Nitric Oxide pp 545-570 | Cite as

The Role of Nitric Oxide in Cardiac Ischaemia-Reperfusion

  • P. A. MacCarthy
  • A. M. Shah
Part of the Handbook of Experimental Pharmacology book series (HEP, volume 143)

Abstract

Myocardial ischaemia, resulting mainly from atherosclerotic coronary artery disease, is the most common pathology in clinical cardiology and is a major cause of mortality and morbidity in the developed world. Iatrogenic myocardial ischaemia is also commonly encountered clinically, especially in the context of cardiac surgery and interventional cardiology procedures, such as percutaneous balloon angioplasty. There have been great advances in the clinical management of myocardial ischaemia over the last 2–3 decades. In particular, the benefits of early reperfusion following coronary occlusion have become well established. Such reperfusion is usually achieved in the clinical setting with thrombolytic drugs (or with balloon angioplasty, in recent years) and translates into a substantial improvement in patient survival (GISSI 1986; ISIS 1988). However, it has also been realised that reperfusion of ischaemic myocardium may itself cause detrimental effects in the tissue to which blood flow is being restored (BRAUNWALD and KLONER 1985).

Keywords

Superoxide Aspirin Adenosine Nitrite Arginine 

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References

  1. Amrani M, Chester AH, Jayakumar J, Schyns CJ, Yacoub MH (1995) L-arginine reverses low coronary reflow and enhances post-ischaemic recovery of cardiac mechanical function. Cardiovasc Res 30:200–204PubMedGoogle Scholar
  2. Bartunek J, Shah AM, Vanderheyden M, Paulus WJ (1997) Dobutamine enhances cardiodepressant effects of receptor-mediated coronary endothelial stimulation. Circulation 95:90–96PubMedGoogle Scholar
  3. Beckman JS, Koppenol WH (1996) Nitric oxide, Superoxide, and peroxynitrite: the good, the bad, and the ugly. Am J Physiol 271:C1424–C1437PubMedGoogle Scholar
  4. Beckman JS, Beckman TW, Chen J, Marshall PA, Freeman BA (1990) Apparent hydroxyl radical production by peroxynitrite: implications for endothelial injury from nitric oxide and Superoxide. Proc Natl Acad Sci USA 87:1620–1624PubMedGoogle Scholar
  5. Beresewicz A, Karwatowska-Prokopczuk E, Lewartowski B, Cedro-Ceremuzynska K (1995) A protective role of nitric oxide in isolated ischaemic/reperfused rat heart. Cardiovasc Res 30:1001–1008PubMedGoogle Scholar
  6. Bolli R (1996) The early and late phases of preconditioning against myocardial stunning and the essential role of oxyradicals in the late phase: an overview. Basic Res Cardiol 91:57–63PubMedGoogle Scholar
  7. Bolli R, Jeroudi MO, Patel BS, Aruoma OI, Halliwell B, Lai EK, McCay PB (1989) Marked reduction of free radical generation and contractile dysfunction by antioxidant therapy begun at the time of reperfusion. Circ Res 65:607–622PubMedGoogle Scholar
  8. Bolli R, Bhatti ZA, Tang X-L, Qui Y, Zhang Q, Guo Y, Jadoon AK (1997) Evidence that late preconditioning against myocardial stunning in conscious rabbits is triggered by the generation of nitric oxide. Circ Res 81:42–52PubMedGoogle Scholar
