Oxidative stress and neutrophil activation - The two keystones of ischemia/reperfusion injury

International Journal of Cardiology

Volumn 86, Issue 1, 2002, Pages 41-59

  Kaminski, Karol A ^a   Bonda, Tomasz A ^a   Korecki, Janusz ^a   Musial, Wlodzimierz J ^a  

^a MEDICAL UNIVERSITY OF BIALYSTOK   (Poland)

Author keywords

Cytokines; Myocardial ischemia; Neutrophils; Oxidative stress; Reactive oxygen species; Reperfusion injury

Indexed keywords

BETA2 INTEGRIN; CELL ADHESION MOLECULE; FIBRINOLYTIC AGENT; INTERCELLULAR ADHESION MOLECULE 1; INTERLEUKIN 1BETA; INTERLEUKIN 2; INTERLEUKIN 6; ION CHANNEL; REACTIVE OXYGEN METABOLITE; SELECTIN; THROMBOCYTE ACTIVATING FACTOR RECEPTOR; TUMOR NECROSIS FACTOR ALPHA;

CELL MEMBRANE; HUMAN; ISCHEMIA; LEUKOCYTE ACTIVATION; LYMPHOCYTE; MACROPHAGE; OXIDATIVE STRESS; POSTOPERATIVE COMPLICATION; PRIORITY JOURNAL; REPERFUSION INJURY; REVIEW; SIGNAL TRANSDUCTION; TRANSLUMINAL CORONARY ANGIOPLASTY;

EID: 0036829765     PISSN: 01675273     EISSN: None     Source Type: Journal    
DOI: 10.1016/S0167-5273(02)00189-4     Document Type: Article

References (212)

1. Chambless L, Keil U, Dobson A et al. for the WHO MONICA Project. Population versus clinical view of case fatality from acute coronary heart disease: Results from the WHO MONICA Project 1985-1990. Circulation 1997;96:3849-59.
2. Herrick J.B. Clinical features of sudden obstruction of the coronary arteries. J. Am. Med. Assoc. 59:1912;2015-2020.
3. Fletcher A.P., Sherry S., Alkjaersig M., et al. The maintenance of as sustained thrombolytic state in man. II. Clinical observations on patients with myocardial infarction and other thromboembolic disorders. J Clin Invest. 38:1959;1111-1119.
4. Gruppo Italiano per lo Studio della Streptochinasi nell'Infarto Miocardico (GISSI) . Effectiveness of intravenous thrombolytic treatment in acute myocardial infarction. Lancet. 1:1986;397-402.
5. ISIS-2 (Second International Study of Infarct Survival) Collaborative Group . Randomised trial of intravenous streptokinase, oral aspirin both or neither among 17187 cases of suspected acute myocardial infarction; ISIS-2. Lancet. 2:1988;349-360.
6. Zahn R., Schiele R., Schneider S., et al. (For the MITRA and the MIR Study Groups) Primary angioplasty versus intravenous thrombolysis in acute myocardial infarction: can we define subgroups of patients benefiting most from primary angioplasty?: results from the pooled data of the maximal individual therapy in acute myocardial infarction registry and the myocardial infarction registry. JACC. 37:2001;1827-1835.
7. French W.J. Trends in acute myocardial infarction management: use of National Registry of Myocardial Infarction in quality improvement. Am J Cardiol. 85:2000;5B-9B.
8. Sommers H.M., Jennings R.B. Experimental acute myocardial infarction. Histologic and histochemical studies of early myocardial infarcts induced by temporary or permanent occlusion of a coronary artery. Lab Invest. 13:1964;1491-1503.
9. Kloner R.A. Does reperfusion injury exist in humans? J Am Coll Cardiol. 21:1993;537-545.
10. Ambrosio G., Tritto I. How important is oxidative stress in ischemia, reperfusion and heart failure? Dialog Cardiovasc Med. 3:1998;25-28.
11. Matsumura K., Jeremy R.W., Schaper J., Becker L.C. Progression of myocardial necrosis during reperfusion of ischemic myocardium. Circulation. 97:1998;795-804.
12. Weinbrenner C., Liu S.G., 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.
13. Bolli R., Marban E. Molecular and cellular mechanisms of myocardial stunning. Physiol Rev. 79:1999;609-634.
14. Zweier J.L., Kuppusamy P., Williams R., et al. Measurement and characterization of postischemic free radical generation in the isolated perfused heart. J Biol Chem. 15:(264):1989;18890-18895.
15. Garlick P.B., Davies M.J., Hearse D.J., Slater T.F. Direct detection of free radicals in the reperfused rat heart using electron spin resonance spectroscopy. Circ Res. 61:1987;757-760.
16. Massoudy P., Mempel T., Raschke P., Becker B.F. Reduction of oxygen delivery during post-ischemic reperfusion protects the isolated guinea pig heart. Basic Res. Cardiol. 94:1999;231-237.
17. Blaustein A.S., Schine L., Brooks W.W., Fanburg B.L., Bing O.H. Influence of exogenously generated oxidant species on myocardial function. Am J Physiol. 250:1986;H595-H599.
18. Vasquez-Vivar J., Kalyanaraman B., Kennedy M.C. Mitochondrial aconitase as a source of hydroxyl radical. An electron spin resonance investigation. J. Biol. Chem. 275:2000;14064-14069.
19. Wang P., Zweier J.L. Measurement of nitric oxide and peroxynitrite generation in the postischemic heart. Evidence for peroxynitrite-mediated reperfusion injury. J Biol Chem. 271:1996;29223-29230.
20. Liu P., Hock C.E., Nagele R., Wong P.Y. Formation of nitric oxide, superoxide, and peroxynitrite in myocardial ischemia-reperfusion injury in rats. Am J Physiol. 272:1997;H2327-2336.
21. 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.
