Computational modeling analysis of mitochondrial superoxide production under varying substrate conditions and upon inhibition of different segments of the electron transport chain

Biochimica et Biophysica Acta - Bioenergetics

Volumn 1847, Issue 6-7, 2015, Pages 656-679

  Markevich, Nikolai I ^a,b   Hoek, Jan B ^a  

^a THOMAS JEFFERSON UNIVERSITY   (United States)

^b INSTITUTE OF THEORETICAL AND EXPERIMENTAL BIOPHYSICS   (Russian Federation)

Author keywords

Computational model; Inhibitory analysis; Membrane potential; Respiratory chain; Semiquinone; Superoxide

Indexed keywords

ANTIMYCIN A1; CYTOCHROME B; CYTOCHROME BL; CYTOCHROME C; CYTOCHROME C OXIDASE; IRON SULFUR PROTEIN; MITOCHONDRIAL PROTEIN; MYXOTHIAZOL; OXYGEN; QUINONE DERIVATIVE; REACTIVE OXYGEN METABOLITE; REDUCED NICOTINAMIDE ADENINE DINUCLEOTIDE DEHYDROGENASE (UBIQUINONE); SEMIQUINONE; STIGMATELLIN; SUCCINATE DEHYDROGENASE; SUCCINIC ACID; SUPEROXIDE; UBIQUINOL CYTOCHROME C REDUCTASE; UNCLASSIFIED DRUG; MULTIENZYME COMPLEX; OXIDOREDUCTASE;

ARTICLE; BINDING SITE; BRAIN REGION; CELL KINETICS; COMPETITIVE INHIBITION; COMPUTER SIMULATION; CONFORMATIONAL TRANSITION; CONTROLLED STUDY; DISSOCIATION; ENZYME KINETICS; HEART MITOCHONDRION; HUMAN; ISOLATED LIVER; LIVER MITOCHONDRION; MATHEMATICAL MODEL; MITOCHONDRIAL ENERGY TRANSFER; MITOCHONDRIAL MEMBRANE POTENTIAL; NONHUMAN; OXIDATION; OXIDATION REDUCTION STATE; PHOSPHOLIPID VESICLE; PIGEON; PREDICTION; PRIORITY JOURNAL; PROTEIN DEPLETION; PROTON TRANSPORT; QUANTITATIVE ANALYSIS; RATE CONSTANT; RESPIRATORY CHAIN; SKELETAL MUSCLE; SUBMITOCHONDRIAL PARTICLE; ANTAGONISTS AND INHIBITORS; ELECTRON TRANSPORT; KINETICS; METABOLISM; MITOCHONDRION; OXIDATION REDUCTION REACTION; OXYGEN CONSUMPTION; PH; THEORETICAL MODEL;

COMPUTER SIMULATION; CYTOCHROME B GROUP; CYTOCHROMES C; ELECTRON TRANSPORT; ELECTRON TRANSPORT COMPLEX III; HUMANS; HYDROGEN-ION CONCENTRATION; IRON-SULFUR PROTEINS; KINETICS; MEMBRANE POTENTIAL, MITOCHONDRIAL; MITOCHONDRIA; MODELS, THEORETICAL; MULTIENZYME COMPLEXES; NADH, NADPH OXIDOREDUCTASES; OXIDATION-REDUCTION; OXYGEN CONSUMPTION; QUINONES; SUPEROXIDES;

EID: 84928485461     PISSN: 00052728     EISSN: 18792650     Source Type: Journal    
DOI: 10.1016/j.bbabio.2015.04.005     Document Type: Article

References (103)

