Stage-specific gene expression during hepatocarcinogenesis in the rat

Journal of Cancer Research and Clinical Oncology

Volumn 122, Issue 5, 1996, Pages 257-265

  Pitot, Henry C ^a  

^a UNIVERSITY OF WISCONSIN MADISON   (United States)

Author keywords

Gene expression; Initiation; Progression; Promotion

Indexed keywords

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; CONTROLLED STUDY; GENE EXPRESSION; LIVER CARCINOGENESIS; NONHUMAN; PRECANCER; PRIORITY JOURNAL; RAT; REVIEW; TUMOR GROWTH; TUMOR PROMOTION;

ANIMALS; GENE EXPRESSION REGULATION, NEOPLASTIC; GLUTATHIONE TRANSFERASE; HUMANS; LIVER NEOPLASMS, EXPERIMENTAL; NEOPLASM STAGING; RATS; TRANSFORMING GROWTH FACTOR ALPHA;

EID: 0029930511     PISSN: 01715216     EISSN: None     Source Type: Journal    
DOI: 10.1007/BF01261401     Document Type: Review

References (98)

1. Aldaz CM, Chen A, Gollahon LS, Russo J, Zappler K (1992) Nonrandom abnormalities involving chromosome 1 and Harvey-ras-1 alleles in rat mammary tumor progression. Cancer Res 52:4791-4798
2. Anderson MW, Reynolds SH, You M, Maronpot M (1992) Role of proto-oncogene activation in carcinogenesis. Environ Health Perspect 98:13-24
3. Barrow BJ, O'Riordan MA, Stellato TA, Calkins BM, Pretlow TP (1990) Enzyme-altered foci in colons of carcinogen-treated rats. Cancer Res 50:1911-1916
4. Bax J, Feringa AW, van Garderen-Hoetmer A, Woutersen RA, Scherer E (1986) Adenosine triphosphatase, a new marker for the differentiation of putative precancerous foci induced in rat pancreas by azaserine. Carcinogenesis 7:457-462
5. Bianchi AB, Fischer SM, Robles AI, Rinchik EM, Conti CJ (1993) Overexpression of cyclin D1 in mouse skin carcinogenesis. Oncogene 8:1127-1133
6. Boutwell RK (1964) Some biological aspects of skin carcinogenesis. Prog Exp Tumor Res 4:207-250
7. Brown K, Buchmann A, Balmain A (1990) Carcinogen-induced mutations in the mouse c-Ha-ras gene provide evidence of multiple pathways for tumor progression. Proc Natl Acad Sci USA 87:538-542
8. Burmer GC, Loeb LA (1989) Mutations in the KRAS2 oncogene during progressive stages of human colon carcinoma. Proc Natl Acad Sci USA 86:2403-2407
9. Campbell HA, Xu YD, Hanigan MH, Pitot HC (1986) Application of quantitative stereology to the evaluation of phenotypically heterogeneous enzyme-altered foci in the rat liver. J Natl Cancer Inst 76:751-767
10. Cavenee WK, Dryja TP, Phillips RA, Benedict WF, Godbout R, Gallie BL, Murphree AL, Strong LC, White RL (1983) Expression of recessive alleles by chromosomal mechanisms in retinoblastoma. Nature 305:779-784
11. Chang WWL (1984) Histogenesis of colon cancer in experimental animals. Scand J Gastroenterol 19:27-43
12. Cohen SM (1985) Multi-stage carcinogenesis in the urinary bladder. Fd Chem Toxicol 23:521-528
13. Deamant FD, Iannaccone PM (1987) Clonal origin of chemically induced papillomas: separate analysis of epidermal and dermal components. J Cell Sci 88:305-312
14. DiGiovanni J (1992) Multistage carcinogenesis in mouse skin. Pharmacol Ther 54:63-128
15. Dragan YP, Pitot HC (1992) The role of the stages of initiation and promotion in phenotypic diversity during hepatocarcinogenesis in the rat. Carcinogenesis 13:739-750
16. Dragan YP, Laufer C, Koleske AJ, Drinkwater N, Pitot HC (1993) Quantitative comparison of initiation and mutation phenotypes in hepatocytes of the analbuminemic rat. Jpn J Cancer Res 84:175-183
17. Dragan YP, Campbell HA, Baker K, Vaughan J, Mass M, Pitot HC (1994) Focal and non-focal hepatic expression of placental glutathione S-transferase in carcinogen-treated rats. Carcinogenesis 15:2587-2591
18. Dragan Y, Teeguarden J, Campbell H, Hsia S, Pitot H (1995) The quantitation of altered hepatic foci during multistage hepatocarcinogenesis in the rat: transforming growth factor α expression as a marker for the stage of progression. Cancer Lett 93:73-83
