Hepatic ischemia-reperfusion injury and therapeutic strategies to alleviate cellular damage

Hepatology Research

Volumn 41, Issue 2, 2011, Pages 103-117

  Dogan, Serdar ^a   Aslan, Mutay ^a  

^a AKDENIZ UNIVERSITY   (Turkey)

Author keywords

Hepatocyte; Injury; Ischemia; Reperfusion

Indexed keywords

GELATINASE A; GELATINASE B; HEAT SHOCK PROTEIN 70; HEAT SHOCK PROTEIN 72; HEME OXYGENASE 1; HEME OXYGENASE 2; INTERCELLULAR ADHESION MOLECULE 1; INTERLEUKIN 1; INTERLEUKIN 10; INTERLEUKIN 12; INTERLEUKIN 13; INTERLEUKIN 18; INTERLEUKIN 6; LYMPHOCYTE FUNCTION ASSOCIATED ANTIGEN 1; MATRILYSIN; MATRIX METALLOPROTEINASE 26; MITOGEN ACTIVATED PROTEIN KINASE; P SELECTIN GLYCOPROTEIN LIGAND 1; PROSTACYCLIN; PROSTAGLANDIN E1; REACTIVE OXYGEN METABOLITE; TISSUE INHIBITOR OF METALLOPROTEINASE; TOLL LIKE RECEPTOR 2; TOLL LIKE RECEPTOR 4; TRANSCRIPTION FACTOR AP 1; TRANSCRIPTION FACTOR NRF2; TUMOR NECROSIS FACTOR ALPHA; UNINDEXED DRUG; VASCULAR CELL ADHESION MOLECULE 1; VERY LATE ACTIVATION ANTIGEN 4;

DETERIORATION; LIVER BLOOD FLOW; LIVER INJURY; LIVER ISCHEMIA; LIVER SURGERY; LIVER TRANSPLANTATION; NONHUMAN; PATHOPHYSIOLOGY; PRIORITY JOURNAL; REPERFUSION INJURY; REVASCULARIZATION; REVIEW; TISSUE INJURY;

EID: 79251522189     PISSN: 13866346     EISSN: 1872034X     Source Type: Journal    
DOI: 10.1111/j.1872-034X.2010.00765.x     Document Type: Review

References (132)

1. Carden DL, Granger DN. Pathophysiology of ischaemia-reperfusion injury. J Pathol 2000; 190: 255-66.
2. Montalvo-Jave EE, Escalante-Tattersfield T, Ortega-Salgado JA, Piña E, Geller DA. Factors in the pathophysiology of the liver ischemia-reperfusion injury. J Surg Res 2008; 147: 153-9.
3. Lemasters JJ, Nieminen AL, Qian T, Trost LC, Herman B. The mitochondrial permeability transition in toxic, hypoxic and reperfusion injury. Mol Cell Biochem 1997; 174: 159-65.
4. Brunati AM, Pagano MA, Bindoli A, Rigobello MP. Thiol redox systems and protein kinases in hepatic stellate cell regulatory processes. Free Radic Res 2010; 44: 363-78.
5. Zipprich A, Loureiro-Silva MR, D'Silva I, Groszmann RJ. The role of hepatic arterial flow on portal venous and hepatic venous wedged pressure in the isolated perfused CCl4-cirrhotic liver. Am J Physiol Gastrointest Liver Physiol 2008; 295: 197-202.
6. 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: 277-84.
7. Arumugam TV, Shiels IA, Woodruff TM, Granger DN, Taylor SM. The role of the complement system in ischemia-reperfusion injury. Shock 2004; 21: 401-9.
8. Lehmann TG, Koeppel TA, Munch S, Kirschfink M, Klar E, Post S. Impact of inhibition of complement by sCR1 on hepatic microcirculation after warm ischemia. Microvasc Res 2001; 62: 284-92.
9. Tsukamoto H. Redox regulation of cytokine expression in Kupffer cells. Antioxid Redox Signal 2002; 4: 741-8.
10. Colletti LM, Kunkel SL, Walz A etal. The role of cytokine networks in the local liver injury following hepatic ischemia/reperfusion in the rat. Hepatology 1996; 23: 506-14.
11. Wanner GA, Ertel W, Müller P etal. Liver ischemia and reperfusion induces a systemic inflammatory response through Kupffer cell activation. Shock 1996; 5: 34-40.
