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Research Article

Role of Reactive Oxygen Species in Hepatic Ischemia-Reperfusion Injury and Preconditioning

Hartmut Jaeschke Liver Research Institute and Department of Pharmacology, University of Arizona, Tucson, Arizona, USA
Pages 127-140 | Published online: 09 Jul 2009

  • Nordstrom G, Seeman T, Hasselgren PO. Beneficial effect of allopurinol in liver ischemia. Surgery. 1985;97:679-684
  • Atalla SL, Toledo-Pereyra LH, MacKenzie GH, Cederna JP. Influence of oxygen-derived free radical scavengers on ischemie livers. Transplantation. 1985; 40:584-590.
  • Adkison D, Hollwarth ME, Benoit JN, Parks DA, McCord JM, Granger DN. Role of free radicals in ischemia-reperfusion injury to the liver. Acta Physiol Scand Suppl. 1986;548:101-107.
  • Jaeschke H. Molecular mechanisms of hepatic ischemiareperfusion injury and preconditioning. Am J Physiol. 2003;284:615-626.
  • Jaeschke H. Reperfusion injury after warm ischemia or cold storage of the liver: Role of apoptotic cell death. Transplant Proc. 2002;34:2656-2658.
  • Menger MD, Vollmar B. Role of microcirculation in transplantation. Microcirculation. 2000;7:291-306.
  • Lichtman SN, Lemasters JJ. Role of cytokines and cytokine-producing cells in reperfusion injury to the liver. Semin Liver Dis. 1999;19:171-187.
  • Okaya T, Lentsch AB. Cytokine cascades and the hepatic inflammatory response to ischemia and reperfusion. J Invest Surg. 2003;16:141-147.
  • Rudiger HA, Graf R, Clavien PA. Liver ischemia: A plea for apoptosis as a central mechanism of injury. J Invest Surg. 2003;16:149-159.
  • Jaeschke H. Reactive oxygen and ischemia-reperfusion injury of the liver. Chem Biol Interact. 1991;79:115-136.
  • Harrison R. Structure and function of xanthine oxidoreductase: Where are we now? Free Radical Biol Med. 2002;33:774-797.
  • Engerson TD, McKelvey TG, Rhyne DB, Boggio EB, Snyder SJ, Jones HP. Conversion of xanthine dehydrogenase to oxidase in ischemic rat tissues. J Clin Invest. 1987;79:1564-1570.
  • Godin DV, Bhimji S. Effects of allopurinol on myocardial ischemic injury induced by coronary artery ligation and reperfusion. Biochem Pharmacol. 1987;36:2101-2107.
  • Jaeschke H. Glutathione disulfide formation and oxidant stress during acetaminophen-induced hepatotoxicity in mice in vivo: The protective effect of allopurinol. J Pharmacol Exp Ther. 1990;255:935-941.
  • 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, Smith CV, Mitchell JR. Reactive oxygen species during ischemia-reflow injury in isolated perfused rat liver. J Clin Invest. 1988;81:1240-1246.
  • Metzger J, Dore SP, Lauterburg BH. Oxidant stress during reperfusion of ischemie liver: No evidence for a role of xanthine oxidase. Hepatology. 1988;8:580-584.
  • Metzger J, Lauterburg BH. Effect of allopurinol on oxidant stress and hepatic function following ischemia and reperfusion in the rat. Liver. 1988;8:344-349.
  • Jaeschke H. Vascular oxidant stress and hepatic Ischemia/reperfusion injury. Free Radical Res Commun. 1991:12-13:737-743.
  • Jaeschke H, Farhood A. Neutrophil and Kupffer cellinduced oxidant stress and ischemia-reperfusion injury in rat liver. Am J Physiol. 1991;260:G355-G362.
  • Jaeschke H. Xanthine oxidase-induced oxidant stress during hepatic ischemia-reperfusion: Are we coming full circle after 20 years? Hepatology. 2002;36:761763.
  • Nakano M, Sugano M,Teresaki M, MorimotoT, Mashima S, Mitsuyoshi A, Sasaki H, Kumada K, Ozawa K. Preserved mitochondrial function by allopurinol despite deteriorated hemodynamics in warm ischemia-damaged canine liver. Res Exp Med. 1992;192:389-399.