19. Ewing MW, Crysup SE, Phillips JL, Slaga TJ, DiGiovanni J (1988) Enhancement of mezerein-promoted papilloma formation by treatment with 12-O-tetradecanoylphorbol-13-acetate or mezerein prior to initiation. Carcinogenesis 9:405-410
20. Fearon ER, Vogelstein B (1990) A genetic model for colorectal tumorigenesis. Cell 61:759-767
21. Furuya K, Williams GM (1985) Iron exclusion by proliferative foci and neoplastic lesions induced by 7,12-dimethylbenz(a)anthracene in the rat adrenal cortex. Histochem J 17:213-221
22. Glick AB, Kulkarni AB, Tennenbaum T, Hennings H, Flanders KC, O'Reilly M, Sporn MB, Karlsson S, Yuspa SH (1993) Loss of expression of transforming growth factor β in skin and skin tumors is associated with hyperproliferation and a high risk for malignant conversion. Proc Natl Acad Sci USA 90:6076-6080
23. Goldsworthy TL, Pitot HC (1985) The quantitative analysis and stability of histochemical markers of altered hepatic foci in rat liver following initiation by diethylnitrosamine administration and promotion with phenobarbital. Carcinogenesis 6:1261-1269
24. Gould MN (1993) Cellular and molecular aspects of the multistage progression of mammary carcinogenesis in humans and rats. Cancer Biol 4:161-169
25. Hartwell LH, Kastan MB (1994) Cell cycle control and cancer. Science 266:1821-1828
26. Hirano T, Franzén B, Kato H, Ebihara Y, Auer G (1994) Genesis of squamous cell lung carcinoma. Sequential changes of proliferation, DNA ploidy, and p53 expression. Am J Pathol 144:296-302
27. Horowitz JM, Park SH, Bogenmann E, Cheng JC, Yandell DW, Kaye FJ, Minna JD, Dryja TP, Weinberg RA (1990) Frequent inactivation of the retinoblastoma antioncogene is restricted to a subset of human tumor cells. Proc Natl Acad Sci USA 87:2775-2779
28. Huber BE, Heilman CA, Thorgeirsson SS (1989) Poly(A +) RNA levels of growth-, differentiation-and transformation-associated genes in the progressive development of hepatocellular carcinoma in the rat. Hepatology 9:756-762
29. Hunter T, Pines J (1994) Cyclins and cancer II: cyclin D and CDK inhibitors come of age. Cell 79:573-582
30. Jang JJ, Henneman JR, Kurata Y, Uno H, Ward JM (1993) Alterations in populations of GST-p-immunoreactive single hepatocytes and hepatocellular foci after a single injection of N-nitrosodiethylamine with or without phenobarbital promotion in male F344/NCr rats. Cancer Lett 71:89-95
31. Kaufmann WK, Zhang Y, Kaufman DG (1992) Association between expression of transforming growth factor-alpha and progression of hepatocellular foci to neoplasms. Carcinogenesis 13: 1481-1483
32. Kemp CJ, Donehower LA, Bradley A, Balmain A (1993) Reduction of p53 gene dosage does not increase initiation or promotion but enhances malignant progression of chemically induced skin tumors. Cell 74:813-822
33. Kiguchi K, Beltrán LM, You J, Rho O, DiGiovanni J (1995) Elevation of transforming growth factor-α mRNA and protein expression by diverse tumor promoters in SENCAR mouse epidermis. Mol Carcinog 12:225-235
34. Kitagawa T, Sugano H (1973) Timetable for hepatocarcinogenesis in rat. In: Nakahara W, Hirayama T, Nishioka K, Sugano H (eds) Symposium of the Princess Takamatsu Cancer Research Fund. Analytical and experimental epidemiology of cancer, vol. 3. University Park Press, Baltimore, pp 91-104
35. Knudson AG (1993) Antioncogenes and human cancer. Proc Natl Acad Sci USA 90:10914-10921
36. Kobusch A-B, Schrenk D, Gans G, Münzel P, Werringloer J, Ingelman-Sundberg M, Bock KW (1991) Immunochemical localization and functional characterization of cytochrome P450IIE1 in rat hepatocyte foci and nodules. Carcinogenesis 12:2353-2356
37. Kunze E (1979) Development of urinary bladder cancer in the rat. Curr Top Pathol 67:145-232
