Induction and regulation of hepatocyte apoptosis by oxidative stress

Antioxidants and Redox Signaling

Volumn 4, Issue 5, 2002, Pages 759-767

  Czaja, Mark J ^a  

^a ALBERT EINSTEIN COLLEGE OF MEDICINE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

BILE ACID; CYTOCHROME P450; IMMUNOGLOBULIN ENHANCER BINDING PROTEIN; MITOGEN ACTIVATED PROTEIN KINASE; REACTIVE OXYGEN METABOLITE; TOXIN; TRANSCRIPTION FACTOR; TRANSCRIPTION FACTOR AP 1; TRANSFORMING GROWTH FACTOR BETA1; TUMOR NECROSIS FACTOR ALPHA;

APOPTOSIS; CELL DEATH; CHEMICAL INTERACTION; CONTROLLED STUDY; ENZYME INDUCTION; HUMAN; HUMAN CELL; INFLAMMATION; LIVER CELL; LIVER INJURY; LIVER ISCHEMIA; METABOLISM; OXIDATION; OXIDATION REDUCTION REACTION; OXIDATIVE STRESS; PRIORITY JOURNAL; REVIEW; SIGNAL TRANSDUCTION;

EID: 0036775096     PISSN: 15230864     EISSN: None     Source Type: Journal    
DOI: 10.1089/152308602760598909     Document Type: Review

References (71)

