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Exercise and Delayed Preconditioning in the Protection of the Heart against Ventricular Arrhythmias: Crucial Role of Nitric Oxide

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Part of the book series: Progress in Experimental Cardiology ((PREC,volume 6))

Summary

Ischaemic preconditioning results not only in a reduction in myocardial ischaemic damage but also a marked suppression of those ventricular arrhythmias that result from a prolonged period of ischaemia and reperfusion insult. This protection is time-dependent and occurs in two distinct phases. There is an “early phase” of the antiarrhythmic protection which occurs immediately after the preconditioning stimulus but fades within 1 or 2 hours. However, the protection against arrhythmias reappears 20–24 hours later and this phase is termed as “delayed protection”. Protection against ischaemia and reperfusion-induced severe, often life-threatening arrhythmias can also result from brief periods of cardiac pacing, which leads to both immediate and delayed protection, and from vigorous physical exercise. Both cardiac pacing and exercise results in marked reduction in the incidence and severity of ischaemia and reperfusion-induced ventricular arrhythmias 24 hours later. This delayed protection against arrhythmias is less marked 48 and 72 hours after preconditioning but can be reinstated, and lasts for a more prolonged period, if either pacing or exercise are repeated at a time when the protection from the initial stimulus begins to wane. Although the precise mechanisms of the delayed protection results from cardiac pacing and exercise are not yet fully understood, there is some evidence that nitric oxide plays a privotal role in the antiarrhythmic protection achieved either by cardiac pacing or exercise.

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References

  1. Murry CE, Jennings RB, Reimer KA. 1986. Preconditioning with ischemia: a delay of lethal cell injury in ischemic myocardium. Circulation 74:1124–1136.

    Article  PubMed  CAS  Google Scholar 

  2. Deftly DV, Chilian WM. 1993. Preconditioning protects coronary arteriolar endothelium from ischemia-reperfusion injury. Am J Physiol 265:H700–H706.

    Google Scholar 

  3. Shiki K, Hearse DJ. 1987. Preconditioning of ischemic myocardium: reperfusion-induced arrhythmias. Am J Physiol 253:H1470–H1476.

    PubMed  CAS  Google Scholar 

  4. Végh Á, Komori S, Szekeres L, Parratt JR. 1992. Antiarrhythmic effects of preconditioning in anaesthetised dogs and rats. Cardiovasc Res 26:487–495.

    Article  PubMed  Google Scholar 

  5. Cave AC. 1995. Preconditioning induced protection against post-ischaemic contractile dysfunction: Characteristics and mechanisms. J Mol Cell Cardiol 27:969–979.

    Article  PubMed  CAS  Google Scholar 

  6. Arstall MA, Zhao YZ, Hornberger L, Kennedy SP, Buchholz RA, Osathanondh R, Kelly RA. 1998. Human ventricular myocytes in vitro exhibit both early and delayed preconditioning responses to stimulated ischaemia. J Mol Cell Cardiol 30:1019–1025.

    Article  PubMed  CAS  Google Scholar 

  7. Tomai F, Crea F, Gaspardone A, Versaci F, De Paulis R, Penta de Peppo A, Chiariello L, Gioffre PA. 1994. Ischemic preconditioning during coronary angioplasty is prevented by glibenclamide, a selective ATP-sensitive K+ channel blocker. Circulation 90:700–705.

    Article  PubMed  CAS  Google Scholar 

  8. Kuzuya T, Hoshida S, Yamashita N, Fuji H, Oe H, Hori M, Kamada T, Tada M. 1993. Delayed effects of sublethal ischemia on the acquisition of tolerance to ischemia. Circ Res 72:1293–1299.

    Article  PubMed  CAS  Google Scholar 

  9. Marber MS, Latchman DS, Walker JM, Yellon DM. 1993. Cardiac stress protein elevation 24 hours after brief ischemia or heat stress is associated with resistance to myocardial infarction. Circulation 88:1264–1272.

    Article  PubMed  CAS  Google Scholar 

  10. Ovize M, Przyklenk K, Kloner RA. 1992. Partial coronary stenosis is sufficient and complete reperfusion is mandatory for preconditioning the canine heart. Circ Res 71:1165–1173.

    Article  PubMed  CAS  Google Scholar 

  11. Shizukuda Y, Maller RT, Lee SC, Downey HF. 1992. Hypoxic preconditioning of ischemic canine myocardium. Cardiovasc Res 26:534–542.

