Apoptosis signal-regulating kinase 1 inhibits hepatocarcinogenesis by controlling the tumor-suppressing function of stress-activated mitogen-activated protein kinase

Hepatology

Volumn 54, Issue 1, 2011, Pages 185-195

  Nakagawa, Hayato ^a   Hirata, Yoshihiro ^a   Takeda, Kohsuke ^a   Hayakawa, Yoku ^a   Sato, Takehiro ^a   Kinoshita, Hiroto ^a   Sakamoto, Kei ^b   Nakata, Wachiko ^a   Hikiba, Yohko ^b   Omata, Masao ^c   Yoshida, Haruhiko ^a   Koike, Kazuhiko ^a   Ichijo, Hidenori ^a   Maeda, Shin ^a,d  

^a UNIVERSITY OF TOKYO   (Japan)

^b INSTITUTE FOR ADULT DISEASES   (Japan)

^c YAMANASHI PREFECTURAL CENTRAL HOSPITAL   (Japan)

^d YOKOHAMA CITY UNIVERSITY   (Japan)

Author keywords

[No Author keywords available]

Indexed keywords

ADENOVIRUS VECTOR; APOPTOSIS SIGNAL REGULATING KINASE 1; DIETHYLNITROSAMINE; DNA; PROTEIN BCL 2; PROTEIN P21; STRESS ACTIVATED PROTEIN KINASE; SYNAPTOPHYSIN;

ADENOVIRUS; ANIMAL EXPERIMENT; ANIMAL MODEL; APOPTOSIS; ARTICLE; CANCER CELL; CANCER INHIBITION; CELL DEATH; CELL PROLIFERATION; CONTROLLED STUDY; DNA DAMAGE; ENZYME ACTIVATION; HUMAN; HUMAN CELL; IN VIVO STUDY; LIVER CARCINOGENESIS; LIVER CELL; LIVER CELL CARCINOMA; MOUSE; NONHUMAN; PRIORITY JOURNAL; SIGNAL TRANSDUCTION; UPREGULATION; WILD TYPE;

ANIMALS; APOPTOSIS; APOPTOSIS REGULATORY PROTEINS; CARCINOMA, HEPATOCELLULAR; CELL PROLIFERATION; DIETHYLNITROSAMINE; DISEASE MODELS, ANIMAL; HEPATOCYTES; LIVER NEOPLASMS; MALE; MAP KINASE KINASE 4; MAP KINASE KINASE KINASE 5; MEMBRANE PROTEINS; MICE; MICE, KNOCKOUT; MITOGEN-ACTIVATED PROTEIN KINASES; P38 MITOGEN-ACTIVATED PROTEIN KINASES; PROTO-ONCOGENE PROTEINS; SIGNAL TRANSDUCTION; STRESS, PHYSIOLOGICAL;

EID: 79959535966     PISSN: 02709139     EISSN: 15273350     Source Type: Journal    
DOI: 10.1002/hep.24357     Document Type: Article

References (38)

