Endogenous protection against reperfusion-induced ventricular fibrillation: Role of neuronal versus non-neuronal sources of nitric oxide and species dependence in the rat versus rabbit isolated heart

Journal of Molecular and Cellular Cardiology

Volumn 28, Issue 10, 1996, Pages 2097-2110

  Pabla, Ravinder ^a   Curtis, Michael J ^a  

^a UNIVERSITY OF LONDON   (United Kingdom)

Author keywords

7 Nitro indazole; L Arginine; L NAME; Nitric oxide; Reperfusion; Ventricular fibrillation

Indexed keywords

7 NITROINDAZOLE; ARGININE; ARGININE METHYL ESTER; NITRIC OXIDE; SUBSTANCE P;

ANIMAL TISSUE; ARTICLE; CHEMOLUMINESCENCE; CONTROLLED STUDY; CORONARY ARTERY BLOOD FLOW; HEART MUSCLE ISCHEMIA; HEART MUSCLE REPERFUSION; HEART PROTECTION; HEART VENTRICLE FIBRILLATION; ISOLATED HEART; MALE; NONHUMAN; PRIORITY JOURNAL; RABBIT; RAT; SPECIES DIFFERENCE; VASODILATATION;

ANIMALIA; ORYCTOLAGUS CUNICULUS;

EID: 0030271605     PISSN: 00222828     EISSN: None     Source Type: Journal    
DOI: 10.1006/jmcc.1996.0202     Document Type: Article

References (62)