  9. Braunwald E, Kloner RA (1982) The stunned myocardium: prolonged, post-ischaemic ventricular dysfunction. Circulation 66:1146–1149PubMedGoogle Scholar
  10. Braunwald E, Kloner RA (1985) Myocardial reperfusion: a double-edged sword? J Clin Invest 76:1713–1719PubMedGoogle Scholar
  11. Clancy RM, Leszczynska-Piziak J, Abramson SB (1992) Nitric oxide, an endothelial cell relaxation factor, inhibits neutrophil Superoxide anion production via a direct action on the NADPH oxidase. J Clin Invest 90:1116–1121PubMedGoogle Scholar
  12. Curtis MJ, Pabla R (1997) Nitric oxide supplementation or synthesis block — which is the better approach to treatment of heart disease? Trends Pharmacol Sci 18:239–244PubMedGoogle Scholar
  13. Darley-Usmar V, Halliwell B (1996) Reactive nitrogen species, reactive oxygen species, transition metal ions, and the vascular system. Pharmaceut Res 13:649–662Google Scholar
  14. Denicola A, Freeman BA,Trujillo M, Radi R (1996) Peroxynitrite reaction with carbon dioxide/bicarbonate kinetics and influence on peroxynitrite-mediated oxidations. Arch Biochem Biophys 333:49–58PubMedGoogle Scholar
  15. Depré C, Vanoverschelde J-L, Goudemant J-F, Mottet I, Hue L (1995) Protection against ischaemic injury by nonvasoactive concentrations of nitric oxide synthase inhibitors in the perfused rabbit heart. Circulation 92:1911–1918PubMedGoogle Scholar
  16. Depré C, Fiérain L, Hue L (1997) Activation of nitric oxide synthase by ischaemia in the perfused heart. Cardiovasc Res 33:82–87PubMedGoogle Scholar
  17. Draper NJ, Shah AM (1997) Beneficial effects of a nitric oxide donor on recovery of contractile function following brief hypoxia in isolated rat heart. J Moll Cell Cardiol 29:1195–1205Google Scholar
  18. Du Toit EF, McCarthy J, Miyashiro J, Opie LH, Brunner F (1998) Effect of nitrovasodilators and inhibitors of nitric oxide synthase on ischaemic and reperfusion function of rat isolated hearts. Br J Pharmacol 123:1159–1167PubMedGoogle Scholar
  19. Eiserich JP, Hristova M, Cross CE, Jones AD, Freeman BA, Halliwell B, Van der Vliet A (1998) Formation of nitric oxide-derived inflammatory oxidants by myeloperoxidase in neutrophils. Nature 391:393–397PubMedGoogle Scholar
  20. Engelman DT, Watanabe M, Engelman RM, Rousou JA, Flack JE, Deaton DW, Das DK (1995) Constitutive nitric oxide release is impaired after ischaemia and reperfusion. J Thorac Cardiovasc Surg 110:1047–1053PubMedGoogle Scholar
  21. Engelman DT, Watanabe M, Maulik N, Engelman RM, Rousou JA, Flack JE, Deaton DW, Das DK (1996) Critical timing of nitric oxide supplementation in cardioplegic arrest and reperfusion. Circulation 94(suppl II): II-407-II-411Google Scholar
  22. Engler RL, Schmid-Schonbein GW, Pravelec RS (1983) Leukocyte capillary plugging in myocardial ischaemia and reperfusion in the dog. Am J Pathol 111:98–111PubMedGoogle Scholar
  23. Ferrari R, Agnoletti L, Comini L, Gaia G, Bachetti T, Cargnoni A, Ceconi C, Curello S, Visioli O (1998) Oxidative stress during myocardial ischaemia and heart failure. Eur Heart J 19(suppl B): B2–B11PubMedGoogle Scholar
  24. Flesch M, Kilter H, Cremers B, Lenz O, Sudkamp M, Kuhn-Regnier F, Bohm M (1997) Acute effects of nitric oxide and cyclic GMP on human myocardial contractility. J Pharmacol Exp Ther 281:1340–1349PubMedGoogle Scholar
