CoChat
Sign Up
Cited by 396Cardiac Ischemia and ReperfusionNitric Oxide and Endothelin EffectsRedox biology and oxidative stress

The oxygen free radical system: from equations through membrane-protein interactions to cardiovascular injury and protection

Open access
Kukreja, R. C, Hess, M. L·1992·Cardiovascular Research
DOI 10.1093/cvr/26.7.641
Open this paper in CoChat — free accountOpen PDF

Abstract

Highly toxic oxygen radicals and their metabolites have been implicated in the pathogenesis of ischaemia/reperfusion injury. These reactive oxygen species include the superoxide anion, hydrogen peroxide, hydroxyl radical, and singlet oxygen. The central theme of this review is first to discuss the basic mechanisms of free radical generation from various potential sources, to point out and emphasise the growing importance of the role of singlet oxygen, and then to discuss in depth membrane-protein interactions that ultimately lead to myocardial damage and dysfunction. With this background, we highlight several novel therapeutic strategies aimed at interrupting the oxygen free radical mediated component of ischaemia/reperfusion injury. It is hoped that this thesis will then serve as a future impetus to challenge these hypotheses and further build on this truly unique system that has assumed such an important role in the pathophysiology of myocardial ischaemia/reperfusion and inflammation. "To those of us who are humbly exploring the mysteries of science, we must project our findings and model our systems. For if correct, we have made a small contribution and, if wrong, we have forced others to eventually think." A V Hill, on the occasion of the 50th anniversary of E H Starling's Linacre lecture (University College, London, 1968).

The claims and statistics of this paper haven’t been checked yet.

Run the check — free, no account needed. It reads the open-access text and checks the sources it cites.

A few free checks a day · papers already verified open instantly · results are public

Integrity signals

Registry

Crossref · 10.1093/cvr/26.7.641

Cites

Statistics

Claims the paper makes

The claims and statistics of this paper haven’t been checked yet.

Run the check — free, no account needed. It reads the open-access text and checks the sources it cites.

A few free checks a day · papers already verified open instantly · results are public

Claims other papers make about this one

Each is checked against this paper’s own text: does it say what the citing paper says it does?

Self-check

Percentages, sums and reported differences re-computed from the paper’s own numbers.

The self-check needs the paper’s full text.

Cites

No references could be resolved yet.

