The role of oxidants and free radicals in reperfusion injury

Cardiovascular Research

Volumn 70, Issue 2, 2006, Pages 181-190

  Zweier, Jay L ^a   Talukder, M A Hassan ^a  

^a OHIO STATE UNIVERSITY   (United States)

Author keywords

Ischemia; Nitric oxide; Oxygen radicals; Preconditioning; Reperfusion

Indexed keywords

CALCIUM; FREE RADICAL; N(G) METHYLARGININE; N(G) NITROARGININE METHYL ESTER; NITRIC OXIDE; NITRIC OXIDE SYNTHASE; NITRITE; OXIDIZING AGENT; PROSTAGLANDIN SYNTHASE; REDUCED NICOTINAMIDE ADENINE DINUCLEOTIDE PHOSPHATE OXIDASE; XANTHINE OXIDASE;

CALCIUM CELL LEVEL; ENDOTHELIUM CELL; HEART MUSCLE CONTRACTILITY; HEART MUSCLE INJURY; HEART MUSCLE ISCHEMIA; HEART PROTECTION; HUMAN; INFLAMMATION; ISCHEMIC PRECONDITIONING; MITOCHONDRIAL RESPIRATION; NEUTROPHIL CHEMOTAXIS; NONHUMAN; OXIDATIVE STRESS; PRIORITY JOURNAL; REPERFUSION INJURY; REVIEW; STUNNED HEART MUSCLE;

CHEMOTAXIS, LEUKOCYTE; CORONARY CIRCULATION; ENDOTHELIAL CELLS; ENDOTHELIUM, VASCULAR; FREE RADICALS; HUMANS; MYOCARDIAL REPERFUSION INJURY; MYOCARDIUM; NITRIC OXIDE; NITRIC OXIDE SYNTHASE; OXIDANTS;

EID: 33646055216     PISSN: 00086363     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.cardiores.2006.02.025     Document Type: Review

References (105)

