Changes in oxygen tension affect cardiac mitochondrial respiration rate via changes in the rate of mitochondrial hydrogen peroxide production

Journal of Molecular and Cellular Cardiology

Volumn 47, Issue 1, 2009, Pages 49-56

  Di Maria, Carla A ^a   Bogoyevitch, Marie A ^b   McKitrick, Douglas J ^c   Arnolda, Leonard F ^d   Hool, Livia C ^a   Arthur, Peter G ^a  

^a UNIVERSITY OF WESTERN AUSTRALIA   (Australia)

^b UNIVERSITY OF MELBOURNE   (Australia)

^c UNIVERSITY OF WESTERN AUSTRALIA   (Australia)

^d The Australian National University   (Australia)

Author keywords

Cardioprotection; Hydrogen peroxide; Hypoxia; Ischemic Preconditioning; Metabolic rate; Mitochondria; Oxygen consumption; Reactive oxygen species; Reperfusion Injury; Respiration

Indexed keywords

CATALASE; HYDROGEN PEROXIDE; NITRIC OXIDE SYNTHASE; REACTIVE OXYGEN METABOLITE;

ANIMAL TISSUE; ARTICLE; BREATHING RATE; CONTROLLED STUDY; ENZYME ACTIVITY; HEART MITOCHONDRION; HEART RATE; MALE; MITOCHONDRIAL RESPIRATION; NONHUMAN; OXYGEN TENSION; PRIORITY JOURNAL; PROTEIN EXPRESSION; RAT;

ANIMALS; ELECTRON TRANSPORT COMPLEX I; ELECTRON TRANSPORT COMPLEX II; ELECTRON TRANSPORT COMPLEX III; ELECTRON TRANSPORT COMPLEX IV; ENZYME INHIBITORS; HYDROGEN PEROXIDE; MALE; MICROSCOPY, ELECTRON, TRANSMISSION; MITOCHONDRIA, HEART; NG-NITROARGININE METHYL ESTER; NITRIC OXIDE SYNTHASE; OXYGEN; OXYGEN CONSUMPTION; RATS; SUPEROXIDES;

EID: 67349256867     PISSN: 00222828     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.yjmcc.2009.03.010     Document Type: Article

References (52)