Research works printed but not linked: 148

  1. Braunwald E. Kloner RA. Myocardial reperfusion: a double-edged word. J Clin Invest I YX5;76: I7 13-9.
  2. Bolli R. Oxygen-derived free radicals and myocardial reperfusion injury: a n overview. Cardio\usc Drugs 7her I99 I ;5:249-68.
  3. Fridovich I. The hiology of oxygen radicals. Science McCord JM. Fridovich 1. The biology and pathology of oxygen radicals. Ann lnrern Med 1978;89: 122-7.
  4. Chambers DE. Parks DA. Patterson G. er a/. Xanthine oxidase as a source of free radical damage in myocardial ischaemia. J Mol Cell Cardiol 1985;17: 145-52.
  5. McCord JM. Oxygen-derived free radicals i n post-ischemic tissue injury. N Engl J Med 1985;313:159-63.
  6. McCord JM. Roy RS. Schaffer SW. Free radicals and myocardial ischemia. The role of xanthine oxidase. Adv Mwcardtol 1985; 5: 183-9.
  7. McCord JM. Oxygen-derived radicals: a link between reperfusion injury and inflammation. Fed Pmc 1987;46:2402-6.
  8. Freenian BA. Crapo JD. Biology of disease. Free radicals and tissue injury. Lh I n i c s t 198?;47:4 12-26.
  9. Singal PK. Kapur N. Dhillon KS. Beamish RE. Dhalla NS. Role of free radicals in catecholamine-induced cardiomyopathy. Cun J P h ~h l Pharmucol 1982: Kukreja RC. Kontos HA, Ellis EF. PGH synthase and lipoxygenase generate superoxide in the presence of NADH or NADPH. Circ Res 1986;59:6 12-9.
  10. McCord JM. Oxygen-derived free radicals in postischemic tissue injury. Free Radic Biol Med 1985;312: 159-63.
  11. Granger DN. Rutill G, McCord JM. Superoxide radicals in feline intestinal ischemia. G u . s t r ~~e , i r e r ~) l o ~~ 198 I ;81:22-9.
  12. Duran N. Singlet oxygen in biological processes. In: Adam W. Cilento G. eds. Chemical and hiologicul generution (4 excired .stares. New York: Academic Press. 1982:345.
  13. Jennings RB, Reimer KA. Lethal myocardial ischemic injury. Am J Parhol 198 1;102:2455.
  14. Burton KP. McCord JM. Ghai G. Myocardial alterations due to free-radical generation. Am J Phvsiol 1984;246:H776-83.
  15. Grisham MB. Russell WJ. Roy RS. McCord JM. Reoxygenation injury in the isolated perfused working rat heart: roles of xanthine oxidasc and transferrin. In: Rotilio G, ed. Superoxide and sr~peroxide di.smuru.vr in chemisrry. biolog. and medicine. Amsterdam: Elsevier. 1986571-5.
  16. Grum CM. Gallagher KP. Kirsh MM. Shlafer M. Absence of detectable xanthine oxidase in human myocardium. J Mol Cell Curdiol I YXY;21:263-7.
  17. Al-Khalidi UAS. Chaglssian TH. The species distribution of xanthine oxidase. Biochem J 1965;97:3 18-20,
  18. Eddy U. Stewart JK. Jones HP. Engerson TD. McCord JM. Downey JM. Free radical-producing enzyme. xanthine oxidase, is undetectable in human hearts. Ani J Physiol 1987;22:H709-11.
  19. Yokoyama Y, Beckman JS. Beckman TK. et a/. Circulating xanthine oxidase: potential mediator of ischemic injury. Am J Ph.vsiol 1990;258:G564-70.
  20. Tauber AI. Gabig TG, Babior BM. Evidence for production of oxidizing radicals by the particulate Oi-forming system from neutrophils. Blood 1979;53:666-76.
  21. Bahior BM. The respiratory burst of phagocytes. J Clin Invesr 1984;73:599-601.
  22. Petrone WF, English DK. Wong K. McCord JM. Free radicals and inflammation: suwroxide-dewndent activation of a neutroohil I97X;201 :X75-X0. CiKttlorion I 986:73:5 18-24, 1 Y83;67: 1016-23. chemotactic faccor in plasma. Proc NO// Acad Sci CSA 19XO;77:115943. 32 33 34 35 36 37 38 39 40 41 42 43 44 45 46 47 48 49 50 51 52 53 54 55 56
  23. Mullane KM. Read N. Salmon JA. Moncada S. Role ot' leukocytcs in acute myocardial infarction in anesthetized dogs: relationship to myocardial salvage by anti-inflammatory drugs. J Phurmacol tip Ther 1984;228:5 ICE. Grisham MB. Jefferson MM. Thomas EL. Role of monochloramine in the oxidation ol' erythrocyte hemoglobin by stimulated neutrophils. J Biol Chem 1984:259:6766-72.
  24. Kukreja RC. Okabe E. Schrier GM, Hess ML; Oxygen radical- mediated lipid peroxidation and inhibition of Ca-'-ATPase activity of cardiac sarcoplasmic reticulum. Arch Bioc/refn Biopli,~.~ lYXX;261:447-57.
  25. Rosen H. Klebanoff SJ. Formation of singlet oxygen by the myeloperoxidase-mediated antimicrobial system. J Biol Cliem 1977;252:4803-6,.
  26. Rowe GT. Eaton LR. Hess ML. NeutroDhil-derived. oxygen free radicahediated cardiovascular dysfunchon. J Ma/ Cell-Cardiol 1984;16: 1075-9.
  27. Westlin W. Mullane KM. Alleviation of myocardial stunning by leukocyte and platelet depletion. Circalution 1989;80: 1828-36.
  28. Ley K. Arfors KE. Changes in macromolecular permeability by intravascular generation of oxygcn-derived free radicals. Micrnvasc Res 1982;24:25-33.