12. Farhood A, McGuire GM, Manning AM. Intercellular adhesion molecule 1 (ICAM-1) expression and its role in neutrophil-induced ischemia-reperfusion injury in rat liver. J Leukoc Biol 1995; 57: 368-74.
13. Shito M, Wakabayashi G, Ueda M etal. Interleukin 1 receptor blockade reduces tumor necrosis factor production, tissue injury, and mortality after hepatic ischemia-reperfusion in the rat. Transplantation 1997; 63: 143-8.
14. Harada H, Wakabayashi G, Takayanagi A etal. Transfer of the interleukin-1 receptor antagonist gene into rat liver abrogates hepatic ischemia-reperfusion injury. Transplantation 2002; 74: 1434-41.
15. Takiguchi M, Totsuka E, Umehara M etal. Attenuation of microcirculatory disturbance after liver ischemia by newly synthesized inflammatory cytokine suppressor, FR167653. Hepatogastroenterology 2003; 50: 789-93.
16. Camargo CA Jr, Madden JF, Gao W, Selvan RS, Clavien PA. Interleukin-6 protects liver against warm ischemia/reperfusion injury and promotes hepatocyte proliferation in the rodent. Hepatology 1997; 26: 1513-20.
17. Minor T, Isselhard W, Yamaguchi T. Involvement of platelet activating factor in microcirculatory disturbances after global hepatic ischemia. J Surg Res 1995; 58: 536-43.
18. Serizawa A, Nakamura S, Suzuki, Baba S, Nakano M. Involvement of platelet-activating factor in cytokine production and neutrophil activation after hepatic ischemia-reperfusion. Hepatology 1996; 23: 1656-63.
19. Quiroga J, Prieto J. Liver cytoprotection by prostaglandins. Pharmacol Ther 1993; 58: 67-91.
20. Hafez T, Moussa M, Nesim I, Baligh N, Davidson B, Abdul-Hadi A. The effect of intraportal prostaglandin E1 on adhesion molecule expression, inflammatory modulator function, and histology in canine hepatic ischemia/reperfusion injury. J Surg Res 2007; 138: 88-99.
21. Natori S, Fujii Y, Kurosawa H, Nakano A, Shimada H. Prostaglandin E1 protects against ischemia-reperfusion injury of the liver by inhibition of neutrophil adherence to endothelial cells. Transplantation 1997; 64: 1514-20.
22. Kim YI, Kai T, Kitano S etal. Hepatoprotection by a PGI2 analogue in complete warm ischemia of the pig liver. Prostanoid release from the reperfused liver. Transplantation 1994; 58: 875-9.
23. Hughes H, Farhood A, Jaeschke H. Role of Leukotriene B4 in the pathogenesis of hepatic ischemia-reperfusion injury in the rat. Prostaglandins Leukot Essent Fatty Acids 1992; 45: 113-19.
24. Takamatsu Y, Shimada K, Chijiiwa K, Kuroki S, Yamaguchi K, Tanaka M. Role of leukotrienes on hepatic ischemia/reperfusion injury in rats. J Surg Res 2004; 119: 14-20.
25. Yoshidome H, Kato A, Edwards MJ, Lentsch AB. Interleukin-10 suppresses hepatic ischemia/reperfusion injury in mice: implications of a central role for nuclear factor kappaB. Hepatology 1999; 30: 203-8.
26. Oreopoulos GD, Wu H, Szaszi K etal. Hypertonic preconditioning prevents hepatocellular injury following ischemia/reperfusion in mice: a role for interleukin 10. Hepatology 2004; 40: 211-20.
27. Lentsch AB, Yoshidome H, Kato A etal. Requirement for interleukin-12 in the pathogenesis of warm hepatic ischemia/reperfusion injury in mice. Hepatology 1999; 30: 1448-53.
28. Motoki A, Adachi N, Liu K etal. Suppression of ischaemia-induced cytokine release by dimaprit and amelioration of liver injury in rats. Basic Clin Pharmacol Toxicol 2008; 102: 394-8.
29. Takeuchi D, Yoshidome H, Kato A etal. Interleukin 18 causes hepatic ischemia/reperfusion injury by suppressing anti-inflammatory cytokine expression in mice. Hepatology 2004; 39: 699-710.
30. Lefer DJ. Pharmacology of selectin inhibitors in ischemia/reperfusion states. Annu Rev Pharmacol Toxicol 2000; 40: 283-94.