  25. Gauthier TW, Davenpeck KL, Lefer AM (1994) Nitric oxide attenuates leukocyteendothelial interaction via P-selectin in splanchnic ischaemia-reperfusion. Am J Physiol 267:H562–H568Google Scholar
  26. Giraldez RR, Panda A, Xia Y, Sanders SP, Zweier JL (1997) Decreased nitric oxide synthase activity causes impaired endothelium-dependent relaxation in the postischaemic heart. J Biol Chem 272(34): 21420–21426PubMedGoogle Scholar
  27. Golino P, Ambrosio G, Pascucci I, Ragni M, Russolillo E, Chiariello M (1992) Experimental carotid stenosis and endothelial injury in the rabbit: an in vivo model to study intravascular platelet aggregation. Thromb Haemost 67(3): 302–305PubMedGoogle Scholar
  28. Grocott-Mason R, Anning P, Evans HG, Lewis MJ, Shah AM (1994a) Modulation of left ventricular relaxation in the isolated ejecting heart by endogenous nitric oxide. Am J Physiol 267:H1804–H1813PubMedGoogle Scholar
  29. Grocott-Mason RM, Fort S, Lewis MJ, Shah AM (1994b) Myocardial relaxant effect of exogenous nitric oxide in isolated ejecting hearts. Am J Physiol 266:H1699–H1705PubMedGoogle Scholar
  30. Gruppo Italiano Per lo Studio della Streptochinasi nell’Infarto miocardico (GISSI) (1986) Effectiveness of intravenous thrombolytic treatment in acute myocardial infarction. Lancet 1(8478): 397–402Google Scholar
  31. Hare JM, Givertz MM, Creager MA, Colucci WS (1998) Increased sensitivity to nitric oxide synthase inhibition in patients with heart failure. Potentiation of β-adrenergic inotropic responsiveness. Circulation 97:161–166PubMedGoogle Scholar
  32. Harrison DG (1997) Cellular and molecular mechanisms of endothelial cell dysfunction. J Clin Invest 100:2153–2157PubMedGoogle Scholar
  33. Hasebe N, Shen Y-T, Vatner SF (1993) Inhibition of endothelium-derived relaxing factor enhances myocardial stunning in conscious dogs. Circulation 88:2862–2871PubMedGoogle Scholar
  34. Hoshida S, Yamashita N, Igarashi J, Nishida M, Hori M, Kamada T, Kuzuya T, Tada M (1995) Nitric oxide synthase protects the heart against ischaemia-reperfusion injury in rabbits. J Pharmacol Exp Ther 274:413–418PubMedGoogle Scholar
  35. Inauen ME, Granger DN, Meininger CJ, Schelling ME, Granger HJ, Kvietys PR (1990) Anoxia-reoxygenation-induced, neutrophil-mediated endothelial cell injury: role of elastase. Am J Physiol 28:H925–931Google Scholar
  36. ISIS-2 (Second International Study of Infarct Survival) Collaborative Group (1988) Randomized trial of intravenous streptokinase, oral aspirin, both, or neither among 17187 cases of acute myocardial infarction: ISIS-2. Lancet 2(8607): 349–360Google Scholar
  37. Johnson G, Tsao PS, Mulloy D, Lefer AM (1990) Cardioprotective effects of acidified sodium nitrite in myocardial ischaemia with reperfusion. J Pharmacol Exp Ther 252(1): 35–41PubMedGoogle Scholar
  38. Johnson G,Tsao PC, Lefer AM (1991) Cardioprotective effects of authentic nitric oxide in myocardial ischaemia with reperfusion. Crit Care Med 19: 244–252PubMedGoogle Scholar
  39. Kelly RA, Balligand JL, Smith TW (1996) Nitric oxide and cardiac function. Circ Res: 79:363–380PubMedGoogle Scholar
