Poly(ADP-ribose) polymerase-1 hyperactivation and impairment of mitochondrial respiratory chain complex I function in reperfused mouse hearts

American Journal of Physiology - Heart and Circulatory Physiology

Volumn 291, Issue 2, 2006, Pages

  Zhou, Hui Zhong ^a,c   Swanson, Raymond A ^a,c   Simonis, Ursula ^d   Ma, Xiaokui ^c   Cecchini, Gary ^a,c   Gray, Mary O ^a,b,c,e  

^a UNIVERSITY OF CALIFORNIA   (United States)

^b UNIVERSITY OF CALIFORNIA   (United States)

^c SAN FRANCISCO VETERANS AFFAIRS MEDICAL CENTER   (United States)

^d SAN FRANCISCO STATE UNIVERSITY   (United States)

^e SAN FRANCISCO GENERAL HOSPITAL   (United States)

Author keywords

Energetics; Glycolysis; Metabolism; Oxidative stress

Indexed keywords

ALLOPURINOL; ANTIOXIDANT; NICOTINAMIDE ADENINE DINUCLEOTIDE ADENOSINE DIPHOSPHATE RIBOSYLTRANSFERASE; POLY(ADENOSINE DIPHOSPHATE RIBOSE)POLYMERASE 1 ENZYME; PROTEIN MITOCHONDRIAL RESPIRATORY COMPLEX 1; REDUCED NICOTINAMIDE ADENINE DINUCLEOTIDE DEHYDROGENASE; REDUCED NICOTINAMIDE ADENINE DINUCLEOTIDE DEHYDROGENASE (UBIQUINONE); TIOPRONIN; UNCLASSIFIED DRUG; XANTHINE OXIDASE INHIBITOR;

ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; CONTROLLED STUDY; ENZYME ACTIVATION; ENZYME ACTIVITY; ENZYME INHIBITION; GENE DISRUPTION; HEART CONTRACTION; HEART MUSCLE CONTRACTILITY; HEART MUSCLE REPERFUSION; HEART PROTECTION; KNOCKOUT MOUSE; NONHUMAN; PRIORITY JOURNAL; PROTEIN FUNCTION; RAT;

ADENOSINE DIPHOSPHATE RIBOSE; ANIMALS; CREATINE KINASE; ELECTRON TRANSPORT; ENZYME ACTIVATION; HEMODYNAMIC PROCESSES; ISCHEMIC PRECONDITIONING, MYOCARDIAL; LIPID PEROXIDATION; MALE; MICE; MICE, INBRED C57BL; MICE, KNOCKOUT; MITOCHONDRIA, HEART; MYOCARDIAL CONTRACTION; MYOCARDIAL INFARCTION; MYOCARDIAL REPERFUSION; MYOCARDIUM; ORGAN SIZE; POLY(ADP-RIBOSE) POLYMERASES; SIGNAL TRANSDUCTION;

EID: 33746806606     PISSN: 03636135     EISSN: 15221539     Source Type: Journal    
DOI: 10.1152/ajpheart.00823.2005     Document Type: Article

References (37)