1. Hansen P.R. Myocardial reperfusion injury: experimental evidence and clinical relevance. Eur Heart J 16 (1995) 734-740
2. Ferrari R. Metabolic disturbances during myocardial ischemia and reperfusion. Am J Cardiol 76 (1995) 17B-24B
3. Whalen D.A., Hamilton D.G., Ganote C.E., and Jennings R.B. Effect of a transient period of ischemia on myocardial cells: I. Effects on cell volume regulation. Am J Path 74 (1974) 381-398
4. Kloner R.A., Ganote C.E., Whalen D.A., and Jennings R.B. Effect of a transient period of ischemia on myocardial cells: II. Fine structure during the first few minutes of reflow. Am J Path 74 (1974) 399-422
5. Gross G.J., Kersten J.R., and Warltier D.C. Mechanisms of postischemic contractile dysfunction. Ann Thorac Surg 68 (1999) 1898-1904
6. Piper H.M., and García-Dorado D. Prime causes of rapid cardiomyocyte death during reperfusion. Ann Thorac Surg 68 (1999) 1913-1919
7. Ambrosio G., Weisfeldt M.L., Jacobus W.E., and Flaherty J.T. Evidence for a reversible oxygen radical mediated component of reperfusion injury: Reduction by recombinant human superoxide dismutase administered at the time of reflow. Circulation 75 (1987) 282-291
8. VanBenthuysen K.M., McMurtry I.F., and Horwitz L.D. Reperfusion after acute coronary occlusion in dogs impairs endothelium-dependent relaxation to acetylcholine and augments contractile reactivity in vitro. J Clin Invest 79 (1987) 265-274
9. Pearson P.J., Schaff H.V., and Vanhoutte P.M. Long-term impairment of endothelium-dependent relaxations to aggregating platelets after reperfusion injury in canine coronary arteries. Circulation 81 (1990) 1921-1927
10. Jeroudi M.O., Hartley C.J., and Bolli R. Myocardial reperfusion injury: Role of oxygen radicals and potential therapy with antioxidants. Am J Cardiol 73 (1994) 2B-7B
11. Hess M.L., and Kukreja R.C. Myocardial stunning. J Card Surg 9 (1994) 382-386
12. Flaherty J.T., and Zweier J.L. Role of oxygen radicals in myocardial reperfusion injury: Experimental and clinical evidence. Klin Wochenschr 69 (1991) 1061-1065
13. Manning A.S., and Hearse D.J. Reperfusion-induced arrhythmias: Mechanisms and prevention. J Mol Cell Cardiol 16 (1984) 497-518
14. Irani K., Xia Y., Zweier J.L., Sollott S.J., Der C.J., et al. Mitogenic signaling mediated by oxidants in ras-transformed fibroblast. Science 275 (1997) 1649-1652
15. Dhalla N.S., Elmoselhi A.B., Hata T., and Makino N. Status of myocardial antioxidants in ischemia-reperfusion injury. Cardiovasc Res 47 (2000) 446-456
16. Hess M.L., Okabe E., and Kontos H.A. Proton and free oxygen radical interaction with the calcium transport system of cardiac sarcoplasmic reticulum. J Mol Cell Cardiol 13 (1981) 767-772
17. Rosen H., and Klebanoff S.J. Hydroxyl radical generation by polymorphonuclear leukocytes measured by electron spin resonance spectroscopy. J Clin Invest 64 (1979) 1725-1729
18. Shlafer M., Kane P.F., and Kirsh M.M. Superoxide dismutase plus catalase enhances the efficacy of hypothermic cardioplegia to protect the globally ischemic, reperfused heart. J Thorac Cardiovasc Surg 83 (1982) 830-839
19. Jolly S.R., Kane W.J., Bailie M.B., Abrams G.D., and Lucchesi B.R. Canine myocardial reperfusion injury. Its reduction by the combined administration of superoxide dismutase and catalase. Circ Res 54 (1984) 277-285
20. Werns S.W., Shea M.J., Driscoll E.M., Cohen C., Abrams G.D., et al. The independent effects of oxygen radical scavengers on canine infarct size. Reduction by superoxide dismutase but not catalase. Circ Res 56 (1985) 895-898
21. Chambers D.E., Parks D.A., Patterson G., Roy R., McCord J.M., et al. Xanthine oxidase as a source of free radical damage in myocardial ischemia. J Mol Cell Cardiol 17 (1985) 145-152
22. Mergner G.W., Weglicki W.B., and Kramer J.H. Postischemic free radical production in the venous blood of the regionally ischemic swine heart. Effect of deferoxamine. Circulation 84 (1991) 2079-2090
