Oxidative stress in hepatic Ischemia-reperfusion injury: The role of antioxidants and iron chelating compounds

Current Pharmaceutical Design

Volumn 12, Issue 23, 2006, Pages 2875-2890

  Galaris, D ^a   Barbouti, A ^a   Korantzopoulos, P ^b  

^a UNIVERSITY OF IOANNINA   (Greece)

^b G HATZIKOSTA GENERAL HOSPITAL   (Greece)

Author keywords

Antioxidants; Iron chelators; Ischemia reperfusion; Liver; Oxidative stress; Preconditioning; Reactive oxygen species

Indexed keywords

ALPHA TOCOPHEROL; ANTIOXIDANT; ASCORBIC ACID; CATALASE; COPPER ZINC SUPEROXIDE DISMUTASE; CYANIDIN 3 GLUCOSIDE; DNA; GLUTATHIONE PEROXIDASE; HYDROGEN PEROXIDE; HYDROXYL RADICAL; IDEBENONE; IMMUNOGLOBULIN ENHANCER BINDING PROTEIN; IRON CHELATING AGENT; KUTKIN; MELATONIN; NORPHENAZONE; PR 39; QUERCETIN; RAC1 PROTEIN; REACTIVE OXYGEN METABOLITE; REDUCED NICOTINAMIDE ADENINE DINUCLEOTIDE PHOSPHATE OXIDASE; SUPEROXIDE; SUPEROXIDE DISMUTASE; TEMPOL; THIOL GROUP; THIONEINE; TRANSCRIPTION FACTOR AP 1; TRANSITION ELEMENT; UNINDEXED DRUG; XANTHINE OXIDASE;

BIOCHEMISTRY; CELL DAMAGE; CLINICAL TRIAL; DNA DAMAGE; HUMAN; ISCHEMIC PRECONDITIONING; KUPFFER CELL; LIVER ISCHEMIA; LIVER PROTECTION; MITOCHONDRION; NEUTROPHIL; NONHUMAN; OXIDATIVE STRESS; PHENOMENOLOGY; PRIORITY JOURNAL; REPERFUSION INJURY; REVIEW; SIGNAL TRANSDUCTION; TISSUE INJURY;

ANIMALS; ANTIOXIDANTS; HUMANS; IRON CHELATING AGENTS; LIVER; LIVER DISEASES; OXIDATIVE STRESS; REACTIVE OXYGEN SPECIES; REPERFUSION INJURY;

EID: 33746921195     PISSN: 13816128     EISSN: None     Source Type: Journal    
DOI: 10.2174/138161206777947614     Document Type: Review

References (182)

1. Selzner N, Rudiger H, Graf R, Clavien PA. Protective strategies against ischemic injury of the liver. Gastrenterology 2003; 125: 917-36.
2. Jaeschke H. Molecular mechanisms of hepatic ischemia-reperfusion injury and preconditioning. Am J Physiol Gastrointest Liver Physiol 2003; 284: G15-26.
3. Wang Q-D, Pernow J, Sjoquist P-O, Ryden L. Pharmacological possibilities for protection against myocardial reperfusion injury. Cardiov Res 2002; 55: 25-37.
4. McCord JM. Oxygen-derived free radicals in postischemic tissue injury. N Engl J Med 1985; 312: 159-63.
5. Becker LB. New concepts in reactive oxygen species and cardiovascular reperfusion physiology. Cardiov Res 2004; 61: 461-70.
6. Hess ML, Mason NH. Molecular oxygen: friend and foe. The role of the oxygen free radical system in the calcium paradox, the oxygen paradox and ischemia/reperfusion injury. J Mol Cell Cardiol 1984; 16: 969-85.
7. Toledo-Pereyra LH, Simmons RL, Najarian JS. Protection of the ischemic liver by donor pre-treatment before transplantation. Am J Surg 1975; 129: 523-7.
8. Teoh NC, Farrell GC. Hepatic ischemia reperfusion injury: pathogenic mechanisms and basis for hepatoprotection. J Gastroenterol Hepatol 2003; 18: 891-902.
9. Glantzounis GK, Tselepis AD, Tambaki AP, Trikalinos TA, Manataki AD, Galaris DA, et al. Laparoscopic surgery-induced changes in oxidative stress markers in human plasma. Surg Endosc 2001; 15: 1315-9.
10. Koti RS, Seifalian AM, Davidson HR. Protection of the liver by ischemic preconditioning: a review of mechanisms and clinical applications. Dig Surg 2003; 20: 383-96.
11. Mitrogianni Z, Barbouti A, Galaris D, Siamopoulos K. Tyrosine nitration in plasma proteins from patients undergoing hemodialysis. Am J Kidney Dis 2004; 44: 286-92.
12. Ischiropoulos H. Biological selectivity and functional aspects of protein tyrosine nitration. Biochem Biophys Res Commun 2003; 305: 776-83.
13. Doulias P-T, Barbouti A, Galaris D, Ishiropoulos H. SIN-1-induced DNA damage in isolated human peripheral blood lymphocytes as assessed by single cell gel electrophoresis (comet assay). Free Radic Biol Med 2001; 30: 679-85.
14. Chance B, Sies H, Boveris A. Hydroperoxide metabolism in mammalian organs. Physiol Rev 1979; 59: 527-605.
15. Antunes F, Cadenas E. Estimation of H2O2 gradients across biomembranes. FEBS Lett 2000; 475: 121-6.
16. Sies H. Oxidative stress: introductory remarks. In, Sies H Ed, Oxidative stress. Orlando, Florida. Academic Press. 1985; 1-7.
