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Mitochondria pp 305-322 | Cite as

Mitochondria and Their Role in Ischemia/Reperfusion Injury

  • Sebastian Phillip
  • James M. Downey
  • Michael V. Cohen
Part of the Advances in Biochemistry in Health and Disease book series (ABHD, volume 2)

Abstract

Acute coronary occlusion is the leading cause of morbidity and mortality in the western world and according to the World Health Organization will be the major cause of death in the world as a whole by the year 2020 (Murray and Lopez 1997). The major complication of the sudden occlusion of a coronary artery is the loss of contractile myocardium served by that artery. The contractile dysfunction resulting from infarction of the ventricle is essentially permanent as the lost heart muscle cannot regenerate. The size of the resultant infarct is the decisive determinant of the extent and severity of remodeling (Pfeffer et al. 1991) and of the prognosis of patients after myocardial infarction (St. John Sutton et al. 1997). Fast revascularization will result in less myocardial necrosis; nevertheless congestive heart failure secondary to myocardial infarction is still common.

Keywords

Ischemic Precondition Mitochondrial Permeability Transition Pore mPTP Opening Isolate Rabbit Heart Index Ischemia 
These keywords were added by machine and not by the authors. This process is experimental and the keywords may be updated as the learning algorithm improves.

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References

  1. Aguilar-Bryan L, Clement JP, IV, Gonzalez G, Kunjilwar K, Babenko A, Bryan J (1998) Toward understanding the assembly and structure of KATP channels. Physiol Rev 78:227–245PubMedGoogle Scholar
  2. Argaud L, Gateau-Roesch O, Chalabreysse L, Gomez L, Loufouat J, Thivolet-Béjui F, Robert D, Ovize M (2004) Preconditioning delays Ca2+-induced mitochondrial permeability transition. Cardiovasc Res 61:115–12CrossRefPubMedGoogle Scholar
  3. Argaud L, Gateau-Roesch O, Raisky O, Loufouat J, Robert D, Ovize M (2005) Postconditioning inhibits mitochondrial permeability transition. Circulation 111:194–197CrossRefPubMedGoogle Scholar
  4. Auchampach JA, Gross GJ (1993) Adenosine A1 receptors, KATP channels, and ischemic preconditioning in dogs. Am J Physiol 264:H1327–H1336PubMedGoogle Scholar
  5. Baines CP, Goto M, Downey JM (1997) Oxygen radicals released during ischemic preconditioning contribute to cardioprotection in the rabbit myocardium. J Mol Cell Cardiol 29:207–216CrossRefPubMedGoogle Scholar
  6. Baines CP, Kaiser RA, Purcell NH, Blair NS, Osinska H, Hambleton MA, Brunskill EW, Sayen MR, yGottlieb RA, Dorn GW II, Robbins J, Molkentin JD (2005) Loss of cyclophilin D reveals a critical role for mitochondrial permeability transition in cell death. Nature 434:658–662CrossRefPubMedGoogle Scholar
  7. Baines CP, Liu GS, Birincioglu M, Critz SD, Cohen MV, Downey JM (1999) Ischemic preconditioning depends on interaction between mitochondrial KATP channels and actin cytoskeleton. Am J Physiol 276:H1361–H1368PubMedGoogle Scholar
  8. Baines CP, Song C-X, Zheng Y-T, Wang G-W, Zhang J, Wang O-L, Guo Y, Bolli R, Cardwell EM, Ping P (2003) Protein kinase Cepsilon interacts with and inhibits the permeability transition pore in cardiac mitochondria. Circ Res 92:873–880CrossRefPubMedGoogle Scholar