23. Zweier J.L., Duke S.S., Kuppusamy P., Sylvester J.T., and Gabrielson E.W. Electron paramagnetic resonance evidence that cellular oxygen toxicity is caused by the generation of superoxide and hydroxyl free radicals. FEBS Lett 252 (1989) 12-16
24. Ambrosio G., Zweier J.L., and Flaherty J.T. The relationship between oxygen radical generation and impairment of myocardial energy metabolism following post-ischemic reperfusion. J Mol Cell Cardiol 23 (1991) 1359-1374
25. Thompson-Gorman S.L., and Zweier J.L. Evaluation of the role of xanthine oxidase in myocardial reperfusion injury. J Biol Chem 265 (1990) 6656-6663
26. 2+ overload during postischemic reperfusion. Am J Physiol 266 (1994) H2174-H2181
27. Hearse D.J., Humphrey S.M., and Chain E.B. Abrupt reoxygenation of the anoxic potassium-arrested perfused rat heart: A study of myocardial enzyme release. J Mol Cell Cardiol 5 (1973) 395-407
28. Lucas S.K., Gardner T.J., Flaherty J.Y., Bulkley B.H., Elmer E.B., and Gott V.L. Beneficial effects of mannitol administration during reperfusion after ischemic arrest. Circulation 62 Suppl I (1980) I34-I41
29. Stewart J.R., Blackwell W.H., Crute S.L., Loughlin V., Greenfield L.J., and Hess M.L. Inhibition of surgically induced ischemia/reperfusion injury by oxygen free radical scavengers. J Thorac Cardiovasc Surg 86 (1983) 262-272
30. Burton K.P., McCord J.M., and Ghai G. Myocardial alterations due to free-radical generation. Am J Physiol 246 (1984) H776-H783
31. Ytrehus K., Myklebust R., and Mjos O.D. Influence of oxygen radicals generated by xanthine oxidase in the isolated perfused rat heart. Cardiovasc Res 20 (1986) 597-603
32. Zweier J.L., Flaherty J.T., and Weisfeldt M.L. Direct measurement of free radical generation following reperfusion of ischemic myocardium. Proc Natl Acad Sci USA 84 (1987) 1404-1407
33. Zweier J.L., Rayburn B.K., Flaherty J.T., and Weisfeldt M.L. Recombinant superoxide dismutase reduces oxygen free radical concentrations in reperfused myocardium. J Clin Invest 80 (1987) 1728-1734
34. Zweier J.L., and Kuppusamy P. Electron paramagnetic resonance measurements of free radicals in the intact beating heart: A technique for detection and characterization of free radicals in whole biological tissues. Proc Natl Acad Sci USA 85 (1988) 5703-5707
35. Zweier J.L., Kuppusamy P., Williams R., Rayburn B.K., Smith D., et al. Measurement and characterization of postischemic free radical generation in the isolated perfused heart. J Biol Chem 264 (1989) 18890-18895
36. Zweier J.L. Measurement of superoxide derived free radicals in the reperfused heart: Evidence for a free radical mechanism of reperfusion injury. J Biol Chem 263 (1988) 1353-1357
37. Bolli R., Jeroudi M.O., Patel B.S., DuBose C.M., Lai E.K., et al. Direct evidence that oxygen-derived free radicals contribute to postischemic myocardial dysfunction in the intact dog. Proc Natl Acad Sci USA 86 (1989) 4695-4699
38. Grill H.P., Zweier J.L., Kuppusamy P., Weisfeldt M.L., and Flaherty J.T. Direct measurement of myocardial free radical generation in an in vivo model: Effects of postischemic reperfusion and treatment with human recombinant superoxide dismutase. J Am Coll Cardiol 20 (1992) 1604-1611
39. Josephson R.A., Silverman H.S., Lakatta E.G., Stern M.D., and Zweier J.L. Study of the mechanisms of hydrogen peroxide and hydroxy free radical induced cellular injury and calcium overload in cardiac myocytes. J Biol Chem 266 (1991) 2354-2361
40. Corretti M.C., Koretsune Y., Kusuoka H., Chako V.P., Zweier J.L., and Marban E. Glycolytic inhibition and calcium overload as consequences of exogenously-generated free radicals in rabbit hearts. J Clin Invest 88 (1991) 1014-1025
41. Flaherty J.T., and Zweier J.L. Does lethal myocardial reperfusion injury exist?. J Thromb Thrombolysis 4 (1997) 91-93
42. Bolli R., Becker L., Gross G., Mentzer Jr. R., Balshaw D., and Lathrop D.A. Myocardial protection at a crossroads. The need for translation into clinical therapy. Circ Res 95 (2004) 125-134
43. Hammond B., and Hess M.L. The oxygen free radical system: Potential mediator of myocardial injury. J Am Col Cardiol 6 (1985) 215-220
