A Computational model of reactive oxygen species and redox balance in cardiac mitochondria

Biophysical Journal

Volumn 105, Issue 4, 2013, Pages 1045-1056

  Gauthier, Laura D ^b   Greenstein, Joseph L ^b   Cortassa, Sonia ^a,b   O'Rourke, Brian ^a   Winslow, Raimond L ^b  

^a JOHNS HOPKINS UNIVERSITY SCHOOL OF MEDICINE   (United States)

^b Johns Hopkins University   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

MULTIENZYME COMPLEX; REACTIVE OXYGEN METABOLITE;

ARTICLE; BIOLOGICAL MODEL; CELL RESPIRATION; CHEMICAL STRUCTURE; CHEMISTRY; COMPUTER SIMULATION; CYTOLOGY; HEART MUSCLE; METABOLISM; MITOCHONDRIAL MEMBRANE POTENTIAL; MITOCHONDRION; OXIDATION REDUCTION REACTION; PROTEIN CONFORMATION;

CELL RESPIRATION; COMPUTER SIMULATION; ELECTRON TRANSPORT CHAIN COMPLEX PROTEINS; MEMBRANE POTENTIAL, MITOCHONDRIAL; MITOCHONDRIA; MODELS, BIOLOGICAL; MODELS, MOLECULAR; MYOCARDIUM; OXIDATION-REDUCTION; PROTEIN CONFORMATION; REACTIVE OXYGEN SPECIES;

EID: 84882973495     PISSN: 00063495     EISSN: 15420086     Source Type: Journal    
DOI: 10.1016/j.bpj.2013.07.006     Document Type: Article

References (82)