1. W. Dröge Free radicals in the physiological control of cell function Physiol. Rev. 82 2002 47 95
2. M. Schieber, and N.S. Chandel ROS function in redox signaling and oxidative stress Curr. Biol. 24 2014 R453 R462
3. Z.W. Ye, J. Zhang, D.M. Townsend, and K.D. Tew Oxidative stress, redox regulation, and. diseases of cellular differentiation Biochim. Biophys. Acta Nov 15 2014 (S0304-4165(14) 00387-0. doi: 10.1016. [Epub ahead of print])
4. A. Boveris, and B. Chance The mitochondrial generation of hydrogen peroxide. General properties and effect of hyperbaric oxygen Biochem. J. 134 1973 707 716
5. J. Hirst Mitochondrial complex I Annu. Rev. Biochem. 82 2013 551 575
6. J. Hirst, M.S. King, and K.R. Pryde The production of reactive oxygen species by complex I Biochem. Soc. Trans. 36 2008 976 980
7. A.J. Lambert, and M.D. Brand Inhibitors of the quinone-binding site allow rapid superoxide. production from mitochondrial NADH:ubiquinone oxidoreductase (complex I) J. Biol. Chem. 279 2004 39414 39420
8. A.R. Crofts, S. Lhee, S.B. Crofts, J. Cheng, and S. Rose Proton pumping in the bc1 complex: a new gating mechanism that prevents short circuits Biochim. Biophys. Acta 1757 2006 1019 1034
9. S.T. Ohnishi, K. Shinzawa-Itoh, K. Ohta, S. Yoshikawa, and T. Ohnishi New insights into the superoxide generation sites in bovine heart NADH-ubiquinone oxidoreductase (Complex I): the significance of protein-associated ubiquinone and the dynamic shifting of generation sites between semiflavin and semiquinone radicals Biochim. Biophys. Acta 1797 2010 1901 1909
10. J.R. Treberg, C.L. Quinlan, and M.D. Brand Evidence for two sites of superoxide production by mitochondrial NADH-ubiquinone oxidoreductase (complex I) J. Biol. Chem. 286 2011 27103 27110
11. C.A. Yu, X. Cen, H.W. Ma, Y. Yin, L. Yu, L. Esser, and D. Xia Domain conformational switch of the iron-sulfur protein in cytochrome bc1 complex is induced by the electron transfer from cytochrome bL to bH Biochim. Biophys. Acta 1777 2008 1038 1043
12. A.R. Crofts, S. Hong, C. Wilson, R. Burton, D. Victoria, C. Harrison, and K. Schulten The mechanism of ubihydroquinone oxidation at the Qo-site of the cytochrome bc1 complex Biochim. Biophys. Acta 1827 2013 1362 1377
13. A.Y. Mulkidjanian Ubiquinol oxidation in the cytochrome bc1 complex: reaction mechanism and prevention of short-circuiting Biochim. Biophys. Acta 1709 2005 5 34
14. T.A. Link The role of the 'Rieske' iron sulfur protein in the hydroquinone oxidation (Q(P)) site of the cytochrome bc1 complex. The 'proton-gated affinity change' mechanism FEBS Lett. 412 1997 257 264
15. J. Zhu, T. Egawa, S.R. Yeh, L. Yu, and C.A. Yu Simultaneous reduction of iron-sulfur protein and cytochrome b(L) during ubiquinol oxidation in cytochrome bc(1) complex Proc. Natl. Acad. Sci. U. S. A. 104 2007 4864 4869
16. D. Xia, L. Esser, L. Yu, and C.A. Yu Structural basis for the mechanism of electron bifurcation at the quinol oxidation site of the cytochrome bc1 complex Photosynth. Res. 92 2007 17 34
17. C.L. Quinlan, A.A. Gerencser, J.R. Treberg, and M.D. Brand The mechanism of superoxide production by the antimycin-inhibited mitochondrial Q-cycle J. Biol. Chem. 286 2011 31361 31372
