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Mitochondrial Reactive Oxygen Species in Myocardial Pre- and Postconditioning

  • Ariel R. Cardoso
  • Bruno B. Queliconi
  • Alicia J. Kowaltowski
Chapter
Part of the Oxidative Stress in Applied Basic Research and Clinical Practice book series (OXISTRESS)

Abstract

Myocardial ischemia followed by reperfusion is a well established condition of medical importance in which reactive oxygen species (ROS) are determinant for the pathological outcome. Indeed, oxidative damage during reperfusion is causative of many of the complications found after ischemia. ROS leading to postischemic myocardial damage come from many sources, including mitochondria, NADPH oxidase, xanthine oxidase, and infiltrated phagocytes [1]. ROS also can act as signaling molecules in the cardiovascular system, including protecting the heart against myocardial ischemic damage, secondarily to ischemic pre- and postconditioning. In this case, there is ample evidence that the source of signaling ROS is mitochondrial [2–7]. This chapter will briefly review aspects of mitochondrial ROS signaling relevant to myocardial ischemic protection by pre- and postconditioning.

Keywords

Electron transport chain Oxidative phosphorylation Uncoupling proteins Mitochondrial KATP channels Mitochondrial membrane potential Mitochondrial free radical production 

References

  1. 1.
    Dröge W (2002) Free radicals in the physiological control of cell function. Physiol Rev 82:47–95PubMedGoogle Scholar
  2. 2.
    Di Lisa F, Bernardi P (2006) Mitochondria and ischemia-reperfusion injury of the heart: fixing a hole. Cardiovasc Res 70:191–199PubMedCrossRefGoogle Scholar
  3. 3.
    Facundo HTF, Carreira RS, de Paula JG, Santos CCX, Ferranti R, Laurindo FRM, Kowaltowski AJ (2006) Ischemic preconditioning requires increases in reactive oxygen release independent of mitochondrial K+ channel activity. Free Radic Biol Med 40:469–479PubMedCrossRefGoogle Scholar
  4. 4.
    Halestrap AP, Clarke SJ, Javadov SA (2004) Mitochondrial permeability transition pore opening during myocardial reperfusion-a target for cardioprotection. Cardiovasc Res 61:372–385PubMedCrossRefGoogle Scholar
  5. 5.
    Sun H, Wang N, Kerendi F, Halkos M, Kin H, Guyton RA, Vinten-Johansen J, Zhao Z (2005) Hypoxic postconditioning reduces cardiomyocyte loss by inhibiting ROS generation and intracellular Ca2+ overload. Am J Physiol Heart Circ Physiol 288:H1900–H1908PubMedCrossRefGoogle Scholar
  6. 6.
    Vanden Hoek TL, Becker LB, Shao Z, Li C, Schumacker PT (1998) Reactive oxygen species released from mitochondria during brief hypoxia induce preconditioning in cardiomyocytes. J Biol Chem 273:18092–18098PubMedCrossRefGoogle Scholar
  7. 7.
    da Silva MM, Sartori A, Belisle E, Kowaltowski AJ (2003) Ischemic preconditioning inhibits mitochondrial respiration, increases H2O2 release, and enhances K+ transport. Am J Physiol Heart Circ Physiol 285:H154–H162PubMedGoogle Scholar
  8. 8.
    Brookes PS, Levonen A, Shiva S, Sarti P, Darley-Usmar VM (2002) Mitochondria: regulators of signal transduction by reactive oxygen and nitrogen species. Free Radic Biol Med 33:755–764PubMedCrossRefGoogle Scholar
  9. 9.
    Kowaltowski AJ, Vercesi AE (1999) Mitochondrial damage induced by conditions of oxidative stress. Free Radic Biol Med 26:463–471PubMedCrossRefGoogle Scholar
  10. 10.