17. Davies KJ. The broad spectrum of responses to oxidants in proliferating cells: a new paradigm for oxidative stress. IUBMB Life 1999; 48: 41-7.
18. Poli G, Leonarduzzi G, Biasi F, Chiarpotto E. Oxidative stress and cell signalling. Curr Med Chem 2004; 11: 1163-82.
19. Pantopoulos K. Iron metabolism and the IRE/IRP regulatory system: an update. Ann N Y Acad Sci 2004; 1012: 1-13.
20. Epsztejn S, Kakhlon O, Glickstein H, Breuer W, Cabantchik I. Fluorescence analysis of the labile iron pool of mammalian cells. Anal Biochem 1997; 248: 31-40.
21. Esposito BP, Epsztejn S, Breuer W, Cabantchik ZI. A review of fluorescence methods for assessing labile iron in cells and biological fluids. Anal Biochem 2002; 304: 1-18.
22. Zhengquan Y, Persson H, Eaton J, Brunk U. Intralysosomal iron: A major determinant of oxidant-induced cell death. Free Radic Biol Med 2003; 34: 1243-52.
23. Ollinger K, Brunk UT. Cellular injury induced by oxidative stress is mediated through lysosomal damage. Free Radic Biol Med 1995; 19: 565-74.
24. Galaris D, Evangelou A. The role of oxidative stress in mechanisms of metal-induced carcinogenesis. Crit Rev Oncol Heamatol 2002; 42: 93-103.
25. Barbouti A, Doulias PT, Zhu BZ, Frei B, Galaris D. Intracellular iron, but not copper, plays a critical role in hydrogen peroxide-induced DNA damage. Free Radic Biol Med 2001; 31: 490-8.
26. Halliwell B, Aruoma O. DNA damage by oxygen-derived species: Its mechanism and measurement in mammalian systems. FEBS Lett 1991; 281: 9-19.
27. Tenopoulou M, Doulias P-T, Barbouti A, Brunk Ulf, Galaris D. The role of compartmentalized redox-active iron on hydrogen peroxide-induced DNA damage and apoptosis. Biochem J 2005; 387: 701-10.
28. Kurz T, Leake A, Zglinicki T, Brunk U. Relocalized redox-active iron is an important mediator of oxidative-stress-induced DNA damage. Biochem J 2004; 378: 1039-45.
29. Doulias PT, Christoforidis S, Brunk UT, Galaris D. Endosomal and lysosomal effects of desferrioxamine: protection of HeLa cells from hydrogen peroxide-induced DNA damage and induction of cell-cycle arrest. Free Radic Biol Med 2003; 35: 719-28.
30. Persson HL, Yu Z, Tirosh O, Eaton JW, Brunk UT. Prevention of oxidant-induced cell death by lysosomotropic iron chelators. Free Radic Biol Med 2003; 34: 1295-305.
31. 2. Arch Biochem Biophys 1988; 262: 221-31.
32. Galaris D, Korantzopoulos P. On the molecular mechanism of metmyoglobin-catalyzed reduction of hydrogen peroxide by ascorbate. Free Radic Biol Med 1997; 22: 657-67.
33. Galaris D, Cadenas E, Hochstein P. Glutathione-dependent reduction of peroxides during ferryl- and met-myoglobin interconversion: a potential protective mechanism in muscle. Free Radic Biol Med 1989; 6: 473-8.
34. Galaris D, Cadenas E, Hochstein P. Redox cycling of myoglobin and ascorbate: a potential protective mechanism against oxidative reperfusion injury in muscle. Arch Biochem Biophys 1989; 273: 497-504.
35. Galaris D, Eddy L, Arduini A, Cadenas E, Hochstein P. Mechanisms of reoxygenation injury in myocardial infarction: implications of a myoglobin redox cycle. Biochem Biophys Res Commun 1989; 160: 1162-8.
36. Galaris D, Sevanian A, Cadenas E, Hochstein P. Ferrylmyoglobin-catalyzed linoleic acid peroxidation. Arch Biochem Biophys 1990; 281: 163-9.
37. Wiese AG, Pacifici RE, Davies KJ. Transient adaptation of oxidative stress in mammalian cells. Arch Biochem Biophys 1995; 318: 231-40.
38. Davies KJ. Oxidative stress, antioxidant defenses, and damage removal, repair, and replacement systems. IUBMB Life 2000; 50: 279-89.
39. Togashi H, Shinzawa H, Matsuo T, Takeda Y, Takahashi T, Aoyama M, et al. Analysis of oxidative stress status by electron spin resonance spectroscopy and imaging. Free Radic Biol Med 2000; 28: 846-53.
40. Togashi H, Shinzawa H, Yong H, Takahashi T, Noda H, Oikawa K, et al. Ascorbic acid radical, superoxide, and hydroxyl radical are detected in reperfusion injury of rat liver using electron spin resonance spectroscopy. Arch Biochem Biophys 1994; 308: 1-7.
41. Burke A, FitzGerald GA, Lucey MR. A prospective analysis of oxidative stress and liver transplantation. Transplantation 2002; 74: 217-21.
42. Biasi F, Bosco M, Chiappino I, Chiarpotto E, Lanfranco G, Ottobrelli A, et al. Oxidative damage in human liver transplantation. Free Radic Biol Med 1995; 19: 311-7.