1. Adamson GM and Billings RE. Tumor necrosis factor induced oxidative stress in isolated mouse hepatocytes. Arch Biochem Biophys 294: 223-229, 1992.
2. Albano E, Clot P, Morimoto M, Thomasi A, Ingelman-Sundberg M, and French SW. Role of cytochrome P450 2El-dependent formation of hydroxyethyl free radical in the development of liver damage in rats intragastrically fed with ethanol. Hepatology 23: 155-163, 1996.
3. Arias-Dias J, Vara E, Garcia C, Villa N, Rodriquez JM, Ortiz P, and Balibrea JL. S-Adenosylmethionine protects hepatocytes against the effects of cytokines. J Surg Res 62: 79-84, 1996.
4. Bai J and Cederbaum Al. Overexpression of catalase in the mitochondrial or cytosolic compartment increases sensitivity of HepG2 cells to tumor necrosis factor-α-induced apoptosis. J Biol Chem 275: 19241-19249, 2000.
5. Benedetti A, Brunelli E, Risicate R, Cilluffo T, Jezequel A-M, and Orlandi F. Subcellular changes and apoptosis induced by ethanol in rat liver. J Hepatol 6: 137-143, 1988.
6. Bradham CA, Qian T, Streetz K, Trautwein C, Brenner DA, and Lemasters JJ. The mitochondrial permeability transition is required for tumor necrosis factor alpha-mediated apoptosis and cytochrome c release. Mol Cell Biol 18: 6353-6364, 1998.
7. Caldwell-Kenkel JC, Currin RT, Tanaka Y, Thurman RG, and Lemasters JJ. Reperfusion injury to endothelial cells following cold storage of rat livers. Hepatology 10: 292-299, 1989.
8. Colell A, Garcia-Ruiz C, Miranda M, Ardite E, Mari M, Morales A, Corrales F, Kaplowitz N, and Ferndndez-Checa JC. Selective glutathione depletion of mitochondria by ethanol sensitizes hepatocytes to tumor necrosis factor. Gastroenterology 115: 1541-1551, 1998.
9. Cursio R, Gugenheim J, Ricci JE, Crenesse D, Rostagno P, Maulon L, Saint-Paul MC, and Auberger AP. A caspase inhibitor fully protects rats against lethal normothermic liver ischemia by inhibition of liver apoptosis. FASEB J 13: 253-261, 1999.
10. Czaja MJ, Schilsky ML, Xu Y, Schmiedeberg P, Compton A, Ridnour L, and Oberley LW. Induction of MnSOD gene expression in a hepatic model of TNF-α toxicity does not result in increased protein. Am J Physiol 266: G737-G744, 1994.
11. Diez-Fernandez C, Sanz N, Alvarez AM, Wolf A, and Cascales M. The effect of nongenotoxic carcinogens, phenobarbital and clofibrate, on the relationship between reactive oxygen species, antioxidant enzyme expression and apoptosis. Carcinogenesis 19: 1715-1722, 1998.
12. Ding WX, Shen HM, and Ong CN. Critical role of reactive oxygen species and mitochondrial permeability transition in microcystin-induced rapid apoptosis in rat hepatocytes. Hepatology 32: 547-555, 2000.
13. Ekstrom G and Ingelman-Sundberg M. Rat liver microsomal NADPH-supported oxidase activity and lipid peroxidation dependent on ethanol-inducible cytochrome P-450 (P-450IIE1). Biochem Pharmacol 38: 1313-1319, 1989.
14. Fan G, Ma X, Kren BT, and Steer CJ. The retinoblastoma gene product inhibits TGF-β1 induced apoptosis in primary rat hepatocytes and human HuH-7 hepatoma cells. Oncogene 12: 1909-1919, 1996.
15. Faubion WA, Guicciardi ME, Miyoshi H, Bronk SF, Roberts PJ, Svingen PA, Kaufmann SH, and Gores GJ. Toxic bile salts induce rodent hepatocyte apoptosis via direct activation of Fas. J Clin Invest 103: 137-145, 1999.
16. Fernandez-Checa JC, Garcia-Ruiz C, Ookhtens M, and Kaplowitz N. Impaired uptake of glutathione by hepatic mitochondria from chronic ethanol-fed rats. J Clin Invest 87: 397-405, 1991.
17. Ferret P-J, Hammoud R, Tulliez M, Tran A, Trébéden H, Jaffray P, Malassagne B, Calmus Y, Weill B, and Batteux F. Detoxification of reactive oxygen species by a nonpeptidyl mimic of superoxide dismutase cures acetaminophen-induced acute liver failure in the mouse. Hepatology 33: 1173-1180, 2001.