    Turrens JF (2003) Mitochondrial formation of reactive oxygen species. J Physiol (Lond) 552:335–344CrossRefGoogle Scholar
  11. 11.
    Liu Y, Fiskum G, Schubert D (2002) Generation of reactive oxygen species by the mitochondrial electron transport chain. J Neurochem 80:780–787PubMedCrossRefGoogle Scholar
  12. 12.
    Brookes PS (2005) Mitochondrial H+ leak and ROS generation: an odd couple. Free Radic Biol Med 38:12–23PubMedCrossRefGoogle Scholar
  13. 13.
    Korshunov SS, Skulachev VP, Starkov AA (1997) High protonic potential actuates a mechanism of production of reactive oxygen species in mitochondria. FEBS Lett 416:15–18PubMedCrossRefGoogle Scholar
  14. 14.
    Skulachev VP (1998) Uncoupling: new approaches to an old problem of bioenergetics. Biochim Biophys Acta 1363:100–124PubMedCrossRefGoogle Scholar
  15. 15.
    Tahara EB, Navarete FD, Kowaltowski AJ (2009) Tissue-, substrate-, and site-specific characteristics of mitochondrial reactive oxygen species generation. Free Radic Biol Med 46:1283–1297PubMedCrossRefGoogle Scholar
  16. 16.
    Caldeira da Silva CC, Cerqueira FM, Barbosa LF, Medeiros MHG, Kowaltowski AJ (2008) Mild mitochondrial uncoupling in mice affects energy metabolism, redox balance and longevity. Aging Cell 7:552–560PubMedCrossRefGoogle Scholar
  17. 17.
    Huang SG, Klingenberg M (1996) Chloride channel properties of the uncoupling protein from brown adipose tissue mitochondria: a patch-clamp study. Biochemistry 35:16806–16814PubMedCrossRefGoogle Scholar
  18. 18.
    Jacobsson A, Stadler U, Glotzer MA, Kozak LP (1985) Mitochondrial uncoupling protein from mouse brown fat. Molecular cloning, genetic mapping, and mRNA expression. J Biol Chem 260:16250–16254PubMedGoogle Scholar
  19. 19.
    Klingenberg M (1988) Nucleotide binding to uncoupling protein. Mechanism of control by protonation. Biochemistry 27:781–791PubMedCrossRefGoogle Scholar
  20. 20.
    Saito S, Saito CT, Shingai R (2008) Adaptive evolution of the uncoupling protein 1 gene contributed to the acquisition of novel nonshivering thermogenesis in ancestral eutherian mammals. Gene 408:37–44PubMedCrossRefGoogle Scholar
  21. 21.
    Cannon B, Nedergaard J (2004) Brown adipose tissue: function and physiological significance. Physiol Rev 84:277–359PubMedCrossRefGoogle Scholar
  22. 22.
    Ricquier D, Bouillaud F (2000) The uncoupling protein homologues: UCP1, UCP2, UCP3, StUCP and AtUCP. Biochem J 345(Pt 2):161–179PubMedCrossRefGoogle Scholar
  23. 23.
    Murray AJ, Anderson RE, Watson GC, Radda GK, Clarke K (2004) Uncoupling proteins in human heart. Lancet 364:1786–1788PubMedCrossRefGoogle Scholar
  24. 24.
    Bo H, Jiang N, Ma G, Qu J, Zhang G, Cao D, Wen L, Liu S, Ji LL, Zhang Y (2008) Regulation of mitochondrial uncoupling respiration during exercise in rat heart: role of reactive oxygen species (ROS) and uncoupling protein 2. Free Radic Biol Med 44:1373–1381PubMedCrossRefGoogle Scholar
  25. 25.
    Villarroya F, Iglesias R, Giralt M (2007) PPARs in the Control of Uncoupling Proteins Gene Expression. PPAR Res 2007:74364PubMedCrossRefGoogle Scholar
  26. 26.