  • Knight TR, Kurtz A, Bajt ML, Hinson JA, Jaeschke H. Vascular and hepatocellular peroxynitrite formation during acetaminophen toxicity: Role of mitochondrial oxidant stress. ToxicolSci. 2001;62:212-220.
  • Knight TR, Jaeschke H. Acetaminophen-induced inhibition of Fas receptor-mediated liver cell apoptosis: Mitochondrial dysfunction versus glutathione depletion. Toxicol Appl Pharmacol. 2002;181:133-141.
  • Jaeschke H, Mitchell JR. Mitochondria and xanthine oxidase both generate reactive oxygen species in isolated perfused rat liver after hypoxic injury. Biochem Biophys Res Commun. 1989;160:140-147.
  • Jaeschke H, Smith CV, Mitchell JR. Hypoxic damage generates reactive oxygen species in isolated perfused rat liver. Biochem Biophys Res Commun. 1988;150:568574.
  • 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.
  • Caraceni P, Ryu HS, van Thiel DH, Borle AB. Source of oxygen free radicals produced by rat hepatocytes during postanoxic reoxygenation. Biochim Biophys Acta. 1995;1268:249-254.
  • Grattagliano I, Vendemiale G, and Lauterburg BH. Reperfusion injury of the liver: Role of mitochondria and protection by glutathione ester. J Surg Res. 1999;86: 2-8.
  • Kumamoto Y, Suematsu M, Shimazu M, Kato Y, Sano T, Makino N, Hirano Kl, Naito M, Wakabayashi G, lshimura Y, Kitajima M. Kupffer cell-independent acute hepatocellular oxidative stress and decreased bile formation in post-cold-ischemic rat liver. Hepatology. 1999;30:14541463.
  • Jaeschke H, Bautista AP, Spolarics Z, Spitzer JJ. Superoxide generation by Kupffer cells and priming of neutrophils during reperfusion after hepatic ischemia. Free Radical Res Commun. 1991;15:277-284.
  • Nunes FA, Kumar C, Chance B, Brass CA. Chemiluminescent measurement of increased free radical formation after ischemia/reperfusion. Mechanisms of free radical formation in the liver. Dig Dis Sci. 1995;40:10451053.
  • Brass CA, Roberts TG. Hepatic free radical production after cold storage: Kupffer cell-dependent and -independent mechanisms in rats. Gastroenterology. 1995;108:1167-1175.
  • Shibuya H, Ohkohchi N, Seya K, Satomi S. Kupffer cells generate Superoxide anions and modulate reperfusion injury in rat livers after cold preservation. Hepatology. 1997;25:356-360.
  • Rymsa B, Wang JF, de Groot H. O2 release by activated Kupffer cells upon hypoxia-reoxygenation. Am J Physiol. 1991;261:G602-G607.
  • Jaeschke H, Farhood A, Bautista AP, Spolarics Z, Spitzer JJ. Complement activates Kupffer cells and neutrophils during reperfusion after hepatic ischemia. Am J Physiol. 1993;264:G801-G809.
  • Jaeschke H, Farhood A, Smith CW. Contribution of complement-stimulated hepatic macrophages and neutrophils to endotoxin-induced liver injury in rats. Hepatology. 1994;19:973-979.
  • Liu P, Vonderfecht SL, Fisher MA, McGuire GM, Jaeschke H. Priming of phagocytes for reactive oxygen production during hepatic ischemia and reperfusion increases the susceptibility for endotoxin-induced liver injury. Ore Shock. 1994;43:9-17.
  • Liu P, McGuire GM, Fisher MA, Farhood A, Smith CW, Jaeschke H. Activation of Kupffer cells and neutrophils for reactive oxygen formation is responsible for endotoxin-enhanced liver injury after hepatic ischemia. Shock. 1995;3:56-62.
  • Jaeschke H, Farhood A. Kupffer cell activation after noflow ischemia versus hemorrhagic shock. Free Radical BIoI Med. 2002;33:210-219.
  • Rensing H, Jaeschke H, Bauer I, Patau C, Datene V, Pannen BH, Bauer M. Differential activation pattern of redox-sensitive transcription factors and stress-inducible dilator systems heme oxygenase-1 and inducible nitric oxide synthase in hemorrhagic and endotoxic shock. Crit CaK Med. 2001;29:1962-1971.
