Oxidative stress, mitochondrial permeability transition pore opening and cell death during hypoxia-reoxygenation in adult cardiomyocytes

European Journal of Pharmacology

Volumn 675, Issue 1-3, 2012, Pages 6-14

  Assaly, Rana ^a,b   De Tassigny, Alexandra D'Anglemont ^a,b   Paradis, Stéphanie ^a,b   Jacquin, Sophie ^a,b   Berdeaux, Alain ^a,b   Morin, Didier ^a,b  

^a FACULTÉ DE MÉDECINE   (France)

^b UNIVERSITÉ PARIS EST CRÉTEIL   (France)

Author keywords

Adult cardiomyocytes; Hypoxia reoxygenation; Mitochondria; Permeability transition pore; Reactive oxygen species

Indexed keywords

CALCEIN; COBALT CHLORIDE; CYCLOPHILIN D; CYCLOSPORIN A; HYDROGEN PEROXIDE; HYDROXYL GROUP; MITOCHONDRIAL PERMEABILITY TRANSITION PORE; REACTIVE OXYGEN METABOLITE;

ANIMAL CELL; ANTIOXIDANT ACTIVITY; ARTICLE; CELL DEATH; CELL ISOLATION; CELL MEMBRANE PERMEABILITY; CELL VIABILITY; CONTROLLED STUDY; DISEASE DURATION; FLUORESCENCE ANALYSIS; HEART MUSCLE CELL; HYPOXIA; MALE; MITOCHONDRION; NONHUMAN; OXIDATIVE STRESS; PRIORITY JOURNAL; RAT; REOXYGENATION;

ANIMALS; ANTIOXIDANTS; CELL DEATH; CELL HYPOXIA; CELL SURVIVAL; CELLS, CULTURED; CYCLOSPORINE; HYDROGEN PEROXIDE; HYDROXYL RADICAL; KINETICS; MALE; MEMBRANE TRANSPORT MODULATORS; MITOCHONDRIAL MEMBRANE TRANSPORT PROTEINS; MYOCARDIAL REPERFUSION INJURY; MYOCYTES, CARDIAC; OXIDATIVE STRESS; RATS; RATS, WISTAR; REACTIVE OXYGEN SPECIES; SUPEROXIDES;

EID: 84855439552     PISSN: 00142999     EISSN: 18790712     Source Type: Journal    
DOI: 10.1016/j.ejphar.2011.11.036     Document Type: Article

References (53)