  40. Kitakaze M, Node K, Komamura K, Minamino T, Inoue M, Hori M, Kamada T (1995) Evidence for nitric oxide generation in the cardiomyocytes: its augmentation by hypoxia. J Mol Cell Cardiol 27:2149–2154PubMedGoogle Scholar
  41. Kloner RA, Ganote CE, Jennings RB (1974) The “no-reflow” phenomenon after temporary coronary occlusion in the dog. J Clin Invest 54:1496–1508PubMedGoogle Scholar
  42. Ku DD (1982) Coronary vascular reactivity after acute myocardial ischaemia. Science 218:576–578PubMedGoogle Scholar
  43. Kumar M, Liu G-J, Floyd RA, Grammas P (1996) Anoxic injury of endothelial cells increases production of nitric oxide and hydroxyl radicals. Biochem Biophys Res Comm 219: 497–501PubMedGoogle Scholar
  44. Lawson DL, Mehta JL, Nichols WW (1990) Coronary reperfusion in dogs inhibits endothelium-dependent relaxation: role of Superoxide radicals. Free Radic Biol Med 8:373–380PubMedGoogle Scholar
  45. Lefer DJ (1995) Myocardial protective actions of nitric oxide donors after myocardial ischaemia and reperfusion. New Horizons 3(1): 105–112PubMedGoogle Scholar
  46. Lefer AM, Lefer DJ (1996) The role of nitric oxide and cell adhesion molecules on the microcirculation in ischaemia-reperfusion. Cardiovasc Res 32:743–751PubMedGoogle Scholar
  47. Lefer AM, Tsao PS, Lefer DJ, Ma X-L (1991) Role of endothelial dysfunction in the pathogenesis of reperfusion injury after myocardial ischaemia. FASEB J 5:2029–2034PubMedGoogle Scholar
  48. Lefer DJ, Nakanishi K, Johnson WE, Vinten-Johansen J (1993a) Antineutrophil and myocardial protection actions of a novel nitric oxide donor after acute myocardial ischaemia and reperfusion in dogs. Circulation 88:2337–2350PubMedGoogle Scholar
  49. Lefer DJ, Klunk DA, Lutty GA (1993b) Nitric oxide (NO) donors reduce basal ICAM-1 expression on human aortic endothelial cells (HAECs). Circulation 88:1–565Google Scholar
  50. Lefer DJ, Nakanishi K, Vinten-Johansen J (1993c) Endothelial and myocardial cell protection by a cysteine-containing nitric oxide donor after myocardial ischaemia and reperfusion. J Cardiovasc Pharmacol 22(suppl 7): S34–S43PubMedGoogle Scholar
  51. Lefer DJ, Scalia R, Campbell B, Nossuli T, Hayward R, Salamon M, Grayson J, Lefer AM (1997) Peroxynitrite inhibits leukocyte-endothelial cell interactions and protects against ischaemia-reperfusion injury in rats. J Clin Invest 99: 684–691PubMedGoogle Scholar
  52. Linz W, Weimer G, Scholkens BA (1992) ACE-inhibition induces NO-formation in cultured bovine endothelial cells and protects isolated ischaemic rat hearts. J Mol Cell Cardiol 24:909–919PubMedGoogle Scholar
  53. Liu P, Hock CE, Nagele R, Wong PY-K (1997) Formation of nitric oxide, Superoxide and peroxynitrite in myocardial ischaemia-reperfusion injury in rats. Am J Physiol 272:H2327–H2336PubMedGoogle Scholar
  54. Lu HR, Remeysen P, de Clerck F (1995) Does the anti-arrhythmic effect of ischaemic preconditioning in rats involve the L-arginine nitric oxide pathway. J Cardiovasc Pharmacol: 25:524–530PubMedGoogle Scholar
  55. Ma X-L, Weyrich AS, Lefer DJ, Lefer AN (1993) Diminished basal nitric oxide release after myocardial neutrophil adherence to coronary endothelium. Circ Res 72:403–412PubMedGoogle Scholar
  56. Manning AS, Hearse DJ (1984) Reperfusion-induced arrhythmias: mechanisms and prevention. J Moll Cell Cardiol 16:497–518Google Scholar