44. Zweier J.L., and Villamena F.A. Chemistry of free radicals in biological systems. In: Kukin M.L., and Fuster V. (Eds). Oxidative stress and cardiac failure (2003), Futura Publishing Company, Inc., Armonk, NY 67-95
45. Henry T.D., Archer S.L., Nelson D., Weir E.K., and From A.H. Enhanced chemiluminescence as a measure of oxygen-derived free radical generation during ischemia and reperfusion. Circ Res 67 (1990) 1453-1461
46. Park J.L., and Lucchesi B.R. Mechanisms of myocardial reperfusion injury. Ann Thorac Surg 68 (1999) 1905-1912
47. Marczin N., El-Habashi N., Hoare G.S., Bundy R.E., and Yacoub M. Antioxidants in myocardial ischemia-reperfusion injury: Therapeutic potential and basic mechanisms. Arch Biochem Biophys 420 (2003) 222-236
48. Ferrari R., Alfieri O., Curello S., Ceconi C., Cargnoni A., et al. Occurrence of oxidative stress during reperfusion of the human heart. Circulation 81 (1990) 201-211
49. Ferrari R., Agnoletti L., Comini L., Gaia G., Bachetti T., et al. Oxidative stress during myocardial ischemia and heart failure. Eur Heart J 19 Suppl B (1998) B2-B11
50. Li Y., Zhu H., Kuppusamy P., Roubaud V., Zweier J.L., and Trush M.A. Validation of lucigenin (bis-n-methylacridinium) as a chemilumigenic probe for detecting superoxide anion radical production by enzymatic and cellular systems. J Biol Chem 273 (1998) 2015-2023
51. Rota C., Fann Y.C., and Mason R.P. Phenoxy free radical formation during the oxidation of the fluorescent dye 2',7'-dichlorofluorescein by horseradish peroxidase. J Biol Chem 274 (1999) 28161-28168
52. Tarpey M.M., Wink D.A., and Grisham M.B. Methods for detection of reactive metabolites of oxygen and nitrogen: In vitro and in vivo considerations. Am J Physiol Regul Integr Com Physiol 286 (2004) R431-R444
53. Ambrosio G., Zweier J.L., Jacobus W.E., Weisfeldt M.L., and Flaherty J.T. Improvement of postischemic myocardial function and metabolism induced by administration of deferoxamine at the time of reflow: The role of iron in the pathogenesis of reperfusion injury. Circulation 76 (1987) 906-915
54. Williams R.E., Zweier J.L., and Flaherty J.T. Treatment with deferoxamine during ischemia improves functional and metabolic recovery and reduces reperfusion-induced oxygen radical generation in rabbit hearts. Circulation 83 (1991) 1006-1014
55. Kuppusamy P., and Zweier J.L. Characterization of free radical generation by xanthine oxidase. Evidence for hydroxyl radical generation. J Biol Chem 264 (1989) 9880-9884
56. Wang P., and Zweier J.L. Measurement of nitric oxide and peroxynitrite generation in the post- ischemic heart. Evidence for peroxynitrite-mediated reperfusion injury. J Biol Chem 271 (1996) 29223-29230
57. Furchgott R.F., and Zawadzki J.V. The obligatory role of endothelial cells in the relaxation of arterial smooth muscle by acetylcholine. Nature 288 (1980) 373-376
58. Palmer R.M., Ferrige A.G., and Moncada S. Nitric oxide release accounts for the biological activity of endothelium-derived relaxing factor. Nature 327 (1987) 524-526
59. Ignarro L.J., Byrns R.E., Buga G.M., and Wood K.S. Endothelium-derived relaxing factor from pulmonary artery and vein possesses pharmacologic and chemical properties identical to those of nitric oxide radical. Circ Res 61 (1987) 866-879
60. Xia Y., and Zweier J.L. Direct measurement of nitric oxide generation from nitric oxide synthase. Proc Natl Acad Sci USA 94 (1997) 12705-12710
61. Moncada S., Palmer R.M., and Higgs E.A. Biosynthesis of nitric oxide from l-arginine. A pathway for the regulation of cell function and communication. Biochem Pharmacol 38 (1989) 1709-1715
62. Hare J.M., and Colucci W.S. Role of nitric oxide in the regulation of myocardial function. Prog Cardiovasc Dis 38 (1995) 155-166
63. Giraldez R.R., Panda A., Xia Y., Sanders S.P., and Zweier J.L. Decreased nitric-oxide synthase activity causes impaired endothelium-dependent relaxation in the postischemic heart. J Biol Chem 272 (1997) 21420-21426
