Reactive oxygen species mediate human hepatocyte injury during hypoxia/reoxygenation

Liver Transplantation

Volumn 16, Issue 11, 2010, Pages 1303-1313

  Bhogal, Ricky Harminder ^a   Curbishley, Stuart M ^a   Weston, Christopher J ^a   Adams, David H ^a   Afford, Simon C ^a  

^a UNIVERSITY DEPARTMENT OF MEDICINE   (United Kingdom)

Author keywords

[No Author keywords available]

Indexed keywords

ANTIOXIDANT; REACTIVE OXYGEN METABOLITE; REDUCED NICOTINAMIDE ADENINE DINUCLEOTIDE PHOSPHATE OXIDASE;

ADULT; ARTICLE; CELL DEATH; CELL ISOLATION; CONTROLLED STUDY; DONOR; HEPATITIS; HUMAN; HUMAN CELL; HUMAN TISSUE; HYPOXIA; LIVER CELL; LIVER DISEASE; LIVER FAILURE; LIVER GRAFT; LIVER INJURY; LIVER ISCHEMIA; MALIGNANT NEOPLASTIC DISEASE; MITOCHONDRION; PRIORITY JOURNAL; REOXYGENATION;

ACETYLCYSTEINE; ANNEXIN A5; ANOXIA; ANTIOXIDANTS; APOPTOSIS; FEMALE; FLOW CYTOMETRY; HEPATOCYTES; HUMANS; INFLAMMATION; KUPFFER CELLS; LIVER; LIVER DISEASES; MALE; MITOCHONDRIA; MODELS, BIOLOGICAL; NADPH OXIDASE; REACTIVE OXYGEN SPECIES; REPERFUSION INJURY; YOUNG ADULT;

EID: 78349265397     PISSN: 15276465     EISSN: 15276473     Source Type: Journal    
DOI: 10.1002/lt.22157     Document Type: Article

References (45)