31. Yadav SS, Howell D, Steeber D, Harland RC, Tedder TF, Clavien PA. P-selectin mediates reperfusion injury through neutrophil sequestration in the warm ischemic mouse liver. Hepatology 1999; 29: 1494-502.
32. Tsuchihashi S, Fondevila C, Shaw GD etal. Molecular characterization of rat leukocyte P-selectin glycoprotein ligand-1 and effect of its blockade: protection from ischemia-reperfusion injury in liver transplantation. J Immunol 2006; 176: 616-24.
33. Yadav SS, Howell DN, Gao W, Steeber DA, Harland RC, Clavien PA. L-selectin and ICAM-1 mediate neutrophil adhesion and reperfusion injury in the warm ischemic mouse liver. Am J Physiol 1998; 275: 1341-52.
34. Burke J, Zibari GB, Brown MF etal. Hepatic ischemia-reperfusion injury causes E-selectin upregulation. Transplant Proc 1998; 30: 2321-3.
35. López-Neblina F, Toledo-Pereyra LH. Anti-ischemic effect of selectin blocker through modulation of tumor necrosis factor-alpha and interleukin-10. J Surg Res 2007; 138: 275-83.
36. Toledo-Pereyra LH, Lopez-Neblina F, Lentsch AB, Anaya-Prado R, Romano SJ, Ward PA. Selectin inhibition modulates NF-kappa B and AP-1 signaling after liver ischemia/reperfusion. J Invest Surg 2006; 19: 313-22.
37. Martinez-Mier G, Toledo-Pereyra LH, Ward PA. Adhesion molecules in liver ischemia and reperfusion. J Surg Res 2000; 94: 185-94.
38. Calvey CR, Toledo-Pereyra LH. Selectin inhibitors and their proposed role in ischemia and reperfusion. J Invest Surg 2007; 20: 71-85.
39. Nakano H, Kuzume M, Namatame K, Yamaguchi M, Kumada K. Efficacy of intraportal injection of anti ICAM-1 monoclonal antibody against liver cell injury following warm ischemia in the rat. Am J Surg 1995; 170: 64-6.
40. Vollmar B, Glasz J, Menger MD, Messmer K. Leukocytes contribute to hepatic ischemia/reperfusion injury via intercellular adhesion molecule-1-mediated venular adherence. Surgery 1995; 117: 195-200.
41. Sternlicht MD, Werb Z. How matrix metalloproteinases regulate cell behavior? Annu Rev Cell Dev Biol 2001; 17: 463-516.
42. Nagase H, Woessner JF Jr. Matrix metalloproteinases. J Biol Chem 1999; 274: 21491-4.
43. Park HI, Ni J, Gerkema FE, Liu D, Belozerov VE, Sang QX. Identification and characterization of human endometase (Matrix metalloproteinase-26) from endometrial tumor. J Biol Chem 2009; 275: 20540-4.
44. Baker AH, Edwards DR, Murphy G. Metalloproteinase inhibitors: biological actions and therapeutic opportunities. J Cell Sci 2002; 115: 3719-27.
45. Viappiani S, Sariahmetoglu M, Schulz R. The role of matrix metalloproteinase inhibitors in ischemia-reperfusion injury in the liver. Curr Pharm Des 2006; 12: 2923-34.
46. Defamie V, Laurens M, Patrono D etal. Matrix metalloproteinase inhibition protects rat livers from prolonged ischemia-warm reperfusion injury. Hepatology 2008; 47: 177-85.
47. Calmus Y, Cynober L, Dousset B etal. Evidence for the detrimental role of proteolysis during liver preservation in humans. Gastroenterology 1995; 108: 1510-16.
48. Upadhya GA, Strasberg SM. Glutathione, lactobionate, and histidine: cryptic inhibitors of matrix metalloproteinases contained in University of Wisconsin and histidine/tryptophan/ketoglutarate liver preservation solutions. Hepatology 2000; 31: 1115-22.
49. Hamada T, Fondevilla C, Busuttil RW, Coito AJ. Metalloproteinase-9 deficiency protects against hepatic ischemia/reperfusion injury. Hepatology 2008; 47: 186-98.
50. Fowell AJ, Benyon RC. Can matrix metalloproteinases be targeted in hepatic ischemia/reperfusion injury? Hepatology 2008; 47: 14-16.
