Apoptosis in stages of mouse hepatocarcinogenesis: Failure to counterbalance cell proliferation and to account for strain differences in tumor susceptibility

Toxicological Sciences

Volumn 85, Issue 1, 2005, Pages 515-529

  Bursch, Wilfried ^a   Chabicovsky, Monika ^a,b   Wastl, Ute ^a   Grasl Kraupp, Bettina ^a   Bukowska, Krystina ^a   Taper, Henryk ^c   Schulte Hermann, Rolf ^a  

^a MEDICAL UNIVERSITY OF VIENNA   (Austria)

^b IGENEON Immunotherapie of Cancer AG   (Austria)

^c UNIVERSITÉ CATHOLIQUE DE LOUVAIN   (Belgium)

Author keywords

Apoptosis; B6C3F1; C3H He; C57BL6J; Cell proliferation; Hepatocarcinogenesis; Phenobarbital; Tumor susceptibility

Indexed keywords

DIETHYLNITROSAMINE; DNA; PHENOBARBITAL;

ANIMAL EXPERIMENT; ANIMAL TISSUE; APOPTOSIS; ARTICLE; CANCER SUSCEPTIBILITY; CELL ACTIVITY; CELL PROLIFERATION; CONTROLLED STUDY; DNA SYNTHESIS; GROWTH RATE; HOMEOSTASIS; LIVER ADENOMA; LIVER CARCINOGENESIS; LIVER CARCINOMA; MALE; MOUSE; NONHUMAN; PRECANCER; STRAIN DIFFERENCE; TUMOR GROWTH;

ANIMALS; APOPTOSIS; CARCINOGENS; CELL DIFFERENTIATION; CELL PROLIFERATION; COCARCINOGENESIS; DIETHYLNITROSAMINE; DNA; LIVER; LIVER NEOPLASMS, EXPERIMENTAL; MALE; MICE; MICE, INBRED STRAINS; PHENOBARBITAL; PRECANCEROUS CONDITIONS; SPECIES SPECIFICITY;

EID: 18144405011     PISSN: 10966080     EISSN: None     Source Type: Journal    
DOI: 10.1093/toxsci/kfi129     Document Type: Article

References (40)

