IKKβ couples hepatocyte death to cytokine-driven compensatory proliferation that promotes chemical hepatocarcinogenesis

Cell

Volumn 121, Issue 7, 2005, Pages 977-990

  Maeda, Shin ^a,b   Kamata, Hideaki ^a,b   Luo, Jun Li ^a,b   Leffert, Hyam ^b   Karin, Michael ^a,b  

^a UNIVERSITY OF CALIFORNIA   (United States)

^b San Diego   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CYTOKINE; DIETHYLNITROSAMINE; I KAPPA B KINASE; MITOGENIC AGENT; REACTIVE OXYGEN METABOLITE; STRESS ACTIVATED PROTEIN KINASE; CARCINOGEN; CHUK PROTEIN, MOUSE; IKBKB PROTEIN, MOUSE; IKBKE PROTEIN, MOUSE; PROTEIN SERINE THREONINE KINASE;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CELL DEATH; CELL PROLIFERATION; CELL REGENERATION; CONTROLLED STUDY; CORRELATION ANALYSIS; ENZYME ACTIVATION; FEMALE; INFLAMMATION; KUPFFER CELL; LIVER CANCER; LIVER CARCINOGENESIS; LIVER CELL; MALE; MOUSE; NONHUMAN; PRIORITY JOURNAL; ANIMAL; C57BL MOUSE; CELL TRANSFORMATION; CHEMICALLY INDUCED DISORDER; DISEASE MODEL; DRUG ANTAGONISM; DRUG EFFECT; GENETICS; LIVER REGENERATION; LIVER TUMOR; METABOLISM; MOUSE MUTANT; OXIDATIVE STRESS; PATHOLOGY; PHYSIOLOGY; TRANSGENIC MOUSE;

ANIMALS; CARCINOGENS; CELL DEATH; CELL PROLIFERATION; CELL TRANSFORMATION, NEOPLASTIC; CYTOKINES; DIETHYLNITROSAMINE; DISEASE MODELS, ANIMAL; FEMALE; HEPATOCYTES; I-KAPPA B KINASE; INFLAMMATION; JNK MITOGEN-ACTIVATED PROTEIN KINASES; KUPFFER CELLS; LIVER NEOPLASMS, EXPERIMENTAL; LIVER REGENERATION; MALE; MICE; MICE, INBRED C57BL; MICE, KNOCKOUT; MICE, TRANSGENIC; OXIDATIVE STRESS; PROTEIN-SERINE-THREONINE KINASES; REACTIVE OXYGEN SPECIES;

EID: 21244472975     PISSN: 00928674     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.cell.2005.04.014     Document Type: Article

References (54)

