Phenobarbital causes apoptosis in conditionally immortalized mouse hepatocytes depending on deregulated c-myc expression: Characterization of an unexpected effect

Cancer Research

Volumn 57, Issue 14, 1997, Pages 2896-2903

  Osanai, Makoto ^a   Ogawa, Katsuhiro ^a   Lee, Gang Hong ^a  

^a ASAHIKAWA MEDICAL COLLEGE   (Japan)

Author keywords

[No Author keywords available]

Indexed keywords

DNA FRAGMENT; PHENOBARBITAL; PROTEIN BAX; PROTEIN BCL 2; PROTEIN P53; VIRUS T ANTIGEN;

ANIMAL CELL; APOPTOSIS; ARTICLE; CANCER RISK; CELL IMMORTALIZATION; DNA DAMAGE; GENE EXPRESSION REGULATION; LIVER CANCER; LIVER CARCINOGENESIS; LIVER CELL; MOUSE; NONHUMAN; ONCOGENE C H RAS; ONCOGENE C MYC; PRIORITY JOURNAL;

ANIMALS; ANTIGENS, POLYOMAVIRUS TRANSFORMING; APOPTOSIS; BCL-2-ASSOCIATED X PROTEIN; CELL LINE; CELL TRANSFORMATION, NEOPLASTIC; FEMALE; GENE EXPRESSION REGULATION; GENES, MYC; GENES, RAS; LIVER; MICE; MICE, INBRED C3H; PHENOBARBITAL; PROTO-ONCOGENE PROTEINS; PROTO-ONCOGENE PROTEINS C-BCL-2; TUMOR SUPPRESSOR PROTEIN P53;

EID: 0030786998     PISSN: 00085472     EISSN: None     Source Type: Journal    
DOI: None     Document Type: Article

References (56)

