Reactive oxygen species production in energized cardiac mitochondria during hypoxia/reoxygenation: Modulation by nitric oxide

Circulation Research

Volumn 103, Issue 8, 2008, Pages 873-880

  Korge, Paavo ^a   Ping, Peipei ^a   Weiss, James N ^a  

^a UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

Hypoxia reoxygenation; Mitochondria; Nitric oxide; Reactive oxygen species

Indexed keywords

ACONITATE HYDRATASE; CITRININ; HYDROGEN PEROXIDE; HYDROXYL GROUP; IRON; NITRIC OXIDE; REACTIVE OXYGEN METABOLITE; REDUCED NICOTINAMIDE ADENINE DINUCLEOTIDE; 2',7'-DICHLORODIHYDROFLUORESCEIN; DICHLORODIHYDROFLUORESCEIN; FLUORESCEIN DERIVATIVE; GLUTATHIONE; NICOTINAMIDE ADENINE DINUCLEOTIDE; OXYGEN;

ANIMAL TISSUE; ANOXIA; ARTICLE; AUTOFLUORESCENCE; CONTROLLED STUDY; ELECTRON TRANSPORT; ENZYME ACTIVITY; HEART MITOCHONDRION; HEART MUSCLE ISCHEMIA; HEART PROTECTION; HYPOXIA; MEMBRANE POTENTIAL; NONHUMAN; OXIDATION; PRIORITY JOURNAL; REOXYGENATION; REPERFUSION INJURY; RESPIRATORY CHAIN; ANIMAL; CELL HYPOXIA; CELL RESPIRATION; ENZYMOLOGY; HEART MUSCLE; METABOLISM; MITOCHONDRIAL MEMBRANE POTENTIAL; OXIDATION REDUCTION REACTION; OXYGEN CONSUMPTION; RABBIT; SIGNAL TRANSDUCTION; TIME;

ACONITATE HYDRATASE; ANIMALS; CELL HYPOXIA; CELL RESPIRATION; ELECTRON TRANSPORT; FLUORESCEINS; GLUTATHIONE; HYDROGEN PEROXIDE; IRON; MEMBRANE POTENTIAL, MITOCHONDRIAL; MITOCHONDRIA, HEART; MYOCARDIAL REPERFUSION INJURY; MYOCARDIUM; NAD; NITRIC OXIDE; OXIDATION-REDUCTION; OXYGEN; OXYGEN CONSUMPTION; RABBITS; REACTIVE OXYGEN SPECIES; SIGNAL TRANSDUCTION; TIME FACTORS;

EID: 54449083292     PISSN: 00097330     EISSN: 15244571     Source Type: Journal    
DOI: 10.1161/CIRCRESAHA.108.180869     Document Type: Article

References (35)