51. Cursio R, Mari B, Louis K etal. Rat liver injury after normothermic ischemia is prevented by a phosphinic matrix metalloproteinase inhibitor. FASEB J 2002; 16: 93-5.
52. Shirahane K, Yamaguchi K, Koga K, Watanabe M, Kuroki S, Tanaka M. Hepatic ischemia/reperfusion injury is prevented by a novel matrix metalloproteinase inhibitor, ONO-4817. Surgery 2006; 139: 653-64.
53. Khandoga A, Kessler JS, Hanschen M etal. Matrix metalloproteinase-9 promotes neutrophil and T cell recruitment and migration in the postischemic liver. J Leukoc Biol 2006; 79: 1295-305.
54. Tsuchihashi S, Fondevila C, Kupiec-Weglinski JW. Heme oxygenase system in ischemia and reperfusion injury. Ann Transplant 2004; 9: 84-7.
55. Farombi EO, Surh YJ. Heme oxygenase-1 as a potential therapeutic target for hepatoprotection. J Biochem Mol Biol 2006; 39: 479-91.
56. Ito K, Ikeda S, Shibata T, Yano T, Horikawa S. Immunohistochemical analysis of heme oxygenase-I in rat liver after ischemia. Biochem Mol Biol Int 1997; 43: 551-6.
57. Elbirt KK, Whitmarsh AJ, Davis RJ, Bonkovsky HL. Mechanism of sodium arsenite-mediated induction of heme oxygenase-1 in hepatoma cells. Role of mitogenactivated protein kinases. J Biol Chem 1998; 273: 8922-31.
58. Amersi F, Buelow R, Kato H etal. Upregulation of heme oxygenase-1 protects genetically fat Zucker rat livers from ischemia/reperfusion injury. J Clin Invest 1999; 104: 1631-9.
59. Ito K, Ozasa H, Sanada K, Horikawa S. Doxorubicin preconditioning: a protection against rat hepatic ischemia-reperfusion injury. Hepatology (Baltimore) 2000; 31: 416-19.
60. Tsuchihashi S, Zhai Y, Fondevila C, Busuttil RW, Kupiec-Weglinski JW. HO-1 upregulation suppresses type 1 IFN pathway in hepatic ischemia/reperfusion injury. Transplant Proc 2005; 37: 1677-8.
61. Lai IR, Chang KJ, Tsai HW, Chen CF. Pharmacological preconditioning with simvastatin protects liver from ischemia-reperfusion injury by heme oxygenase-1 induction. Transplantation 2008; 85: 732-8.
62. Schmidt R, Tritschler E, Hoetzel A etal. HO-1 induction by the clinically used anesthetic isoflurane protects rat livers from ischemia/reperfuison injury. Ann Surg 2007; 245: 931-42.
63. Fondevila C, Shen XD, Tsuchiyashi S etal. Biliverdin therapy protects rat livers from ischemia and reperfusion injury. Hepatology 2004; 40: 1333-41.
64. Kato Y, Shimazu M, Kondo M etal. Bilirubin rinse: A simple protectant against the rat liver graft injury mimicking heme oxygenase-1 preconditioning. Hepatology 2003; 38: 364-73.
65. Amersi F, Shen XD, Anselmo D etal. Ex vivo exposure to carbon monoxide prevents hepatic ischemia/reperfusion injury through p38 MAP kinase pathway. Hepatology 2002; 35: 815-23.
66. Takeda K, Akira S. STAT family of transcription factors in cytokine-mediated biological responses. Cytokine Growth Factor Rev 2000; 11: 199-207.
67. Kaplan MH, Schindler U, Smiley ST, Grusby MJ. Stat6 is required for mediating responses to IL-4 and for the development of Th2 cells. Immunity 1996; 4: 313-19.
68. Thierfelder WE, Van Deursen JM, Yamamoto K etal. Requirement for Stat4 in interleukin-12-mediated responses of natural killer and T cells. Nature 1996; 382: 171-4.
69. Shen XD, Ke B, Zhai Y etal. Stat4 and Stat6 signaling in hepatic ischemia/reperfusion injury in mice: HO-1 dependence of Stat4 disruption-mediated cytoprotection. Hepatology 2003; 37: 296-303.
70. Tsung A, Hoffman RA, Izuishi K etal. Hepatic ischemia/reperfusion injury involves functional TLR4 signaling in nonparenchymal cells. J Immunol 2005; 175: 7661-8.