  • Witthaut R, Farhood A, Smith CW, Jaeschke H. Complement and tumor necrosis factor-a contribute to Mac1 (CD11b/CD18) upregulation and systemic neutrophil activation during endotoxemia in vivo. J Leukocyte BioI. 1994;55:105-111.
  • Colletti LM, Remick DG, Burtch GD, Kunkel SL, Strieter RM, Campbell DA Jr. Role of tumor necrosis factor-alpha in the pathophysiologic alterations after hepatic ischemia/reperfusion injury in the rat. J Clin Invest. 1990;85:1936-1943.
  • Lentsch AB, Yoshidome H, Cheadle WG, Miller FN, Edwards MJ. Chemokine involvement in hepatic ischemia/reperfusion injury in mice: Roles for macrophage inflammatory protein-2 and KC. Hepatology. 1998;27:507-512.
  • Colletti LM, Kunkel SL, Walz A, Burdick MD, Kunkel RG, Wilke CA, Strieter RM. The role of cytokine networks in the local liver injury following hepatic ischemia/reperfusion in the rat. Hepatology. 1996;23:506-514.
  • Bautista AP, Spitzer JJ. Platelet activating factor stimulates and primes the liver, Kupffer cells and neutrophils to release Superoxide anion. Free Radical Res Commun. 1992;17:195-209.
  • Bajt, ML, Farhood A, Jaeschke H. Effects of CXC chemokines on neutrophil activation and sequestration in the hepatic vasculature. Am J Physiol. 2001;281 :G1188-G1195.
  • Hughes H, Farhood A, Jaeschke H. The role of leukotriene B4 in the pathogenesis of hepatic ischemiareperfusion injury in the rat. Prostaglandins Leukotrienes Essential Fatty Acids 1992;45:113-119.
  • Curzio M, Esterbauer H, Di Mauro C, Cecchini G, Dianzani MU. Chemotactic activity of the lipid peroxidation product 4-hydroxynonenal and homologous hydroxyalkenals. BioI Chem Hoppe Seyler. 1986;367:321329.
  • Liu P, Vonderfecht SL, McGuire GM, Fisher MA, Farhood A, Jaeschke H. The 21-aminosteroid tirilazad mesylate protects in a model of endotoxin shock and acute liver failure in rats. J Pharmacol Exp Ther. 1994;271:438445.
  • Jaeschke H, Farhood A, Smith CW. Neutrophils contribute to ischemia-reperfusion injury in rat liver in vivo. FASEBJ.1990;4:3355-3359.
  • Chosay JG, Essani NA, Dunn CJ, Jaeschke H. Neutrophil margination and extravasation in sinusoids and venules of the liver during endotoxin-induced injury. Am J Physiol. 1997;272:G1195-G1200.
  • Jaeschke H, and Smith CW. Mechanisms of neutrophilinduced parenchymal cell injury. J Leukocyte Biol. 1997;61:647-653.
  • Essani NA, Fisher MA, Farhood A, Manning AM, Smith CW, Jaeschke H. Cytokine-induced hepatic intercellular adhesion molecule-1 (ICAM-1) mRNA expression and its role in the pathophysiology of murine endotoxin shock and acute liver failure. Hepatology. 1995;21:16321639.
  • Essani NA, Bajt ML, Vonderfecht SL, Farhood A, Jaeschke H. Transcriptional activation of vascular cell adhesion molecule-1 (VCAM-1) gene in vivo and its role in the pathophysiology of neutrophil-induced liver injury in murine endotoxin shock. J lmmunol. 1997;158:59415948.
  • Jaeschke H, Fisher MA, Lawson JA, Simmons CA, Farhood A, Jones DA. Activation of caspase 3 (CPP32)-like proteases is essential for TNF-alphainduced hepatic parenchymal cell apoptosis and neutrophil-mediated necrosis in a murine endotoxin shock model. J lmmunol. 1998;160:34803486.
  • Lawson JA, Fisher MA, Simmons CA, Farhood A, Jaeschke H. Parenchymal cell apoptosis as a signal for sinusoidal sequestration and transendothelial migration of neutrophils in murine models endotoxin- and Fas-antibody-mediated liver injury. Hepatology. 1998; 28:761-767.