1. Moore, M. A., and Kitagawa, T. Hepatocarcinogenesis in the rat: the effect of promotors and carcinogens in vivo and in vitro. Int. Rev. Cytol., 101: 125-173, 1986.
2. Peraino, C., Fry, R. J. M., and Staffeldt, E. Reduction and enhancement by phenobarbital of hepatocarcinogenesis induced in the rat by 2-acetylaminofluorene. Cancer Res., 31: 1506-1512, 1971.
3. Mills, J. J., Jirtle, R. L., and Boyer, I. J. Mechanisms of liver tumor promotion. In: R. L. Jirtle (ed.), Liver Regeneration and Carcinogenesis, pp. 199-226. San Diego: Academic Press, Inc., 1995.
4. Schulte-Hermann, R., Grasl-Kraupp, B., and Bursch, W. Apoptosis and hepatocarcinogenesis. In: R. L. Jirtle (ed.). Liver Regeneration and Carcinogenesis, pp. 179-197. San Diego: Academic Press, Inc., 1995.
5. Peraino, C., Fry, R. J. M., and Staffeldt, E. Enhancement of spontaneous hepatotumorigenesis in C3H mice by dietary phenobarbital. J. Natl. Cancer Inst., 51: 1349-1350, 1973.
6. Diwan, B. A., Rice, J. M., Ward, J. M., Ohshima, M., and Lynch, P. H. Inhibition by phenobarbital and lack of effect of amoharbital on the development of liver tumors induced by N-nitrosodiethylamine in juvenile B6C3F1 mice. Cancer Lett., 23: 223-234, 1984.
7. Pereira, M. A., Klaunig, J. E., Herren-Freund, S. L., and Ruch, R. J. Effect of phenobarbital on the development of liver tumors in juvenile and adult mice. J. Natl. Cancer Inst., 77: 449-452, 1986.
8. Ward, J. M., Rice J. M., Creasin, D., Lynch, P., and Riggs, C. Dissimilar patterns of promotion by di(2-ethylhexyl) phthalate and phenobarbital of hepatocellular neoplasia initiated by diethylnitrosamine in B6C3F1 mice. Carcinogenesis (Lond.), 4: 1021-1029, 1983.
9. Becker, F. F. Morphological classification of mouse liver tumors based on biological characteristics. Cancer Res., 42: 3918-3923, 1982.
10. Diwan, B. A., Rice, J. M., Ohshima, M., and Ward, J. M. Interstrain difference in susceptibility to liver carcinogenesis initiated by N-nitrosodiethylamine and its promotion by phenobarbital in C57BL/6NCr, C3H/HeNCr and DBA/2NCr mice. Carcinogenesis (Lond.), 7: 215-220, 1986.
11. Lee, G-H., Nomura, K., and Kitagawa, T. Comparative study of diethylnitrosamine-initiated two-stage hepatocarcinogenesis in C3H, C57BL and BALB mice promoted by various hepatopromoters. Carcinogenesis (Lond.), 10: 2227-2230, 1989.
12. Sawada, N., Lee, G-H., Mochizuki, Y., and Ishikawa, T. Active proliferation of mouse hepatocytes in primary culture under defined conditions as compared to rat hepatocytes. Jpn. J. Cancer Res., 79: 987-988, 1988.
13. Edward, A.M., and Lucas, C-M. Phenobarbital and some other liver tumor promoters stimulate DNA synthesis in cultured rat hepatocytes. Biochem. Biophys. Res. Commun., 131: 103-108, 1985.
14. Armato, U., Andreis, P. G., and Romano, F. The stimulation by the tumour promoters 12-0-tetradecanoyl-phorbol-13-acetate and phenobarbital of the growth of primary neonatal hepatocytes. Carcinogenesis (Lond.), 60: 811-822, 1985.
15. Sawada, N., Staecker, J. L., and Pilot, H. C. Effects of tumor-promoting agents 12-0-tetradecanoylphorbol-13-acetate and phenobarbital on DNA synthesis of rat hepatocytes in primary cultures. Cancer Res., 47: 5665-5671, 1987.
16. Kitagawa, T., Watanabe, R., Kayano, T., and Sugano, H. In vitro carcinogenesis of hepatocytes obtained from acetylaminofluorene-treated rat liver, and promotion of their growth by phenobarbital. Gann. 71: 747-754, 1980.
17. Kaufmann, W. K., Tsao, M-S., and Novicki, D. L. In vitro colonization ability appears soon after initiation of hepatocarcinogenesis in the rat. Carcinogenesis (Lond.), 7: 669-671, 1986.
18. Lee, G-H., Sawada, N., Mochizuki, Y., Nomura, K., and Kitagawa, T. Immortal epithelial cells of normal C3H mouse liver in culture: possible precursor populations for spontaneous hepatocellular carcinoma. Cancer Res., 49: 403-409, 1989.
19. Chiao, C., Zhang, Y., Kaufmann, D. G., and Kaufmann, W. K. Derivation of phenobarbital-responsive immortal rat hepatocytes. Am J. Pathol., 146: 1248-1259, 1995.
20. Worner, W., and Schrenk, D. Influence of liver tumor promoters on apoptosis in rat hepatocytes induced by 2-acetylaminofluorene, ultraviolet light, or transforming growth factor β1. Cancer Res., 56: 1272-1278, 1996.
21. Oberhammer, F. A., and Qin, H-M. Effect of three tumour promoters on the stability of hepatocyte cultures and apoptosis after transforming growth factor-β1. Carcinogenesis (Lond.), 16: 1363-1372, 1995.
22. Cayama, E., Tsuda, H., Sarma, D. S. R., and Ferber, B. Initiation of chemical carcinogenesis requires cell proliferation. Nature (Lond.), 275: 60-61, 1978.
23. Lee, G-H., Ogawa, K., and Drinkwater, N. R. Conditional transformation of mouse liver epithelial cells: an in vitro model for analysis of genetic events in hepatocarcinogenesis. Am. J. Pathol., 147: 1811-1822, 1995.
24. Chou, J. Y. Temperature-sensitive adult liver cell line dependent on glucocorticoid for differentiation. Mol. Cell. Biol., 3: 1013-1020, 1983.
25. Zaret, K. S., DiPersio, C. M., Jackson, D. A., Montigny, W. J., and Weinstat, D. L. Conditional enhancement of liver-specific gene transcription. Proc. Natl. Acad. Sci. USA, 85: 9076-9080, 1988.
26. Yanai, N., Saguchi, M., and Obinata, M. Hepatocyte cell lines established from transgenic mice harboring temperature-sensitive simian virus 40 large T-antigen gene. Exp. Cell. Res., 197: 50-56, 1991.
