729
Views
132
CrossRef citations to date
0
Altmetric
Review Article

Current knowledge on oxidative stress in hepatic ischemia/reperfusion

, , &
Pages 555-568 | Received 21 Mar 2013, Accepted 31 May 2013, Published online: 26 Jun 2013

References

  • Selzner N, Rudiger H, Graf R, Clavien PA. Protective strategies against ischemic injury of the liver. Gastroenterology 2003;125:917–936.
  • Casillas-Ramírez A, Mosbah IB, Ramalho F, Roselló-Catafau J, Peralta C. Past and future approaches to ischemia-reperfusion lesion associated with liver transplantation. Life Sci 2006;79:1881–1894.
  • Connor HD, Gao W, Nukina S, Lemasters JJ, Mason RP, Thurman RG. Evidence that free radicals are involved in graft failure following liver transplantation in the rat – an electron – paramagnetic resonance spin trapping study. Transplantation 1992;54:199–204.
  • Sumimoto K, Matsura T, Oku JI, Fukuda Y, Yamada K, Dohi K. Protective effect of UW solution on postischemic injury in rat liver: suppression of reduction in hepatic antioxidants during reperfusion. Transplantation 1996; 27:1391–1398.
  • Glantzounis GK, Salacinski HJ, Yang W, Davidson BR, Seifalian AM. The contemporary role of antioxidant therapy in attenuating liver ischemia-reperfusion injury: a review. Liver Transpl 2005;11:1031–1047.
  • Tapuria N, Kumar Y, Habib MM, Abu Amara M, Seifalian AM, Davidson BR. Remote ischemic preconditioning: a novel protective method from ischemia reperfusion injury. J Surg Res 2008;150:304–330.
  • Cutrin JC, Perrelli MG, Cavalieri B, Peralta C, Rosell Catafau J, Poli G. Microvascular dysfunction induced by reperfusion injury and protective effect of ischemic preconditioning. Free Radic Biol Med 2002;33:1200–1208.
  • Jegatheeswaran S, Siriwardena AK. Experimental and clinical evidence for modification of hepatic ischaemia-reperfusion injury by N-acetylcysteine during major liver surgery. HPB (Oxford) 2011;12:71–78.
  • Fan J, Li Y, Levy RM, Fan JJ, Hackam DJ, Vodovotz Y, et al. Hemorrhagic shock induces NAD(P)H oxidase activation in neutrophils: role of HMGB1-TLR4 signaling. J Immunol 2007;178:6573–6580.
  • Kim JS, He L, Lemasters JJ. Mitochondrial permeability transition: a common pathway to necrosis and apoptosis. Biochem Biophys Res Commun 2003;304:463–470.
  • Kim JS, He L, Qian T, Lemasters JJ. Role of the mitochondrial permeability transition in apoptotic and necrotic death after ischemia/reperfusion injury to hepatocytes. Curr Mol Med 2003;3:527–535.
  • Van Remmen H, Richardson A. Oxidative damage to mitochondria and aging. Exp Gerontol 2001;36: 957–968.
  • Fernandez L, Heredia N, Grande L, Gómez G, Rimola A, Marco A, et al. Preconditioning protects liver and lung damage in rat liver transplantation: role of xanthine/xanthine oxidase. Hepatology 2002;36:562–572.
  • Jaeschke H. Xanthine oxidase-induced oxidant stress during hepatic ischemia-reperfusion: are we coming full circle after 20 years?Hepatology 2002;36:761–763.
  • Jeon BR, Yeom DH, Lee SM. Protective effect of allopurinol on hepatic energy metabolism in ischemic and reperfused rat liver. Shock 2001;15:112–117.
  • Jaeschke H. Reactive oxygen and ischemia/reperfusion injury of the liver. Chem Biol Interact 1991;79:115–136.