43. Togashi H, Shinzawa H, Matsuo T, Takeda Y, Takahashi T, Aoyama M, et al. Analysis of hepatic oxidative stress status by electron spin resonance spectroscopy and imaging. Free Radic Biol Med 2000; 28: 846-53.
44. Zweier JL, Flaherty JT, Weisfeldt ML. Direct measurement of free radical generation following reperfusion of ischemic myocardium. Proc Natl Acad Sci USA 1987; 84: 1404-7.
45. Ambrosio G, Zweier JL, Flaherty JT. The relationship between oxygen radical generation and impairment of myocardial energy metabolism following post-ischemic reperfusion. J Mol Cell Cardiol 1991; 23: 1359-74.
46. 2 radicals in intact hearts with ischemia and reperfusion. Am J Physiol Heart Circ Physiol 2003; 284: H566-74.
47. Becker LB, vanden Hoek TL, Shao ZH, Li CQ, Schumacker PT. Generation of superoxide in cardiomyocytes during ischemia before reperfusion. Am J Physiol 1999; 277: H2240-6.
48. - release as a by-product of respiration. Free Radic Res Commun 1993; 18: 127-37.
49. Zorov DB, Filburn CR, Klotz LO, Zweier JL, Sollott SJ. Reactive oxygen species (ROS)-induced ROS release: a new phenomenon accompanying induction of the mitochondrial permeability transition in cardiac myocytes. J Exp Med 2000; 192: 1001-14.
50. Fan C, Zwacka RM, Engelhardt JF. Therapeutic approaches for ischemia/ reperfusion injury. J Mol Med 1999; 77: 577-92.
51. Higucgi M, Aggarwal BB, Yet ET. Activation of CPP32-like protease in tumor necrosis factor-induced apoptosis is dependent on mitochondrial function. J Clin Invest 1997; 99: 1751-8.
52. Quillet-Mary A, Jaffrezou JP, Mansat V, Bordier C, Naval J, Laurent G. Implication of mitochondrial hydrogen peroxide generation in ceramide-induced apoptosis. J Biol Chem 1997; 272: 21388-95.
53. Li JM, Shah AM. Differential NADPH- versus NADH-dependent superoxide production by phagocyte-type endothelial cell NADPH oxidase. Cardiovasc Res 2001; 52: 477-86.
54. Ozaki M, Deshpande SS, Angkeow P, Bellan J, Lowenstein CJ, Dinauer MC, et al. Inhibition of the Rac1 GTPase protects against non-lethal ischemic/reperfusion-induced necrosis and apoptosis in vivo. FASEB J 2000; 14: 418-29.
55. Harada H, Hines IN, Flores S, Gao B, McCord J, Scheerens H, et al. Role of NADPH oxidase-derived superoxide in reduced size liver ischemia and reperfusion injury. Arch Biochem Biophys 2004; 423: 103-8.
56. Hines IN, Hoffman JM, Scheerens H, Day BJ, Harada H, Pavlick KP, et al. Regulation of postischemic liver injury following different durations of ischemia. Am J Physiol Gastrointest Liver Physiol 2003; 284: G536-45.
57. Zulueta JJ, Sawhney R, Yu FS, Cote CC, Hassoun PM. Intracellular generation of reactive oxygen species in endothelial cells exposed to anoxia-reoxygenation. Am J Physiol 1997; 272: L897-902.
58. Rupin A, Paysant J, Sansilvestri-Morel P, Lembrez N, Lacoste JM, Cordi A, et al. Role of NADPH oxidase-mediated superoxide production in the regulation of E-selectin expression by endothelial cells subjected to anoxia/reoxygenation. Cardiovasc Res 2004; 63: 323-30.
59. Jaeschke H, Farhood A, Bautista AP. Complement activates Kupffer cells and neutrophils during reperfusion after hepatic ischemia. Am J Physiol 1993; 264: G801-9.
60. 2-released by activated Kuppfer cells upon hypoxia-reoxygenation. Am J Physiol Gastrointest Liver Physiol 1991; 261: G602-7.
61. Bilzer M, Jaeschke H, Vollmar AM, Paumgartner G, Gerbes AL. Prevention of Kuppfer cell-induced injury in rat liver by atrial natriuretic peptide (ANP): A novel endogenous defense mechanism against oxidant injury. Am J Physiol Gastrointest Liver Physiol 1999; 276: G1137-44.
62. Jaeschke H, Farhood A. Neutrophil and Kupffer cell-induced oxidant stress and ischemia-reperfusion injury in rat lever. Am J Physiol 1991; 260: G355-62.
63. Serracino-Inglott F, Habib NA, Mathie RT. Hepatic ischemia-reperfusion injury. Am J Surg; 2001; 181: 160-6.
64. Cutrin JC, Boveris A, Zingaro B, Corvetti G, Poli G. In situ determination by surface chemiluminescence of temporal relationships between evolving warm ischemia-reperfusion injury in rat liver and phagocyte activation and recruitment. Hepatology 2000; 31: 622-32.
65. Martinez-Mier G, Toledo-Pereyra LH, McDuffie E, Warner RL, Ward PA. L-Selectin and chemokine response after liver ischemia and reperfusion. J Surg Res 2000; 93: 156-62.
66. Fernandez L, Heredia N, Grande L, Gomez G, Rimola A, Marco A, et al. Preconditioning protects liver and lung damage in rat liver transplantation: role of xanthine/xanthine oxidase. Hepatology 2002; 36: 562-72.