1. Zweier JL, Talukder MA. The role of oxidants and free radicals in reperfusion injury. Cardiovasc Res. 2006;70:181-190.
2. Yellon DM, Downey JM. Preconditioning the myocardium: from cellular physiology to clinical cardiology. Physiol Rev. 2003;83:1113-1151.
3. Jezek P, Hlavata L. Mitochondria in homeostasis of reactive oxygen species in cell, tissues, and organism. Int J Biochem Cell Biol. 2005;37: 2478-2503.
4. Andrukhiv A, Costa AD, West IC, Garlid KD. Opening mitoKATP increases superoxide generation from complex I of the electron transport chain. Am J Physiol Heart Circ Physiol. 2006;291:H2067-H2074.
5. Vanden Hoek TL, Becker LB, Shao Z, Li C, Schumacker PT. Reactive oxygen species released from mitochondria during brief hypoxia induce preconditioning in cardiomyocytes. J Biol Chem. 1998;273: 18092-18098.
6. Vanden Hoek T, Becker LB, Shao ZH, Li CQ, Schumacker PT. Preconditioning in cardiomyocytes protects by attenuating oxidant stress at reperfusion. Circ Res. 2000;86:541-548.
7. Chen Q, Moghaddas S, Hoppel CL, Lesnefsky EJ. Ischemic defects in the electron transport chain increase the production of reactive oxygen species from isolated rat heart mitochondria. Am J Physiol Cell Physiol. 2008;294:C460-C466.
8. Jones SP, Bolli R. The ubiquitous role of nitric oxide in cardioprotection. J Mol Cell Cardiol. 2006;40:16-23.
9. Korge P, Honda HM, Weiss JN. Regulation of the mitochondrial permeability transition by matrix Ca(2 + ) and voltage during anoxia/reoxygen-ation. Am J Physiol Cell Physiol. 2001;280:C517-C526.
10. Robinson KM, Janes MS, Pehar M, Monette JS, Ross MF, Hagen TM, Murphy MP, Beckman JS. Selective fluorescent imaging of superoxide in vivo using ethidium-based probes. Proc Natl Acad Sci USA. 2006;103: 15038-15043.
11. Esposito BP, Epsztejn S, Breuer W, Cabantchik ZI. A review of fluorescence methods for assessing labile iron in cells and biological fluids. Anal Biochem. 2002;304:1-18.
12. Gostimskaya IS, Grivennikova VG, Zharova TV, Bakeeva LE, Vinogradov AD. In situ assay of the intramitochondrial enzymes: use of alamethicin for permeabilization of mitochondria. Anal Biochem. 2003; 313:46-52.
13. Gnaiger E. Bioenergetics at low oxygen: dependence of respiration and phosphorylation on oxygen and adenosine diphosphate supply. Respir Physiol. 2001;128:277-297.
14. Wrona M, Patel KB, Wardman P. The roles of thiol-derived radicals in the use of 2',7'-dichlorodihydrofluorescein as aprobe for oxidative stress. Free Radic Biol Med. 2008;44:56-62.
15. Cohen MV, Yang XM, Downey JM. Nitric oxide is a preconditioning mimetic and cardioprotectant and is the basis of many available infarct-sparing strategies. Cardiovasc Res. 2006;70:231-239.
16. Wink DA, Hanbauer I, Krishna MC, DeGeaff W, Gamson J, Mitchell JB. Nitric oxide protects against cellular damage and cytotoxicity from reactive oxygen species. Proc Natl Acad Sci USA. 1993;90:9813-9817.
17. Chang J, Rao NV, Markewitz BA, Hoidal JR, Michael JR. Nitric oxide donor prevents hydrogen peroxide-mediated endothelial cell injury. Am J Physiol. 1996;270:L931-L940.
18. Lu C, Koppenol WH. Inhibition of the Fenton reaction by nitrogen monoxide. J Biol Inorg Chem. 2005;10:732-738.
19. Graf E, Mahoney JR, Bryant RG, Eaton JW. Iron-catalyzed hydroxyl radical formation. Stringent requirement for free iron coordination site. J Biol Chem. 1984;259:3620-3624.
20. Bulteau AL, Ikeda-Saito M, Szweda LI. Redox-dependent modulation of aconitase activity in intact mitochondria. Biochemistry. 2003;42: 14846-14855.
21. Bulteau AL, Lundberg KC, Ikeda-Saito M, Isaya G, Szweda LI. Reversible redox-dependent modulation of mitochondrial aconitase and proteolytic activity during in vivo cardiac ischemia/reperfusion. Proc Natl Acad Sci U S A. 2005;102:5987-5991.
22. Richardson DR, Lok HC. The nitric oxide-iron interplay in mammalian cells: transport and storage of dinitrosyl iron complexes. Biochim Biophys Acta. 2008;1780:638-651.
23. Robin E, Guzy RD, Loor G, Iwase H, Waypa GB, Marks JP, Hoek TJ, Schumacker PT. Oxidant stress during simulated ischemia primes cardio-myocytes for cell death during reperfusion. J Biol Chem. 2007;282: 19133-19143. (Pubitemid 47100157)
24. Lesnefsky EJ, Moghaddas S, Tandler B, Kerner J, Hoppel CL. Mito-chondrial dysfunction in cardiac disease: ischemia-reperfusion, aging, and heart failure. J Mol Cell Cardiol. 2001;33:1065-1089.
25. Jang S, Imlay JA. Micromolar intracellular hydrogen peroxide disrupts metabolism by damaging iron-sulfur enzymes. J Biol Chem. 2007;282: 929-937.
26. Costa AD, Pierre SV, Cohen MV, Downey JM, Garlid KD. cGMP signalling in pre-and post-conditioning: the role of mitochondria. Cardiovasc Res. 2008;77:344-352.
27. Lizasoain I, Moro MA, Knowles RG, Darley-Usmar V, Moncada S. Nitric oxide and peroxynitrite exert distinct effects on mitochondrial respiration which are differentially blocked by glutathione or glucose. Biochem J. 1996;314:877-880.
28. Tarpey MM, Fridovich I. Methods of detection of vascular reactive species: nitric oxide, superoxide, hydrogen peroxide, and peroxynitrite. Circ Res. 2001;89:224-236.
29. Nadtochiy SM, Burwell LS, Brookes PS. Cardioprotection and mito-chondrial S-nitrosation: effects of S-nitroso-2-mercaptopropionyl glycine (SNO-MPG) in cardiac ischemia-reperfusion injury. J Mol Cell Cardiol. 2007;42:812-825.
30. Shiva S, Sack MN, Greer JJ, Durbanski M, Ringwood LA, Burwell L, Wang X, MacArthur PH, Shoja A, Raghavarchari N, Calvert JW, Brooks PS, Lefer DJ, Gladwin MT. Nitrite augments tolerance to ischemia/ reperfusion injury via the modulation of mitochondrial electron transfer. J Exp Med. 2007;204:2089-2102.
31. Whiteman M, Chua YL, Zhang D, Duan W, Lion YC, Armstrong JS. Nitric oxide protects against mitochondrial permeabilization induced by glutathione depletion: role of S-nitrosylation? Biochem Biophys Res Commun. 2006;339:255-262.
32. Costa AD, Garlid KD. Intramitochondrial signaling: interactions among mitoKATP, PKC{varepsilon}, ROS, and MPT. Am J Physiol Heart Circ Physiol. 2008;295:H874-H882.
33. Wardman P. Fluorescent and luminescent probes for measurement of oxidative and nitrosative species in cells and tissues: progress, pitfalls, and prospects. Free Radic Biol Med. 2007;43:995-1022.
34. Dunn LL, Rahmanto YS, Richardson DR. Iron uptake and metabolism in the new millennium. Trends in Cell Biol. 2006;17:93-100.
35. Burkitt MJ, Wardman P. Cytochrome C is a potent catalyst of dichlo-rofluorescin oxidation: implications for the role of reactive oxygen species in apoptosis. Biochem Biophys Res Commun. 2001;282:329-333