22. Balligand J.L., Ungureanu-Longrois D., Simmons W.W., Pimental D. Cytokine-inducible nitric oxide synthase (iNSO) expression in cardiac myocytes: characterization and regulation of iNOS expression and detection of INOS activity in single cardiac myocytes in vitro. J Biol Chem. 269:1994;27580-27588.
23. Wildhirt S.M., Weismueller S., Schulze C., Conrad N. 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.
24. Wang D., Yang X.P., Liu Y.H., Carretero O.A., LaPointe M.C. Reduction of myocardial infarct size by inhibition of inducible nitric oxide synthase. Am J Hypertens. 12:1999;174-182.
25. Kanno S., Lee P.C., Zhang Y. Attenuation of myocardial ischemia/reperfusion injury by superinduction of inducible nitric oxide synthase. Circulation. 101:2000;2742-2748.
26. Zingarelli B., Hake P.W., Yang Z., et al. Absence of inducible nitric oxide synthase modulates early reperfusion-induced NF-B and AP-1 activation and enhances myocardial damage. FASEB J. 16:2002;327-342.
27. Jones S.P., Trocha S.D., Lefer D.J. Cardioprotective actions of endogenous IL-10 are independent of iNOS. Am J Physiol Heart Circ Physiol. 281:(1):2001;H48-52.
28. Xi L., Jarrett N.C., Hess M.L., Kukreja R.C. Myocardial ischemia/reperfusion injury in the inducible nitric oxide synthase knockout mice. Life Sci. 65:1999;935-945.
29. Zweier J.L., Fertmann J., Wei G. Nitric oxide and peroxynitrite in postischemic myocardium. Antioxid Redox Signal. 3:2001;11-22.
30. 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.
31. Ronson RS, Thourani VH, Ma XL et al. Peroxynitrite, the breakdown product of nitric oxide, is beneficial in blood cardioplegia but injurious in crystalloid cardioplegia. Circulation 1999;100:II-384-91.
32. 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. 275:1998;509-519.
33. 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.
34. Lee C., Liu X., Zweier J.L. Regulation of xanthine oxidase by nitric oxide and peroxynitrite. J Biol Chem. 275:2000;9369-9376.
35. Wang W., Sawicki G., Schulz R. Peroxynitrite-induced myocardial injury is mediated through matrix metalloproteinase-2. Cardiovasc Res. 53:2002;165-174.
36. Cheung P.Y., Sawicki G., Wozniak M., et al. Matrix metalloproteinase-2 contributes to ischemia-reperfusion injury in the heart. Circulation. 101:2000;1833-1839.
37. Duilio C., Ambrosio G., Kuppusamy P., DiPaula A., Becker L.C., Zweier J.L. Neutrophils are primary source of O2 radicals during reperfusion after prolonged myocardial ischemia. Am J Physiol Heart Circ Physiol. 280:2001;H2649-2657.
38. Ambrosio G., Zweier J.L., Duilio C., et al. Evidence that mitochondrial respiration is a source of potentially toxic oxygen free radicals in intact rabbit hearts subjected to ischemia and reflow. J Biol Chem. 268:1993;18532-18541.
39. Hardy L., Clark J.B., Darley-Usmar V.M., Smith D.R., Stone D. Reoxygenation-dependent decrease in mitochondrial NADH:CoQ reductase (Complex I) activity in the hypoxic/reoxygenated rat heart. Biochem J. 274:1991;133-137.
40. Xu K.Y., Zweier J.L., Becker L.C. Hydroxyl radical inhibits sarcoplasmic reticulum Ca2+-ATPase function by direct attack on the ATP binding site. Circ Res. 80:1997;76-81.
41. Powell S.R., Gurzenda E.M., Wahezi S.E. Actin is oxidized during myocardial ischemia. Free Radic Biol Med. 30:2001;1171-1176.
42. Suzuki S., Kaneko M., Chapman D.C., Dhalla N.S. Alterations in cardiac contractile proteins due to oxygen free radicals. Biochim Biophys Acta. 1074:1991;95-100.
43. Bulteau A.L., Lundberg K.C., Humphries K.M., et al. Oxidative modification and inactivation of the proteasome during coronary occlusion/reperfusion. J Biol Chem. 276:2001;30057-30063.
44. Ambrosio G., Flaherty J.T., Duilio C., et al. Oxygen radicals generated at reflow induce peroxidation of membrane lipids in reperfused hearts. J Clin Invest. 87:1991;2056-2066.
45. Paradies G., Petrosillo G., Pistolese M., Di Venosa N., Serena D., Ruggiero F.M. Lipid peroxidation and alterations to oxidative metabolism in mitochondria isolated from rat heart subjected to ischemia and reperfusion. Free Radic Biol Med. 27:1999;42-50.
46. Li Q., Bolli R., Qiu Y., Tang X.L., Guo Y., French B.A. Gene therapy with extracellular superoxide dismutase protects conscious rabbits against myocardial infarction. Circulation. 103:2001;1893-1898.
47. Yamakura F., Taka H., Fujimura T., Murayama K. Inactivation of human manganese-superoxide dismutase by peroxynitrite is caused by exclusive nitration of tyrosine 34 to 3-nitrotyrosine. J Biol Chem. 273:1998;14085-14089.
48. Quijano C., Hernandez-Saavedra D., Castro L., McCord J.M., Freeman B.A., Radi R. Reaction of peroxynitrite with Mn-superoxide dismutase. Role of the metal centre in decomposition kinetics and nitration. J Biol Chem. 276:2001;11631-11638.
49. Ceconi C., Bernocchi P., Boraso A., et al. New insights on myocardial pyridine nucleotides and thiol redox state in ischemia and reperfusion damage. Cardiovasc Res. 47:(3):2000;586-594.
50. Stephens N.G., Parsons A., Schofield M., et al. Randomised controlled trial of vitamin E in patients with coronary disease: Cambridge Heart Antioxidant Study (CHAOS). Lancet. 347:1996;781-786.
