Nitric oxide in myocardial ischemia/reperfusion injury

Cardiovascular Research

Volumn 61, Issue 3, 2004, Pages 402-413

  Schulz, Rainer ^a   Kelm, Malte ^b   Heusch, Gerd ^a  

^a UNIVERSITY HOSPITAL ESSEN   (Germany)

^b UNIVERSITY HOSPITAL DÜSSELDORF   (Germany)

Author keywords

Infarct size; Nitric oxide; Stunning

Indexed keywords

CYCLIC GMP; ISOENZYME; NITRIC OXIDE; NITRIC OXIDE SYNTHASE;

APOPTOSIS; BLOOD COMPONENT; BLOOD VESSEL FUNCTION; CELL FUNCTION; CIRCULATION; CONCENTRATION (PARAMETERS); CORONARY ARTERY; ENZYME ACTIVITY; ENZYME INHIBITION; ENZYME METABOLISM; HEART CONTRACTION; HEART FUNCTION; HEART MUSCLE CELL; HEART MUSCLE ISCHEMIA; IN VITRO STUDY; INFLAMMATION; MAMMAL; MITOCHONDRION; NONHUMAN; PLASMA; PRIORITY JOURNAL; REPERFUSION INJURY; REVIEW; SIGNAL TRANSDUCTION; TISSUE INJURY;

ANIMALS; ANOXIA; APOPTOSIS; ENDOTHELIUM, VASCULAR; HUMANS; MAMMALS; MODELS, ANIMAL; MYOCARDIAL CONTRACTION; MYOCARDIAL REPERFUSION INJURY; MYOCYTES, CARDIAC; NITRIC OXIDE; NITRIC OXIDE DONORS; NITRIC OXIDE SYNTHASE;

EID: 1142285456     PISSN: 00086363     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.cardiores.2003.09.019     Document Type: Review

References (134)

1. Bolli R. Cardioprotective function of inducible nitric oxide synthase and role of nitric oxide in myocardial ischemia and preconditioning: an overview of a decade of research. J. Mol. Cell Cardiol. 33:2001;1897-1918.
2. Lefer A.M., Campbell B., Shin Y.-K.et al. Simvastatin preserves the ischemic-reperfused myocardium in normocholesterolemic rat hearts. Circulation. 100:1999;178-184.
3. Asanuma H., Kitakaze M., Funaya H.et al. Nifedipine limits infarct size via NO-dependent mechanisms in dogs. Basic Res. Cardiol. 96:2001;497-505.
4. Hartman J.C., Kurc G.M., Hullinger T.G.et al. Inhibition of nitric oxide synthase prevents myocardial protection by ramipril. J. Pharmacol. Exp. Ther. 3:1994;1071-1076.
5. Hafezi-Moghadam A., Simoncini T., Yang Z.et al. Acute cardiovascular protective effects of corticosteroids are mediated by non-transcriptional activation of endothelial nitric oxide synthase. Nat. Med. 8:2002;473-479.
6. Schulz R., Cohen M.V., Behrends M., Downey J.M., Heusch G. Signal transduction of ischemic preconditioning. Cardiovasc. Res. 52:2001;181-198.
7. Bolli R. The late phase of preconditioning. Circ. Res. 87:2000;972-983.
8. Baxter G.F. Role of adenosine in delayed preconditioning of myocardium. Cardiovasc. Res. 55:2002;483-494.
9. Kelm M. Nitric oxide metabolism and breakdown. Biochim. Biophys. Acta. 1411:1999;273-289.
10. Becker B.F., Kupatt C., Massoudy P., Zahler S. Reactive oxygen species and nitric oxide in myocardial ischemia and reperfusion. Z. Kardiol. 89(Suppl. 9):2000;IX88-IX91.
11. Pabla R., Curtis M.J. 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. J. Mol. Cell Cardiol. 28:1996;2097-2110.
12. Brahmajothi M.V., Campbell D.L. Heterogeneous basal expression of nitric oxide synthase and superoxide dismutase isoforms in mammalian heart. Circ. Res. 85:1999;575-587.