1. S. Akira, H. Isshiki, T. Sugita, O. Tanabe, S. Kinoshita, Y. Nishio, T. Nakajima, T. Hirano, and T. Kishimoto A nuclear factor for IL-6 expression (NF-IL6) is a member of a C/EBP family EMBO J. 9 1990 1897 1906
2. I. Berenblum Carcinogenesis and tumor pathogenesis Adv. Cancer Res. 2 1954 129 175
3. F.X. Bosch, J. Ribes, M. Diaz, and R. Cleries Primary liver cancer: worldwide incidence and trends Gastroenterology 127 2004 S5 S16
4. L.G. Cavin, M. Venkatraman, V.M. Factor, S. Kaur, I. Schroeder, F. Mercurio, A.A. Beg, S.S. Thorgeirsson, and M. Arsura Regulation of α-fetoprotein by NF-κB protects hepatocytes from TNFα cytotoxicity during fetal liver development and hepatic oncogenesis Cancer Res. 64 2004 7030 7038
5. F.V. Chisari Hepatitis B virus transgenic mice: insights into the virus and the disease Hepatology 22 1995 1316 1325
6. L.M. Coussens, and Z. Werb Inflammation and cancer Nature 420 2002 860 867
7. M. Dajee, M. Lazarov, J.Y. Zhang, T. Cai, C.L. Green, A.J. Russell, M.P. Marinkovich, S. Tao, Q. Lin, Y. Kubo, and P.A. Khavari NF-κB blockade and oncogenic Ras trigger invasive human epidermal neoplasia Nature 421 2003 639 643
8. M.C. Dyroff, F.C. Richardson, J.A. Popp, M.A. Bedell, and J.A. Swenberg Correlation of O4-ethyldeoxythymidine accumulation, hepatic initiation and hepatocellular carcinoma induction in rats continuously administered diethylnitrosamine Carcinogenesis 7 1986 241 246
9. R. Eferl, R. Ricci, L. Kenner, R. Zenz, J.P. David, M. Rath, and E.F. Wagner Liver tumor development. c-Jun antagonizes the proapoptotic activity of p53 Cell 112 2003 181 192
10. H. Esterbauer, and K.H. Cheeseman Determination of aldehydic lipid peroxidation products: malonaldehyde and 4-hydroxynonenal Methods Enzymol. 186 1990 407 421
11. V.M. Factor, D. Laskowska, M.R. Jensen, J.T. Woitach, N.C. Popescu, and S.S. Thorgeirsson Vitamin E reduces chromosomal damage and inhibits hepatic tumor formation in a transgenic mouse model Proc. Natl. Acad. Sci. USA 97 2000 2196 2201
12. J.L. Farber, and R.J. Gerson Mechanisms of cell injury with hepatotoxic chemicals Pharmacol. Rev. 36 1984 71S 75S
13. N. Fausto Mouse liver tumorigenesis: models, mechanisms, and relevance to human disease Semin. Liver Dis. 19 1999 243 252
14. N. Fausto Liver regeneration J. Hepatol. Suppl. 1 32 2000 19 31
15. S. Ghosh, and M. Karin Missing pieces in the NF-κB puzzle Cell Suppl. 109 2002 S81 S96
16. F.R. Greten, L. Eckmann, T.F. Greten, J.M. Park, Z.W. Li, L.J. Egan, M.F. Kagnoff, and M. Karin IKKβ links inflammation and tumorigenesis in a mouse model of colitis-associated cancer Cell 118 2004 285 296
17. D. Hanahan, and R.A. Weinberg The hallmarks of cancer Cell 100 2000 57 70
18. A. Hara, N. Yoshimi, Y. Yamada, K. Matsunaga, K. Kawabata, S. Sugie, and H. Mori Effects of Fas-mediated liver cell apoptosis on diethylnitrosamine- induced hepatocarcinogenesis in mice Br. J. Cancer 82 2000 467 471
19. M.J. Hardonk, F.W. Dijkhuis, C.E. Hulstaert, and J. Koudstaal Heterogeneity of rat liver and spleen macrophages in gadolinium chloride-induced elimination and repopulation J. Leukoc. Biol. 52 1992 296 302
20. N. Horiguchi, H. Takayama, M. Toyoda, T. Otsuka, T. Fukusato, G. Merlino, H. Takagi, and M. Mori Hepatocyte growth factor promotes hepatocarcinogenesis through c-Met autocrine activation and enhanced angiogenesis in transgenic mice treated with diethylnitrosamine Oncogene 21 2002 1791 1799