67. Jaeschke H. Xanthine oxidase-induced oxidant stress during hepatic ischemia-reperfusion: Are we caming full circle after 20 years? Hepatology 2002; 36: 761-3.
68. Harris CM, Massey V. The oxidative half-reaction of xanthine oxidoreductase with NAD: reaction kinetics and steady state mechanisms. J Biol Chem 1997; 272: 28335-41.
69. Vega VL, Mardones L, Maldonado M, Nicovani S, Manriquez V, Roa J, et al. Xanthine oxidase released from reperfused hind limbs mediate kupffer cell activation, neutrophil sequestration, and hepatic oxidative stress in rats subjected to tourniquet shock. Shock 2000; 14:565-71.
70. Zwacka RM, Zhang Y, Zhou W, Halldorson J, Engelhardt JF. Ischemia/ reperfusion injury in the liver of BALB/c mice activates AP-1 and nuclear factor kappaB independently of IkappaB degradation. Hepatology 1998; 28: 1022-30.
71. Bradham CA, Stachlewitz RF, Gao W, Qian T, Jayadev S, Jenkins G, et al. Reperfusion after liver transplantation in rats differentially activates the mitogen activated protein kinases. Hepatology 1997; 25: 1128-35.
72. Schreck R, Meier B, Mannel DN, Droge W, Baeuerly PA. Dithiocarbamates as potent inhibitors of nuclear factor kappa B activation in intact cells. J Exp Med 1992; 175: 1181-94.
73. Denu JM, Tanner KG. Specific and reversible inactivation of protein tyrosine phosphatases by hydrogen peroxide: evidence for a sulphenic acid intermediate and implications for redox regulation. Biochemistry 1998; 37: 5633-42.
74. Karin M, Liu Z, Zandi E. AP-1 function and regulation. Curr Opin Cell Biol 1997; 9: 940-6.
75. Mechta-Grigoriou F, Gerard D, Yaniv M. The mammalian Jun proteins: redundancy and specificity. Oncogen 2001; 20: 2378-89.
76. Xu S, Cobb MH. MEKK1 binds directly to the c-Jun N-terminal kinases/ stress activated protein kinases. J Biol Chem 1997; 272: 32056-60.
77. Pfarr CM, Mechta F, Spyrou G, Lallemand D, Carillo S, Yaniv M. Mouse JunD negatively regulates fibroblast growth and antagonizes transformation in rats. Cell 1994; 76: 747-60.
78. Gerard D, Berra E, Frapart YM, Chan DA, Giaccia AJ, Mansuy D, et al. JunD reduces tumor angiogenesis by protecting cells from oxidative stress. Cell 2004; 118: 781-94.
79. Mallick IH, Yang W, Winslet MC, Seifalian AM. Ischemia-reperfusion injury of the intestine and protective strategies against injury. Dig Dis Sci 2004; 49: 1359-77.
80. Zhang SJ, Chen S. The role of ischemic preconditioning in rat liver graft. Transplant Proc 2004; 36: 1970-2.
81. Carini R, Albano E. Recent insights on the mechanisms of liver preconditioning. Gastroenterology 2003; 125: 1480-91.
82. Cavalieri B, Perrelli MG, Aragno M, Mastrocola R, Corvetti G, Durazzo M, et al. Ischemic preconditioning attenuates the oxidant-dependent mechanisms of reperfusion cell damage and death in rat liver. Liver Transpl 2002; 8: 990-9.
83. Rudiger HA, Graf R, Clavien PA. Sublethal oxidative stress triggers the protective effects of ischemic preconditioning in the mouse liver. J Hepatol 2003; 39: 672-7.
84. Jaeschke H. Role of reactive oxygen species in hepatic ischemia-reperfusion injury and preconditioning. J Invest Surg 2003; 16: 127-40.
85. Sindram D, Rudiger HA, Upadhya AG, Strasberg SM, Clavien PA. Ischemic preconditioning protects against cold ischemic injury through an oxidative stress dependent mechanism. J Hepatol 2002; 36: 78-84.
86. Cutrn JC, Perrelli MG, Cavalieri B, Peralta C, Rosello-Catafau J, Poli G. Microvascular dysfunction induced by reperfusion injury and protective effect of ischemic preconditioning. Free Radic Biol Med 2002; 33: 1200-8.
87. Tejima K, Arai M, Ikeda H, Tomiya T, Yanase M, Inoue Y, et al. Ischemic preconditioning protects hepatocytes via reactive oxygen species derived from Kupffer cells in rats. Gastroenterology 2004: 127: 1488-96.
88. Schauer RJ, Gerbes AL, Vonier D, op den Winkel M, Fraunberger P, Bilzer M. Induction of cellular resistance against Kupffer cell-derived oxidant stress: a novel concept of hepatoprotection by ischemic preconditioning. Hepatology 2003; 37: 286-95.
89. Sharma A, Singh M. Protein kinase C activation and cardioprotective effect of preconditioning with oxidative stress in isolated rat heart. Mol Cell Biochem 2001; 219: 1-6.
90. Yaguchi Y, Satoh H, Wakahara N, Katoh H, Uehara A, Terada H, et al. Protective effects of hydrogen peroxide against ischemia/reperfusion injury in perfused rat hearts. Circ J 2003; 67: 253-8.
91. Bajgar R, Seetharaman S, Kowaltowski AJ, Garlid KD, Paucek P. Identification and properties of a novel intracellular (mitochondrial) ATP-sensitive potassium channel in brain. J Biol Chem 2001; 276: 33369-74.
