Dysregulation of apoptosis by c-myc in transgenic hepatocytes and effects of growth factors and nongenotoxic carcinogens

Molecular Carcinogenesis

Volumn 25, Issue 4, 1999, Pages 273-284

  Christensen, James G ^a,b,e   Goldsworthy, Thomas L ^a,c   Cattley, Russell C ^a,d  

^a CIIT CENTERS FOR HEALTH RESEARCH   (United States)

^b NORTH CAROLINA STATE UNIVERSITY   (United States)

^c INTEGRATED LABORATORY SYSTEMS   (United States)

^d AMGEN INC   (United States)

^e PFIZER INC   (United States)

Author keywords

bcl 2; Mouse liver carcinogenesis; p53; Phenobarbital; Transforming growth factor

Indexed keywords

BLEOMYCIN; CANCER GROWTH FACTOR; CARCINOGEN; NAFENOPIN; PHENOBARBITAL; PROTEIN BAK; PROTEIN BAX; PROTEIN BCL 2; PROTEIN P53; SOMATOMEDIN B; TRANSFORMING GROWTH FACTOR ALPHA;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; APOPTOSIS; ARTICLE; CONTROLLED STUDY; GENE OVEREXPRESSION; LIVER CARCINOGENESIS; LIVER CELL; MOUSE; NONHUMAN; ONCOGENE C MYC; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN INTERACTION; REGULATORY MECHANISM; TUMOR PROMOTION;

EID: 0032805029     PISSN: 08991987     EISSN: None     Source Type: Journal    
DOI: 10.1002/(SICI)1098-2744(199908)25:4<273::AID-MC6>3.0.CO;2-N     Document Type: Article

References (64)

