Mechanisms of liver injury. I. TNF-α-induced liver injury: Role of IKK, JNK, and ROS pathways

American Journal of Physiology - Gastrointestinal and Liver Physiology

Volumn 290, Issue 4, 2006, Pages

  Schwabe, Robert F ^a   Brenner, David A ^a  

^a New York Presbyterian Columbia University Medical Center   (United States)

Author keywords

c Jun NH2 terminal kinase; Hepatocyte; I B kinase; Reactive oxygen species

Indexed keywords

CONCANAVALIN A; I KAPPA B KINASE; I KAPPA B KINASE INHIBITOR; REACTIVE OXYGEN METABOLITE; STRESS ACTIVATED PROTEIN KINASE; STRESS ACTIVATED PROTEIN KINASE INHIBITOR; TUMOR NECROSIS FACTOR ALPHA;

APOPTOSIS; CELL DEATH; CELL FUNCTION; CELL PROLIFERATION; ENZYME ACTIVITY; HEPATITIS; INFLAMMATION; ISCHEMIA; LIVER CARCINOGENESIS; LIVER CELL; LIVER CELL CARCINOMA; LIVER INJURY; LIVER REGENERATION; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN INTERACTION; PROTEIN PHOSPHORYLATION; REVIEW;

ANIMALS; HUMANS; I-KAPPA B KINASE; LIVER; MAP KINASE KINASE 4; REACTIVE OXYGEN SPECIES; REPERFUSION INJURY; SIGNAL TRANSDUCTION; TUMOR NECROSIS FACTOR-ALPHA;

EID: 33645799492     PISSN: 01931857     EISSN: 15221547     Source Type: Journal    
DOI: 10.1152/ajpgi.00422.2005     Document Type: Review

References (44)