  29. Korthuis RJ. Granger DN. Townsley MI, Taylor AE. The role of oxygen-derived free radicals in ischemia-induced increases in canine skeletal muscle vascular pernieahility. Circ Re.$ I985;57:599-609.
  30. Semb AG. Ytrehus K, Vaage J. Myklcburst R, Mjos OD. Functional impairment in isolated rat hearts induced by activated leukocytes: protective effect of oxygen free radical scavengers. J Mol Cell Curdiol 1989;21:877-87.
  31. Boveris A. Chance B. The mitochondria1 generation of hydrogen peroxide: general properties and effect of hyperbaric oxygen. Binchem J 1973;134:707-16.
  32. Boveris A, Cadenas E. Mitochondrial production of superoxide anion and its relationship to the antimycin-insensitive respiration. FEBS Lptt I975;54:3 1 14. Turrens JF. Boveris A. Generation of superoxide anion by the NADH dehydrogenase of bovine heart mitochondria. Riochem J I980;191:42 1-7.
  33. Karrnazyn M, Moffdt MP. Toxic properties of arachidonic acid on normal. ischemic and reperfused hearts. Indirect evidence for free radical involvement. Prostoglondins hukotricnes Med 1985; 17:251-64.
  34. Duran N. Farias Furtado ST. Faljoni-Alario A. Campa A, Brunet JE. Freer J. Singlet oxygen generation from the peroxidase- catalyzed aerobic oxidation of an activated -CH: substrate. J Phorochem I984;25:285-9.
  35. Seuter F. Fiedler VB, Philipp E. Nafazatroni. In: Scriabine A. ed. New cardinvasc~rrlur drugs. New York: Raven Press, 1986: 163-83.
  36. Fiedler VB, Mardin M. Perzborn E. Gritzmann R. The effects of nafuatrom in an acute occlusion-reperfusion model of canine mvocardial iniurv. Arch Pharrnacd 1985:331:267-74. 17~223-32. 1984; 16:43-52.
  37. Hinderson Ic'. krei E. Adriamycin cardiotoxicity. Am Heart J 1980;99:67 1-8.
  38. Doroshow JH. Effect of anthracycline antibiotics on oxygen radical formation in rat heart. Cancer Res 1983;43:460-72.
  39. Llesuy SF, Milei J, Gonzalez Flecha BS, Boveris A. Myocardial damage induced by doxorubicins: hydroperoxide-initiated chemiluminescence and morphology. Free Radic Biol Med 1990;8:259-64.
  40. Thayer W. Adriamycin stimulated superoxide formation in submitochondrial particles. Chem Biol Interact 1977;19:265-78.
  41. Ditchey RV, LeWinter MM, Higgins CB: Acute effects of doxorubicin (Adriamycin) on left ventricular function in dogs. Int J Cardiol 1989;6:341-50.
  42. Unverferth DV, Leier CV, Balcerzak SP, Hamlin RL. Usefulness of a free radical scavenger in preventing doxorubicin-induced heart failure in dogs. Am J Cardiol 1985;56:157-61.
  43. Lee BH, Goodenday LS, Muswick GJ, Yashoff WA, Leighton RF, Skeel RT. Alterations in left ventricular diastolic function with doxorubicin therapy. J Am Coll Cardiol 1987;9: 184-8.
  44. Singal PK. Subcellular effects of adriamycin in the heart: a concise review. J Mol Cell Cardiol 1987;9:817-28.
  45. Arena E, D'Alessandro N, Dusonchet L, et al. Influence of pharmacokinetic variations on the pharmacologic properties of adriamycin. In: Larter SK, DiMarco A, Ghione M, Krakoff IH, Mathe G , eds. International symposium on Adriamycin. Berlin: Springer-Verlag, l972:9-22.
  46. Lefrak EA, Pitha J. Rosenheim S, Gottlieb J. A clinicopathologic analysis of adriamycin cardiotoxicity. Cancer 1973;32:302-14.
  47. Lee V, Randhawa AK, Singal PK. Adriamycin-induced myocardial dysfunction in vitro is mediated by free radicals. Am J Physiol 68 Ondrias K, Borgatta L, Kim DH, Ehrlich BE. Biphasic effects of doxorubicin on the calcium release channel from sarcoplasmic reticulum of cardiac muscle. Circ Res 1990;67:1167-74.
  48. Roy RS, McCord JM. Superoxide and ischemia: conversion of xanthine dehydrogenase to xanthine oxidase. In: Greenwald R, Cohen G, eds. Oxy radicals and their scavenger systems. Vol 11. New York: Elsevier, 1983:145-53.
  49. Schaffer SW, Roy RS, McCord JM. Possible role for calmodulin in calcium paradox-induced heart failure. Eur Heart J 71 Ganote CE, Nayler WG. Editorial review. Contracture and the calcium paradox. J Mol Cell Cardiol 1985;17:733-45.
  50. Steenbergen C, Murphy E, Watts JA, London RE. Correlation between cytosolic free calcium, contracture, ATP, and irreversible ischemic injury in perfused rat heart. Circ Res 1990;66:13546.
  51. Parr DR, Wimshurst JM, Harris EJ. Calcium-induced damage of rat heart mitochondria. Cardiovasc Res 1975;9:36&72.
  52. Zweier JL, Kuppusamy P, Lutty GA. Measurement of endothelial cell free radical generation: Evidence for a central mechanism of free radical injury in postischemic tissues. Proc Natl Acad Sci USA 1988;85:406&50.
  53. Garlick PB, Davies MJ, Hearse DJ, Slater TF. Direct detection of free radicals in the reperfused rat heart using electron spin resonance spectroscopy. Circ Res 1987;61:757-60.