18. Fischer MA, Eversole RR, Beuving LJ, and Jaeschke H. Sinusoidal endothelial cell and parenchymal cell injury during endotoxemia and hepatic ischemia-reperfusion: Protection by the 21-aminosteroid tirilazad mesylate. Int Hepatol Commun 6: 121-129, 1997.
19. Goldin RD, Hunt NC, Clark J, and Wickramasinghe SN. Apoptotic bodies in a murine model of alcoholic liver disease: Reversibility of ethanol-induced changes. J Pathol 171: 73-76, 1993.
20. Gujral JS, Bucci TJ, Farhood A, and Jaeschke H. Mechanism of cell death during warm hepatic ischemia-reperfusion in rats: Apoptosis or necrosis? Hepatology 33: 397-405, 2001.
21. Haouzi D, Lekehal M, Moreau A, Moulis C, Feldmann G, Robin MA, Letteron P, Fau PD, and Pessayre D. Cytochrome P450-generated reactive metabolites cause mitochondrial permeability transition, caspase activation, and apoptosis in rat hepatocytes. Hepatology 32: 303-311, 2000.
22. Haouzi D, Lekehal M, Tinel M, Vadrot N, Caussanel L, Lettéron P, Moreau A, Feldmann G, Fau D, and Pessayre D. Prolonged, but not acute, glutathione depletion promotes fas-mediated mitochondrial permeability transition and apoptosis in mice. Hepatology 33: 1181-1188, 2001.
23. Hentze H, Gantner F, Kolb SA, and Wendel A. Depletion of hepatic glutathione prevents death receptor-dependent apoptotic and necrotic liver injury in mice. Am J Pathol 156: 2045-2056, 2000.
24. Herbst H, Milani S, Schuppan D, and Stein H. Temporal and spatial patterns of proto-oncogene expression at early stages of toxic liver injury in the rat. Lab Invest 65: 324-333, 1991.
25. Hug H, Strand S, Grambihler A, Galle J, Hack V, Stremmel W, Krammer PH, and Galle PR. Reactive oxygen intermediates are involved in the induction of CD95 ligand mRNA expression by cytostatic drugs in hepatoma cells. J Biol Chem 272: 28191-28193, 1997.
26. Inoue M. Protective mechanism against reactive oxygen species. In: The Liver: Biology and Pathobiology, edited by Arias IM, Boyer JL, Fausto N, Jakoby WB, Schachter DA, and Shafritz, DA. New York, NY: Raven Press, Ltd., 1994, pp. 443-459.
27. Jaeschke H. Kupffer cell-induced oxidant stress during hepatic ischemia-reperfusion: does the controversy continue? Hepatology 30: 1527-1528, 1999.
28. Jaeschke H. Reactive oxygen and mechanisms of inflammatory liver injury. J Gastroenterol Hepatol 15: 718-724, 2000.
29. Jaeschke H, Ho YS, Fisher MA, Lawson JA, and 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 29: 443-450, 1999.
30. Jones BE, Lo CR, Liu H, Pradhan Z, Garcia L, Srinivasan A, Valentino KL, and Czaja MJ. Role of caspases and NF-κB signaling in hydrogen peroxide- and superoxide-induced hepatocyte apoptosis. Am J Physiol Gastrointest Liver Physiol 278: G693-G699, 2000.
31. Jones BE, Lo CR, Liu H, Srinivasan A, Streetz K, Valentino KL, and Czaja MJ. Hepatocytes sensitized to tumor necrosis factor-α cytotoxicity undergo apoptosis through caspase-dependent and caspase-independent pathways. J Biol Chem 275: 705-712, 2000.
32. Kanno S, Ishikawa M, Takayanagi M, Takayanagi Y, and Sasaki K. Exposure to hydrogen peroxide induces cell death via apoptosis in primary cultured mouse hepatocytes. Biol Pharm Bull 22: 1296-1300, 1999.
33. Kayanoki Y, Fujii J, Suzuki K, Kawata S, Matsuzawa Y, and Taniguchi N. Suppression of antioxidative enzyme expression by transforming growth factor-β1 in rat hepatocytes. J Biol Chem 269: 15488-15492, 1994.
34. Kohli V, Selzner M, Madden JF, Bentley RC, and Clavien PA. Endothelial cell and hepatocyte deaths occur by apoptosis after ischemia-reperfusion injury in the rat liver. Transplantation 67: 1099-1105, 1999.
35. Kroemer G and Reed JC. Mitochondrial control of cell death. Nat Med 6: 513-519, 2000.
36. Kurose I, Higuchi H, Miura S, Saito H, Watanabe N, Hokari R, Hirokawa M, Takaishi M, Zeki S, Nakamura T, Ebinuma H, Kato S, and Ishii H. Oxidative stress-mediated apoptosis of hepatocytes exposed to acute ethanol intoxication. Hepatology 25: 368-378, 1997.