13. Massion P.B., Balligand J.-L. Modulation of cardiac contraction, relaxation and rate by the endothelial nitric oxide synthase (eNOS): lessons from genetically modified mice. J. Physiol. 546:2003;63-75.
14. Barouch L.A., Harrison R.W., Skaf M.W.et al. Nitric oxide regulates the heart by spatial confinement of nitric oxide synthase isoforms. Nature. 416:2002;337-339.
15. Sears C.E., Bryant S.M., Ashley E.A.et al. Cardiac neuronal nitric oxide synthase isoform regulates myocardial contraction and calcium handling. Circ. Res. 92:2003;e52-e59.
16. Radomski M.W., Palmer R.M.J., Moncada S. Comparative pharmacology of endothelium-derived relaxing factor, nitric oxide and prostacyclin in platelets. Br. J. Pharmacol. 92:1987;181-187.
17. McCall T.B., Boughton-Smith N.K., Palmer R.M.J., Whittle B.J.R., Moncada S. Synthesis of nitric oxide from L-arginine by neutrophils. Biochem. J. 261:1989;293-296.
18. De Frutos T., de Miguel L.S., Farré J.et al. Expression of an endothelial-type nitric oxide synthase isoform in human neutrophils: modification by tumor necrosis factor-alpha and during acute myocardial infarction. J. Am. Coll. Cardiol. 37:2001;800-807.
19. Sánchez De Miguel L., Arriero M., Farré J.et al. Nitric oxide production by neutrophils obtained from patients during acute coronary syndromes: expression of the nitric oxide synthase isoforms. J. Mol. Cell Cardiol. 39:2002;818-825.
20. Woditsch I., Schrör K. Prostacyclin rather than endogenous nitric oxide is a tissue protective in myocardial ischemia. Am. J. Physiol. 263:1992;H1390-H1396.
21. Depre C., Fierain L., Hue L. Activation of nitric oxide synthase by ischaemia in the perfused heart. Cardiovasc. Res. 33:1997;82-87.
22. Csonka C., Szilvássy Z., Fülöp F.et al. Classic preconditioning decreases the harmful accumulation of nitric oxide during ischemia and reperfusion in rat hearts. Circulation. 100:1999;2260-2266.
23. Wang P., Zweier J.L. Measurement of nitric oxide and peroxynitrite generation in the postischemic heart. J. Biol. Chem. 271:1996;29223-29230.
24. Giraldez R.R., Panda A., Xia Y., Sanders P., Zweier J.L. Decreased nitric oxide synthase activity causes impaired endothelium-dependent relaxation in the postischemic heart. J. Biol. Chem. 272:1997;21420-21426.
25. Amrani M., Chester A.H., Jayakumar J., Schyns C.J., Yacoub M.H. L-Arginine reverses low coronary reflow and enhances postischaemic recovery of cardiac mechanical function. Cardiovasc. Res. 30:1995;200-204.
26. Noda K., Sasaguri M., Ideishi M., Ikeda M., Arakawa K. Role of locally formed angiotensin II and bradykinin in the reduction of myocardial infarct size in dogs. Cardiovasc. Res. 27:1993;334-340.
27. Mollnau H., Wendt M., Szöcs K.et al. Effects of angiotensin II infusion on the expression and function of NAD(P)H oxidase and components of nitric oxide/cGMP signaling. Circ. Res. 90:2002;e58-e65.
28. Gurevitch J., Frolkis I., Yuhas Y.et al. Tumor necrosis factor-alpha is released from the isolated heart undergoing ischemia and reperfusion. J. Am. Coll. Cardiol. 28:1996;247-252.
29. Frangogiannis N.G., Lindsey M.L., Michael L.H.et al. Resident cardiac mast cells degranulate and release preformed TNF-α, initiating the cytokine cascade in experimental canine myocardial ischemia/reperfusion. Circulation. 98:1998;699-710.
30. Irwin M.W., Mak S., Mann D.L.et al. Tissue expression and immunolocalization of tumor necrosis factor-α in postinfarction dysfunctional myocardium. Circulation. 99:1999;1492-1498.