21. L.C. Hsu, J.M. Park, K. Zhang, J.L. Luo, S. Maeda, R.J. Kaufman, L. Eckmann, D.G. Guiney, and M. Karin The protein kinase PKR is required for macrophage apoptosis after activation of Toll-like receptor 4 Nature 428 2004 341 345
22. Y.H. Im, H.T. Kim, I.Y. Kim, V.M. Factor, K.B. Hahm, M. Anzano, J.J. Jang, K. Flanders, D.C. Haines, and S.S. Thorgeirsson Heterozygous mice for the transforming growth factor-β type II receptor gene have increased susceptibility to hepatocellular carcinogenesis Cancer Res. 61 2001 6665 6668
23. V.V. Kalinichenko, M.L. Major, X. Wang, V. Petrovic, J. Kuechle, H.M. Yoder, M.B. Dennewitz, B. Shin, A. Datta, P. Raychaudhuri, and R.H. Costa Foxm1b transcription factor is essential for development of hepatocellular carcinomas and is negatively regulated by the p19ARF tumor suppressor Genes Dev. 18 2004 830 850
24. H. Kamata, S. Honda, S. Maeda, L. Chang, H. Hirata, and M. Karin Reactive oxygen species promote TNF-α-induced cell death and sustained JNK activation by oxidixing MAP kinase phosphatases Cell 120 2005 649 661
25. M. Karin, Y. Cao, F.R. Greten, and Z.W. Li NF-κB in cancer: from innocent bystander to major culprit Nat. Rev. Cancer 2 2002 301 310
26. M. Karin, Y. Yamamoto, and Q.M. Wang The IKK NF-κB system: a treasure trove for drug development Nat. Rev. Drug Discov. 3 2004 17 26
27. G. Klein, and E. Klein Evolution of tumours and the impact of molecular oncology Nature 315 1985 190 195
28. A. Kobayashi, T. Ohta, and M. Yamamoto Unique function of the Nrf2-Keap1 pathway in the inducible expression of antioxidant and detoxifying enzymes Methods Enzymol. 378 2004 273 286
29. S.J. Korsmeyer Bcl-2 initiates a new category of oncogenes: regulators of cell death Blood 80 1992 879 886
30. Q. Li, D. Van Antwerp, F. Mercurio, K.F. Lee, and I.M. Verma Severe liver degeneration in mice lacking the IκB kinase 2 gene Science 284 1999 321 325
31. W.S. Liao, A.R. Conn, and J.M. Taylor Changes in rat α 1-fetoprotein and albumin mRNA levels during fetal and neonatal development J. Biol. Chem. 255 1980 10036 10039
32. A. Lieber, C.Y. He, L. Meuse, D. Schowalter, I. Kirillova, B. Winther, and M.A. Kay The role of Kupffer cell activation and viral gene expression in early liver toxicity after infusion of recombinant adenovirus vectors J. Virol. 71 1997 8798 8807
33. S. Maeda, L. Chang, Z.-W. Li, J.-L. Luo, H.L. Leffert, and M. Karin IKKβ is required for prevention of apoptosis mediated by cell-bound but not by circulating TNFα Immunity 19 2003 725 737
34. T.H. Mauad, C.M. van Nieuwkerk, K.P. Dingemans, J.J. Smit, A.H. Schinkel, R.G. Notenboom, M.A. van den Bergh Weerman, R.P. Verkruisen, A.K. Groen, and R.P. Oude Elferink Mice with homozygous disruption of the mdr2 P-glycoprotein gene. A novel animal model for studies of nonsuppurative inflammatory cholangitis and hepatocarcinogenesis Am. J. Pathol. 145 1994 1237 1245
35. M. Philip, D.A. Rowley, and H. Schreiber Inflammation as a tumor promoter in cancer induction Semin. Cancer Biol. 14 2004 433 439
36. R.H. Pierce, M.E. Vail, L. Ralph, J.S. Campbell, and N. Fausto Bcl-2 expression inhibits liver carcinogenesis and delays the development of proliferating foci Am. J. Pathol. 160 2002 1555 1560