1. ADKINS WK, TAYLOR AE, 1990. Role of xanthine and neutrophils in ischemia-reperfusion injury in rabbit lung. J Appl Physiol 69: 2012-2018.
2. AMEZCUA JL, PALMER RMJ, DE SOUZA BM, MONCADA S, 1989. Nitric oxide synthesised from L-arginine regulates vascular tone in the coronary circulation of the rabbit. Br J Pharmacol 97: 1119-1124.
3. BABBEDGE RC, BLAND-WARD P, HART SL, MOORE PK, 1993. Inhibition of rat cerebellar nitric oxide synthase by 7-nitro indazole and related substituted indazoles. Br J Pharmacol 110: 225-228.
4. BARNES CS, COKER SJ, 1993. The effects of zaprinast on ischaemia-induced arrhythmias and cardiac cyclic nucleotides (Abstract). Br J Pharmacol 108: 119.
5. BERNIER M, CURTIS MJ, HEARSE DJ, 1989. Ischaemia-induced and reperfusion-induced arrhythmias: the importance of heart rate. Am J Physiol 256: H21-H31.
6. CANO J-P, GUILLEN J-C, JOUVRE R, LANGLET F, PUDDU P-E, ROLLAND P-H, SERRADIMIGNI A, 1986. Molsidomine prevents post-ischaemic ventricular fibrillation in dogs. Br J Pharmacol 88: 779-789.
7. COKER SJ, 1989. Anesthetized rabbits as a model for ischemia-and reperfusion-induced arrhythmias. J Pharmacol Methods 21: 263-279.
8. CURTIS MJ, HEARSE DJ, 1989a. Reperfusion-induced arrhythmias are critically dependent upon occluded zone size: relevance to the mechanism of arrhythmogenesis. J Mol Cell Cardiol 21: 625-637.
9. CURTIS MJ, HEARSE DJ, 1989b. Ischemia-induced and reperfusion-induced arrhythmias differ in their sensitivity to potassium: implications for mechanism of initiation and maintenance of ventricular fibrillation. J Mol Cell Cardiol 21: 21-40.
10. CURTIS MJ, PUGSLEY MK, WALKER MJA, 1993. Endogenous chemical mediators of ventricular arrhythmias in ischaemic heart disease. Cardiovasc Res 27: 703-719.
11. DOWNEY JM, MIURA T, EDDY LJ, CHAMBERS DE, MELLERT T, HEARSE DJ, YELLON DM, 1987. Xanthine oxidase is not a source of free radicals in the ischemic rabbit heart. J Mol Cell Cardiol 19: 1053-1060.
12. ELFELLAH MS, OGILVIE RI, 1985. Effect of vasodilator drugs on coronary occlusion and reperfusion arrhythmias in anaesthetised dogs. J Cardiovasc Pharmacol 7: 826-832.
13. FEELISCH M, NOACK E, 1987. Nitric oxide (NO) formation from nitrovasodilators occurs independently of hemoglobin or non-heme iron. Eur J Pharmacol 142: 465-469.
14. FURCHGOTT RF, 1984. The role of endothelium in the responses of vascular smooth muscle to drugs. Ann Rev Pharmacol Toxicol 24: 175-197.
15. GALINANES M, HEARSE DJ, 1990. Species differences in susceptibility to ischemic injury and response to myocardial protection. Cardioscience 2: 127-142.
16. GODIN DV, BHIMJI S, 1987. Effects of allopurinol on myocardial ischemic injury induced by coronary artery ligation and reperfusion. Biochem Pharmacol 36: 2101-2107.
17. GRYGLEWSKI RJ, PALMER RMT, MONCADA S, 1986. Superoxide anion is involved in the breakdown of endothelium-derived vascular relaxing factor. Nature 320: 454-456.
18. HASSALL CJS, SAFFREY MJ, BELAI A, HOYLE CHV, MOULES EW, MOSS J, SCHMIDT HHHW, MURAD F, FÖRSTERMANN U, BURNSTOCK G, 1992. Nitric oxide synthase immunoreactivity and NADPH-diaphorase activity in a subpopulation of intrinsic neurones of the guinea-pig heart. Neurosci Lett 143: 65-68.
19. HIBBS JB, TAINTOR RR, VAVRIN Z, RACHLIN EM, 1988. Nitric oxide: a cytotoxic activated macrophage effector molecule. Biochem Biophys Res Commun 157: 87-94.
20. IBUKI C, HEARSE DJ, AVKIRAN M, 1992. Rate of reflow and reperfusion induced arrhythmias: studies with dual coronary perfusion. Cardiovasc Res 26: 316-323.
21. KENNEDY TP, PAO NV, HOPKINS C, PENNINGTON L, TOLLEY E, HOIDAL JR, 1989. Role of reactive oxygen species in reperfusion injury of the rabbit lung. J Clin Invest 83: 1326-1335.
22. KLIMASCHEWSKI L, KUMMER W, MAYER B, COURAUD JY, PREISSLER U, PHILIPPIN B, HEYM C, 1992. Nitric oxide synthase in cardiac nerve fibers and neurons of rat and guinea pig heart. Circ Res 71: 1533-1537.