1. Amanullah A, Azam N, Balliet A, Hollander C, Hoffman B, Fornace A, and Liebermann D. Cell signalling: cell survival and a Gadd45-factor deficiency. Nature 424: 741-742, 2003.
2. Aoki H, Kang PM, Hampe J, Yoshimura K, Noma T, Matsuzaki M, and Izumo S. Direct activation of mitochondrial apoptosis machinery by c-Jun N-terminal kinase in adult cardiac myocytes. J Biol Chem 277: 10244-10250, 2002.
3. Bonnard M, Mirtsos C, Suzuki S, Graham K, Huang J, Ng M, Itie A, Wakeham A, Shahinian A, Henzel WJ, Elia AJ, Shillinglaw W, Mak TW, Cao Z, and Yeh WC. Deficiency of T2K leads to apoptotic liver degeneration and impaired NF-κB-dependent gene transcription. EMBO J 19: 4976-4985, 2000.
4. Bradham CA, Qian T, Streetz K, Trautwein C, Brenner DA, and Lemasters JJ. The mitochondrial permeability transition is required for tumor necrosis factor α-mediated apoptosis and cytochrome c release. Mol Cell Biol 18: 6353-6364, 1998.
5. Chaisson ML, Brooling JT, Ladiges W, Tsai S, and Fausto N. Hepatocyte-specific inhibition of NF-κB leads to apoptosis after TNF treatment, but not after partial hepatectomy. J Clin Invest 110: 193-202, 2002.
6. 5a. Chang L, Kamata H, Solinas G, Luo JL, Maeda S, Venuprasad K, Liu YC, and Karin M. The E3 ubiquitin ligase Itch couples JNK activation to TNF-α-induced cell death by inducing c-FLIP(L) turnover. Cell 124: 601-613, 2006.
7. Chen LW, Egan L, Li ZW, Greten FR, Kagnoff MF, and Karin M. The two faces of IKK and NF-κB inhibition: prevention of systemic inflammation but increased local injury following intestinal ischemia-reperfusion. Nat Med 9: 575-581, 2003.
8. Colletti LM, Remick DG, Burtch GD, Kunkel SL, Strieter RM, and Campbell DA Jr. Role of tumor necrosis factor-α in the pathophysiologic alterations after hepatic ischemia/reperfusion injury in the rat. J Clin Invest 85: 1936-1943, 1990.
9. Deng Y, Ren X, Yang L, Lin Y, and Wu X. A JNK-dependent pathway is required for TNFα-induced apoptosis. Cell 115: 61-70, 2003.
10. De Smaele E, Zazzeroni F, Papa S, Nguyen DU, Jin R, Jones J, Cong R, and Franzoso G. Induction of gadd45β by NF-κB downregulates pro-apoptotic JNK signalling. Nature 414: 308-313, 2001.
11. Fan C, Li Q, Zhang Y, Liu X, Luo M, Abbott D, Zhou W, and Engelhardt JF. IκBα and IκBβ possess injury context-specific functions that uniquely influence hepatic NF-κB induction and inflammation. J Clin Invest 113: 746-755, 2004.
12. Ghosh S and Karin M. Missing pieces in the NF-κB puzzle. Cell 109, Suppl: S81-S96, 2002.
13. Goossens V, Grooten J, De Vos K, and Fiers W. Direct evidence for tumor necrosis factor-induced mitochondrial reactive oxygen intermediates and their involvement in cytotoxicity. Proc Natl Acad Sci USA 92: 8115-8119, 1995.
14. Grell M, Zimmermann G, Gottfried E, Chen CM, Grunwald U, Huang DC, Wu Lee YH, Durkop H, Engelmann H, Scheurich P, Wajant H, and Strasser A. Induction of cell death by tumour necrosis factor (TNF) receptor 2, CD40 and CD30: a role for TNF-R1 activation by endogenous membrane-anchored TNF. EMBO J 18: 3034-3043, 1999.
15. Ha HC and Snyder SH. Poly(ADP-ribose) polymerase is a mediator of necrotic cell death by ATP depletion. Proc Natl Acad Sci USA 96: 13978-13982, 1999.
16. Hoeflich KP, Luo J, Rubie EA, Tsao MS, Jin O, and Woodgett JR. Requirement for glycogen synthase kinase-3β in cell survival and NF-κB activation. Nature 406: 86-90, 2000.
17. Jaeschke H and Lemasters JJ. Apoptosis versus oncotic necrosis in hepatic ischemia/reperfusion injury. Gastroenterology 125: 1246-1257, 2003.
18. Kamata H, Honda S, Maeda S, Chang L, Hirata H, and Karin M. Reactive oxygen species promote TNFα-induced death and sustained JNK activation by inhibiting MAP kinase phosphatases. Cell 120: 649-661, 2005.
19. Kucharczak J, Simmons MJ, Fan Y, and Gelinas C. To be, or not to be: NF-κB is the answer - role of Rel/NF-κB in the regulation of apoptosis. Oncogene 22: 8961-8982, 2003.
20. Lehmann TG, Wheeler MD, Schwabe RF, Connor HD, Schoonhoven R, Bunzendahl H, Brenner DA, Jude Samulski R, Zhong Z, and Thurman RG. Gene delivery of Cu/Zn-superoxide dismutase improves graft function after transplantation of fatty livers in the rat. Hepatology 32: 1255-1264, 2000.
21. Liu H, Lo CR, and 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.
22. Liu J, Minemoto Y, and Lin A. c-Jun N-terminal protein kinase 1 (JNK1), but not JNK2, is essential for tumor necrosis factor α-induced c-Jun kinase activation and apoptosis. Mol Cell Biol 24: 10844-10856, 2004.