  • Shappell SB, Toman C, Anderson DC, Taylor AA, Entman ML, Smith CW. Mac-1 (CD11b/CD18) mediates adherence-dependent hydrogen peroxide production by human and canine neutrophils. J lmmunol. 1990;144:2702-2711.
  • 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 Leukocyte BIoI. 1992;52:377-382.
  • Jaeschke H, Farhood A, Bautista AP, Spolarics Z, Spitzer JJ, Smith CW. Functional inactivation of neutrophils with a Mac-1 (CD11b/CD18) monoclonal antibody protects against ischemia-reperfusion injury in rat liver. Hepatology 1993;17:915-923.
  • Li JM, Shah AM. Differential NADPH- versus NADHdependent Superoxide production by phagocyte-type endothelial cell NADPH oxidase. Cardiovasc Res 2001;52:477-486.
  • Ozaki M, Deshpande SS, Angkeow P, Bellan J, Lowenstein CJ, DinauerMC, Goldschmidt-Clermont PJ, Irani K. Inhibition of the Rac1 GTPase protects against nonlethal ischemia/reperfusion-induced necrosis and apoptosis in vivo. FASEBJ. 2000;14:418-429.
  • Wang Y, Mathews WR, Guido D, Jaeschke H. The 21aminosteroid tirilazad mesylate protects against liver injury via membrane stabilization not inhibition of lipid peroxidation. J Pharmacol Exp Ther. 1996;277:714720.
  • Wendel A, Jaeschke H, Gloger M. Drug-induced lipid peroxidation in mice II: Protection against paracetamol-induced liver necrosis by intravenous Iiposomally entrapped glutathione. Biochem Pharmacol. 1982;31:3601-3605.
  • Jaeschke H, Kleinwaechter C, Wendel A. The role of acrolein in allyl alcohol-induced lipid peroxidation and liver cell damage in mice. Biochem Pharmacol 1987;36:51-57.
  • Jaeschke H, Kleinwaechter C, Wendel A. NADHdependent reductive stress and ferritin-bound iron in allyl alcohol-induced lipid peroxidation in vivo: The protective effect of vitamin E. Chem BIoI Interact 1992;81:5768.
  • Mathews WR, Guido DM, Fisher MA, Jaeschke H. Lipid peroxidation as molecular mechanism of liver cell injury during reperfusion after ischemia. Free Radical BioI Med. 1994;16:763-770.
  • Mavier P, Preaux A-M, Guigui B, Lescs MC, Zafrani ES, Dhumeaux D. In vitro toxicity of polymorphonuclear neutrophils to rat hepatocytes: Evidence for a proteinasemediated mechanism. Hepatology. 1988;8:254-258.
  • Harbrecht BG, Billiar TR, Curran RD, Stadler J, Simmons RL. Hepatocyte injury by activated neutrophils in vitro is mediated by proteases. Ann Surg 1993;218:120128.
  • Ganey PE, Bailie MB, VanCise S, Colligan ME, Madhukar BV, Robinson JP, Roth RA. Activated neutrophils from rat injured isolated hepatocytes. Lab Invest. 1994;70:53-60.
  • Weiss SJ. Tissue destruction by neutrophils. N Engl J Med. 1989:320:365-376.
  • Jaeschke H, Ho Y-S, Fisher MA, Lawson JA, Farhood A. Glutathione peroxidase deficient mice are more susceptible to neutrophil-mediated hepatic parenchymal cell injury during endotoxemia: Importance of an intracellular oxidant stress. Hepatology. 1999;29:443-450.
  • Jaeschke H, Farhood A, Smith CW. Neutrophil-induced liver cell injury in endotoxin shock is a CD11b/CD18dependent mechanism. Am J Physiol. 1991;261:G1051G1056.
  • Farhood A, McGuire GM, Manning AM, Miyasaka M, Smith CW, Jaeschke, H. Intercellular adhesion molecule1 (ICAM-1) gene expression and its role in neutrophilinduced ischemia-reperfusion injury in the liver. JLeukocyte Biol. 1995;57:368-374.