31. Sanders D.B., Larson D.F., Hunter K., Gorman M., Yang B. Comparison of tumor necrosis factor-alpha effect on the expression of iNOS in macrophage and cardiac myocytes. Perfusion. 16:2001;67-74.
32. Zweier J.L., Samouilov A., Kuppusamy P. Non-enzymatic nitric oxide synthesis in biological systems. Biochim. Biophys. Acta. 1411:1999;250-262.
33. Kitakaze M., Node K., Takashima S.et al. Role of cellular acidosis in production of nitric oxide in canine ischemic myocardium. J. Mol. Cell Cardiol. 33:2001;1727-1737.
34. Godber B.L.J., Doel J.J., Sapkota G.P.et al. Reduction of nitrite to nitric oxide catalyzed by xanthine oxidoreductase. J. Biol. Chem. 275:2000;7757-7763.
35. Feelisch M., Rassaf T., Mnaimneh S.et al. Concomitant S-, N-, and heme-nitros(yl)ation in biological tissues and fluids: implications for the fate of NO in vivo. FASEB J. 16:2002;1775-1785.
36. Brovkovych V., Stolarczyk E., Oman J., Tomboulian P., Malinski T. Direct electrochemical measurement of nitric oxide in vascular endothelium. J. Pharm. Biomed. Anal. 19:1999;135-143.
37. Bolli R., Jeroudi M.O., Patel B.S.et al. Direct evidence that oxygen-derived free radicals contribute to postischemic myocardial dysfunction in the intact dog. Proc. Natl. Acad. Sci. U. S. A. 86:1989;4695-4699.
38. Rassaf T., Preik M., Kleinbongard P.et al. Evidence for in vivo transport of bioactive nitric oxide in human plasma. J. Clin. Invest. 109:2002;1241-1248.
39. Friebe A., Koesling D. Regulation of nitric oxide-sensitive guanylyl cyclase. Circ. Res. 93:2003;96-105.
40. Gewaltig M.T., Kojda G. Vasoprotection by nitric oxide: mechanisms and therapeutic potential. Cardiovasc. Res. 55:2002;250-260.
41. Kojda G., Kottenberg K. Regulation of basal myocardial function by NO. Cardiovasc. Res. 41:1999;514-523.
42. Agulló L., Garcia-Dorado D., Escalona N.et al. Effect of ischemia on soluble and particulate guanylyl cyclase-mediated cGMP synthesis in cardiomyocytes. Am. J. Physiol. Heart Circ. Physiol. 284:2003;H2170-H2176.
43. Du Toit E.F., Meiring J., Opie L.H. Relation of cyclic nucleotide ratios to ischemic and reperfusion injury in nitric oxide-donor treated rat hearts. J. Cardiovasc. Pharmacol. 38:2001;529-538.
44. Heusch G., Post H., Michel M.C., Kelm M., Schulz R. Endogenous nitric oxide and myocardial adaptation to ischemia. Circ. Res. 87:2000;146-152.
45. Bloch W., Mehlhorn U., Krahwinkel A.et al. Ischemia increases detectable endothelial nitric oxide synthase in rat and human myocardium. Nitric Oxide: Biol. Chem. 5:2001;317-333.
46. Mehlhorn U., Bloch W., Krahwinkel A.et al. Activation of myocardial constitutive nitric oxide synthase during coronary artery surgery. Eur. J. Cardiothorac. Surg. 17:2000;305-311.
47. Padilla F., Garcia-Dorado D., Agulló L.et al. Intravenous administration of the natriuretic peptide urodilatin at low doses during coronary reperfusion limits infarct size in anesthetized pigs. Cardiovasc. Res. 51:2001;592-600.
48. Ehring T., Baumgart D., Krajcar M.et al. Attenuation of myocardial stunning by the ACE-inhibitor ramiprilat through a signal cascade of bradykinin and prostaglandins, but not nitric oxide. Circulation. 90:1994;1368-1385.