18. S. Drose, and U. Brandt The mechanism of mitochondrial superoxide production by the cytochrome bc1 complex J. Biol. Chem. 283 2008 21649 21654
19. V.A. Selivanov, T.V. Votyakova, J.A. Zeak, M. Trucco, J. Roca, and M. Cascante Bistability of mitochondrial respiration underlies paradoxical reactive oxygen species generation induced by anoxia PLoS Comput. Biol. 5 2009 e1000619
20. V.A. Selivanov, T.V. Votyakova, V.N. Pivtoraiko, J. Zeak, T. Sukhomlin, M. Trucco, J. Roca, and M. Cascante Reactive oxygen species production by forward and reverse electron fluxes in the mitochondrial respiratory chain PLoS Comput. Biol. 7 2011 e1001115
21. O.V. Demin, B.N. Kholodenko, and V.P. Skulachev A model of O2.-generation in the complex III of the electron transport chain Mol. Cell. Biochem. 184 1998 21 33
22. Y. Orii, and T. Miki Oxidation process of bovine heart ubiquinol-cytochrome c reductase as studied by stopped-flow rapid-scan spectrophotometry and simulations based on the mechanistic Q cycle model J. Biol. Chem. 272 1997 17594 17604
23. L.D. Gauthier, J.L. Greenstein, S. Cortassa, B. O'Rourke, and R.L. Winslow A computational model of reactive oxygen species and redox balance in cardiac mitochondria Biophys. J. 105 2013 1045 1056
24. J.N. Bazil, K.C. Vinnakota, F. Wu, and D.A. Beard Analysis of the kinetics and bistability of ubiquinol:cytochrome c oxidoreductase Biophys. J. 105 2013 343 355
25. B. Korzeniewski, and J.A. Zoladz A model of oxidative phosphorylation in mammalian skeletal muscle Biophys. Chem. 92 2001 17 34
26. D.A. Beard A biophysical model of the mitochondrial respiratory system and oxidative phosphorylation PLoS Comput. Biol. 1 2005 e36
27. N.I. Markevich, and J.B. Hoek Computational analysis of hysteresis and bistability in the mitochondrial respiratory chain Math. Biol. Bioinformatics 9 2014 89 111
28. L. Kussmaul, and J. Hirst The mechanism of superoxide production by NADH:ubiquinone oxidoreductase (complex I) from bovine heart mitochondria Proc. Natl. Acad. Sci. U. S. A. 103 2006 7607 7612
29. A.D. Vinogradov NADH/NAD + interaction with NADH: ubiquinone oxidoreductase complex I Biochim. Biophys. Acta 1777 2008 729 734
30. J.A. Birrell, G. Yakovlev, and J. Hirst Reactions of the flavin mononucleotide in complex I: a combined mechanism describes NADH oxidation coupled to the reduction of APAD +, ferricyanide, or molecular oxygen Biochemistry 48 2009 12005 12013
31. S. Ransac, M. Heiske, and J.P. Mazat From in silico to in spectro kinetics of respiratory complex I Biochim. Biophys. Acta 1817 2012 1958 1969
32. U. Brandt Energy converting NADH:quinone oxidoreductase (complex I) Annu. Rev. Biochem. 75 2006 69 92
33. C.C. Moser, T.A. Farid, S.E. Chobot, and P.L. Dutton Electron tunneling chains of mitochondria Biochim. Biophys. Acta 1757 2006 1096 1109
34. M.L. Verkhovskaya, N. Belevich, L. Euro, M. Wikstrom, and M.I. Verkhovsky Real-time electron transfer in respiratory complex I Proc. Natl. Acad. Sci. U. S. A. 105 2008 3763 3767
35. S. Ransac, C. Arnarez, and J.P. Mazat The flitting of electrons in complex I: a stochastic approach Biochim. Biophys. Acta 1797 2010 641 648
36. R.G. Efremov, R. Baradaran, and L.A. Sazanov The architecture of respiratory complex I Nature 465 2010 441 445