27. 1 mouse. Proc. Natl. Acad. Sci. USA, 83: 33-37, 1986.
28. 1 mouse. Proc. Natl. Acad. Sci. USA, 83: 5825-5829, 1986.
29. Dragani, T. A., Manenti, G., Porta, G. D., Gattoni-Celli, S., and Weinstein, I. B. Expression of retroviral sequences and oncogenes in murine hepatocellular tumors. Cancer Res., 46: 1915-1919, 1986.
30. Oltvai, Z. N., Milliman, C. L., and Karsmeyer, S. J. Bcl-2 heteromerizes in vitro with a conserved homolog, Bax, that accelerates programmed cell death. Cell. 74: 609-619, 1993.
31. Tsujimoto, Y., Cossman, J., Jaffe, E., and Croce, C. M. Involvement of the bcl-2 gene in human follicular lymphoma. Science (Washington DC), 228: 1440-1443, 1985.
32. Vaux, D. L., Corg, S., and Adams, J. M. Bcl-2 gene promotes haemopoietic cell survival and cooperates with c-myc to immortalize pre-B cells. Nature (Lond.), 335: 440-442, 1988.
33. Hamada, M., Aime-Sempe, C., Sato, T., and Reed, J. C. Structure-function analysis of Bcl-2 protein: identification of conserved domains important for homodimerization with Bcl-2 and heterodimerization with Bax. J. Biol. Chem., 270: 11962-11969, 1995.
34. Izumi, M., Miyagawa, H., Kamakura, T., Yamaguchi, I., Endo, T., and Hanaoka, F. Blasticidin S-resistance gene (bsr): a novel selectable marker for mammalian cells. Exp. Cell Res., 197: 229-223, 1991.
35. Land, H., Purada, L. F., and Weinberg, R. A. Tumorigenic conversion of primary embryo fibroblasts requires at least two cooperating oncogenes. Nature (Lond.), 304: 596-602, 1983.
36. Sekiya, T., Fushimi, M., Hori, H., Hirohashi, S., Nishimura, S., and Sugimura, T. Molecular cloning and the tolal nucleotide sequence of the human c-H-ras-1 gene activated in a melanoma from a Japanese patient. Proc. Natl. Acad. Sci. USA, 81: 4771-4775, 1984.
37. Guilhot, S., Cornman, T. M. G., and Isom, H. C. Apoptosis induced by tumor necrosis factor-α in rat hepatocyte cell lines expressing hepatitis B virus. Am. J. Pathol., 148: 801-814, 1996.
38. Cohen, J. J., and Duke, R. C. Glucocorticoid activation of a calcium-dependent endonucleases in thymocyte nuclei leads to cell death. J. Immunol., 132: 38-42, 1984.
39. Burton, K. A study of the conditions and mechanism of the diphenylamine reaction for the colorimetric estimation of deoxyribonucleic acid. Biochem. J., 62: 315-323, 1956.
40. Lee, G-H., Sakai, R., Nagao, M., and Kitagawa, T. Role of activated c-H-ras oncogene in the induction and progression of immortal liver epithelial cell lines derived from normal C3H mice. Int. J. Cancer, 47: 60-65, 1991.
41. Sambrook, J., Fritsch, E. F., and Maniatis, T. Molecular Cloning: A Laboratory Manual, Ed. 2, pp. 18.60-18.75. Cold Spring Harbor, NY: Cold Spring Harbor Laboratory, 1989.
42. Wyllie, A. H., Kerr, J. F. R., and Kurrie, A. R. Cell death: the significance of apoptosis. Int. Rev. Cytol., 6: 251-306, 1980.
43. Deppert, W., Steinmayer, T., and Richter, W. Cooperation of SV40 large T antigen and the cellular protein p53 in maintenance of cell transformation. Oncogene, 4: 1103-1110, 1989.
44. Zheng, D. O., Vayssiere, J. L., Petit, P. X., LeCoeur, H., Spatz, A., Mignotte, B., and Feunteum, J. Apoptosis is antagonized by large T antigenes in the pathway to immortalization by polyomaviruses. Oncogene, 9: 3345-3351, 1994.
45. Miyashita, T., and Reed, J. C. Tumor suppressor p53 is a direct transcriptional activator of the human bax gene. Cell, 80: 293-299, 1995.
46. Sugden, B., Marsh, K., and Yates, J. A vector that replicates as a plasmid and can be efficiently selected in B-lymphoblasts transformed by Epstein-Barr virus. Mol. Cell. Biol., 5: 410-413, 1985.
47. Beer, D. G., and Pilot, H. C. Biological markers characterizing the development of preneoplastic and neoplastic lesions in rodent liver. Arch. Toxicol. Suppl., 10: 68-80, 1987.
48. Chiao, C., Zhang, Y., Kaufmann, D. G., and Kaufmann, W. K. Phenobarbital modulates the type of cell death by rat hepatocytes during deprivation of serum in vitro. Hepatology. 22: 297-303, 1995.
49. Camman, C. B., and Kastan, M. B. Induction of apoptosis by tumor suppressor genes and oncogenes. Semin. Cancer Biol., 6: 17-25, 1995.
50. Hermeking, H., and Hick, D. Mediation of c-Myc-induced apoptosis by p53. Science (Washington DC), 265: 2091-2093, 1994.
51. Saito, Y., and Ogawa, K. Wild type p53 and c-myc co-operation in generating apoptosis of a rat hepatocellular carcinoma cell line (FAA-HTC1). Oncogene, 11: 1013-1018, 1995.
52. Smith, J. R., and Pereira-Smith, O. M. Replicative senescence: implications for in vivo aging and tumor suppression. Science (Washington DC), 273: 63-67, 1996.
53. Bauer-Hofmann, R., Buchmann, A., Mahr, J., Kress, S., and Schwarz, M. The tumor promoters dieldrin and phenobarbital increase the frequency of c-Ha-ras wild-type, but not of c-Ha-ras mutated focal liver lesions in male C3H/He mice. Carcinogenesis (Lond.), 13: 447-481, 1992.
54. Marsman, D. S., and Barren, J. C. Apoptosis and chemical carcinogenesis. Risk Analysis. 14: 321-326, 1994.
55. Clemmesen, J., and Hjalgrim-Jensen, S. Is phenobarbital carcinogenic? A follow up of 8078 epileptics. Ecotoxicol. Environ. Safety, 1: 457-470, 1978.
56. Clemmesen, J., and Hjalgrim-Jensen, S. Epidemiological studies of medically used drugs. Arch. Toxicol. Suppl., 3: 19-25, 1980.