64. Zweier J.L., and Jacobus W.E. Substrate-induced alterations of high energy phosphate metabolism and contractile function in the perfused heart. J Biol Chem 262 (1987) 8015-8021
65. Beckman J.S., Beckman T.W., Chen J., Marshall P.A., and Freeman B.A. Apparent hydroxyl radical production by peroxynitrite: Implications for endothelial injury from nitric oxide and superoxide. Proc Natl Acad Sci USA 87 (1990) 1620-1624
66. Lefer A.M., Tsao P.S., Lefer D.J., and Ma X.L. Role of endothelial dysfunction in the pathogenesis of reperfusion injury after myocardial ischemia. FASEB J 5 (1991) 2029-2034
67. Zweier J.L., Wang P., and Kuppusamy P. Direct measurement of nitric oxide generation in the ischemic heart using electron paramagnetic resonance spectroscopy. J Biol Chem 270 (1995) 304-307
68. Zweier J.L., Samouilov A., and Kuppusamy P. Non-enzymatic nitric oxide synthesis in biological systems. Biochim Biophys Acta 1411 (1999) 250-262
69. Zweier J.L., Wang P., Samouilov A., and Kuppusamy P. Enzyme-independent formation of nitric oxide in biological tissues. Nat Med 1 (1995) 804-809
70. McCord J.M. Oxygen derived free radicals in post-ischemic tissue injury. N Engl J Med 312 (1985) 159-163
71. Guarnieri C., Flamigni F., and Caldarera C.M. Role of oxygen in the cellular damage induced by re-oxygenation of hypoxic hearts. J Mol Cell Cardiol 12 (1980) 797-808
72. Zweier J.L., Kuppusamy P., and Lutty G.A. Measurement of endothelial cell free radical generation: Evidence for a central mechanism of free radical injury in post-ischemic tissues. Proc Natl Acad Sci USA 85 (1988) 4046-4050
73. Xia Y., Khatchikian G., and Zweier J.L. Adenosine deaminase inhibition prevents free radical mediated injury in the postischemic heart. J Biol Chem 271 (1996) 10096-10102
74. Zweier J.L., Broderick R., Kuppusamy P., Thompson-Gorman S., and Lutty G.A. Determination of the mechanisms of free radical generation in human aortic endothelial cells exposed to anoxia and reoxygenation. J Biol Chem 269 (1994) 24156-24162
75. Xia Y., and Zweier J.L. Substrate control of free radical generation from xanthine oxidase in the postischemic heart. J Biol Chem 270 (1995) 18797-18803
76. Eddy L.J., Stewart J.R., Jones H.P., Engerson T.D., McCord J.M., and Downey J.M. Free radical-producing enzyme, xanthine oxidase, is undetectable in human hearts. Am J Physiol 253 (1987) H709-H711
77. de Jong J.W., van der Meer P., Nieukoop A.S., Huizer T., Stroeve R.J., and Bos E. Xanthine oxidoreductase activity in perfused hearts of various species, including humans. Circ Res 67 (1990) 770-773
78. Cappola T.P., Kass D.A., Nelson G.S., Berger R.D., Rosas G.O., et al. Allopurinol improves myocardial efficiency in patients with idiopathic dilated cardiomyopathy. Circulation 104 (2001) 2407-2411
79. Coghlan J.G., Flitter W.D., Clutton S.M., Panda R., Daly R., et al. Allopurinol pretreatment improves postoperative recovery and reduces lipid peroxidation in patients undergoing coronary artery bypass grafting. J Thorac Cardiovasc Surg 107 (1994) 248-256
80. Adachi H., Motomatsu K., and Yara I. Effect of allopurinol (zyloric) on patients undergoing open heart surgery. Jpn Circ J 43 (1979) 395-401
81. Gimpel J.A., Lahpor J.R., van der Molen A., Damen J., and Hitchcock J.F. Reduction of reperfusion injury of human myocardium by allopurinol: A clinical study. Free Radic Biol Med 19 (1995) 251-255
82. Berry C.E., and Hare J.M. Xanthine oxidoreductase and cardiovascular disease: Molecular mechanisms and pathophysiological implications. J Physiol 555 (2004) 589-606
83. Zorov D.B., Filburn C.R., Klotz L.-O., Zweier J.L., and Sollott S.J. Reactive oxygen species (ros)-induced ros release: A new phenomenon accompanying induction of the mitochondrial permeability transition in cardiac myocytes. J Exp Med 192 (2000) 1001-1014
84. Xia Y., Dawson V.L., Dawson T.M., Snyder S.H., and Zweier J.L. Nitric oxide synthase generates superoxide and nitric oxide in arginine-depleted cells leading to peroxynitrite mediated cellular injury. Proc Nat Acad Sci USA 93 (1996) 6770-6774