    Article  PubMed  CAS  Google Scholar 

  12. Ovize M, Kloner RA, Przyklenk K. 1994. Stretch preconditions canine myocardium. Am J Physiol 266:H137–H146.

    PubMed  CAS  Google Scholar 

  13. Przyklenk K, Bauer B, Ovize M, Kloner RA, Whittaker P. 1993. Regional ischemic “preconditioning” protects remote virgin myocardium from subsequent sustained coronary occlusion. Circulation 87:893–899.

    Article  PubMed  CAS  Google Scholar 

  14. McClanahan TB, Nao BS, Wolke LJ, Martin BJ, Metz TE, Gallagher KP. 1993. Brief renal occlusion and reperfusion reduces myocardial infarct size in rabbits. FASEB J:A176.

    Google Scholar 

  15. Liu Y, Kato H, Nakata N, Kogure K. 1992. Protection of rat hippocampus against ischemic neuronal damage by pretreatment with sublethal ischemia. Brain Res 586:121–124.

    Article  PubMed  CAS  Google Scholar 

  16. Mounsey RA, Pang CY, Boyd JB, Forrest C. 1992. Augmentation of skeletal mucle survival in the latissimus dorsi porcine model using acute ischemic preconditioning. J Otolaryngol 21:315–320.

    PubMed  CAS  Google Scholar 

  17. Végh Á, Szekeres L, Parratt JR. 1991. Transient ischaemia induced by rapid cardiac pacing results in myocardial preconditioning. Cardiovasc Res 25:1051–1053.

    Article  PubMed  Google Scholar 

  18. Kaszala K, Végh Á, Papp JGy, Parratt JR. 1996. Time course of the protection against ischaemia and reperfusion induced ventricular arrhythmias resulting from brief periods of cardiac pacing. J Mol Cell Cardiol 28:2085–2095.

    Article  PubMed  CAS  Google Scholar 

  19. Babai L, Szigeti Zs, Parratt JR, Végh Á. 2002. Delayed cardioprotective effects of exercise in dogs are aminoguanidine sensitive: possible involvement of nitric oxide. Clin Sci 102:435–445.

    Article  PubMed  CAS  Google Scholar 

  20. Komori S, Fukimaki S, Ijili H, Asakawa T, Watanabe Y, Tamura Y, Parratt JR. 1990. Inhibitory effect of ischaemic preconditioning on ischemic arrhythmias using a rat coronary artery ligation model. Jpn Electrocardiol 10:774–782.

    Article  Google Scholar 

  21. Végh Á, Szekeres L, Parratt JR. 1990. Protective effects of preconditioning of the ischaemic myocardium involve cyclo-oxygenase products. Cardiovasc Res 24:1020–1023.

    Article  PubMed  Google Scholar 

  22. Végh Á, Kis A, Papp JGy, Parratt JR. 1998. Early and delayed protection against ventricular arrhythmias induced by preconditioning. In: The Ischaemic Heart. Ed. S Mochizuki, N Takeda, M Nagano, NS Dhalla, 279–305. Kluwer Academic Publisher.

    Chapter  Google Scholar 

  23. Li Y, Kloner RA. 1992. Cardioprotective effects of ischemic preconditioning is not mediated by prostanoids. Cardiovasc Res 26:226–231.

    Article  PubMed  CAS  Google Scholar 

  24. Lawson CS, Avkiran M, Shattock MJ, Coltart DJ, Hearse DJ. 1993. Preconditioning and reperfusion arrhythmias in the isolated rat heart: true protection or temporal shift in vulnerability? Cardiovasc Res 27:2274–2281.

    Article  PubMed  CAS  Google Scholar 

  25. Piacentini L, Wainwright CL, Parratt JR. 1993. The antiarrhythmic effect of ischaemic preconditioning in isolated rat hearts involves a pertussis toxin sensitive mechanism. Cardiovasc Res 27:674–680.

    Article  PubMed  CAS  Google Scholar 

  26. Li Y, Vasquez JA, Gallagher KP, Lucchesi BR. 1990. Myocardial protection with preconditioning. Circulation 82:609–619.

    Article  PubMed  CAS  Google Scholar 

  27. Wainwright CL, Parratt JR. 1990. Electrocardiographic and haemodynamic effects of myocardial preconditioning in pigs. J Mol Cell Cardiol 22:(Suppl. III):PF65.

    Google Scholar 

  28. Ovize M, Aupetit JF, Rioufol G, Laufona J, Andre-Fouet X, Minaire Y, Faucon G. 1995. Preconditioning reduces infarct size but accelerates time to ventricular fibrillation in ischemic pig heart. Am J Physiol 269:H72–H79.