  • Grattagliano I, Vendemiale G, Lauterburg BH. Reperfusion injury of the liver: role of mitochondria and protection by glutathione ester. J Surg Res 1999;86:2–8.
  • Jaeschke H, Bautista AP, Spolarics Z, Spitzer JJ. Superoxide generation by Kupffer cells and priming of neutrophils during reperfusion after hepatic ischemia. Free Radic Res Commun 1991;15:277–284.
  • Jaeschke H. Vascular oxidant stress and hepatic ischemia/reperfusion injury. Free Radic Res Commun 1991;12–13: 737–743.
  • Rymsa B, Wang JF, de Groot H. O2 release by activated Kupffer cells upon hypoxia-reoxygenation. Am J Physiol 1991;261:G602–G607.
  • Lentsch AB, Yoshidone H, Cheadle WG, Miller FN, Edwards MJ. Chemokine involvement in hepatic ischemia/reperfusion injury in mice: roles for macrophage inflammatory protein-2 and Kupffer cells. Hepatology 1998;27: 1172–1177.
  • Shigeki A, Masayuki I. Physiological role of sinusoidal endothelial cells and Kupffer cells and their implication in the pathogenesis of liver injury. J Hepatobiliary Pancreat Surg 2000;7:40–48.
  • Imamura H, Sutto F, Brault A, Huet PM. Role of Kupffer cells in cold ischemia/reperfusion injury of rat liver. Gastroenterology 1995;109:189–197.
  • Teoh NC, Farell GC. Hepatic ischemia reperfusion injury: pathogenic mechanisms and basis for hepatoprotection. J Gastroenterol Hepatol 2003;18:891–902.
  • Gujral RS, Farhood A, Bajt ML, Jaeschke H. Neutrophils aggravate acute liver injury during obstructive cholestasis in bile duct-ligated mice. Hepatology 2003;38:355–363.
  • El-Benna J, Dang PM, Gougerot-Pocidalo MA. Priming of the neutrophil NADPH oxidase activation: role of p47 phox phosphorylation and NOX2 mobilization to the plasma membrane. Semin Immunopathol 2008;30:279–289.
  • Jaeschke H, Lemasters JJ. Apoptosis versus oncotic necrosis in hepatic ischemia/reperfusion injury. Gastroenterology 2003;125:1246–1257.
  • Vardanian AJ, Busuttil RW, Kupiec-Weglinski JW. Molecular mediators of liver ischemia and reperfusion injury: a brief review. Mol Med 2008;14:337–345.
  • Hasegawa T, Malle E, Farhood A, Jaeschke H. Generation of hypochloritemodified proteins by neutrophils during ischemia–reperfusion injury in rat liver: attenuation by ischemic preconditioning. Am J Physiol Gastrointest Liver Physiol 2005;289:G760–G767.
  • Clemens MG. Nitric oxide in liver injury. Hepatology 1999;30:1–5.
  • Farzaneth-Far R, Moore K. Nitric oxide and the liver. Liver 2001;21:161–174.
  • Moncada S, Erusalimsky JD. Does nitric oxide modulate mitochondrial energy generation and apoptosis?Nature 2002;3:214–219.
  • Ferdinandy P, Schulz R. Nitric oxide, superoxide, and peroxynitrite in myocardial ischaemia-reperfusion injury and preconditioning. Br J Pharmacol 2003;138:532–543.
  • Stamler JS. Redox signalling: nitrosylation and related target interactions of nitric oxide. Cell 1994;78:931–936.
  • MacMillan-Crow LA, Crow JP, Thompson JA. Peroxynitritemediated inactivation of Manganese Superoxide Dismutase involves nitration and oxidation of critical tyrosine residues. Biochemistry 1998;37:1613–1622.
  • Koneru B, Fisher A, He Y, Klein KM, Skurnick J, Wilson DJ, et al. Ischemic preconditioning in deceased donor liver transplantation: a prospective randomized clinical trial of safety and efficacy. Liver Transpl 2005;11:196–202.