  9. Baines CP, Zhang J, Wang G-W, Zheng Y-T, Xiu JX, Cardwell EM, Bolli R, Ping P (2002) Mitochondrial PKCepsilon and MAPK form signaling modules in the murine heart: enhanced mitochondrial PKCepsilon-MAPK interactions and differential MAPK activation in PKCepsilon-induced cardioprotection. Circ Res 90:390–397CrossRefPubMedGoogle Scholar
  10. 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 276:33369–33374.CrossRefPubMedGoogle Scholar
  11. Borutaite V, Brown GC (2003) Mitochondria in apoptosis of ischemic heart. FEBS Lett 541:1–5CrossRefPubMedGoogle Scholar
  12. Cohen MV, Yang X-M, Liu GS, Heusch G, Downey JM (2001) Acetylcholine, bradykinin, opioids, and phenylephrine, but not adenosine, trigger preconditioning by generating free radicals and opening mitochondrial KATP channels. Circ Res 89:273–278CrossRefPubMedGoogle Scholar
  13. 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 97:329–336CrossRefPubMedGoogle Scholar
  14. Costa ADT, Quinlan CL, Andrukhiv A, West IC, Jaburek M, Garlid KD (2005b) The direct physiological effects of MitoKATP opening on heart mitochondria . Am J Physiol (in press)Google Scholar
  15. Critz SD, Liu G-S, Chujo M, Downey JM (1997) Pinacidil but not nicorandil opens ATP-sensitive K+ channels and protects against simulated ischemia in rabbit myocytes. J Mol Cell Cardiol 29:1123–1130CrossRefPubMedGoogle Scholar
  16. Das M, Parker JE, Halestrap AP (2003) Matrix volume measurements challenge the existence of diazoxide/glibenclamide-sensitive KATP channels in rat mitochondria. J Physiol 547:893–902CrossRefPubMedGoogle Scholar
  17. Forbes RA, Steenbergen C, Murphy E (2001) Diazoxide-induced cardioprotection requires signaling through a redox-sensitive mechanism. Circ Res 88:802–809CrossRefPubMedGoogle Scholar
  18. Garlid KD (1996) Cation transport in mitochondria - the potassium cycle. Biochim Biophys Acta 1275:123–126CrossRefPubMedGoogle Scholar
  19. Garlid KD (2000) Opening mitochondrial KATP in the heart - what happens, and what does not happen. Basic Res Cardiol 95:275–279CrossRefPubMedGoogle Scholar
  20. Garlid KD, Paucek P (2003) Mitochondrial potassium transport: the K+ cycle. Biochim Biophys Acta 1606:23–41CrossRefPubMedGoogle Scholar
  21. 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 81:1072–1082PubMedGoogle Scholar
  22. Goto M, Liu Y, Yang X-M, Ardell JL, Cohen MV, Downey JM (1995) Role of bradykinin in protection of ischemic preconditioning in rabbit hearts. Circ Res 77:611–621PubMedGoogle Scholar
  23. Green DR, Reed JC (1998) Mitochondria and apoptosis. Science 281:1309–1312CrossRefPubMedGoogle Scholar
  24. Gross GJ, Auchampach JA (1992) Blockade of ATP-sensitive potassium channels prevents myocardial preconditioning in dogs. Circ Res 70:223–233PubMedGoogle Scholar
  25. Gross GJ, Fryer RM (1999) Sarcolemmal versus mitochondrial ATP-sensitive K+ channels and myocardial preconditioning. Circ Res 84:973–979PubMedGoogle Scholar
  26. Grover GJ, Garlid KD (2000) ATP-sensitive potassium channels: a review of their cardioprotective pharmacology. J Mol Cell Cardiol 32:677–695CrossRefPubMedGoogle Scholar
  27. Halestrap AP (1994) Regulation of mitochondrial metabolism through changes in matrix volume. Biochem Soc Trans 22:522–529PubMedGoogle Scholar
  28. Halestrap AP (1999) The mitochondrial permeability transition: its molecular mechanism and role in reperfusion injury. Biochem Soc Symp 66:181–203PubMedGoogle Scholar
  29. Halestrap AP, Clarke SJ, Javadov SA (2004) Mitochondrial permeability transition pore opening during myocardial reperfusion–a target for cardioprotection. Cardiovasc Res 61:372–385CrossRefPubMedGoogle Scholar