    PubMed  CAS  Google Scholar 

  29. Parratt JR, Végh Á, Kaszala K, Papp JGy. 1996. Suppression of life-threatening ventricular arrhythmias by brief periods of ischaemia and by cardiac pacing with particular reference to delayed myocardial protection. In. Ischaemia, Preconditioning and Adaptation. Ed: M Marber and DM Yellon, 85–113. Oxford: BIOS Scientific Publishers.

    Google Scholar 

  30. Végh Á, Parratt JR. 1996. Ischaemic preconditioning markedly reduces the severity of ischaemia and reperfusion-induced arrhythmias; role of endogenous myocardial protective substances. In: Myocardial Preconditioning. Ed. CL Wainwright and JR Parratt, Berlin: Springer.

    Google Scholar 

  31. Végh Á, Papp JGy, Parratt JR. 1994. Prevention by dexamethasone of the marked antiarrhythmic effects of preconditioning induced 20 h after rapid cardiac pacing. Br J Pharmacol 113:1081–1082.

    Article  PubMed  Google Scholar 

  32. Szilvássy Z, Ferdinandy P, Bor P, Jalab I, Lonovics J, Koltai M. 1994. Ventricular overdrive pacing-induced anti-ischemic effect: a conscious rabbit model of preconditioning. Am J Physiol 266:H2033–H2141.

    PubMed  Google Scholar 

  33. Marshall RJ, Parratt JR. 1980. The early consequences of myocardial ischaemia and their modification. J Physiol (Paris) 76:699–715.

    CAS  Google Scholar 

  34. Kis A, Végh Á, Papp JG, Parratt JR. 1999. Repeated cardiac pacing extends the time during which canine hearts are protected against ischaemia-induced arrhythmias: role of nitric oxide. J Mol Cell Cardiol 31:1229–1241.

    Article  PubMed  CAS  Google Scholar 

  35. Paffenbarger RS, Hale WE, Brand RJ, Hyde RT. 1997. Work-energy level, personal characteristics, and fatal heart attack: a birthcohort effect. Am J Epidemol 105:200–213.

    Google Scholar 

  36. Siscovick DS, Weiss NS, Hallstrom AP, Inui TS, Peterson DR. 1982. Physical activity and primary cardiac arrest. JAMA 248:3113–3117.

    Article  PubMed  CAS  Google Scholar 

  37. Siskovick DS, Weiss NS, Fletcher R, Lasky T. 1984. The incidence of primary cardiac arrest during vigorous exercise. N Engl J Med 311:874–877.

    Article  Google Scholar 

  38. Morris J, Everitt M, Pollard R, Chave S, Semmence A. 1980. Vigorous exercise in leisure time: protection against coronary heart disease. Lancet 2:1207–1212.

    Article  PubMed  CAS  Google Scholar 

  39. Mittleman MA, Maclure M, Tofler GH, Sherwood JB, Goldberg RJ, Muller JE. 1993. Triggering of acute myocardial infarction by heavy physical exertion. Protection against triggering by regular exertion. N Engl J Med 329:1677–1683.

    Article  PubMed  CAS  Google Scholar 

  40. Tofler GH, Mittleman MA, Muller JE. 1996. Physical activity and triggering of myocardial infarction: the case for regular exercise (editorial). Heart 75:323–325.

    Article  PubMed  CAS  Google Scholar 

  41. Billman GE, Schwartz PJ, Stone HL. 1984. The effects of daily exercise on susceptibility to sudden cardiac death. Circulation 69:1182–1189.

    Article  PubMed  CAS  Google Scholar 

  42. Hull SS, Vanoli E, Adamson PB, Verrier RL, Foreman RD, Schwartz PJ. 1994. Exercise training confers anticipatory protection from sudden death during acute myocardial ischemia. Circulation 89:548–552.

    Article  PubMed  Google Scholar 

  43. Smyth HS, Sleight P Pickering GW 1969. Reflex regulation of arterial pressure during sleep in man. A quantitative method of assessing baroreflex sensitivity. Circ Res 24:109–121.

    Article  PubMed  CAS  Google Scholar 

  44. Kleiger RE, Miller JP, Bigger JT Jr, Moss AJ. 1987. Multicenter Postinfarction Research Group. Decreased heart rate variability and its association with increased mortality after acute myocardial infarction. Am J Cardiol 59:256–262.