    Nègre-Salvayre A, Hirtz C, Carrera G, Cazenave R, Troly M, Salvayre R, Pénicaud L, Casteilla L (1997) A role for uncoupling protein-2 as a regulator of mitochondrial hydrogen peroxide generation. FASEB J 11:809–815PubMedGoogle Scholar
  27. 27.
    Garlid KD, Jabůrek M, Jezek P, Varecha M (2000) How do uncoupling proteins uncouple? Biochim Biophys Acta 1459:383–389PubMedCrossRefGoogle Scholar
  28. 28.
    Arvier M, Lagoutte L, Johnson G, Dumas J, Sion B, Grizard G, Malthièry Y, Simard G, Ritz P (2007) Adenine nucleotide translocator promotes oxidative phosphorylation and mild uncoupling in mitochondria after dexamethasone treatment. Am J Physiol Endocrinol Metab 293:E1320–E1324PubMedCrossRefGoogle Scholar
  29. 29.
    Schönfeld P (1990) Does the function of adenine nucleotide translocase in fatty acid uncoupling depend on the type of mitochondria? FEBS Lett 264:246–248PubMedCrossRefGoogle Scholar
  30. 30.
    Tikhonova IM, Andreyev AYu, Antonenko YuN, Kaulen AD, Komrakov AYu, Skulachev VP (1994) Ion permeability induced in artificial membranes by the ATP/ADP antiporter. FEBS Lett 337:231–234PubMedCrossRefGoogle Scholar
  31. 31.
    Shabalina IG, Kramarova TV, Nedergaard J, Cannon B (2006) Carboxyatractyloside effects on brown-fat mitochondria imply that the adenine nucleotide translocator isoforms ANT1 and ANT2 may be responsible for basal and fatty-acid-induced uncoupling respectively. Biochem J 399:405–414PubMedCrossRefGoogle Scholar
  32. 32.
    Esposito LA, Melov S, Panov A, Cottrell BA, Wallace DC (1999) Mitochondrial disease in mouse results in increased oxidative stress. Proc Natl Acad Sci USA 96:4820–4825PubMedCrossRefGoogle Scholar
  33. 33.
    Garlid KD, Paucek P (2003) Mitochondrial potassium transport: the K+ cycle. Biochim Biophys Acta 1606:23–41PubMedCrossRefGoogle Scholar
  34. 34.
    Facundo HTF, Fornazari M, Kowaltowski AJ (2006) Tissue protection mediated by mitochondrial K+ channels. Biochim Biophys Acta 1762:202–212PubMedCrossRefGoogle Scholar
  35. 35.
    Kowaltowski AJ, Seetharaman S, Paucek P, Garlid KD (2001) Bioenergetic consequences of opening the ATP-sensitive K+ channel of heart mitochondria. Am J Physiol Heart Circ Physiol 280:H649–H657PubMedGoogle Scholar
  36. 36.
    Bajgar R, Seetharaman S, Kowaltowski AJ, Garlid KD, Paucek P (2001) Identification and properties of a novel intracellular (mitochondrial) ATP-sensitive potassium channel in brain. J Biol Chem 276:33369–33374PubMedCrossRefGoogle Scholar
  37. 37.
    Daum G (1985) Lipids of mitochondria. Biochim Biophys Acta 822:1–42PubMedCrossRefGoogle Scholar
  38. 38.
    Crompton M (1999) The mitochondrial permeability transition pore and its role in cell death. Biochem J 341:233–249PubMedCrossRefGoogle Scholar
  39. 39.
    Kowaltowski AJ, Castilho RF, Vercesi AE (2001) Mitochondrial permeability transition and oxidative stress. FEBS Lett 495:12–15PubMedCrossRefGoogle Scholar
  40. 40.