38. Lang P, Maurer J, Höher D, Bornhöft G, Montenarh M, Berdel WE, Thiel E, Kreuser E-D (1993) Mutation and expression of the p53 tumor suppressor gene in tumor samples and cancer cell lines: comparison of non-isotopic direct DNA-sequencing, immunoblotting and immunohistochemistry. Int J Oncol 2: 347-355
39. Lee DC, Luetteke NC, Petch LA (1993) Transforming growth factor-alpha and its role in neoplastic progression. In: Benz CC, and Liu ET (eds) Oncogenes and tumor suppressor genes in human malignancies. Kluwer, Boston, pp 233-254
40. Li ZH, Zheng J, Weiss LM, Shibata D (1994) c-K-ras and p53 mutations occur very early in adenocarcinoma of the lung. Am J Pathol 144:303-309
41. Maskens AP (1981) Confirmation of the two-step nature of chemical carcinogenesis in the rat colon adenocarcinoma model. Cancer Res 41:1240-1245
42. Matsukura N, Suzuki K, Kawachi T, Aoyagi M, Sugimura T, Kitaoka H, Numajiri H, Shirota A, Itabashi M, Hirota T (1980) Distribution of marker enzymes and mucin in intestinal metaplasia in human stomach and relation of complete and incomplete types of intestinal metaplasia to minute gastric carcinomas. J Natl Cancer Inst 65:231-240
43. Meyel DJ van, Ramsay DA, Casson AG, Keeney M, Chambers AF, Cairncross JG (1994) p53 Mutation, expression, and DNA ploidy in evolving gliomas: evidence for two pathways of progression. J Natl Cancer Inst 86:1011-1017
44. Moore MA, Kitagawa T (1986) Hepatocarcinogenesis in the rat: the effect of promoters and carcinogens in vivo and in vitro. Int Rev Cytol 101:125-173
45. Moore MA, Bannasch P, Satoh T, Hacker HJ, Ito N (1987a) Immunohistochemically demonstrated increase in glutathione S-transferase species in propylnitrosamine-induced focal proliferative and neoplastic Syrian hamster pancreatic lesions. Virchows Arch 52:479-488
46. Moore MA, Nakagawa K, Satoh K, Ishikawa T, Sato K (1987b) Single GST-P positive liver cells - putative initiated hepatocytes. Carcinogenesis 8:483-486
47. Moore MA, Thamavit W, Ito N (1987c) Comparison of lesions induced in the Syrian golden hamster by diethylnitrosamine. dimethylhydrazine, and dibutylnitrosamine: influence of subsequent butylated hydroxyanisole treatment. J Natl Cancer Inst 78:295-301
48. Moriyama S, Kawaoi A, Hirota N (1983) Localization and significance of gamma-glutamyl transpeptidase during experimental thyroid carcinogenesis in rats. Acta Histochem Cytochem 16:567-576
49. Müller H, Lukas J, Schneider A, Warthoe P, Bartek J, Eilers M, Strauss M (1994) Cyclin D1 expression is regulated by the retinoblastoma protein. Proc Natl Acad Sci USA 91: 2945-2949
50. Nakano H, Hatayama I, Satoh K, Suzuki S, Sato K, Tsuchida S (1994) c-Jun expression in single cells and preneoplastic foci induced by diethylnitrosamine in B6C3F1 mice: comparison with the expression of pi-class glutathione S-transferase. Carcinogenesis 15:1953-1957
51. Navone NM, Troncoso P, Pisters LL, Goodrow TL, Palmer JL, Nichols WW, Eschenbach ACvon Conti CJ (1993) p53 Protein accumulation and gene mutation in the progression of human prostate carcinoma. J Natl Cancer Inst 85:1657-1669
52. Neveu MJ, Hully JR, Paul DL, Pilot HC (1990) Reversible alteration in the expression of the gap junctional protein connexin 32 during tumor promotion in rat liver and its role during cell proliferation. Cancer Commun 2:21-31
53. Newman MJ (1993) Transforming growth factor beta and the cell surface in tumor progression. Cancer Metast Rev 12:239-254
54. Nishimura S, Sekiya T (1987) Human cancer and cellular oncogenes. Biochem J 243:313-327
55. Ohmori T, Hiasa Y, Murata Y, Williams GM (1982) Gamma glutamyl transpeptidase activity in carcinogen-induced epithelial lesions of rat kidney. Gann 73:543-548
56. Ordman AB, Cleaveland JS, Boutwell RK (1985) 12-O-Tetradecanoylphorbol-13-acetate promotes tumors prior to initiation in two-stage promotion. Cancer Lett 29:79-84