    Article  PubMed  CAS  Google Scholar 

  45. Bigger JT, Fleiss JL, Rolnitzky LM, Steinman RC. 1993. The ability of several short-term measures of RR variability to predict mortality after myocardial infarction. 88:927–943.

    CAS  Google Scholar 

  46. Babai L, Papp JGy, Parratt JR, Vegh A. 2002. The antiarrhythmic effects of ischaemic preconditioning in anaesthetised dogs are prevented by atropine; role of changes in baroreceptor reflex sensitivity. Br J Pharmacol 135:55–64.

    Article  PubMed  CAS  Google Scholar 

  47. Rea RF, Martins JB, Mark AL. 1988. Baroreflex impairment and sudden death after myocardial infarction. Circulation 78:1072–1074.

    CAS  Google Scholar 

  48. Wit AL, Janse MJ. 1993. The ventricular arrhythmias of ischemia and infarction. Electrophysiological mechanisms. Futura Publishing Company, Mount Kisco, NY

    Google Scholar 

  49. Billman GE, Schwartz PJ, Stone HL. 1982. Baroreceptor reflex control of heart rate: a predictor of sudden cardiac death. Circulation 66:874–880.

    Article  PubMed  CAS  Google Scholar 

  50. Takeshita A, Matsuguchi H, Nakamura M. 1980. Effect of coronary occlusion on arterial baroreflex control of heart rate. Cardiovasc Res 14:303–306.

    Article  PubMed  CAS  Google Scholar 

  51. Farrell TG, Odemuyiwa O, Bashir Y, et al. 1992. Prognostic value of baroreflex sensitivity testing after acute myocardial infarction. Br Heart J 67:129–137.

    Article  PubMed  CAS  Google Scholar 

  52. Banerjee A, Locke-Winter C, Rogers KB, Mitchell MB, Brew EC, Cairns CB, Bensard DD, Harken AH. 1993. Preconditioning against myocardial dysfunction after ischemia and reperfusion by an α1-adrenergic mechanism. Circ Res 73:656–670.

    Article  PubMed  CAS  Google Scholar 

  53. Tsuchida A, Liu Y, Liu GS, Cohen MV, Downey JM. 1994. α1-Adrenergic agonists precondition rabbit ischemic myocardium independent of adenosine by direct activation of protein kinase C. Circ Res 75:576–585.

    Article  PubMed  CAS  Google Scholar 

  54. Hale SL, Kloner RA. 1994. Protection of myocardium by transient, preischemic administration of phenylephrine in the rabbit. Coronary Artery Disease 5:605–610.

    Article  PubMed  CAS  Google Scholar 

  55. Meesmann W 1982. Early arrhythmias and primary ventricular fibrillation after myocardial ischaemia in relation to preexisting coronary collaterals. In Early Arrhythmias Resulting from Myocardial Ischaemia. Ed. JR Parratt, 93–112. New York: Oxford University Press.

    Google Scholar 

  56. Laughlin M, McAllister R. 1992. Exercise training-induced coronary vascular adaptation. J Appl Physiol 73:2209–2225.

    PubMed  CAS  Google Scholar 

  57. Parratt JR. 1995. Possibilities for the pharmacological exploitation of ischaemic preconditioning. J Mol Cell Cardiol 27:991–1000.

    Article  PubMed  CAS  Google Scholar 

  58. Parratt JR. 1993. Endogenous myocardial protective (antiarrhythmic) substances. Cardiovasc Res 27:693–702.

    Article  PubMed  CAS  Google Scholar 

  59. Curtis MJ, Pugsley MK, Walker MJA. 1993. Endogenous chemical mediators of ventricular arrhythmias in ischaemic heart disease. Cardiovasc Res 27:703–719.

    Article  PubMed  CAS  Google Scholar 

  60. Végh Á, Szekeres L, Parratt JR. 1992. Preconditioning of the ischaemic myocardium; involvement of the L-arginine—nitric oxide pathway. Br J Pharmacol 107:648–652.

    Article  PubMed  Google Scholar 

  61. Végh Á, György K, Papp JGy, Sakai K, Parratt JR. 1996. The local intracoronary administration of nicorandil suppresses ventricular arrhythmias in a canine model of myocardial ischaemia. Eur J Pharmacol 305:163–168.

    Article  PubMed  Google Scholar 

  62. György K, Végh Á, Rastegar MA, Papp JGy, Parratt JR. 2000. Isosorbide-2-mononitrate reduces the consequences of myocardial ischaemia, including arrhythmia severity: implications for preconditioning. Cardiovasc Drugs Ther 14:481–488.