37. Leclercq IA, Farrell GC, Field J, Bell DR, Gonzalez FJ, and Robertson GR. CYP2E1 and CYP4A as microsomal catalysts of lipid peroxides in murine nonalcoholic steatohepatitis. J Clin Invest 105: 1067-1075, 2000.
38. Lee FYJ, Li Y, Zhu H, Yang SQ, Lin HZ, Trush M, and Diehl AM. Tumor necrosis factor increases mitochondrial oxidant production and induces expression of uncoupling protein-2 in the regenerating rat liver. Hepatology 29: 677-687, 1999.
39. Lee SST, Buters JTM, Pineau T, Fernandez-Salguero P, and Gonzalez FJ. Role of CYP2E1 in the hepatotoxicity of acetaminophen. J Biol Chem 271: 12063-12067, 1996.
40. Lemasters JJ. Mechanisms of hepatic toxicity V. Necrapoptosis and the mitochondrial permeability transition: shared pathways to necrosis and apoptosis. Am J Physiol 276: G1-G6, 1999.
41. Lin HL, Liu TY, Chau GY, Lui WY, and Chi CW. Comparison of 2-methoxyestradiol-induced, docetaxel-induced, and paclitaxel-induced apoptosis in hepatoma cells and its correlation with reactive oxygen species. Cancer 89: 983-994, 2000.
42. Liu H, Lo CR, Jones BE, Pradhan Z, Srinivasan A, Valentino KL, Stockert RJ, and Czaja MJ. Inhibition of cmyc expression sensitizes hepatocytes to tumor necrosis factor-induced apoptosis and necrosis. J Biol Chem 275: 40155-40162, 2000.
43. Liu SL, Degli Esposti S, Yao T, Diehl AM, and Zern MA. Vitamin E therapy of acute CCl4-induced hepatic injury in mice is associated with inhibition of nuclear factor kappa B binding. Hepatology 22: 1474-1481, 1995.
44. Mendelson KG, Contois L-R, Tevosian SG, Davis RJ, and Paulson KE. Independent regulation of JNK/p38 mitogen-activated protein kinases by metabolic oxidative stress in the liver. Proc Natl Acad Sci U S A 93: 12908-12913, 1996.
45. Morales A, Garcia-Ruiz C, Miranda M, Mari M, Colell A, Ardite E, and Fernandez-Checa JC. Tumor necrosis factor increases hepatocellular glutathione by transcriptional regulation of the heavy subunit chain of η-glutamylcysteine synthetase. J Biol Chem 272: 30371-30379, 1997.
46. Müller M, Strand S, Hug H, Heinemann E-M, Walczak H, Hofmann WJ, Stremmel W, Krammer PH, and Galle PR. Drug-induced apoptosis in hepatoma cells is mediated by the CD95 (APO-1/Fas) receptor/ligand system and involves activation of wild-type p53. J Clin Invest 99: 403-413, 1997.
47. Nanji AA and Zakim D. Alcoholic liver disease. In: Hepatology, edited by Zakim D and Boyer TD. Philadelphia, PA: W.B. Saunders, 1996, pp. 891-961.
48. Nishikawa Y, Carr BI, Wang M, Kar S, Finn F, Dowd P, Zheng ZB, Kerns J, and Naganathan S. Growth inhibition of hepatoma cells induced by vitamin K and its analogs. J Biol Chem 270: 28304-28310, 1995.
49. Öllinger K and Roberg K. Nutrient deprivation of cultured rat hepatocytes increases the desferrioxamine-available iron pool and augments the sensitivity of hydrogen peroxide. J Biol Chem 272: 23707-23711, 1997.
50. Osawa Y, Nagaki M, Banno Y, Yamada Y, Imose M, Nozawa Y, Moriwaki H, and Nakashima S. Possible involvement of reactive oxygen species in D-galactosamine-induced sensitization against tumor necrosis factor-α-induced hepatocyte apoptosis. J Cell Physiol 187: 374-385, 2001.
51. Pierce RH, Campbell JS, Stephenson AB, Franklin CC, Chaisson M, Poot M, Kavanagh TJ, Rabinovitch PS, and Fausto N. Disruption of redox homeostasis in tumor necrosis factor-induced apoptosis in a murine hepatocyte cell line. Am J Pathol 157: 221-236, 2000.]
52. Ribeiro A, Bronk SF, Roberts PJ, Urrutia R, and Gores GJ. The transforming growth factor beta (1)-inducible transcription factor TIEG1, mediates apoptosis through oxidative stress. Hepatology 30: 1490-1497, 1999.