    Lemasters JJ, Nieminen AL, Qian T, Trost LC, Elmore SP, Nishimura Y, Crowe RA, Cascio WE, Bradham CA, Brenner DA, Herman B (1998) The mitochondrial permeability transition in cell death: a common mechanism in necrosis, apoptosis and autophagy. Biochim Biophys Acta 1366:177–196PubMedCrossRefGoogle Scholar
  41. 41.
    Zoratti M, Szabò I (1995) The mitochondrial permeability transition. Biochim Biophys Acta 1241:139–176PubMedCrossRefGoogle Scholar
  42. 42.
    Rodriguez-Enriquez S, He L, Lemasters JJ (2004) Role of mitochondrial permeability transition pores in mitochondrial autophagy. Int J Biochem Cell Biol 36:2463–2472PubMedCrossRefGoogle Scholar
  43. 43.
    Castilho RF, Kowaltowski AJ, Vercesi AE (1996) The irreversibility of inner mitochondrial membrane permeabilization by Ca2+ plus prooxidants is determined by the extent of membrane protein thiol cross-linking. J Bioenerg Biomembr 28:523–529PubMedCrossRefGoogle Scholar
  44. 44.
    Ichas F, Mazat JP (1998) From calcium signaling to cell death: two conformations for the mitochondrial permeability transition pore. Switching from low- to high-conductance state. Biochim Biophys Acta 1366:33–50PubMedCrossRefGoogle Scholar
  45. 45.
    Di Lisa F, Menabò R, Canton M, Barile M, Bernardi P (2001) Opening of the mitochondrial permeability transition pore causes depletion of mitochondrial and cytosolic NAD+ and is a causative event in the death of myocytes in postischemic reperfusion of the heart. J Biol Chem 276:2571–2575PubMedCrossRefGoogle Scholar
  46. 46.
    Griffiths EJ, Halestrap AP (1995) Mitochondrial non-specific pores remain closed during cardiac ischaemia, but open upon reperfusion. Biochem J 307:93–98PubMedGoogle Scholar
  47. 47.
    Gottlieb RA, Burleson KO, Kloner RA, Babior BM, Engler RL (1994) Reperfusion injury induces apoptosis in rabbit cardiomyocytes. J Clin Invest 94:1621–1628PubMedCrossRefGoogle Scholar
  48. 48.
    Murry CE, Jennings RB, Reimer KA (1986) Preconditioning with ischemia: a delay of lethal cell injury in ischemic myocardium. Circulation 74:1124–1136PubMedCrossRefGoogle Scholar
  49. 49.
    Vanden Hoek T, Becker LB, Shao ZH, Li CQ, Schumacker PT (2000) Preconditioning in cardiomyocytes protects by attenuating oxidant stress at reperfusion. Circ Res 86:541–548PubMedCrossRefGoogle Scholar
  50. 50.
    Costa ADT, Garlid KD, West IC, Lincoln TM, Downey JM, Cohen MV, Critz SD (2005) Protein kinase G transmits the cardioprotective signal from cytosol to mitochondria. Circ Res 97:329–336PubMedCrossRefGoogle Scholar
  51. 51.
    Dorn GW 2nd, Souroujon MC, Liron T, Chen CH, Gray MO, Zhou HZ, Csukai M, Wu G, Lorenz JN, Mochly-Rosen D (1999) Sustained in vivo cardiac protection by a rationally designed peptide that causes epsilon protein kinase C translocation. Proc Natl Acad Sci USA 96:12798–12803PubMedCrossRefGoogle Scholar
  52. 52.
    Lebuffe G, Schumacker PT, Shao Z, Anderson T, Iwase H, Vanden Hoek TL (2003) ROS and NO trigger early preconditioning: relationship to mitochondrial KATP channel. Am J Physiol Heart Circ Physiol 284:H299–H308PubMedGoogle Scholar
  53. 53.
    Mitchell MB, Meng X, Ao L, Brown JM, Harken AH, Banerjee A (1995) Preconditioning of isolated rat heart is mediated by protein kinase C. Circ Res 76:73–81PubMedCrossRefGoogle Scholar
  54. 54.