71. Wu HS, Zhang JX, Wang L, Tian Y, Wang H, Rotstein O. Toll-like receptor 4 involvement in hepatic ischemia/reperfusion injury in mice. Hepatobiliary Pancreat Dis Int 2004; 3: 250-3.
72. Zhai Y, Shen XD, Gao F etal. CXCL10 regulates liver innate immune response against ischemia and reperfusion injury. Hepatology 2008; 47: 207-14.
73. Tsuchihashi S, Zhai Y, Bo Q, Busuttil RW, Kupiec-Weglinski JW. Heme oxygenase-1 mediated cytoprotection against liver ischemia and reperfusion injury: inhibition of type-1 interferon signaling. Transplantation 2007; 83: 1628-34.
74. Schmitt E, Gehrmann M, Brunet M, Multhoff G, Garrido C. Intracellular and extracellular functions of heat shock proteins: repercussions in cancer therapy. J Leukoc Biol 2007; 81: 15-27.
75. Kuboki S, Schuster R, Blanchard J, Pritts TA, Wong HR, Lentsch AB. Role of heat shock protein 70 in hepatic ischemia-reperfusion injury in mice. Am J Physiol Gastrointest Liver Physiol 2007; 292: 1141-9.
76. Shen SQ, Zhang Y, Xiang JJ, Xiong CL. Protective effect of curcumin against liver warm ischemia/reperfusion injury in rat model is associated with regulation of heat shock protein and antioxidant enzymes. World J Gastroenterol 2007; 13: 1953-61.
77. Bedirli A, Sakrak O, Muhtaroglu S etal. Ergothioneine pretreatment protects the liver from ischemia-reperfusion injury caused by increasing hepatic heat shock protein 70. J Surg Res 2004; 122: 96-102.
78. Matsuo K, Togo S, Sekido H etal. Pharmacologic preconditioning effects: prostaglandin E1 induces heat-shock proteins immediately after ischemia/reperfusion of the mouse liver. J Gastrointest Surg 2005; 9: 758-68.
79. Okaya T, Blanchard J, Schuster R etal. Age-dependent responses to hepatic ischemia/reperfusion injury. Shock 2005; 24: 421-7.
80. Asea A, Kraeft SK, Kurt-Jones EA etal. HSP70 stimulates cytokine production through a CD14-dependant pathway, demonstrating its dual role as a chaperone and cytokine. Nat Med 2000; 6: 435-42.
81. McCubrey JA, Lahair MM, Franklin RA. Reactive oxygen species-induced activation of the MAP kinase signaling pathways. Antioxid Redox Signal 2006; 8: 1775-89.
82. Davis RJ. Signal transduction by the JNK group of MAP kinases. Cell 2000; 103: 239-52.
83. 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: 1500-4.
84. Shinoda M, Shimazu M, Matsuda S etal. c-Jun N-terminal kinase activation during warm hepatic ischemia/reperfusion injuries in a rat model. Wound Repair Regen 2002; 10: 314-19.
85. Uehara T, Xi-Peng X, Bennett B etal. c-Jun N-terminal kinase mediates hepatic injury after rat liver transplantation. Transplantation 2004; 78: 324-32.
86. Uehara T, Bennett B, Sakata ST etal. JNK mediates hepatic ischemia reperfusion injury. J Hepatol 2005; 42: 850-9.
87. Crenesse D, Laurens M, Heurteaux C etal. Rat liver ischemia-reperfusion-induced apoptosis and necrosis are decreased by FK506 pretreatment. Eur J Pharmacol 2003; 473: 177-84.
88. Kobayashi M, Takeyoshi I, Yoshinari D, Matsumoto K, Morishita Y. P38 mitogen-activated protein kinase inhibition attenuates ischemia/reperfusion injury of the rat liver. Surgery 2002; 131: 344-9.
89. Xu J, Yang Z, Zeng J. Role of NF-kappa B in liver ischemia reperfusion injury of rats. J Huazhong Univ Sci Technolog Med Sci 2003; 23: 158-60.
90. Funaki H, Shimizu K, Harada S etal. Essential role for nuclear factor kappaB in ischemic preconditioning for ischemia-reperfusion injury of the mouse liver. Transplantation 2002; 74: 551-6.