  54. Blasig IE, Ebert B, Wallukat G, Loewe H. Spin trapping evidence for radical generation by isolated hearts and cultured heart cells. Free Rad Res Commun 1990;6:303-10.
  55. Sekizuka E, Benoit JN, Grisham MB, Granger DN. Dimethylsulfoxide prevents chemoattractant-induced leukocyte adherence. Am J Physiol 1989;256:H5947.
  56. Woodward B, Zakaria MNM. Effects of some free radical scavengers on reperfusion-induced arrhythmias in the isolated rat heart. J Mol Cell Cardiol 1985;17:485-99.
  57. Manning AS, Coltart DJ, Hearse DJ. Ischemia-and reperfusion- induced arrhythmias in the rat: effects of xanthine oxidase inhibition with allopurinol. Circ Res 1984;55:545-50.
  58. Svingen AS, O'Neal FO, Aust SD. The role of superoxide and singlet oxygen in lipid peroxidation. Photochem Photobiol 82 Rao PS, Cohen MV, Mueller HS. Production of free radicals and lipid peroxides in early experimental myocardial ischemia. J Mol Cell Cardiol I983;15:7 13-6.
  59. Nakano M. Noguchi T, Kaneda T. Mechanism of the generation of singlet oxygen in NADPH-dependent microsomal lipid peroxidation. In: Hayaishi 0, Asada K, eds. Biochemical and medical aspects of active oxygen. Tokyo: University of Tokyo Press, 1977:29-42.
  60. Loesser KE, Qian Y-Z, Wei EP, Omarzai RK, Hess ML, Jesse RL, Kukreja RC. In vivo protection of ischemidreperfusion injury by histidine, a singlet oxygen scavenger (abstract). FASEB J 1992;6:A1342.
  61. Boveris A, Cadenas E, Reiter R, Filipowsky M, Nakase Y, Chance B. Organ chemiluminescence: non-invasive assay for oxidative radical reactions. Proc Natl Acad Sci USA 1980;77:347-5 I .
  62. Ferreira R, Burgos M, Llesuy S, e? al. Reduction of reper- 1991 ;261:H989-95. 1984;4(~~ppl):H81-7. 6:2 15-20. 1978;28:803-9. fusion injury with mannitol cardioplegia. Ann Thorac Surg
  63. Kumar C, Okuda M, Ikai I, Chance B. Luminol enhanced chemiluminescence of the perfused rat heart during ischemia and reperfusion. FEES Lett 1990;272: 121-4.
  64. Buttriss JL, Diplock AT. High performance liquid chromatography methods for vitamin E in tissues. In: Methods in enzymology. New York: Academic Press. 1984:13147.
  65. Cadenas E. Oxidative stress and formation of excited species. In: Sie H, ed. Oxidative stress. San Diego: Academic Press, 1985:3 11-30.
  66. Cadenas E, Varsavsky A, Boveris A, Chance B. Oxygen and organic hydroperoxide-induced chemiluminescence of brain and liver homogenate. Biochem J I98 1 ;198:645-54.
  67. Steinbeck MJ, Khan AU, Karnovsky MJ. A chemical trap method that specifically measures intracellular singlet oxygen generation by neutrophils (abstract). FASEB J 1991;5:A599.
  68. Beauchamp C, Fridovich I. A mechanism for the production of ethylene from methionine. The generation of the hydroxyl radical. J Biol Chem 1970;245:4641-6.
  69. Smith LL, Kulig Mj. Singlet molecular oxygen from hydrogen peroxide disproportionation. J Am Chem Soc 1976;98: 1027-9.
  70. Russel GA. Deuterium isotope effects in the autoxidation of aralkyl hydrocarbons. Mechanism of the interaction of peroxy radicals. J Am Chem Soc 1957;79:387 1-5.
  71. Krinksy NI. Biological roles of singlet oxygen. In: Wasserman HH, Murray WA, eds. Singlet oxygen. New York: Academic Press, 1979:597.
  72. Tappel AL. Measurement of and protection from in vivo lipid peroxidation. In: Zimmerman RS, ed. Free radicals in biology. Orlando: Academic Press, 1980: 1-19.
  73. Kellogg EW. Superoxide, hydrogen peroxide and singlet oxygen in lipid peroxidation by a xanthine oxidase system. J Biol Chem 99 Mead JF. Free radical mechanisms in lipid peroxidation and prostaglandin. In: Free radicals in molecular biology and disease. New York: Raven Press, 1984:53-65. 100 Tappel AL. Lipid peroxidation damage to cell components. Fed Proc 1973;32: 1870-4. 101
  74. Kalyanaraman B, Feix JB, Sieber F, Thomas JP, Girotti AW. Photodynamic action of merocyanine 540 on artificial and natural cell membranes: involvement of singlet molecular oxygen. Proc Nut1 Acad Sci USA 1987;84:2999-3003. 102
  75. Wefers H. Singlet oxygen in biological systems. Bioelectrochem Bioenerg 1987;18:9 1-1 04. 103
  76. Wefers H, Schulte-Frohlinde D, Sies H. Loss of transforming activity of plasmid DNA (pBR322) in E coli caused by singlet molecular oxygen. FEES Let? 1987;211:49-52. 104
  77. Peters G, Rodgers AJ. On the feasibility of electron transfer to singlet oxygen from mitochondria1 components. Biochem Biophys Res Commun 1980;96:77&6. 105
  78. Kukreja RC, Weaver AB, Hess ML. Stimulated human neutrophils damage cardiac sarcoplasmic reticulum function by generation of oxidants. Biochim Biophys Acta I989;990: 198-205. 106
