Chronic oxidative stress sensitizes hepatocytes to death from 4-hydroxynonenal by JNK/c-Jun overactivation

American Journal of Physiology - Gastrointestinal and Liver Physiology

Volumn 297, Issue 5, 2009, Pages

  Singh, Rajat ^a   Wang, Yongjun ^a   Schattenberg, Jörn M ^a   Xiang, Youqing ^a   Czaja, Mark J ^a  

^a ALBERT EINSTEIN COLLEGE OF MEDICINE   (United States)

Author keywords

Glutathione; Lipid peroxidation; Nonalcoholic fatty liver disease

Indexed keywords

4 HYDROXYNONENAL; CYTOCHROME P450 2E1; GLUTAMATE CYSTEINE LIGASE; GLUTATHIONE; MITOGEN ACTIVATED PROTEIN KINASE KINASE 4; STRESS ACTIVATED PROTEIN KINASE;

ANIMAL CELL; ANIMAL TISSUE; ARTICLE; CELL DEATH; CONTROLLED STUDY; DISEASE COURSE; ENZYME ACTIVITY; FATTY LIVER; LIPID PEROXIDATION; LIVER CELL DAMAGE; NONALCOHOLIC FATTY LIVER; NONHUMAN; OXIDATIVE STRESS; PATHOPHYSIOLOGY; PRIORITY JOURNAL; RAT;

ALDEHYDES; ANIMALS; APOPTOSIS; CATALASE; CELL DEATH; CELL LINE, TRANSFORMED; CYTOCHROME P-450 CYP2E1; EXTRACELLULAR SIGNAL-REGULATED MAP KINASES; GLUTAMATE-CYSTEINE LIGASE; GLUTATHIONE; GLUTATHIONE TRANSFERASE; HEAT-SHOCK RESPONSE; HEPATOCYTES; HYDROGEN PEROXIDE; JNK MITOGEN-ACTIVATED PROTEIN KINASES; MALEATES; MALONDIALDEHYDE; MAP KINASE KINASE 4; NECROSIS; OXIDATIVE STRESS; PHOSPHORYLATION; PROTO-ONCOGENE PROTEINS C-JUN; RATS; REACTIVE OXYGEN SPECIES; SIGNAL TRANSDUCTION; TRANSCRIPTION FACTOR AP-1; TRANSFECTION;

EID: 72249097158     PISSN: 01931857     EISSN: 15221547     Source Type: Journal    
DOI: 10.1152/ajpgi.00151.2009     Document Type: Article

References (47)