1. El-Serag HB, Rudolph KL. Hepatocellular carcinoma: epidemiology and molecular carcinogenesis. Gastroenterology 2007; 132: 2557-2676.
2. Maeda S. NF-kappaB, JNK, and TLR signaling pathways in hepatocarcinogenesis. Gastroenterol Res Pract 2010; 2010: 367694.
3. Sakurai T, Maeda S, Chang L, 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 2006; 103: 10544-10551.
4. Hui L, Bakiri L, Mairhorfer A, Schweifer N, Haslinger C, Kenner L, et al. p38alpha suppresses normal and cancer cell proliferation by antagonizing the JNK-c-Jun pathway. Nat Genet 2007; 39: 741-749.
5. Hui L, Zatloukal K, Scheuch H, Stepniak E, Wagner EF. Proliferation of human HCC cells and chemically induced mouse liver cancers requires JNK1-dependent p21 downregulation. J Clin Invest 2008; 118: 3943-3953.
6. Sakurai T, He G, Matsuzawa A, Yu GY, Maeda S, Hardiman G, et al. Hepatocyte necrosis induced by oxidative stress and IL-1 alpha release mediate carcinogen-induced compensatory proliferation and liver tumorigenesis. Cancer Cell 2008; 14: 156-165.
7. Wagner EF, Nebreda AR. Signal integration by JNK and p38 MAPK pathways in cancer development. Nat Rev Cancer 2009; 9: 537-549.
8. She QB, Chen N, Bode AM, Flavell RA, Dong Z. Deficiency of c-Jun-NH(2)-terminal kinase-1 in mice enhances skin tumor development by 12-O-tetradecanoylphorbol-13-acetate. Cancer Res 2002; 62: 1343-1348.
9. Shibata W, Maeda S, Hikiba Y, Yanai A, Sakamoto K, Nakagawa H, et al. c-Jun NH2-terminal kinase 1 is a critical regulator for the development of gastric cancer in mice. Cancer Res 2008; 68: 5031-5039.
10. Takeda K, Noguchi T, Naguro I, Ichijo H. Apoptosis signal-regulating kinase 1 in stress and immune response. Annu Rev Pharmacol Toxicol 2008; 48: 199-225.
11. Ichijo H, Nishida E, Irie K, ten Dijke P, Saitoh M, Moriguchi T, et al. Induction of apoptosis by ASK1, a mammalian MAPKKK that activates SAPK/JNK and p38 signaling pathways. Science 1997; 275: 90-94.
12. Nakagawa H, Maeda S, Hikiba Y, Ohmae T, Shibata W, Yanai A, et al. Deletion of apoptosis signal-regulating kinase 1 attenuates acetaminophen-induced liver injury by inhibiting c-Jun N-terminal kinase activation. Gastroenterology 2008; 135: 1311-1321.
13. Iriyama T, Takeda K, Nakamura H, Morimoto Y, Kuroiwa T, Mizukami J, et al. ASK1 and ASK2 differentially regulate the counteracting roles of apoptosis and inflammation in tumorigenesis. EMBO J 2009; 28: 843-853.
14. Hayakawa Y, Hirata Y, Nakagawa H, Sakamoto K, Hikiba Y, Otsuka M, et al. Apoptosis signal-regulating kinase 1 regulates colitis and colitis-associated tumorigenesis by the innate immune responses. Gastroenterology 2010; 138: 1055-1067.
15. Tobiume K, Matsuzawa A, Takahashi T, Nishitoh H, Morita K, Takeda K, et al. ASK1 is required for sustained activations of JNK/p38 MAP kinases and apoptosis. EMBO Rep 2001; 2: 222-228.
16. Tobiume K, Saitoh M, Ichijo H. Activation of apoptosis signal-regulating kinase 1 by the stress-induced activating phosphorylation of pre-formed oligomer. J Cell Physiol 2002; 191: 95-104.
17. Nagai H, Noguchi T, Homma K, Katagiri K, Takeda K, Matsuzawa A, et al. Ubiquitin-like sequence in ASK1 plays critical roles in the recognition and stabilization by USP9X and oxidative stress-induced cell death. Mol Cell 2009; 36: 805-818.
18. Saitoh M, Nishitoh H, Fujii M, Takeda K, Tobiume K, Sawada Y, et al. Mammalian thioredoxin is a direct inhibitor of apoptosis signal-regulating kinase (ASK) 1. EMBO J 1998; 17: 2596-2606.