  79. Donck LV, Van Reempts J, Vandeplassche G, Borgers M. A new method to study activated oxygen sqecies induced damage in cardiomyocytes and protection by Ca-' antagonists. J Ma1 Cell Cardiol 1988;20:811-23. 107
  80. Hearse DJ, Kusama Y, Bernier M. Rapid electrophysiological changes leading to arrhythmias in the aerobic rat heart: photosensitization studies with rose bengal-derived reactive oxygen intermediates. Circ Res 1989;65: 146-53. 108
  81. Tarr M, Valenzeno DP. Modification of cardiac action potential by photosensitizer-generated reactive oxygen. J Mol Cell Cardiol 1989;21:53943. 109
  82. Vandeplassche G, Bernier M, Kusama BM, Hearse DJ. Singlet oxygen and myocardial injury: ultrastructural. cytochemical and electrocardiographic consequences of photoactivation of rose bengal. J Mol Cell Cardiol 1990;22:287-301. 110
  83. Krause S, Hess ML. Characterization of cardiac sarcoplasmic reticulum dysfunction during short-term, normothermic, global ischemia. Circ Res 1984;55: 176-84. 112
  84. Arora RC, Hess ML. Effect of reduced oxygen intermediates on sarcolemmal muscarinic receptors from canine heart. Biochem Biophys Res Commun 1985;130:133-40. 113
  85. Kramer JH, Mak IT, Weglicki WB. Differential sensitivity of canine cardiac sarcolemmal and microsomal enzymes to inhibition by free radical-induced lipid peroxidation. Circ Res 1984; 55: 120-4. 1989;48:77-84. 1975;250:8812-7. Downloaded from academic.oup.com/cardiovascres/article/26/7/641/265256 by guest on 18 August 2026
  86. I14 Rowe GT, Manson NH, Caplan M, Hess ML. Hydrogen peroxide and hydroxyl radical mediation of activated leukocyte depression of cardiac sarcoplasmic reticulum. Circ Res 1983;53:584-9 1. 115
  87. Kim M-S, Akera T. 0 2 free radicals: cause of ischemia-reperfusion injury to cardiac Na'-Kt-ATPase. Am J Physiol 1987;252:H252-7. 116
  88. Krause SM, Hess ML. The effect of acidosis and short-term normothermic global ischemia on cardiac myofibrillar Ca2'-Mg2' ATPase activity. J Mol Cell Cardiol 1983;17:523-6. 117
  89. Okabe E, Hess ML, Oyama M, Ito H. Characterization of free radical-mediated damage of canine cardiac sarcoplasmic reticulum. Arch Biochem Biophys 1983;225: 164-77. 118
  90. I19 Konno K, Yanagishita T, Geshi E, Katagiri T. Degradation of the cardiac sarcoolasmic reticulum in acute mvocardial ischemia. J m Circ J 1987;51:41l-20. 120
  91. Bolli R. ZhuWei-Xi. Hartlev CJ. et al. Attenuation of dysfunction in the postischemic stunned myocardium by dimethylthiourea. Circulation 1987;76:458-68. 121
  92. Bolli R, Patel BS, Jeroudi MO, Lai EK, McCay PB. Demonstration of free radical generation in stunned myocardium of intact dogs with the use of the sDin traD a-Dhenvl N-tert-butvl . L . nitrone. J C%n Invest 1988;82:47&85. 122
  93. Bolli R. Patel BS. Zhu WX. O'Neill PG. Charlat ML, Roberts R. The iron chelator desfenioxamine attenuates postischemic ventricular dysfunction. Am J Physiol 1987;253:H1372-80. 123
  94. Jolly SR, Kane WJ, Bailie MB, Abrams GD, Lucchesi BR. Canine myocardial reperfusion injury; its reduction by the combined administration of suoeroxide dismutase and catalase. Circ Res 1984;54:277-85. 124
  95. Stewart JR. Blackwell WH. Crute SL. Loughlin V. Greenfield LJ. Inhibition of surgically induced ischemiireperfusion injury by oxygen free radical scavengers. Thorac Cardiovasc Surg 125 Werns SW, Shea MJ, Driscoll EM, et al. The independent effects of oxygen radical scavengers on canine infarct size. Reduction by superoxide dismutase, but not catalase. Circ Res 1985;56:895-8. 126
  96. Przyklenk K, Kloner RA. Superoxide dismutase plus catalase improves contractile function in the canine model of the "stunned myocardium". Circ Res 1986;58: 148-56. 127
  97. Kukreja RC, Kearns AA, Zweier JL, Kuppusamy P, Hess ML. Singlet oxygen interaction with Ca2 -ATPase of cardiac sarcoplasmic reticulum. Circ Res 1991 ;69: 1003-14. 128
  98. Holmberg SRM, Cumming DVE, Kusama Y, et al. Reactive oxygen species modify the structure and function of the cardiac sarcoplasmic reticulum calcium-release channel. Cardioscience 1991 ;2: 19-25. 129
  99. Albrich JM, McCarthy CA, Hurst JK. Biological reactivity of hypochlorous acid: implications for microbicidal mechanisms of leukocyte myeloperoxidase. Proc Nut1 Acad Sci USA 1981; 78:210-4. 130
  100. Garrison WM, Jayko ME, Bennett W. Radiation-induced oxidation of protein in aqueous solution. Radical Res 1962;16:483-502. I3 1 Yamamoto 0. Protein crosslinking: biochemical and molecular aspects. New York: Plenum Press, 1977:509-56. 132