  30. Hanley PJ, Mickel M, Löffler M, Brandt U, Daut J (2002) KATP channel-independent targets of diazoxide and 5-hydroxydecanoate in the heart. J Physiol 542:735–741CrossRefPubMedGoogle Scholar
  31. Haunstetter A, Izumo S (1998) Apoptosis: basic mechanisms and implications for cardiovascular disease. Circ Res 82:1111–1129PubMedGoogle Scholar
  32. Hausenloy DJ, Maddock HL, Baxter GF, Yellon DM (2002) Inhibiting mitochondrial permeability transition pore opening: a new paradigm for myocardial preconditioning? Cardiovasc Res 55:534–543CrossRefPubMedGoogle Scholar
  33. Hausenloy DJ, Tsang A, Mocanu MM, Yellon DM (2005) Ischemic preconditioning protects by activating prosurvival kinases at reperfusion. Am J Physiol 288:H971–H976Google Scholar
  34. Hausenloy DJ, Yellon DM, Mani-Babu S, Duchen MR (2004) Preconditioning protects by inhibiting the mitochondrial permeability transition. Am J Physiol 287:H841–H849Google Scholar
  35. Holmuhamedov EL, Jovanovic S, Dzeja PP, Jovanovic A, Terzic A (1998) Mitochondrial ATP-sensitive K+ channels modulate cardiac mitochondrial function. Am J Physiol 275:H1567–H1576Google Scholar
  36. Holmuhamedov EL, Wang L, Terzic A (1999) ATP-sensitive K+ channel openers prevent Ca2+ overload in rat cardiac mitochondria. J Physiol 519:347–360CrossRefPubMedGoogle Scholar
  37. Inagaki N, Gonoi T, Clement JP IV, Namba N, Inazawa J, Gonzalez G, Aguilar-Bryan L, Seino S, Bryan J (1995a) Reconstitution of IKATP: an inward rectifier subunit plus the sulfonylurea receptor. Science 270:1166–1170CrossRefPubMedGoogle Scholar
  38. Inagaki N, Gonoi T, Clement JP IV, Wang C-Z, Aguilar-Bryan L, Bryan J, Seino S (1996) A family of sulfonylurea receptors determines the pharmacological properties of ATP-sensitive K+ channels. Neuron 16:1011–1017CrossRefPubMedGoogle Scholar
  39. Inagaki N, Tsuura Y, Namba N, Masuda K, Gonoi T, Horie M, Seino Y, Mizuta M, Seino S (1995b) Cloning and functional characterization of a novel ATP-sensitive potassium channel ubiquitously expressed in rat tissues, including pancreatic islets, pituitary, skeletal muscle, and heart. J Biol Chem 270:5691–5694CrossRefPubMedGoogle Scholar
  40. Inoue I, Nagase H, Kishi K, Higuti T (1991) ATP-sensitive K+ channel in the mitochondrial inner membrane. Nature 352:244–247CrossRefPubMedGoogle Scholar
  41. Javadov SA, Lim KHH, Kerr PM, Suleiman M-S, Angelini GD, Halestrap AP (2000) Protection of hearts from reperfusion injury by propofol is associated with inhibition of the mitochondrial permeability transition. Cardiovasc Res 45:360–369CrossRefPubMedGoogle Scholar
  42. Juhaszova M, Zorov DB, Kim S-H, Pepe S, Fu Q, Fishbein KW, Ziman BD, Wang S, Ytrehus K, Antos CL, Olson EN, Sollott SJ (2004) Glycogen synthase kinase-3b mediates convergence of protection signaling to inhibit the mitochondrial permeability transition pore. J Clin Invest 113:1535–1549PubMedGoogle Scholar
  43. Kluck RM, Bossy-Wetzel E, Green DR, Newmeyer DD (1997) The release of cytochrome c from mitochondria: a primary site for Bcl-2 regulation of apoptosis. Science 275:1132–1136CrossRefPubMedGoogle Scholar
  44. Korge P, Honda HM, Weiss JN (2002) Protection of cardiac mitochondria by diazoxide and protein kinase C: implications for ischemic preconditioning. Proc Natl Acad Sci 99:3312–3317CrossRefPubMedGoogle Scholar
  45. 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 97:365–373CrossRefPubMedGoogle Scholar