37. A.D. Vinogradov, V.D. Sled, D.S. Burbaev, V.G. Grivennikova, I.A. Moroz, and T. Ohnishi Energy-dependent Complex I-associated ubisemiquinones in submitochondrial particles FEBS Lett. 370 1995 83 87
38. S. Magnitsky, L. Toulokhonova, T. Yano, V.D. Sled, C. Hagerhall, V.G. Grivennikova, D.S. Burbaev, A.D. Vinogradov, and T. Ohnishi EPR characterization of ubisemiquinones and iron-sulfur cluster N2, central components of the energy coupling in the NADH-ubiquinone oxidoreductase (complex I) in situ J. Bioenerg. Biomembr. 34 2002 193 208
39. M.C. Kao, E. Nakamaru-Ogiso, A. Matsuno-Yagi, and T. Yagi Characterization of the membrane domain subunit NuoK (ND4L) of the NADH-quinone oxidoreductase from Escherichia coli Biochemistry 44 2005 9545 9554
40. T.V. Votyakova, and I.J. Reynolds DeltaPsi(m)-Dependent and -independent production of reactive oxygen species by rat brain mitochondria J. Neurochem. 79 2001 266 277
41. A.D. Vinogradov, and V.G. Grivennikova Generation of superoxide-radical by the NADH:ubiquinone oxidoreductase of heart mitochondria Biochemistry (Mosc) 70 2005 120 127
42. S. Raha, and B.H. Robinson Mitochondria, oxygen free radicals, disease and ageing Trends Biochem. Sci. 25 2000 502 528
43. P. Mitchell Protonmotive redox mechanism of the cytochrome b-c1 complex in the respiratory chain: protonmotive ubiquinone cycle FEBS Lett. 56 1975 1 6
44. Z. Zhang, L. Huang, V.M. Shulmeister, Y.I. Chi, K.K. Kim, L.W. Hung, A.R. Crofts, E.A. Berry, and S.H. Kim Electron transfer by domain movement in cytochrome bc1 Nature 392 1998 677 684
45. J.L. Cape, M.K. Bowman, and D.M. Kramer A semiquinone intermediate generated at the Qo site of the cytochrome bc1 complex: importance for the Q-cycle and superoxide production Proc. Natl. Acad. Sci. U. S. A. 104 2007 7887 7892
46. F.L. Muller, Y. Liu, and H. Van Remmen Complex III releases superoxide to both sides of the inner mitochondrial membrane J. Biol. Chem. 279 2004 49064 49073
47. U. Deichmann, S. Schuster, J.P. Mazat, and A. Cornish-Bowden Commemorating the 1913 Michaelis-Menten paper Die Kinetik der Invertinwirkung: three perspectives FEBS J. 281 2014 435 463
48. K.C. Vinnakota, and J.B. Bassingthwaighte Myocardial density and composition: a basis for calculating intracellular metabolite concentrations Am. J. Physiol. Heart Circ. Physiol. 286 2004 H1742 H1749
49. C.R. Hackenbrock, B. Chazotte, and S.S. Gupte The random collision model and a critical assessment of diffusion and collision in mitochondrial electron transport J. Bioenerg. Biomembr. 18 1986 331 368
50. F. Wu, F. Yang, K.C. Vinnakota, and D.A. Beard Computer modeling of mitochondrial tricarboxylic acid cycle, oxidative phosphorylation, metabolite transport, and electrophysiology J. Biol. Chem. 282 2007 24525 24537
51. K. Schwerzmann, L.M. Cruz-Orive, R. Eggman, A. Sanger, and E.R. Weibel Molecular architecture of the inner membrane of mitochondria from rat liver: a combined biochemical and stereological study J. Cell Biol. 102 1986 97 103
52. Y. Kushnareva, A.N. Murphy, and A. Andreyev Complex I-mediated reactive oxygen species generation: modulation by cytochrome c and NAD(P) + oxidation-reduction state Biochem. J. 368 2002 545 553
53. A.P. Kudin, N.Y. Bimpong-Buta, S. Vielhaber, C.E. Elger, and W.S. Kunz Characterization of superoxide-producing sites in isolated brain mitochondria J. Biol. Chem. 279 2004 4127 4135