49. Stamler J.S., Loh E., Roddy M.-A., Currie K.E., Creager M.A. Nitric oxide regulates basal systemic and pulmonary vascular resistance in healthy humans. Circulation. 89:1994;2035-2040.
50. Huang P.L., Huang Z., Mashimo H.et al. Hypertension in mice lacking the gene for endothelial nitric oxide synthase. Nature. 377:1995;239-242.
51. Duncker D.J., Bache R.J. Inhibition of nitric oxide production aggravates myocardial hypoperfusion during exercise in the presence of a coronary artery stenosis. Circ. Res. 74:1994;629-640.
52. Ehring T., Krajcar M., Baumgart D.et al. Cholinergic and α-adrenergic coronary vasomotion with increasing ischemia-reperfusion injury. Am. J. Physiol. 268:1995;H886-H894.
53. Kim S.-J., Ghaleh B., Kudej R.K.et al. Delayed enhanced nitric oxide-mediated coronary vasodilation following brief ischemia and prolonged reperfusion in conscious dogs. Circ. Res. 81:1997;53-59.
54. Ma X.-L., Weyrich A.S., Lefer D.J., Lefer A.M. Diminished basal nitric oxide release after myocardial ischemia and reperfusion promotes neutrophil adherence to coronary endothelium. Circ. Res. 72:1993;403-412.
55. Pabla R., Buda A.J., Flynn D.M.et al. Nitric oxide attenuates neutrophil-mediated myocardial contractile dysfunction after ischemia and reperfusion. Circ. Res. 78:1996;65-72.
56. Sato H., Zhao Z.Q., McGee D.S.et al. Supplemental L-arginine during cardioplegic arrest and reperfusion avoids regional postischemic injury. J. Thorac. Cardiovasc. Surg. 110:1995;302-314.
57. Lefer D.J., Nakanishi K., Johnston W.E., Vinten-Johansen J. Antineutrophil and myocardial protection actions of a novel nitric oxide donor after acute myocardial ischemia and reperfusion in dogs. Circulation. 88:1993;2337-2350.
58. Nossuli T.O., Hayward R., Scalia R., Lefer A.M. Peroxynitrite reduces myocardial infarct size and preserves coronary endothelium after ischemia and reperfusion in cats. Circulation. 96:1997;2317-2324.
59. Wildhirt S.M., Weismueller S., Schulze C.et al. Inducible nitric oxide synthase activation after ischemia/reperfusion contributes to myocardial dysfunction and extent of infarct size in rabbits: evidence for a late phase of nitric oxide-mediated reperfusion injury. Cardiovasc. Res. 43:1999;698-711.
60. Woolfson R.G., Patel V.C., Neild Gh., Yellon D.M. Inhibition of nitric oxide synthesis reduces infarct size by an adenosine-dependent mechanism. Circulation. 91:1995;1545-1551.
61. Minamino T., Kitakaze M., Node K., Funaya H., Hori M. Inhibition of nitric oxide synthesis increases adenosine production via an extracellular pathway through activation of protein kinase C. Circulation. 96:1997;1586-1592.
62. Obata T. Adenosine production and its interaction with protection of ischemic and reperfusion injury of the myocardium. Life Sci. 71:2002;2083-2103.
63. Belosjorow S., Bolle I., Duschin A., Heusch G., Schulz R. TNFα antibodies are as effective as ischemic preconditioning in reducing infarct size in rabbits. Am. J. Physiol. Heart Circ. Physiol. 284:2003;H927-H930.
64. Wagner D.R., McTiernan C., Sanders V.J., Feldman A.M. Adenosine inhibits lipopolysaccharide-induced secretion of tumor necrosis factor-α in the failing human heart. Circulation. 97:1998;521-524.
65. Thielmann M., Dörge H., Martin C.et al. Myocardial dysfunction with coronary microembolization: signal transduction through a sequence of nitric oxide, tumor necrosis factor-α and sphingosine. Circ. Res. 90:2002;807-813.