    Article  PubMed  Google Scholar 

  63. Kis A, Végh Á, Papp JGy, Parratt JR. 1999. Pacing-induced delayed protection against arrhythmias is attenuated by aminoguanidine, an inhibitor of nitric oxide synthase. Br J Pharmacol 127:1545–1550.

    Article  PubMed  CAS  Google Scholar 

  64. Végh Á, György K, Rastegar MA, Papp JGy, Parratt JR. 1999. Delayed protection against ventricular arrhythmias by monophosphoryl lipid-A in a canine model of ischaemia and reperfusion. Eur J Pharmacol 382:81–90.

    Article  PubMed  Google Scholar 

  65. Kingwell BA. 2000. Nitric oxide as a metabolic regulator during exercise: Effect of training in health and disease. Clin Exp Pharmacol Physiol 27:239–250.

    Article  PubMed  CAS  Google Scholar 

  66. Matsumoto A, Hirata Y, Momomura S, et al. 1994. Increased nitric oxide production during exercise. Lancet 343:849–850.

    Article  PubMed  CAS  Google Scholar 

  67. Sessa WC, Pritchard K, Seyedi N, Wang J, Hintze TH. 1994. Chronic exercise in dogs increases coronary vascular nitric oxide production and endothelial cell nitric oxide synthase gene expression. Circ Res 74:349–353.

    Article  PubMed  CAS  Google Scholar 

  68. Bernstein RD, Ochoa FY, Xu X, et al. 1996. Function and production of nitric oxide in the coronary circulation of the conscious dog during exercise. Circ Res 79:840–848.

    Article  PubMed  CAS  Google Scholar 

  69. Wang J, Wolin MS, Hintze TH. 1993. Chronic exercise enhances endothelium-mediated dilation of epicardial coronary artery in conscious dogs. Circ Res 73:829–838.

    Article  PubMed  CAS  Google Scholar 

  70. Zhao G, Zhang X, Xu X, Ochoa M, Hintze TH. 1997. Short-term exercise training enhances reflex cholinergic nitric oxide-dependent coronary vasodilation in conscious dogs. Circ Res 80:868–876.

    Article  PubMed  CAS  Google Scholar 

  71. Ishibashi Y, Quebbeman BB, Duncker DJ, Klassen C, Bache RJ. 1998. Acadesine increases blood flow in the collateralized heart during exercise. J Cardiovasc Pharmacol 32:552–561.

    Article  PubMed  CAS  Google Scholar 

  72. Egashira K, Katsuda Y, Mohri M, et al. 1996. Role of endothelium-derived nitric oxide in coronary vasodilatation induced by pacing tachycardia in humans. Circ Res 79:331–335.

    Article  PubMed  CAS  Google Scholar 

  73. Green DJ, Cable NT, Fox C, Rankin JM, Taylor RR. 1994. Modification of forearm resistance vessels by exercise training in young men. J Appl Physiol 77:1829–1833.

    PubMed  CAS  Google Scholar 

  74. Radegran G, Saltin B. 1999. Nitric oxide in the regulation of vasomotor tone in human skeletal muscle. Am J Physiol 276:H1951–1960.

    PubMed  CAS  Google Scholar 

  75. Koller A, Huang A, Sun D, Kaley G. 1995. Exercise training augments flow-dependent dilation in rat skeletal muscle arterioles. Role of endothelial nitric oxide and prostaglandins. Circ Res 76:544–550.

    Article  PubMed  CAS  Google Scholar 

  76. Roberts CK, Barnard RJ, Jasman A, Balon TW 1999. Acute exercise increases nitric oxide synthase activity in skeletal muscle. Am J Physiol 277:E390–394.

    PubMed  CAS  Google Scholar 

  77. Schwartz P, Diem R, Dun NJ, Förstermann U. 1995. Endogenous and exogenous nitric oxide inhibits norepinephrine release from rat heart sympathetic nerves. Circ Res 77:841–848.

    Article  Google Scholar 

  78. Balon T, Nadler J. 1997. Evidence that nitric oxide increases glucose transport in skeletal muscle. J Appl Physiol 82:359–363.

    PubMed  CAS  Google Scholar 

  79. Ostrowski K, Hermann C, Bangash A, Schjerling P, Nielsen JN, Pedersen BK. 1998. A trauma-like elevation of plasma cytokines in humans in response to treadmill running. J Physiol 513:889–894.