92. Lebaffe G, Schumacker PT, Shao ZH, Anderson T, Iwase H, Vanden Hoek TL. ROS and NO trigger early preconditioning: relationship to mitochondrial K+-ATP channel. Am. J. Physiol. Heart Circ. Physiol. 2003; 284: H299-308.
93. Yadav SS, Sindram D, Perry DK, Clavien PA. Ischemic preconditioning protects the mouse liver by inhibition of apoptosis through a caspase-dependent pathway. Hepatology 1999; 30: 1223-31
94. 2. Free Radic Biol Med 2002; 33: 691-702.
95. Suzuki M, Takeuchi H, Kakita T, Unno M, Katayose Y, Matsuno S. The involvement of the intracellular superoxide production system in hepatic ischemia-reperfusion injury. In vivo and in vitro experiments using transgenic mice manifesting excessive CuZn-SOD activity. Free Radic Biol Med 2000; 29: 756-63.
96. Lehmann TG, Wheeler MD, Schoonhoven R, Bunzendahl H, Samulski RJ, Thurman RG. Delivery of Cu/Zn-superoxide dismutase genes with a viral vector minimizes liver injury and improves survival after liver transplantation in the rat. Transplantation 2000; 69: 1051-7.
97. Zwacka RM, Zhou W, Zhang Y, Darby CJ, Dudus L, Halldorson J, et al. Redox gene therapy for ischemia/reperfusion injury of the liver reduces AP1 and NF-kappaB activation. Nat Med 1998; 4: 698-704.
98. Hines IN, Harada H, Wolf R, Grisham MB. Superoxide and post-ischemic liver injury: potential therapeutic target for liver transplantation. Curr Med Chem 2003; 10: 2661-7.
99. Wheeler M, Katuna M, Smutney O, Froh M, Dikalova A, Mason R et al. Comparison of the effect of adenoviral delivery of three superoxide dismutase genes against hepatic ischemia-reperfusion injury. Hum Gene Ther 2001; 12: 2167-77.
100. Lehmann TG, Wheeler MD, Froh M, Schwabe RF, Bunzendahl H, Samulski RJ, et al. Effects of three superoxide dismutase genes delivered with an adenovirus on graft function after transplantation of fatty livers in the rat. Transplantation 2003; 76: 28-37.
101. Froh M, Wheeler MD, Smutney O, Zhong Z, Bradford BU, Thurman RG. New method of delivering gene-altered Kupffer cells to rat liver: studies in an ischemia-reperfusion model. Gastroenterology 2003; 124: 172-83.
102. Zhou W, Zhang Y, Hosch MS, Lang A, Zwacka RM, Engelhardt JF. Subcellular site of superoxide dismutase expression differentially controls AP-1 activity and injury in mouse liver following ischemia/reperfusion. Hepatology 2001; 33: 902-14.
103. Nguyen WD, Kim DH, Alam HB, Provido HS, Kirkpatrick JR. Polyethylene glycol-superoxide dismutase inhibits lipid peroxidation in hepatic ischemia/reperfusion injury. Crit Care 1999; 3: 127-30.
104. Fujita T, Furitsu H, Nishikawa M, Takakura Y, Sezaki H, Hashida M. Therapeutic effects of superoxide dismutase derivatives modified with mono- or polysaccharides on hepatic injury induced by ischemia/ reperfusion. Biochem Biophys Res Common 1992; 189: 191-6.
105. Yabe Y, Nishikawa M, Tamada A, Takakura Y, Hashida M.J. Targeted delivery and improved therapeutic potential of catalase by chemical modification: combination with superoxide dismutase derivatives. Pharmacol Exp Ther 1999; 289: 1176-84.
106. Mun KC, Lee HG, Lee TH, Kim YH, Kwak CS, Kim SP, et al. Effect of modified polyhemoglobin on the ischemia/reperfusion injury in kidney. Transplant Proc 2003; 35: 99-100.
107. Chang EJ, Lee SH, Mun KC, Suh SI, Bae JH, Kim SP, et al. Effect of artificial cells on hepatic function after ischemia-reperfusion injury in liver. Transplant Proc 2004; 36: 1959-61.
108. Salvemini D, Wang ZQ, Zweier JL, Samouilov A, Macarthur H, Misko TP, et al. A nonpeptidyl mimic of superoxide dismutase with therapeutic activity in rats. Science 1999; 286: 304-6.
109. Yabe Y, Koyama Y, Nishikawa M, Takakura Y, Hashida M. Hepatocyte-specific distribution of catalase and its inhibitory effect on hepatic ischemia/reperfusion injury in mice. Free Radic Res 1999; 30: 265-74.
110. Yabe Y, Nishikawa M, Tamada A, Takakura Y, Hashida M. Targeted delivery and improved therapeutic potential of catalase by chemical modification: combination with superoxide dismutase derivatives. J Pharmacol Exp Ther 1999; 289: 1176-84.
111. Jaeschke H, Ho YS, Fisher MA, Lawson JA, Farhood A. Glutathione peroxidase deficient mice are more susceptible to neutrophil-mediated hepatic parechymal cell injury during endotoxemia: importance of an intracellular oxidant stress. Hepatology 1999; 29: 443-50.
112. Halliwell B, Gutteridge JMC, Eds. Free radicals in biology and medicine. 3rd edition. Oxford, Oxford University Press 1999. University Press
113. Bartels M, Biesalski HK, Engelhart K, Sendlhofer G, Rehak P, Nagel E. Pilot study on the effect of parenteral vitamin E on ischemia and reperfusion induced liver injury: a double blind, randomized, placebo-controlled trial. Clin Nutr 2004; 23: 1360-70.