66. Vila-Petroff M.G., Younes A., Egan J., Lakatta E.G., Sollott S.J. Activation of distinct cAMP-dependent and cGMP-dependent pathways by nitric oxide in cardiac myocytes. Circ. Res. 84:1999;1020-1031.
67. 2+ in intact cardiac myocytes. Circ. Res. 74:1994;970-978.
68. Naim K.L., Rabindranauth P., Weiss H.R.et al. Positive inotropy due to lowering cyclic GMP is also mediated by increase in cyclic AMP in control and hypertrophic hearts. Can. J. Physiol. Pharmacol. 76:1998;605-612.
69. Post H., Schulz R., Gres P., Heusch G. No involvement of nitric oxide in the limitation of β-adrenergic inotropic responsiveness during ischemia. Am. J. Physiol. Heart Circ. Physiol. 281:2001;H2392-H2397.
70. Abe K., Hayashi N., Terada H. Effect of endogenous nitric oxide on energy metabolism of rat heart mitochondria during ischemia and reperfusion. Free Radic. Biol. Med. 26:1999;379-387.
71. Jekabsone A., Ivanoviene L., Brown G.C., Borutaite V. Nitric oxide and calcium together inactivate mitochondrial complex I and induce cytochrome c release. J. Mol. Cell Cardiol. 35:2003;803-809.
72. Bell R.M., Maddock H.L., Yellon D.M. The cardioprotective and mitochondrial depolarising properties of exogenous nitric oxide in mouse heart. Cardiovasc. Res. 57:2003;405-415.
73. Rakhit R.D., Mojet M.H., Marber M.S., Duchen M.R. Mitochondria as targets for nitric oxide-induced protection during simulated ischemia and reoxygenation in isolated neonatal cardiomyocytes. Circulation. 103:2001;2617-2623.
74. Taimor G., Hofstaetter B., Piper H.M. Apoptosis induction by nitric oxide in adult cardiomyocytes via cGMP-signaling and its impairment after simulated ischemia. Cardiovasc. Res. 45:2000;588-594.
75. Hofstaetter B., Taimor G., Inserte J., Garcia-Dorado D., Piper H.M. Inhibition of apoptotic responses after ischemic stress in isolated hearts and cardiomyocytes. Basic Res. Cardiol. 97:2002;479-488.
76. Leist M., Single B., Naumann H.et al. Inhibition of mitochondrial ATP generation by nitric oxide switches apoptosis to necrosis. Exp. Cell Res. 249:1999;396-403.
77. Han O., Joe K.H., Kim S.W.et al. Involvement of p38 mitogen-activated protein kinase and apoptosis signal-regulating kinase-1 in nitric oxide-induced cell death in PC12 cells. Neurochem. Res. 26:2001;525-532.
78. Taimor G., Rakow A., Piper H.M. Transcription activator protein 1 (AP-1) mediates NO-induced apoptosis of adult cardiomyocytes. FASEB J. 15:2001;2518-2520.
79. Yang B.C., Nichols W.W., Mehta J.L. Cardioprotective effects of red blood cells on ischemia and reperfusion injury in isolated rat heart: release of nitric oxide as a potential mechanism. J. Cardiovasc. Pharmacol. Ther. 1:2003;297-306.
80. Black S.C., Galinski M.R., Friedrichs G.S.et al. Cardioprotective effects of heparin or N-acetylheparin in an in vivo model of myocardial ischaemic and reperfusion injury. Cardiovasc. Res. 29:1995;629-636.
81. Hoshida S., Yamashita N., Igarashi J.et al. Nitric oxide synthase protects the heart against ischemia-reperfusion injury in rabbits. J. Pharmacol. Exp. Ther. 274:1995;413-418.
82. Moroz L.L., Norby S.W., Cruz L.-A.et al. Non-enzymatic production of nitric oxide (NO) from NO synthase inhibitors. Biochem. Biophys. Res. Commun. 253:1998;571-579.
83. Kanno S., Lee P.C., Zhang Y.et al. Attenuation of myocardial ischemia/reperfusion injury by superinduction of inducible nitric oxide synthase. Circulation. 101:2000;2742-2748.