23. KU DD, 1982. Coronary vascular reactivity after acute myocardial ischemia. Science 218: 576-578.
24. LEFER DJ, NAKANISHI K, JOHNSTON WE, VINTEN-JOHANSEN J, 1993. Antineutrophil and myocardial protecting actions of a novel nitric oxide donor after acute myocardial ischemia and reperfusion in dogs. Circulation 88: 2337-2350.
25. LOWENSTEIN CJ, SNYDER SH, 1992. Nitric oxide, a novel biologic messenger. Cell 70: 705-707.
26. MAINLAND D, HARRERA L, SUTCLIFFE MI, 1956. Statistical Tables for Use With Binomial Samples: Contingency Tests, Confidence Limits and Sample Size Estimates. New York: University College of Medicine Publications.
27. MANNING AS, HEARSE DJ, 1984. Reperfusion-induced arrhythmias: Mechanisms and prevention. J Mol Cell Cardiol 16: 497-518.
28. MARLETTA MA, YOON PS, IYENKAR R, LEAF CD, WISHNIK JS, 1988. Macrophage oxidation of L-arginine to nitrite and nitrate: nitric oxide is an intermediate. Biochem 27: 8706-8711.
29. MARTORANA PA, MOGILEV AM, KETTENBACH B, NITZ R-E, 1983. Effect of molsidomine on spontaneous ventricular fibrillation following myocardial ischaemia and reperfusion in the dog. Adv Myocardiol 4: 606-613.
30. MAXWELL MP, HEARSE DJ, YELLON DM, 1987. Species variation in the collateral circulation during regional myocardial infarction. Cardiovasc Res 21: 737-746.
31. MENON NK, PATARICZA T, BINDER T, BING RJ, 1991. Reduction of biological effluents in purge and trap micro reaction vessels and detection of endothelium-derived nitric oxide (Edno) by chemiluminescence. J Mol Cell Cardiol 23: 389-393.
32. MONCADA S, PALMER RMJ, HIGGS EA, 1991. Nitric oxide: physiology, pathophysiology and pharmacology. Pharmacol Rev 43: 109-142.
33. MOORE PK AL-SWAYEH OA, CHONG NW, EVANS RA, GIBSON A, 1990. L-NG-nitro arginine (L-NOARG), a novel, L-arginine-reversible inhibitor of endothelium-dependent vasodilatation in vitro. Br J Pharmacol 99: 408-412.
34. MOORE PK, BABBEDGE RC, WALLACE P, GAFFEN Z, HART SL, 1993a. 7-Nitro-indazole, an inhibitor of nitric oxide synthase, exhibits anti-nociceptive activity in the mouse without increasing blood pressure. Br J Pharmacol 108: 296-297.
35. MOORE PK, WALLACE P, GAFFEN Z, HART SL, BABBEDGE RC, 1993b. Characterisation of the novel nitric oxide synthase inhibitor 7-nitro indazole and related indazoles: antinociceptive and cardiovascular effects. Br J Pharmacol 110: 219-224.
36. MUXFELDT M, SCHAPER W, 1987. The activity of xanthine oxidase in heart of pigs, guinea pigs, rabbits, rats and humans. Basic Res Cardiol 82: 486-492.
37. MYERS CL, WEISS SJ, KIRSCH MM, SHEPARD BM, SHLAFER M, 1986. Effects of supplementing hypothermic crystalloid cardioplegic solution with catalase, superoxide dismutase, allopurinol, or deferoxamine on functional recovery of globally ischemic and reperfused isolated hearts. J Thorac Cardiovasc Surg 91: 281-289.
38. NASEEM SM, KONTOS MC, RAO PS, JESSE RL, HESS ML, KUKREJA RC, 1995. Sustained inhibition of nitric oxide by NG-nitro-L-arginine improves myocardial function following ischemia/reperfusion in isolated perfused rat heart. J Mol Cell Cardiol 27: 419-426.
39. PABLA R, BUDA AJ, FLYNN DM, SALZBERG DB, LEFER DJ, 1995a. Intracoronary nitric oxide improves post-ischemic coronary blood flow and myocardial contractile function following ischemia and reperfusion. Am J Physiol 269: H113-H121.
40. PABLA R, BLAND-WARD P, MOORE PK, CURTIS MJ, 1995b. An endogenous protectant effect of cardiac cyclic GMP against reperfusion-induced ventricular fibrillation in the rat heart. Br J Pharmacol 116: 2923-2930.
41. PABLA R, CURTIS MJ, 1995. Effect of nitric oxide modulation on cardiac arrhythmias in the rat isolated heart. Circ Res 77: 984-992.
42. PABLA R, CURTIS MJ, 1996. Effect of endogenous nitric oxide on cardiac systolic and diastolic function during ischemia and reperfusion in the rat isolated perfused heart. J Mol Cell Cardiol 28: 2111-2121.
