The contemporary role of antioxidant therapy in attenuating liver ischemia-reperfusion injury: A review

Liver Transplantation

Volumn 11, Issue 9, 2005, Pages 1031-1047

  Glantzounis, Georgios K ^a,b   Salacinski, Henryk J ^a   Yang, Wenxuan ^a   Davidson, Brian R ^a,b   Seifalian, Alexander M ^a,b  

^a ROYAL FREE AND UNIVERSITY COLLEGE MEDICAL SCHOOL   (United Kingdom)

^b ROYAL FREE LONDON NHS FOUNDATION TRUST   (United Kingdom)

Author keywords

[No Author keywords available]

Indexed keywords

ACETYLCYSTEINE; ALLOPURINOL; ALPHA TOCOPHEROL; AMINOGUANIDINE; ANTIOXIDANT; ASCORBIC ACID; BUCILLAMINE; CATALASE; CYANIDIN; DEFEROXAMINE; GLUTATHIONE; GLUTATHIONE REDUCTASE; GREEN TEA EXTRACT; HERBACEOUS AGENT; IDEBENONE; MELATONIN; NITRIC OXIDE; NITRIC OXIDE SYNTHASE; PENTOXIFYLLINE; PHENOL DERIVATIVE; PLANT EXTRACT; QUERCETIN; REACTIVE OXYGEN METABOLITE; SUPEROXIDE DISMUTASE; THIOCTIC ACID; THIOREDOXIN; TRIMETAZIDINE; TROLOX C; UBIQUINONE; UNCLASSIFIED DRUG; UNINDEXED DRUG; VIRUS VECTOR;

ANTIOXIDANT ACTIVITY; ATTENUATION; CLINICAL TRIAL; DRUG MECHANISM; EXPERIMENTATION; FLUID THERAPY; GENE THERAPY; HEMORRHAGIC SHOCK; HUMAN; LIVER ISCHEMIA; LIVER SURGERY; LIVER TRANSPLANTATION; MODULATION; MORBIDITY; MORTALITY; NONHUMAN; OXIDATIVE STRESS; PRIORITY JOURNAL; REPERFUSION INJURY; RESUSCITATION; REVIEW; VIRAL GENE DELIVERY SYSTEM;

ANTIOXIDANTS; HUMANS; ISCHEMIA; LIVER; LIVER DISEASES; OXIDATIVE STRESS; REPERFUSION INJURY;

EID: 25144463539     PISSN: 15276465     EISSN: None     Source Type: Journal    
DOI: 10.1002/lt.20504     Document Type: Review

References (191)

1. Liu DL, Jeppsson B, Hakansson CH, Odselius R. Multiple-system organ damage resulting from prolonged hepatic inflow interruption. Arch Surg 1996;131:442-447.
2. Caldwell-Kenkel JC, Currin RT, Tanaka Y, Thurman RG, Lemasters JJ. Kupffer cell activation and endothelial cell damage after storage of rat livers: Effects of reperfusion. Hepatology 1991;13:83-95.
3. Deschenes M, Belle SH, Krom RA, Zetterman RK, Lake JR. Early allograft dysfunction after liver transplantation: A definition and predictors of outcome. National Institute of Diabetes and Digestive and Kidney Diseases Liver Transplantation Database. Transplantation 1998;66:302-310.
4. Yamakawa Y, Takano M, Patel M, Tien N, Takada T, Bulkley GB. Interaction of platelet activating factor, reactive oxygen species generated by xanthine oxidase, and leukocytes in the generation of hepatic injury after shock/resuscitation. Ann Surg 2000;231:387-398.
5. Okano N, Miyoshi S, Owada R, Fujita N, Kadoi Y, Saito S, et al. Impairment of hepatosplanchnic oxygenation and increase of serum hyaluronate during normothermic and mild hypothermic cardiopulmonary bypass. Anesth Analg 2002;95:278-86.
6. 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;15:1315-1319.
7. Glantzounis GK, Tsimaris I, Tselepis AD, Thomas C, Tambaki AP, Galaris DA, et al. Alterations in plasma oxidative stress markers after laparoscopic operations of the upper and lower abdomen. 272. Angiology 2005. In press.
8. Rezende-Neto JB, Moore EE, Masuno T, Moore PK, Johnson JL, Sheppard FR, et al. The abdominal compartment syndrome as a second insult during systemic neutrophil priming provokes multiple organ injury. Shock 2003;20:303-308.
9. Isozaki H, Okajima K, Kobayashi M, Hara H, Akimoto H. Experimental study of liver injury after partial hepatectomy with intermittent or continuous hepatic vascular occlusion. Differences in tolerance to ischemia between normal and cirrhotic livers. Eur Surg Res 1995;27:313-322.
10. Pocard M, Vincent-Salomon A, Girodet J, Salmon RJ. Effects of preoperative chemotherapy on liver function tests after hepatectomy. Hepatogastroenterology 2001;48:1406-1408.
11. Kaibori M, Matsui Y, Kitade H, Kwon AH, Kamiyama Y. Hepatic resection for hepatocellular carcinoma in severely cirrhotic livers. Hepatogastroenterology 2003;50:491-496.
