Reactive oxygen species production by forward and reverse electron fluxes in the mitochondrial respiratory chain

PLoS Computational Biology

Volumn 7, Issue 3, 2011, Pages

  Selivanov, Vitaly A ^a,b   Votyakova, Tatyana V ^c   Pivtoraiko, Violetta N ^d   Zeak, Jennifer ^c   Sukhomlin, Tatiana ^e   Trucco, Massimo ^c   Roca, Josep ^a   Cascante, Marta ^a  

^a UNIVERSITY OF BARCELONA   (Spain)

^b MOSCOW STATE UNIVERSITY   (Russian Federation)

^c UNIVERSITY OF PITTSBURGH SCHOOL OF MEDICINE   (United States)

^d University of Alabama at Birmingham   (United States)

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

Author keywords

[No Author keywords available]

Indexed keywords

CHAINS; ELECTRON TRANSPORT PROPERTIES; MITOCHONDRIA;

CELL SURVIVAL; CELLULAR ADAPTATION; CONDITION; ELECTRON FLUX; ELECTRON TRANSPORT; MITOCHONDRIAL RESPIRATORY CHAIN; REACTIVE OXYGEN SPECIES; REOXYGENATION; RESPIRATORY CHAINS; SYSTEMIC DISEASE;

FREE RADICALS;

REACTIVE OXYGEN METABOLITE; REDUCED NICOTINAMIDE ADENINE DINUCLEOTIDE DEHYDROGENASE (UBIQUINONE); UBIQUINOL CYTOCHROME C REDUCTASE; PROTON TRANSPORTING ADENOSINE TRIPHOSPHATASE;

ANIMAL CELL; ARTICLE; BRAIN MITOCHONDRION; CONTROLLED STUDY; ELECTRON TRANSPORT; ENZYME SUBSTRATE; MATHEMATICAL MODEL; MITOCHONDRIAL RESPIRATION; NONHUMAN; OXIDATIVE PHOSPHORYLATION; PROTON MOTIVE FORCE; PROTON TRANSPORT; QUALITATIVE ANALYSIS; RAT; RESPIRATORY CHAIN; STEADY STATE; ALGORITHM; ANIMAL; BIOLOGY; BRAIN; CHEMISTRY; CITRIC ACID CYCLE; COMPUTER SIMULATION; ELECTRON; METABOLISM; METHODOLOGY; MITOCHONDRIAL MEMBRANE POTENTIAL; MITOCHONDRION; SPECTROFLUOROMETRY; WISTAR RAT;

RATTUS;

ALGORITHMS; ANIMALS; ATP SYNTHETASE COMPLEXES; BRAIN; CITRIC ACID CYCLE; COMPUTATIONAL BIOLOGY; COMPUTER SIMULATION; ELECTRON TRANSPORT; ELECTRONS; MEMBRANE POTENTIAL, MITOCHONDRIAL; MITOCHONDRIA; RATS; RATS, WISTAR; REACTIVE OXYGEN SPECIES; SPECTROMETRY, FLUORESCENCE;

EID: 79953667930     PISSN: 1553734X     EISSN: 15537358     Source Type: Journal    
DOI: 10.1371/journal.pcbi.1001115     Document Type: Article

References (45)

