Antiapoptotic Effect of c-Jun N-terminal Kinase-1 through Mcl-1 Stabilization in TNF-Induced Hepatocyte Apoptosis

Gastroenterology

Volumn 136, Issue 4, 2009, Pages 1423-1434

  Kodama, Yuzo ^a   Taura, Kojiro ^a   Miura, Kouichi ^a   Schnabl, Bernd ^a   Osawa, Yosuke ^b   Brenner, David A ^a  

^a UNIVERSITY OF CALIFORNIA SAN DIEGO   (United States)

^b GIFU UNIVERSITY GRADUATE SCHOOL OF MEDICINE   (Japan)

Author keywords

[No Author keywords available]

Indexed keywords

GALACTOSAMINE; PROTEIN MCL 1; STRESS ACTIVATED PROTEIN KINASE 1; TUMOR NECROSIS FACTOR;

ADENOVIRUS; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; APOPTOSIS; ARTICLE; CONTROLLED STUDY; ENZYME ACTIVATION; ENZYME ACTIVITY; ENZYME SUBSTRATE; FEMALE; GENE DELETION; GENE OVEREXPRESSION; LIVER CELL; LIVER INJURY; MALE; MOUSE; MUTANT; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN PHOSPHORYLATION; PROTEIN STABILITY; REGULATORY MECHANISM; WILD TYPE;

EID: 62949138866     PISSN: 00165085     EISSN: None     Source Type: Journal    
DOI: 10.1053/j.gastro.2008.12.064     Document Type: Article

References (43)