57. Ozanne B, Shum A, Richards CS, Cassells D, Grossman D, Trent J, Gusterson B, Hendler F (1985) Evidence for an increase of EGF receptors in epidermoid malignancies. In: Feremisco J, Ozanne B, Stiles C (eds) Cancer cells 3, Growth factors and transformation. Cold Spring Harbor Laboratory, Cold Spring Harbor pp 41-48
58. Ozono S, Homma Y, Oyasu R (1985) Gamma glutamyl transpeptidase activity in rat urothelium treated with bladder carcinogens. Cancer Lett 29:49-57
59. Peraino C, Staffeldt EF, Carnes BA, Ludeman VA, Blomquist JA, Vesselinovitch SD (1984) Characterization of histochemically detectable altered hepatocyte foci and their relationship to hepatic tumorigenesis in rats treated once with diethylnitrosamine or benzo(a)pyrene within one day after birth. Cancer Res 44: 3340-3347
60. Pitot HC (1986) Fundamentals of oncology, 3rd ed. Marcel Dekker, New York
61. Pitot HC (1989) Progression: the terminal stage in carcinogenesis. Jpn J Cancer Res 80:599-607
62. Pitot HC (1990) Altered hepatic foci: their role in murine hepatocarcinogenesis. Annu Rev Pharmacol Toxicol 30:465-500
63. Pitot HC (1993) The molecular biology of carcinogenesis. Cancer 72:962-970
64. Pitot HC (1995) The role of receptors in multistage carcinogenesis. Mutat Res (in press)
65. Pretlow TP, O'Riordan MA, Kolman MF, Jurcisek JA (1990) Colonic aberrant crypts in azoxymethane-treated F344 rats have decreased hexosaminidase activity. Am J Pathol 136:13-16
66. Rainier S, Feinberg AP (1994) Genomic imprinting, DNA methylation, and cancer. J Natl Cancer Inst 86:753-759
67. Rao MS, Reddy JK (1987) Phenotypic properties of preneoplastic and neoplastic hepatic lesions induced by peroxisome proliferators in rats. In: Fahimi HD, Sies H (eds) Peroxisomes in biology and medicine. Springer, Heidelberg, Berlin New York, pp 263-272
68. Reed JA, McNutt NS, Prieto VG, Albino AP (1994) Expression of transforming growth factor-β2 in malignanl melanoma correlates with the depth of tumor invasion. Am J Pathol 145:97-104
69. Rho O, Beltrán LM, Gimenez-Conti IB, DiGiovanni J (1994) Altered expression of the epidermal growth factor receptor and transforming growth factor-α during multistage skin carcinogenesis in SENCAR mice. Mol Carcinog 11:19-28
70. Robles AI, Conti CJ (1995) Early overexpression of cyclin D1 protein in mouse skin carcinogenesis. Carcinogenesis 16:781-786
71. Roomi MW, Ho RK, Sarma DSR, Farber E (1985) A common biochemical pattern in preneoplastic hepatocyte nodules generated in four different models in the rat. Cancer Res 45:564-571
72. Ruggeri B, Caamano J, Goodrow T, DiRado M, Bianchi A, Trono D, Conti CJ, Klein-Szanto AJP (1991) Alterations of the p53 tumor suppressor gene during mouse skin tumor progression. Cancer Res 51:6615-6621
73. +-adenosine triphosphatase during mouse skin tumor progression. Am J Pathol 140:1179-1185
74. Said TK, Medina D (1995) Cell cyclins and cyclin-dependent kinase activities in mouse mammary tumor development. Carcinogenesis 16:823-830
75. Sato K (1989) Glutathione transferases as markers of preneoplasia and neoplasia. Adv Cancer Res 52:205-255
76. Satoh K, Halayama I, Tateoka N, Tamai K, Shimizu T, Tatematsu M, Ito N, Sato K (1989) Transient induction of single GST-P positive hepatocytes by DEN. Carcinogenesis 10:2107-2111
77. Schaff Z, Hsia CC, Sarosi I, Tabor E (1994) Overexpression of transforming growth factor-α in hepatocellular carcinoma and focal nodular hyperplasia from European patients. Hum Pathol 25:644-651
78. Scherer E, Feringa AW, Emmelot P (1984) Initiation-promotion-initiation. Induction of neoplastic foci within islands of precancerous liver cells in the rat. In: Börzsönyi M, Lapis K, Day NE, Yamasaki H (eds) Models, mechanisms and etiology of tumour promotion. International Agency for Research on Cancer, Lyon, pp 57-66
79. Schulte-Hermann R, Bursch W, Kraupp-Grasl B, Oberhammer F, Wagner A, Jirtle R (1993) Cell proliferation and apoptosis in normal liver and preneoplastic foci. Environ Health Perspect 101:87-90