53. Roberts RA, James NH, and Cosulich SC. The role of protein kinase B and mitogen-activated protein kinase in epidermal growth factor and tumor necrosis factor α-mediated rat hepatocyte survival and apoptosis. Hepatology 31: 420-427, 2000.
54. Rodrigues CMP, Fan G, Ma X, Kren BT, and Steer CJ. A novel role of ursodeoxycholic acid in inhibiting apoptosis by modulating mitochondrial membrane perturbation. J Clin Invest 101: 2790-2799, 1998.
55. Rust C, Karnitz LM, Paya CV, Moscat J, Simari RD, and Gores GJ. The bile acid taurochenodeoxycholate activates a phosphatidylinositol 3-kinase-dependent survival signaling cascade. J Biol Chem 275: 20210-20216, 2000.
56. Samali A, Nordgren H, Zhivotovsky B, Peterson E, and Orrenius S. A comparative study of apoptosis and necrosis in HepG2 cells: Oxidant-induced caspase inactivation leads to necrosis. Biochem Biophys Res Commun 255: 6-11, 1999.
57. Sanchez A, Alvarez AM, Benito AM, and Fabregat I. Apoptosis induced by transforming growth factor-β in fetal hepatocyte primary cultures: Involvement of reactive oxygen intermediates. J Biol Chem 271: 7416-7422, 1996.
58. Sanchez A, Alvarez AM, Benito M, and Fabregat I. Cycloheximide prevents apoptosis, reactive oxygen species production and glutathione depletion induced by transforming growth factor β in fetal rat hepatocytes in primary culture. Hepatology 26: 935-943, 1997.
59. Schmiedeberg P, Biempica L, and Czaja MJ. Timing of protooncogene expression varies in toxin-induced liver regeneration. J Cell Physiol 154: 294-300, 1993.
60. Stadler J, Bentz BG, Harbrecht BG, Di Silvio M, Curran RD, Billiar TR, Hoffman RA, and Simmons RL. Tumor necrosis factor alpha inhibits hepatocyte mitochondrial respiration. Ann Surg 216: 539-546, 1992.
61. Starke PE and Farber JL. Endogenous defenses against the cytotoxicity of hydrogen peroxide in cultured rat hepatocytes. J Biol Chem 260: 86-92, 1985.
62. Strand S, Hofmann WJ, Grambihler A, Hug H, Volkmann M, Otto G, Wesch H, Mariani SM, Hack V, Stremmel W, Krammer PH, and Galle PR. Hepatic failure and liver cell damage in acute Wilson's disease involve CD95 (APO-1/Fas) mediated apoptosis. Nat Med 4: 588-593, 1998.
63. Tsutsumi M, Lasker JM, Shimizu M, Rosman AS, and Lieber CS. The intralobular distribution of ethanol-inducible P450IIE1 in rat and human liver. Hepatology 10: 437-446, 1989.
64. Weltman MD, Farrell GC, and Liddle C. Increased hepatocyte CYP2E1 expression in a rat nutritional model of hepatic steatosis with inflammation. Gastroenterology 111: 1645-1653, 1996.
65. Weltman MD, Farrell GC, Hall P, Ingelman-Sundberg M, and Liddle C. Hepatic cytochrome P450 2E1 is increased in patients with nonalcoholic steatohepatitis. Hepatology 27: 128-133, 1998.
66. Wu D and Cederbaum AI. Ethanol cytotoxicity to a transfected HepG2 cell line expressing human cytochrome P4502E1. J Biol Chem 271: 23914-23919, 1996.
67. Xu Y, Bradham C, Brenner DA, and Czaja MJ. Hydrogen peroxide-induced liver cell necrosis is dependent on AP-1 activation. Am J Physiol 273: G795-G803, 1997.
68. Xu Y, Bialik S, Jones BE, Iimuro Y, Kitsis RN, Srinivasan A, Brenner DA, and Czaja MJ. NF-κB inactivation converts a hepatocyte cell line TNF-α response from proliferation to apoptosis. Am J Physiol 275: C1058-C1066, 1998.
69. Xu Y, Jones BE, Neufeld DS, and Czaja MJ. Glutathione modulates rat and mouse hepatocyte sensitivity to tumor necrosis factor α toxicity. Gastroenterology 115: 1229-1237, 1998.
70. Yerushalmi B, Dahl R, Devereaux MW, Gumpricht E, and Sokol RJ. Bile acid-induced rat hepatocyte apoptosis is inhibited by antioxidants and blockers of the mitochondrial permeability transition. Hepatology 33: 616-626, 2001.
71. Zwacka RM, Zhou W, Zhang Y, Darby CJ, Dudus L, Halldorson J, Oberley L, and Engelhardt JF. Redox gene therapy for ischemia/reperfusion injury of the liver reduces AP1 and NF-κB activation. Nat Med 4: 698-704, 1998.