12. Clavien PA, Harvey PR, Strasberg SM. Preservation and reperfusion injuries in liver allografts. An overview and synthesis of current studies. Transplantation 1992;53:957-978.
13. Fellstrom B, Akuyrek LM, Backman U, Larsson E, Melin J, Zezina L. Postischemic reperfusion injury and allograft arteriosclerosis. Transplant Proc 1998;30:4278-4280.
14. Selzner M, Clavien PA. Fatty liver in liver transplantation and surgery. Semin Liver Dis 2001;21:105-113.
15. Seifalian AM, Chidambaram V, Rolles K, Davidson BR. In vivo demonstration of impaired microcirculation in steatotic human liver grafts. Liver Transpl Surg 1998;4:71-77.
16. Ijaz S, Yang W, Winslet MC, Seifalian AM. Impairment of hepatic microcirculation in fairy liver. Microcirculation 2003; 10:447-456.
17. Czaja MJ. Induction and regulation of hepatocyte apoptosis by oxidative stress. Antioxid Redox Signal 2002;4:759-767.
18. Haddad JJ. Antioxidant and prooxidant mechanisms in the regulation of redox(y)-sensitive transcription factors. Cell Signal 2002;14:879-897.
19. Bilzer M, Gerbes AL. Preservation injury of the liver: mechanisms and novel therapeutic strategies. J Hepatol 2000;32:508-515.
20. Jaeschke H. Molecular mechanisms of hepatic ischemia-reperfusion injury and preconditioning. Am J Physiol Gastrointest Liver Physiol 2003;284:G15-G26.
21. Koti RS, Seifalian AM, Davidson BR. Protection of the liver by ischemic preconditioning: a review of mechanisms and clinical applications. Dig Surg 2003;20:383-396.
22. Lentsch AB, Kato A, Yoshidome H, McMasters KM, Edwards MJ. Inflammatory mechanisms and therapeutic strategies for warm hepatic ischemia/reperfusion injury. Hepatology 2000; 32:169-173.
23. Selzner N, Rudiger H, Graf R, Clavien PA. Protective strategies against ischemic injury of the liver. Gastroenterology 2003; 125:917-936.
24. Gonzalez-Flecha B, Cutrin JC, Boveris A. Time course and mechanism of oxidative stress and tissue damage in rat liver subjected to in vivo ischemia-reperfusion. J Clin Invest 1993; 91:456-464.
25. Blum H, Osbakken MD, Johnson RG, Jr. Sodium flux and bioenergetics in the ischemic rat liver. Magn Reson Med 1991; 18:348-357.
26. Dhar DK, Takemoto Y, Nagasue N, Uchida M, Ono T, Nakamura T. FK506 maintains cellular calcium homeostasis in ischemia-reperfusion injury of the canine liver. J Surg Res 1996;60: 142-146.
27. Farber JL. The role of calcium in cell death. Life Sci 1981;29: 1289-1295.
28. Kim JS, He L, Lemasters JJ. Mitochondrial permeability transition: A common pathway to necrosis and apoptosis. Biochem Biophys Res Common 2003;304:463-470.
29. Nishimura Y, Lemasters JJ. Glycine blocks opening of a death channel in cultured hepatic sinusoidal endothelial cells during chemical hypoxia. Cell Death Differ 2001;8:850-858.
30. Zahrebelski G, Nieminen AL, al Ghoul K, Qian T, Herman B, Lemasters JJ. Progression of subcellular changes during chemical hypoxia to cultured rat hepatocytes: A laser scanning confocal microscopic study. Hepatology 1995;21:1361-1372.
31. Ishii K, Suita S, Sumimoto H. Effect of verapamil on conversion of xanthine dehydrogenase to oxidase in ischemic rat liver. Res Exp Med (Berl) 1990;190:3891-399.
32. Churchill TA, Cheetham KM, Fuller BJ. Glycolysis and energy metabolism in rat liver during warm and cold ischemia: Evidence of an activation of the regulatory enzyme phosphofructokinase. Cryobiology 1994;31:441-452.
33. Baumann M, Bender E, Stommer G, Gross G, Brand K. Effects of warm and cold ischemia on mitochondrial functions in brain, liver and kidney. Mol Cell Biochem 1989;87:137-145.
34. Mochida S, Arai M, Ohno A, Masaki N, Ogata I, Fujiwara K. Oxidative stress in hepatocytes and stimulatory state of Kupffer cells after reperfusion differ between warm and cold ischemia in rats. Liver 1994;14:234-240.
35. Ikeda T, Yanaga K, Kishikawa K, Kakizoe S, Shimada M, Sugimachi K. Ischemic injury in liver transplantation: Difference in injury sites between warm and cold ischemia in rats. Hepatology 1992;16:454-461.
36. Jaeschke H, Farhood A. Neutrophil and Kupffer cell-induced oxidant stress and ischemia-reperfusion injury in rat liver. Am J Physiol 1991;260:G355-G362.
37. Fondevila C, Busuttil RW, Kupiec-Weglinski JW. Hepatic ischemia/reperfusion injury - a fresh look. Exp Mol Pathol 2003;74:86-93.