1. Chauvin C, De Oliveira F, Ronot X, Mousseau M, Leverve X, and Fontaine E. Rotenone inhibits the mitochondrial permeability transition-induced cell death in U937 and KB cells. J Biol Chem 276: 41394-41398, 2001.
2. + and is a causative event in the death of myocytes in postischemic reperfusion of the heart. J Biol Chem 276: 2571-2575, 2001.
3. + depletion and cell death by oxidative stress. J Biol Chem 278: 18426-18433, 2003.
4. Fontaine E, Eriksson O, Ichas F, and Bernardi P. Regulation of the permeability transition pore in skeletal muscle mitochondria: modulation by electron flow through the respiratory chain complex I. J Biol Chem 273: 12662-12668, 1998.
5. Gray MO, Zhou HZ, Schafhalter-Zoppoth I, Zhu P, Mochly-Rosen D, and Messing RO. Preservation of baseline hemodynamic function and loss of inducible cardioprotection in mice lacking protein kinase C ε. J Biol Chem 279: 3596-3604, 2004.
6. Grupp IL, Jackson TM, Hake P, Grupp G, and Szabó C. Protection against hypoxia-reoxygenation in the absence of poly (ADP-ribose) synthetase in isolated working hearts. J Mol Cell Cardiol 31: 297-303, 1999.
7. Halmosi R, Berente Z, Osz E, Toth K, Literati-Nagy P, and Sumegi B. Effect of poly(ADP-ribose) polymerase inhibitors on the ischemia-reperfusion- induced oxidative cell damage and mitochondrial metabolism in Langendorff heart perfusion system. Mol Pharmacol 59: 1497-1505, 2001.
8. Han D, Canali R, Rettori D, and Kaplowitz N. Effect of glutathione depletion on sites and topology of superoxide and hydrogen peroxide production in mitochondria. Mol Pharmacol 64: 1136-1144, 2003.
9. Hardy L, Clark JB, Darley-Usmar VM, Smith DR, and Stone D. Reoxygenation-dependent decrease in mitochondrial NADH:CoQ reductase (complex I) activity in the hypoxic/reoxygenated rat heart. Biochem J 274: 133-137, 1991.
10. Ikai K and Ueda K. Immunohistochemical demonstration of poly(adenosine diphosphate-ribose) synthetase in bovine tissues. J Histochem Cytochem 31: 1261-1264, 1983.
11. Kerbey AL, Randle PJ, Cooper RH, Whitehouse S, Pask HT, and Denton RM. Regulation of pyruvate dehydrogenase. Biochem J 154: 327-348, 1976.
12. Kudej RK, White LT, Kudej AB, Vatner SF, and Lewandowski ED. Brief increase in carbohydrate oxidation after reperfusion reverses myocardial stunning in conscious pigs. Circulation 106: 2836-2841, 2002.
13. Liaudet L, Yang Z, Al-Affar EB, and Szabó C. Myocardial ischemic preconditioning in rodents is dependent on poly(ADP-ribose) synthetase. Mol Med 7: 406-417, 2001.
14. Maklashina E, Sher Y, Zhou HZ, Gray MO, Karliner JS, and Cecchini G. Effect of anoxia/reperfusion on the reversible active/deactive transition of NADH-ubiquinone oxidoreductase (complex I) in rat heart. Biochim Biophys Acta 1556: 6-12, 2002.
15. Ohkawa H, Ohishi N, and Yagi K. Assay for lipid peroxides in animal tissues by thiobarbituric acid reaction. Anal Biochem 95: 351-358, 1979.
16. Pálfi A, Tóth A, Kulcsár G, Hantó K, Deres P, Bartha E, Halmosi R, Szabados E, Czopf L, Kálai T, Hideg K, Sümegi B, and Tóth K. The role of Akt and mitogen-activated protein kinase systems in protective effect of poly(ADP-ribose) polymerase inhibition in Langendorff perfused and in isoproterenol-damaged rat hearts. J Pharmacol Exp Ther 315: 273-282, 2005.
17. Paradies G, Petrosillo G, Pistolese M, Di Venosa N, Federici A, and Ruggiero F. Decrease in mitochondrial complex I activity in ischemic/reperfused rat heart: involvement of reactive oxygen species and cardiolipin. Circ Res 94: 53-59, 2004.
18. Pieper AA, Walles T, Wei G, Clements EE, Verma A, Snyder SH, and Zweier JL. Myocardial postischemic injury is reduced by polyADPribose polymerase-1 gene disruption. Mol Med 6: 271-282, 2000.
19. Raha S, Myint AT, Johnstone L, and Robinson BH. Control of oxygen free radical formation from mitochondrial complex I: roles for protein kinase A and pyruvate dehydrogenase kinase. Free Radic Biol Med 32: 421-430, 2002.