1. V.J. Adlam, J.C. Harrison, C.M. Porteous, A.M. James, R.A. Smith, M.P. Murphy, and I.A. Sammut Targeting an antioxidant to mitochondria decreases cardiac ischemia-reperfusion injury FASEB J. 19 2005 1088 1095 (Pubitemid 40946434)
2. G. Ambrosio, J.L. Zweier, C. Duilio, P. Kuppusamy, G. Santoro, P.P. Elia, I. Tritto, P. Cirillo, M. Condorelli, M. Chiariello, and J.T. Flaherty Evidence that mitochondrial respiration is a source of potentially toxic oxygen free radicals in intact rabbit hearts subjected to ischemia and reflow J. Biol. Chem. 268 1993 18532 18541 (Pubitemid 23273786)
3. L.B. Becker New concepts in reactive oxygen species and cardiovascular reperfusion physiology Cardiovasc. Res. 61 2004 461 470 (Pubitemid 38210152)
4. L.B. Becker, T.L. Vanden Hoek, Z.H. Shao, C.Q. Li, and P.T. Schumacker Generation of superoxide in cardiomyocytes during ischemia before reperfusion Am. J. Physiol. 277 1999 H2240 H2246 (Pubitemid 30048143)
5. R. Bolli, B.S. Patel, M.O. Jeroudi, E.K. Lai, and P.B. McCay Demonstration of free radical generation in "stunned" myocardium of intact dogs with the use of the spin trap alpha-phenyl N-tert-butyl nitrone J. Clin. Invest. 82 1998 476 485
6. C. Ceconi, P. Bernocchi, A. Boraso, A. Cargnoni, P. Pepi, S. Curello, and R. Ferrari New insights on myocardial pyridine nucleotides and thiol redox state in ischemia and reperfusion damage Cardiovasc. Res. 47 2000 586 594 (Pubitemid 30646080)
7. F. Di Lisa, and P.A. Bernardi CaPful of mechanisms regulating the mitochondrial permeability transition J. Mol. Cell. Cardiol. 46 2009 775 780
8. F. Di Lisa, M. Canton, R. Menabo, N. Kaludercic, and P. Bernardi Mitochondria and cardioprotection Heart Fail. Rev. 12 2007 249 260 (Pubitemid 350176698)
9. S. Dikalov, V. Khramtsov, and G. Zimmer Determination of rate constants of the reactions of thiols with superoxide radical by electron paramagnetic resonance: critical remarks on spectrophotometric approaches Arch. Biochem. Biophys. 326 1996 207 218 (Pubitemid 26060135)
10. S. Dikalov, K.K. Griendling, and D.G. Harrison Measurement of reactive oxygen species in cardiovascular studies Hypertension 49 2007 717 727 (Pubitemid 351688335)
11. J. Duranteau, N.S. Chandel, A. Kulisz, Z. Shao, and P.T. Schumacker Intracellular signaling by reactive oxygen species during hypoxia in cardiomyocytes J. Biol. Chem. 273 1998 11619 11624 (Pubitemid 28272061)
12. D. Farbstein, A. Kozak-Blickstein, and A.P. Levy Antioxidant vitamins and their use in preventing cardiovascular disease Molecules 15 2010 8098 8110
13. J.T. Flaherty, and M.L. Weisfeldt Reperfusion injury Free Radic. Biol. Med. 5 1998 409 419
14. T.P. Geisbuhler, and M.J. Rovetto Lactate does not enhance anoxia/reoxygenation damage in adult rat cardiac myocytes J. Mol. Cell. Cardiol. 22 1990 1325 1335
15. T. Geisbuhler, R.A. Altschuld, R.W. Trewyn, A.Z. Ansel, K. Lamka, and G.P. Brierley Adenine nucleotide metabolism and compartmentalization in isolated adult rat heart cells Circ. Res. 54 1984 536 546 (Pubitemid 14112737)
16. E.J. Griffiths, C.J. Ocampo, J.S. Savage, M.D. Stern, and H.S. Silverman Protective effects of low and high doses of cyclosporin A against reoxygenation injury in isolated rat cardiomyocytes are associated with differential effects on mitochondrial calcium levels Cell Calcium 27 2000 87 95 (Pubitemid 30150797)
17. C. Guarnieri, F. Flamigni, and C.M. Caldarera Role of oxygen in the cellular damage induced by re-oxygenation of hypoxic heart J. Mol. Cell. Cardiol. 12 1980 797 808 (Pubitemid 10056520)
18. A.P. Halestrap What is the mitochondrial permeability transition pore? J. Mol. Cell. Cardiol. 46 2009 821 831
19. A.P. Halestrap, S.J. Clarke, and S.A. Javadov Mitochondrial permeability transition pore opening during myocardial reperfusion - a target for cardioprotection Cardiovasc. Res. 61 2004 372 385 (Pubitemid 38210145)