1. Schwabe R.F., and Brenner D.A. Mechanisms of liver injury. I. TNF-alpha-induced liver injury: role of IKK, JNK, and ROS pathways. Am J Physiol Gastrointest Liver Physiol 290 (2006) G583-G589
2. Wajant H., Pfizenmaier K., and Scheurich P. Tumor necrosis factor signaling. Cell Death Differ 10 (2003) 45-65
3. Micheau O., and Tschopp J. Induction of TNF receptor I-mediated apoptosis via two sequential signaling complexes. Cell 114 (2003) 181-190
4. Doi T.S., Marino M.W., Takahashi T., et al. Absence of tumor necrosis factor rescues RelA-deficient mice from embryonic lethality. Proc Natl Acad Sci U S A 96 (1999) 2994-2999
5. Geisler F., Algul H., Paxian S., and Schmid R.M. Genetic inactivation of RelA/p65 sensitizes adult mouse hepatocytes to TNF-induced apoptosis in vivo and in vitro. Gastroenterology 132 (2007) 2489-2503
6. Beraza N., Ludde T., Assmus U., et al. Hepatocyte-specific IKK gamma/NEMO expression determines the degree of liver injury. Gastroenterology 132 (2007) 2504-2517
7. Karin M., and Lin A. NF-kappaB at the crossroads of life and death. Nat Immunol 3 (2002) 221-227
8. Burstein E., and Duckett C.S. Dying for NF-kappaB?. Control of cell death by transcriptional regulation of the apoptotic machinery. Curr Opin Cell Biol 15 (2003) 732-737
9. Dong C., Yang D.D., Wysk M., Whitmarsh A.J., Davis R.J., and Flavell R.A. Defective T cell differentiation in the absence of Jnk1. Science 282 (1998) 2092-2095
10. Yang D.D., Conze D., Whitmarsh A.J., et al. Differentiation of CD4+ T cells to Th1 cells requires MAP kinase JNK2. Immunity 9 (1998) 575-585
11. Sabapathy K., Jochum W., Hochedlinger K., Chang L., Karin M., and Wagner E.F. Defective neural tube morphogenesis and altered apoptosis in the absence of both JNK1 and JNK2. Mech Dev 89 (1999) 115-124
12. Qiao L., Han S.I., Fang Y., et al. Bile acid regulation of C/EBPbeta, CREB, and c-Jun function, via the extracellular signal-regulated kinase and c-Jun NH2-terminal kinase pathways, modulates the apoptotic response of hepatocytes. Mol Cell Biol 23 (2003) 3052-3066
13. Schattenberg J.M., Singh R., Wang Y., et al. JNK1 but not JNK2 promotes the development of steatohepatitis in mice. Hepatology 43 (2006) 163-172
14. Malhi H., Bronk S.F., Werneburg N.W., and Gores G.J. Free fatty acids induce JNK-dependent hepatocyte lipoapoptosis. J Biol Chem 281 (2006) 12093-12101
15. Gunawan B.K., Liu Z.X., Han D., Hanawa N., Gaarde W.A., and Kaplowitz N. c-Jun N-terminal kinase plays a major role in murine acetaminophen hepatotoxicity. Gastroenterology 131 (2006) 165-178
16. Varfolomeev E.E., and Ashkenazi A. Tumor necrosis factor: an apoptosis JuNKie?. Cell 116 (2004) 491-497
17. Liu J., and Lin A. Role of JNK activation in apoptosis: a double-edged sword. Cell Res 15 (2005) 36-42
18. Weston C.R., and Davis R.J. The JNK signal transduction pathway. Curr Opin Cell Biol 19 (2007) 142-149
19. De Smaele E., Zazzeroni F., Papa S., et al. Induction of gadd45beta by NF-kappaB downregulates pro-apoptotic JNK signalling. Nature 414 (2001) 308-313
20. Ventura J.J., Hubner A., Zhang C., Flavell R.A., Shokat K.M., and Davis R.J. Chemical genetic analysis of the time course of signal transduction by JNK. Mol Cell 21 (2006) 701-710
21. Chang L., Kamata H., Solinas G., et al. The E3 ubiquitin ligase itch couples JNK activation to TNFalpha-induced cell death by inducing c-FLIP(L) turnover. Cell 124 (2006) 601-613
22. Wang Y., Singh R., Lefkowitch J.H., Rigoli R.M., and Czaja M.J. Tumor necrosis factor-induced toxic liver injury results from JNK2-dependent activation of caspase-8 and the mitochondrial death pathway. J Biol Chem 281 (2006) 15258-15267
23. Kozopas K.M., Yang T., Buchan H.L., Zhou P., and Craig R.W. MCL1, a gene expressed in programmed myeloid cell differentiation, has sequence similarity to BCL2. Proc Natl Acad Sci U S A 90 (1993) 3516-3520
24. Craig R.W. MCL1 provides a window on the role of the BCL2 family in cell proliferation, differentiation and tumorigenesis. Leukemia 16 (2002) 444-454
25. Zhong Q., Gao W., Du F., and Wang X. Mule/ARF-BP1, a BH3-only E3 ubiquitin ligase, catalyzes the polyubiquitination of Mcl-1 and regulates apoptosis. Cell 121 (2005) 1085-1095
26. Opferman J.T. Unraveling MCL-1 degradation. Cell Death Differ 13 (2006) 1260-1262
27. Domina A.M., Vrana J.A., Gregory M.A., Hann S.R., and Craig R.W. MCL1 is phosphorylated in the PEST region and stabilized upon ERK activation in viable cells, and at additional sites with cytotoxic okadaic acid or taxol. Oncogene 23 (2004) 5301-5315
28. Maurer U., Charvet C., Wagman A.S., Dejardin E., and Green D.R. Glycogen synthase kinase-3 regulates mitochondrial outer membrane permeabilization and apoptosis by destabilization of MCL-1. Mol Cell 21 (2006) 749-760
29. Inoshita S., Takeda K., Hatai T., et al. Phosphorylation and inactivation of myeloid cell leukemia 1 by JNK in response to oxidative stress. J Biol Chem 277 (2002) 43730-43734
30. Kobayashi S., Lee S.H., Meng X.W., et al. Serine 64 phosphorylation enhances the antiapoptotic function of Mcl-1. J Biol Chem 282 (2007) 18407-18417
31. Schulze-Bergkamen H., Brenner D., Krueger A., et al. Hepatocyte growth factor induces Mcl-1 in primary human hepatocytes and inhibits CD95-mediated apoptosis via Akt. Hepatology 39 (2004) 645-654
32. Baskin-Bey E.S., Huang W., Ishimura N., Isomoto H., et al. Constitutive androstane receptor (CAR) ligand, TCPOBOP, attenuates Fas-induced murine liver injury by altering Bcl-2 proteins. Hepatology 44 (2006) 252-262
33. Osawa Y., Uchinami H., Bielawski J., Schwabe R.F., Hannun Y.A., and Brenner D.A. Roles for C16-ceramide and sphingosine 1-phosphate in regulating hepatocyte apoptosis in response to tumor necrosis factor-alpha. J Biol Chem 280 (2005) 27879-27887
34. Sabapathy K., Hochedlinger K., Nam S.Y., Bauer A., Karin M., and Wagner E.F. Distinct roles for JNK1 and JNK2 in regulating JNK activity and c-Jun-dependent cell proliferation. Mol Cell 15 (2004) 713-725
35. Jaeschke A., Karasarides M., Ventura J.J., et al. JNK2 is a positive regulator of the cJun transcription factor. Mol Cell 23 (2006) 899-911
36. Tuncman G., Hirosumi J., Solinas G., Chang L., Karin M., and Hotamisligil G.S. Functional in vivo interactions between JNK1 and JNK2 isoforms in obesity and insulin resistance. Proc Natl Acad Sci U S A 103 (2006) 10741-10746
37. Sieghart W., Losert D., Strommer S., et al. Mcl-1 overexpression in hepatocellular carcinoma: a potential target for antisense therapy. J Hepatol 44 (2006) 151-157
38. Opferman J.T., Letai A., Beard C., Sorcinelli M.D., Ong C.C., and Korsmeyer S.J. Development and maintenance of B and T lymphocytes requires antiapoptotic MCL-1. Nature 426 (2003) 671-676
39. Opferman J.T., Iwasaki H., Ong C.C., et al. Obligate role of anti-apoptotic MCL-1 in the survival of hematopoietic stem cells. Science 307 (2005) 1101-1104
40. Schulze-Bergkamen H., Fleischer B., Schuchmann M., et al. Suppression of Mcl-1 via RNA interference sensitizes human hepatocellular carcinoma cells towards apoptosis induction. BMC Cancer 6 (2006) 232
41. Sakurai T., Maeda S., Chang L., and Karin M. Loss of hepatic NF-kappa B activity enhances chemical hepatocarcinogenesis through sustained c-Jun N-terminal kinase 1 activation. Proc Natl Acad Sci U S A 103 (2006) 10544-10551
42. Sakurai T., He G., Matsuzawa A., et al. Hepatocyte necrosis induced by oxidative stress and IL-1 alpha release mediate carcinogen-induced compensatory proliferation and liver tumorigenesis. Cancer Cell 14 (2008) 156-165
43. Hui L., Zatloukal K., Scheuch H., Stepniak E., and Wagner E.F. Proliferation of human HCC cells and chemically induced mouse liver cancers requires JNK1-dependent p21 downregulation. J Clin Invest 118 (2008) 3943-3953