51. GISSI-Prevenzione Investigators . Dietary supplementation with polyunsaturated fatty acids and vitamin E after myocardial infarction: results of the GISSI-Prevenzione trial. Lancet. 54:1999;447-455.
52. Sethi R., Takeda N., Nagano M., Dhalla N.S. Beneficial effects of vitamin E treatment in acute myocardial infarction. J Cardiovasc Pharmacol Ther. 5:2000;51-58.
53. Westhuyzen J., Cochrane A.D., Tesar P.J., et al. Effect of preoperative supplementation with alpha-tocopherol and ascorbic acid on myocardial injury in patients undergoing cardiac operations. J Thorac Cardiovasc Surg. 113:(5):1997;942-948.
54. Miwa K., Igawa A., Nakagawa K., Hirai T., Inoue H. Consumption of vitamin E in coronary circulation in patients with variant angina. Cardiovasc Res. 41:1999;291-298.
55. Meagher A.A., Barry O.P., Lawson J.L., Rokach J., Fitzgerald G.A. Effects of vitamin E on lipid peroxidation in healthy persons. J Am Med Assoc. 285:2001;1178-1182.
56. Vergely C., Perrin C., Laubriet A., et al. Postischemic myocardial recovery and oxidative stress status of vitamin C deficient rat hearts. Cardiovasc Res. 51:2001;89-99.
57. Guan W., Osanai T., Kamada T., Ishizaka H., Hanada H., Okumura K. Time course of free radical production after primary coronary angioplasty for acute myocardial infarction and the effect of vitamin C. Jpn Circ J. 63:1999;924-928.
58. Halliwell B. Vitamin C: poison, prophylactic or panacea? TIBS. 24:1999;255-259.
59. Kalaycioglu S., Sinci V., Imren Y., Oz E. Metoprolol prevents ischemia-reperfusion injury by reducing lipid peroxidation. Jpn Circ J. 63:1999;718-721.
60. Yue T.L., Cheng H.-Y., Lysko P., et al. Carvedilol, a new vasodilator and beta-adrenoceptor antagonist is an antioxidant and free radical scavenger. J Pharmacol Exp Ther. 263:1992;92-98.
61. Ide T., Tsutsui H., Kinugawa S., et al. Amiodarone protects cardiac myocytes against oxidative injury by its free radical scavenging action. Circulation. 100:1999;690-692.
62. Tardif J.-C., Cote G., Lesperance J., Bourassa M., et al. Prevention of restenosis by pre and post-PTCA probucol therapy: a randomized clinical trial. Circulation. 94:1996;I-91.
63. Sia Y.T., Parker T.G., Liu P., et al. Improved post-myocardial infarction survival with probucol in rats: effects on left ventricular function, morphology, cardiac oxidative stress and cytokine expression. J Am Coll Cardiol. 39:2002;148-156.
64. Arstall M.A., Yang J., Stafford I., et al. N-Acetylcysteine in combination with nitroglycerin and streptokinase for the treatment of evolving acute myocardial infarction. Circulation. 92:1995;2855-2862.
65. Kowaltowski A.J., Netto L.E., Vercesi A.E. The thiol-specific antioxidant enzyme prevents mitochondrial permeability transition. Evidence for the participation of reactive oxygen species in this mechanism. J Biol Chem. 273:1998;12766-12769.
66. Kowaltowski A.J., Vercesi A.E. Mitochondrial damage induced by conditions of oxidative stress. Free Radic Biol Med. 26:1999;463-471.
67. Lee M.G., Lee K.T., Chi S.G., Park J.H. Costunolide induces apoptosis by ROS-mediated mitochondrial permeability transition and cytochrome c release. Biol Pharm Bull. 24:2001;303-306.
68. Hockenbery D.M., Oltvai Z.N., Yin X.M., Milliman C.L., Korsmeyer S.J. Bcl-2 functions in an antioxidant pathway to prevent apoptosis. Cell. 75:1993;241-251.
69. Marzo I., Brenner C., Zamzami N., et al. The permeability transition pore complex: a target for apoptosis regulation by caspases and bcl-2-related proteins. J Exp Med. 187:1998;1261-1271.
70. Zamzami N., Marzo I., Susin S.A., et al. The thiol crosslinking agent diamide overcomes the apoptosis-inhibitory effect of Bcl-2 by enforcing mitochondrial permeability transition. Oncogene. 16:1998;1055-1063.
71. Shimizu S., Eguchi Y., Kosaka H., et al. Prevention of hypoxia-induced cell death by Bcl-2 and Bcl-xL. Nature. 374:1995;811-813.
72. Akao M., Ohler A., O'Rourke B., Marban E. Mitochondrial ATP-sensitive potassium channels inhibit apoptosis induced by oxidative stress in cardiac cells. Circ. Res. 88:2001;1267-1275.
73. Maziere C., Conte M.A., Degonville J., Ali D., Maziere J.C. Cellular enrichment with polyunsaturated fatty acids induces an oxidative stress and activates the transcription factors AP1 and NFkappaB. Biochem Biophys Res Commun. 265:1999;116-122.
74. Chandel N.S., Trzyna W.C., McClintock D.S., Schumacker P.T. Role of oxidants in NF-kB activation and TNF-a gene transcription induced by hypoxia and endotoxin 1. J Immunol. 165:2000;1013-1021.
75. Matsui H., Ihara Y., Fujio Y., et al. Induction of interleukin (IL)-6 by hypoxia is mediated by nuclear factor (NF)-kB and NF-IL6 in cardiac myocytes. Cardiovasc Res. 42:1999;104.
76. Baumgarten W. Infarction of the heart. Am J Physiol. 2:1899;243-265.
77. Libby P., Marokko P.R., Bloor C.M., et al. Reduction of experimental myocardial infarct size by corticosteroid administration. J Clin Invest. 3:1973;599-607.
78. Roberts R., DeMello V., Sobel B.E. Deleterious effects of methylprednisolone in patients with myocardial infarction. J Am Coll Cardiol. 53:1976;204-206.