84. Depre C., Vanoverschelde J.L., Goudemant J.F., Mottet I., Hue L. Protection against ischemic injury by nonvasoactive concentrations of nitric oxide synthase inhibitors in the perfused rabbit heart. Circulation. 92:1995;1911-1918.
85. Hasebe N., Shen Y.T., Vatner S.F. Inhibition of endothelium-derived relaxing factor enhances myocardial stunning in conscious dogs. Circulation. 88:1993;2862-2871.
86. Beresewicz A., Karwatowska-Prokopczuk E., Lewartowski B., Cedro-Ceremuzynska K. A protective role of nitric oxide in isolated ischaemic/reperfused rat heart. Cardiovasc. Res. 30:1995;1001-1008.
87. Engelman D.T., Watanabe M., Engelman R.M.et al. Constitutive nitric oxide release is impaired after ischemia and reperfusion. J. Thorac. Cardiovasc. Surg. 110:1995;1047-1053.
88. Hiramatsu T., Forbess J.M., Miura T., Mayer J.E. Jr. Effects of L-arginine and L-nitro-arginine methyl ester on recovery of neonatal lamb hearts after cold ischemia. Evidence for an important role of endothelial production of nitric oxide. J. Thorac. Cardiovasc. Surg. 109:1995;81-87.
89. G-nitro-L-arginine improves myocardial function following ischemia/reperfusion in isolated perfused rat heart. J. Mol. Cell Cardiol. 27:1995;419-426.
90. Schulz R., Wambolt R. Inhibition of nitric oxide synthesis protects the isolated working rabbit heart from ischaemia-reperfusion injury. Cardiovasc. Res. 30:1995;432-439.
91. Wanna F.S., Obayashi D.Y., Young J.N., DeCampli W.M. Simultaneous manipulation of the nitric oxide and prostanoid pathways reduces myocardial injury. J. Thorac. Cardiovasc. Surg. 110:1995;1054-1062.
92. Zweier J.L., Wang P., Kuppusamy P. Direct measurement of nitric oxide generation in the ischemic heart using electron paramagnetic resonance spectroscopy. J. Biol. Chem. 270:1995;304-307.
93. Pabla R., Curtis M.J. 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. 28:1996;2111-2121.
94. Tveita T., Skandfer M., Refsum H., Ytrehus K. Experimental hypothermia and rewarming: changes in mechanical function and metabolism. J. Appl. Physiol. 80:1996;291-297.
95. Luo Z., Diaco M., Murohara T.et al. Vascular endothelial growth factor attenuates myocardial ischemia-reperfusion injury. Ann. Thorac. Surg. 64:1997;993-998.
96. Massoudy P., Zahler S., Kupatt C.et al. Cardioprotection by cyclosporine A in experimental ischemia and reperfusion - evidence for a nitric oxide-dependent mechanism mediated by endothelin. J. Mol. Cell Cardiol. 29:1997;535-544.
97. Yang B.C., Mehta J.L. Inhibition of nitric oxide does not affect reperfusion-induced myocardial injury, but it prevents lipid peroxidation in the isolated rat heart. Life Sci. 61:1997;229-236.
98. Yasmin W., Strynadka K.D., Schulz R. Generation of peroxynitrite contributes to ischemia-reperfusion injury in isolated rat hearts. Cardiovasc. Res. 33:1997;422-432.
99. Du Toit E.F., McCarthy J., Miyashiro J., Opie L.H., Brunner F. Effect of nitrovasodilators and inhibitors of nitric oxide synthase on ischaemic and reperfusion function of rat isolated hearts. Br. J. Pharmacol. 123:1998;1159-1167.
100. Mori E., Haramaki N., Ikeda H., Imaizumi T. Intra-coronary administration of L-arginine aggravates myocardial stunning through production of peroxynitrite in dogs. Cardiovasc. Res. 40:1998;113-123.