20. D.J. Hausenloy, D.M. Yellon, S. Mani-Babu, and M.R. Duchen Preconditioning protects by inhibiting the mitochondrial permeability transition Am. J. Physiol. Heart Circ. Physiol. 287 2004 H841 H849 (Pubitemid 38955321)
21. R.A. Haworth, D.R. Hunter, H.A. Berkoff, and R.L. Moss Metabolic cost of the stimulated beating of isolated adult rat heart cells in suspension Circ. Res. 52 1983 342 351 (Pubitemid 13158750)
22. S.A. Javadov, S. Clarke, M. Das, E.J. Griffiths, K.H. Lim, and A.P. Halestrap Ischaemic preconditioning inhibits opening of mitochondrial permeability transition pores in the reperfused rat heart J. Physiol. 549 2003 513 524 (Pubitemid 36701762)
23. J.S. Kim, Y. Jin, and J.J. Lemasters Reactive oxygen species, but not Ca2 + overloading, trigger pH- and mitochondrial permeability transition-dependent death of adult rat myocytes after ischemia-reperfusion Am. J. Physiol. Heart Circ. Physiol. 290 2006 H2024 H2034
24. A.J. Kowaltowski, R.F. Castilho, and A.E. Vercesi Mitochondrial permeability transition and oxidative stress FEBS Lett. 495 2001 12 15 (Pubitemid 32367965)
25. Y.T. Lam, M.T. Aung-Htut, Y.L. Lim, H. Yang, and I.W. Dawes Changes in reactive oxygen species begin early during replicative aging of Saccharomyces cerevisiae cells Free Radic. Biol. Med. 50 2011 963 970
26. F. Laurindo, D.C. Fernandes, and C.X. Santos Assessment of superoxide production and NADPH oxidase activity by HPLC analysis of dihydroethidium oxidation products Methods Enzymol. 441 2008 237 260
27. J.J. Lemasters, J. DiGuiseppi, A.L. Nieminen, and B. Herman Blebbing, free Ca2 + and mitochondrial membrane potential preceding cell death in hepatocytes Nature 325 1987 78 81 (Pubitemid 17059475)
28. L. Lorgis, M. Zeller, G. Dentan, P. Sicard, C. Richard, P. Buffet, I. L'Huillier, J.C. Beer, Y. Cottin, L. Rochette, and C. Vergely The free oxygen radicals test (FORT) to assess circulating oxidative stress in patients with acute myocardial infarction Atherosclerosis 213 2010 616 621
29. D. Morin, R. Assaly, S. Paradis, and A. Berdeaux Inhibition of mitochondrial membrane permeability as a putative pharmacological target for cardioprotection Curr. Med. Chem. 16 2009 4382 4398
30. E. Murphy, and C. Steenbergen Mechanisms underlying acute protection from cardiac ischemia-reperfusion injury Physiol. Rev. 88 2008 581 609 (Pubitemid 351520088)
31. F.N. Obame, C. Plin-Mercier, R. Assaly, R. Zini, J.L. Dubois-Rande, A. Berdeaux, and D. Morin Cardioprotective effect of morphine and a blocker of glycogen synthase kinase 3 beta, SB216763 [3-(2,4-dichlorophenyl)-4(1-methyl-1H- indol-3-yl)-1H-pyrrole-2,5-dione], via inhibition of the mitochondrial permeability transition pore J. Pharmacol. Exp. Ther. 326 2008 252 258 (Pubitemid 351872117)
32. L.H. Opie Reperfusion injury and its pharmacologic modification Circulation 80 1989 1049 1062 (Pubitemid 19261653)
33. M. Ovize, G.F. Baxter, F. Di Lisa, P. Ferdinandy, D. Garcia-Dorado, D.J. Hausenloy, G. Heusch, J. Vinten-Johansen, D.M. Yellon, and R. Schulz Postconditioning and protection from reperfusion injury: where do we stand? Position paper from the Working Group of Cellular Biology of the Heart of the European Society of Cardiology Cardiovasc. Res. 87 2010 406 423
34. S.S. Park, H. Zhao, R.A. Mueller, and Z. Xu Bradykinin prevents reperfusion injury by targeting mitochondrial permeability transition pore through glycogen synthase kinase 3beta J. Mol. Cell. Cardiol. 40 2006 708 716
35. K.M. Peterson, A. Aly, A. Lerman, L.O. Lerman, and M. Rodriguez-Porcel Improved survival of mesenchymal stromal cell after hypoxia preconditioning: role of oxidative stress Life Sci. 88 2011 65 73
36. V. Petronilli, G. Miotto, M. Canton, M. Brini, R. Colonna, P. Bernardi, and F. Di Lisa Transient and long-lasting openings of the mitochondrial permeability transition pore can be monitored directly in intact cells by changes in mitochondrial calcein fluorescence Biophys. J. 76 1999 725 734 (Pubitemid 29264555)