38. Liu TZ, Lee KT, Chern CL, Cheng JT, Stern A, Tsai LY. Free radical-triggered hepatic injury of experimental obstructive jaundice of rats involves overproduction of proinflammatory cytokines and enhanced activation of nuclear factor kappaB. Ann Clin Lab Sci 2001;31:383-390.
39. Jaeschke H. Reactive oxygen and mechanisms of inflammatory liver injury. J Gastroenterol Hepatol 2000;15:718-724.
40. Weiss SJ. Tissue destruction by neutrophils. N Engl J Med 1989;320:365-376.
41. Matsuda T, Yamaguchi Y, Matsumura F, Akizuki E, Okabe K, Liang J, et al. Immunosuppressants decrease neutrophil chemoattractant and attenuate ischemia/reperfusion injury of the liver in rats. J Trauma 1998;44:475-484.
42. Shen XD, Ke B, Zhai Y, Amersi F, Gao F, Anselmo DM, et al. CD154-CD40 T-cell costimulation pathway is required in the mechanism of hepatic ischemia/reperfusion injury, and its blockade facilitates and depends on heme oxygenase-1 mediated cytoprotection. Transplantation 2002;74:315-319.
43. Suzuki S, Toledo-Pereyra LH, Rodriguez FJ, Cejalvo D. Neutrophil infiltration as an important factor in liver ischemia and reperfusion injury. Modulating effects of FK506 and cyclosporine. Transplantation 1993;55:1265-1272.
44. Clavien PA, Harvey PR, Sanabria JR, Cywes R, Levy GA, Strasberg SM. Lymphocyte adherence in the reperfused rat liver: Mechanisms and effects. Hepatology 1993;17:131-142.
45. Zwacka RM, Zhang Y, Halldorson J, Schlossberg H, Dudus L, Engelhardt JF. CD4(+) T-lymphocyres mediate ischemia/reperfusion-induced inflammatory responses in mouse liver. J Clin Invest 1997;100:279-289.
46. Halliwell B, Gutteridge JMC. Free Radicals in Biology and Medicine. 3rd ed. New York: Oxford University Press; 1999.
47. Nohl H, Gille L, Kozlov A, Staniek K. Are mitochondria a spontaneous and permanent source of reactive oxygen species? Redox Rep 2003;8:135-141.
48. Ischiropoulos H, Zhu L, Beckman JS. Peroxynitrite formation from macrophage-derived nitric oxide. Arch Biochem Biophys 1992;298:446-451.
49. Cuzzocrea S, Riley DP, Caputi AP, Salvemini D. Antioxidant therapy: A new pharmacological approach in shock, inflammation, and ischemia/reperfusion injury. Pharmacol Rev 2001;53: 135-159.
50. Sutton HC, Winterbourn CC. On the participation of higher oxidation states of iron and copper in Fenton reactions. Free Radic Biol Med 1989;6:53-60.
51. Bilzer M, Paumgartner G, Gerbes AL. Glutathione protects the rat liver against reperfusion injury after hypothermic preservation. Gastroenterology 1999;117:200-210.
52. Giakoustidis D, Papageorgiou G, Iliadis S, Kontos N, Kostopoulou E, Papachrestou A, et al. Intramuscular administration of very high dose of alpha-tocopherol protects liver from severe ischemia/reperfusion injury. World J Surg 2002;26:872-877.
53. Rauen U, Polzar B, Stephan H, Mannherz HG, de Groot H. Cold-induced apoptosis in cultured hepatocytes and liver endothelial cells: mediation by reactive oxygen species. FASEB J 1999;13:155-168.
54. Rudiger HA, Clavien PA. Tumor necrosis factor alpha, but not Fas, mediates hepatocellular apoptosis in the murine ischemic liver. Gastroenterology 2002;122:202-210.
55. Fan C, Zwacka RM, Engelhardt JF. Therapeutic approaches for ischemia/reperfusion injury in the liver. J Mol Med 1999;77: 577-592.
56. Jaeschke H. Xanthine oxidase-induced oxidant stress during hepatic ischemia-reperfusion: Are we coming full circle after 20 years? Hepatology 2002;36:761-763.
57. Nieminen AL, Byrne AM, Herman B, Lemasters JJ. Mitochondrial permeability transition in hepatocytes induced by t-BuOOH: NAD(P)H and reactive oxygen species. Am J Physiol 1997;272:C1286-C1294.
58. 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;28:1022-1030.
59. Harada N, Iimuro Y, Nitta T, Yoshida M, Uchinami H, Nishio T, et al. Inactivation of the small GTPase Rac1 protects the liver from ischemia/reperfusion injury in the rat. Surgery 2003;134: 480-491.
60. Paxian M, Rensing H, Rickauer A, Schonhofen S, Schmeck J, Pannen BH, et al. Kupffer cells and neutrophils as paracrine regulators of the heme oxygenase-1 gene in hepatocytes after hemorrhagic shock. Shock 2001;15:438-445.
61. Nakatani T, Inouye M, Mirochnitchenko O. Overexpression of antioxidant enzymes in transgenic mice decreases cellular ploidy during liver regeneration. Exp Cell Res 1997;236:137-146.