1. Toledo-Pereyra LH, Simmons RL, Najarian JS., Protection of the ischemic liver by donor pre-treatment before transplantation. Am J Surg 1975; 129: 513 - 517.
2. Massip-Salcedo M, Rosello-Catafau J, Prieto J, Avila MA, Peralta C., The response of the hepatocyte to ischemia. Liver Int 2007; 27: 6 - 17.
3. Vardanian AJ, Busuttil RW, Kupiec-Weglinski JW., Molecular mediators of liver ischemia and reperfusion injury: a brief review. Mol Med 2008; 14: 337 - 345.
4. Fondevila C, Busuttil RW, Kupiec-Weglinski JW., Hepatic ischemia/reperfusion injury-a fresh look. Exp Mol Pathol 2003; 74: 86 - 93.
5. Jaeschke H, Farhood A., Neutrophil and Kupffer cell-induced oxidant stress and ischemia-reperfusion injury in the rat liver. Am J Physiol 1991; 260 (pt 1): G355 - G362.
6. Jaeschke H., Molecular mechanisms of hepatic ischemia-reperfusion injury and preconditioning. Am J Physiol Gastrointest Liver Physiol 2003; 284: G15 - G26.
7. Zhang W, Wang M, Xie HY, Zhou L, Meng XQ, Shi J, et al. Role of reactive oxygen species in mediating hepatic ischemia-reperfusion injury and its therapeutic applications in liver transplantation. Transplant Proc 2007; 39: 1332 - 1337.
8. Decker K., Biologically active products of stimulated liver macrophages (Kupffer cells). Eur J Biochem 1990; 192: 245 - 261.
9. Jaeschke H., Reperfusion injury after warm ischemia or cold storage of the liver: role of apoptotic cell death. Transplant Proc 2002; 34: 2656 - 2658.
10. Taniai H, Hines IN, Bharwani S, Maloney RE, Nimura Y, Gao B, et al. Susceptibility of murine periportal hepatocytes to hypoxia-reoxygenation: role for NO and Kupffer cell-derived oxidants. Hepatology 2004; 39: 1544 - 1552.
11. 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.
12. Adkinson D, Hollwarth ME, Beniot 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.
13. 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.
14. Lluis JM, Buricchi F, Chiarugi P, Morales A, Fernandez-Checa JC., Dual role of mitochondrial reactive oxygen species in hypoxia signalling: activation of nuclear factor-kB via c-SRC- and oxidant dependent cell death. Cancer Res 2007; 67: 7368 - 7377.
15. 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.
16. Young TA, Cunningham CC, Bailey SM., Reactive oxygen species production by the mitochondrial respiratory chain in isolated rat hepatocytes and liver mitochondria: studies using myxothiazol. Arch Biochem Biophys 2002; 405: 65 - 72.
17. Schulze-Bergkamen H, Schuchmann M, Fleischer B, Galle PR., The role of apoptosis versus oncotic necrosis in liver injury: facts or faith? J Hepatol 2006; 44: 984 - 993.
18. Sasaki H, Matsuno T, Tanaka N, Orita K., Activation of apoptosis during the perfusion phase after rat liver ischemia. Transplant Proc 1996; 28: 1980 - 1989.
19. Smith MK, Rosser BG, Mooney DJ., Hypoxia leads to necrotic hepatocyte death. J Biomed Mater Res A 2007; 80: 520 - 529.
20. Jaeschke H, Lemasters JJ., Apoptosis versus oncotic necrosis in hepatic ischemia/reperfusion injury. Gastroenterology 2003; 125: 1246 - 1257.
21. Gonzalez R, Collado JA, Nell S, Briceno J, Tamayo MJ, Fraga E, et al. Cytoprotection properties of alpha-tocopherol are related to gene regulation in cultured D-galactosamine-treated human hepatocytes. Free Radic Biol Med 2007; 43: 1439 - 1452.
22. Cao L, Li Y, Cheng F, Li S, Long D., Hypoxia/reoxygenation up-regulated the expression of death receptor 5 and enhanced apoptosis in human hepatocyte line. Transplant Proc 2006; 38: 2207 - 2209.
23. Anderson CD, Belous A, Pierce J, Nicoud IB, Knox C, Wakata A, et al. Mitochondrial calcium uptake regulates cold preservation-induced Bax translocation and early reperfusion apoptosis. Am J Transplant 2004; 4: 352 - 362.
24. Schroedl C, McClintock DS, Budinger GRS, Chandel NS., Hypoxic but not anoxic stabilization of HIF-1α requires mitochondrial reactive oxygen species. Am J Physiol Lung Cell Mol Physiol 2002; 283: L922 - L931.
25. Conde de la Rosa L, Moshage H, Nieto N., Hepatocyte oxidant stress and alcoholic liver disease. Rev Esp Enferm Dig 2008; 100: 156 - 163.
26. Lluis JM, Morales A, Blasco C, Colell A, Mari M, Garcia-Ruiz C, et al. Critical role of mitochondrial glutathione in the survival of hepatocytes during hypoxia. J Biol Chem 2005; 280: 3224 - 3232.
27. Haga S, Terui K, Fukai M, Oikawa Y, Irani K, Furukawa H, et al. Preventing hypoxia/reoxygenation damage to hepatocytes by p66shc ablation: up-regulation of anti-oxidant and anti-oxidant proteins. J Hepatol 2008; 48: 422 - 432.
28. Crenesse D, Schmid-Alliana A, Laurens M, Cursio R, Gugenheim J., JNK1/SAPK1 involvement in hypoxia-reoxygenation-induced apoptosis in rat hepatocytes. Transplant Proc 2001; 33: 260 - 261.
29. Cotgreave IA., N-Acetylcysteine: pharmacological considerations and experimental and clinical applications. Adv Pharmacol 1997; 38: 205 - 227.
30. 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.
31. Jaeshcke H, Gores GJ, Cederbaum AI, Hinson JA, Pessayre D, Lemasters JJ., Mechanisms of hepatotoxicity. Toxicol Sci 2002; 65: 166 - 176.
32. Block KI, Koch AC, Mead MN, Tothy PK, Newman RA, Gyllenhaal C., Impact of antioxidant supplementation on chemotherapeutic efficacy: a systematic review of the evidence from randomised controlled trials. Cancer Treat Rev 2007; 33: 407 - 418.
33. Rosser BG, Gores GJ., Liver cell necrosis: cellular mechanisms and clinical implications. Gastroenterology 1995; 108: 252 - 275.
34. Golstein P, Kroemer G., Cell death by necrosis: towards a molecular definition. Trends Biochem Sci 2007; 32: 37 - 43.
35. Wang Y, Xu Y, Wang H, Xue P, Li X, Li B, et al. Arsenic induces mitochondria-dependent apoptosis by reactive oxygen species generation rather than glutathione depletion in Chang human hepatocytes. Arch Toxicol 2009; 83: 899 - 908.
36. Motoyama S, Minamiya Y, Saito S, Saito R, Matsuzaki I, Abo S, et al. Hydrogen peroxide derived from hepatocytes induces sinusoidal cell apoptosis in perfused hypoxic rat liver. Gastroenterology 1998; 114: 153 - 163.
37. Bilzer M, Jaeschke H, Vollmar AM, Paumgartner G, Gerbes AL., Prevention of Kupffer cell-induced oxidant injury in rat liver by atrial natriuretic peptide. Am J Physiol 1999; 276 (pt 1): G1137 - G1144.
38. Conti A, Scala S, D'Agostino P, Alimenti E, Morelli D, Andria B, et al. Wide gene expression profiling of ischemia-reperfusion injury in human liver transplantation. Liver Transpl 2007; 13: 99 - 113.
39. Yuzawa H, Fujioka H, Mizoe A, Azuma T, Furui J, Nishikawa M, et al. Inhibitory effects of safe and novel SOD derivatives, galactosylated-SOD, on hepatic warm ischemia/reperfusion injury in pigs. Hepatogastroenterology 2005; 52: 839 - 843.
40. Sener G, Sehrili O, Ercan F, Sirvanci S, Gedil N, Kacmaz A., Protective effect of MENSA (2-mercaptoethane sulfonate) against hepatic ischemia/reperfusion injury in rats. Surg Today 2005; 357: 575 - 580.
41. He SQ, Zhang YH, Venugopal SK, Dicus CW, Perez RV, Ramsamooj R, et al. Delivery of antioxidative enzyme genes protects against ischemia/reperfusion induced injury in mice. Liver Transpl 2006; 12: 1869 - 1879.
42. Menger MD, Vollmar B., Pathomechanisms of ischemia-reperfusion injury as the basis for novel preventive strategies: is it time for the introduction of pleiotropic compounds? Transplant Proc 2007; 39: 485 - 488.
43. D'Amico F, Vitale A, Bassi D, Bonsignore P, Scopelliti M, Boetto D, et al. Use of N-acetylcysteine during liver procurement: final report of a prospective randomized controlled study. Liver Transpl 2010; 16 (6): S71.
44. Grattaglino 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.
45. 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.