    Ping P, Zhang J, Qiu Y, Tang XL, Manchikalapudi S, Cao X, Bolli R (1997) Ischemic preconditioning induces selective translocation of protein kinase C isoforms epsilon and eta in the heart of conscious rabbits without subcellular redistribution of total protein kinase C activity. Circ Res 81:404–414PubMedCrossRefGoogle Scholar
  55. 55.
    Ping P, Takano H, Zhang J, Tang XL, Qiu Y, Li RC, Banerjee S, Dawn B, Balafonova Z, Bolli R (1999) Isoform-selective activation of protein kinase C by nitric oxide in the heart of conscious rabbits: a signaling mechanism for both nitric oxide-induced and ischemia-induced preconditioning. Circ Res 84:587–604PubMedCrossRefGoogle Scholar
  56. 56.
    Sato T, O’Rourke B, Marbán E (1998) Modulation of mitochondrial ATP-dependent K+ channels by protein kinase C. Circ Res 83:110–114PubMedCrossRefGoogle Scholar
  57. 57.
    Saurin AT, Pennington DJ, Raat NJH, Latchman DS, Owen MJ, Marber MS (2002) Targeted disruption of the protein kinase C epsilon gene abolishes the infarct size reduction that follows ischaemic preconditioning of isolated buffer-perfused mouse hearts. Cardiovasc Res 55:672–680PubMedCrossRefGoogle Scholar
  58. 58.
    Klann E, Roberson ED, Knapp LT, Sweatt JD (1998) A role for superoxide in protein kinase C activation and induction of long-term potentiation. J Biol Chem 273:4516–4522PubMedCrossRefGoogle Scholar
  59. 59.
    Tritto I, D’Andrea D, Eramo N, Scognamiglio A, De Simone C, Violante A, Esposito A, Chiariello M, Ambrosio G (1997) Oxygen radicals can induce preconditioning in rabbit hearts. Circ Res 80:743–748PubMedCrossRefGoogle Scholar
  60. 60.
    Garlid KD, Paucek P, Yarov-Yarovoy V, Murray HN, Darbenzio RB, D’Alonzo AJ, Lodge NJ, Smith MA, Grover GJ (1997) Cardioprotective effect of diazoxide and its interaction with mitochondrial ATP-sensitive K+ channels. Possible mechanism of cardioprotection. Circ Res 81:1072–1082PubMedCrossRefGoogle Scholar
  61. 61.
    Grover GJ (1994) Protective effects of ATP-sensitive potassium-channel openers in experimental myocardial ischemia. J Cardiovasc Pharmacol 24:S18–S27PubMedCrossRefGoogle Scholar
  62. 62.
    Richer C, Pratz J, Mulder P, Mondot S, Giudicelli JF, Cavero I (1990) Cardiovascular and biological effects of K+ channel openers, a class of drugs with vasorelaxant and cardioprotective properties. Life Sci 47:1693–1705PubMedCrossRefGoogle Scholar
  63. 63.
    Yao Z, Gross GJ (1994) Effects of the KATP channel opener bimakalim on coronary blood flow, monophasic action potential duration, and infarct size in dogs. Circulation 89:1769–1775PubMedCrossRefGoogle Scholar
  64. 64.
    Andrukhiv A, Costa AD, West IC, Garlid KD (2006) Opening mitoKATP increases superoxide generation from complex I of the electron transport chain. Am J Physiol Heart Circ Physiol 291:H2067–H2074PubMedCrossRefGoogle Scholar
  65. 65.
    Carroll R, Gant VA, Yellon DM (2001) Mitochondrial KATP channel opening protects a human atrial-derived cell line by a mechanism involving free radical generation. Cardiovasc Res 51:691–700PubMedCrossRefGoogle Scholar
  66. 66.