79. Romson J.L., Hook B.G., Kunkel S.L., et al. Reduction of the extent of ischemic myocardial injury by neutrophil depletion in the dog. Circulation. 67:1983;1016-1023.
80. Lucchesi B.R. Modulation of leukocyte-mediated myocardial reperfusion injury. Annu. Rev. Physiol. 52:1990;561-576.
81. Albertine K.H., Weyrich A.S., Ma X.L., et al. Quantification of neutrophil migration following myocardial ischemia and reperfusion in cats and dogs. J Leukocyte Biol. 55:1994;557-566.
82. McIntyre TM, Patel KD, Zimmerman GA, Prescott SM. Oxygen radical-mediated leukocyte adherence. In: Granger DN, Schmidt-Schinbein GW, editors. Physiology and Pathophysiology of Leukocyte Adhesion. New York: Oxford University Press, 1995, pp. 261-77.
83. Delanty N., Reilly M.P., Pratico D., et al. 8-Epi-PGF2 generation during coronary reperfusion: a potential quantitative marker of oxidant stress in vivo. Circulation. 95:1997;2492-2499.
84. Minuz P., Andrioli G., Degan M., et al. The F2-isoprostane 8-epiprostaglandin F2a increases platelet adhesion and reduces antiadhesive and antiaggregatory effects of NO. Arterioscler Thromb Vasc Biol. 18:1998;1248-1256.
85. Takahashi K., Nammour T.M., Fukunaga M., et al. Glomerular actions of a free radical-generated novel prostaglandin, 8-epi-prostaglandin F2 alpha, in the rat: evidence for interaction with thromboxane AZ receptors. J Clin Invest. 90:1992;130-141.
86. Fontana L., Giagulli C., Minuz P., et al. 8-iso-PGF(2alpha)induces beta(2)-integrin-mediated rapid adhesion of human polymorphonuclear neutrophils: a link between oxidative stress and ischemia/reperfusion. Arterioscler Thromb Vasc Biol. 21:2001;55-60.
87. Tsao P.S., Aoki N., Lefer D.J., et al. Time course of endothelial dysfunction and myocardial injury during myocardial ischemia and reperfusion in the cat. Circulation. 82:1990;1402-1412.
88. DeCaterina R., Libby O., Peng H., et al. Nitric oxide decreases cytokine-induced endothelial activation. J Clin Invest. 96:1995;60-68.
89. Lindemann S., Sharafi M., Spiecker M., et al. NO Reduces PMN adhesion to human vascular endothelial cells due to downregulation of ICAM-1 mRNA and surface expression. Thromb. Res. 97:2000;113-123.
90. Kubes P., Suzuki M., Granger N. Nitric oxide: an endogenous modulator of leukocyte adhesion. Proc Natl Acad Sci USA. 88:1991;4651-4655.
91. Ohashi Y., Kawashima S., Hirata K., et al. Nitric oxide inhibits neutrophil adhesion to cytokine-activated cardiac myocytes. Am J Physiol. 272:1997;H2807-2814.
92. Clancy R.M., Leszczynska-Piziak J., Abramson S.B. Nitric oxide, an endothelial cell relaxation factor, inhibits neutrophil superoxide anion production via a direct action on the NADPH oxidase. J Clin Invest. 90:1992;1116-1121.
93. 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.
94. Pinsky D.J., Naka Y., Liao H., et al. Hypoxia induced excitosis of endothelial cell Weibel-Palade bodies: a mechanism of rapid neutrophil recruitment after cardiac preservation. J Clin Invest. 97:1996;493-500.
95. Ma X.-L., Tsao P.S., Viehman G.E., Lefer A.M. Neutrophil-mediated vasoconstriction and endothelial dysfunction in low-flow perfusion-reperfused cat coronary artery. Circ Res. 69:1991;95-106.
96. Yang X.P., Liu Y.H., Shesely E.G., et al. Endothelial nitric oxide gene knockout mice: cardiac phenotypes and the effect of angiotensin-converting enzyme inhibitor on myocardial ischemia/reperfusion injury. Hypertension. 34:1999;24-30.
97. Iwata A., Sai S., Nitta Y., et al. Liposome-mediated gene transfection of endothelial nitric oxide synthase reduces endothelial activation and leukocyte infiltration in transplanted hearts. Circulation. 103:2001;2753-2759.
98. Glyn M.C., Ward B.J. Contraction in cardiac endothelial cells contributes to changes in capillary dimension following ischaemia and reperfusion. Cardiovasc Res. 48:2000;346-356.
99. Engler R.L., Schmid-Schönbein G.W., Pavelec R.S. Leukocyte capillary plugging in myocardial ischemia and reperfusion in the dog. Am J Pathol. 111:1983;98-111.
100. Rezkalla S.H., Kloner R.A. No-reflow phenomenon. Circulation. 105:2002;656-662.
101. Siminiak T., Flores N.A., Sheridan D.J. Neutrophil interactions with endothelium and platelets: possible role in the development of cardiovascular injury. Eur Heart J. 16:1995;160-170.
102. Kogaki S., Sawa Y., Sano T., et al. Selectin on activated platelets enhances neutrophil endothelial adherence in myocardial reperfusion injury. Cardiovasc Res. 43:1999;968-973.
103. Kharbanda R.K., Peters M., Walton B., et al. Ischemic preconditioning prevents endothelial injury and systemic neutrophil activation during ischemia-reperfusion in humans in vivo. Circulation. 103:2001;1624-1630.
104. Valen G., Hansson G.K., Dumitrescu A., Vaage J. Unstable angina activates myocardial heat shock protein 72, endothelial nitric oxide synthase and transcription factors NFkB and AP-1. Cardiovasc Res. 47:2000;49-56.
105. Frangogiannis N.G., Smith C.W., Entman M.L. The inflammatory response in myocardial infarction. Cardiovasc Res. 53:2002;31-47.