  57. Massoudy P, Becker BF, Gerlach E (1995) Nitric oxide accounts for post-ischaemic cardioprotection resulting from angiotensin-converting enzyme inhibition: indirect evidence for a radical scavenger effect in isolated guinea pig heart. J Cardiovasc Pharmacol 25:440–447PubMedGoogle Scholar
  58. Matheis G, Sherman MP, Buckberg GD, Haybron DM, Young HH, Ignarro LJ (1992) Role of L-arginine-nitric oxide pathway in myocardial reoxygenation injury. Am J Physiol 262:H616–H620PubMedGoogle Scholar
  59. Mayer B, Hemmens B (1997) Biosynthesis and action of nitric oxide in mammalian cells. Trends Biochem Sci 22(12): 477–481PubMedGoogle Scholar
  60. Mehta JL, Lawson DL, Nichols WW (1989a) Attenuated coronary relaxation after reperfusion: effects of superoxide dismutase and TxA2 inhibitor U63557. Am J Physiol 257:H1240–H1246PubMedGoogle Scholar
  61. Mehta JL, Nichols WW, Donnelly WH, Lawson DL, Thompson L, Riet Mt, Saldeen TGP (1989b) Protection by Superoxide dismutase from myocardial dysfunction and attenuation of vasodilator reserve after coronary occlusion and reperfusion in the dog. Circ Res 65:1283–1295PubMedGoogle Scholar
  62. Méry PF, Abi-Gerges N, Vandecasteele G, Jurevicius J, Eschenhagen T, Fischmeister R (1997) Muscarinic regulation of the L-type calcium current in isolated cardiac myocytes. Life Sci 60:1113–1120PubMedGoogle Scholar
  63. Michel T, Feron O (1997) Nitric oxide synthases: which, where, how and why? J Clin Invest 100:2146–2152PubMedGoogle Scholar
  64. Mohan P, Brutsaert DL, Paulus WJ, Sys SU (1996) Myocardial contractile response to nitric oxide and cGMP. Circulation 93:1223–1229PubMedGoogle Scholar
  65. Morita K, Sherman NSP, Buckberg GD, Ihnken K, Matheis G, Young HH, Ignarro LJ (1995) Studies of hypoxaemic/reperfusion injury: without aortic clamping. Role of the L-arginine-nitric oxide pathway: the nitric oxide paradox. J Thorac Cardiovasc Surg 110:1200–1211PubMedGoogle Scholar
  66. Murry CE, Jennings RB, Reimer KA (1986) Preconditioning with ischaemia: a delay of lethal cell injury in ischaemic myocardium. Circulation 74:1124–1136PubMedGoogle Scholar
  67. Nakanishi K, Vinten-Johansen J, Lefer DJ, Zhao Z, Fowler WC, McGee S, Johnston WE (1992) Intracoronary L-arginine during reperfusion improves endothelial function and reduces infarct size. Am J Physiol 263:H1650–H1658PubMedGoogle Scholar
  68. Naseem SA, Kontos MC, Rao PS, Jesse RL, Hess ML, Kukreja RC (1995) Sustained inhibition of nitric oxide by N G-nitro-L-arginine improves myocardial function following ischaemia/reperfusion in isolated perfused rat heart. J Moll Cell Cardiol 27:419–426Google Scholar
  69. Node K, Kitakaze M, Kosaka H, Komamura K, Minamino T, Tada M, Inoue M, Hori M, Kamada T (1995) Plasma nitric oxide end-products are increased in the ischaemic canine heart. Biochem Biophys Res Comm 211(2): 370–374PubMedGoogle Scholar
  70. Nossuli TO, Hayward R, Scalia R, Lefer AM (1997) Peroxynitrite reduces myocardial infarct size and preserves coronary endothelium after ischaemia and reperfusion in cats. Circulation 96:2317–2324PubMedGoogle Scholar