  • 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.
  • Nardo B, Caraceni P, Pasini P, Domenicali M, Catena F, Cavallari G, et al. Increased generation of reactive oxygen species in isolated rat fatty liver during postischemic reoxygenation. Transplantation 2001;71:1816–1820.
  • Massip-Salcedo M, Roselló-Catafau J, Prieto J, Avíla MA, Peralta C. The respomse of the hepatocyte to ischemia. Liver Int 2007;27:6–16.
  • Caraceni P, Domenicali M, Vendemiale G, Grattagliano I, Pertosa A, Nardo B, et al. The reduced tolerance of rat fatty liver to ischemia reperfusion is associated with mitochondrial oxidative injury. J Surg Res 2005;124: 160–168.
  • Serafín A, Roselló-Catafau J, Prats N, Xaus C, Gelpí E, Peralta C. Ischemic preconditioning increases the tolerance of Fatty liver to hepatic ischemia-reperfusion injury in the rat. Am J Pathol 2002;161:587–601.
  • Polat KY, Aydinli B, Polat O, Aydin U, Yazici P, Ozturk G, et al. The protective effect of aprotinin and alpha-tocopherol on ischemia-reperfusion injury of the rat liver. Transplant Proc 2008;40:63–68.
  • Nakano H, Nagasaki H, Barama A, Boudjema K, Jaeck D, Kumada K, et al. The effects of N-acetylcysteine and anti-intercellular adhesion molecule-1 monoclonal antibody against ischemiareperfusion injury of the rat steatotic liver produced by a choline-methionine-deficient diet. Hepatology 1997;26:670–678.
  • Mármol F, Sánchez J, López D, Martínez N, Xaus C, Peralta C, et al. Role of oxidative stress and adenosine stress and adenosine nucleotides in the liver of aging rats. Physiol Res 2010;59:553–560.
  • Theodoraki K, Arkadopoulos N, Nastos C, Vassiliou I, Karmaniolou I, Smyrniotis V. Small liver remnants are more vulnerable to ischemia/reperfusion injury after extended hepatectomies: a case-control study. World J Surg 2012; 36:2895–2900.
  • Franco-Gou R, Roselló-Catafau J, Casillas-Ramirez A, Massip-Salcedo M, Rimola A, Calvo N, et al. How ischaemic preconditioning protects small liver grafts. J Pathol 2006; 208:62–73.
  • Kobayashi T, Sato Y, Yamamoto S, Takeishi T, Hirano K, Watanabe T, et al. Augmentation of heme oxygenase-1 expression in the graft immediately after implantation in adult living-donor liver transplantation. Transplantation 2005;79:977–980.
  • de Rougemont O, Lehmann K, Clavien PA. Preconditioning, organ preservation, and postconditioning to prevent ischemia–reperfusion injury to the liver. Liver Transpl 2009; 15:1172–1182.
  • Carini R, Albano E. Recent insights on the mechanisms of liver preconditioning. Gastroenterology 2003;125: 1480–1491.
  • Serafin A, Fernandez-Zabalegui L, Prats N, Wu Z, Rosello-Catafau J, Peralta C. Ischemic preconditioning: tolerance to hepatic ischemia-reperfusion injury. Histol Histopathol 2004;19:281–289.
  • Nakayama H, Yamamoto Y, Kume M, Yamagami K, Yamamoto H, Kimoto S, et al. Pharmacologic stimulation of adenosine A2 receptor supplants ischemic preconditioning in providing ischemic tolerance in rat livers. Surgery 1999; 126:945–954.
  • Gerbes AL, Vollmar AM, Kiemer AK, Bilzer M. The guanylate cyclasecoupled natriuretic peptide receptor: a new target for prevention of cold ischemia–reperfusion damage of the rat liver. Hepatology 1998;28:1309–1317.