1. Depre C., and Vatner S.F. Cardioprotection in stunned and hibernating myocardium. Heart Fail Rev. 12 3-4 (2007 Dec) 307-317
2. Stone J.R., and Yang S. Hydrogen peroxide: a signaling messenger. Antioxid. Redox. Signal. 8 3-4 (2006 Mar-Apr) 243-270
3. Turrens J.F. Mitochondrial formation of reactive oxygen species. J. Physiol. 552 Pt 2 (2003 Oct 15) 335-344
4. Gnaiger E., Steinlechner-Maran R., Mendez G., Ebert T., and Margreiter R. Control of mitochondrial and cellular respiration by oxygen. J. Bioenerg. Biomembranes 27 (1995) 583-596
5. Gnaiger E., and Kuznetsov A.V. Mitochondrial respiration at low levels of oxygen and cytochrome c. Biochem. Soc. Trans. 30 2 (2002 Apr) 252-258
6. Arthur P.G., Cam-Tu Ngo C.T., Moretta P., and Guppy M. Lack of oxygen sensing by mitochondria in platelets. Eur. J. Biochem. 266 (1999) 215-219
7. Marcinek D.J., Ciesielski W.A., Conley K.E., and Schenkman K.A. Oxygen regulation and limitation to cellular respiration in mouse skeletal muscle in vivo. Am. J. Physiol. Heart Circ. Physiol. 285 5 (2003 Nov) H1900-H1908
8. Gnaiger E., Lassnig B., Kuznetsov A., Rieger G., and Margreiter R. Mitochondrial oxygen affinity, respiratory flux control and excess capacity of cytochrome c oxidase. J. Exp. Biol. 201 Pt 8 (1998 Apr) 1129-1139
9. Chandel N., Budinger G.R.S., Kemp R.A., and Schumacker P.T. Inhibition of cytochrome-c oxidase activity during prolonged hypoxia. Am. J. Physiol. 268 (1995) L918-L925
10. Chavez J.C., Pichiule P., Boero J., and Arregui A. Reduced mitochondrial respiration in mouse cerebral cortex during chronic hypoxia. Neurosci. Lett. 193 3 (1995 Jul 7) 169-172
11. Budinger G.R.S., Duranteau J., Chandel N.S., and Schumacker P.T. Hibernation during hypoxia in cardiomyocytes. J. Biol. Chem. 273 (1998) 3320-3326
12. Casey T.M., and Arthur P.G. Hibernation in non-contracting mammalian cardiomyocytes. Circulation 102 (2000) 3124-3129
13. Schumacker P.T., Chandel N., and Agusti A.G.N. Oxygen conformance of cellular respiration in hepatocytes. Am. J. Physiol. 265 (1993) L395-L402
14. Chandel N.S., Budinger G.R.S., Choe S.H., and Schumacker P.T. Cellular respiration during hypoxia. J. Biol. Chem. 272 (1997) 18808-18816
15. Munns S.E., Lui J.K., and Arthur P.G. Mitochondrial hydrogen peroxide production alters oxygen consumption in an oxygen-concentration-dependent manner. Free Radic. Biol. Med. 38 12 (2005 Jun 15) 1594-1603
16. Clementi E., Brown G.C., Foxwell N., and Moncada S. On the mechanism by which vascular endothelial cells regulate their oxygen consumption. Proc. Natl. Acad. Sci. 96 (1999) 1559-1562
17. Chandel N., Budinger G.R., Kemp R.A., and Schumacker P.T. Inhibition of cytochrome-c oxidase activity during prolonged hypoxia. Am. J. Physiol. 268 6 Pt 1 (1995 Jun) L918-L925
18. Hochachka P. Defense strategies against hypoxia and hypothermia. Science 231 (1986) 234-241
19. Gibbs C.L., and Loiselle D.S. Cardiac basal metabolism. Japanese Journal of Physiology 51 (2001) 399-426
20. Casey T.M., Pakay J.L., Guppy M., and Arthur P.G. Hypoxia causes downregulation of protein and RNA synthesis in noncontracting mammalian cardiomyocytes. Circ. Res. 90 7 (2002 Apr 19) 777-783
21. Cadenas E. Mitochondrial free radical production and cell signaling. Mol. Aspects. Med. 25 1-2 (2004 Feb-Apr) 17-26
22. Nulton-Persson A.C., and Szweda L.I. Modulation of mitochondrial function by hydrogen peroxide. J. Biol. Chem. 276 26 (2001 Jun 29) 23357-23361
23. Hool L.C., and Arthur P.G. Decreasing cellular hydrogen peroxide with catalase mimics the effects of hypoxia on the sensitivity of the L-type Ca2+ channel to beta-adrenergic receptor stimulation in cardiac myocytes. Circ. Res. 91 7 (2002 Oct 4) 601-609
24. Sayen M.R., Gustafsson A.B., Sussman M.A., Molkentin J.D., and Gottlieb R.A. Calcineurin transgenic mice have mitochondrial dysfunction and elevated superoxide production. Am. J. Physiol. 284 (2003) C562-C570
25. Lowry O.H., Rosebrough N.J., Farr A.L., and Randall R.J. Protein measurement with the Folin phenol reagent. J. Biol. Chem. 193 1 (1951 Nov) 265-275
26. Hool L.C., Di Maria C.A., Viola H.M., and Arthur P.G. Role of NAD(P)H oxidase in the regulation of cardiac L-type Ca2+ channel function during acute hypoxia. Cardiovasc. Res. 67 (2005) 624-635
27. Zhao H., Kalivendi S., Zhang H., Joseph J., Nithipatikom K., Vasquez-Vivar J., et al. Superoxide reacts with hydroethidine but forms a fluorescent product that is distinctly different from ethidium: potential implications in intracellular fluorescence detection of superoxide. Free Radic. Biol. Med. 34 11 (2003 Jun 1) 1359-1368
28. Trounce I.A., Kim Y.L., Jun A.S., and Wallace D.C. Assessment of mitochondrial oxidative phophorylation in patient biopsies, lymphoblasts, and transmitochondrial cell lines. Methods Enzymol. 24 (1996) 484-509