114. Soltys K, Dikdan G, Koneru B. Oxidative stress in fatty livers of obese Zucker rats: rapid amelioration and improved tolerance to warm ischemia with tocopherol. Hepatology 2001; 34: 13-8.
115. Giakoustidis D, Kontos N, Iliadis S, Papageorgiou G, Tsantilas D, Spyridis C, et al. Severe total hepatic ischemia and reperfusion: relationship between very high alpha-tocopherol uptake and lipid peroxidation. Free Radic Res 2001; 35: 103-9.
116. Eum HA, Lee SH, Lee SM. Trolox C ameliorates hepatic drug metabolizing dysfunction after ischemia/reperfusion. Arch Pharm Res 2002; 25: 940-5.
117. Azzi A, Gysin R, Kempna P, Munteanu A, Villacorta L, Visarius T, et al. Regulation of gene expression by alpha-tocopherol. Biol Chem 2004; 385: 585-91.
118. Frei B, England L, Ames BN. Ascorbate is an outstanding antioxidant in human blood plasma. Proc Natl Acad Sci USA 1989; 86: 6377-81.
119. Arroyo A, Rodriguez-Aguilera JC, Santos-Ocana C, Villalba JM, Navas P. Stabilization of extracellular ascorbate mediated by coenzyme Q transmembrane electron transport. Methods Enzymol 2004; 378: 207-17.
120. Seo MY, Lee SM. Protective effect of low dose of ascorbic acid on hepatobiliary function in hepatic ischemia/reperfusion in rats. J Hepatol 2002; 36: 72-7.
121. Ozaki M, Fuchinoue S, Teraoka S, Ota K. The in vivo cytoprotection of ascorbic acid against ischemia/reoxygenation injury of rat liver. Arch Biochem Biophys 1995; 318: 439-45.
122. Taha MO, Souza HS, Carvalho CA, Fagundes DJ, Simões MJ, Novo NF, et al. Cytoprotective effects of ascorbic acid on the ischemia-reperfusion injury of rat liver. Transplantation Proc 2004; 36: 296-300.
123. Biasi F, Poli G, Salizzoni M, Cerutti E, Battista S, Mengozzi G, et al. Effect of perioperative infusion of antioxidants on neutrophil activation during liver transplantation in humans. Transplant Proc 2002; 34: 755-8.
124. Cerwenka H, Khoschsorur G, Bacher H, Werkgartner G, El-Shabrawi A, Quehenberger F, et al. Normothermic liver ischemia and antioxidant treatment during hepatic resections. Free Radic Res 1999; 30: 463-9.
125. Schauer RJ, Gerbes AL, Vonier D, Meissner H, Michl P, Leiderer R, et al. Glutathione protects the rat liver against reperfusion injury after prolonged warm ischemia. Ann Surg 2004; 239: 220-31.
126. Schauer RJ, Kalmuk S, Gerbes AL, Leiderer R, Meissner H, Schildberg FW, et al. Intravenous administration of glutathione protects parenchymal and non-parenchymal liver cells against reperfusion injury following rat liver transplantation. World J Gastroenterology 2004; 10: 864-70.
127. Glantzounis GK, Yang W, Koti RS, Michailidis DP, Seifalian AM, Davidson BR. Continuous infusion of N-acetylcysteine reduces liver warm ischaemia-reperfusion injury. Br J Surg 2004; 91:1330-9.
128. Sener G, Tosun O, Sehirli AO, Kacmaz A, Arbak S, Ersoy Y, et al. Melatonin and N-acetylcysteine have beneficial effects during hepatic ischemia and reperfusion. Life Sci 2003: 72: 2707-18.
129. Demir S, Inal-Erden M. Pentoxifylline and N-acetylcysteine in hepatic ischemia/reperfusion injury. Clin Chim Acta 1998; 275: 127-35.
130. Weigand MA, Plachky J, Thies JC, Spies-Martin D, Otto G, Martin E, et al. N-Acetylcysteine attenuates the increase in a-glutathione S-transferase and circulating ICAM-1 and VCAM-1 after reperfusion in humans undergoing liver transplantation. Transplantation 2001; 72: 694-698.
131. Horwitz LD. Bucillamine: a potent thiol donor with multiple clinical applications. Cardiovasc Drug Rev 2003; 21: 77-90.
132. Amersi F, Nelson SK, Shen XD, Kato H, Melinek J, Kupiec-Weglinski JW, et al. Bacillamine, a thiol antioxidant, prevents transplantation-associated reperfusion injury. Proc. Natl. Acad. Sci USA 2002; 99: 8915-20.
133. Su JF, Guo CJ, Wei JY, Yang JJ, Jiang YG, Li YF. Protection against hepatic ischemia-reperfusion injury in rats by oral pretreatment with quercetin. Biomed Environ Sci 2003; 16: 1-8.
134. Tsuda T, Horio F, Kitoh J, Osawa T. Protective effects of dietary cyanidin 3-O-beta-D-glucoside on liver ischemia-reperfusion injury in rats. Arch Biochem Biophys 1999; 368: 361-6.
135. Andrabi SA, Sayeed I, Siemen D, Wolf G, Horn TF. Direct inhibition of the mitochondrial permeability transition pore: a possible mechanism responsible for anti-apoptotic effects of melatonin. FASEB J 2004; 18: 869-71.