1. Anderson ME, Powrie F, Puri RN, Meister A. Glutathione monoethyl ester: preparation, uptake by tissues, and conversion to glutathione. Arch Biochem Biophys 239: 538-548, 1985. (Pubitemid 15013769)
2. Benedetti A, Comporti M, Fulceri R, Esterbauer H. Cytotoxic aldehydes originating from the peroxidation of liver microsomal lipids. Identification of 4,5-dihydroxydecenal. Biochim Biophys Acta 792: 172-181, 1984.
3. Botta D, Shi S, White CC, Dabrowski MJ, Keener CL, Srinouanprachanh SL, Farin FM, Ware CB, Ladiges WC, Pierce RH, Fausto N, Kavanagh TJ. Acetaminophen-induced liver injury is attenuated in male glutamate-cysteine ligase transgenic mice. J Biol Chem 281: 28865-28875, 2006. (Pubitemid 44507030)
4. Bradham CA, Hatano E, Brenner DA. Dominant-negative TAK1 induces c-Myc and G0 exit in liver. Am J Physiol Gastrointest Liver Physiol 281: G1279-G1289, 2001. (Pubitemid 33121719)
5. Bruckner SR, Estus S. JNK3 contributes to c-jun induction and apoptosis in 4-hydroxynonenal-treated sympathetic neurons. J Neurosci Res 70: 665-670, 2002. (Pubitemid 35397140)
6. Chalasani N, Deeg MA, Crabb DW. Systemic levels of lipid peroxidation and its metabolic and dietary correlates in patients with nonalcoholic steatohepatitis. Am J Gastroenterol 99: 1497-1502, 2004. (Pubitemid 39193189)
7. Chalasani N, Gorski JC, Asghar MS, Asghar A, Foresman B, Hall SD, Crabb DW. Hepatic cytochrome P450 2E1 activity in nondiabetic patients with nonalcoholic steatohepatitis. Hepatology 37: 544-550, 2003. (Pubitemid 36258775)
8. Chen Q, Cederbaum AI. Cytotoxicity and apoptosis produced by cytochrome P450 2E1 in Hep G2 cells. Mol Pharmacol 53: 638-648, 1998. (Pubitemid 28196485)
9. Chou JY. Temperature-sensitive adult liver cell line dependent on glucocorticoid for differentiation. Mol Cell Biol 3: 1013-1020, 1983.
10. Chou JY, Yeoh GC. Tyrosine aminotransferase gene expression in a temperature-sensitive adult rat liver cell line. Cancer Res 47: 5415-5420, 1987.
11. Czaja MJ. Cell signaling in oxidative stress-induced liver injury. Semin Liver Dis 27: 378-389, 2007. (Pubitemid 350071838)
12. Czaja MJ, Liu H, Wang Y. Oxidant-induced hepatocyte injury from menadione is regulated by ERK and AP-1 signaling. Hepatology 37: 1405-1413, 2003. (Pubitemid 36667321)
13. Hartley DP, Ruth JA, Petersen DR. The hepatocellular metabolism of 4-hydroxynonenal by alcohol dehydrogenase, aldehyde dehydrogenase, and glutathione S-transferase. Arch Biochem Biophys 316: 197-205, 1995.
14. Hattori M, Tugores A, Westwick JK, Veloz L, Leffert HL, Karin M, Brenner DA. Activation of activating protein 1 during hepatic acute phase response. Am J Physiol Gastrointest Liver Physiol 264: G95-G103, 1993. (Pubitemid 23055994)
15. Huan JY, Koop DR. Tightly regulated and inducible expression of rabbit CYP2E1 using a tetracycline-controlled expression system. Drug Metab Dispos 27: 549-554, 1999. (Pubitemid 29177650)
16. Iimuro Y, Nishiura T, Hellerbrand C, Behrns KE, Schoonhoven R, Grisham JW, Brenner DA. NFκB prevents apoptosis and liver dysfunction during liver regeneration. J Clin Invest 101: 802-811, 1998. (Pubitemid 28096077)
17. Ikura Y, Ohsawa M, Suekane T, Fukushima H, Itabe H, Jomura H, Nishiguchi S, Inoue T, Naruko T, Ehara S, Kawada N, Arakawa T, Ueda M. Localization of oxidized phosphatidylcholine in nonalcoholic fatty liver disease: impact on disease progression. Hepatology 43: 506-514, 2006.
18. Iles KE, Liu RM. Mechanisms of glutamate cysteine ligase (GCL) induction by 4-hydroxynonenal. Free Radic Biol Med 38: 547-556, 2005.
19. Jones BE, Liu H, Lo CR, Koop DR, Czaja MJ. Cytochrome P450 2E1 expression induces hepatocyte resistance to cell death from oxidative stress. Antioxid Redox Signal 4: 701-709, 2002.
20. Jones BE, Lo CR, Liu H, Srinivasan A, Streetz K, Valentino KL, 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. (Pubitemid 30039037)
21. Leclercq IA, Farrell GC, Field J, Bell DR, Gonzalez FJ, Robertson GR. CYP2E1 and CYP4A as microsomal catalysts of lipid peroxides in murine nonalcoholic steatohepatitis. J Clin Invest 105: 1067-1075, 2000. (Pubitemid 30217691)
22. Liu H, Jones BE, Bradham C, Czaja MJ. Increased cytochrome P-450 2E1 expression sensitizes hepatocytes to c-Jun-mediated cell death from TNF-α. Am J Physiol Gastrointest Liver Physiol 282: G257-G266, 2002. (Pubitemid 34651682)
23. Liu H, Lo CR, Czaja MJ. NF-κB inhibition sensitizes hepatocytes to TNF-induced apoptosis through a sustained activation of JNK and c-Jun. Hepatology 35: 772-778, 2002. (Pubitemid 34258370)
24. Liu H, Lo CR, Jones BE, Pradhan Z, Srinivasan A, Valentino KL, Stockert RJ, Czaja MJ. Inhibition of c-Myc expression sensitizes hepatocytes to tumor necrosis factor-induced apoptosis and necrosis. J Biol Chem 275: 40155-40162, 2000. (Pubitemid 32064643)