  71. Pabla R, Curtis MJ (1995) Effects of NO modulation on cardiac arrhythmias in the rat isolated heart. Circ Res 77:984–992PubMedGoogle Scholar
  72. Pabla R, Curtis NJ (1996) Effect of endogenous nitric oxide on cardiac systolic and diastolic function during ischaemia and reperfusion in the rat isolated perfused heart. J Mol Cell Cardiol 28:2111–2121PubMedGoogle Scholar
  73. Pabla R, Buda AJ, Flynn DM, Salzberg DB, Lefer DJ (1995) Intracoronary nitric oxide improves post-ischaemic coronary blood flow and myocardial contractile function. Am J Physiol 269: H1113–H1121PubMedGoogle Scholar
  74. Pabla R, Buda AJ, Flynn DM, Blessé SA, Shin AM, Curtis MJ, Lefer DJ (1996) Nitric oxide attenuates neutrophil-mediated myocardial contractile dysfunction after ischaemia and reperfusion. Circ Res 78:65–72PubMedGoogle Scholar
  75. Patel VC, Yellon DM, Singh KJ, Neild GH, Woolfson RG (1993) Inhibition of nitric oxide limits infarct size in the in situ rabbit heart. Biochem Biophys Res Comm 194:234–238PubMedGoogle Scholar
  76. Paulus WJ, Vantrimpont PJ, Shah AM (1994) Acute effects of nitric oxide on left ventricular relaxation and diastolic distensibility in man. Circulation 89: 2070–2078PubMedGoogle Scholar
  77. Paulus WJ, Vantrimpont PJ, Shah AM (1995) Paracrine coronary endothelial control of left ventricular function in humans. Circulation 92:2119–2126PubMedGoogle Scholar
  78. Pearson PJ, Lin PJ, Schaff HV (1992) Global myocardial ischaemia and reperfusion impair endothelium-dependent relaxations to aggregating platelets in the canine coronary artery. J Thorac Cardiovasc Surg 103:1147–1154PubMedGoogle Scholar
  79. Pinsky DJ, Patton S, Mesaros S, Brovkovych V, Kubaszewski E, Grunfeld S, Malinski T (1997) Mechanical transduction of nitric oxide synthesis in the beating heart. Circ Res 81:372–379PubMedGoogle Scholar
  80. Piper HM, Garcia-Dorado D, Ovize M (1998) A fresh look at reperfusion injury. Cardiovasc Res 38:291–300PubMedGoogle Scholar
  81. Prendergast BD, Sagach VF, Shah AM (1997) Basal release of nitric oxide augments the Frank-Starling response in the isolated heart. Circulation 96:1320–1329PubMedGoogle Scholar
  82. Reimer KA, Jennings RB (1979) The “wavefront phenomenon” of myocardial ischaemic cell death. IL Transmural progression of necrosis within the framework of ischaemic bed size (myocardium at risk) and collateral flow. Lab Invest 40:633–644PubMedGoogle Scholar
  83. Sato H, Zhao ZQ, McGee D, Williams MW, Hammon JW, Vinten-Johansen J (1995) Supplemental L-arginine during cardioplegic arrest and reperfusion avoids regional post-ischaemic injury. J Thorac Cardiovasc Surg 110:302–314PubMedGoogle Scholar
  84. Schluter KD, Weber M, Schraven E, Piper HM (1994) NO donor SIN-1 protects against reoxygenation-induced cardiomyocyte injury by a dual action. Am J Physiol 267:H1461–H1466PubMedGoogle Scholar
  85. Schluter KD, Jakob G, Ruiz-Meana M, Garcia-Dorado D, Piper HM (1996) Protection of reoxygenated cardiomyocytes against osmotic fragility by nitric oxide donors. Am J Physiol 271:H428–H434PubMedGoogle Scholar
  86. Schulz R, Wambolt R (1995) Inhibition of nitric oxide synthesis protects the isolated working rabbit heart from ischaemia-reperfusion injury. Cardiovasc Res 30:432–439PubMedGoogle Scholar