19. Corazza N, Jakob S, Schaer C, Frese S, Keogh A, Stroka D, et al. TRAIL receptor-mediated JNK activation and Bim phosphorylation critically regulate Fas-mediated liver damage and lethality. J Clin Invest 2006; 116: 2493-2499.
20. Kaufmann T, Jost PJ, Pellegrini M, Puthalakath H, Gugasyan R, Gerondakis S, et al. Fatal hepatitis mediated by tumor necrosis factor TNF-alpha requires caspase-8 and involves the BH3-only proteins Bid and Bim. Immunity 2009; 30: 56-66.
21. French LE, Tschopp J. Defective death receptor signaling as a cause of tumor immune escape. Semin Cancer Biol 2002; 12: 51-55.
22. Walter D, Schmich K, Vogel S, Pick R, Kaufmann T, Hochmuth FC, et al. Switch from type II to I Fas/CD95 death signaling on in vitro culturing of primary hepatocytes. HEPATOLOGY 2008; 48: 1942-1953.
23. Faouzi S, Burckhardt BE, Hanson JC, Campe CB, Schrum LW, Rippe RA, et al. Anti-Fas induces hepatic chemokines and promotes inflammation by an NF-kappa B-independent, caspase-3-dependent pathway. J Biol Chem 2001; 276: 49077-49082.
24. Chen D, Zhou Q. Caspase cleavage of BimEL triggers a positive feedback amplification of apoptotic signaling. Proc Natl Acad Sci U S A 2004; 101: 1235-1240.
25. Lei K, Davis RJ. JNK phosphorylation of Bim-related members of the Bcl2 family induces Bax-dependent apoptosis. Proc Natl Acad Sci U S A 2003; 100: 2432-2437.
26. Chen L, Park SM, Tumanov AV, Hau A, Sawada K, Feig C, et al. CD95 promotes tumour growth. Nature 2010; 465: 492-496.
27. Desbarats J, Newell MK. Fas engagement accelerates liver regeneration after partial hepatectomy. Nat Med 2000; 6: 920-923.
28. Maeda S, Chang L, Li ZW, Luo JL, Leffert H, Karin M. IKKbeta is required for prevention of apoptosis mediated by cell-bound but not by circulating TNF-alpha. Immunity 2003; 19: 725-737.
29. Maeda S, Kamata H, Luo JL, Leffert H, Karin M. IKKbeta couples hepatocyte death to cytokine-driven compensatory proliferation that promotes chemical hepatocarcinogenesis. Cell 2005; 121: 977-990.
30. Thornton TM, Rincon M. Non-classical p38 map kinase functions: cell cycle checkpoints and survival. Int J Biol Sci 2009; 5: 44-51.
31. Fabregat I, Roncero C, Fernandez M. Survival and apoptosis: a dysregulated balance in liver cancer. Liver Int 2007; 27: 155-162.
32. Saxena NK, Fu PP, Nagalingam A, Wang J, Handy J, Cohen C, et al. Adiponectin modulates C-jun N-terminal kinase and mammalian target of rapamycin and inhibits hepatocellular carcinoma. Gastroenterology 2010; 139: 1762-1773, 1773 e1-5.
33. Wang Y, Singh R, Lefkowitch JH, Rigoli RM, Czaja MJ. Tumor necrosis factor-induced toxic liver injury results from JNK2-dependent activation of caspase-8 and the mitochondrial death pathway. J Biol Chem 2006; 281: 15258-15267.
34. Das M, Garlick DS, Greiner DL, Davis RJ. The role of JNK in the development of hepatocellular carcinoma. Genes Dev 2011; 25: 634-645.
35. Dolado I, Swat A, Ajenjo N, De Vita G, Cuadrado A, Nebreda AR. p38alpha MAP kinase as a sensor of reactive oxygen species in tumorigenesis. Cancer Cell 2007; 11: 191-205.
36. Chang HY, Nishitoh H, Yang X, Ichijo H, Baltimore D. Activation of apoptosis signal-regulating kinase 1 (ASK1) by the adapter protein Daxx. Science 1998; 281: 1860-1863.
37. Youle RJ, Strasser A. The BCL-2 protein family: opposing activities that mediate cell death. Nat Rev Mol Cell Biol 2008; 9: 47-59.
38. Hatai T, Matsuzawa A, Inoshita S, Mochida Y, Kuroda T, Sakamaki K, et al. Execution of apoptosis signal-regulating kinase 1 (ASK1)-induced apoptosis by the mitochondria-dependent caspase activation. J Biol Chem 2000; 275: 26576-26581.