54. V.G. Grivennikova, and A.D. Vinogradov Generation of superoxide by the mitochondrial Complex I Biochim. Biophys. Acta 1757 2006 553 561
55. A.A. Starkov, and G. Fiskum Regulation of brain mitochondrial H2O2 production by membrane potential and NAD(P)H redox state J. Neurochem. 86 2003 1101 1107
56. H. Rottenberg, R. Covian, and B.L. Trumpower Membrane potential greatly enhances superoxide generation by the cytochrome bc1 complex reconstituted into phospholipid vesicles J. Biol. Chem. 284 2009 19203 19210
57. A.J. Lambert, and M.D. Brand Superoxide production by NADH:ubiquinone oxidoreductase (complex I) depends on the pH gradient across the mitochondrial inner membrane Biochem. J. 382 2004 511 517
58. C. Batandier, B. Guigas, D. Detaille, M.Y. El-Mir, E. Fontaine, M. Rigoulet, and X.M. Leverve The ROS production induced by a reverse-electron flux at respiratory-chain complex 1 is hampered by metformin J. Bioenerg. Biomembr. 38 2006 33 42
59. D.L. Hoffman, and P.S. Brookes Oxygen sensitivity of mitochondrial reactive oxygen species generation depends on metabolic conditions J. Biol. Chem. 284 2009 16236 16245
60. B. Chance, H. Sies, and A. Boveris Hydroperoxide metabolism in mammalian organs Physiol. Rev. 59 1979 527 605
61. A.Y. Andreyev, Y.E. Kushnareva, and A.A. Starkov Mitochondrial metabolism of reactive oxygen species Biochemistry (Mosc) 70 2005 200 214
62. M.P. Murphy How mitochondria produce reactive oxygen species Biochem. J. 417 2009 1 13
63. M.A. Aon, B.A. Stanley, V. Sivakumaran, J.M. Kembro, B. O'Rourke, N. Paolocci, and S. Cortassa Glutathione/thioredoxin systems modulate mitochondrial H2O2 emission: an experimental-computational study J. Gen. Physiol. 139 2012 479 491
64. E. Cadenas, and A. Boveris Enhancement of hydrogen peroxide formation by protophores and ionophores in antimycin-supplemented mitochondria Biochem. J. 188 1980 31 37
65. A.L. Tsai, and G. Palmer The role of phospholipids in the binding of antimycin to yeast Complex III Biochim. Biophys. Acta 852 1986 100 105
66. A.A. Kroger, and M. Klingenberg Further evidence for the pool function of ubiquinone as derived from the inhibition of the electron transport by antimycin Eur. J. Biochem. 39 1973 313 323
67. G. Bechmann, H. Weiss, and P.R. Rich Non-linear inhibition curves for tight-binding inhibitors of dimeric ubiquinol-cytochrome c oxidoreductases. Evidence for rapid inhibitor mobility Eur. J. Biochem. 208 1992 315 325
68. M. Castellani, R. Covian, T. Kleinschroth, O. Anderka, B. Ludwig, and B.L. Trumpower Direct demonstration of half-of-the-sites reactivity in the dimeric cytochrome bc1 complex: enzyme with one inactive monomer is fully active but unable to activate the second ubiquinol oxidation site in response to ligand binding at the ubiquinone reduction site J. Biol. Chem. 285 2010 502 510
69. S. Ransac, and J.P. Mazat How does antimycin inhibit the bc1 complex? A part-time twin Biochim. Biophys. Acta 1797 2010 1849 1857
70. A.A. Starkov, and G. Fiskum Myxothiazol induces H(2)O(2) production from mitochondrial respiratory chain Biochem. Biophys. Res. Commun. 281 2001 645 650