91. Sun Z, Andersson R. NF-κB activation and inhibition. Shock 2002; 18: 99-106.
92. Rothwarf DM, Zandi E, Natoli G, Karin M. IKK-gamma is an essential regulatory subunit of the IkappaB kinase complex. Nature 1998; 395: 297-330.
93. Luedde T, Assmus U, Wüstefeld T etal. Deletion of IKK2 in hepatocytes does not sensitize these cells to TNF-induced apoptosis but protects from ischemia/reperfusion injury. J Clin Invest 2005; 115: 849-59.
94. Beraza N, Lüdde T, Assmus U, Roskams T, Vander Borght S, Trautwein C. Hepatocyte-specific IKK gamma/NEMO expression determines the degree of liver injury. Gastroenterology 2007; 132: 2504-17.
95. Su GL, Klein RD, Aminlari A etal. Kupffer cell activation by lipopolysaccharide in rats: role for lipopolysaccharide binding protein and toll-like receptor 4. Hepatology 2000; 31: 932-6.
96. Matsumura T, Degawa T, Takii T etal. TRAF6-NF-κB pathway is essential for interleukin-1-induced TLR2 expression and its functional response to TLR2 ligand in murine hepatocytes. Immunology 2003; 109: 127-36.
97. Paik YH, Schwabe RF, Bataller R, Russo MP, Jobin C, Brenner DA. Toll-like receptor 4 mediates inflammatory signaling by bacterial lipopolysaccharide in human hepatic stellate cells. Hepatology 2003; 37: 1043-55.
98. Uhrig A, Banafsche R, Kremer M etal. Development and functional consequences of LPS tolerance in sinusoidal endothelial cells of the liver. J Leukoc Biol 2005; 77: 626-33.
99. Seki E, Brenner DA. Toll-like receptors and adaptor molecules in liver disease: update. Hepatology 2008; 48: 322-35.
100. O'Neill LA. How Toll-like receptors signal: what we know and what we don't know. Curr Opin Immunol 2006; 18: 3-9.
101. Zhai Y, Shen XD, O'Connell R etal. Cutting edge: TLR4 activation mediates liver ischemia/reperfusion inflammatory response via IFN regulatory factor 3-dependent MyD88-independent pathway. J Immunol 2004; 173: 7115-19.
102. Tsung A, Sahai R, Tanaka H etal. The nuclear factor HMGB1 mediates hepatic injury after murine liver ischemia-reperfusion. J Exp Med 2005; 201: 1135-43.
103. Jin X, Wang L, Wu HS etal. N-acetylcysteine inhibits activation of toll-like receptor 2 and 4 gene expression in the liver and lung after partial hepatic ischemia-reperfusion injury in mice. Hepatobiliary Pancreat Dis Int 2007; 6: 284-9.
104. Zhang JX, Wu HS, Wang H, Zhang JH, Wang Y, Zheng QC. Protection against hepatic ischemia/reperfusion injury via downregulation of toll-like receptor 2 expression by inhibition of Kupffer cell function. World J Gastroenterol 2005; 11: 4423-6.
105. Cardinal J, Pan P, Dhupar R etal. Cisplatin prevents high mobility group box 1 release and is protective in a murine model of hepatic ischemia/reperfusion injury. Hepatology 2009; 50: 565-74.
106. Urakami H, Abe Y, Grisham MB. Role of reactive metabolites of oxygen and nitrogen in partial liver transplantation: lessons learned from reduced-size liver ischemia and reperfusion injury. Clin Exp Pharmacol Physiol 2007; 34: 912-19.
107. Aslan M, Freeman BA. Redox-dependent impairment of vascular function in sickle cell disease. Free Radic Biol Med 2007; 43: 1469-83.
108. Enroth C, Eger BT, Okamoto K, Nishino T, Nishino T, Pai EF. Crystal structures of bovine milk xanthine dehydrogenase and xanthine oxidase: structure-based mechanism of conversion. Proc Natl Acad Sci USA 2000; 97: 10723-8.
109. 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: 15640-70.
110. Yokoyama Y, Beckman JS, Beckman TK etal. Circulating xanthine oxidase: potential mediator of ischemic injury. Am J Physiol 1990; 258: 564-70.
111. Houston M, Estevez A, Chumley P etal. Binding of xanthine oxidase to vascular endothelium. Kinetic characterization and oxidative impairment of nitric oxide-dependent signaling. J Biol Chem 1999; 274: 4985-94.