62. Pannen BH. New insights into the regulation of hepatic blood flow after ischemia and reperfusion. Anesth Analg 2002;94: 1448-1457.
63. Bauer M, Bauer I. Heme oxygenase-1: Redox regulation and role in the hepatic response to oxidative stress. Antioxid Redox Signal 2002;4:749-758.
64. Moncada S, Higgs A. The L-arginine-nitric oxide pathway. N Engl J Med 1993;329:2002-2012.
65. Vasquez-Vivar J, Kalyanaraman B, Martasek P, Hogg N, Masters BS, Karoui H, et al. Superoxide generation by endothelial nitric oxide synthase: The influence of cofactors. Proc Natl Acad Sci U S A 1998;95:9220-9225.
66. Schmidt HH, Lohmann SM, Walter U. The nitric oxide and cGMP signal transduction system: regulation and mechanism of action. Biochim Biophys Acta 1993;1178:153-175.
67. Gauthier TW, Davenpeck KL, Lefer AM. Nitric oxide attenuates leukocyte-endothelial interaction via P-selectin in splanchnic ischemia-reperfusion. Am J Physiol 1994;267:G562-G568.
68. Mittal MK, Gupta TK, Lee FY, Sieber CC, Groszmann RJ. Nitric oxide modulates hepatic vascular tone in normal rat liver. Am J Physiol 1994;267:G416-G422.
69. McCuskey RS. Morphological mechanisms for regulating blood flow through hepatic sinusoids. Liver 2000;20:3-7.
70. Ming Z, Han C, Lautt WW. Nitric oxide mediates hepatic arterial vascular escape from norepinephrine-induced constriction. Am J Physiol 1999;277:G1200-G1206.
71. Hur GM, Ryu YS, Yun HY, Jeon BH, Kim YM, Seok JH, et al. Hepatic ischemia/reperfusion in rats induces iNOS gene transcription by activation of NF-kappaB. Biochem Biophys Res Commun 1999;261:917-922.
72. Kimura H, Katsuramaki T, Isobe M, Nagayama M, Meguro M, Kukita K, et al. Role of inducible nitric oxide synthase in pig liver transplantation. J Surg Res 2003;111:28-37.
73. Meguro M, Katsuramaki T, Nagayama M, Kimura H, Isobe M, Kimura Y, et al. A novel inhibitor of inducible nitric oxide synthase (ONO-1714) prevents critical warm ischemia-reperfusion injury in the pig liver. Transplantation 2002;73:1439-1446.
74. Serracino-Inglott F, Habib NA, Mathie RT. Hepatic ischemia-reperfusion injury. Am J Surg 2001;181:160-166.
75. Hsu CM, Wang JS, Liu CH, Chen LW. Kupffer cells protect liver from ischemia-reperfusion injury by an inducible nitric oxide synthase-dependent mechanism. Shock 2002;17:280-285.
76. Wang Y, Lawson JA, Jaeschke H. Differential effect of 2-aminoethyl-isothiourea, an inhibitor of the inducible nitric oxide synthase, on microvascular blood flow and organ injury in models of hepatic ischemia-reperfusion and endotoxemia. Shock 1998;10:20-25.
77. Hines IN, Kawachi S, Harada H, Pavlick KP, Hoffman JM, Bharwani S, et al. Role of nitric oxide in liver ischemia and reperfusion injury. Mol Cell Biochem 2002;234-235:229-237.
78. Rivera-Chavez FA, Toledo-Pereyra LH, Dean RE, Crouch L, Ward PA. Exogenous and endogenous nitric oxide but not iNOS inhibition improves function and survival of ischemically injured livers. J Invest Surg 2001;14:267-273.
79. Lee VG, Johnson ML, Baust J, Laubach VE, Watkins SC, Billiar TR. The roles of iNOS in liver ischemia-reperfusion injury. Shock 2001;16:355-360.
80. Doulias PT, Barbouti A, Galaris D, Ischiropoulos 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;30:679-685.
81. Hon WM, Lee KH, Khoo HE. Nitric oxide in liver diseases: friend, foe, or just passerby? Ann N Y Acad Sci 2002;962:275-295.
82. Szabo C. Multiple pathways of peroxynitrite cytotoxicity. Toxicol Lett 2003;140-141:105-112.
83. Gutteridge JM. Lipid peroxidation and antioxidants as biomarkers of tissue damage. Clin Chem 1995;41:1819-1828.
84. Sies H. Oxidative Stress II Oxidants and Antioxidants. London: Academic Press; 1991.
85. Marczin N, El Habashi N, Hoare GS, Bundy RE, Yacoub M. Antioxidants in myocardial ischemia-reperfusion injury: Therapeutic potential and basic mechanisms 1. Arch Biochem Biophys 2003;420:222-236.
86. Vertuani S, Angusti A, Manfredini S. The antioxidants and pro-antioxidants network: An overview. Curr Pharm Des 2004; 10:1677-1694.
87. Sherman L, Dafni N, Lieman-Hurwitz J, Groner Y. Nucleotide sequence and expression of human chromosome 21-encoded superoxide dismutase mRNA. Proc Natl Acad Sci U S A 1983; 80:5465-5469.