  • Jaeschke H. Reactive oxygen and mechanisms of inflammatory liver injury. J Gastroenterol Hepatol. 2000; 15:718-724.
  • Bilzer M, Jaeschke H, Vollmar AM, Paumgartner G, Gerbes AL. Prevention of Kupffer cell-induced injury in rat liver by atrial natriuretic peptide (ANP): A novel endogenous defense mechanism against oxidant injury. Am J Physiol 1999;276:G1137-G1144.
  • 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.
  • Nieminen AL, Saylor AK, Tesfai SA, Herman B, Lemasters JJ. Contribution of the mitochondrial permeability transition to lethal injury after exposure of hepatocytes to f-butylhydroperoxide. Biochem J 1995;307:99106.
  • Kurokawa T, Kobayashi H, Nonami T, Harada A, Nakao A, Sugiyama S, Ozawa T, and Takagi H. Beneficial effects of cyclosporine on postischemic liver injury in rats. Transplantation. 1992;53:308-311.
  • 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.
  • Leducq N, Delmas-Beauvieux MC, Bourdel-Marchasson I, Dufour S, Gallis JL, Canioni P, Diolez P. Mitochondrial and energetic dysfunctions of the liver during normothermic reperfusion: Protective effect of cyclosporine and role of the mitochondrial permeability transition pore. Transplant Proc. 2000;32:479-480.
  • Elimadi A, Settaf A, Morin D, Sapena R, Lamchouri F, Cherrah Y, Tillement JP. Trimetazidine counteracts the hepatic injury associated with ischemia-reperfusion by preserving mitochondrial function. JPharmacolExpTher. 1998;286:23-28.
  • Elimadi A, Sapena R, Settaf A, Le Louet H, Tillement J, Morin D. Attenuation of liver normothermic ischemiareperfusion injury by preservation of mitochondrial functions with S-15176, a potent trimetazidine derivative. Biochem Pharmacol. 2001;62:509-516.
  • Sasaki H, Matsuno T, Tanaka N, Orita K. Activation of apoptosis during the reperfusion phase after rat liver ischemia. Transplant Proc. 1996;28:1908-1909.
  • Kohli V, Selzner M, Madden JF, Bentley RC, Clavien PA. Endothelial cell and hepatocyte deaths occur by apoptosis after ischemia-reperfusion injury in the rat liver. Transplantation. 1999;67:1099-1105.
  • Natori S, Selzner M, Valentino KL, Fritz LC, Srinivasan A, Clavien PA, Gores GJ. Apoptosis of sinusoidal endothelial cells occurs during liver preservation injury by a caspasedependent mechanism. Transplantation. 1999;68:8996.
  • Cursio R, Gugenheim J, Ricci JE, Crenesse D, Rostagno P, Maulon L, Saint-Paul MC, Ferrua B, Auberger AP. A caspase inhibitor fully protects rats against lethal normothermic liver ischemia by inhibition of liver apoptosis. FASEBJ. 1999;13:253-261.
  • Gujral JS, Bucci TJ, Farhood A, Jaeschke H. Mechanism of cell death during warm hepatic ischemia-reperfusion in rats: Apoptosis or necrosis? Hepatology. 2001;33:397405.
  • Lawson JA, Fisher MA, Simmons CA, Farhood A, Jaeschke H. Inhibition of Fas receptor (CD95)-induced hepatic caspase activation and apoptosis by acetaminophen in mice. Toxicol Appl Pharmacol. 1999; 156;179-186.
  • Bajt ML, Lawson JA, Vonderfecht SL, Gujral JS, Jaeschke H. Protection against Fas receptor-mediated apoptosis in hepatocytes and nonparenchymal cells by a caspase8 inhibitor in vivo: Evidence for postmitochondrial processing of caspase-8. Toxicol Sd. 2000;58:109-117.
  • Jaeschke H, Farhood A, Cai SX, Tseng BY, Bajt ML. Protection against TNF-induced liver parenchymal cell apoptosis during endotoxemia by a novel caspase inhibitor in mice. TUX/CO/ Appl Pharmacol. 2000;169:77-83.