37. E. Pikarsky, R.M. Porat, I. Stein, R. Abramovitch, S. Amit, S. Kasem, E. Gutkovich-Pyest, S. Urieli-Shoval, E. Galun, and Y. Ben-Neriah NF-κB functions as a tumour promoter in inflammation-associated cancer Nature 431 2004 461 466
38. S. Sakon, X. Xue, M. Takekawa, T. Sasazuki, T. Okazaki, Y. Kojima, J.H. Piao, H. Yagita, K. Okumura, T. Doi, and H. Nakano NF-κB inhibits TNF-induced accumulation of ROS that mediate prolonged MAPK activation and necrotic cell death EMBO J. 22 2003 3898 3909
39. D.S. Sarma, P.M. Rao, and S. Rajalakshmi Liver tumour promotion by chemicals: models and mechanisms Cancer Surv. 5 1986 781 798
40. K. Satoh, K. Itoh, M. Yamamoto, M. Tanaka, M. Hayakari, K. Ookawa, T. Yamazaki, T. Sato, S. Tsuchida, and I. Hatayama Nrf2 transactivator-independent GSTP1-1 expression in "GSTP1-1 positive" single cells inducible in female mouse liver by DEN: a preneoplastic character of possible initiated cells Carcinogenesis 23 2002 457 462
41. P. Scaffidi, T. Misteli, and M.E. Bianchi Release of chromatin protein HMGB1 by necrotic cells triggers inflammation Nature 418 2002 191 195
42. P. Schirmacher, A. Geerts, W. Jung, A. Pietrangelo, C.E. Rogler, and H.P. Dienes The role of Ito cells in the biosynthesis of HGF-SF in the liver EXS 65 1993 285 299
43. S. Sell, and H.L. Leffert An evaluation of cellular lineages in the pathogenesis of experimental hepatocellular carcinoma Hepatology 2 1982 77 86
44. D.I. Tai, S.L. Tsai, Y.H. Chang, S.N. Huang, T.C. Chen, K.S. Chang, and Y.F. Liaw Constitutive activation of NF-κB in hepatocellular carcinoma Cancer 89 2000 2274 2281
45. D. Talbot, P. Descombes, and U. Schibler The 5′ flanking region of the rat LAP (C/EBP beta) gene can direct high-level, position-independent, copy number-dependent expression in multiple tissues in transgenic mice Nucleic Acids Res. 22 1994 756 766
46. G. Tang, Y. Minemoto, B. Dibling, N.H. Purcell, Z. Li, M. Karin, and A. Lin Inhibition of JNK activation through NF-κB target genes Nature 414 2001 313 317
47. S.S. Thorgeirsson, and J.W. Grisham Molecular pathogenesis of human hepatocellular carcinoma Nat. Genet. 31 2002 339 346
48. S.S. Thorgeirsson, V.M. Factor, and E.G. Snyderwine Transgenic mouse models in carcinogenesis research and testing Toxicol. Lett. 112-113 2000 553 555
49. L. Verna, J. Whysner, and G.M. Williams N-nitrosodiethylamine mechanistic data and risk assessment: bioactivation, DNA-adduct formation, mutagenicity, and tumor initiation Pharmacol. Ther. 71 1996 57 81
50. G.M. Williams Inhibition of chemical-induced experimental cancer by synthetic phenolic antioxidants Toxicol. Ind. Health 9 1993 303 308
51. G.H. Wong, and D.V. Goeddel Induction of manganous superoxide dismutase by tumor necrosis factor: possible protective mechanism Science 242 1988 941 944
52. Y. Yamada, I. Kirillova, J.J. Peschon, and N. Fausto Initiation of liver growth by tumor necrosis factor: deficient liver regeneration in mice lacking type I tumor necrosis factor receptor Proc. Natl. Acad. Sci. USA 94 1997 1441 1446
53. J.Y. Zhang, C.L. Green, S. Tao, and P.A. Khavari NF-κB RelA opposes epidermal proliferation driven by TNFR1 and JNK Genes Dev. 18 2004 17 22
54. Z. Zhou, L. Wang, Z. Song, J.T. Saari, C.J. McClain, and Y.J. Kang Abrogation of NF-κB ac tivation is involved in zinc inhibition of lipopolysaccharide-induced TNFα production and liver injury Am. J. Pathol. 164 2004 1547 1556