1. Koopman WJ, Nijtmans LG, Dieteren CE, Roestenberg P, Valsecchi F, et al. (2010) Mammalian mitochondrial complex I: biogenesis, regulation, and reactive oxygen species generation. Antioxid Redox Signal 12: 1431-1470.
2. McCord JM, Fridovich I, Superoxide dismutase: the first twenty years (1968-1988) (1988). Free Radic Biol Med 5: 363-369.
3. Acker H, (2005) The oxygen sensing signal cascade under the influence of reactive oxygen species. Philos Trans R Soc Lond B Biol Sci 360: 2201-2210.
4. Brookes PS, Yoon Y, Robotham JL, Anders MW, Sheu SS, (2004) Calcium, ATP, and ROS: a mitochondrial love-hate triangle. Am J Physiol Cell Physiol 287: C817-C833.
5. Waypa GB, Marks JD, Guzy R, Mungai PT, Schriewer J, et al. (2010) Hypoxia triggers subcellular compartmental redox signaling in vascular smooth muscle cells. Circ Res 106: 526-535.
6. Cheng Y, Zhu P, Yang J, Liu X, Dong S, et al. (2010) Ischemic preconditioning-regulated miR-21 protects the heart from ischemia/reperfusion injury via anti-apoptosis through its target PDCD4. Cardiovasc Res 87: 431-439.
7. Won Kim H, Haider HK, Jiang S, Ashraf M, (2009) Ischemic preconditioning augments survival of stem cells via miR-210 expression by targeting caspase-8-associated protein 2. J Biol Chem 284: 33161-33168.
8. Kroemer G, Blomgren K, (2007) Mitochondrial Cell Death Control in Familial Parkinson Disease. PLoS Biol 5 (7): e206 doi:10.1371/journal.pbio.0050206.
9. Armann B, Hanson MS, Hatch E, Steffen A, Fernandez LA, (2007) Quantification of basal and stimulated ROS levels as predictors of islet potency and function. Am J Transplant 7: 38-47.
10. Rea SL, Ventura N, Johnson TE, (2007) Relationship Between Mitochondrial Electron Transport Chain Dysfunction, Development, and Life Extension in Caenorhabditis elegans. PLoS Biol 5 (10): e259 doi:10.1371/journal.pbio.0050259.
11. Chen Q, Vazquez EJ, Moghaddas S, Hoppel CL, Lesnefsky EJ, (2003) Production of reactive oxygen species by mitochondria: central role of complex III. J Biol Chem 278: 36027-36031.
12. St-Pierre J, Buckingham JA, Roebuck SJ, Brand MD, (2002) Topology of superoxide production from different sites in the mitochondrial electron transport chain. J Biol Chem 277: 44784-44790.
13. Hoffman DL, Brookes PS, (2009) Oxygen sensitivity of mitochondrial reactive oxygen species generation depends on metabolic conditions. J Biol Chem 284: 16236-1623645.
14. Boveris A, Chance B, (1973) The mitochondrial generation of hydrogen peroxide: general properties and effect of hyperbaric oxygen. Biochem J 134: 707-716.
15. Votyakova TV, Reynolds IJ, (2001) DeltaPsi(m)-Dependent and -independent production of reactive oxygen species by rat brain mitochondria. J Neurochem 79: 266-277.
16. Schönfeld P, Wojtczak L, (2007) 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: 1032-1040.
17. Dutton PL, Moser CC, Sled VD, Daldal F, Ohnishi T, (1998) A reductant-induced oxidation mechanism for complex I. Biochim Biophys Acta 1364: 245-257.
18. Ohnishi T, Salerno JC, (2005) Conformation-driven and semiquinone-gated proton-pump mechanism in the NADH-ubiquinone oxidoreductase (complex I). FEBS Lett 579: 4555-4561.
19. Orii Y, Miki T, (1997) 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: 17594-17604.
20. Selivanov VA, Puigjaner J, Sillero A, Centelles JJ, Ramos-Montoya A, et al. (2004) An optimized algorithm for flux estimation from isotopomer distribution in glucose metabolites. Bioinformatics 20: 3387-3397.
21. Selivanov VA, Meshalkina LE, Solovjeva ON, Kuchel PW, Ramos-Montoya A, et al. (2005) Rapid simulation and analysis of isotopomer distributions using constraints based on enzyme mechanisms: an example from HT29 cancer cells. Bioinformatics 21: 3558-3564.
22. Selivanov VA, Marin S, Lee PWN, Cascante M, (2006) Software for dynamic analysis of tracer-based metabolomic data: estimation of metabolic fluxes and their statistical analysis. Bioinformatics 22: 2806-2812.
