in the reaction of membrane-bound cytochrome oxidase with oxygen. J Biol Chem, 250, 9226-9237 (1975)
107. Han, S., Y.-C. Ching & D. L. Rousseau: Primary intermediate in the reaction of oxygen with fully reduced cytochrome c oxidase. Proc Natl Acad Sci USA, 87, 2491-2495 (1990)
108. 3 in the mixed valence cytochome oxidase/dioxygen reaction. J Biol Chem, 265, 11131-11136 (1990)
109. Woodruff, W. H.: Coordination dynamics of hemecopper oxidases. The ligand shuttle and the control and coupling of electron transfer and proton translocation. J Bioenerg Biomembr, 25, 177-188 (1993)
110. Belevich, I., A. Tuukkanen, M. Wikstrom & M. I. Verkhovsky: Proton-coupled electron equilibrium in soluble and membrane-bound cytochrome c oxidase from Paracoccus denitrificans . BIochemistry, 45, 4000-4006 (2006)
111. Belevich, I., M. I. Verkhovsky & M. Wikstrom: Proton-coupled electron transfer drives the proton pump of cytochrome c oxidase. Nature, 440|, 829-832 (2006)
112. Popovic, D. M. & A. A. Stuchebrukhov: Electrostatic study of the proton pumping mechanism in bovine heart cytochrome c oxidase. J Am Chem Soc, 126, 1858-71 (2004)
113. Lepp, H., E. Svahn, K. Faxen & P. Brzezinski: Charge transfer in the K proton pathway linked to electron transfer to the catalytic site in cytochrome c oxidase. Biochemistry, 47, 4929-4935 (2008)
114. Gorbikova, E. A., M. Wikstrom & M. I. Verkhovsky: The protonation state of the cross-linked tyrosine during the catalytic cycle of cytochrome c oxidase. J Biol Chem., 283, 34907-34912 (2008)
115. 3 oxidase from Thermus thermophilus. Biochim Biophys Acta, 1767, 1383-92 (2007)
116. Jasaitis, A., C. Backgren, J. E. Morgan, A. Puustinen, M. I. Verkhovsky & M. Wikstrom: Electron and proton transfer in the arginine-54-methionine mutant of cytochrome c oxidase from Paracoccus denitrificans . Biochemistry, 40, 5269-5274 (2001)
117. Belevich, I., E. Gorbikova, N. P. Belevich, V. Rauhamaki, M. Wikstrom & M. I. Verkhovsky: Initiation of the proton pump of cytochrome c oxidase. Proc Natl Acad Sci U S A, 107, 18469-74 (2010)
118. Hinkle, P. & P. Mitchell: Effect of membrane potential on the redox poise between cytochrome a and cytochrome c in rat liver mitochondria. J Bioenerg 1, 45-60 (1970)
119. Tsukihara, T., H. Aoyama, E. Yamashita, T. Tomizaki, H. Yamaguchi, K. Shinzawa-Itoh, T. Nakashima, R. Yaono & S. Yoshikawa: Structures of metal sites of oxidized bovine heart cytochrome c oxidase at 2.8 A. Science, 269, 1069-1074 (1995)
120. Verkhovsky, M. I., A. Jasaitis, M. L. Verkhovskaya, L. Morgan & M. Wikstrom: Proton translocation by cytochrome c oxidase. Nature, 400, 480-483 (1999)
121. Faxen, K., G. Gilderson, P. Adelroth & P. Brzezinski: A mechanistic principle for proton pumping by cytochrome c oxidase. Nature, 437, 286-289 (2005)
122. M intermediate of cytochrome c oxidase. Biochim Biophys Acta, 1757, 1122-32 (2006)
123. Kaila, V. R., M. I. Verkhovsky & M. Wikstrom: Proton-coupled electron transfer in cytochrome oxidase. Chem Rev, 110, 7062-81 (2010)
124. Smirnova, I., P. Adelroth, R. B. Gennis & P. Brzezinski: Aspartate-132 in cytochrome c oxidase from Rhodobacter sphaeroides is involved in a two-step proton transfer during oxo-ferryl formation. Biochemistry, 38, 6826-6833 (1999)
125. Namslauer, A., A. Pawate, R. Gennis & P. Brzezinski: Redox-coupled proton translocation in biological systems: Proton shuttling in cytochrome c oxidase. Proc Natl Acad Sci USA, 100, 15543-15547 (2003)
126. Gorbikova, E. A., N. P. Belevich, M. Wikstrom & M. I. Verkhovsky: Time-resolved ATR-FTIR spectroscopy of the oxygen reaction in the D124N mutant of cytochrome c oxidase from Paracoccus denitrificans . Biochemistry, 46, 13141-13148 (2007)
127. Branden, G., R. B. Gennis & P. Brzezinski: Transmembrane proton translocation by cytochrome c oxidase. Biochim Biophys Acta, 1757, 1052-1063 (2006)
128. Zaslavsky, D., R. C. Sadoski, K. Wang, B. Durham, R. B. Gennis & F. Millett: Single electron reduction of cytochrome c oxidase compound F: resolution of partial steps by transient spectroscopy. Biochemistry, 37, 14910-14916 (1998)