71. T.A. Young, C.C. Cunningham, and S.M. Bailey Reactive oxygen species production by the mitochondrial respiratory chain in isolated rat hepatocytes and liver mitochondria: studies using myxothiazol Arch. Biochem. Biophys. 405 2002 65 72
72. J. Sun, and B.L. Trumpower Superoxide anion generation by the cytochrome bc1 complex Arch. Biochem. Biophys. 419 2003 198 206
73. D. Xia, C.A. Yu, H. Kim, J.Z. Xia, A.M. Kachurin, L. Zhang, L. Yu, and J. Deisenhofer Crystal structure of the cytochrome bc1 complex from bovine heart mitochondria Science 277 1997 60 66
74. T.A. Link, U. Haase, U. Brandt, and G. von Jagow What information do inhibitors provide about the structure of the hydroquinone oxidation site of ubihydroquinone: cytochrome c oxidoreductase? J. Bioenerg. Biomembr. 25 1993 221 232
75. H. Kim, D. Xia, C.A. Yu, J.Z. Xia, A.M. Kachurin, L. Zhang, L. Yu, and J. Deisenhofer What information do inhibitors provide about the structure of the hydroquinone oxidation site of ubihydroquinone: cytochrome c oxidoreductase? Proc. Natl. Acad. Sci. U. S. A. 95 1998 8026 8033
76. T.L. Dawson, G.J. Gores, A.L. Nieminen, B. Herman, and J.J. Lemasters Mitochondria as a source of reactive oxygen species during reductive stress in rat hepatocytes Am. J. Physiol. 264 1993 C961 C967
77. Q. Chen, E.J. Vazquez, S. Moghaddas, C.L. Hoppel, and E.J. Lesnefsky Production of reactive oxygen species by mitochondria: central role of complex III J. Biol. Chem. 278 2003 36027 36031
78. G. Ambrosio, J.L. Zweier, C. Duilio, P. Kuppusamy, G. Santoro, P.P. Elia, I. Tritto, P. Cirillo, M. Condorelli, and M. Chiariello Evidence that mitochondrial respiration is a source of potentially toxic oxygen free radicals in intact rabbit hearts subjected to ischemia and reflow J. Biol. Chem. 268 1993 18532 18541
79. K.R. Pryde, and J. Hirst Superoxide is produced by the reduced flavin in mitochondrial complex I: a single, unified mechanism that applies during both forward and reverse electron transfer J. Biol. Chem. 286 2011 18056 18065
80. P. Pasdois, J.E. Parker, E.J. Griffiths, and A.P. Halestrap The role of oxidized cytochrome c in regulating mitochondrial reactive oxygen species production and its perturbation in ischaemia Biochem. J. 436 2011 493 505
81. J.F. Turrens, A. Alexandre, and A.L. Lehninger Ubisemiquinone is the electron donor for superoxide formation by complex III of heart mitochondria Arch. Biochem. Biophys. 237 1985 408 414
82. M. Erecinska, and D.F. Wilson The effect of antimycin A on cytochromes b561, b566, and their relationship to ubiquinone and the iron-sulfer centers S-1 (+ N-2) and S-3 Arch. Biochem. Biophys. 174 1976 143 157
83. M. Sarewicz, A. Borek, E. Cieluch, M. Swierczek, and A. Osyczka Discrimination between two possible reaction sequences that create potential risk of generation of deleterious radicals by cytochrome bc. Implications for the mechanism of superoxide production Biochim. Biophys. Acta 1797 2010 1820 1827
84. P. Schonfeld, and L. Wojtczak Fatty acids decrease mitochondrial generation of reactive oxygen species at the reverse electron transport but increase it at the forward transport Biochim. Biophys. Acta 1767 2007 1032 1040
85. S. Drose, P.J. Hanley, and U. Brandt Ambivalent effects of diazoxide on mitochondrial ROS production at respiratory chain complexes I and III Biochim. Biophys. Acta 1790 2009 558 565