37. H.M. Piper, Y. Abdallah, and C. Schafer The first minutes of reperfusion: a window of opportunity for cardioprotection Cardiovasc. Res. 61 2004 365 371 (Pubitemid 38210144)
38. C. Poizat, C. Keriel, and P. Cuchet Is oxygen supply sufficient to induce normoxic conditions in isolated rat heart? Basic Res. Cardiol. 89 1994 535 844
39. H. Possel, H. Noack, W. Augustin, G. Keilhoff, and G. Wolf 2,7-Dihydrodichlorofluorescein diacetate as a fluorescent marker for peroxynitrite formation FEBS Lett. 416 1997 175 178 (Pubitemid 27462782)
40. M.L. Riess, A.K. Camara, L.G. Kevin, J. An, and D.F. Stowe Reduced reactive O2 species formation and preserved mitochondrial NADH and [Ca2 +] levels during short-term 17 degrees C ischemia in intact hearts Cardiovasc. Res. 61 2004 580 590 (Pubitemid 38210163)
41. E. Robin, R.D. Guzy, G. Loor, H. Iwase, G.B. Waypa, J.D. Marks, T.L. Hoek, and P.T. Schumacker Oxidant stress during simulated ischemia primes cardiomyocytes for cell death during reperfusion J. Biol. Chem. 282 2007 19133 19143 (Pubitemid 47100157)
42. M. Ruiz-Meana, A. Abellan, E. Miro-Casas, and D. Garcia-Dorado Opening of mitochondrial permeability transition pore induces hypercontracture in Ca2 + overloaded cardiac myocytes Basic Res. Cardiol. 102 2007 542 552 (Pubitemid 47578399)
43. S. Schaller, S. Paradis, G.A. Ngoh, R. Assaly, B. Buisson, C. Drouot, M.A. Ostuni, J.J. Lacapere, F. Bassissi, T. Bordet, A. Berdeaux, S.P. Jones, D. Morin, and R.M. Pruss TRO40303, a new cardioprotective compound, inhibits mitochondrial permeability transition J. Pharmacol. Exp. Ther. 333 2010 696 706
44. H. Seguchi, M. Ritter, M. Shizukuishi, H. Ishida, G. Chokoh, H. Nakazawa, K.W. Spitzer, and W.H. Barry Propagation of Ca2 + release in cardiac myocytes: role of mitochondria Cell Calcium 38 2005 1 9 (Pubitemid 40903755)
45. V.G. Sharov, A. Todor, S. Khanal, M. Imai, and H.N. Sabbah Cyclosporine A attenuates mitochondrial permeability transition and improves mitochondrial respiratory function in cardiomyocytes isolated from dogs with heart failure J. Mol. Cell. Cardiol. 42 2007 150 158 (Pubitemid 44958623)
46. S.S. Sheu, W. Wang, H. Cheng, and R.T. Dirksen Superoxide flashes: illuminating new insights into cardiac ischemia/reperfusion injury Future Cardiol. 4 2008 551 554
47. C. Thomas, M.M. Mackey, A.A. Diaz, and D.P. Cox Hydroxyl radical is produced via the Fenton reaction in submitochondrial particles under oxidative stress: implications for diseases associated with iron accumulation Redox Rep. 14 2009 102 108
48. R. Tissier, M. Chenoune, B. Ghaleh, M.V. Cohen, J.M. Downey, and A. Berdeaux The small chill: mild hypothermia for cardioprotection? Cardiovasc. Res. 88 2010 406 414
49. P.A. Townsend, S.M. Davidson, S.J. Clarke, I. Khaliulin, C.J. Carroll, T.M. Scarabelli, R.A. Knight, A. Stephanou, D.S. Latchman, and A.P. Halestrap Urocortin prevents mitochondrial permeability transition in response to reperfusion injury indirectly by reducing oxidative stress Am. J. Physiol. Heart Circ. Physiol. 293 2007 H928 H
50. T.L. Vanden Hoek, C. Li, Z. Shao, P.T. Schumacker, and L.B. Becker Significant levels of oxidants are generated by isolated cardiomyocytes during ischemia prior to reperfusion J. Mol. Cell. Cardiol. 29 1997 2571 2583 (Pubitemid 27404448)
51. Q.S. Wang, Y.M. Zheng, L. Dong, Y.S. Ho, Z. Guo, and Y.X. Wang Role of mitochondrial reactive oxygen species in hypoxia-dependent increase in intracellular calcium in pulmonary artery myocytes Free Radic. Biol. Med. 42 2007 642 653 (Pubitemid 46205150)
52. W. Wang, H. Fang, L. Groom, A. Cheng, W. Zhang, and J. Liu Superoxide flashes in single mitochondria Cell 134 2008 279 290 (Pubitemid 352010332)
53. D.M. Yellon, and D.J. Hausenloy Myocardial reperfusion injury N. Engl. J. Med. 357 2007 1121 1135