1. Gold LS, Slone TH, Manley NB, Bernstein L. Target organs in chronic bioassays of 533 chemical carcinogens. Environ Health Perspect 1991;93:233-246.
2. Tennant RW, Margolin BH, Shelby MD, et al. Prediction of chemical carcinogenicity in rodents from in vitro genetic toxicity assays. Science 1987;236:933-941.
3. Bursch W, Lauer B. Influence of liver tumor promoters on cell death by apoptosis in mouse liver. Arch Pharmacol Suppl 1983;322:R119.
4. Bursch W, Lauer B, Timmerman-Trosiener I, Barthel G, Schuppler J, Schulte-Hermann R. Controlled cell death (apoptosis) of normal and putative neoplastic cells in rat liver following withdrawal of tumor promoters. Carcinogenesis 1984;5:53-58.
5. Schulte-Hermann R, Timmerman-Trosiener I, Schuppler J. Response of liver foci in rats to hepatic tumor promoters. Toxicol Pathol 1982;10:63-70.
6. Schulte-Hermann R, Timmerman-Trosnier I, Barthel G, Bursch W. DNA synthesis, apoptosis and phenotypic expression as determinants of growth altered foci in rat liver during phenobarbital promotion. Cancer Res 1990;50: 5127-5135.
7. Schulte-Hermann R, Grasl-Kraupp B, Bursch W. Apoptosis and hepatocarcinogenesis. In: Jirtle RJ, editor. Liver regeneration and carcinogenesis. San Diego: Academic Press; 1995. p 141-178.
8. Nagy P, Evarts RP, Mardsen E, Roach J, Thorgeirsson SS. Cellular distribution of c-myc transcripts during chemical carcinogenesis in rats. Cancer Res 1988;48: 5522-5527.
9. Luscher B, Eisenman RN. New light on myc and myb. Genes Dev 1990;4:2025-2035.
10. Moray T, Alt FW, DiPihno RA. Use of transgenic mice to study normal and abnormal mammalian development. In: Broder S, editor. Molecular foundations of oncology. Baltimore, MD: Williams and Wilkins; 1991. p 455-487.
11. Yaswen P, Goyette M, Shank PR, Fausto N. Expression of c-Ki-ras, c-ha-ras and c-myc in specific cell types during hepatocarcinogenesis. Mol Cell Biol 1985;5:780-786.
12. Sandgren EP, Quaife CJ, Pinkert CA, Palmiter RD, Brinster RL. Oncogene induced liver neoplasia in transgenic mice. Oncogene 1989;4:715-724.
13. Liu C, Tsao MS, Grisham JW. Transforming growth factors produced by normal and neoplastically transformed rat liver epithelial cells in culture. Cancer Res 1988;48: 850-855.
14. Derynck R, Goeddel DV, Ullrich A, et al. Synthesis of messenger RNAs for transforming growth factors α and β and the epidermal growth factor receptor by human tumors. Cancer Res 1987;47:707-712.
15. Massague J. Interaction with epidermal growth factor II. Interaction with epidermal growth factor receptors on human placental membrane and A431 cells. J Biol Chem 1983;258:13614-13620.
16. Jhappan C, Stahle C, Harkins RN, Fausto N, Smith GH, Merlino GT. TGFα overexpression in transgenic mice induces liver neoplasia and abnormal development of the mammary gland and pancreas. Cell 1990;61: 1137-1146.
17. Sandgren EP, Lutteke NC, Palmiter RD, Brinster RL, Lee DC. Overexpression of TGF-α in transgenic mice: Induction of epithelial hyperplasia, pancreatic metaplasia, and carcinoma of the breast. Cell 1990;61:1121-1135.
18. Murakami H, Sanderson N, Nagy P, Marino P, Merlino GT, Thorgeirsson SS. Transgenic mouse model for synergistic effects of nuclear oncogenes and growth factors in tumorgenesis: Interaction of c-myc and TGF-alpha in hepatic oncogenesis. Cancer Res 1993;53:1719-1723.
19. Sandgren EP, Lutteke NC, Qiu TH, Palmiter RD, Brinster RL, Lee DC. Transforming growth factor-α dramatically enhances oncogene-induced carcinogenesis in transgenic mice. Mol Cell Biol 1993;13:320-330.
20. Santoni-Rugiu E, Nagy P, Jensen MR, Factor VM, Thorgeirsson SS. Evolution of neoplastic development in the liver of transgenic mice co-expressing c-myc and transforming growth factor-alpha. Am J Pathol 1996;149: 407-428.
21. Santoni-Rugiu E, Jensen MR, Thorgeirsson SS. Disruption of the pRb/E2F pathway and inhibition of apoptosis are major oncogenic events in liver constitutively expressing c-myc and transforming growth factor-α. Cancer Res 1998;58:123-134.
22. Santoni-Rugiu E, Preisegger KH, Kiss A, et al. Inhibition of neoplastic development in the liver by hepatocyte growth factor in a transgenic mouse model. Proc Natl Acad Sci 1996;93:9577-9582.