88. Ho YS, Crapo JD. Isolation and characterization of complementary DNAs encoding human manganese-containing superoxide dismutase. FEBS Lett 1988;229:256-260.
89. Dufaure JP, Lareyre JJ, Schwaab V, Mattei MG, Drevet JR. Structural organization, chromosomal localization, expression and phylogenetic evaluation of mouse glutathione peroxidase encoding genes. C R Acad Sci III 1996;319:559-568.
90. Meister A. Glutathione metabolism and its selective modification. J Biol Chem 1988;263:17205-17208.
91. Hanna PM, Mason RP. Direct evidence for inhibition of free radical formation from Cu(I) and hydrogen peroxide by glutathione and other potential ligands using the EPR spin-trapping technique. Arch Biochem Biophys 1992;295:205-213.
92. Halliwell B, Gutteridge J. Antioxidant defences. In: Halliwell B, Gutteridge JMC, eds. Free Radicals in Biology and Medicine. Oxford: Oxford University Press; 1999:105-245.
93. Kang SW, Chae HZ, Seo MS, Kim K, Baines IC, Rhee SG. Mammalian peroxiredoxin isoforms can reduce hydrogen peroxide generated in response to growth factors and tumor necrosis factor-alpha. J Biol Chem 1998;273:6297-6302.
94. Seo MS, Kang SW, Kim K, Baines IC, Lee TH, Rhee SG. Identification of a new type of mammalian peroxiredoxin that forms an intramolecular disulfide as a reaction intermediate. J Biol Chem 2000;275:20346-20354.
95. Hirota K, Nakamura H, Masutani H, Yodoi J. Thioredoxin superfamily and thioredoxin-inducing agents. Ann N Y Acad Sci 2002;957:189-199.
96. Guo X, Shin VY, Cho CH. Modulation of heme oxygenase in tissue injury and its implication in protection against gastrointestinal diseases. Life Sci 2001;69:3113-3119.
97. Betteridge DJ. What is oxidative stress? Metabolism 2000;49: 3-8.
98. Halliwell B, Gutteridge JM. The antioxidants of human extracellular fluids. Arch Biochem Biophys 1990;280:1-8.
99. Gutteridge JM. Iron and oxygen: a biologically damaging mixture. Acta Paediatr Scand Suppl 1989;361:78-85.
100. Ames BN, Cathcart R, Schwiers E, Hochstein P. Uric acid provides an antioxidant defense in humans against oxidant- and radical-caused aging and cancer: A hypothesis. Proc Natl Acad Sci USA 1981;78:6858-6862.
101. Frei B, Stocker R, Ames BN. Antioxidant defenses and lipid peroxidation in human blood plasma. Proc Natl Acad Sci U S A 1988;85:9748-9752.
102. Layton ME, Wood JG, Yan ZY, Forster J. Ischemia/reperfusion alters uric acid and ascorbic acid levels in liver. J Surg Res 1996;64:1-5.
103. Glantzounis G, Tsimoyiannis E, Kappas AM, Galaris DA. Uric acid and oxidative stress. Curr Pharm Des 2005. In press.
104. Reyes AJ, Leary WP. The increase in serum uric acid induced by diuretics could be beneficial to cardiovascular prognosis in hypertension: A hypothesis. J Hypertens 2003;21:1775-1777.
105. Chamorro A, Planas AM, Muner DS, Deulofeu R. Uric acid administration for neuroprotection in patients with acute brain ischemia. Med Hypotheses 2004;62:173-176.
106. Waring WS, Convery A, Mishra V, Shenkin A, Webb DJ, Maxwell SR. Uric acid reduces exercise-induced oxidative stress in healthy adults. Clin Sci (Lond) 2003;105:425-430.
107. Birlouez-Aragon I, Tessier FJ. Antioxidant vitamins and degenerative pathologies. A review of vitamin C. J Nutr Health Aging 2003;7:103-109.
108. Traber MG. Determinants of plasma vitamin E concentrations. Free Radic Biol Med 1994;16:229-239.
109. Liebler DC, McClure TD. Antioxidant reactions of beta-carotene: Identification of carotenoid-radical adducts. Chem Res Toxicol 1996;9:8-11.
110. Rice-Evans CA, Miller NJ, Paganga G. Structure-antioxidant activity relationships of flavonoids and phenolic acids. Free Radic Biol Med 1996;20:933-956.
111. Shahidi F, Wanasundara PK. Phenolic antioxidants. Crit Rev Food Sci Nutr 1992;32:67-103.
112. Haramaki N, Stewart DB, Aggarwal S, Ikeda H, Reznick AZ, Packer L. Networking antioxidants in the isolated rat heart are selectively depleted by ischemia-reperfusion. Free Radic Biol Med 1998;25:329-339.
113. Brigelius-Flohe R, Kelly FJ, Salonen JT, Neuzil J, Zingg JM, Azzi A. The European perspective on vitamin E: Current knowledge and future research. Am J Clin Nutr 2002;76:703-716.