106. Jordan J.E., Zhao Z.-Q., Vinten-Johansen J. The role of neutrophils in myocardial ischemia-reperfusion injury. Cardiovasc Res. 43:1999;860-878.
107. Vermeiren G.L.J., Claeys M.J., Van Bockstaele D., et al. Reperfusion injury after focal myocardial ischemia: polymorphonuclear leukocyte activation and its clinical implications. Resuscitation. 45:2000;35-61.
108. Litt M.R., Jeremy R.W., Weisman H.F., et al. Neutrophil depletion limited to reperfusion reduces myocardial infarct size after 90 minutes of ischemia. Evidence for neutrophil-mediated reperfusion injury. Circulation. 80:1989;1816-1827.
109. Sawa Y., Matsuda H., Shimazaki Y., et al. Evaluation of leukocyte-depleted terminal blood cardioplegic solution in patients undergoing elective and emergency coronary artery bypass grafting. J Thorac Cardiovasc Surg. 108:1994;1125-1131.
110. Hayashi Y., Sawa Y., Nishimura M., et al. Clinical evaluation of leukocyte-depleted blood cardioplegia for pediatric open heart operation. Ann Thorac Surg. 69:2000;1914-1919.
111. Kubes P., Jutila M., Payne D. Therapeutic potential of inhibiting leukocyte rolling in ischemia/reperfusion. J Clin Invest. 95:1995;2510-2519.
112. Lefer D.J., Flynn D.M., Philips M.L., et al. A novel sialyl LewisX analog attenuates neutrophil accumulation and myocardial necrosis after ischemia and reperfusion. Circulation. 90:1994;2390-2401.
113. Briaud S.A., Ding Z.-M., Michael L.H., et al. Leukocyte trafficking and myocardial reperfusion injury in ICAM-1/P-selectin-knockout mice. Am J Physiol Heart Circ Physiol. 280:2001;H60-67.
114. Jones S.P., Girod W.G., Granger N., et al. Reperfusion injury is not affected by blockade of P-selectin in the diabetic mouse heart. Am J Physiol. 277:1999;H763-H769.
115. Sayers T.J., Wiltrout T.A., Bull C.A., et al. Effect of cytokines on polymorphonuclear neutrophil infiltration in the mouse. Prostaglandin and leukotriene-independent induction of infiltration by IL-1 and tumor necrosis factor. J Immunol. 141:1988;1670-1677.
116. Chensue S.W., Remick D.G., Schmyr-Forsch C., et al. Immunohistochemical demonstration of cytoplasmic and membrane associated TNF in murine macrophages. Am J Pathol. 133:1988;564-572.
117. Frangiogiannis N.G., Lindsey M.L., Michael L.H., et al. Resident cardiac mast cells degranulate and release preformed TNF-alpha, initiating the cytokine cascade in experimental canine myocardial/reperfusion. Circulation. 98:1998;699-710.
118. Azzawi M., Hasleton P. Tumour necrosis factor alpha and the cardiovascular system: its role in cardiac allograft rejection and heart disease. Cardiovasc Res. 43:1999;850-859.
119. Ikeda U., Ikeda M., Kano S., Shimada K. Neutrophil adherence to rat cardiac myocyte by proinflammatory cytokines. J Cardiovasc Pharmacol. 23:1994;647-652.
120. Meldrum D.R., Cleveland J.C.J., Cain B.S., et al. Increased myocardial tumor necrosis factor alpha in a crystalloid-perfused model of cardiac ischemia-reperfusion injury. Ann Thorac Surg. 65:1998;439-443.
121. Cannon C.P., McCabe C.H., Wilcox R.G., et al. Association of white blood cell count with increased mortality in acute myocardial infarction and unstable angina pectoris. OPUS-TIMI 16 Investigators. Am J Cardiol. 87:2001;636-639.
122. Gao Y., Yokota R., Tang S., et al. Reversal of angiogenesis in vitro, induction of apoptosis and inhibition of Akt phosphorylation in endothelial cells by thromboxane A2. Circ Res. 87:2000;739-741.
123. Ford H.A., Bray M.A., Doig M.V., et al. Leukotrien B, a potent chemokinetic and aggregating substance released from polymorphonuclear leukocytes. Nature. 286:1980;264-265.
124. Carry M., Korley V., Willerson J.T., et al. Increased urinary leukotriene excretion in patients with cardiac ischemia. In vivo evidence for 5-lipoxygenase activation. Circulation. 85:1992;230-236.
125. Elgebaly S.A., Hashmi F.H., Houser S.L., et al. Cardiac-derived neutrophil chemotactic factors: detection in coronary sinus effluents of patients undergoing myocardial revascularisation. J Thorac Cardiovasc Surg. 103:1992;952-959.
126. Shekher A., Singh M. Role of eicosanoid inhibition of ischemia reperfusion injury: intact and isolated heart studies. Methods Find Exp Clin Pharmacol. 19:1997;223-229.
127. Oddis C.V., Mayer O.H., Finkel M.S. Inotropic, chronotropic and radioligand binding characteristics of leukotriene B4 in cardiac myocyte, papillary muscle and membrane preparations. Prostaglandins Leukot Essent Fatty Acids. 54:1996;223-228.
128. Gok S., Ulker S., Evine A. Possible contribution of leukotrienes in the arrhytmogenic effects of digoxin on isolated guinea pig hearts. Pharmacology. 57:1998;279-284.
129. Amsterdam E.A., Pan H.L., Rendig S.V., et al. Limitation of myocardial infarct size in pigs with a dual lipoxygenase-cyclooxygenase blocking agent by inhibition of neutrophil activity without reduction of neutrophil migration. J Am Coll Cardiol. 22:1993;1738-1744.
130. Hahn R.A., MacDonald B.R., Morgan E., et al. Evaluation of LY203647 on cardiovascular leukotriene D4 receptors and myocardial reperfusion injury. J Pharmacol Exp Ther. 260:1992;979-989.