  • Bajt ML, Vonderfecht SL, Jaeschke H. Differential protection with inhibitors of caspase-8 and caspase-3 in murine models of TNF and Fas receptor-mediated hepatocellular apoptosis. ToxicolAppI Pharmacol 2001;175:243-252.
  • Kobayashi A, lmamura H, lsobe M, Matsuyama Y, Soeda J, Matsunaga K, Kawasaki S. Mac-1 (CD11b/CD18) and intercellular adhesion molecule-1 in ischemia-reperfusion injury of rat liver. Am J Physlol. 2001;281:G577-G585.
  • Bajt ML, Ho Y-S, Vonderfecht SL, Jaeschke H. Reactive oxygen as modulator of TNF and Fas receptor-mediated apoptosis in vivo: Studies with glutathione peroxidasedeficient mice. Antiox Redox Signal. 2002;4:733-740.
  • Koo A, Komatsu H, Tao G, lnoue M, Guth PH, Kaplowitz N. Contribution of no-reflow phenomenon to hepatic injury after ischemia-reperfusion: Evidence for a role for Superoxide anion. Hepatology. 1991;15:507-514.
  • Schauer RJ, Bilzer M, Kalmuk S, Gerbes AL, Leiderer R, Schildberg FW, Messmer K. Microcirculatory failure after rat liver transplantation is related to Kupffer cell-derived oxidant stress but not involved in early graft dysfunction. Transplantation. 2001;72:1692-1699.
  • lkai I, Chance B, Kumar C. Reactive oxygen inducing vasoconstriction in the isolated perfused rat liver. Free Radical Biol Med. 1994;16:539-545.
  • Clemens MG, Zhang JX. Regulation of sinusoidal perfusion: In vivo methodology and control by endothelins. Semin Liver Dis. 1999;19:383-396.
  • McCuskey RS. Morphological mechanisms for regulating blood flow through hepatic sinusoids. Liver. 2000;20:37.
  • Yokoyama Y, Baveja R, Sonin N, Nakanishi K, Zhang JX, Clemens MG. Altered endothelin receptor subtype expression in hepatic injury after ischemia/reperfusion. Shock. 2000;13:72-78.
  • Vollmar B, Glasz J, Leiderer R, Post S, Menger MD. Hepatic microcirculatory perfusion failure is a determinant of liver dysfunction in warm ischemia-reperfusion. Am J Pathol. 1994;145:1421-1431.
  • Chun K, Zhang J, Biewer J, Ferguson D, Clemens MG. Microcirculatory failure determines lethal hepatocyte injury in ischemic/reperfused rat livers. Shock. 1994;1: 3-9.
  • Janssen-Heininger YM, Poynter ME, Baeuerle PA. Recent advances towards understanding redox mechanisms in the activation of nuclear factor kappa B. Free Radical Biol Med. 2000;28:1317-1327.
  • Karin M, Takahashi T, Kapahi P, Delhase M, Chen Y, Makris C, Rothwarf D, Baud V, Natoli G, Guido F, Li N. Oxidative stress and gene expression: The AP-1 and NF-kappa B connections. Biofactors. 2001 ;15: 87-89.
  • Jaeschke H. Cellular adhesion molecules: Regulation and functional significance in the pathogenesis of liver diseases. Am J Physiol. 1997;273:G602-G611.
  • Collins T, Read MA, Neish AS, Whitley MZ, Thanos D, Maniatis T. Transcriptional regulation of endothelial cell adhesion molecules: NF-kappa B and cytokine-indudble enhancers. FASEBJ. 1995;9:899-909.
  • Bell FP, Essani NA, Manning AM, Jaeschke H. lschemiareperfusion activates the nuclear transcription factor NF-?B and upregulates messenger RNA synthesis of adhesion molecules in the liver in vivo. Hepatol Res. 1997;8:178-188.
  • Zwacka RM, Zhou W, Zhang Y, Darby CJ, Dudus L, Halldorson J, Oberley L, Engelhardt JF. Redox gene therapy for ischemia/reperfusion injury of the liver reduces AP1 and NF-kappa B activation. Nat Med. 1998;4:698704.
  • 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.
  • Funaki H, Shimizu K, Harada S, Tsuyama H, Fushida S, Tani T, Miwa K. Essential role for nuclear factor kappa B in ischemic preconditioning for ischemia-reperfusion injury of the mouse liver. Transplantation. 2002;74:551556.