85. Xia Y., and Zweier J.L. Superoxide and peroxynitrite generation from inducible nitric oxide synthase in macrophages. Proc Nat Acad Sci USA 94 (1997) 6954-6958
86. Xia Y., Roman L.J., Masters B.S.S., and Zweier J.L. Inducible nitric oxide synthase generates superoxide from the reductase domain. J Biol Chem 273 (1998) 22625-22639
87. Shandelya S.M., Kuppusamy P., Weisfeldt M.L., and Zweier J.L. Evaluation of the role of polymorphonuclear leukocytes on contractile function in myocardial reperfusion injury. Evidence for plasma-mediated leukocyte activation. Circulation 87 (1993) 536-546
88. Shandelya S.M., Kuppusamy P., Herskowitz A., Weisfeldt M.L., and Zweier J.L. Soluble complement receptor type 1 inhibits the complement pathway and prevents contractile failure in the postischemic heart. Evidence that complement activation is required for neutrophil-mediated reperfusion injury. Circulation 88 (1993) 2821-2826
89. Serrano Jr. C.V., Mikhail E.A., Wang P., Noble B., Kuppusamy P., and Zweier J.L. Superoxide and hydrogen peroxide induce cd18-mediated adhesion in the postischemic heart. Biochim Biophys Acta 1316 (1996) 191-202
90. Williams F.M. Neutrophils and myocardial reperfusion injury. Pharmacol Ther 72 (1996) 1-12
91. Vinten-Johansen J. Involvement of neutrophils in the pathogenesis of lethal myocardial reperfusion injury. Cardiovasc Res 61 (2004) 481-497
92. Kuppusamy P., Wang P., Samouilov A., and Zweier J.L. Spatial mapping of nitric oxide generation in the ischemic heart using electron paramagnetic resonance imaging. Magn Reson Med 36 (1996) 212-218
93. Samouilov A., Kuppusamy P., and Zweier J.L. Evaluation of the magnitude and rate of nitric oxide production from nitrite in biological systems. Arch Biochem Biophys 357 (1998) 1-7
94. Samouilov A., and Zweier J.L. Analytical implications of iron-dithiocarbamates for the measurement of nitric oxide. Methods Enzymol 352 (2002) 506-522
95. Vanin A.F., Liu X., Samouilov A., Stukan R.A., and Zweier J.L. Redox properties of iron-dithiocarbamates and their nitrosyl derivatives: Implications for their use as traps of nitric oxide in biological systems. Biochim Biophys Acta 1474 (2000) 365-377
96. Tiravanti E., Samouilov A., and Zweier J.L. Nitrosyl-heme complexes are formed in the ischemic heart: Evidence of nitrite-derived no formation, storage and signaling in postischemic tissues. J Biol Chem 279 (2004) 11065-11073
97. Li H., Samouilov A., Liu X., and Zweier J.L. Characterization of the magnitude and kinetics of xanthine oxidase-catalyzed nitrite reduction. J Biol Chem 276 (2001) 24482-24489
98. Li H., Samouilov A., Liu X., and Zweier J.L. Characterization of the effects of oxygen on xanthine oxidase-mediated nitric oxide formation. J Biol Chem 279 (2004) 16939-16946
99. Lee C.I., Liu X., and Zweier J.L. Regulation of xanthine oxidase by nitric oxide and peroxynitrite. J Biol Chem 275 (2000) 9369-9376
100. Lee C., Miura K., Liu X., and Zweier J.L. Biphasic regulation of leukocyte superoxide generation by nitric oxide and peroxynitrite. J Biol Chem 275 (2000) 38965-38972
101. 2+/calmodulin dependent and tetrahydrobiopterin regulatory process. J Biol Chem 273 (1998) 25804-25808
102. Yellon D.M., and Downey J.M. Preconditioning the myocardium: From cellular physiology to clinical cardiology. Physiol Rev 83 (2003) 1113-1151
103. Wang P., and Zweier J.L. Ischemic preconditioning decreases nitric oxide formation and no mediated injury in the postischemic heart. Circulation 96 8 (1997) I-I72 [abstract]
104. Csonka C., Szilvassy Z., Fulop F., Pali T., Blasig I.E., et al. Classic preconditioning decreases the harmful accumulation of nitric oxide during ischemia and reperfusion in rat hearts. Circulation 100 (1999) 2260-2266
105. Zhao X., He G., Chen Y.-R., Pandian R., Kuppusamy P., and Zweier J.L. Endothelium-derived nitric oxide regulates postischemic myocardial oxygenation and oxygen consumption by modulation of mitochondrial electron transport. Circulation 111 (2005) 2966-2972