29. Suenaga M., Arakaki N., Morokami K., Himeda T., Shibata H., Kuwajima M., et al. Functional disorders of the oxidative phosphorylation system in the heart mitochondria of mice with juvenile visceral steatosis. Biol. Pharm. Bull. 26 3 (2003 Mar) 289-294
30. Turrens J.F. Superoxide production by the mitochondrial respiratory chain. Biosci. Rep. 17 (1997) 3-8
31. Talbot D.A., Lambert A.J., and Brand M.D. Production of endogenous matrix superoxide from mitochondrial complex I leads to activation of uncoupling protein 3. FEBS Lett. 556 1-3 (2004) 111-115
32. Arthur P.G., Ngo C.T., Moretta P., and Guppy M. Lack of oxygen sensing by mitochondria in platelets. Eur. J. Biochem. 266 1 (1999 Nov) 215-219
33. Xie Y.W., and Wolin M.S. Role of nitric oxide and its interaction with superoxide in the suppression of cardiac muscle mitochondrial respiration. Involvement in response to hypoxia/reoxygenation. Circulation 94 10 (1996 Nov 15) 2580-2586
34. Richter C., Gogvadze V., Laffranchi R., Schlapbach R., Schweizer M., Suter M., et al. Oxidants in mitochondria: from physiology to diseases. Biochim. Biophys. Acta 1271 1 (1995 May 24) 67-74
35. Papapostolou I., Patsoukis N., and Georgiou C.D. The fluorescence detection of superoxide radical using hydroethidine could be complicated by the presence of heme proteins. Anal. Biochem. 332 2 (2004 Sep 15) 290-298
36. Fernandez-Checa J.C., Kaplowitz N., Garcia-Ruiz C., Colell A., Miranda M., Mari M., et al. GSH transport in mitochondria: defense against TNF-induced oxidative stress and alcohol-induced defect. Am. J. Physiol. 273 1 Pt 1 (1997 Jul) G7-17
37. Vinogradov A.D., and Grivennikova V.G. Generation of superoxide-radical by the NADH:ubiquinone oxidoreductase of heart mitochondria. Biochemistry (Mosc) 70 2 (2005 Feb) 120-127
38. Hashimoto Y., Itoh K., Nishida K., Okano T., Miyazawa Y., and Okinaga K. Rapid superoxide production by endothelial cells and their injury upon reperfusion. J. Surg. Res. 57 6 (1994 Dec) 693-697
39. 2 modulate superoxide anion production in bovine cardiac myocytes: potential role of NADH oxidase. Circulation 96 (1997) 614-620
40. Eigel B.N., Gursahani H., and Hadley R.W. ROS are required for rapid reactivation of Na+/Ca2+ exchanger in hypoxic reoxygenated guinea pig ventricular myocytes. Am. J. Physiol. Heart Circ. Physiol. 286 3 (2004 Mar) H955-H963
41. Duranteau J., Chandel N.S., Kulisz A., Shao Z., and Schumacker P.T. Intracellular signaling by reactive oxygen species during hypoxia in cardiomyocytes. J. Biol. Chem. 273 (1998) 11619-11624
42. Chandel N.S., Maltepe E., Goldwasser E., Mathieu C.E., and Schumacker P.T. Mitochondrial reactive oxygen species trigger hypoxia induced transcription. Proc. Natl. Acad. Sci. 95 (1998) 11715-11720
43. Waypa G.B., Marks J.D., Mack M.M., Boriboun C., Mungai P.T., and Schumacker P.T. Mitochondrial reactive oxygen species trigger calcium increases during hypoxia in pulmonary arterial myocytes. Circ. Res. 91 (2002) 719-726
44. Yano H., Kuroda S., and Buchanan B.B. Disulfide proteome in the analysis of protein function and structure. Proteomics 2 9 (2002) 1090-1096
45. Kotlyar A.B., and Vinogradov A.D. Slow active/inactive transition of the mitochondrial NADH-ubiquinone reductase. Biochim. Biophys. Acta 1019 2 (1990) 151-158
46. Grivennikova V.G., Kapustin A.N., and Vinogradov A.D. Catalytic activity of NADH-ubiquinone oxidoreductase (complex I) in intact mitochondria. evidence for the slow active/inactive transition. J. Biol. Chem. 276 12 (2001 Mar 23) 9038-9044
47. Lee K., and Esselman W.J. Inhibition of PTPs by H(2)O(2) regulates the activation of distinct MAPK pathways. Free Radic. Biol. Med. 33 8 (2002 Oct 15) 1121-1132
48. Purdom S., and Chen Q.M. Epidermal growth factor receptor-dependent and -independent pathways in hydrogen peroxide-induced mitogen-activated protein kinase activation in cardiomyocytes and heart fibroblasts. J. Pharmacol. Exp. Ther. 312 3 (2005 Mar) 1179-1186
49. Bhat N.R., and Zhang P. Hydrogen peroxide activation of multiple mitogen-activated protein kinases in an oligodendrocyte cell line: role of extracellular signal-regulated kinase in hydrogen peroxide-induced cell death. J. Neurochem. 72 1 (1999 Jan) 112-119
50. Preston T.J., Muller W.J., and Singh G. Scavenging of extracellular H2O2 by catalase inhibits the proliferation of HER-2/Neu-transformed rat-1 fibroblasts through the induction of a stress response. J. Biol. Chem. 276 12 (2001 Mar 23) 9558-9564
51. Cantin A.M., Larivee P., and Begin R.O. Extracellular glutathione suppresses human lung fibroblast proliferation. Am. J. Respir. Cell Mol. Biol. 3 1 (1990 Jul) 79-85
52. Snabaitis A.K., Hearse D.J., and Avkiran M. Regulation of sarcolemmal Na(+)/H(+) exchange by hydrogen peroxide in adult rat ventricular myocytes. Cardiovasc. Res. 53 2 (2002 Feb 1) 470-480