  • Essani NA, Fisher MA, Jaeschke H. Inhibition of NF-?B by dimethyl sulfoxide correlates with suppression of TNFa formation, reduced ICAM-1 gene transcription, and protection against endotoxin-induced liver injury. Shock. 1997;7:90-96.
  • Bellezzo JM, Leingang KA, BuIIa GA, Britton RS, Bacon BR, Fox ES. Modulation of lipopolysaccharide-mediated activation in rat Kupffer cells by antioxidants. J Lab Clin Med. 1998:131:36-44.
  • Wheeler MD, Yamashina S, Froh M, Rusyn I, Thurman RG. Adenoviral gene delivery can inactivate Kupffer cells: Role of oxidants in NF-kappa B activation and cytokine production. J Leukocyte Biol. 2001;69:622-630.
  • Sanlioglu S, Williams CM, Samavati L, Butler NS, Wang G, McCray PB Jr, Ritchie TC, Hunninghake GW, Zandi E, Engelhardt JF. Lipopolysaccharide induces Rac1-dependent reactive oxygen species formation and coordinates tumor necrosis factor-alpha secretion through IKK regulation of NF-kappa B. J Biol Chem. 2001:276:30188-30198.
  • Roebuck KA. Oxidant stress regulation of IL-8 and ICAM1 gene expression: Differential activation and binding of the transcription factors AP-1 and NF-kappa B. lnt J MoI Med. 1999;4223-230.
  • Fan J, Frey RS, Rahman A, Malik AB. Role of neutrophil NADPH oxidase in the mechanism of tumor necrosis factor-alpha-induced NF-kappa B activation and intercellular adhesion molecule-1 expression in endothelial cells. J Biol Chem. 2002;277:3404-3411.
  • Kokura S, Wolf RE, Yoshikawa T, Granger DN, Aw TY. Molecular mechanisms of neutrophil-endothelial cell adhesion induced by redox imbalance. Ore Res. 1999;84:516-524.
  • Rensing H, Bauer I, Peters I, Wein T, Silomon M, Jaeschke H, Bauer M. Role of reactive oxygen species for hepatocellular injury and heme oxygenase-1 gene expression after hemorrhage and resuscitation. Shock. 1999;12:300308.
  • Amersi F, Buelow R, Kato H, Ke B, Coito AJ, Shen XD, Zhao D, Zaky J, Melinek J, Lassman CR, KoIIs JK, Alam J, Ritter T, Volk HD, Farmer DG, Ghobrial RM, Busuttil RW, Kupiec-Weglinski JW. Upregulation of heme oxygenase1 protects genetically fat Zucker rat livers from ischemia/reperfusion injury. J Clin Invest. 1999;104:16311639.
  • Redaelli CA, Tian YH, Schaffner T, Ledermann M, Baer HU, Dufour JF. Extended preservation of rat liver graft by induction of heme oxygenase-1. Hepatology. 2002;35:1082-1092.
  • Bauer M, Bauer I. Heme oxygenase-1: Redox regulation and role in the hepatic response to oxidative stress. Antiox Redox Signal. 2002;4:749-758.
  • Katori M, Busuttil RW, Kupiec-Weglinski JW. Heme oxygenase-1 system in organ transplantation. Transplantation. 2002;74:905-912.
  • Ozaki M, Suzuki S, Irani K. Redox factor-1/APE suppresses oxidative stress by inhibiting the rad GTPase. FASEBJ. 2002;16889-890.
  • Koneru B, Dikdan G. Hepatic steatosis and liver transplantation current clinical and experimental perspectives. Transplantation. 2002;73:325-330.
  • Hui AM, Kawasaki S, Makuuchi M, Nakayama J, lkegami T, Miyagawa S. Liver injury following normothermic ischemia in steatotic rat liver. Hepatology. 1994;20:12871293.
  • Koneru B, Reddy MC, dela Torre AN, Patel D, lppolito T, Ferrante RJ. Studies of hepatic warm ischemia in the obese Zucker rat. Transplantation. 1995;59:942946.
  • Taneja C, Prescott L, Koneru B. Critical preservation injury in rat fatty liver is to hepatocytes, not sinusoidal lining cells. Transplantation. 1998:65:167-172.