129. Weng, L. & G. M. Baker: Reaction of hydrogen peroxide with the rapid form of resting cytochrome oxidase. Biochemistry, 30, 5727-5733 (1991)
130. Siletsky, S., D. Zaslavsky, I. Smirnova, A. Kaulen & A. Konstantinov: F-to-O transition of cytochrome c oxidase: pH and temperature effects on kinetics of charge translocation Biochem Soc Trans, 28, A457 (2000)
131. 3-cytochrome c oxidase from Thermus thermophilus: comparison of A- and B-type enzymes. Biochemistry, in press, (2010)
132. Laidler, K. J.: Unconvenitonal applications of the Arrhenius Law J Chem Educ 49, 343-344 (1972)
133. Moser, C. C., C. C. Page & P. L. Dutton: Darwin at the molecular scale: selection and variance in electron tunnelling proteins including cytochrome c oxidase. Philos Trans R Soc Lond B Biol Sci, 361, 1295-1305 (2006)
134. Tittor, J., C. Soell, D. Oesterhelt, H. J. Butt & E. Bamberg: A defective proton pump, point-mutated bacteriorhodopsin Asp96-Asn is fully reactivated by azide. EMBO J, 8, 3477-3482 (1989)
135. B-transition. FEBS Lett, 412, 490-494 (1997)
136. Decoursey, T. E.: Voltage-gated proton channels and other proton transfer pathways. Physiol Rev, 83, 475-579 (2003)
137. Mamedov, M. D., A. A. Tyunyatkina, S. A. Siletsky & A. Y. Semenov: Voltage changes involving photosystem II quinone-iron complex turnover. Eur Biophys J, 35, 647-654 (2006)
138. Kozlova, M. A., H. D. Juhnke, D. A. Cherepanov, C. R. Lancaster & A. Y. Mulkidjanian: Proton transfer in the photosynthetic reaction center of Blastochloris viridis. FEBS Lett, 582, 238-242 (2008)
139. -state of bacterial photosynthetic reaction centers: rate limitation within the protein. Biophys J, 73, 367-381 (1997)
140. Kuznetsova, S. S., N. V. Azarkina, T. V. Vygodina, S. A. Siletsky & A. A. Konstantinov: Zinc ions as cytochrome c oxidase inhibitors: two sites of action. Biochemistry (Mosc), 70, 128-136 (2005)
141. 2+. Proc Natl Acad Sci U S A, 96, 6183-6188 (1999)
142. 1 complex by blocking a protonatable group. J Biol Chem, 270, 25001-25006 (1995)
143. 2+ binding to the cytoplasmic side of Paracoccus denitrificans cytochrome c oxidase selectively uncouples electron transfer and proton translocation. FEBS Lett, 503, 142-146 (2001)
144. Aagaard, A., A. Namslauer & P. Brzezinski: Inhibition of proton transfer in cytochrome c oxidase by zinc ions: delayed proton uptake during oxygen reduction. Biochim Biophys Acta, 1555, 133-139 (2002)
145. Siletsky, S. A., A. D. Kaulen & A. A. Konstantinov: Electrogenic events associated with peroxy-to-ferryl-oxo state transition in cytochrome c oxidase. Eur J Biophys, 26, 98 (1997)
146. Verkhovsky, M. I., I. Belevich, D. A. Bloch & M. Wikstrom: Elementary steps of proton translocation in the catalytic cycle of cytochrome oxidase. Biochim Biophys Acta, 1757, 401-407 (2006)
147. Medvedev, D. M., E. S. Medvedev, A. I. Kotelnikov & A. A. Stuchebrukhov: Analysis of the kinetics of the membrane potential generated by cytochrome c oxidase upon single electron injection. Biochim Biophys Acta, 1710, 47-56 (2005)
148. Hill, B. C. & C. Greenwood: The reaction of fully reduced cytochrome c oxidase with oxygen studied by flow-flash spectrophotometry at room temperature. Biochem J, 218, 913-921 (1984)
149. Sharpe, M. A. & S. Ferguson-Miller: A chemically explicit model for the mechanism of proton pumping in heme-copper oxidases. J Bioenerg Biomembr, 40, 541-549 (2008)
150. Adelroth, P., R. B. Gennis & P. Brzezinski: Role of the pathway through K(I-362) in proton transfer in cytochrome c oxidase from R. sphaeroides . Biochemistry, 37, 2470-2476 (1998)
151. Wikstrom, M. K. F., A. Jasaitis, C. Backgren, A. Puustinen & M. I. Verkhovsky: The role of the D- and K-pathways of proton transfer in the function of the haemcopper oxidases. Biochim Biophys Acta, 1459, 514-520 (2000)
152. Pfitzner, U., K. Hoffmeier, A. Harrenga, A. Kannt, H. Michel, E. Bamberg, O.-M. H. Richter & B. Ludwig: Tracing the D-pathway in reconstituted site-directed mutants of cytochrome c oxidase from Paracoccus denitrificans. Biochemistry, 39, 6756-6762 (2000)