  46. Krieg T, Cui L, Qin Q, Cohen MV, Downey JM (2004a) Mitochondrial ROS generation following acetylcholine-induced EGF receptor transactivation requires metalloproteinase cleavage of proHB-EGF. J Mol Cell Cardiol 36:435–443CrossRefPubMedGoogle Scholar
  47. Krieg T, Qin Q, McIntosh EC, Cohen MV, Downey JM (2002) ACh and adenosine activate PI3-kinase in rabbit hearts through transactivation of receptor tyrosine kinases. Am J Physiol 283:H2322–H2330Google Scholar
  48. Krieg T, Qin Q, Philipp S, Alexeyev MF, Cohen MV, Downey JM (2004b) Acetylcholine and bradykinin trigger preconditioning in the heart through a pathway that includes Akt and NOS. Am J Physiol 287:H2606–H2611Google Scholar
  49. Liu GS, Thornton J, Van Winkle DM, Stanley AWH, Olsson RA, Downey JM (1991) Protection against infarction afforded by preconditioning is mediated by A1 adenosine receptors in rabbit heart. Circulation 84:350–356PubMedGoogle Scholar
  50. Liu Y, Sato T, O’Rourke B, Marban E (1998) Mitochondrial ATP-dependent potassium channels: novel effectors of cardioprotection? Circulation 97:2463–2469PubMedGoogle Scholar
  51. Liu Y, Tsuchida A, Cohen MV, Downey JM (1995) Pretreatment with angiotensin II activates protein kinase C and limits myocardial infarction in isolated rabbit hearts. J Mol Cell Cardiol 27:883–892CrossRefPubMedGoogle Scholar
  52. Lorenz E, Terzic A (1999) Physical association between recombinant cardiac ATP-sensitive K+ channel subunits Kir6.2 and SUR2A. J Mol Cell Cardiol 31:425–434CrossRefPubMedGoogle Scholar
  53. Miki T, Cohen MV, Downey JM (1998) Opioid receptor contributes to ischemic preconditioning through protein kinase C activation in rabbits. Mol Cell Biochem 186:3–12CrossRefPubMedGoogle Scholar
  54. Mocanu MM, Baxter GF, Yue Y, Critz SD, Yellon DM (2000) The p38 MAPK inhibitor, SB203580, abrogates ischaemic preconditioning in rat heart but timing of administration is critical. Basic Res Cardiol 95:472–478CrossRefPubMedGoogle Scholar
  55. Murata M, Akao M, O’Rourke B, Marbán E (2001) Mitochondrial ATP-sensitive potassium channels attenuate matrix Ca2+ overload during simulated ischemia and reperfusion: possible mechanism of cardioprotection. Circ Res 89:891–898CrossRefPubMedGoogle Scholar
  56. Murray CJL, Lopez AD (1997) Alternative projections of mortality and disability by cause 1990-2020: Global Burden of Disease Study. Lancet 349:1498–1504CrossRefPubMedGoogle Scholar
  57. Murry CE, Jennings RB, Reimer KA (1986) Preconditioning with ischemia: a delay of lethal cell injury in ischemic myocardium. Circulation 74:1124–1136PubMedGoogle Scholar
  58. Nakano A, Baines CP, Kim SO, Pelech SL, Downey JM, Cohen MV, Critz SD (2000) Ischemic preconditioning activates MAPKAPK2 in the isolated rabbit heart: evidence for involvement of p38 MAPK. Circ Res 86:144–151PubMedGoogle Scholar
  59. Newmeyer DD, Ferguson-Miller S (2003) Mitochondria: releasing power for life and unleashing the machineries of death. Cell 112:481–490CrossRefPubMedGoogle Scholar
  60. Nozawa Y, Miura T, Miki T, Ohnuma Y, Yano T, Shimamoto K (2003) Mitochondrial KATP channel-dependent and -independent phases of ischemic preconditioning against myocardial infarction in the rat. Basic Res Cardiol 98:50–58CrossRefPubMedGoogle Scholar
  61. Oldenburg O, Critz SD, Cohen MV, Downey JM (2003) Acetylcholine-induced production of reactive oxygen species in adult rabbit ventricular myocytes is dependent on phosphatidylinositol 3- and Src-kinase activation and mitochondrial KATP channel opening. J Mol Cell Cardiol 35:653–660CrossRefPubMedGoogle Scholar