23. Woerner W, Schrenk D. Influence of liver tumor promoters on apoptosis in rat hepatocytes induced by 2-acetylamino-fluorine, ultraviolet light, or transforming growth factor-β1. Cancer Res 1996;56:1272-1278.
24. Bayly AC, Roberts RA, Dive C. Suppression of liver cell apoptosis in vitro by the nongenotoxic carcinogen and peroxisome proliferator nafenopin. J Cell Biol 1994;125: 197-203.
25. Miyazaki A, Bai L, Sato J. Influence of liver tumor promoters and structurally related chemicals on survival of normal adult rat hepatocytes in primary culture. J Cancer Res Clin Oncol 1990;116:259-263.
26. Christensen JG, Gonzales AJ, Cattley RC, Goldsworthy TL. Regulation of apoptosis in mouse hepatocytes and alteration of apoptosis by nongenotoxic carcinogens. Cell Growth Differ 1998;9:815-825.
27. Columbano A, Ledda-Columbano GM, Rao PM, Rajalakshmit S, Sarma DSR. Occurrence of cell death (apoptosis) in preneoplastic and neoplastic liver cells: a sequential study. Am J Pathol 1984;116:441-446.
28. Lowe SW, Schmitt EM, Smith SW, Osborne BA, Jacks T. p53 is required for radiation induced apoptosis in mouse thymocytes. Nature 1993;362:847-849.
29. Tsujimoto Y, Cossman J, Jaffe E, Croce CM. Involvement of the bcl-2 gene in human follicular lymphoma. Science 1985;228:1440-1443.
30. Reed JC. Bcl-2 and the regulation of programmed cell death. J Cell Biol 1994;124:1-6.
31. Vaux DL, Cory S, Adams JM. Bcl-2 gene promotes haemotopoetic cell survival and cooperates with c-myc to immortalize pre-B cells. Nature 1988;335:440-442.
32. Kedderis GL, Held SD. Prediction of furan pharmacokinetics from hepatocyte studies: Comparison of bioactivation and hepatic dosimetry in rats mice and humans. Toxicol Appl Pharmacol 1996;140:124-130.
33. McGahon A, Martin SJ, Bissonnette RP, et al. The end of the cell line: Methods for the study of apoptosis in vitro. Methods Cell Biol 1995;46:172-173.
34. Dunnett CW, A multiple comparisons procedure for comparing several treatments with a control. Journal of the American Statistical Association 1955;50:1096-1121.
35. Steel RGD, Torrie JH. Principles and procedures of statistics New York: McGraw-Hill; 1980. 562 p.
36. Miyashita T, Reed JC. Tumor supressor p53 is a direct transcriptional activator of the human bax gene. Cell 1995;80:293-299.
37. Bissonnette R, Echeverri F, Mahboubi A, Green D. Apoptotic cell death induced by c-myc is inhibited by bcl-2. Nature 1992;359:552-554.
38. Land H, Parada LF, Weinberg RA. Tumorgenic conversion of primary embryo fibroblasts requires at least 2 cooperating oncogenes. Nature 1983;304:596-598.
39. Fanidi A, Harrington EA, Evan GI. Cooperative interaction between c-myc and bcl-2 proto-oncogenes. Nature 1992; 359:554-556.
40. Amundadottir LT, Nass SJ, Berchem GJ, Johnson MD, Dickson RB. Cooperation of TGF-α and c-Myc in mouse mammary tumorgenesis: coordinated stimulation of growth and suppression of apoptosis. Oncogene 1996;13: 757-765.
41. Amundadottir LT, Johnson MD Merlino G, Smith GH, Dickson RB. Synergistic interaction of transforming growth factor alpha and c-myc in mouse mammary and salivary gland tumorgenesis. Cell Growth Differ 1995;6:737-748.
42. Wang XJ, Greenhalgh DA, Jiang A, et al. Expression of a p53 mutant in the epidermis of transgenic mice accelerates chemical carcinogenesis. Oncogene 1998;17:35-45.
43. Rodriguez-Villanueva J, Greenhalgh D, Wang XJ, et al. Human keratin-1.bcl-2 transgenic mice aberrently express keratin 6, exhibit reduced sensitivity to keratinocyte cell death induction, and are suceptible to skin tumor formation. Oncogene 1998;16:853-863.
44. Owens DM, Spalding JW, Tennant RW, Smart RC. Genetic alterations cooperate with Ha-ras to accelerate multistage carcinogenesis in TG.AC transgenic mouse skin. Cancer Res 1995;55:3171-3178.
45. Shibata MA, Ward JM, Green JE, Merlino G. Enhanced sensitivity to tumor growth and development in multistage skin carcinogenesis by transforming growth factor-α-induced receptor activation but not p53 activation. Mol Carcinog 1997;18:160-170.
46. O'Brien TG, Megosh LC, Gillard G, Soler AP. Ornithine decarboxylase overexpression is a sufficient condition for tumor promotion in mouse skin. Cancer Res 1997;57: 2630-2637.