80. Sidransky D, Mikkelsen T, Schwechheimer K, Rosenblum ML, Cavanee W, Vogelstein B (1992) Clonal expansion of p53 mutant cells is associated with brain tumour progression. Nature 355:846-847
81. Silverman JA, Kuhlmann ET, Zurlo J, Yager JD, Longnecker DS (1990) Expression of c-myc, c-raf-1, and c-Ki-ras in azaserine-induced pancreatic carcinomas and growing pancreas in rats. Mol Carcinog 3:379-386
82. Slaga TJ, Fischer SM, Weeks CE, Klein-Szanto AJP, Reiners J (1982) Studies on the mechanisms involved in multistage carcinogenesis in mouse skin. J Cell Biochem 18:99-119
83. Solt DB, Calderon-Solt L, Odajima T (1985) Rapid induction of carcinomas and γ-glutamyl transpeptidase-rich clones in N-methyl-N-benzylnitrosamine-treated hamster buccal pouch. J Natl Cancer Inst 74:437-445
84. Srivastava S, Wang S, Tong YA, Hao Z-M, Chang EH (1993) Dominant negative effect of a germ-line mutant p53: a step fostering tumorigenesis. Cancer Res 53:4452-4455
85. Tanaka S, Toh Y, Adachi E, Matsumata T, Mori R, Sugimachi K (1993) Tumor progression in hepatocellular carcinoma may be mediated by p53 mutation. Cancer Res 53:2884-2887
86. Tendler Y, Reshef R, Cohen I, Barzilai M, Shasha SM, Rotter V, Shkolnik T (1994) Histochemical studies of progressive p53 mutations during colonic carcinogenesis in Sprague-Dawley rats induced by N-methyl-N-nitro-nitrosoguanidine or azoxymethane. Pathobiology 62:232-237
87. Tsuda H, Hacker HJ, Katayama H, Masui T, Ito N, Bannasch P (1986) Correlative histochemical studies on preneoplastic and neoplastic lesions in the kidney of rats treated with nitrosamines. Virchows Arch 51:385-404
88. Tsuda H, Inoue T, Asamoto M, Fukushima S, Ito N, Okamura T, Ohtaguro K, Washida H, Satoh K, Amelizad Z, Oesch F (1989) Comparison of enzyme phenotypes in human bladder tumours and experimentally induced hyperplastic and neoplastic lesions of the rat urinary bladder. Virchows Arch [B] Cell Pathol 56:307-316
89. Tsuda H, Asamoto M, Baba H, Iwahori Y, Matsumoto K, Iwase T, Nishida Y, Nagao S, Hakoi K, Yamaguchi S, Ozaki K, Yamasaki H (1995) Cell proliferation and advancement of hepatocarcinogenesis in the rat are associated with a decrease in connexin 32 expression. Carcinogenesis 16:101-105
90. 1-induced glutathione S-transferase placental form in single hepatocytes. Cancer Lett 66:249-254
91. Vesselinovitch SD, Hacker HJ, Bannasch P (1985) Histochemical characterization of focal hepatic lesions induced by single diethylnitrosamine treatment in infant mice. Cancer Res 45: 2774-2780
92. Weinberg WC, Berkwits L, Iannaccone PM (1987) The clonal nature of carcinogen-induced altered foci of γ-glutamyl transpeptidase expression in rat liver. Carcinogenesis 8:565-570
93. Wildrick DM, Boman BM (1994) Does the human retinoblastoma gene have a role in colon cancer? Mol Carcinog 10:10-7
94. Yamaguchi F, Saya H, Bruner JM, Morrison RS (1994) Differential expression of two fibroblast growth factor-receptor genes is associated with malignant progression in human astrocytomas. Proc Natl Acad Sci USA 91:484-488
95. Yokota J, Sugimura T (1993) Multiple steps in carcinogenesis involving alterations of multiple tumor suppressor genes. FASEB J 7:920-925
96. Yokota K, Singh U, Shinozuka H (1990) Effects of a choline-deficient diet and a hypolipidemic agent on single glutathione S-transferase placental form-positive hepatocytes in rat liver. Jpn J Cancer Res 81:129-134
97. Yoshida T (1933) Über die serienweise Verfolgung der Veränderungen der Leber der experimentellen Hepatomerzeugung durch o-amiazotoluol. Trans Japan Pathol Soc 23:636-638
98. Yuspa SH, Kilkenny A, Cheng C, Roop D, Hennings H, Kruszewski F, Lee E, Strickland J, Greenhalgh DA (1991) Alterations in epidermal biochemistry as a consequence of stage-specific genetic changes in skin carcinogenesis. Environ Health Perspect 93:3-10