  87. Seccombe JF, Schaff HV (1995) Coronary artery endothelial function after myocardial ischaemia and reperfusion. Ann Thorac Surg 60:778–788PubMedGoogle Scholar
  88. Shah AM (1996) Paracrine modulation of heart cell function by endothelial cells. Cardiovasc Res 31:847–867PubMedGoogle Scholar
  89. Shah AM, Spurgeon H, Sollott SJ, Talo A, Lakatta EG (1994) 8-Bromo cyclic GMP reduces the myofilament response to calcium in intact cardiac myocytes. Circ Res 74:970–978PubMedGoogle Scholar
  90. Shah AM, Silverman HS, Griffiths EJ, Spurgeon HA, Lakatta EG (1995) cGMP prevents delayed relaxation at reoxygenation after brief hypoxia in isolated cardiac myocytes. Am J Physiol 268:H2396–H2404PubMedGoogle Scholar
  91. Shiki K, Hearse DJ (1987) Preconditioning of ischaemic myocardium: reperfusioninduced arrhythmias. Am J Physiol 253:H1470–H1476PubMedGoogle Scholar
  92. Siegfried MR, Erhardt J, Rider T, Ma X-L, Lefer AM (1992a) Cardioprotection and attenuation of endothelial dysfunction by organic nitric oxide donors in myocardial ischaemia-reperfusion. J Pharmacol Exp Ther 260:668–675PubMedGoogle Scholar
  93. Siegfried MR, Carey C, Ma X-L, Lefer AM (1992b) Beneficial effects of SPM 5185, a cysteine-containing NO donor in myocardial ischaemia-reperfusion. Am J Physiol 263:H771–H777PubMedGoogle Scholar
  94. Smith JA, Shah AM, Lewis MJ, (1991) Factors released from endocardium of the ferret and pig modulate myocardial contraction. J Physiol Lond 439:1–14PubMedGoogle Scholar
  95. Sun W, Wainwright CL (1997) The role of nitric oxide in modulating ischaemia-induced arrhythmias in rats. J Cardiovasc Pharmacol 29: 554–562PubMedGoogle Scholar
  96. Szabolcs M, Michler RE, Yang X, Aji W, Roy D, Athan E, Sciacca RR, Minanov OP, Cannon PJ (1996) Apoptosis of cardiac myocytes during cardiac allograft rejection. Relation to induction of nitric oxide synthase. Circulation 94:1665–1673PubMedGoogle Scholar
  97. Szekeres M, Dezsi L, Monos E, Metsa-Ketela T (1997) Effect of a new nitric oxide donor on the biomechanical performance of the isolated ischaemic rat heart. Acta Physiol Scand 161:55–61PubMedGoogle Scholar
  98. Thompson and Hess (1986) The oxygen free radical system: a fundamental mechanism in the production of myocardial necrosis. Prog Cardiovasc Dis 28:449–492Google Scholar
  99. Tsao PS, Lefer AM (1990) Time course and mechanism of endothelial dysfunction in isolated ischaemic and hypoxic perfused rat hearts. Am J Physiol 259: H1660–H1666PubMedGoogle Scholar
  100. Tsao PS, Aoki N, Lefer DJ, Johnson G, Lefer AM (1990) Time course of endothelial dysfunction and myocardial injury during myocardial ischaemia and reperfusion in the cat. Circulation 82:1402–1412PubMedGoogle Scholar
  101. Van Benthuysen KM, McMurtry IF, Horowitz LD (1987) Reperfusion after acute coronary occlusion in dogs impairs endothelium-dependent relaxation to acetylcholine and augments contractile reactivity in vitro. J Clin Invest 79: 265–274Google Scholar
  102. Vegh A, Szekeres L, Parratt JR (1992a) Preconditioning of the ischaemic myocardium; involvement of the L-arginine nitric oxide pathway. Br J Pharmacol 107:648–652PubMedGoogle Scholar