25. Liu RM, Borok Z, Forman HJ. 4-Hydroxy-2-nonenal increases γ-glutamylcysteine synthetase gene expression in alveolar epithelial cells. Am J Respir Cell Mol Biol 24: 499-505, 2001. (Pubitemid 32324740)
26. Lu SC. Regulation of hepatic glutathione synthesis: current concepts and controversies. FASEB J 13: 1169-1183, 1999.
27. Malhi H, Bronk SF, Werneburg NW, Gores GJ. Free fatty acids induce JNK-dependent hepatocyte lipoapoptosis. J Biol Chem 281: 12093-12101, 2006. (Pubitemid 43855473)
28. Mari M, Cederbaum AI. Induction of catalase, alpha, and microsomal glutathione S-transferase in CYP2E1 overexpressing HepG2 cells and protection against short-term oxidative stress. Hepatology 33: 652-661, 2001. (Pubitemid 32185228)
29. Mosmann T. Rapid colorimetric assay for cellular growth and survival: application to proliferation and cytotoxicity assays. J Immunol Methods 65: 55-63, 1983. (Pubitemid 14203433)
30. Pabst MJ, Habig WH, Jakoby WB. Glutathione S-transferase A. A novel kinetic mechanism in which the major reaction pathway depends on substrate concentration. J Biol Chem 249: 7140-7147, 1974.
31. Parola M, Robino G, Marra F, Pinzani M, Bellomo G, Leonarduzzi G, Chiarugi P, Camandola S, Poli G, Waeg G, Gentilini P, Dianzani MU. HNE interacts directly with JNK isoforms in human hepatic stellate cells. J Clin Invest 102: 1942-1950, 1998.
32. Poli G, Dianzani MU, Cheeseman KH, Slater TF, Lang J, Esterbauer H. Separation and characterization of the aldehydic products of lipid peroxidation stimulated by carbon tetrachloride or ADP-iron in isolated rat hepatocytes and rat liver microsomal suspensions. Biochem J 227: 629-638, 1985. (Pubitemid 15067738)
33. Schattenberg JM, Singh R, Wang Y, Lefkowitch JH, Rigoli RM, Scherer PE, Czaja MJ. JNK1 but not JNK2 promotes the development of steatohepatitis in mice. Hepatology 43: 163-172, 2006. (Pubitemid 43733603)
34. Schattenberg JM, Wang Y, Rigoli RM, Koop DR, Czaja MJ. CYP2E1 overexpression alters hepatocyte death from menadione and fatty acids by activation of ERK1/2 signaling. Hepatology 39: 444-455, 2004. (Pubitemid 38222185)
35. Schattenberg JM, Wang Y, Singh R, Rigoli RM, Czaja MJ. Hepatocyte CYP2E1 overexpression and steatohepatitis lead to impaired hepatic insulin signaling. J Biol Chem 280: 9887-9894, 2005. (Pubitemid 40395836)
36. Schwabe RF, Uchinami H, Qian T, Bennett BL, Lemasters JJ, Brenner DA. Differential requirement for c-Jun NH2-terminal kinase in TNFα- and Fas-mediated apoptosis in hepatocytes. FASEB J 18: 720-722, 2004.
37. Seelig GF, Meister A. Glutathione biosynthesis; γ-glutamylcysteine synthetase from rat kidney. Methods Enzymol 113: 379-390, 1985. (Pubitemid 16195807)
38. Siems WG, Zollner H, Grune T, Esterbauer H. Metabolic fate of 4-hydroxynonenal in hepatocytes: 1,4-dihydroxynonene is not the main product. J Lipid Res 38: 612-622, 1997. (Pubitemid 27166704)
39. Singh R, Wang Y, Xiang Y, Tanaka KE, Gaarde WA, Czaja MJ. Differential effects of JNK1 and JNK2 inhibition on murine steatohepatitis and insulin resistance. Hepatology 49: 87-96, 2008.
40. Tonks NK. Redox redux: revisiting PTPs and the control of cell signaling. Cell 121: 667-670, 2005.
41. Tsukamoto H, Horne W, Kamimura S, Niemela O, Parkkila S, Yla-Herttuala S, Brittenham GM. Experimental liver cirrhosis induced by alcohol and iron. J Clin Invest 96: 620-630, 1995.
42. Wang Y, Schattenberg JM, Rigoli RM, Storz P, Czaja MJ. Hepatocyte resistance to oxidative stress is dependent on protein kinase C-mediated down-regulation of c-Jun/AP-1. J Biol Chem 279: 31089-31097, 2004. (Pubitemid 39037770)
43. Weltman MD, Farrell GC, Hall P, Ingelman-Sundberg M, Liddle C. Hepatic cytochrome P450 2E1 is increased in patients with nonalcoholic steatohepatitis. Hepatology 27: 128-133, 1998. (Pubitemid 28041545)
44. Weltman MD, Farrell GC, Liddle C. Increased hepatocyte CYP2E1 expression in a rat nutritional model of hepatic steatosis with inflammation. Gastroenterology 111: 1645-1653, 1996. (Pubitemid 26404230)
45. Xu Y, Bialik S, Jones BE, Iimuro Y, Kitsis RN, Srinivasan A, Brenner DA, Czaja MJ. NF-κB inactivation converts a hepatocyte cell line TNF-α response from proliferation to apoptosis. Am J Physiol Cell Physiol 275: C1058-C1066, 1998. (Pubitemid 28491799)
46. Xu Y, Jones BE, Neufeld DS, Czaja MJ. Glutathione modulates rat and mouse hepatocyte sensitivity to tumor necrosis factor toxicity. Gastroenterology 115: 1229-1237, 1998. (Pubitemid 28485615)
47. Yaglom J, O'Callaghan-Sunol C, Gabai V, Sherman MY. Inactivation of dual-specificity phosphatases is involved in the regulation of extracellular signal-regulated kinases by heat shock and hsp72. Mol Cell Biol 23: 3813-3824, 2003. (Pubitemid 36597461)