Increased tumor proliferation and genomic instability without decreased apoptosis in MMTV-ras mice deficient in p53

Molecular and Cellular Biology

Volumn 17, Issue 2, 1997, Pages 723-731

  Hundley, Jeff E ^a   Koester, Steven K ^c,e   Troyer, Dean A ^a   Hilsenbeck, Susan G ^b   Subler, Mark A ^c   Windle, Jolene J ^a,c,d  

^a UNIVERSITY OF TEXAS HEALTH SCIENCE CENTER AT SAN ANTONIO   (United States)

^b Univ of Texas Health Science Center ^*  (United States)

^c University of Texas Health Science Center at San Antonio   (United States)

^d CTRC Institute for Drug Development   (United States)

^e BECKMAN COULTER INC   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

PROTEIN P53; RAS PROTEIN;

ANIMAL CELL; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BREAST TUMOR; CELL CYCLE; CELL DEATH; CHROMOSOME ANALYSIS; CONTROLLED STUDY; GENOME; GENOTYPE; MOUSE MAMMARY TUMOR ONCOVIRUS; NONHUMAN; ONCOGENE RAS; PRIORITY JOURNAL; SALIVARY GLAND TUMOR; TRANSGENIC MOUSE; TUMOR GROWTH; TUMOR SUPPRESSOR GENE;

EID: 0031012977     PISSN: 02707306     EISSN: None     Source Type: Journal    
DOI: 10.1128/MCB.17.2.723     Document Type: Article

References (54)