131. Hoffman B.F., Guo S.D., Feinmark S.J. Arrhytmias caused by platelet activating factor. J Cardiovasc Electrophysiol. 7:1996;120-133.
132. Koltai M., Tosaki A., Hosford D., et al. Effect of BN 50750739, a new platelet activating factor antagonist, on ischemia induced ventricular arrhytmias in isolated working rat hearts. Cardiovasc Res. 25:1991;391-397.
133. Stafforini D.M., McIntyre T.M., Zimmerman G.A., Prescott S.M. Platelet-activating factor acetylhydrolases. J Biol Chem. 272:1997;17895-17898.
134. Morgan E.N., Boyle E.M., Yun W., et al. Platelet-activating factor acetylhydrolase prevents myocardial ischemia-reperfusion injury. Circulation. 100:1999;II-365-368.
135. Saraste A., Pulkki K., Kallajoki M., et al. Apoptosis in human acute myocardial infarction. Circulation. 95:1997;320-323.
136. Zhao Z.-Q., Nakamura M., Wang N.-P., et al. Reperfusion induces myocardial apoptotic cell death. Cardiovasc Res. 45:2000;651-660.
137. Bacon K.B., Premack B.A., Gardner P., Schall T.J. Accumulation of dual T cell signalling pathways by the chemokine RANTES. Science. 269:1995;1727-1730.
138. Clavien P.-A., Harvey P.R.C., Sanabria J.R., et al. Lymphocyte adherence in the reperfused rat liver: mechanisms and effects. Hepatology. 17:1993;131-142.
139. Rabb H., Daniels F., O'Donnel M., et al. Pathophysiological role of T lymphocytes in renal ischemia-reperfusion injury in mice. Am J Physiol Renal Physiol. 279:2000;F525-531.
140. Kokura S., Wolf R.E., Yoshikawa T., et al. T-lymphocyte-derived tumor necrosis factor exacerbates anoxia-reoxygenation-induced neutrophil-endothelial cell adhesion. Circ Res. 86:2000;205-213.
141. Nakajima T., Schulte S., Warrington K.J., et al. T-cell-mediated lysis of endothelial cells in acute coronary syndromes. Circulation. 105:(5):2002;570-575.
142. Molkentin J.D. Calcineurin and beyond. Cardiac hypertrophic signalling. Circ. Res. 87:2000;731-738.
143. Saito S., Hiroi Y., Zou Y., et al. b-Adrenergic pathway induces apoptosis through calcineurin activation in cardiac myocytes. J Biol Chem. 275:2000;34528-34533.
144. Squadrito F., Altavilla D., Squadrito G., et al. Cyclosporin A reduces leukocyte accumulation and protects against myocardial ischemia reperfusion injury in rats. Eur J Pharmacol. 364:1999;159-168.
145. Murry C.E., Giachelli C.M., Schwartz S.M., Vracko R. Macrophages express osteopontin during repair of myocardial necrosis. Am J Pathol. 145:1994;1450-1462.
146. Herskowitz A., Choi S., Ansari A.A., Wesselingh S. Cytokine mRNA expression in postischemic/reperfused myocardium. Am J Pathol. 146:1995;419-428.
147. Rampart M., Wiliams T.J. Evidence that neutrophil accumulation induced by interleukin-1 requires both local protein biosyntesis and neutrophil CD18 antigen expression in vivo. Br J Pharmacol. 94:1988;1143-1148.
148. Arstall M.A., Sawyer D.B., Fukazawa R., et al. Cytokine-mediated apoptosis in cardiac myocytes: the role of inducible nitric oxide synthase induction and peroxynitrate generation. Circ Res. 85:1999;829-840.
149. Lotz M. Interleukin-6. Cancer Invest. 11:1993;732-742.
150. Kukielka G.L., Smith W., Manning A.M., et al. Induction of interleukin-6 synthesis in the myocardium: potential role in reperfusion inflammatory injury. Circulation. 92:1995;1866-1875.
151. Neumann F.J., Ott I., Gawaz M., et al. Cardiac release of cytokines and inflammatory responses in acute myocardial infarction Circulation. 92:1995;748-755.
152. Xing Z., Gauldie J., Cox G., et al. IL-6 is an antiinflammatory cytokine required for controlling local or systemic acute inflammatory responses. J Clin Invest. 101:1998;311-320.
153. Kharazmi A., Nielsen H., Rechnitzer C., Bendtzen K. Interleukin-6 primes human neutrophil and monocyte oxidative burst response. Immunol Lett. 21:1989;177-184.
154. Kukielka G.L., Hawkins H.K., Michael L., et al. Regulation of intercellular adhesion molecule-1 (ICAM-1) in ischemic and reperfused canine myocardium. J Clin Invest. 92:1993;1504-1516.
155. Wollert K.C., Drexler H. The role of interleukin-6 in the failing heart. Heart Fail Rev. 6:2001;95-103.
156. Birdsall H.H., Green D.M., Trial J.A., et al. Complement C5a, TGF-1, and MCP-1, in sequence, induce migration of monocytes into ischemic canine myocardium within the first one to five hours after reperfusion. Circulation. 95:1997;684-692.
157. Formigli L., Manneschi L.I., Nediani C., et al. Are macrophages involved in early myocardial reperfusion injury? Ann Thorac Surg. 71:2001;1596-1602.
158. Green D.M., Trial J.A., Birdsall H.H. TNFa released by comigrating monocytes promotes transendothelial migration of activated lymphocytes. J Immunol. 161:1998;2481-2489.
159. Zhao Z.-Q., Nakamura M., Wang N.-P., et al. Dynamic progression of contractile and endothelial dysfunction and infarct extension in the late phase of reperfusion. J Surg Res. 94:2000;133-144.
160. Dreyer W.J., Michael L.H., West M.W., et al. Neutrophil accumulation in ischemic canine myocardium: Insights into time course, distribution and mechanism of localization during early reperfusion. Circulation. 84:1991;400-411.