  103. Vegh A, Gy Papp J, Szekeres L, Parratt JR (1992b) The local intracoronary administration of methylene blue prevents the pronounced anti-arrhythmic effect of ischaemic preconditioning. Br J Pharmacol 107:910–911PubMedGoogle Scholar
  104. Vegh A, Gy Papp J, Szekeres L, Parratt JR (1993) Prevention by an inhibitor of the L-arginine-nitric oxide pathway of the anti-arrhythmic effects of bradykinin in anaesthetized dogs. Br J Pharmacol 110:18–19PubMedGoogle Scholar
  105. Wang P, Zweier JL (1996) Measurement of nitric oxide and peroxynitrite generation in the post-ischaemic heart. J Biol Chem 271:29223–29230PubMedGoogle Scholar
  106. Weselcouch EO, Baird AJ, Sleph P, Grover GJ (1995) Inhibition of nitric oxide synthesis does not affect ischaemic preconditioning in isolated perfused rat hearts. Am J Physiol 268:H242–H249PubMedGoogle Scholar
  107. Weyrich AS, Ma X-L, Lefer AM (1992) The role of L-arginine in ameliorating reperfusion injury after myocardial ischaemia in the cat. Circulation 86:279–288PubMedGoogle Scholar
  108. Wildhirt SM, Dudek RR, Suzuki H, Pinto V, Narayan KS, Bing RJ (1995) Immunohistochemistry in the identification of nitric oxide synthase isoenzymes in myocardial infarction. Cardiovasc Res 29:526–531PubMedGoogle Scholar
  109. Williams MW,Taft CS, Ramnauth S, Zhao Z-Q, Vinten-Johansen J (1995) Endogenous nitric oxide (NO) protects against ischaemia-reperfusion injury in the rabbit. Cardiovasc Res 30:79–86PubMedGoogle Scholar
  110. Wink DA, Hanbauer I, Krishna MC, DeGraff W, Gamson J, Mitchell JB (1993) Nitric oxide protects aginst cellular damage and cytotoxicity from reactive oxygen species. Proc Natl Acad Sci USA 90:9813–9817PubMedGoogle Scholar
  111. Woolfson RG, Patel VC, Neild GH, Yellon DM (1995) Inhibition of nitric oxide synthesis reduces infarct size by an adenosine-dependent mechanism. Circulation 91:1545–1551PubMedGoogle Scholar
  112. Xie Y-W, Shen W, Zhao G, Xu X, Wolin MS, Hintze TH (1996) Role of endotheliumderived nitric oxide in the modulation of canine myocardial mitochondrial respiration in vitro. Circ Res 79:382–387Google Scholar
  113. Xie Y-W, Kaminski PM, Wolin MS (1998) Inhibition of rat cardiac muscle contraction and mitochondrial respiration by endogenous peroxynitrite formation during post-hypoxic reoxygenation. Circ Res 82:891–897PubMedGoogle Scholar
  114. Yasmin W, Strynadka KD, Schulz R (1997) Generation of peroxynitrite contributes to ischaemia-reperfusion injury in isolated rat hearts. Cardiovasc Res 33:422–432PubMedGoogle Scholar
  115. Yellon DM, Baxter GF, Garcia-Dorado D, Heusch G, Sumeray MS (1998) Ischaemic preconditioning: present position and future directions. Cardiovasc Res 37:21–33PubMedGoogle Scholar
  116. Zhang X, Xie Y-W, Nasjletti A, Xu X, Wolin MS, Hintze TH (1997) ACE inhibitors promote nitric oxide accumulation to modulate myocardial oxygen consumption. Circulation 95:176–182PubMedGoogle Scholar
  117. Zweier JL (1988) Measurement of superoxide-derived free radicals in the reperfused heart. Evidence for a free radical mechanism of reperfusion injury. J Biol Chem 263:1353–1357PubMedGoogle Scholar

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Authors and Affiliations

  • P. A. MacCarthy
  • A. M. Shah

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