    Article  PubMed  CAS  Google Scholar 

  80. Parratt JR, Stoclet J-C. 1995. Vascular smooth muscle function under conditions of sepsis and endotoxemia. In: Role of Nitric Oxide in Sepsis and ARDS. Ed. MP Fink and D Payer, 44–61. Berlin: Springer.

    Chapter  Google Scholar 

  81. Parratt JR, Végh, Á. 1997. Delayed protection against ventricular arrhythmias by cardiac pacing. Heart 78:423–425.

    PubMed  CAS  Google Scholar 

  82. Griffiths MJ, Messent M, MacAllister RJ, Evans TW 1993. Aminoguanidine selectively inhibits inducible nitric oxide synthase. Br J Pharmacol 110:963–968.

    Article  PubMed  CAS  Google Scholar 

  83. Misko TP, Moore WM, Kasten TP, et al. 1993. Selective inhibition of the inducible nitric oxide synthase by aminoguanidine. Eur J Pharmacol 233:119–125.

    Article  PubMed  CAS  Google Scholar 

  84. Kengatharan KM, De Kimpe SJ, Thiemermann C. 1996. Role of nitric oxide in the circulatory failure and organ injury in a rodent model of gram-positive shock. Br J Pharmacol 119:1411–1421.

    Article  PubMed  CAS  Google Scholar 

  85. László F, Evans SM, Whittle BJ. 1995. Aminoguanidine inhibits both constitutive and inducible nitric oxide synthase isoforms in rat intestinal microvasculature in vivo. Eur J Pharmacol 272:169–175.

    Article  PubMed  Google Scholar 

  86. Armour JA, Smith FM, Losier AM, Ellenberger HH, Hopkins A. 1995. Modulation of intrinsic cardiac neuronal activity by nitric oxide donors induces cardiodynamic changes. Am J Physiol 268:R403–R413.

    PubMed  CAS  Google Scholar 

  87. Wei C, Jiang S, Lust JA, Daly RC, McGregor CG. 1996. Genetic expression of endothelial nitric oxide synthase in human atrial myocardium. Mayo Clin Proc 71:346–350.

    Article  PubMed  CAS  Google Scholar 

  88. Xu KY, Huso DL, Dawson TM, Bredt DS, Becker LC. 1999. Nitric oxide synthase in cardiac sarcoplasmic reticulum. Proc NY Acad Sci 96:657–662.

    Article  CAS  Google Scholar 

  89. Bolli R. 1996. The early and late phases of preconditioning against stunning and the essential role of oxyradicals in the late phase: an overview. Basic Res Cardiol 91:57–63.

    Article  PubMed  CAS  Google Scholar 

  90. Qiu Y, Rizvi A, Tang XL, Manchikalapudi S, Takano H, Jadoon AK, Wu WJ, Bolli R. 1997. Nitric oxide triggers late preconditioning against myocardial infarction in conscious rabbits. Am J Physiol 273:H2931–2936.

    PubMed  CAS  Google Scholar 

  91. Bolli R, Manchikalapudi S, Tang XL. 1997. The protective effect of late preconditioning against myocardial stunning in conscious rabbits is mediated by nitric oxide synthase. Evidence that nitric oxide acts both as a trigger and as a mediator of the late phase of ischemic preconditioning. Circ Res 81:1094–1107.

    Article  PubMed  CAS  Google Scholar 

  92. Bolli R, Dawn B, Tang XL, Qiu Y, Ping P, Xuan YT, Jones WK, Takano H, Guo Y, Zhang J. 1998. The nitric oxide hypothesis of late preconditioning. Basic Res Cardiol 93:325–338.

    Article  PubMed  CAS  Google Scholar 

  93. Sears CE, Choate JK, Paterson DJ. 1999. NO-cGMP pathway accentuates the decrease in heart rate caused by cardiac vagal nerve stimulation. J Appl Physiol 86:510–516.

    PubMed  CAS  Google Scholar 

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Végh, Á., Parratt, J.R., Babai, L., Szigeti, Z., Papp, J.G. (2003). Exercise and Delayed Preconditioning in the Protection of the Heart against Ventricular Arrhythmias: Crucial Role of Nitric Oxide. In: Dhalla, N.S., Takeda, N., Singh, M., Lukas, A. (eds) Myocardial Ischemia and Preconditioning. Progress in Experimental Cardiology, vol 6. Springer, Boston, MA. https://doi.org/10.1007/978-1-4615-0355-2_30

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