114. Calfee-Mason KG, Spear BT, Glauert HP. Vitamin E inhibits hepatic NF-kappaB activation in rats administered the hepatic tumor promoter, phenobarbital. J Nutr 2002;132:3178-3185.
115. Masaki H, Okano Y, Ochiai Y, Obayashi K, Akamatsu H, Sakurai H. alpha-tocopherol increases the intracellular glutathione level in HaCaT keratinocytes. Free Radic Res 2002;36: 705-709.
116. Ricciarelli R, Zingg JM, Azzi A. The 80th anniversary of vitamin E: Beyond its antioxidant properties. Biol Chem 2002; 383:457-465.
117. Marubayashi S, Dohi K, Yamada K, Kawasaki T. Changes in the levels of endogenous coenzyme Q homologs, alpha-tocopherol, and glutathione in rat liver after hepatic ischemia and reperfusion, and the effect of pretreatment with coenzyme Q10. Biochim Biophys Acta 1984;797:1-9.
118. 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;34:13-18.
119. Gondolesi GE, Lausada N, Schinella G, Semplici AM, Vidal MS, Luna GC, et al. Reduction of ischemia-reperfusion injury in parenchymal and nonparenchymal liver cells by donor treatment with DL-alpha-tocopherol prior to organ harvest. Transplant Proc 2002;34:1086-1091.
120. Eum HA, Lee SH, Lee SM. Trolox C ameliorates hepatic drug metabolizing dysfunction after ischemia/reperfusion. Arch Pharm Res 2002;25:940-945.
121. Vardareli E, Saricam T, Koken T, Degirmenci I, Aral E, Erenoglu E. The effect of alpha-tocopherol and pentoxyfilline on ischemia-reperfusion induced liver injury in rats. Hepatogastroenterology 1998;45:1505-1508.
122. Seo MY, Lee SM. Protective effect of low dose of ascorbic acid on hepatobiliary function in hepatic ischemia/reperfusion in rats. J Hepatol 2002;36:72-77.
123. 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;30:463-469.
124. Rodriguez-Reynoso S, Leal C, Portilla E, Olivares N, Muniz J. Effect of exogenous melatonin on hepatic energetic status during ischemia/reperfusion: Possible role of tumor necrosis factor-alpha and nitric oxide. J Surg Res 2001;100:141-149.
125. Chen JC, Ng CJ, Chiu TF, Chen HM. Altered neutrophil apoptosis activity is reversed by melatonin in liver ischemia-reperfusion. J Pineal Res 2003;34:260-264.
126. Muller C, Dunschede F, Koch E, Vollmar AM, Kiemer AK. Alpha-lipoic acid preconditioning reduces ischemia-reperfusion injury of the rat liver via the PI3-kinase/Akt pathway. Am J Physiol Gastrointest Liver Physiol 2003;285:G769-G778.
127. Genova ML, Bonacorsi E, D'Aurelio M, Formiggini G, Nardo B, Cuccomarino S, et al. Protective effect of exogenous coenzyme Q in rats subjected to partial hepatic ischemia and reperfusion. Biofactors 1999;9:345-349.
128. 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: 619-624.
129. Portakal O, Inal-Erden M. Effects of pentoxifylline and coenzyme Q10 in hepatic ischemia/reperfusion injury. Clin Biochem 1999;32:461-466.
130. Omar R, Nomikos I, Piccorelli G, Savino J, Agarwal N. Prevention of postischaemic lipid peroxidation and liver cell injury by iron chelation. Gut 1989;30:510-514.
131. Bailey SM, Reinke LA. Antioxidants and gadolinium chloride attenuate hepatic parenchymal and endothelial cell injury induced by low flow ischemia and reperfusion in perfused rat livers. Free Radic Res 2000;32:497-506.
132. 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;35:117-119.
133. Tsimoyiannis EC, Moutesidou KJ, Moschos CM, Karayianni M, Karkabounas S, Kotoulas OB. Trimetazidine for prevention of hepatic injury induced by ischaemia and reperfusion in rats. Eur J Surg 1993;159:89-93.
134. Elimadi A, Sapena R, Settaf A, Le Louet H, Tillement J, Morin D. Attenuation of liver normothermic ischemia - reperfusion injury by preservation of mitochondrial functions with S-15176, a potent trimetazidine derivative. Biochem Pharmacol 2001;62:509-516.
135. Tselepis A, Doulias P, Lourida E, Glantzounis G, Tsimoyiannis E, Galaris D. Trimetazidine protects low-density lipoproteins from oxidation and cultured cells exposed to H(2)O(2) from DNA damage. Free Radic Biol Med 2001;30:1357-1364.
136. 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.
137. Tsuda T, Horio F, Kato Y, Osawa T. Cyanidin 3-O-beta-D-glucoside attenuates the hepatic ischemia-reperfusion injury through a decrease in the neutrophil chemoattractant production in rats. J Nutr Sci Vitaminol (Tokyo) 2002;48:134-141.
138. Nagai T, Egashira T, Kudo Y, Yamanaka Y, Shimada T. Attenuation of dysfunction in the ischemia-reperfused liver by glycyrrhizin. Jpn J Pharmacol 1992;58:209-218.