47. Bol DK, Kiguchi K, Gimenez-Conti I, Rupp T, DiGiovanni J. Overexpression of insulin-like growth factor-1 induces hyperplasia, dermal abnormalities, and spontaneous tumor formation in transgenic mice. Oncogene 1997;14: 1725-1734.
48. Greenhalgh DA, Wang XJ, Eckhardt JN, Roop DR. 12-O-tetradecanoylphorbol-13-acetate promotion of transgenic mice expressing epidermal targeted v-fos induces rasHA-activated papillomas and carcinomas without p53 mutation: Association of v-fos expression with promotion and tumor autonomy. Cell Growth Differ 1995;6:579-586.
49. Sanders S, Thorgeirsson SS. Phenobarbital promotes growth in c-myc/TGF-α mice by hypertrophy and inhibiting apoptosis. Carcinogenesis 1998;20:41-49.
50. Moser GJ, Wolf DC, Goldsworthy TL. Quantitative relationship between transforming growth factor-alpha and hepatic focal phenotype and progression in female mouse liver. Toxicol Pathol 1997;25:275-283.
51. Moser G, Goldsworthy TL. Growth factor regulation in mouse liver carcinogenesis. CIIT Activities 1996;16:1-8.
52. Pilot HC. Protooncogene activation in multistage murine hepatocarcinogenesis. In: Stevenson DE, McClain RM, Popp JA, Ward JM, Slaga TJ, and Pilot HC, editors. Mouse liver carcinogenesis: Mechanisms and species comparisons. New York: Wiley-Liss; 1990. p 311-324.
53. Ward JM, Diwan BA, Lubet RA, Henneman JR, Devor DE. Liver tumor promoters and other mouse carcinogens. In: Stevenson DE, McClain RM, Popp JA, Ward JM, Slaga TJ, Pilot HC editors. Mouse liver carcinogenesis: Mechanisms and species comparisons. New York: Wiley-Liss; 1990. p 85-108.
54. Ward JM, Rice JM, Creasia D, Lynch P, Riggs C. Dissimilar patterns of promotion by di(2-ethylhexyl)phthalate and phenobarbital of hepatocellular neoplasia initiated by diethylnitrosamine in B6C3F1 mice. Carcinogenesis 1983; 4:1021-1029.
55. Ward JM, Ohshima M, Lynch P, Riggs C. Di(2-ethylhexyl)phthalate but not phenobarbital promotes N-nitrosodiethyl amine initiated hepatocellular proliferate lesions after short term exposure in male B6C3F1 mice. Cancer Lett 1984;24:49-55.
56. Sills RC, Goldsworthy TL, Sleight SD. Tumor-promoting effects of 2,3,7,8-tetrachlorodibenzo-ρ-dioxin and phenobarbital in initiated weaning Sprague-Dawley rats: A quantitative, phenotypic, and ras p21 protein study. Toxicol Pathol 1994;22:270-281.
57. Coppola JA, Cole MD. Constitutive c-myc oncogene expression blocks mouse erythroleukemia cell differentiation but not committment. Nature 1986;320:760-762.
58. Holt JT, Redner RL, Niehuis AW. An oligomer complimentary to c-myc RNA inhibits proliferation of HL60 promyleocytic leukemia cells and induces differentiation. Mol Cell Biol 1988;8:963-973.
59. Factor VM, Jensen MR, Thorgeirsson SS. Coexpression of c-myc and transforming growth factor alpha in the liver promotes early replicative senescence and diminishes regenerative capacity after partial hepatectomy in transgenic mice. Hepatology 1997;26:1434-1443.
60. Sargent LM, Sanderson ND, Thorgeirsson SS. Ploidy and karyotypic alterations associated with early events in the development of hepatocarcinogenesis in transgenic mice harboring c-Myc and TGF-α transgenes. Cancer Res 1996;56:2137-2142.
61. Sue SR, Chari RS, Kong FM, et al. Transforming growth factor-beta receptors and mannose-6-phosphate/ insulin-like growlh factor-II receptor expression in human hepatocellular carcinoma. Ann Surg 1995;222: 171-178.
62. Russell WE, Coffey RJ, Ouellette RJ, Moses HL. Transforming growth factor beta reversibly inhibits the early proliferative response to partial hepatectomy in rat. Proc Natl Acad Sci USA 1988;89:5126-5130.
63. Jirtle RL, Hankins GR, Reisenbichler H, Boyer IJ. Regulation of mannose-6-phosphate/insulin-like growth factor-II receptors and trans forming growth factor beta during liver tumor promotion with phenobarbital. Carcinogenesis 1994;15: 1473-1478.
64. Factor VM, Kao CY, Santoni-Rugiu E, Woitach JT, Jensen MR, Thorgeirsson SS. Constitutive expression of mature transforming growth factor-beta 1 in the liver accelerates carcinogenesis in transgenic mice. Cancer Res 1997;57: 2089-2095.