20. Satoh MS and Lindahl T. Role of poly(ADP-ribose) formation in DNA repair. Nature 356: 356-358, 1992.
21. Sheline CT, Behrens MM, and Choi DW. Zinc-induced cortical neuronal death: contribution of energy failure attributable to loss of NAD(+) and inhibition of glycolysis. J Neurosci 20: 3139-3146, 2000.
22. Szabados E, Literati-Nagy P, Farkas B, and Sumegi B. BGP-15, a nicotinic amidoxime derivate protecting heart from ischemia reperfusion injury through modulation of poly(ADP-ribose) polymerase. Biochem Pharmacol 59: 937-945, 2000.
23. Szabó G, Liaudet L, Hagl S, and Szabó C. Poly(ADP-ribose) polymerase activation in the reperfused myocardium. Cardiovasc Res 61: 471-480, 2004.
24. Tapodi A, Debreceni B, Hanto K, Bognar Z, Wittmann I, Gallyas F, Varbiro G, and Sumegi B. Pivotal role of Akt activation in mitochondrial protection and cell survival by poly(ADP-ribose)polymerase-1 inhibition in oxidative stress. J Biol Chem 280: 35767-35775, 2005.
25. Thiemermann C, Bowes J, Myint FP, and Vane JR. Inhibition of the activity of poly(ADP-ribose) synthetase reduces ischemia-reperfusion injury in the heart and skeletal muscle. Proc Natl Acad Sci USA 94: 679-683, 1997.
26. Veitch K, Hombroeckx A, Caucheteux D, Pouleur H, and Hue L. Global ischemia induces a biphasic response of the mitochondrial respiratory chain: anoxic pre-perfusion protects against ischaemic damage. Biochem J 281: 709-715, 1992.
27. Vinogradov AD. Catalytic properties of the mitochondrial NADH-ubiquinone oxidoreductase (complex I) and the pseudo-reversible active/inactive enzyme transition. Biochim Biophys Acta 1364: 169-185, 1998.
28. Virág L, Salzman AL, and Szabó C. Poly(ADP-ribose) synthetase activation mediates mitochondrial injury during oxidant-induced cell death. J Immunol 161: 3753-3759, 1998.
29. Wang ZQ, Auer B, Stingl L, Berghammer H, Haidacher D, Schweiger M, and Wagner EF. Mice lacking ADPRT and poly(ADP-ribosyl)ation develop normally but are susceptible to skin disease. Genes Dev 9: 509-520, 1995.
30. Weiss JN, Korge P, Honda HM, and Ping P. Role of the mitochondrial permeability transition in myocardial disease. Circ Res 93: 292-301, 2003.
31. Ying W, Chen Y, Alano CC, and Swanson RA. Tricarboxylic acid cycle substrates prevent PARP-mediated death of neurons and astrocytes. J Cereb Blood Flow Metab 22: 774-779, 2002.
32. Ying W, Sevigny MB, Chen Y, and Swanson RA. Poly(ADP-ribose) glycohydrolase mediates oxidative and excitotoxic neuronal death. Proc Natl Acad Sci USA 98: 12227-12232, 2001.
33. Zhou HZ, Karliner JS, and Gray MO. Moderate alcohol consumption induces sustained cardioprotection by activating PKC-ε and Akt. Am J Physiol Heart Circ Physiol 283: H165-H174, 2002.
34. Zingarelli B, Cuzzocrea S, Zsengeller Z, Salzman AL, and Szabó C. Protection against myocardial ischemia and reperfusion injury by 3-aminobenzamide, an inhibitor of poly(ADP-ribose) synthetase. Cardiovasc Res 36: 205-215, 1997.
35. Zingarelli B, Hake PW, O'Connor M, Denenberg A, Kong S, and Aronow BJ. Absence of poly(ADP-ribose) polymerase-1 alters nuclear factor-κB activation and gene expression of apoptosis regulators after reperfusion injury. Mol Med 9: 5-8, 2003.
36. Zingarelli B, Hake PW, O'Connor M, Denenberg A, Wong HR, Kong S, and Aronow BJ. Differential regulation of activator protein-1 and heat shock factor-1 in myocardial ischemia and reperfusion injury: role of poly(ADP-ribose) polymerase-1. Am J Physiol Heart Circ Physiol 286: H1408-H1415, 2004.
37. Zingarelli B, Salzman AL, and Szabó C. Genetic disruption of poly (ADP-ribose) synthetase inhibits the expression of P-selectin and intercellular adhesion molecule-1 in myocardial ischemia/reperfusion injury. Circ Res 83: 85-94, 1998.