1. W. Dröge Free radicals in the physiological control of cell function Physiol. Rev. 82 2002 47 95
2. C.P. Baines, M. Goto, and J.M. Downey Oxygen radicals released during ischemic preconditioning contribute to cardioprotection in the rabbit myocardium J. Mol. Cell. Cardiol. 29 1997 207 216
3. V. Petronilli, and P. Costantini P. Bernardi The voltage sensor of the mitochondrial permeability transition pore is tuned by the oxidation-reduction state of vicinal thiols. Increase of the gating potential by oxidants and its reversal by reducing agents J. Biol. Chem. 269 1994 16638 16642
4. L.-H. Xie, and F. Chen J.N. Weiss Oxidative-stress-induced afterdepolarizations and calmodulin kinase II signaling Circ. Res. 104 2009 79 86
5. F.J. Giordano Oxygen, oxidative stress, hypoxia, and heart failure J. Clin. Invest. 115 2005 500 508
6. R. Nakamura, and K. Egashira A. Takeshita Probucol attenuates left ventricular dysfunction and remodeling in tachycardia-induced heart failure: roles of oxidative stress and inflammation Circulation 106 2002 362 367
7. C.E. Murdoch, and M. Zhang A.M. Shah NADPH oxidase-dependent redox signalling in cardiac hypertrophy, remodelling and failure Cardiovasc. Res. 71 2006 208 215
8. T. Ide, and H. Tsutsui A. Takeshita Mitochondrial electron transport complex I is a potential source of oxygen free radicals in the failing myocardium Circ. Res. 85 1999 357 363
9. M.A. Aon, S. Cortassa, and B. O'Rourke Redox-optimized ROS balance: a unifying hypothesis Biochim. Biophys. Acta 1797 2010 865 877
10. 2+ uptake in myocytes from failing hearts restores energy supply and demand matching Circ. Res. 103 2008 279 288
11. + increases mitochondrial formation of reactive oxygen species in failing cardiac myocytes Circulation 121 2010 1606 1613
12. R.D. Guzy, and B. Hoyos P.T. Schumacker Mitochondrial complex III is required for hypoxia-induced ROS production and cellular oxygen sensing Cell Metab. 1 2005 401 408
13. + oxidation-reduction state Biochem. J. 368 2002 545 553
14. L. Kussmaul, and J. Hirst The mechanism of superoxide production by NADH:ubiquinone oxidoreductase (complex I) from bovine heart mitochondria Proc. Natl. Acad. Sci. USA 103 2006 7607 7612
15. 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
16. V.G. Grivennikova, and A.D. Vinogradov Generation of superoxide by the mitochondrial Complex I Biochim. Biophys. Acta 1757 2006 553 561
17. 1 complex reconstituted into phospholipid vesicles J. Biol. Chem. 284 2009 19203 19210
18. S.S. Korshunov, V.P. Skulachev, and A.A. Starkov High protonic potential actuates a mechanism of production of reactive oxygen species in mitochondria FEBS Lett. 416 1997 15 18
19. J.F. Turrens, and A. Boveris Generation of superoxide anion by the NADH dehydrogenase of bovine heart mitochondria Biochem. J. 191 1980 421 427
20. J. St-Pierre, and J.A. Buckingham M.D. Brand Topology of superoxide production from different sites in the mitochondrial electron transport chain J. Biol. Chem. 277 2002 44784 44790
21. 2 release at mitochondrial complex I: negative modulation by malate, positive by cyanide J. Bioenerg. Biomembr. 41 2009 387 393
22. 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
23. J. Carroll, and I.M. Fearnley J.E. Walker Bovine complex I is a complex of 45 different subunits J. Biol. Chem. 281 2006 32724 32727
24. R.G. Efremov, and L.A. Sazanov Structure of the membrane domain of respiratory complex I Nature 476 2011 414 420
25. A. Mourier, and N.-G. Larsson Tracing the trail of protons through complex I of the mitochondrial respiratory chain PLoS Biol. 9 2011 e1001129
26. U. Brandt A two-state stabilization-change mechanism for proton-pumping complex I Biochim. Biophys. Acta 1807 2011 1364 1369
27. S. Dröse, and U. Brandt Molecular mechanisms of superoxide production by the mitochondrial respiratory chain B. Kadenbach, Mitochondrial Oxidative Phosphorylation 2012 Springer New York 145 169
28. 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
29. 1 complex: importance for the Q-cycle and superoxide production Proc. Natl. Acad. Sci. USA 104 2007 7887 7892
30. H. Zhang, and A. Osyczka C.C. Moser Exposing the complex III Qo semiquinone radical Biochim. Biophys. Acta 1767 2007 883 887
31. 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
32. D. Han, and F. Antunes E. Cadenas Voltage-dependent anion channels control the release of the superoxide anion from mitochondria to cytosol J. Biol. Chem. 278 2003 5557 5563
33. 2 emission: an experimental-computational study J. Gen. Physiol. 139 2012 479 491
34. O.V. Demin, and I.I. Goryanin H.V. Westerhoff Kinetic modeling of energy metabolism and superoxide generation in hepatocyte mitochondria Mol. Biol. (Mosk.) 35 2001 940 949
35. 2.- generation in the complex III of the electron transport chain Mol. Cell. Biochem. 184 1998 21 33
36. 1 complex Biophys. J. 102 2012 1194 1203
37. 2+ handling Am. J. Physiol. 273 1997 C717 C733
38. M. Erecińska, and D.F. Wilson Regulation of cellular energy metabolism J. Membr. Biol. 70 1982 1 14
39. K. Sato, and Y. Kashiwaya R.L. Veech Insulin, ketone bodies, and mitochondrial energy transduction FASEB J. 9 1995 651 658
40. S. Mintz, and E.D. Robin Redox state of free nicotinamide-adenine nucleotides in the cytoplasm and mitochondria of alveolar macrophages J. Clin. Invest. 50 1971 1181 1186
41. 1 complex Biochem. J. 225 1985 399 405
42. B. Kadenbach Intrinsic and extrinsic uncoupling of oxidative phosphorylation Biochim. Biophys. Acta 1604 2003 77 94
43. B. Kadenbach, and R. Ramzan S. Vogt The role of mitochondrial membrane potential in ischemic heart failure Mitochondrion 11 2011 700 706
44. W.A. Cramer, and D. Knaff Energy Transduction in Biological Membranes. A Textbook of Bioenergetics 1991 Springer-Verlag New York