  101. Adams GE, Willson RL, Bisby RH, Cundall RB. On the mechanism of the radiation-induced inactivation of ribonuclease in dilute aqueous solution. In? J Radiat Biol Relat Stud Phys Chem Med 1971;20:405-15. 133
  102. Schuessler H. Schilling K. Oxygen effect in the radiolysis of proteins: part 2. Bovine serum albumin. fnt J Radio? Biol Relat Stud Phys Chem Med 1984;45:267-8 1. 135
  103. Zs-Nagy I, Floyd RA. Hydroxyl free radical reactions with amino acids and proteins studies by electron spin resonance spectroscopy and spin trapping. Biochim Biophys Acta 1984;790:238-50. 136
  104. Gajewski E, Dizdaroglu M, Krutzsch HC, Simic MG. OH-radical induced crosslinks of methionine peptides. Int J Radiat Biol Relat Stud Phys Chem Med 1984;46:47-55. 137
  105. Wolff SP, Gamer A, Dean RT. Free radicals, lipids and protein degradation. Trends Biochem Sci 1986;11:27-3 I. 138
  106. Jorgensen PL. Mechanism of the Na'K' pump. Protein structure and conformations of the Dure (Na+Kt)ATPase. Biochim BioDhvs 1984;86:262-72.
  107. L . . , Acta 1982;694:27-68. 139
  108. Langer GA. Frank JS. Nudd LM. Correlation of calcium exciange, structure, and function in myocardial tissue culture. Am J Physiol 1979;237:H23946. 140
  109. Reeves JP, Sutko JL. Sodium-calcium ion exchange in cardiac membrane vesicles. Proc Natl Acad Sci USA 1979;76:590-.1. 141
  110. Reeves JP, Bailey CA, Hale CC. Redox modification of sodium- calcium exchange activity in cardiac sarcolemal vesicles. J Biol Chem 1986;261:4948-55. 142
  111. Vinnikova AK, Kukreja RC, Keams AA, Hess ML. Singlet oxygen-induced inhibition of isolated cardiac sarcolemmal Na+,K'-ATPase. J Mol Cell Cardiol 1992 (in press). 144
  112. Halliwell B, Gutteridge JMC. Oxygen toxicity, oxygen radicals, transition metals and disease. Biochem J 1984;219: 1-14. 146
  113. Klaasen CD. Heavy metals and heavy metal antagonists. In: Gilman AG, Rall TW, Nies AS, Taylor P, eds. Goodman and Gilman 's Pharmacological basis of therapeutics. New York: Pergamon Press, 1990:1611-2. 147
  114. Myers CL, Weiss SJ. Kirsh MM, Schlafer M. Involvement of hydrogen peroxide and hydroxyl radical in the "oxygen paradox". Reduction of creatine kinase release by catalase, allopurinol or deferoxamine, but not by superoxide disrnutase. J Mol Cell Cardiol 1985;17:675-84. 149
  115. Badylak SF, Simmons A, Turek J, Babbs CF. Protection from reDerfusion iniurv in the isolated rat heart by postischaemic 184:469-72. diferoxamine -aid allopurinol administration. Cardiovasc Res 1987;21:5W. 150
  116. Ambrosio G. Zweier J. Jacobus WE. Weisfeldt ML. Flahertv JT. 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 1987;76:90&15. 151
  117. Maxwell MP, Hearse DJ, Yellon DM. Inability of desferrioxamine to limit tissue injury in the ischemic and reperfused rabbit heart. J Cardiovasc Pharmacol 1989;13:608-15. 154
  118. Pitarys CJ, Virmani R, Vildibill HD, Jackson EK. Forman MB. Reduction of myocardial reperfusion injury by intravenous adenosine administered during the early reperfusion period. Circulation 1991;83:23747. 156
  119. Cronstein BN, Rosenstein ED, Kramer SB, Weissmann G, Hirschhorn R. Adenosine: a physiologic modulator of superoxide anion generation by human neutrophils. J fmmunol 1985; 135: 1366-7 1. 157
  120. Simpson PJ, Todd RF, Fantone JC, Mickelson JK, Greiffin JD, Lucchesi BR. Reduction of experimental canine reperfusion injury by a monoclonal antibody (anti-Mol, anti-CD1 Ib) that inhibits leukocyte adhesion. J Clin Invest 1988;81:624-9. 158
  121. Arfors KE, Lundberg C, Lindbom L, Lundberg K, Beatty PG, Harlan JM. A monoclonal antibody of the membrane glycoprotein complex CDI 8 inhibits polymorphonuclear leukocyte accumu- lation and plasma leakage in vivo. Blood 1987;69:33840. 159
  122. Simpson PJ, Todd RF, Mickelson JK, et al. Sustained limitation of myocardial reperfusion injury by a monoclonal antibody that alters leukocyte function. Circulation 1990;81:226-37. 160
  123. Guarnieri C, Ferrari R, Visioli 0, Caldarera CM, Nayler WG. Effect of a-tocopherol on hypoxic-perfused and reoxygenated rabbit heart muscle. J Mol Cell Cardiol 1978;10:893-906. 161
  124. Janero DR, Burghardt B. Oxidative injury to myocardial membrane: direct modulation by endogenous a-tocopherol. J Mol Cell Cardiol 1989;21:1111-24. 163
  125. Massey KD, Burton KP. a-Tocopherol treatment enhances recovery of isolated hearts made ischemic and reperfused (abstract). FASEE J 1988;2:A823. 165
  126. Kok F, DeBruijn AM, Vermeeren R, Hofman A, VanLaar A. Serum selenium. vitamin antioxidants and cardiovascular mortality: a 86: 10108-1 2. nine-year follow up study in The Netherlands. Am J Clin k r r 1987;45:462-8. Downloaded from academic.oup.com/cardiovascres/article/26/7/641/265256 by guest on 18 August 2026 166