  • Bilzer M, Jaeschke H, Vollmar AM, Paumgartner G, Gerbes AL. Prevention of Kupffer cellinduced oxidant injury in rat liver by atrial natriuretic peptide. Am J Physiol 1999;276:G1137–G1144.
  • Lv X, Yang L, Tao K, Liu Y, Yang T, Chen G, et al. Isoflurane preconditioning at clinically relevant doses induce protective effects of heme oxygenase-1 on hepatic ischemia reperfusion in rats. BMC Gastroenterol 2011;11:31.
  • Beck-Schimmer B, Breitenstein S, Urech S, De Conno E, Wittlinger M, Puhan M, et al. A randomized controlled trial on pharmacological preconditioning in liver surgery using a volatile anesthetic. Ann Surg 2008;248:909–918.
  • Zhang L, Huang H, Cheng J, Liu J, Zhao H, Vizcaychipi MP, Ma D. Pre-treatment with isoflurane ameliorates renal ischemic-reperfusion injury in mice. Life Sci 2001;88: 1102–1107.
  • Guo JY, Yang T, Sun XG, Zhou NY, Li FS, Long D, et al. Ischemic postconditioning attenuates liver warm ischemia-reperfusion injury through Akt-eNOS-NO-HIF pathway. J Biomed Sci 2001;18:79.
  • Klaassen CD, Reisman SA. Nrf2 the rescue: effects of the antioxidative/electrophilic response on the liver. Toxicol Appl Pharmacol 2010;244:57–65.
  • Kensler TW, Wakabayashi N, Biswal S. Cell survival responses to environmental stresses via the Keap1–Nrf2– ARE pathway. Annu Rev Pharmacol Toxicol 2007;47: 89–116.
  • Baird L, Dinkova-Kostova AT. The cytoprotective role of the Keap1–Nrf2 pathway. Arch Toxicol 2011;85:241–272.
  • Franssen C, Defralgne JO, Detry O, Pincernail J, Deby C, Lamy M. Antioxidant defense and free radical production in a rabbit model of kidney ischemia-reperfusion. Transplant Proc 1995;27:2880–2883.
  • Zhang Y, Gu J, Zhao L, He L, Qian W, Wang J, et al. Complete elimination of colorectal tumor xenograft by combined manganese superoxide dismutase with tumor necrosis factor-related apoptosis-inducing ligand gene virotherapy. Cancer Res 2006;66:4291–4298.
  • Winterbourn CC, Stern A. Human red cells scavenge extracellular hydrogen peroxide and inhibit formation of hypochlorous acid and hydroxyl radical. J Clin Invest 1987;80: 1486–1491.
  • He SQ, Zhang YH, Venugopal SK, Dicus CW, Perez RV, Ramsamooj R, et al. Delivery of antioxidative enzyme genes protects against ischemia/reperfusion-induced liver injury in mice. Liver Transpl 2006;12:1869–1879.
  • Luedde T, Trautwein C. The role of oxidative stress and antioxidant treatment in liver surgery and transplantation. Liver Transpl 2006;12:1733–1735.
  • Atalla SL, Toledo-Pereyra LH, MacKenzie GH, Cederna JP. Influence of oxygen-derived free radical scavengers on ischemic livers. Transplantation 1985;40:584–590.
  • 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.
  • 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.
  • Lambotte L, d’Udekem Y, Amrani M, Taper H. Free radicals and liver ischemia-reperfusion injury. Transplant Proc 1988; 20:977.
  • Wu J, Danielsson A, Zern MA. Toxicity of hepatotoxins: new insights into mechanisms and therapy. Expert Opin Investig Drugs 1999;8:585–607.
  • Arteel GE. Oxidants and antioxidants in alcohol-induced liver disease. Gastroenterology 2003;124:778–790.
  • He SQ, Zhang YH, Venugopal SK, Dicus CW, Perez RV, Ramsamooj R, et al. Delivery of antioxidative enzyme genes protects against ischemia/reperfusion-induced liver injury in mice. Liver Transpl 1996;12:1869–1879.