23. Selivanov VA, Votyakova TV, Zeak JA, Trucco M, Roca J, Cascante M, (2009) Bistability of mitochondrial respiration underlies paradoxical reactive oxygen species generation induced by anoxia. PLoS Comput Biol 5 (12): e1000619.
24. Tang HL, Trumpower BL, (1986) Triphasic reduction of cytochrome b and the protonmotive Q cycle pathway of electron transfer in the cytochrome bc1 complex of the mitochondrial respiratory chain. J Biol Chem 261: 6209-6215.
25. Selivanov VA, Zeak JA, Roca J, Cascante M, Trucco M, (2008) The role of external and matrix pH in mitochondrial reactive oxygen species generation. J Biol Chem 283: 29292-29300.
26. Boveris A, Cadenas E, Stoppani AO, (1976) Role of ubiquinone in the mitochondrial generation of hydrogen peroxide. Biochem J 156: 435-444.
27. Cadenas E, Boveris A, Ragan CI, Stoppani AO, (1977) Production of superoxide radicals and hydrogen peroxide by NADH-ubiquinone reductase and ubiquinol-cytochrome c reductase from beef-heart mitochondria. Arch Biochem Biophys 180: 248-257.
28. Kwong LK, Sohal RS, (1998) Substrate and site specificity of hydrogen peroxide generation in mouse mitochondria. Arch Biochem Biophys 350: 118-126.
29. Zickermann V, Dröse S, Tocilescu MA, Zwicker K, Kerscher S, Brandt U, (2008) Challenges in elucidating structure and mechanism of proton pumping NADH:ubiquinone oxidoreductase (complex I). J Bioenerg Biomembr 40: 475-483.
30. Fato R, Bergamini C, Bortolus M, Maniero AL, Leoni S, Ohnishi T, Lenaz G, (2009) Differential effects of mitochondrial Complex I inhibitors on production of reactive oxygen species. Biochim Biophys Acta 1787: 384-392.
31. Press WH, Flannery BP, Teukolsky SA, Vetterling WT, (2002) Numerical Recipes in C: The Art of Scientific Computing New York Cambridge University Press.
32. Blinov ML, Faeder JR, Goldstein B, Hlavacek WS, (2004) BioNetGen: software for rule-based modeling of signal transduction based on the interactions of molecular domains. Bioinformatics 20: 3289-3291.
33. Hlavacek WS, Faeder JR, Blinov ML, Posner RG, Hucka M, Fontana W, (2006) Rules for modeling signal-transduction systems. Sci STKE 344: re6.
34. Kudin AP, Debska-Vielhaber G, Kunz WS, (2005) Characterization of superoxide production sites in isolated rat brain and skeletal muscle mitochondria. Biomed Pharmacother 59: 163-168.
35. Genova ML, Ventura B, Giuliano G, Bovina C, Formiggini G, Parenti Castelli G, Lenaz G, (2001) 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: 364-368.
36. Brand MD, (2010) The sites and topology of mitochondrial superoxide production. Exp Gerontol 45: 466-472.
37. Lambert AJ, Brand MD, (2009) Reactive oxygen species production by mitochondria. Methods Mol Biol 554: 165-181.
38. Zorov DB, Filburn CR, Klotz LO, Zweier JL, Sollott SJ, (2000) Reactive oxygen species (ROS)-induced ROS release: a new phenomenon accompanying induction of the mitochondrial permeability transition in cardiac myocytes. J Exp Med 192: 1001-1014.
39. Brandt U, (2006) Energy converting NADH:quinone oxidoreductase (complex I). Annu Rev Biochem 75: 69-92.
40. Ohnishi T, (1998) Iron-sulfur clusters/semiquinones in complex I. Biochim Biophys Acta 1364: 186-206.
41. Vinogradov AD, (1998) Catalytic properties of the mitochondrial NADH-ubiquinone oxidoreductase (Complex I) and the pseudo-reversible active/inactive enzyme transition. Biochim Biophys Acta 1364: 169-185.
42. Ohnishi T, Johnson JE Jr, Yano T, LoBruttoc R, Widgerb WR, (2005) Thermodynamic and EPR studies of slowly relaxing ubisemiquinone species inthe isolated bovine heart complex I. FEBS Lett 579: 500-506.
43. Sled VD, Rudnitzky NI, Hatefi Y, Ohnishi T, (1994) Thermodynamic analysis of flavin in mitochondrial NADH:ubiquinone oxidoreductase (complex I). Biochemistry 33: 10069-10075.
44. Massari S, Frigeri L, Azzone G, (1972) A quantitative correlation between the kinetics of solutes and water translocation in Liver Mitochondria. J Membr Biol 9: 71-82.
45. Lass A, Agarwal S, Sohal RS, (1997) Mitochondrial ubiquinone homologues, superoxide radical generation, and longevity in different mammalian species. J Biol Chem 272: 19199-19204.