    Facundo HTF, Kowaltowski AJ (2005) Letter regarding article by Argaud et al, “postconditioning inhibits mitochondrial permeability transition”. Circulation 111:e442; author reply e442PubMedCrossRefGoogle Scholar
  67. 67.
    Facundo HTF, de Paula JG, Kowaltowski AJ (2007) Mitochondrial ATP-sensitive K+ channels are redox-sensitive pathways that control reactive oxygen species production. Free Radic Biol Med 42:1039–1048PubMedCrossRefGoogle Scholar
  68. 68.
    Zhang DX, Chen YF, Campbell WB, Zou AP, Gross GJ, Li PL (2001) Characteristics and superoxide-induced activation of reconstituted myocardial mitochondrial ATP-sensitive potassium channels. Circ Res 89:1177–1183PubMedCrossRefGoogle Scholar
  69. 69.
    Forbes RA, Steenbergen C, Murphy E (2001) Diazoxide-induced cardioprotection requires signaling through a redox-sensitive mechanism. Circ Res 88:802–809PubMedCrossRefGoogle Scholar
  70. 70.
    Pain T, Yang XM, Critz SD, Yue Y, Nakano A, Liu GS, Heusch G, Cohen MV, Downey JM (2000) Opening of mitochondrial KATP channels triggers the preconditioned state by generating free radicals. Circ Res 87:460–466PubMedCrossRefGoogle Scholar
  71. 71.
    Fornazari M, de Paula JG, Castilho RF, Kowaltowski AJ (2008) Redox properties of the adenoside triphosphate-sensitive K+ channel in brain mitochondria. J Neurosci Res 86:1548–1556PubMedCrossRefGoogle Scholar
  72. 72.
    Krenz M, Oldenburg O, Wimpee H, Cohen MV, Garlid KD, Critz SD, Downey JM, Benoit JN (2002) Opening of ATP-sensitive potassium channels causes generation of free radicals in vascular smooth muscle cells. Basic Res Cardiol 97:365–373PubMedCrossRefGoogle Scholar
  73. 73.
    Scorrano L, Petronilli V, Colonna R, Di Lisa F, Bernardi P (1999) Interactions of chloromethyltetramethylrosamine (Mitotracker Orange) with isolated mitochondria and intact cells. Ann N Y Acad Sci 893:391–395PubMedCrossRefGoogle Scholar
  74. 74.
    Scorrano L, Petronilli V, Colonna R, Di Lisa F, Bernardi P (1999) Chloromethyltetramethylrosamine (Mitotracker Orange) induces the mitochondrial permeability transition and inhibits respiratory complex I. Implications for the mechanism of cytochrome c release. J Biol Chem 274:24657–24663PubMedCrossRefGoogle Scholar
  75. 75.
    Dröse S, Brandt U, Hanley PJ (2006) K+-independent actions of diazoxide question the role of inner membrane KATP channels in mitochondrial cytoprotective signaling. J Biol Chem 281:23733–23739PubMedCrossRefGoogle Scholar
  76. 76.
    Oldenburg O, Cohen MV, Yellon DM, Downey JM (2002) Mitochondrial KATP channels: role in cardioprotection. Cardiovasc Res 55:429–437PubMedCrossRefGoogle Scholar
  77. 77.
    Ferranti R, da Silva MM, Kowaltowski AJ (2003) Mitochondrial ATP-sensitive K+ channel opening decreases reactive oxygen species generation. FEBS Lett 536:51–55PubMedCrossRefGoogle Scholar
  78. 78.
    Wrona M, Wardman P (2006) Properties of the radical intermediate obtained on oxidation of 2,7-dichlorodihydrofluorescein, a probe for oxidative stress. Free Radic Biol Med 41:657–667PubMedCrossRefGoogle Scholar
  79. 79.
    Costa ADT, Quinlan CL, Andrukhiv A, West IC, Jabůrek M, Garlid KD (2006) The direct physiological effects of mitoKATP opening on heart mitochondria. Am J Physiol Heart Circ Physiol 290:H406–H415PubMedCrossRefGoogle Scholar
  80. 80.