101. Zhang X., Recchia F.A., Bernstein R.et al. Kinin-mediated coronary nitric oxide production contributes to the therapeutic action of angiotensin-converting enzyme and neutral endopeptidase inhibitors and amlodipine in the treatment in heart failure. J. Pharmacol. Exp. Ther. 288:1999;742-751.
102. Lochner A., Marais E., Genade S., Moolman J.A. Nitric oxide: a trigger for classic preconditioning? Am. J. Physiol. Heart Circ. Physiol. 279:2000;H2752-H2765.
103. Öz E., Arsakay G., Dincer S., Erbas D. Role of the nitric oxide pathway on ischemia-reperfusion injury in an isolated perfused guinea pig heart. Gen. Pharmacol. 34:2000;3-7.
104. Zhang Y., Bissing J.W., Xu L.et al. Nitric oxide synthase inhibitors decrease coronary sinus-free radical concentration and ameliorate myocardial stunning in an ischemia-reperfusion model. J. Am. Coll. Cardiol. 38:2001;546-554.
105. Flögel U., Decking U.K.M., Gödecke A., Schrader J. Contribution of NO to ischemia-reperfusion injury in the saline-perfused heart: a study in endothelial NO synthase knockout mice. J. Mol. Cell Cardiol. 31:1999;827-836.
106. Hannan R.L., John M.C., Kouretas P.C.et al. Deletion of endothelial nitric oxide synthase exacerbates myocardial stunning in an isolated mouse heart model. J. Surg. Res. 93:2000;127-132.
107. Siker D., Pagel P.S., Pelc L.R.et al. Nitrous oxide impairs functional recovery of stunned myocardium in barbiturate-anesthetized, acutely instrumented dogs. Anesth. Analg. 75:1992;539-548.
108. Konorev E.A., Tarpey M.M., Joseph J., Baker J.E., Kalyanaraman B. S-nitrosoglutathione improves functional recovery in the isolated rat heart after coardioplegic ischemia arrest - evidence for a cardioprotective effect of nitric oxide1. J. Pharmacol. Exp. Ther. 274:1995;200-206.
109. Engelman D.T., Watanabe M., Maulik N.et al. Critical timing of nitric oxide supplementation in cardioplegic arrest and reperfusion. Circulation. 94(Suppl. II):1996;II407-II411.
110. Cope J.T., Banks D., Laubach V.E.et al. Sodium nitroprusside exacerbates myocardial ischemia-reperfusion injury. Ann. Thorac. Surg. 64:1997;1656-1660.
111. Lefer D.J., Scalia R., Campbell B.et al. Peroxynitrite inhibits leukocyte-endothelial cell interactions and protects against ischemia-reperfusion injury in rats. J. Clin. Invest. 99:1997;684-691.
112. Ma X.L., Lopez B.L., Liu G.-L., Christopher T.A., Ischiropoulos H. Peroxynitrite aggravates myocardial reperfusion injury in the isolated perfused rat heart. Cardiovasc. Res. 36:1997;195-204.
113. Gandhi A., Yan L., Scholz P.M., Huang M.W., Weiss H.R. Cyclic GMP reduces ventricular myocyte stunning after simulated ischemia-reperfusion. Nitric Oxide: Biol. Chem. 3:1999;473-480.
114. Brunner F., Maier R., Andrew P.et al. Attenuation of myocardial ischemia/reperfusion injury in mice with myocyte-specific overexpression of endothelial nitric oxide synthase. Cardiovasc. Res. 57:2003;55-62.
115. Patel V.C., Yellon D.M., Singh K.J., Neild Gh., Woolfson R.G. Inhibition of nitric oxide limits infarct size in the in situ rabbit hearts. Biochem. Biophys. Res. Commun. 194:1993;234-238.
116. Weselcouch E.O., Baird A.J., Sleph P., Grover G.J. Inhibition of nitric oxide synthesis does not affect ischemic preconditioning in isolated perfused rat hearts. Am. J. Physiol. 268:1995;H242-H249.
117. Williams M.W., Taft C.S., Ramnauth S., Zhao Z.-Q., Vinten-Johansen J. Endogenous nitric oxide (NO) protects against ischaemia-reperfusion injury in the rabbit. Cardiovasc. Res. 30:1995;79-86.