  62. Oldenburg O, Qin Q, Krieg T, Yang X-M, Philipp S, Critz SD, Cohen MV, Downey JM (2004) Bradykinin induces mitochondrial ROS generation via NO, cGMP, PKG, and mitoKATP channel opening and leads to cardioprotection. Am J Physiol 286:H468–H476Google Scholar
  63. Oldenburg O, Qin Q, Sharma AR, Cohen MV, Downey JM, Benoit JN (2002) Acetylcholine leads to free radical production dependent on KATP channels, Gi proteins, phosphatidylinositol 3-kinase and tyrosine kinase. Cardiovasc Res 55:544–552CrossRefPubMedGoogle Scholar
  64. Ozcan C, Bienengraeber M, Dzeja PP, Terzic A (2002) Potassium channel openers protect cardiac mitochondria by attenuating oxidant stress at reoxygenation. Am J Physiol 282:H531–H539Google Scholar
  65. Pain T, Yang X-M, 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 87:460–466PubMedGoogle Scholar
  66. Paucek P, Mironova G, Mahdi F, Beavis AD, Woldegiorgis G, Garlid KD (1992) Reconstitution and partial purification of the glibenclamide-sensitive, ATP-dependent K+ channel from rat liver and beef heart mitochondria. J Biol Chem 267:26062–26069PubMedGoogle Scholar
  67. Paucek P, Yarov-Yarovoy V, Sun X, Garlid KD (1996) Inhibition of the mitochondrial KATP channel by long-chain acyl-CoA esters and activation by guanine nucleotides. J Biol Chem 271:32084–32088.CrossRefPubMedGoogle Scholar
  68. Pfeffer JM, Pfeffer MA, Fletcher PJ, Braunwald E (1991) Progressive ventricular remodeling in rat with myocardial infarction. Am J Physiol 260:H1406–H1414PubMedGoogle Scholar
  69. Ping P, Zhang J, Qiu Y, Tang X-L, Manchikalapudi S, Cao X, Bolli R (1997) Ischemic preconditioning induces selective translocation of protein kinase C isoforms e and h in the heart of conscious rabbits without subcellular redistribution of total protein kinase C activity. Circ Res 81:404–414PubMedGoogle Scholar
  70. Qin Q, Downey JM, Cohen MV (2003) Acetylcholine but not adenosine triggers preconditioning through PI3-kinase and a tyrosine kinase. Am J Physiol 284:H727–H734Google Scholar
  71. Sato T, Sasaki N, Seharaseyon J, O’Rourke B, Marbán E (2000) Selective pharmacological agents implicate mitochondrial but not sarcolemmal KATP channels in ischemic cardioprotection. Circulation 101:2418–2423PubMedGoogle Scholar
  72. Schultz JEJ, Rose E, Yao Z, Gross GJ (1995) Evidence for involvement of opioid receptors in ischemic preconditioning in rat hearts. Am J Physiol 268:H2157–H2161PubMedGoogle Scholar
  73. Schulz R, Gres P, Heusch G (2003) Activation of ATP-dependent potassium channels is a trigger but not a mediator of ischaemic preconditioning in pigs. Br J Pharmacol 139:65–72CrossRefPubMedGoogle Scholar
  74. Solenkova N, Cohen MV, Downey JM (2006) Endogenous adenosine protects the preconditioned heart during the early minutes of reperfusion by activating Akt. Am J Physiol 290:H441–449Google Scholar
  75. St .John Sutton M, Pfeffer MA, Moye L, Plappert T, Rouleau JL, Lamas G, Rouleau J, Parker JO, Arnold MO, Sussex B, Braunwald E, for the SAVE Investigators (1997) Cardiovascular death and left ventricular remodeling two years after myocardial infarction. Baseline predictors and impact of long-term use of captopril: information from the Survival and Ventricular Enlargement (SAVE) trial. Circulation 96:3294–3299PubMedGoogle Scholar
  76. Thornton JD, Liu GS, Downey JM (1993) Pretreatment with pertussis toxin blocks the protective effects of preconditioning: evidence for a G-protein mechanism. J Mol Cell Cardiol 25:311–320CrossRefPubMedGoogle Scholar