161. Simpson P.J., Fantone J.C., Mickelson J.K., et al. Identification of a time window for therapy to reduce experimental canine myocardial injury: suppression of neutrophil activation during 72 hours of reperfusion. Circ Res. 63:1988;1070-1079.
162. Simon S.I., Burns A.R., Taylor A.D., et al. L-selectin (CD62L) cross-linking signals neutrophil adhesive functions via the Mac-1 (CD11b/18) beta2-integrin. J Immunol. 155:1995;1502-1514.
163. Ma X.-L., Lefer D.J., Lefer A.M., Rothlein R. Coronary endothelial and cardiac protective effects of a monoclonal antibody to intercellular adhesion molecule-1 in myocardial ischemia and reperfusion. Circulation. 86:1992;937-946.
164. Hartman J.C., Anderson D.C., Wiltse A.L., et al. Protection of ischemic/reperfused myocardium by CL18/6, a monoclonal antibody to adhesion molecule ICAM-1. Cardiovasc Res. 30:1995;47-54.
165. Lefer D.J., Shandelya S.M., Serrano C.V. Jr., et al. Cardioprotective actions of a monoclonal antibody against CD-18 in myocardial ischemia-reperfusion injury. Circulation. 88:1993;1779-1787.
166. Palazzo A.J., Jones S.P., Girod W.G., et al. Myocardial ischemia-reperfusion injury in CD18- and ICAM-1-deficient mice. Am J Physiol. 275:1998;H2300-H2307.
167. Arai M., Lefer D.J., So T., et al. An anti-CD18 antibody limits infarct size and preserves left ventricular function in dogs with ischemia and 48-hour reperfusion. J Am Coll Cardiol. 27:1996;1278-1285.
168. Metzler B., Mair J., Lercher A., et al. Mouse model of myocardial remodelling after ischemia: role of intercellular adhesion molecule-1. Cardiovasc Res. 49:2001;399-407.
169. Briaud S.A., Ding Z.-M., Michael L.H., et al. Leukocyte trafficking and myocardial reperfusion injury in ICAM-1/P-selectin-knockout mice. Am J Physiol Heart Circ Physiol. 280:2001;H60-67.
170. Jones S.P., Girod W.G., Granger N., et al. Reperfusion injury is not affected by blockade of P-selectin in the diabetic mouse heart. Am J Physiol. 277:1999;H763-H769.
171. Hoffmeyer M.R., Jones S.P., Ross C.R., et al. Myocardial ischemia/reperfusion injury in NADPH oxidase-deficient mice. Circ Res. 87:2000;812-819.
172. Williams F.M., Tanda K., Kus M., Williams T.J. Trimetazidine inhibits neutrophil accumulation after myocardial ischemia and reperfusion in rabbits. J Cardiovasc Pharmacol. 22:1993;828-833.
173. Frangiogiannis N.G., Mendoza L.H., Lindsey M.L., et al. IL-10 is induced in the reperfused myocardium and may modulate the reaction to injury. J Immunol. 165:2000;2798-2808.
174. Yang Z., Zingarelli B., Szabo C. Crucial role of endogenous interleukin-10 production in myocardial ischemia/reperfusion injury. Circulation. 101:2000;1019-1026.
175. De Waal Malefyt R., Abrams J., Bennett B., et al. Interleukin 10 (IL-10) inhibits cytokine synthesis by human monocytes: an autoregulatory role of IL-10 produced by monocytes. J Exp Med. 174:1991;1209-1220.
176. Vermeiren G.L.J., Claeys M.J., Van Bockstaele D., et al. Reperfusion injury after focal myocardial ischemia: polymorphonuclear leukocyte activation and its clinical implications. Resuscitation. 45:2000;35-61.
177. Lefer A.M., Ma X.L., Weyrich A.S., Scalia R. Mechanism of the cardioprotective effect of transforming growth factor beta 1 in feline myocardial ischemia and reperfusion. Proc Natl Acad Sci USA. 90:1993;1018-1022.
178. Meldrum D.R., Cleveland J.C.J., Cain B.S., et al. Increased myocardial tumor necrosis factor alpha in a crystalloid-perfused model of cardiac ischemia-reperfusion injury. Ann Thorac Surg. 65:1998;439-443.
179. Cain B.S., Meldrum D.R., Dinarello C.A., et al. Tumor necrosis factor-alpha and interleukin-1beta synergistically depress human myocardial function. Crit Care Med. 27:1999;1309-1318.
180. Levine B., Kalman J., Mayer L., et al. Elevated circulating levels of tumor necrosis factor in severe chronic heart failure. New Engl J Med. 323:1990;236-241.
181. Hegewish S., Weh H.J., Hossfeld D.K. TNF-induced cardiomyopathy. Lancet. 2:1990;294-295.
182. Herskowitz A., Choi S., Ansari A.A., Wesselingh S. Cytokine mRNA expression in postischemic/reperfused myocardium. Am J Pathol. 146:1995;419-428.
183. Vaddi K., Nicolini F.A., Mehta P., Mehta J.P. Increased secretion of tumour necrosis factor alpha and interferon-gamma by mononuclear leukocytes in patients with ischemic heart disease: relevance in superoxide anion generation. Circulation. 90:1994;694-699.
184. Ridker P.M., Rifai N., Pfeffer M., et al. Elevation of tumor necrosis factor-α and increased risk of recurrent coronary events after myocardial infarction. Circulation. 101:2000;2149-2153.
185. Kurrelmeyer K.M., Michael L.H., Baumgarten G., et al. Endogenous tumor necrosis factor protects the adult cardiac myocyte against ischemic-induced apoptosis in a murine model of acute myocardial infarction. Proc Natl Acad Sci. 97:2000;5456-5461.
186. Sack M.N., Smith R.M., Opie L.H. Tumor necrosis factor in myocardial hypertrophy and ischemia - an anti-apoptotic perspective. Cardiovasc Res. 45:2000;688-695.