23. Luedde T, Assmus U, Wustefeld T, Meyer zu Vilsendorf A, Roskams T, Schmidt-Supprian M, Rajewsky K, Brenner DA, Manns MP, Pasparakis M, and Trautwein C. Deletion of IKK2 in hepatocytes does not sensitize these cells to TNF-induced apoptosis but protects from ischemia/reperfusion injury. J Clin Invest 115: 849-859, 2005.
24. Maeda S, Chang L, Li ZW, Luo JL, Leffert H, and Karin M. IKKβ is required for prevention of apoptosis mediated by cell-bound but not by circulating TNFα. Immunity 19: 725-737, 2003.
25. Maeda S, Kamata H, Luo JL, Leffert H, and Karin M. IKKβ couples hepatocyte death to cytokine-driven compensatory proliferation that promotes chemical hepatocarcinogenesis. Cell 121: 977-990, 2005.
26. Rudiger HA and Clavien PA. Tumor necrosis factor α, but not Fas, mediates hepatocellular apoptosis in the murine ischemic liver. Gastroenterology 122: 202-210, 2002.
27. Sabapathy K, Hochedlinger K, Nam SY, Bauer A, Karin M, and Wagner EF. Distinct roles for JNK1 and JNK2 in regulating JNK activity and c-Jun-dependent cell proliferation. Mol Cell 15: 713-725, 2004.
28. Sakon S, Xue X, Takekawa M, Sasazuki T, Okazaki T, Kojima Y, Piao JH, Yagita H, Okumura K, Doi T, and Nakano H. NF-κB inhibits TNF-induced accumulation of ROS that mediate prolonged MAPK activation and necrotic cell death. EMBO J 22: 3898-3909, 2003.
29. Schwabe RF, Bennett BL, Manning AM, and Brenner DA. Differential role of IκB kinase 1 and 2 in primary rat hepatocytes. Hepatology 33: 81-90, 2001.
30. Schwabe RF, Bradham CA, Uehara T, Hatano E, Bennett BL, Schoonhoven R, and Brenner DA. c-Jun-N-terminal kinase drives cyclin D1 expression and proliferation during liver regeneration. Hepatology 37: 824-832, 2003.
31. Schwabe RF and Brenner DA. Role of glycogen synthase kinase-3 in TNF-α-induced NF-βB activation and apoptosis in hepatocytes. Am J Physiol Gastrointest Liver Physiol 283: G204-G211, 2002.
32. Schwabe RF and Sakurai H. IKKβ phosphorylates p65 at S468 in transactivation domain 2. FASEB J 19: 1758-1760, 2005.
33. Schwabe RF, Uchinami H, Qian T, Bennett BL, Lemasters JJ, and Brenner DA. Differential requirement for c-Jun NH2-terminal kinase in TNFα- and Fas-mediated apoptosis in hepatocytes. FASEB J 18: 720-722, 2004.
34. Senftleben U, Cao Y, Xiao G, Greten FR, Krahn G, Bonizzi G, Chen Y, Hu Y, Fong A, Sun SC, and Karin M. Activation by IKKα of a second, evolutionary conserved, NF-κB signaling pathway. Science 293: 1495-1499, 2001.
35. Shen HM, Lin Y, Choksi S, Tran J, Jin T, Chang L, Karin M, Zhang J, and Liu ZG. Essential roles of receptor-interacting protein and TRAF2 in oxidative stress-induced cell death. Mol Cell Biol 24: 5914-5922, 2004.
36. Streetz K, Fregien B, Plumpe J, Korber K, Kubicka S, Sass G, Bischoff SC, Manns MP, Tiegs G, and Trautwein C. Dissection of the intracellular pathways in hepatocytes suggests a role for Jun kinase and IFN regulatory factor-1 in Con A-induced liver failure. J Immunol 167: 514-523, 2001.
37. Suetsugu H, Iimuro Y, Uehara T, Nishio T, Harada N, Yoshida M, Hatano E, Son G, Fujimoto J, and Yamaoka Y. Nuclear factor κB inactivation in the rat liver ameliorates short term total warm ischaemia/ reperfusion injury. Gut 54: 835-842, 2005.
38. Tang G, Minemoto Y, Dibling B, Purcell NH, Li Z, Karin M, and Lin A. Inhibition of JNK activation through NF-κB target genes. Nature 414: 313-317, 2001.
39. Tournier C, Dong C, Turner TK, Jones SN, Flavell RA, and Davis RJ. MKK7 is an essential component of the JNK signal transduction pathway activated by proinflammatory cytokines. Genes Dev 15: 1419-1426, 2001.
40. Uchinami H, Yamamoto Y, Kume M, Yonezawa K, Ishikawa Y, Taura K, Nakajima A, Hata K, and Yamaoka Y. Effect of heat shock preconditioning on NF-κB/I-κB pathway during I/R injury of the rat liver. Am J Physiol Gastrointest Liver Physiol 282: G962-G971, 2002.
41. Uehara T, Bennett B, Sakata ST, Satoh Y, Bilter GK, Westwick JK, and Brenner DA. JNK mediates hepatic ischemia reperfusion injury. J Hepatol 42: 850-859, 2005.
42. Uehara T, Xi Peng X, Bennett B, Satoh Y, Friedman G, Currin R, Brenner DA, and Lemasters J. c-Jun N-terminal kinase mediates hepatic injury after rat liver transplantation. Transplantation 78: 324-332, 2004.
43. Vercammen D, Beyaert R, Denecker G, Goossens V, Van Loo G, Declercq W, Grooten J, Fiers W, and Vandenabeele P. Inhibition of caspases increases the sensitivity of L929 cells to necrosis mediated by tumor necrosis factor. J Exp Med 187: 1477-1485, 1998.
44. Wajant H, Pfizenmaier K, and Scheurich P. Tumor necrosis factor signaling. Cell Death Differ 10: 45-65, 2003.