43. PARRATT JR, 1993. Endogenous myocardial protective (antiarrhythmic) substances. Cardiovasc Res 27: 693-702.
44. PATEL VC, YELLON DM, SINGH KJ, WOOLFSON RG, 1993. Inhibition of nitric oxide limits infarct size in the in situ rabbit heart. Biochem Biophys Res Commun 194: 234-238.
45. PODZUWEIT T, DALBY AJ, CHERRY DW, OPIE LH, 1978. Cyclic AMP levels in ischemic and non-ischemic myocardium following coronary artery ligation: relation to ventricular fibrillation. J Mol Cell Cardiol 10: 81-84.
46. RADOMSKI MW, PALMER RMJ, MONCADA S, 1990. An L-arginine/nitric oxide pathway present in human platelets regulates aggregation. Proc Natl Acad Sci USA 86: 5193-5197.
47. RAVINGEROVA T, TRIBULOVA N, SLEZAK J, CURTIS MJ, 1995. Brief, intermediate and prolonged ischemia in the isolated crystalloid perfused rat heart: relationship between susceptibility to arrhythmias and degree of ultrastructural injury. J Mol Cell Cardiol 27: 1937-1951.
48. REES SA, CURTIS MJ, 1993. Specific IK1 blockade: a new antiarrhythmic mechanism? Effect of RP58866 on ventricular arrhythmias in rat, rabbit, and primate. Circulation 87: 1979-1989.
49. RUBANYI GM, DESIDERIO D, LUISI A, JOHNS A, SYBERTZ EJ, 1989. Phorbol dibutyrate inhibits release and action of endothelium-derived relaxing factor(s) in canine blood vessels. J Pharmacol Exp Ther 249: 858-863.
50. SNYDER SH, BREDT DS, 1992. Biological roles of nitric oxide. Scientific American May: 28-35.
51. TANAKA K, HEARSE DJ, 1988. Reperfusion-induced arrhythmias in the isolated rabbit heart: characterisation of the influence of the duration of regional ischemia and the extracellular potassium concentration. J Mol Cell Cardiol 20: 201-211.
52. TANAKA K, HASSALL CJS, BURNSTOCK G, 1993. Distribution of intracardiac neurones and nerve terminals that contain a marker for nitric oxide. NADPH-diaphorase in the guinea-pig heart. Cell Tissue Res 273: 293-300.
53. TENNANT R, WIGGERS CJ, 1935. The effects of coronary occlusion on myocardial contraction. Am J Physiol 112: 351-361.
54. TERADA LS, RUBINSTEIN JD, LESNEFSKY EJ, HORWITZ LD, LEFF JA, REPINE JE, 1991. Existence and participation of xanthine oxidase in reperfusion injury of ischemic rabbit myocardium. Am J Physiol 260: H805-H810.
55. TSAO PS, AOKI N, LEFER DJ, JOHNSON G, LEFER AM, 1990. Time course of endothelial dysfunction and myocardial injury during myocardial ischemia and reperfusion in the cat. Circulation 82: 1402-1412.
56. TSUCHIHASHI K, CURTIS MJ, 1991. Influence of tedisamil on the initiation and maintenance of ventricular fibrillation: chemical defibrillation by Ito blockade? J Cardiovasc Pharmacol 18: 445-456.
57. URSELL PC, MAYES M, 1993. The majority of nitric oxide ssynthase in pig heart is vascular and not neural. Cardiovasc Res 27: 1920-1924.
58. VAN BENTHUYSEN KM, MCMURTRY IF, HORWITZ LD, 1987. Reperfusion after acute coronary occlusion in dogs impairs endothelium-dependant relaxation to acetylcholine and augments contractile reactivity in vitro. J Clin Invest 79: 265-274.
59. WAINWRIGHT CL, MARTORANA PA, 1993. Pirsidomine, a novel nitric oxide donor, suppresses ischemic arrhythmias in anesthetised pigs. J Cardiovasc Pharmacol 22 (Suppl.7): S44-S50.
60. WALKER MJA, CURTIS MJ, HEARSE DJ, CAMPBELL RWF, JANSE MJ, YELLON DM, COBB SM, COKER SJ, HARNESS JB, HARRON DWG, HIGGINS AJ, JULAN DG, LAB MJ, MANNING AS, NORTHOVER BJ, PARRATT JR, REIMERSMA RA, RIVA E, RUSSELL D, SHERIDAN DJ, WINSLOW E, WOODWARD B, 1988. The Lambeth Conventions: guidelines for the study of arrhythmias in ischaemia, infarction and reperfusion. Cardiovasc Res 22: 447-455.
61. WESSELING H, DE GRAEFF PA, VAN GILST WH, KINGMA JH, DE LANGEN CDJ, 1989. Cardiac arrhythmias - a new indication for angiotensin-converting enzyme inhibitors? J Human Hypertens 3: 89-95.
62. WOOLFSON RG, PATEL VC, NEILD GH, YELLON DM, 1995. Inhibition of nitric oxide synthesis reduces infarct size by an adenosine-dependent mechanism. Circulation 91: 1545-1551.