  • Fan C, Zwacka RM, Engelhardt JF. Therapeutic approaches for ischemia/reperfusion injury in the liver. J Mol Med 1999;77:577–592.
  • Mari M, Bai J, Cederbaum AI. Adenovirus-mediated overexpression of catalase in the cytosolic or mitochondrial compartment protects against toxicity caused by glutathione depletion in HepG2 cells expressing CYP2E1. J Pharmacol Exp Ther 2002;301:111–118.
  • 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.
  • 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.
  • 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;29:756–763.
  • Yuan L, Kaplowitz N. Glutathione in liver diseases and hepatotoxicity. Mol Aspects Med 2009;30:29–41.
  • Jegatheeswaran S, Siriwardena AK. Experimental and clinical evidence for modification of hepatic ischaemia– reperfusion injury by N-acetylcysteine during major liver surgery. HPB (Oxford) 2011;13:71–78.
  • Smyrniotis V, Arkadopoulos N, Kostopanagiotou G, Theodoropoulos T, Theodoraki K, Farantos C, et al. Attenuation of ischemic injury by N-acetylcysteine preconditioning of the liver. J Surg Res 2005;129:31–37.
  • Nagasaki H, Nakano H, Boudjema K, Jaeck D, Alexandre E, Baek Y, et al. Efficacy of preconditioning with N- acetylcysteine against reperfusion injury after prolonged cold ischaemia in rats liver in which glutathione had been reduced by buthionine sulphoximine. Eur J Surg 1998; 164:139–146.
  • Fusai G, Glantzounis GK, Hafez T, Yang W, Quaglia A, Sheth H, et al. N-acetylcysteine ameliorates the late phase of liver ischaemia/reperfusion injury in the rabbit with hepatic steatosis. Clin Sci 2005;109:465–473.
  • Sener G, Tosun O, Sehirli AO, Kaçmaz A, Arbak S, Ersoy Y, Ayanoğlu-Dülger G. Melatonin and N- acetylcysteine have beneficial effects during hepatic ischemia and reperfusion. Life Sci 2003;72:2707–2718.
  • Saito C, Zwingmann C, Jaeschke H. Novel mechanisms of protection against acetaminophen hepatotoxicity in mice by glutathione and Nacetylcysteine. Hepatology 2010;51: 246–254.
  • Liu P, Fisher MA, Farhood A, Smith CW, Jaeschke H. Beneficial effects of extracellular glutathione against endotoxin-induced liver injury during ischemia and reperfusion. Circ Shock 1994;43:64–70.
  • Knight TR, Ho YS, Farhood A, Jaeschke H. Peroxynitrite is a critical mediator of acetaminophen hepatotoxicity in murine livers: protection by glutathione. J Pharmacol Exp Ther 2002;303:468–475.
  • 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.
  • 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: S390–S392.
  • Weigand MA, Plachky J, Thies JC, Spies-Martin D, Otto G, Martin E, Bardenheuer HJ. Nacetylcysteine 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.
  • 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.
  • 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;239:220–231.
  • Cho WH, 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.
  • Wendel A, Cikryt P. The level and half-life of glutathione in human plasma. FEBS Lett 1980;120:209–211.
  • Takeda A, Onodera H, Sugimoto A, Itoyama Y, Kogure K, Shibahara S. Increased expression of heme oxygenase mRNA in rat brain following transient forebrain ischemia. Brain Res 1994;666:120–124.
  • Maines MD, Mayer RD, Ewing JF, McCoubrey WK Jr. Induction of kidney heme oxygenase-1 (HSP32) mRNA and protein by ischemia/reperfusion: possible role of heme as both promotor of tissue damage and regulator of HSP32. J Pharmacol Exp Ther 1993;264:457–462.