    Costa ADT, Jakob R, Costa CL, Andrukhiv K, West IC, Garlid KD (2006) The mechanism by which the mitochondrial ATP-sensitive K+ channel opening and H2O2 inhibit the mitochondrial permeability transition. J Biol Chem 281:20801–20808PubMedCrossRefGoogle Scholar
  81. 81.
    Clarke SJ, Khaliulin I, Das M, Parker JE, Heesom KJ, Halestrap AP (2008) Inhibition of mitochondrial permeability transition pore opening by ischemic preconditioning is probably mediated by reduction of oxidative stress rather than mitochondrial protein phosphorylation. Circ Res 102:1082–1090PubMedCrossRefGoogle Scholar
  82. 82.
    Costa ADT, Garlid KD (2008) Intramitochondrial signaling: interactions among mitoKATP, PKCepsilon, ROS, and MPT. Am J Physiol Heart Circ Physiol 295:H874–H882PubMedCrossRefGoogle Scholar
  83. 83.
    Ljubkovic M, Shi Y, Cheng Q, Bosnjak Z, Jiang MT (2007) Cardiac mitochondrial ATP-sensitive potassium channel is activated by nitric oxide in vitro. FEBS Lett 581:4255–4259PubMedCrossRefGoogle Scholar
  84. 84.
    Burwell LS, Nadtochiy SM, Tompkins AJ, Young S, Brookes PS (2006) Direct evidence for S-nitrosation of mitochondrial complex I. Biochem J 394:627–634PubMedCrossRefGoogle Scholar
  85. 85.
    Heinen A, Aldakkak M, Stowe DF, Rhodes SS, Riess ML, Varadarajan SG, Camara AKS (2007) Reverse electron flow-induced ROS production is attenuated by activation of mitochondrial Ca2+-sensitive K+ channels. Am J Physiol Heart Circ Physiol 293:H1400–H1407PubMedCrossRefGoogle Scholar
  86. 86.
    Wang Y, Ashraf M (1999) Role of protein kinase C in mitochondrial KATP channel-mediated protection against Ca2+ overload injury in rat myocardium. Circ Res 84:1156–1165PubMedCrossRefGoogle Scholar
  87. 87.
    Chen C, Budas GR, Churchill EN, Disatnik M, Hurley TD, Mochly-Rosen D (2008) Activation of aldehyde dehydrogenase-2 reduces ischemic damage to the heart. Science 321:1493–1495PubMedCrossRefGoogle Scholar
  88. 88.
    Carreira RS, Miyamoto S, Di Mascio P, Gonçalves LM, Monteiro P, Providência LA, Kowaltowski AJ (2007) Ischemic preconditioning enhances fatty acid-dependent mitochondrial uncoupling. J Bioenerg Biomembr 39:313–320PubMedCrossRefGoogle Scholar
  89. 89.
    Nadtochiy SM, Tompkins AJ, Brookes PS (2006) Different mechanisms of mitochondrial proton leak in ischaemia/reperfusion injury and preconditioning: implications for pathology and cardioprotection. Biochem J 395:611–618PubMedCrossRefGoogle Scholar
  90. 90.
    Korde AS, Pettigrew LC, Craddock SD, Maragos WF (2005) The mitochondrial uncoupler 2,4-dinitrophenol attenuates tissue damage and improves mitochondrial homeostasis following transient focal cerebral ischemia. J Neurochem 94:1676–1684PubMedCrossRefGoogle Scholar
  91. 91.
    Mattiasson G, Shamloo M, Gido G, Mathi K, Tomasevic G, Yi S, Warden CH, Castilho RF, Melcher T, Gonzalez-Zulueta M, Nikolich K, Wieloch T (2003) Uncoupling protein-2 prevents neuronal death and diminishes brain dysfunction after stroke and brain trauma. Nat Med 9:1062–1068PubMedCrossRefGoogle Scholar
  92. 92.