139. Chiu JH, Wang JC, Lui WY, Wu CW, Hong CY. Effect of magnolol on in vitro mitochondrial lipid peroxidation and isolated cold-preserved warm-reperfused rat livers. J Surg Res 1999;82:11-16.
140. 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;395:229-239.
141. Topp S, Knoefel WT, Schutte A, Brilloff S, Rogiers X, Gundlach M. Ginkgo biloba (EGB 761) improves microcirculation after warm ischemia of the rat liver. Transplant Proc 2001;33: 979-981.
142. Zhong Z, Froh M, Connor HD, Li X, Conzelmann LO, Mason RP, et al. Prevention of hepatic ischemia-reperfusion injury by green tea extract. Am J Physiol Gastrointest Liver Physiol 2002; 283:G957-G964.
143. Sanchez GM, Rodriguez HM, Giuliani A, Nunez Selles AJ, Rodriguez NP, Leon Fernandez OS. et al. Protective effect of Mangifera indica L. extract (Vimang) on the injury associated with hepatic ischaemia reperfusion. Phytother Res 2003;17: 197-201.
144. Moran LK, Gutteridge JM, Quinlan GJ. Thiols in cellular redox signalling and control 1. Curr Med Chem 2001;8:763-772.
145. Bilzer M, Lauterburg BH. Effects of hypochlorous acid and chloramines on vascular resistance, cell integrity, and biliary glutathione disulfide in the perfused rat liver: Modulation by glutathione. J Hepatol 1991;13:84-89.
146. Winterbourn CC, Metodiewa D. The reaction of superoxide with reduced glutathione. Arch Biochem Biophys 1994;314: 284-290.
147. Jaeschke H. Reactive oxygen and ischemia/reperfusion injury of the liver. Chem Biol Interact 1991;79:115-136.
148. Cho WE, Kim DG, Murase N, Mischinger HJ, Todo S, Starzl TE. Comparison of superoxide dismutase, allopurinol, coenzyme Q10, and glutathione for the prevention of warm ischemic injury. Transplantation 1990;50:353-355.
149. 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 Gastroenterol 2004;10:864-870.
150. Schauer RJ, Gerbes AL, Vonier D, Meissner H, Michl P, Leideter R, et al. Glutathione protects the rat liver against reperfusion injury after prolonged warm ischemia. Ann Surg 2004; 239:220-231.
151. Boman G, Backer U, Larsson S, Melander B, Wahlander L. Oral acetylcysteine reduces exacerbation rate in chronic bronchitis: Report of a trial organized by the Swedish Society for Pulmonary Diseases. Eur J Respir Dis 1983;64:405-415.
152. Cotgreave IA. N-acetylcysteine: Pharmacological considerations and experimental and clinical applications. Adv Pharmacol 1997;38:205-227.
153. Winniford MD, Kennedy PL, Wells PJ, Hillis LD. Potentiation of nitroglycerin-induced coronary dilatation by N-acetyl-cysteine. Circulation 1986;73:138-142.
154. Moldeus P, Cotgreave IA, Berggren M. Lung protection by a thiol-containing antioxidant: N-acetylcysteine. Respiration 1986;50(Suppl 1):31-42.
155. Chavez-Cartaya R, Jamieson NV, Ramirez P, Marin J, Pino-Chavez G. Free radical scavengers to prevent reperfusion injury following experimental warm liver ischaemia. Is there a real physiological benefit? Transpl Int 1999;12:213-221.
156. Koeppel TA, Thies JC, Lehmann T, Gebhard MM, Herfarth C, Otto G, et al. Improvement of hepatic microhemodynamics; by N-acetylcysteine after warm ischemia. Eur Surg Res 1996; 28:270-277.
157. Glantzounis GK, Yang W, Koti RS, Mikhailidis DP, Seifalian AM, Davidson BR. Continuous infusion of N-acetylcysteine reduces liver warm ischaemia-reperfusion injury. Br J Surg 2004;91:1330-1339.
158. 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;72:2707-2718.
159. Bromley PN, Cottam SJ, Hilmi I, Tan KC, Heaton N, Ginsburg R, et al. Effects of intraoperative N-acetylcysteine in orthotopic liver transplantation. Br J Anaesth 1995;75:352-354.
160. Steib A, Freys G, Collin F, Launoy A, Mark G, Boudjema K. Does N-acetylcysteine improve hemodynamics and graft function in liver transplantation? Liver Transpl Surg 1998;4:152-157.
161. Thies JC, Teklote J, Clauer U, Tox U, Klar E, Hofmann WJ, et al. The efficacy of N-acetylcysteine as a hepatoprotective agent in liver transplantation. Transpl Int 1998;11(Suppl 1):S390-S392.
162. Weigand MA, Plachky J, Thies JC, Spies-Martin D, Otto G, Martin E, et al. N-acetylcysteine attenuates the increase in alpha-glutathione S-transferase and circulating ICAM-1 and VCAM-1 after reperfusion in humans undergoing liver transplantation. Transplantation 2001;72:694-698.
163. Bucuvalas JC, Ryckman FC, Krug S, Alonso MH, Balistreri WF, Kotagal U. Effect of treatment with prostaglandin E1 and N-acetylcysteine on pediatric liver transplant recipients: A single-center study. Pediatr Transplant 2001;5:274-278.