1. Ashby, J. (2001). Expectations for transgenic rodent cancer bioassay models. Toxicol. Pathol. 29 (Suppl.), 177-183.
2. Bannasch, P., and Gossner, W. (1994). Pathology of Neoplasia and Preneoplasia in Rodents (P. Bannasch and W. Gössner, Eds.), Schattauer, New York.
3. Bannasch, P., Nehrbass, D., and Kopp-Schneider, A. (2001). Significance of hepatic preneoplasia for cancer chemoprevention. IARC Sci. Publ. 154, 223-240.
4. Bursch, W., Lauer, B., Timmermann-Trosiener, I., Barthel, G., Schuppler, J., and Schulte-Hermann, R. (1984). Controlled death (apoptosis) of normal and putative preneoplastic cells in rat liver following withdrawal of tumor promoters. Carcinogenesis 5, 453-458.
5. Bursch, W., Oberhammer, F., and Schulte-Hermann, R. (1992). Cell death by apoptosis and its protective role against disease. Trends Pharmacol. Sci. 13, 245-251.
6. Bursch, W., Wastl, U., Hufnagl, K., and Schulte-Hermann, R. (2005). Apoptosis in mouse liver with high and low cancer susceptibility: I. Failure of apoptosis to increase in regressing mouse liver after withdrawal of growth stimuli or food restriction. Toxicol. Sci. (accompanying manuscript).
7. Carter, J. H., Carter, H. W., Deddens, J. A., Hurst, B. M., George, M. H., and DeAngelo, A. B. (2003). A 2-year dose-response study of lesion sequences during hepatocellular carcinogenesis in the male B6C3F(1) mouse given the drinking water chemical dichloroacetic acid. Environ. Health Perspect. 111, 53-64.
8. Chabicovsky, M., Wastl, U., Taper, H., Grasl-Kraupp, B., Schulte-Hermann, R., and Bursch, W. (2003). Induction of apoptosis in mouse liver adenoma and carcinoma in vivo by transforming growth factor-β1. J. Cancer Res. Clin. Oncol. 129, 536-542.
9. Dragani, T. A. (2003). 10 years of mouse cancer modifier loci: Human relevance. Cancer Res. 63, 3011-3018.
10. Evans, J. G., Collins, M. A., Lake, B. G., and Butler. W. H. (1992). The histology and development of hepatic nodules and carcinoma in C3H/He and C57BL/6 mice following chronic phenobarbitone administration. Toxicol. Pathol. 20, 585-594.
11. Fausto, N. (1999). Mouse liver tumorigenesis: Models, mechanisms, and relevance to human disease. Semin. Liver Dis. 19, 243-252.
12. Frey, S., Buchmann, A., Bursch, W., Schulte-Hermann, R., and Schwarz, M. (2000). Suppression of apoptosis in C3H mouse liver tumors by activated Ha-ras oncogene. Carcinogenesis 21, 161-166.
13. Gold, L. S., Slone, T. H., and Ames, B. N. (1998). What do animal cancer tests tell us about human cancer risk?: Overview of analyses of the carcinogenic potency database. Drug Metab. Rev. 30, 359-404.
14. Goldsworthy, T. L., and Fransson-Steen, R. (2002). Quantification of the cancer process in C57B1/6J, B6C3F1 and C3H/HeJ mice. Toxicol. Pathol. 30, 97-105.
15. Grasl-Kraupp, B., Bursch, W., Ruttkay-Nedecky, B., Wagner, A., Lauer, B., and Schulte-Hermann, R. (1994). Food restriction eliminates preneoplastic cells through apoptosis and antagonizes carcinogenesis in rat liver. Proc. Natl. Acad. Sci. U. S.A. 91, 9995-9999.
16. Grasl-Kraupp, B., Ruttkay-Nedecky, B., Koudelka, H-, Bukowska, K., Bursch, W., and Schulte-Hermann, R. (1995). In situ detection of fragmented DNA (TUNEL assay) fails to discriminate among apoptosis, necrosis, and autolytic cell death: A cautionary note. Hepatology 21, 1465-1468.
17. Grasl-Kraupp, B., Ruttkay-Nedecky, B., Müllauer, L., Taper, H., Huber, W., Bursch W., and Schulte-Hermann R. (1997). Inherent increase of apoptosis in liver tumors: Implications for carcinogenesis and tumor regression. Hepatology 25, 906-912.
18. Hanigan, M. H., Kemp, C. J., Ginsler, J. J., and Drinkwater, N. R. (1988) Rapid growth of preneoplastic lesions in hepatocarcinogen-sensitive C3H/HeJ male mice relative to C57BL/6J male mice. Carcinogenesis 9, 885-890.
19. James, N. H., and Roberts, R. A. (1996). Species differences in response to peroxisome proliferators correlate in vitro with induction of DNA synthesis rather than suppression of apoptosis. Carcinogenesis 17, 1623-1632.
20. James, N. H. Soames, A. R., and Roberts, R. A (1998). Suppression of hepatocyte apoptosis and induction of DNA synthesis by the rat and mouse hepatocarcinogen diethylhexylphlathate (DEHP) and the mouse hepatocarcinogen 1,4-dichlorobenzene (DCB). Arch. Toxicol. 72, 784-790.