    Na HS, Kim YI, Yoon YW, Han HC, Nahm SH, Hong SK (1996) Ventricular premature beat-driven intermittent restoration of coronary blood flow reduces the incidence of reperfusion-induced ventricular fibrillation in a cat model of regional ischemia. Am Heart J 132:78–83PubMedCrossRefGoogle Scholar
  93. 93.
    Philipp S, Yang X, Cui L, Davis AM, Downey JM, Cohen MV (2006) Postconditioning protects rabbit hearts through a protein kinase C-adenosine A2b receptor cascade. Cardiovasc Res 70:308–314PubMedCrossRefGoogle Scholar
  94. 94.
    Yang X, Proctor JB, Cui L, Krieg T, Downey JM, Cohen MV (2004) Multiple, brief coronary occlusions during early reperfusion protect rabbit hearts by targeting cell signaling pathways. J Am Coll Cardiol 44:1103–1110PubMedCrossRefGoogle Scholar
  95. 95.
    Kin H, Zhao Z, Sun H, Wang N, Corvera JS, Halkos ME, Kerendi F, Guyton RA, Vinten-Johansen J (2004) Postconditioning attenuates myocardial ischemia-reperfusion injury by inhibiting events in the early minutes of reperfusion. Cardiovasc Res 62:74–85PubMedCrossRefGoogle Scholar
  96. 96.
    Serviddio G, Di Venosa N, Federici A, D’Agostino D, Rollo T, Prigigallo F, Altomare E, Fiore T, Vendemiale G (2005) Brief hypoxia before normoxic reperfusion (postconditioning) protects the heart against ischemia-reperfusion injury by preventing mitochondria peroxyde production and glutathione depletion. FASEB J 19:354–361PubMedCrossRefGoogle Scholar
  97. 97.
    Argaud L, Gateau-Roesch O, Raisky O, Loufouat J, Robert D, Ovize M (2005) Postconditioning inhibits mitochondrial permeability transition. Circulation 111:194–197PubMedCrossRefGoogle Scholar
  98. 98.
    Bopassa JC, Vandroux D, Ovize M, Ferrera R (2006) Controlled reperfusion after hypothermic heart preservation inhibits mitochondrial permeability transition-pore opening and enhances functional recovery. Am J Physiol Heart Circ Physiol 291: H2265–H2271PubMedCrossRefGoogle Scholar
  99. 99.
    Cohen MV, Yang X, Downey JM (2008) Acidosis, oxygen, and interference with mitochondrial permeability transition pore formation in the early minutes of reperfusion are critical to postconditioning’s success. Basic Res Cardiol 103:464–471PubMedCrossRefGoogle Scholar
  100. 100.
    Penna C, Rastaldo R, Mancardi D, Raimondo S, Cappello S, Gattullo D, Losano G, Pagliaro P (2006) Post-conditioning induced cardioprotection requires signaling through a redox-sensitive mechanism, mitochondrial ATP-sensitive K+ channel and protein kinase C activation. Basic Res Cardiol 101:180–189PubMedCrossRefGoogle Scholar
  101. 101.
    Chu F, Ward NE, O’Brian CA (2003) PKC isozyme S-cysteinylation by cystine stimulates the pro-apoptotic isozyme PKC delta and inactivates the oncogenic isozyme PKC epsilon. Carcinogenesis 24:317–325PubMedCrossRefGoogle Scholar

Copyright information

© Springer Science+Business Media, LLC 2010

Authors and Affiliations

  • Ariel R. Cardoso
    • 1
  • Bruno B. Queliconi
    • 1
  • Alicia J. Kowaltowski
    • 1
  1. 1.Departamento de BioquímicaInstituto de Química, Universidade de São PauloSão PauloBrazil

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