86. R.S. Sohal Aging, cytochrome oxidase activity, and hydrogen peroxide release by mitochondria Free Radic. Biol. Med. 14 1993 583 588
87. M. Degli Esposti, A. Ghelli, M. Crimi, E. Estornell, R. Fato, and G. Lenaz Complex I and complex III of mitochondria have common inhibitors acting as ubiquinone antagonists Biochem. Biophys. Res. Commun. 190 1993 1090 1096
88. V.G. Grivennikova, and A.D. Vinogradov Kinetics of ubiquinone reduction by the resolved succinate: ubiquinone reductase Biochim. Biophys. Acta 682 1982 491 495
89. V.D. Sled, N.I. Rudnitzky, Y. Hatefi, and T. Ohnishi Thermodynamic analysis of flavin in mitochondrial NADH:ubiquinone oxidoreductase complex I Biochemistry 33 1994 10069 10075
90. T. Ohnishi Iron-sulfur clusters/semiquinones in complex I Biochim. Biophys. Acta 1364 1998 186 206
91. Z.Q. Jin, H.Z. Zhou, G. Cecchini, M.O. Gray, and J.S. Karliner MnSOD in mouse heart: acute responses to ischemic preconditioning and ischemia-reperfusion injury Am. J. Physiol. Heart Circ. Physiol. 288 2005 H2986 H2994
92. J.L. Hsu, Y. Hsieh, C. Tu, D. O'Connor, H.S. Nick, and D.N. Silverman Catalytic properties of human manganese superoxide dismutase J. Biol. Chem. 271 1996 17687 17691
93. V.P. Shinkarev, and C.A. Wraight Intermonomer electron transfer in the bc1 complex dimer is controlled by the energized state and by impaired electron transfer between low and high potential hemes FEBS Lett. 581 2007 1535 1541
94. A.R. Crofts, V.P. Shinkarev, D.R. Kolling, and S. Hong The modified Q-cycle explains the apparent mismatch between the kinetics of reduction of cytochromes c1 and bH in the bc1 complex J. Biol. Chem. 278 2003 36191 36201
95. B.H. Bielski, and D.E. Cabelli Highlights of current research involving superoxide and perhydroxyl radicals in aqueous solutions Int. J. Radiat. Biol. 59 1991 291 319
96. J. Butler, G.G. Jayson, and A.J. Swallow The reaction between the superoxide anion radical and cytochrome c Biochim. Biophys. Acta 408 1975 215 222
97. J. Butler, W.H. Koppenol, and E. Margoliash Kinetics and mechanism of the reduction of ferricytochrome c by the superoxide anion J. Biol. Chem. 257 1982 10747 10750
98. R. Covian, and B.L. Trumpower The dimeric structure of the cytochrome bc(1) complex prevents center P inhibition by reverse reactions at center N Biochim. Biophys. Acta 1777 2008 1044 1052
99. G. Engstrom, R. Rajagukguk, A.J. Saunders, C.N. Patel, S. Rajagukguk, T. Merbitz-Zahradnik, K. Xiao, G.J. Pielak, B. Trumpower, C.A. Yu, L. Yu, B. Durham, and F. Millett Design of a ruthenium-labeled cytochrome c derivative to study electron transfer with the cytochrome bc1 complex Biochemistry 42 2003 2816 2824
100. F. Millett, and B. Durham Kinetics of electron transfer within cytochrome bc (1) and between cytochrome bc (1) and cytochrome c Photosynth. Res. 82 2004 1 16
101. D.P. Jones Intracellular diffusion gradients of O2 and ATP Am. J. Physiol. 250 1986 C663 C675
102. A.D. Vinogradov NADH/NAD + interaction with NADH: ubiquinone oxidoreductase (complex I) Biochim. Biophys. Acta 1364 1998 169 185
103. A.J. Lambert, J.A. Buckingham, H.M. Boysen, and M.D. Brand Low complex I content explains the low hydrogen peroxide production rate of heart mitochondria from the long-lived pigeon, Columba livia Aging Cell 9 2010 78 91