45. P. Randle, and P. Tubbs Carbohydrate and fatty acid metabolism R.M. Berne, N. Sperelakis, R. Geiger, Handbook of Physiology 1979 American Physiological Society Bethesda, MD 805 844
46. V. Adam-Vizi, and C. Chinopoulos Bioenergetics and the formation of mitochondrial reactive oxygen species Trends Pharmacol. Sci. 27 2006 639 645
47. S.S. Liu Cooperation of a "reactive oxygen cycle" with the Q cycle and the proton cycle in the respiratory chain - superoxide generating and cycling mechanisms in mitochondria J. Bioenerg. Biomembr. 31 1999 367 376
48. 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
49. A.-C. Wei, and M.A. Aon S. Cortassa Mitochondrial energetics, pH regulation, and ion dynamics: a computational-experimental approach Biophys. J. 100 2011 2894 2903
50. V.A. Selivanov, and J.A. Zeak T.V. Votyakova The role of external and matrix pH in mitochondrial reactive oxygen species generation J. Biol. Chem. 283 2008 29292 29300
51. E. Cadenas, and A. Boveris Enhancement of hydrogen peroxide formation by protophores and ionophores in antimycin-supplemented mitochondria Biochem. J. 188 1980 31 37
52. Reference deleted in proof.
53. V.D. Sled, and N.I. Rudnitzky T. Ohnishi Thermodynamic analysis of flavin in mitochondrial NADH:ubiquinone oxidoreductase (complex I) Biochemistry 33 1994 10069 10075
54. S. Cortassa, and M.A. Aon R.L. Winslow A computational model integrating electrophysiology, contraction, and mitochondrial bioenergetics in the ventricular myocyte Biophys. J. 91 2006 1564 1589
55. F.Q. Schafer, and G.R. Buettner Redox environment of the cell as viewed through the redox state of the glutathione disulfide/glutathione couple Free Radic. Biol. Med. 30 2001 1191 1212
56. T.L. Dawson, and G.J. Gores J.J. Lemasters Mitochondria as a source of reactive oxygen species during reductive stress in rat hepatocytes Am. J. Physiol. 264 1993 C961 C967
57. B.S. Zuckerbraun, and B.Y. Chin L.E. Otterbein Carbon monoxide signals via inhibition of cytochrome c oxidase and generation of mitochondrial reactive oxygen species FASEB J. 21 2007 1099 1106
58. J.F. Turrens Mitochondrial formation of reactive oxygen species J. Physiol. 552 2003 335 344
59. 1 complex J. Biol. Chem. 283 2008 21649 21654
60. o site for reaction with oxygen Biochemistry 47 2008 12365 12370
61. H. Zhang, and S.E. Chobot C.C. Moser Quinone and non-quinone redox couples in Complex III J. Bioenerg. Biomembr. 40 2008 493 499
62. 1 complex in Rhodobacter capsulates chromatophores Biochim. Biophys. Acta 1100 1992 67 74
63. K. Krab, H. Kempe, and M. Wikström Explaining the enigmatic KM for oxygen in cytochrome c oxidase: a kinetic model Biochim. Biophys. Acta 1807 2011 348 358
64. 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
65. V.A. Selivanov, and M. Cascante T.V. Votyakova Multistationary and oscillatory modes of free radicals generation by the mitochondrial respiratory chain revealed by a bifurcation analysis PLOS Comput. Biol. 8 2012 e1002700
66. V.A. Selivanov, and T.V. Votyakova M. Cascante Reactive oxygen species production by forward and reverse electron fluxes in the mitochondrial respiratory chain PLOS Comput. Biol. 7 2011 e1001115
67. V.A. Selivanov, and T.V. Votyakova M. Cascante Bistability of mitochondrial respiration underlies paradoxical reactive oxygen species generation induced by anoxia PLOS Comput. Biol. 5 2009 e1000619
68. Q. Jin, and C.M. Bethke Kinetics of electron transfer through the respiratory chain Biophys. J. 83 2002 1797 1808
69. S. Cortassa, and M.A. Aon B. O'Rourke A mitochondrial oscillator dependent on reactive oxygen species Biophys. J. 87 2004 2060 2073
70. S. Cortassa, and M.A. Aon B. O'Rourke An integrated model of cardiac mitochondrial energy metabolism and calcium dynamics Biophys. J. 84 2003 2734 2755
71. G. Lenaz, and M.L. Genova Kinetics of integrated electron transfer in the mitochondrial respiratory chain: random collisions vs. solid state electron channeling American Journal of Physiology - Cell Physiology 292 2007 C1221 C1239
72. L. Zhou, and S. Cortassa B. O'Rourke Modeling cardiac action potential shortening driven by oxidative stress-induced mitochondrial oscillations in guinea pig cardiomyocytes Biophys. J. 97 2009 1843 1852
73. X. Chen, and F. Qi D.A. Beard Kinetics and regulation of mammalian NADH-ubiquinone oxidoreductase (Complex I) Biophys. J. 99 2010 1426 1436
74. M.L. Genova, and B. Ventura G. Lenaz The site of production of superoxide radical in mitochondrial Complex I is not a bound ubisemiquinone but presumably iron-sulfur cluster N2 FEBS Lett. 505 2001 364 368
75. F. Qi, and R.K. Dash D.A. Beard Generating rate equations for complex enzyme systems by a computer-assisted systematic method BMC Bioinformatics 10 2009 238
76. S. Muraoka, and E.C. Slater The redox states of respiratory-chain components in rat-liver mitochondria II. The "crossover" on the transition from State 3 to State 4 Biochim. Biophys. Acta 180 1969 227 236
77. P. Brzezinski, and P. Ädelroth Pathways of proton transfer in cytochrome c oxidase J. Bioenerg. Biomembr. 30 1998 99 107
78. R.P. Hafner, G.C. Brown, and M.D. Brand Analysis of the control of respiration rate, phosphorylation rate, proton leak rate and protonmotive force in isolated mitochondria using the "top-down" approach of metabolic control theory Eur. J. Biochem. 188 1990 313 319
79. L. Lionetti, and S. Iossa G. Liverini Relationship between membrane potential and respiration rate in isolated liver mitochondria from rats fed an energy dense diet Mol. Cell. Biochem. 158 1996 133 138
80. A. Marcinkeviciute, and V. Mildaziene B. Kholodenko Kinetics and control of oxidative phosphorylation in rat liver mitochondria after chronic ethanol feeding Biochem. J. 349 2000 519 526
81. C.C. Moser, and T.A. Farid P.L. Dutton Electron tunneling chains of mitochondria Biochim. Biophys. Acta 1757 2006 1096 1109
82. 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