164. Matsuno H, Sugiyama E, Muraguchi A, Nezuka T, Kubo T, Matsuura K, et al. Pharmacological effects of SA96 (bucillamine) and its metabolites as immunomodulating drugs - the disulfide structure of SA-96 metabolites plays a critical role in the pharmacological action of the drug. Int J Immunopharmacol 1998;20:295-304.
165. Amersi F, Nelson SK, Shen XD, Kato H, Melinek J, Kupiec-Weglinski JW, et al. Bucillamine, a thiol antioxidant, prevents transplantation-associated reperfusion injury. Proc Natl Acad Sci U S A 2002;99:8915-8920.
166. Horwitz LD. Bucillamine: A potent thiol donor with multiple clinical applications. Cardiovasc Drug Rev 2003;21:77-90.
167. Atalla SL, Toledo-Pereyra LH, MacKenzie GH, Cederna JP. Influence of oxygen-derived free radical scavengers on ischemic livers. Transplantation 1985;40:584-590.
168. Nauta RJ, Tsimoyiannis E, Uribe M, Walsh DB, Miller D, Butterfield A. Oxygen-derived free radicals in hepatic ischemia and reperfusion injury in the rat. Surg Gynecol Obstet 1990; 171:120-125.
169. Lambotte L, d'Udekem Y, Amrani M, Taper H. Free radicals and liver ischemia-reperfusion injury. Transplant Proc 1988; 20:977.
170. Minor T, Chung CW, Yamamoto Y, Obara M, Saad S, Isselhard W. Evaluation of antioxidant treatment with superoxide dismutase in rat liver transplantain after warm ischemia. Eur Surg Res 1992;24:333-338.
171. 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;289:1176-1184.
172. Veronese FM, Caliceti P, Schiavon O, Sergi M. Polyethylene glycol-superoxide dismutase, a conjugate in search of exploitation. Adv Drug Deliv Rev 2002;54:587-606.
173. 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 Commun 1992;189:191-196.
174. 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;3:127-130.
175. Nordstrom G, Saljo A, Hasselgren PO. Studies on the possible role of oxygen-derived free radicals for impairment of protein and energy metabolism in liver ischemia. Circ Shock 1988;26: 115-126.
176. Tanaka J, Malchesky PS, Omokawa S, Goldcamp JB, Harasaki H, Vogt DP, et al. Effects of prostaglandin I2, superoxide dismutase, and catalase on ischemia-reperfusion injury in liver transplantation. ASAIO Trans 1990;36:M600-M603.
177. 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;30:265-274.
178. Yabe Y, Kobayashi N, Nishihashi T, Takahashi R, Nishikawa M, Takakura Y, et al. Prevention of neutrophil-mediated hepatic ischemia/reperfusion injury by superoxide dismutase and catalase derivatives. J Pharmacol Exp Ther 2001;298:894-899.
179. Jeon BR, Yeom DH, Lee SM. Prouctive effect of allopurinol on hepatic energy metabolism in ischemic and reperfused rat liver. Shock 2001;15:112-117.
180. Knight TR, Kurtz A, Bajt ML, Hinson JA, Jaeschke H. Vascular and hepatocellular peroxynitrite formation during acetaminophen toxicity: role of mitochondrial oxidant stress. Toxicol Sci 2001;62:212-220.
181. Serracino-Inglott F, Virlos IT, Habib NA, Williamson RC, Mathie RT. Differential nitric oxide synthase expression during hepatic ischemia-reperfusion. Am J Surg 2003;185:589-595.
182. Isobe M, Katsuramaki T, Hirata K, Kimura H, Nagayama M, Matsuno T. Beneficial effects of inducible nitric oxide synthase inhibitor on reperfusion injury in the pig liver. Transplantation 1999;68:803-813.
183. Engelhardt JF. Redox-mediated gene therapies for environmental injury: Approaches and concepts. Antioxid Redox Signal 1999;1:5-27.
184. 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.
185. 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;69:1051-1057.
186. 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.
187. Wheeler MD, Katuna M, Smutney OM, Froh M, Dikalova A, Mason RP, et al. Comparison of the effect of adenoviral delivery of three superoxide dismutase genes against hepatic ischemia-reperfusion injury. Hum Gene Ther 2001;12:2167-2177.
188. Shau H, Merino A, Chen L, Shih CC, Colquhoun SD. Induction of peroxiredoxins in transplanted livers and demonstration of their in vitro cytoprotection activity. Antioxid Redox Signal 2000;2:347-354.
189. Iimuro Y, Nishiura T, Hellerbrand C, Behrns KE, Schoonhoven R, Grisham JW, et al. NFkappaB prevents apoptosis and liver dysfunction during liver regeneration. J Clin Invest 1998; 101:802-811.
190. Gutteridge JM, Halliwell B. Free radicals and antioxidants in the year 2000. A historical look to the future. Ann N Y Acad Sci 2000;899:136-147.
191. Olthoff KM. Molecular pathways of regeneration and repair after liver transplantation. World J Surg 2002;26: 831-837.