  • Pachori AS, Melo LG, Zhang L, Solomon SD, Dzau VJ. Chronic recurrent myocardial ischemic injury is significantly attenuated by pre-emptive adeno-associated virus heme oxygenase-1 gene delivery. J Am Coll Cardiol 2006; 47:635–643.
  • McCarter SD, Badhwar A, Scott JR, Akyea TG, Bihari A, Dungey AA, et al. Remote liver injury is attenuated by adenovirus-mediated gene transfer of heme oxygenase-1 during the systemic inflammatory response syndrome. Microcirculation 2004;11:587–595.
  • Sass G, Soares MC, Yamashita K, Seyfried S, Zimmermann WH, Eschenhagen T, et al. Heme oxygenase-1 and its reaction product, carbon monoxide, prevent inflammation-related apoptotic liver damage in mice. Hepatology 2003;38: 909–918.
  • Amersi F, Buelow R, Kato H, Ke B, Coito AJ, Shen XD, et al. Upregulation of heme oxygenase-1 protects genetically fat Zucker rat livers from ischemia/reperfusion injury. J Clin Invest 1999;104:1631–1639.
  • Amersi F, Shen XD, Anselmo D, Melinek J, Iyer S, Southard DJ, et al. Ex vivo exposure to carbon monoxide prevents hepatic ischemia/reperfusion injury through p38 MAP kinase pathway. Hepatology 2002;35:815–823.
  • Massip-Salcedo M, Casillas-Ramirez A, Franco-Gou R, Bartrons R, Ben Mosbah I, Serafin A, et al. Heat shock proteins and mitogen-activated protein kinases in steatotic livers undergoing ischemia-reperfusion: some answers. Am J Pathol 2006;168:1474–1785.
  • Tsuchihashi S, Fondevila C, Kupiec-Weglinski JW. Heme oxygenase system in ischemia and reperfusion injury. Ann Transplant 2004;9:84–87.
  • Rigotti A. Absorption, transport, and tissue delivery of vitamin E. Mol Aspects Med 2007;28:423–436.
  • Blatt DH, Leonard SW, Traber MG. Vitamin E kinetics and the function of tocopherol regulatory proteins. Nutrition 2001;17:799–805.
  • McCall MR, Frei B. Can antioxidant vitamins materially reduce oxidative damage in humans?Free Radic Biol Med 1999;26:1034–1053.
  • Chow B, Jacobson JM. Biologically inspired molecular assembly lines. Bt Technol J 2004;22:270–277.
  • Martin A, Janigian D, Shukitt-Hale B, Prior RL, Joseph JA. Effect of vitamin E intake on levels of vitamins E and C in the central nervous system and peripheral tissues: implications for health recommendations. Brain Res 1999;845: 50–59.
  • 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.
  • 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.
  • 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.
  • 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.
  • Ricciarelli R, Zingg JM, Azzi A. The 80th anniversary of vitamin E: beyond its antioxidant properties. Biol Chem 2002;383:457–465.
  • Vardareli E, Saricam T, Koken T, Degirmenci I, Aral E, Erenoglu E. The effect of alphatocopherol and pentoxyfilline on ischemia-reperfusion induced liver injury in rats. Hepatogastroenterology 1998;45:1505–1508.
  • Eum HA, Lee SH, Lee SM. Trolox C ameliorates hepatic drug metabolizing dysfunction after ischemia/reperfusion. Arch Pharm Res 2002;25:940–945.
  • Koga H, Hagiwara S, Inomata M, Kusaka J, Asai N, Oyama M, et al. Vitamin E derivative ETSGS reduces liver ischemia–reperfusion injury in rats. J Surg Res 2011; 75:118–122.
  • 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.
  • 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.
  • Hassan-Khabbar S, Cottart CH, Wendum D, Vibert F, Clot JP, Savouret JF, et al. Postischemic treatment by trans-resveratrol in rat liver ischemia–reperfusion: a possible strategy in liver surgery. Liver Transpl 2008;14:451–459.