  77. 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 80:743–748PubMedGoogle Scholar
  78. Tsuchida A, Liu GS, Wilborn WH, Downey JM (1993) Pretreatment with the adenosine A1 selective agonist, 2-chloro-N6-cyclopentyladenosine (CCPA), causes a sustained limitation of infarct size in rabbits. Cardiovasc Res 27:652–656CrossRefPubMedGoogle Scholar
  79. Tsuchida A, Liu Y, Liu GS, Cohen MV, Downey JM (1994) a1-Adrenergic agonists precondition rabbit ischemic myocardium independent of adenosine by direct activation of protein kinase C. Circ Res 75:576–585PubMedGoogle Scholar
  80. Van Winkle DM, Thornton JD, Downey DM, Downey JM (1991) The natural history of preconditioning: cardioprotection depends on duration of transient ischemia and time to subsequent ischemia. Coron Artery Dis 2:613–619Google Scholar
  81. Vanden Hoek TL, Becker LB, Shao Z-H, Li C-Q, Schumacker PT (2000) Preconditioning in cardiomyocytes protects by attenuating oxidant stress at reperfusion. Circ Res 86:541–548PubMedGoogle Scholar
  82. Wall TM, Sheehy R, Hartman JC (1994) Role of bradykinin in myocardial preconditioning. J Pharmacol Exp Ther 270:681–689PubMedGoogle Scholar
  83. Wang P, Gallagher KP, Downey JM, Cohen MV (1996) Pretreatment with endothelin-1 mimics ischemic preconditioning against infarction in isolated rabbit heart. J Mol Cell Cardiol 28:579–588CrossRefPubMedGoogle Scholar
  84. Wang S, Cone J, Liu Y (2001) Dual roles of mitochondrial KATP channels in diazoxide-mediated protection in isolated rabbit hearts. Am J Physiol 280:H246–H255Google Scholar
  85. Weiss JN, Korge P, Honda HM, Ping P (2003) Role of the mitochondrial permeability transition in myocardial disease. Circ Res 93:292–301CrossRefPubMedGoogle Scholar
  86. Yang X-M, 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 44:1103–1110CrossRefPubMedGoogle Scholar
  87. Yarov-Yarovoy V, Paucek P, Jaburek,M, Garlid KD (1997) The nucleotide regulatory sites on the mitochondrial KATP channel face the cytosol. Biochim Biophys Acta 1321:128–136CrossRefPubMedGoogle Scholar
  88. Yellon DM, Downey JM (2003) Preconditioning the myocardium: from cellular physiology to clinical cardiology. Physiol Rev 83:1113–1151PubMedGoogle Scholar
  89. Yue Y, Krenz M, Cohen MV, Downey JM, Critz SD (2001) Menadione mimics the infarct-limiting effect of preconditioning in isolated rat hearts. Am J Physiol 281:H590–H595Google Scholar
  90. Zhao Z-Q, Corvera JS, Halkos ME, Kerendi F, Wang N-P, Guyton RA, Vinten-Johansen J (2003) Inhibition of myocardial injury by ischemic postconditioning during reperfusion: comparison with ischemic preconditioning. Am J Physiol 285:H579–H588Google Scholar
  91. Zorov DB, Filburn CR, Klotz L-O, Zweier JL, Sollott SJ (2000) Reactive oxygen species (ROS)-induced ROS release: a new phenomenon accompanying induction of the mitochondrial permeability transition in cardiac myocytes. J Exp Med 192:1001–1014CrossRefPubMedGoogle Scholar
  92. Zweier JL, Flaherty JT, Weisfeldt ML (1987) Direct measurement of free radical generation following reperfusion of ischemic myocardium. Proc Natl Acad Sci 84:1404–1407CrossRefPubMedGoogle Scholar

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© Springer Science+Business Media, LLC 2007

Authors and Affiliations

  • Sebastian Phillip
  • James M. Downey
  • Michael V. Cohen

There are no affiliations available

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