  • Selzner M, Clavien PA. Failure of regeneration of the steatotic rat liver: Disruption at two different levels in the regeneration pathway. Hepatology. 2000;31:35-42.
  • Vendemiale G, Grattagliano I, Caraceni P, Caraccio G, Domenicali M, Dall'Agata M, Trevisani F, Guerrieri F, Bernard! M, Altomare E. Mitochondrial oxidative injury and energy metabolism alteration in rat fatty liver: Effect of the nutritional status. Hepatology. 2001;37: 286-295.
  • Nardo B, Caraceni P, Pasini P, Domenicali M, Catena F, Cavallari G, Santoni B, Maiolini E, Grattagliano I, Vendemiale G, Trevisani F, Roda A, Bernardi M, Cavallari A. Increased generation of reactive oxygen species in isolated rat fatty liver during postischemic reoxygenation. Transplantation. 2001;71:1816-1820.
  • 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.
  • Fan C, Zwacka RM, Engelhardt JF. Therapeutic approaches for ischemia/reperfusion injury in the liver. J MoI Med. 1999;77:577-592.
  • Liu P, Fisher MA, Farhood A, Smith CW, Jaeschke H. Beneficial effects of extracellular glutathione against endotoxin-induced liver injury during ischemia and reperfusion. Cire Shock. 1994;43:64-70.
  • Bilzer M, Paumgartner G, Gerbes AL. Glutathione protects the rat liver against reperfusion injury after hypothermie preservation. Gastroenterology. 1999:117:200-210.
  • Bilzer M, Lauterburg BH. Oxidant stress and potentiation of ischemia-reperfusion injury to the perfused rat liver by human polymorphonuclear leukocytes. JHepatol. 1994;20:473-477.
  • Knight TR, Ho Y-S, Farhood A, Jaeschke H. Peroxynitrite is a critical mediator of acetaminophen hepatotoxicity in murine livers: Protection by glutathione. J PharmacolExp Ther. 2002;303:468-475.
  • 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;33:902-914.
  • Wheeler MD, Katuna M, Smutney OM, Froh M, Dikalova A, Mason RP, Samulski RJ, Thurman RG. Comparison of the effect of adenoviral delivery of three Superoxide dismutase genes against hepatic ischemia-reperfusion injury. Hum Gene Ther. 2001;12:2167-2177.
  • Yabe Y, Kobayashi N, Nishihashi T, Takahashi R, Nishikawa M, Takakura Y, Hashida M. Prevention of neutrophil-mediated hepatic ischemia/reperfusion injury by Superoxide dismutase and catalase derivatives. J Pharmacol Exp Ther. 2001;298:894-899.
  • Carini R, De Cesaris MG, Splendore R, Vay D, Domenicotti C, Nitti MP, Paola D, Pronzato MA, Albano E. Signal pathway involved in the development of hypoxic preconditioning in rat hepatocytes. Hepatology. 2001;33:131139.
  • Peralta C, Bulbena O, Xaus C, Prats N, Cutrin JC, PoIi G, Gelpi E, Rosello-Catafau J. Ischemic preconditioning: a defense mechanism against the reactive oxygen species generated after hepatic ischemia reperfusion. Transp/anfai/on. 2002;73:1203-1211.
  • 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; in press.
  • Teoh N, Dela Pena A, Farrell G. Hepatic ischemic preconditioning in mice is associated with activation of NF-kappaB, p38 kinase, and cell cycle entry. Hepatology. 2002;36:94-102.
  • Zahler S, Kupatt C, Becker BF. Endothelial preconditioning by transient oxidative stress reduces inflammatory responses of cultured endothelial cells to TNF-alpha. FASEB 7.2000;14:555-564.
  • 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.
  • Kiemer AK, Heinze SK, Gerwig T, Gerbes AL, Vollmar AM. Stimulation of p38 MARK by hormonal preconditioning with atrial natriuretic peptide. World J Gastroenterol. 2002;8:707-711.
  • Clavien PA, Yadav S, Sindram D, Bentley RC. Protective effects of ischemic preconditioning for liver resection performed under inflow occlusion in humans. Ann Surg. 2000;232:155-162.

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