  • Gedik E, Girgin S, Ozturk H, Obay BD, Ozturk H, Buyukbayram H. Resveratrol attenuates oxidative stress and histological alterations induced by liver ischemia/reperfusion in rats. World J Gastroenterol 2008;14:7101–7106.
  • Sehirli O, Ozel Y, Dulundu E, Topaloglu U, Ercan F, Sener G. Grape seed extract treatment reduces hepatic ischemia–reperfusion injury in rats. Phytother Res 2008; 22:43–48.
  • Liang R, Nickkholgh A, Kern M, Schneider H, Benzing S, Zorn M, et al. Green tea extract ameliorates reperfusion injury to rat livers after warm ischemia in a dosedependent manner. Mol Nutr Food Res 2011;55:855–863.
  • Cheng F, Li Y, Feng L, Li S. Effects of tetrandine on ischemia/reperfusion injury in mouse liver. Transplant Proc 2008;40:2163–2166.
  • 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.
  • 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 2002;48:134–141.
  • 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.
  • Kantrow SP, Tatro LG, Piantadosi CA. Oxidative stress and adenine nucleotide control of mitochondrial permeability transition. Free Radic Biol Med 2000;28:251–260.
  • Theruvath TP, Snoddy MC, Zhong Z, Lemasters JJ. Mitochondrial permeability transition in liver ischemia and reperfusion: role of c-Jun N-terminal kinase 2. Transplantation 2008;85:1500–1504.
  • Theruvath TP, Zhong Z, Pediaditakis P, Ramshesh VK, Currin RT, Tikunov A, et al. Minocycline and N-methyl- 4-isoleucine cyclosporin (NIM811) mitigate storage/reperfusion injury after rat liver transplantation through suppression of the mitochondrial permeability transition. Hepatology 2008;1:236–246.
  • Zhong Z, Ramshesh VK, Rehman H, Currin RT, Sridharan V, Theruvath TP, et al. Activation of the oxygensensing signal cascade prevents mitochondrial injury after mouse liver ischemia–reperfusion. Am J Physiol Gastrointest Liver Physiol 2008;95:G823–G832.
  • 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;469:145–152.
  • Okatani Y, Wakatsuki A, Enzan H, Miyahara Y. Edaravone protects against ischemia/reperfusion-induced oxidative damage to mitochondria in rat liver. Eur J Pharmacol 2003; 465:163–170.
  • Hanawa N, Shinohara M, Saberi B, Gaarde WA, Han D, Kaplowitz N. Role of JNK translocation to mitochondria leading to inhibition of mitochondria bioenergetics in acetaminophen-induced liver injury. J Biol Chem 2008;283: 13565–13577.
  • Saito C, Lemasters JJ, Jaeschke H. c-Jun N-terminal kinase modulates oxidant stress and peroxynitrite formation independent of inducible nitric oxide synthase in acetaminophen hepatotoxicity. Toxicol Appl Pharmacol 2010; 246:8–17.
  • Ward PA, Cunningham TW, McCulloch KK, Johnson KJ. Regulatory effects of adenosine and adenine nucleotides on oxygen radical responses of neutrophils. Lab Invest 1988; 58:438–447.
  • Mullan K, Bullough D. Harnessing an endogenous cardioprotective mechanism: Cellular sources and sites of action of adenosine. J Moll Cell Cardiaol 1995;27: 1041–1054.
  • Jimenez-Castro MB, Casillas-Ramirez A, Massip-Salcedo M, Elias-Miró M, Serafin A, Rimola A, et al. Cyclic adenosine 3’,5’-monophosphate in rat steatotic liver transplantation. Liver Transpl 2011;17:1099–1110.