  127. Mak IT. Kramer JH. Freedman AM, Tse SYH, Weglicki WB. Oxygen radical-mediated injury of myocytes -protection by propranolol. J Mol Cell Carcliol 1990;22:687-95. 169
  128. Weglicki WB, Dickens BF, Pflug BR, Maki T. Protective effects of sulfhydryl-containing ACE inhibitors against lipid peroxidation in endothelial and smooth muscle cells (abstract). FASEB J 1989;3:A593. 171
  129. Bagchi D, Prasad R, Das DK. Direct scavenging of free radicals by captopril. an angiotensin converting enzyme inhibitor. Biochem Biophys Res Commun I989;158:52-7. 175
  130. Kukreja RC, Kontos HA, Hess ML. Captopril and enalaprilat do not scavenge the superoxide anion. Am J Cardiol 1990;65:24-7. 176
  131. Sevilla MD, Neta P, Marnett LJ. Reaction of the antithrombotic and antimetastatic agent, nafazatrom, with oxidizing radicals. Biochetn Biophys Res Commun 1983;115:800-6. 177
  132. Honn KV, Dunn JR. Nafazatrom (Bay g 6575) inhibition of tumor cell lipoxygenase activity and cellular proliferation. FEBS Lett 179 Halliwell B. How to characterize a biological antioxidant? Free Radic Res Commun I990;9: 1-32. 180
  133. Warner KG, Khuri SF, Marston W, et al. Significance of the transmural diminution in regional hydrogen ion production after coronary artery occlusions. Circ Res 1989;64:616-28. 183
  134. Murry CE, Richard VJ, Reimer KA, Jennings RB. Ischemic preconditioning slows energy metabolism and delays ultrastructural damage during a sustained ischemic episode. Circ 1988;48: 1226-32. 1988;63:262-6. 69:1207-11. I982;139:65-8.
  135. R ~. s I990;66:9 13-3 1. I84 Reimer KA, Murry CE, Yamasawa 1. Hill ML, Jennings RB. Four brief periods of myocardial ischemia cause no cumulative ATP loss or necrosis. Am J Physiol 1986;251:H1306-15. 185
  136. Iwamoto T. Miura T. Adachi T. et a/. Mvocardial infarct size- limiting effect of ischemic preconditioningwas not attenuated by oxygen free-radical scavengers in the rabbit. Circulation 199 I;83: 101 5-22. 187
  137. Liu GS, Thornton J, Van Winkle DM, Stanley AWH, Olsson RA. Downey JM. Protection against infarction afforded hy preconditioning is mediated by AI adenosine receptors in rabbit heart. Circulation 1991 ;84:350-6. 188
  138. Miller WL, Belardinelli L, Bacchus A. Foley KH, Rubio R, Berne RM. Canine myocardial adenosine and lactate production, oxygen consumption, and coronary blood flow during stellate ganglia stimulation. Circ Res 1979;45:708-18. 189 Editorial. Stress proteins and myocardial protection. Lancet 199 I ;337:27 1. 190
  139. Lindquist S, Craig EA. The heat shock proteins. Annu Rev Genet 191 Currie RW. Effects of ischemia and perfusion temperature on the synthesis of stress induced (heat shock) proteins in isnlated and perfused hearts. J Mol Cell Cardiol 1987;19:795-808.
  140. I92 Howard G , Geoghegan TE. Altered cardiac tissue gene expression during acute hypoxic exposure. Mol Cell Biol 1986;69: 155-60. 193
  141. Low I, Friedrich T, Schoeppe W. Synthesis of shock proteins in cultured fetal mouse myocardial cells. Exp Cell Res 194 Delcayre C, Samuel JL, Marrothe F, Mescadier JJ, Rappaport L. Synthesis of stress proteins in rat cardiac myocytes 2-4 days after imposition of hemodynamic overload. J Clin Invest 1988; 82:460-8. 195 Pelham HRB. Speculation on the functions of the major heat shock and glucose related proteins. Cell 1986;46:959-61. 196
  142. Currie RW, Karmazyn M, Kloc M, Maller K. Heat-shock response is associated with enhanced postischemic ventricular recovery. Circ Res 1988;63:543-9. 197
  143. Mehta HB, Popovich BK, Dillman WH. Ischemia induces changes in the level of mRNA's coding for stress protein 71 and creatine kinase. Circ Res 1988;63:512-7. 198
  144. Yellon DM, Latchman DS. Stress proteins and myocardial protection. J Mol Cell Cardiol 1992;24:113-24.. 199
  145. Karmazyn M, Mailer K, Currie RW. Acquisition and decay of heat-shock enhanced postischemic ventricular recovery. Am J Physiol 1990;259:H424-3 I. 200
  146. Thornton J, Striplin S, Liu G , et ctl. Inhibition of protein synthesis does not block myocardial protection afforded by preconditioning. Am J Physiol 1990;259:H1822-5. 201
  147. Bolli R. Superoxide dismutase 10 years later: a drug in search of a use. JAm Coll Cardiol 1991;18:231-3. 202
  148. Stadtman ER, Berlett BS. Fenton chemistry. Amino acid oxidation. J Biol Chem 1991;266:17201-11. 1988;22:63 1-7. 1989;180:45 1-9. Downloaded from academic.oup.com/cardiovascres/article/26/7/641/265256 by guest on 18 August 2026