136. Okatani Y, Wakatsuki A, Reiter RJ, Enzan H, Miyahara Y. Protective effect of melatonin against mitochondrial injury induced by ischemia and reperfusion of rat liver. Eur J Pharmacol 2003; 469: 145-52.
137. Bedirli A, Sakrak O, Muhtaroglu S, Soyuer I, Guler I, Riza Erdogan A, et al. Ergothioneine pretreatment protects the liver from ischemia-reperfusion injury caused by increasing hepatic heat shock protein 70. J Surg Res 2004; 122: 96-102.
138. Singh AK, Mani H, Seth P, Gaddipati JP, Kumari R, Banuadha KK, et al., Picroliv preconditioning protects the rat liver against ischemia-reperfusion injury. Eur J Pharmacol 2000; 395: 229-39.
139. Ninomiya M, Shimada M, Harada N, Soejima Y, Suehiro T, Maehara Y. The hydroxyl radical scavenger MCI-186 protects the liver from experimental cold ischaemia-reperfusion injury. Br J Surg 2004; 91: 184-90.
140. Ninomiya M, Shimada M, Harada N, Shiotani S, Hiroshige S, Soejima Y, et al. Beneficial effect of MCI-186 on hepatic warm ischemia-reperfusion in the rat. Transplantation 2002; 74: 1470-2.
141. Sepodes B, Maio R, Pinto R, Marques C, Mendes-do-Vale J, McDonald MC, et al. Tempol, an intracelullar free radical scavenger, reduces liver injury in hepatic ischemia-reperfusion in the rat, Transplant Proc 2004; 36: 849-53.
142. Schutz E, Wieland E, Hensel A, Niedmann PD, Dreiss A, Armstrong VW, et al. Suppression of leukocyte-enhanced cold ischemia/reperfusion injury of liver endothelium with the benzoquinone antioxidant idebenone. Clin Biochem 1997; 30: 619-24.
143. Strubelt O, Younes M, Li Y. Protection by albumin against ischaemia- and hypoxia-induced hepatic injury. Pharmacol Toxicol 1994; 75: 280-4.
144. Giakoustidis D, Papageorgiou G, Iliadis S, Kontos N, Kostopoulou E, Papachrestou A, et al. Intramuscular administration of very high dose of a-tocopherol protects liver from severe ischemia/reperfusion injury. World J Surg 2002; 26: 872-7.
145. Azzi A, Davies KJA, Kelly F. Free radical biology - terminology and critical thinking. FEBS Lett 2004, 558: 3-6.
146. Lehnert M, Arteel GE, Smutney OM, Conzelmann LO, Zhong Z, Thurman RG, et al. Dependence of liver injury after hemorrhage/resuscitation in mice on NADPH oxidase-derived superoxide. Shock 2003; 19: 345-51.
147. Akgur FM, Brown MF, Zibari GB, McDonald JC, Epstein CJ, Ross CR, et al. Role of superoxide in hemorrhagic shock-induced P-selectin expression. Am J Physiol Heart Circ Physiol 2000; 279: H791-7.
148. Gennaro R, Zanetti M, Benincasa M, Podda E, Miani M. Pro-rich antimicrobial peptides from animals: structure, biological functions and mechanism of action. Curr Pharmac Des 2002; 8: 763-78.
149. Ikeda Y, Young LH, Scalia R, Ross CR, Lefer AM. PR-39, a proline/ arginine-rich antimicrobial peptide, exerts cardioprotective effects in myocardial ischemia-reperfusion. Cardiovasc Res 2001: 49: 69-77.
150. Bao J, Sato K, Li M, Gao Y, Abid R, Aird W, et al. PR-39 and PR-11 peptides inhibit ischemia-reperfusion injury by blocking proteasome-mediated I kappa B alpha degradation. Am J Physiol Heart Circ Physiol 2001; 281: H2612-8.
151. Karwinski W, Soreide O. Allopurinol improves scavenging ability of the liver after ischemia/reperfusion injury. Liver 1997; 17: 139-43.
152. Das DK, Engelman RM, Clement R, Otani H, Prasad MR, Rao PS. Role of xanthine oxidase inhibitor as free radical scavenger: a novel mechanism of action of allopurinol and oxypurinol in myocardial salvage. Biochem Biophys Res Commun 1987; 148: 314-9.
153. Moorhouse PC, Grootveld M, Halliwell B, Quinlan JG, Gutteridge JM. Allopurinol and oxypurinol are hydroxyl radical scavengers. FEBS Lett 1987; 213: 23-8.
154. Knight TR, Jaeschke H. Acetaminophen-induced inhibition of Fas receptor-mediated liver cell apoptosis: mitochondrial dysfunction versus glutathione depletion. Toxicol Appl Pharmacol 2002; 181: 133-41.
155. Jeon BR, Yeon DH, Lee SM. Protective effect of allopurinol on hepatic energy metabolism in ischemic and reperfused rat liver. Shock 2001; 15: 112-7.
156. Jaeschke H, Bautista AP, Spolarics Z, Spitzer JJ. Superoxide generation by neutrophils and Kupffer cells during in vivo reperfusion after hepatic ischemia in rats. J Leukoc Biol 1992; 52: 377-82.
157. Bremer C, Bradford BU, Hunt KJ, Knecht KT, Connor HD, Mason RP, et al. Role of Kupffer cells in the pathogenesis of hepatic reperfusion injury. Am J Physiol 1994; 267: G630-6.