  • Alfany-Fernandez I, Casillas-Ramirez A, Bintanel-Morcillo M, Brosnihan KB, Ferrario CM, Serafin A, et al. Therapeutic targets in liver transplantation: angiotensin II in nonsteatotic grafts and angiotensin-(1-7) in steatotic grafts. Am J Transplant 2009;9:439–451.
  • Massip-Salcedo M, Zaouali MA, Padrissa-Altés S, Casillas-Ramirez A, Rodés J, Roselló-Catafau J, Peralta C. Activation of peroxisome proliferator-activated receptor-alpha inhibits the injurious effects of adiponectin in rat steatotic liver undergoing ischemia-reperfusion. Hepatology 2008;47:461–472.
  • Serafín A, Roselló-Catafau J, Prats N, Gelpí E, Rodés J, Peralta C. Ischemic preconditioning affects interleukin release in fatty livers of rats undergoing ischemia/reperfusion. Hepatology 2004;39:688–698.
  • Ben Mosbah I, Alfany-Fernández I, Martel C, Zaouali MA, Bintanel-Morcillo M, Rimola A, et al. Endoplasmic reticulum stress inhibition protects steatotic and non-steatotic livers in partial hepatectomy under ischemia-reperfusion. Cell Death Dis 2010;1:e52.
  • Ramalho FS, Alfany-Fernandez I, Casillas-Ramirez A, Massip-Salcedo M, Serafín A, Rimola A, et al. Are angiotensin II receptor antagonists useful strategies in steatotic and nonsteatotic liver in conditions of partial hepatectomy under ischemia/reperfusion?J Pharmacol Exp Ther 2009;329:130–140.
  • Liu PG, He SQ, Zhang YH, Wu J. Protective effects of apocynin and allopurinol on ischemia/reperfusion-induced liver injury in mice. World J Gastroenterol 2008;14: 2832–7283.
  • Peralta C, Xaus C, Bartrons R, Leon OS, Gelpi E, Roselló-Catafau J. Effect of ozone treatment on reactive oxygen species and adenosine production during hepatic ischemia-reperfusion. Free Radic Res 2000;33: 595–605.
  • Shiotani S, Shimada M, Taketomi A, Soejima Y, Yoshizumi T, Hashimoto K, et al. Rho-kinase as a novel gene therapeutic target in treatment of cold ischemia/reperfusion-induced acute lethal liver injury: effect on hepatocellular NADPH oxidase system. Gene Ther 2007;14:1425–1433.
  • Park SW, Ueno R, Hayaishi O. Prostaglandin synthesizing enzyme activities of hepatocytes and non-hepatocytes in rat liver as a function of age. Biochem Int 1986;13: 827–834.
  • Hossain MA, Wakabayashi H, Izuishi K, Okano K, Yachida S, Maeta H. The role of prostaglandins in liver ischemia-reperfusion injury. Curr Pharm Des 2006;12: 2935–2951.
  • Portakal O, Inal-Erden M. Effects of pentoxifylline and coenzyme Q10 in hepatic ischemia/reperfusion injury. Clin Biochem 1999;32:461–466.
  • 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.
  • 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.
  • 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.
  • 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.
  • 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.
  • 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.
  • Jiménez-Castro MB, Elias-Miró M, Mendes-Braz M, Lemoine A, Rimola A, Rodés J, et al. Tauroursodeoxycholic Acid Affects PPARγ and TLR4 in Steatotic Liver Transplantation. Am J Transplant 2012;12: 3257–3271.

Reprints and Corporate Permissions

Please note: Selecting permissions does not provide access to the full text of the article, please see our help page How do I view content?

To request a reprint or corporate permissions for this article, please click on the relevant link below:

Academic Permissions

Please note: Selecting permissions does not provide access to the full text of the article, please see our help page How do I view content?

Obtain permissions instantly via Rightslink by clicking on the button below:

If you are unable to obtain permissions via Rightslink, please complete and submit this Permissions form. For more information, please visit our Permissions help page.