Cited by

Sorted by citations

Related

Authors
Kukreja, R. C., & Hess, M. L.
Affiliations
Virginia Commonwealth University (US)
Corresponding author
Kukreja, R. C
Venue
Cardiovascular Research
Publisher
Oxford University Press (OUP)
Published
1992-07-01
Volume
26
Issue
7
Pages
641-655
ISSN
0008-6363 (ISSN-L)
DOI
10.1093/cvr/26.7.641
OpenAlex
W2069563551
Cited by
396
References
0
Citations by year
2026: 1 · 2025: 1 · 2024: 3 · 2023: 6 · 2022: 4 · 2021: 7 · 2020: 11 · 2019: 1 · 2018: 4 · 2017: 9 · 2016: 7 · 2015: 6 · 2014: 13 · 2013: 7 · 2012: 13
FWCI
5.27
Type
journal article
Language
en
Open access
Locations
  • Cardiovascular Research (publishedVersion)
  • PubMed (publishedVersion)
Topics
  • Health Sciences › Medicine › Pathology and Forensic Medicine › Cardiac Ischemia and Reperfusion
  • Health Sciences › Medicine › Physiology › Nitric Oxide and Endothelin Effects
  • Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Redox biology and oxidative stress
Keywords
oxygen free radicals, reactive oxygen species, ischemia-reperfusion injury, singlet oxygen, superoxide, hydrogen peroxide, hydroxyl radicals, membrane protein interactions, myocardial injury, cardiac dysfunction, cardioprotection, inflammation
MeSH terms
Antioxidants, Cell Membrane, Free Radicals, Histidine, Humans, Membrane Proteins, Oxygen, Myocardial Reperfusion Injury

About these checks

Registry, retraction, Cites and statistics results are computed, not judged, with one exception: a printed reference that no index lists is read once by a model before it counts as a citation error. Claims are extracted by a model and kept only when their quote appears verbatim in the text; each cited source is then checked, with a model’s help, for whether it says what the claim relies on. Those verdicts can be wrong — read the claim’s quote and the cited source before relying on one.

Statistics and arithmetic are recomputed, not judged.

Confidence bands are shown only for fields calibrated on our annotated test set. None is calibrated yet, so no band is shown.

What counts as a claim ›How we measure confidence ›How we check this ›

Are you an author, or do you see a problem with this page? Request a review