158. Shiratori Y, Kiriyama H, Fukushi Y, Nagura T, Takada H, Hai K, et al. Modulation of ischemia-reperfusion-induced hepatic injury by Kupffer cells. Dig Dis Sci 1994; 39: 1265-72.
159. von Frankenberg M, Golling M, Mehrabi A, Nentwich H, Klar E, Kraus TW. Donor pretreatment with gadolinium chloride improves early graft function and survival after porcine liver transplantation. Transpl Int 2003; 16: 806-13.
160. Meneghini R. Iron homeostasis, oxidative stress, and DNA damage. Free Radic Biol Med 1997; 23: 783-92.
161. Symons MCR, Gutteridge JMC, Eds, Free radicals and iron: chemistry, biology, and medicine. Oxford, Oxford Science Publications. 1998, Publications
162. Berenshtein E, Mayer B, Goldberg C, Kitrossky N, Chevion M. Patterns of mobilization of copper and iron following myocardial ischemia: possible predictive criteria for tissue injury. J Mol Cell Cardiol 1997; 29: 3025-34
163. Ozaki M, Fuchinoue S, Teraoka S, Ota K. Mobilization of low-molecular-weight iron and peroxidative damage during ischemia and reoxygenation of the rat liver. Transplant Proc 1994; 26: 918-21.
164. Lesnefsky EJ. Tissue iron overload and mechanisms of iron-catalyzed oxidative injury. Adv Exp Med Biol 1994; 366: 129-46.
165. Baliga R, Ueda N, Shah SV. Increase in bleomycin-detectable iron in ischaemia/reperfusion injury to rat kidneys. Biochem J 1993; 291: 901-5.
166. Chevion M, Jiang Y, Har-El R, Bernshtein E, Uretzky G, Kitrofssky N. Copper and iron are mobilized following myocardial ischemia: possible predictive criteria for tissue injury. Proc Natl Acad Sci USA 1993; 90: 1102-6.
167. Boucher F, Pucheu S, Coundray C, Favier A, de Leiris J. Evidence for cytosolic iron release during post-ischemic reperfusion of isolated rat hearts. Influence on spin-trapping experiments with DMPO. FEBS Lett 1992; 302: 261-4.
168. Park K, Chung KY, Sung SH, Kim BR, Kim YS. Protective effect of desferrioxamine during canine liver transplantation: significance of peritransplant liver biopsy, Transplant Proc 2003; 35: 117-9.
169. Arora AS, Gores GJ. The role of metals in ischemia/reperfusion injury of the liver. Semin Liver Dis 1996; 16: 31-8.
170. Colletti LM, Remick DG, Campbell DA Jr. Desferal attenuates TNF release following hepatic ischemia/reperfusion. J Surg Res 1994; 57: 447-53.
171. Drugas GT, Paidas CN, Yahanda AM, Ferguson D, Clemens MG. Conjugated desferoxamine attenuates hepatic microvascular injury following ischemia/ reperfusion. Circ Shock 1991; 34: 278-83.
172. Yu Z, Persson HL, Eaton JW, Brunk UT. Intralysosomal iron: a major determinant of oxidant-induced cell death. Free Radic Biol Med 2003; 34: 1243-52.
173. Amersi F, Dulkanchainun T, Nelson SK, Farmer DG, Kato H, Zaky J, et al. A novel iron chelator in combination with a P-selectin antagonist prevents ischemia/reperfusion injury in a rat liver model. Transplantation 2001; 71: 112-8.
174. Iwanami K, Takeyoshi I, Ohwada S, Kobayashi J, Kawashima Y, Aiba M, et al. The effect of Lazaroid U-74389G on extended liver resection with ischemia in dogs. Surgery 1999; 126: 908-17.
175. Ishizaki N, Zhu Y, Zhang S, Nemoto A, Kobayashi Y, Subbotin V, et al. Comparison of various lazaroid compounds for protection against ischemic liver injury. Transplantation 1997; 63: 202-8.
176. Pucheau CS, Coundray C, Tresallet N, Favier A, de Leiris J. Effect of iron overload in the isolated ischemic and reperfused rat heart. Cardiov Drug Ther 1993; 4: 701-11.
177. Collis CS, Davies MJ, Rice-Evans C. Comparison of N-methyl hexanoylhydroxamic acid, a novel antioxidant, with desferrioxamine and N-acetyl cystein against reperfusion-induced dysfunction in isolated rat heart, J Cardiov Pharmac 1993; 22: 336-42.
178. Berberat PO, Katori M, Kaczmarek E, Anselmo D, Lassman C, Ke B, et al. Heavy chain ferritin acts as an antiapoptotic gene that protects livers from ischemia reperfusion injury. FASEB J 2003; 17:1724-6.
179. van Jaarsveld H, Schulenburg DH. Dietary iron alters liver, erythrocyte and plasma antioxidant and nitrite levels, and also sensitizes the heart to ischemia/reperfusion. Res Commun Mot Pathol Pharmacol 1997; 97: 347-60.
180. Bergamini CM, Gambetti S, Dondi A, Cervellati C. Oxygen, reactive oxygen species and tissue damage. Curr Pharm Des 2004; 10(14): 1611-26.
181. Fylaktakidou KC, Hadjipavlou-Litina DJ, Litinas KE, Nicolaides DN. Natural and synthetic coumarin derivatives with anti-inflammatory/ antioxidant activities. Curr Pharm. Des 2004; 10(30): 3813-33.
182. Vertuani S, Angusti A, Manfredini S. The antioxidants and pro-antioxidants network: an overview. Curr Pharm Des 2004; 10(14): 1677-94.