153. Pawate, A. S., J. Morgan, A. Namslauer, D. Mills, P. Brzezinski, S. Ferguson-Miller & R. B. Gennis: A mutation in subunit I of cytochrome oxidase from Rhodobacter sphaeroides results in an increase in steady-state activity but completely eliminates proton pumping. Biochemistry, 41, 13417-13423. (2002)
154. Salomonsson, L., K. Faxen, P. Adelroth & P. Brzezinski: The timing of proton migration in membrane-reconstituted cytochrome c oxidase. Proc Natl Acad Sci U S A, 102, 17624-17629 (2005)
155. Siletsky, S., F. Thomson, R. Gennis, A. D. Kaulen & A. Konstantinov: Time-resolved studies of intraprotein proton transfer in the D-channel mutants of Rhodobacter sphaeroides cytochrome c oxidase. Biochim Biophys Acta, EBEC Short Reports, 1555, 114 (2002)
156. 3 from Rhodobacter sphaeroides is involved in proton uptake during the reaction of the fully-reduced enzyme with dioxygen. Biochemistry, 36, 13824-13829 (1997)
157. Siletsky, S. & A. A. Konstantinov: Electrogenic mechanism of cytochrome c oxidase. The 8th European Biological Chemistry Conference, 80 (2006)
158. Sadoski, R. C., D. Zaslavsky, R. B. Gennis, B. Durham & F. Millett: Exposure of bovine cytochrome c oxidase to high triton X-100 or to alkaline conditions causes a dramatic change in the rate of reduction of compound F. J Biol Chem, 276, 33616-33620 (2001)
159. Wikstrom, M., K. Krab & M. Saraste: Cytochrome oxidase - a synthesis. Academic Press, New York (1981)
160. Brzezinski, P. & G. Larsson: Redox-driven proton pumping by heme-copper oxidases. Biochim Biophys Acta, 1605, 1-13 (2003)
161. Kaila, V. R., M. I. Verkhovsky, G. Hummer & M. Wikstrom: Glutamic acid 242 is a valve in the proton pump of cytochrome c oxidase. Proc Natl Acad Sci U S A, 105, 6255-6259 (2008)
162. Olsson, M. H. M., P. K. Sharma & A. Warshel: Simulating redox coupled proton transfer in cytochrome c oxidase: looking for the proton bottleneck.
163. Yoshikawa, S.: A cytochrome c oxidase proton pumping mechanism that excludes the O2 reduction site. FEBS Lett., 555, 8-12 (2003)
164. Papa, S., N. Capitanio & G. Capitanio: A cooperative model for proton pumping in cytochrome c oxidase. Biochim Biophys Acta, 1655, 353-364 (2004)
165. Namslauer, A. & P. Brzezinski: Structural elements involved in electron-coupled proton transfer in cytochrome c oxidase. FEBS Lett, 567, 103-110 (2004)
166. Seibold, S. A., D. A. Mills, S. Ferguson-Miller & R. I. Cukier: 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 (2005)
167. Wikstrom, M.: Mechanism of proton translocation by cytochrome c oxidase: a new four-stroke histidine cycle. Biochim Biophys Acta, 1458, 188-198 (2000)
168. Kannt, A., T. Soulimane, G. Buse, A. Becker, E. Bamberg & H. Michel: Electrical current generation and proton pumping catalyzed by the ba3-type cytochrome c oxidase from Thermus thermophilus . FEBS Lett, 434, 17-22 (1998)
169. Siletskiy, S., T. Soulimane, N. Azarkina, T. V. Vygodina, G. Buse, A. Kaulen & A. Konstantinov: Time-resolved generation of membrane potential by ba3 cytochrome c oxidase from Thermus thermophilus . Evidence for reduction-induced opening of the binuclear centre. FEBS Lett, 457, 98-102 (1999)
170. von Ballmoos, C., R. B. Gennis, P. Adelroth & P. Brzezinski: Kinetic design of the respiratory oxidases. Proc Natl Acad Sci U S A, 108, 11057-11062 (2011)
171. Chakrabarty, S., I. Namslauer, P. Brzezinski & A. Warshel: Exploration of the cytochrome c oxidase pathway puzzle and examination of the origin of elusive mutational effects. Biochim Biophys Acta, 1807, 413-426 (2011)
172. Henry, R. M., C.-H. Yu, T. Rodinger & R. Pomes: Functional Hydration and Conformational Gating of Proton Uptake in Cytochrome c Oxidase. J. Mol. Biol., 387, 1165-1185 (2009)
173. Humphrey, W., A. Dalke & K. Schulten: VMID visual molecular dynamics. J. Mol. Graph., 14, 33- (1996)
174. Siletsky, S. A.: Studies of electrogenic transfer of protons in cytochrome oxidase. Moscow State University, 108 (1998)