118. Bugge E., Ytrehus K. Bradykinin protects against infarction but does not mediate ischemic preconditioning in the isolated rat heart. J. Mol. Cell Cardiol. 28:1996;2333-2341.
119. Weinbrenner C., Liu G.S., Downey J.M., Cohen M.V. Cyclosporine A limits myocardial infarct size even when administered after onset of ischemia. Cardiovasc. Res. 38:1998;676-684.
120. Masini E., Salvemini D., Ndisang J.F.et al. Cardioprotective activity of endogenous and exogenous nitric oxide on ischemia reperfusion injury in isolated guinea pig hearts. Inflamm. Res. 48:1999;561-568.
121. Nakano A., Liu G.S., Heusch G., Downey J.M., Cohen M.V. Exogenous nitric oxide can trigger a preconditioned state through a free radical mechanism, but endogenous nitric oxide is not a trigger of classical ischemic preconditioning. J. Mol. Cell Cardiol. 32:2000;1159-1167.
122. Post H., Schulz R., Behrends M.et al. No involvement of endogenous nitric oxide in classical ischemic preconditioning in swine. J. Mol. Cell Cardiol. 32:2000;725-733.
123. Novalija E., Varadarajan S.G., Camara A.K.S.et al. Anesthetic preconditioning: triggering role of reactive oxygen and nitrogen species in isolated hearts. Am. J. Physiol. Heart Circ. Physiol. 283:2002;H44-H52.
124. Jones S.P., Girod W.G., Palazzo A.J.et al. Myocardial ischemia-reperfusion injury is exacerbated in absence of endothelial cell nitric oxide synthase. Am. J. Physiol. 276:1999;H1567-H1573.
125. Sumeray M.S., Rees D.D., Yellon D.M. Infarct size and nitric oxide synthase in murine myocardium. J. Mol. Cell Cardiol. 32:2000;35-42.
126. Sharp B.R., Jones S.P., Rimmer D.M., Lefer D.J. Differential response to myocardial reperfusion injury in eNOS-deficient mice. Am. J. Physiol. Endocrinol. Metab. 282:2002;H2422-H2426.
127. Bell R.M., Yellon D.M. Bradykinin limits infarction when administered as an adjunct to reperfusion in mouse heart: the role of PI3K, Akt and eNOS. J. Mol. Cell Cardiol. 35:2003;185-193.
128. Johnson G. III, Tsao P.S., Lefer A.M. Cardioprotective effects of authentic nitric oxide in myocardial ischemia with reperfusion. Crit. Care Med. 19:1991;244-252.
129. Siegfried M.R., Erhardt J., Rider T., Ma X.L., Lefer A.M. Cardioprotection and attenuation of endothelial dysfunction by organic nitric oxide donors in myocardial inschemia-reperfusion. J. Pharmacol. Exp. Ther. 260:1992;668-675.
130. Weyrich A.S., Ma X.-L., Lefer A.M. The role of L-arginine in ameliorating reperfusion injury after myocardial ischemia in the cat. Circulation. 86:1992;279-288.
131. Pernow J., Uriuda Y., Wang Q.-D.et al. The protective effect of L-arginine on myocardial injury and endothelial function following ischaemia and reperfusion in the pig. Eur. Heart J. 15:1994;1712-1719.
132. Schlack W., Uebing A., Schäfer M.et al. Intracoronary SIN-1C during reperfusion reduces infarct size in dog. J. Cardiovasc. Pharmacol. 25:1995;424-431.
133. Pabla R., Buda A.J., Flynn D.M., Salzberg D.B., Lefer D.J. Intracoronary nitric oxide improves postischemic coronary blood flow and myocardial contractile function. Am. J. Physiol. 38:1995;H1113-H1121.
134. Nossuli T.O., Hayward R., Jensen D., Scalia R., Lefer A.M. Mechanisms of cardioprotection by peroxynitrite in myocardial ischemia and reperfusion injury. Am. J. Physiol. 44:1998;H509-H519.