187. Natoli G., Constanzo A., Guido F., et al. Apoptotic, non-apoptotic and anti-apoptotic pathways of tumor necrosis factor signalling. Biochem Pharmacol. 56:1998;915-920.
188. Hefti M.A., Harder B.A., Eppenberger H.M., Schaub M.C. Signalling pathways in cardiac myocyte hypertrophy. J Moll Cell Cardiol. 29:1997;2873-2892.
189. Nelson S.K., Wong G.H., McCord J.M. Leukemia inhibitory factor and tumor necrosis factor induce manganese superoxide dismutase and protect rabbit hearts from reperfusion injury. J Moll Cell Cardiol. 27:1995;223-229.
190. Zhao Z.Q., Nakamura M., Wang N.-P., et al. Administration of adenosine during reperfusion reduces injury of vascular endothelium and death of myocytes. Coronary Artery Dis. 10:1999;617-628.
191. Mahaffey K.W., Puma J.A., Barbagelata A., et al. Adenosine as an adjunct to thrombolytic therapy for acute myocardial infarction. J Am Coll Cardiol. 34:1999;1711-1720.
192. Marzilli M., Orsini E., Marraccini P., Testa R. Beneficial effect of intracoronary adenosine as an adjunct to primary angioplasty in acute myocardial infarction. Circulation. 101:2000;2154-2159.
193. Buerke M., Rupprecht H.J., vom Dahl J., et al. Sodium-hydrogen exchange inhibition: novel strategy to prevent myocardial injury following ischemia and reperfusion. Am J Cardiol. 83:1999;19G-22G.
194. Theroux P. Protection of the myocardial cell during ischemia. Am J Cardiol. 83:1999;3G-9G.
195. Yamada K., Horikawa N., Matsui K., et al. Inhibitory effect of SM-20550, an Na+/H+ exchange inhibitor, on accumulation of leukocytes in ischemia and reperfusion. Naunyn Schmiedebergs Arch Pharmacol. 363:(6):2001;597-603.
196. Rupprecht H.J., vom Dahl J., Terres W., et al. Cardioprotective effects of the Na(+)/H(+) exchange inhibitor cariporide in patients with acute anterior myocardial infarction undergoing direct PTCA. Circulation. 101:2000;2902-2908.
197. Theroux P., Chaitman B.R., Danchin N., et al. Inhibition of the sodium-hydrogen exchanger with cariporide to prevent myocardial infarction in high risk ischemic situations. Circulation. 102:2000;3032-3038.
198. Mickelson J.K., Ali M.N., Kleiman N.S., et al. Chimeric 7E3 Fab (ReoPro) decreases detectable CD11b on neutrophils from patients undergoing angioplasty. J Am Coll Cardiol. 33:1999;97-106.
199. Neumann F.J., Blasini R., Scmitt C., et al. Effects of glycoprotein IIb/IIIa receptor blockade on recovery of coronary blood flow and left ventricular function after the placement of coronary artery stents in acute myocardial infarction. Circulation. 98:1998;2695-2701.
200. Topol E.J., Moliterno D.J., Herrmann H.C., et al. Comparison of two platelet glycoprotein IIb/IIIa inhibitors, tirofiban and abciximab, for the prevention of ischemic events with percutaneous coronary revascularization. New Engl J Med. 344:2001;1888-1894.
201. Vakeva A.P., Agah A., Rollins S.A., et al. Myocardial infarction and apoptosis after myocardial infarction and reperfusion. Role of the terminal complement components and inhibition by anti-C5 therapy. Circulation. 97:1998;2259-2267.
202. Kowalski J., Kosmider M., Pawlicki L., et al. Complement activates neutrophils during PTCA procedure in patients with unstable angina pectoris. Int J Cardiol. 58:1997;229-240.
203. Lazar H.L., Bao Y., Gaudiani J., Rivers S., Marsh H. Total complement inhibition. An effective strategy to limit ischemic injury during coronary revascularization on cardiopulmonary bypass. Circulation. 100:1999;1438-1442.
204. Shalabi E.A. Acetaminophen inhibits the human polymorphonuclear leukocyte function in vitro. Immunopharmacology. 24:1992;37-45.
205. Kapiotis S., Sengoelge G., Hermann M., et al. Paracetamol catalyzes myeloperoxidase-initiated lipid oxidation in LDL. Arterioscler Thromb Vasc Biol. 17:1997;2855-2860.
206. Merill G., McConnel P., Vandyke K., Powell S. Coronary and myocardial effects of acetaminophen:protection during ischemia-reperfusion. Am J Physiol. 280:2001;H2631-2638.
207. Yue T., Chen J., Bao W., et al. In vivo myocardial protection from ischemia/reperfusion injury by the peroxisome proliferator-activated receptor-agonist rosiglitazone. Circulation. 104:2001;2588.
208. Abunasra H.J., Smolenski R.T., Morrison K., et al. Efficacy of adenoviral gene transfer with manganese superoxide dismutase and endothelial nitric oxide synthase in reducing ischemia and reperfusion injury. Eur J Cardiothorac Surg. 20:2001;153-158.
209. Okubo S., Wildner O., Shah M., Chelliah J.C., Hess M.L., Kukreja R.C. Gene transfer of heat-shock protein 70 reduces infarct size in vivo after ischemia/reperfusion in the rabbit heart. Circulation. 103:2001;877-881.
210. + T-lymphocytes mediate ischemia/reperfusion-induced inflammatory responses in mouse liver. J Clin Invest. 100:1997;279-289.
211. Gu H., Marth J.D., Orban P.C., Mossmann H., Rajewsky K. Deletion of a DNA polymerase beta gene segment in T cells using cell type-specific gene targeting. Science. 265:1994;103-106.
212. Kuhn R., Schwenk F., Aguet M., Rajewsky K. Inducible gene targeting in mice. Science. 269:1995;1427-1429.