112. Isobe M, Katsuramaki T, Kimura H etal. Role of inducible nitric oxide synthase on hepatic ischemia and reperfusion injury. Transplant Proc 2000; 32: 1650-2.
113. Lee VG, Johnson ML, Baust J, Laubach VE, Watkins SC, Billiar TR. The roles of iNOS in liver ischemia-reperfusion injury. Shock 2001; 16: 355-60.
114. Hines IN, Harada H, Bharwani S, Pavlick KP, Hoffman JM, Grisham MB. Enhanced post-ischemic liver injury in iNOS-deficient mice: a cautionary note. Biochem Biophys Res Commun 2001; 284: 972-6.
115. Abe Y, Hines I, Zibari G, Grisham MB. Hepatocellular protection by nitric oxide or nitrite in ischemia and reperfusion injury. Arch Biochem Biophys 2009; 484: 232-7.
116. Llacuna L, Marí M, Lluis JM, García-Ruiz C, Fernández-Checa JC, Morales A. Reactive oxygen species mediate liver injury through parenchymal nuclear factor-kappaB inactivation in prolonged ischemia/reperfusion. Am J Pathol 2009; 174: 1776-85.
117. Heyninck K, Wullaert A, Beyaert R. Nuclear factor-kappa B plays a central role in tumour necrosis factor-mediated liver disease. Biochem Pharmacol 2003; 66: 1409-15.
118. Wheeler MD, Katuna M, Smutney OM etal. Comparison of the effect of adenoviral delivery of three superoxide dismutase genes against hepatic ischemia-reperfusion injury. Hum Gene Ther 2001; 12: 2167-77.
119. Ninomiya M, Shimada M, Harada N etal. Beneficial effect of MCI-186 on hepatic warm ischemia-reperfusion in the rat. Transplantation 2002; 74: 1470-2.
120. Sener G, Sehirli O, Ercan F, Sirvanci S, Gedik N, Kacmaz A. Protective effect of MESNA (2-mercaptoethane sulfonate) against hepatic ischemia/reperfusion injury in rats. Surg Today 2005; 35: 575-80.
121. Bi W, Cai J, Xue P etal. Protective effect of nitronyl nitroxide-amino acid conjugates on liver ischemia-reperfusion induced injury in rats. Bioorg Med Chem Lett 2008; 18: 1788-94.
122. Dulundu E, Ozel Y, Topaloglu U etal. Alpha-lipoic acid protects against hepatic ischemia-reperfusion injury in rats. Pharmacology 2007; 79: 163-70.
123. Tselepidis S, Papazoglou L, Dessiris A etal. Liver injury after ischemia and reperfusion: the role of oxygen free radicals. Mil Med 2004; 169: 531-5.
124. Wu TJ, Khoo NH, Zhou F, Day BJ, Parks DA. Decreased hepatic ischemia-reperfusion injury by manganese-porphyrin complexes. Free Radic Res 2007; 41: 127-34.
125. Curek GD, Cort A, Yucel G etal. Effect of astaxanthin on hepatocellular injury following ischemia/reperfusion. Toxicology 2010; 267: 147-53.
126. Okatani Y, Wakatsuki A, Reiter RJ, Enzan H, Miyahara Y. Protective effect of melatonin against mitochondrial injury induced by ischemia and reperfusion of rat liver. Eur J Pharmacol 2003; 469: 145-52.
127. Rodríguez-Reynoso S, Leal C, Portilla E, Olivares N, Muñiz 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: 141-9.
128. Lin HI, Wang D, Leu FJ, Chen CF, Chen HI. Ischemia and reperfusion of liver induces eNOS and iNOS expression: effects of a NO donor and NOS inhibitor. Chin J Physiol 2004; 47: 121-7.
129. Meguro M, Katsuramaki T, Nagayama M etal. A novel inhibitor of inducible nitric oxide synthase (ONO-1714) prevents critical warm ischemia-reperfusion injury in the pig liver. Transplantation 2002; 73: 1439-46.
130. Tsuchihashi S, Kaldas F, Chida N etal. FK330, a novel inducible nitric oxide synthase inhibitor, prevents ischemia and reperfusion injury in rat liver transplantation. Am J Transplant 2006; 6: 2013-22.
131. Jeyabalan G, Klune JR, Nakao A etal. Arginase blockade protects against hepatic damage in warm ischemia-reperfusion. Nitric Oxide 2008; 19: 29-35.
132. 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: 280-5.