21. Kamendulis, L. M., Kolaja, K. L., Stevenson, D. E., Walborg, E. F., Jr., and Klaunig, J. E. (2001). Comparative effects of dieldrin on hepatic ploidy, cell proliferation, and apoptosis in rodent liver. J Toxicol. Environ. Health A 62, 127-141.
22. Klaunig, J. E., Babich, M. A., Baetcke, K. P., Cook, J. C., Corton, J. C., David, R. M., DeLuca, J. G., Lai, D. Y., McKee, R. H., Peters, J. M., et al. (2003). PPARalpha agonist-induced rodent tumors: Modes of action and human relevance. Crit. Rev. Toxicol. 33, 655-780.
23. Kraupp-Grasl, B., Huber, W., Taper, H., and Schulte-Hermann, R. (1991). Increased susceptibility of aged rats to hepatocarcinogenesis by the peroxisome proliferator nafenopin and the possible involvement of altered liver foci occurring spontaneously. Cancer Res. 51, 666-671.
24. Lee, G.H. (2000). Paradoxical effects of phenobarbital on mouse hepatocarcinogenesis. Toxicol. Pathol. 28, 215-225.
25. Luebeck, G. E., Grasl-Kraupp, B., Timmermann-Trosiener, I., Bursch, W., Schulte-Hermann, R., and Moolgavkar, S. H. (1995). Growth kinetics of enzyme altered liver foci in rats treated with phenobarbital or α-hexachlorocylohexane. Toxicol. Apppl. Pharmacol. 130, 304-315.
26. Maronpot, R. R., and Boorman, G. A. (1996). The contribution of the mouse in hazard identification studies. Toxicol. Pathol. 24, 726-731.
27. Maronpot, R. R., Haseman, J. K., Boorman, G. A., Eustis, S. E., Rao, G. N., and Huff, J. E. (1987). Liver lesions in B6C3F1 mice: The National Toxicology Program, experience and position. Arch. Toxicol. Suppl. 10, 10-26.
28. Oliver, J. D., and Roberts, R. A. (2002). Receptor-mediated hepatocarcinogenesis: Role of hepatocyte proliferation and apoptosis. Pharmacol. Toxicol. 91, 1-7.
29. Parzefall, W., Kainzbauer, E., Hong-Min, Q., Chabicovsky, M., and Schulte-Hermann, R. (2002). Response of isolated hepatocytes from carcingen sensitive (C3H) and insensitive mice to signals inducing replication or apoptosis. Arch. Toxicol. 76, 699-706.
30. Pereira, M. A. (1993). Comparison in C3H and C3B6F1 mice of the sensitivity to diethylnitrosamine-initiation and phenobarbital-promotion to the extent of cell proliferation. Carcinogenesis 14, 299-302.
31. Pitot, H. C., Hikita, H., Dragan, Y., Sargent, L., and Haas, M. (2000). Review article: The stages of gastrointestinal carcinogenesis-application of rodent models to human disease. Aliment. Phannacol. Ther. 14 (Suppl. 1), 153-160.
32. Poole, T. M., and Drinkwater, N. R. (1996). Two genes abrogate the inhibition of murine hepatocarcinogenesis by ovarian hormones. Proc. Natl. Acad. Sci. U.S.A. 93, 5848-5853.
33. Sanders, S., and Thorgeirsson, S. S. (2000). Promotion of hepatocarcinogenesis by phenobarbital in c-myc/TGF-alpha transgenic mice. Mol. Carcinog. 28, 168-173.
34. Schulte-Hermann, R., Timmermann-Trosiener, I., Barthel, G., and Bursch, W. (1990). DNA synthesis, apoptosis, and phenotypic expression as determinants of growth of altered foci in rat liver during phenobarbital promotion. Cancer Res. 50, 5127-5135.
35. Schwarz, M., Buchmann, A., Stinchcombe, S., Kalkuhl, A., Bock, K. (2000). Ah receptor ligands and tumor promotion: Survival of neoplastic cells. Toxicol. Lett. 112-113, 69-77.
36. Stevenson, D. E., Walborg, E. F., Jr, North, D. W., Sielken, R. L., Jr, Ross, C. E., Wright, A. S., Xu, Y., Kamendulis, L. M., and Klaunig, J. E. (1999). Monograph: Reassessment of human cancer risk of aldrin/dieldrin. Toxicol. Lett. 109, 123-186.
37. Takahashi, M., Dinse, G. E., Foley, J. F., Hardisty, J. F., and Maronpot, R. R. (2002). Comparative prevalence, multiplicity, and progression of spontaneous and vinyl carbamate-induced liver lesions in five strains of male mice. Toxicol. Pathol. 30, 599-605.
38. Tharappel, J. C., Lee, E. Y., Robertson, L. W., Spear, B. T., and Glauert, H. P. (2002). Regulation of cell proliferation, apoptosis, and transcription factor activities during the promotion of liver carcinogenesis by polychlorinated biphenyls. Toxicol. Appl. Pharmacol. 179, 172-184.
39. Turusov, V S., and Turusov, S. (1979). Tumours of the liver. In Pathology of Tumours in Laboratory Animals (V. S. Turusov, Ed.), pp. 193-234. International Agency für Research on Cancer, Lyon.
40. Whysner, J., Ross, P. M., and Williams GM. (1996). Phenobarbital mechanistic data and risk assessment: Enzyme induction, enhanced cell proliferation, and tumor promotion. Pharmacol. Ther. 71(1-2), 153-191.