1. Arenas, M. J., A. H. McGregor, N. J. Toft, E. J. H. Brown, and A. H. Wyllie, 1993. Susceptibility to apoptosis is differentially regulated by c-myc and mutated Ha-ras oncogenes and is associated with endonuclease availability. Br. J. Cancer 68:1127-1133.
2. Arends, M. J., A. H. McGregor, and A. H. Wyllie. 1994. Apoplosis is inversely related to necrosis and determines net growth in tumors hearing constitutively expressed myc, ras, and HPV oncogenes. Am. J. Pathol. 144:1045-1057.
3. Auer, G. U., K. M. Heselmeyer, R. G. Steinbeck, E. Munck-Wikland, and A. D. Zetterberg. 1994. The relationship between aneuploidy and p53 overexpression during genesis of colorectal adenocarcinoma. Virchows Arch. 424:343-347.
4. Billadeau, D., D. F. Jelinek, N. Shah, T. W. LeBien, and B. Van Ness. 1995. Introduction of and activated N-ras oncogene alters the growth characteristics of the interleukin 6-dcpendent myeloma cell line ANBL6. Cancer Res. 55:3640-3646.
5. Canman, C. E., T. M. Gilmer, S. B. Coutts, and M. B. Kastan. 1995. Growth factor modulation of p53-mediated growth arrest versus apoplosis. Genes Dev. 9:600-611.
6. Clarke, A. R., M. C. Cummings, and D. J. Harrison. 1995. Interaction between murine germline mutations in p53 and APC predisposes to pancreatic neoplasia but not to increased intestinal malignancy. Oncogene 11:1913-1920.
7. Cox, D. R., and D. Oakes. 1984. Analysis of survival data. Chapman and Hall. New York, N.Y.
8. Debbas, M., and E. White. 1993. Wild-type p53 mediates apoptosis by E1A, which is inhibited by E1B. Genes Dev. 7:546-554.
9. Donehower, L. A., L. A. Godley, C. M. Aldaz, R. Pyle, Y. P. Shi, D. Pinkel, J. Gray, A. Bradley, D. Medina, and H. E. Varmus. 1995. Deficiency of p53 accelerates mammary tumorigenesis in Wnt-1 transgenic mice and promotes chromosomal instability. Genes Dev. 9:882-895.
10. Donehower, L. A., M. Harvey, B. L. Slagle, M. J. McArthur, C. A. J. Montgomery, J. S. Butel, and A. Bradley. 1992. Mice deficient for p53 are developmentally normal but susceptible to spontaneous tumours. Nature 356:215-221.
11. Elledge, R. M., G. M. Clark, S. A. W. Fuqua, Y. Yu, and D. C. Allred. 1994. p53 protein accumulation detected by five different antibodies: relationship to prognosis and heat shock protein 70 in breast cancer. Cancer Res. 54: 3752-3757.
12. Elledge, R. M., S. A. W. Fuqua, G. M. Clark, P. Pujol, and D. C. Allred. 1993. The role and prognostic significance of p53 gene alterations in breast cancer. Breast Cancer 27:95-102.
13. Elson, A., C. Deng, J. Campos-Torres, L. A. Donehower, and P. Leder. 1995. The MMTV/c-myc transgene and p53 null alleles collaborate to induce T-cell lymphomas, but not mammary carcinomas in transgenic mice. Oncogene 11:181-190.
14. Evan, G. I., A. H. Wyllie, C. S. Gilbert, T. D. Littlewood, H. Land, M. Brooks, C. M. Waters, L. Z. Penn, and D. C. Hancock. 1992. Induction of apoptosis in fibroblasts by c-myc protein. Cell 69:119-128.
15. Fujimoto, K., Y. Yaniada, E. Okajima, T. Kakizoe, H. Sasaki, T. Sugimura, and M. Terada. 1992. Frequent association of p53 gene mutation in invasive bladder cancer. Cancer Res. 52:1393-1398.
16. Gavrieli, Y., Y. Sherman, and S. A. Ben-Sasson. 1992. Identification of programmed cell death in situ via specific labeling of nuclear DNA fragmentation. J. Cell Biol. 119:493-501,
17. Hansen, R., R. Reddel, and A. Braithwaite. 1995. The transforming oncoproteins determine the mechanism by which p53 suppresses cell transformation: pRb-mediated growth arrest or apoptosis. Oncogene 11:2535-2545.
18. Harrington, E. A., M. R. Bennett, A. Fanidi, and G. I. Evan. 1994. c-myc induced apoptosis in fibroblasts is inhibited by specific cytokines. EMBO J. 13:3286-3295.
19. Harvey, M., A. T. Sands, R. S. Weiss, M. E. Hegi, R. W. Wiseman, P. Pantazis, B. C. Giovanella, M. A. Tainsky, A. Bradley, and L. A. Donehower. 1993. In vitro growth characteristics of embryo fibroblasts isolated from p53-deficient mice. Oncogene 8:2457-2467.
20. Heitjan, D. F., A. Manni, and R. J. Santen. 1993. Statistical analysis of in vivo tumor growth experiments. Cancer Res. 53:6042-6050.
21. Henneking, H., and D. Eick. 1994. Mediation of c-myc-Induced apoptosis by p53. Science 265:2091-2093.
22. Hogan, B., R. Beddington, F. Costantini, and E. Lacy. 1994. Manipulating the mouse embryo: a laboratory manual. Cold Spring Harbor Laboratory, Cold Spring Harbor, N.Y.
23. Hollstein, M., D. Sidransky, B. Vogelstein, and C. C. Harris. 1991. P53 mutations in human cancers. Science 253:49-53.
24. Hsu, B., M. C. Marin, A. K. El-Naggar, L. C. Stephens, S. Brisbay, and T. J. McDonnell. 1995. Evidence that c-myc mediated apoptosis does not require wild-type p53 during lymphomagenesis. Oncogene 11:175-179.
25. Iwaya, K., H. Tsuda, H. Hiraide, K. Tamaki, S. Tamakuma, T. Fukutomi, K. Mukai, and S. Hirohashi. 1991. Nuclear p53 immunoreaction associated with poor prognosis of breast cancer. Jpn. J. Cancer Res. 82:835-840.
26. Jerry, D. J., M. A. Ozbun, F. S. Kittrell, D. P. Lane, D. Medina, and J. S. Butel. 1993. Mutations in p53 are frequent in the preneoplastic stage of mouse mammary tumor development. Cancer Res. 53:3374-3381.
27. Kaplan. E. L., and P. L. Meier. 1958. Nonparametric estimation from incomplete observations. J. Am. Stat. Assoc. 53:457-481.
28. Krishan, A. 1975. Rapid flow cytofluorometric analysis of mammalian cell cycle by propidium iodide staining. J. Cell Biol. 66:188-195.
29. Lawce, H. J., and M. G. Brown. 1991. Harvesting, slide-making, and chromosome elongation techniques. Raven Press, New York, N.Y.
30. Liebermann, D. A., B. Hoffman, and R. A. Steinman. 1995. Molecular controls of growth arrest and apoptosis: p53-dependent and independent pathways. Oncogene 11:199-210.
31. 1 phase. Proc. Natl. Acad. Sci. USA 89:9210-9214.
32. Lin, H. J., V. Eviner, G. C. Prendergast, and E. White. 1995. Activated H-ras rescues E1A-induced apoptosis and cooperates with E1A to overcome p53-dependent growth arrest. Mol. Cell. Biol. 15:4536-4544.
33. 1 arrest. Mol. Cell. Biol. 15:6045-6054.
34. Lmngstone, L. R., A. White, E. Sprouse, E. Livanos, T. Jacks, and T. D. Tlsty. 1992. Altered cell cycle arrest and gene amplification potential accompany loss of wild-type p53. Cell 70:923-935.
35. Lowe, S. W., and H. E. Ruley. 1993. Stabilization of the p53 tumor suppressor is induced by adenovirus 5 E1A and accompanies apoptosis. Genes Dev. 7:535-545.
36. Martinez, J., I. Georgoff, J. Martinez, and A. J. Levine. 1991. Cellular localization and cell cycle regulation by a temperature-sensitive p53 protein. Genes Dev. 5:151-159.
37. Michalovitz, D., O. Halevy, and M. Oren. 1990. Conditional inhibition of transformation and of cell proliferation by a temperature-sensitive mutant of p53. Cell 62:671-680.
38. Okan, I., Y. Wang, F. Chen, L. F. Hu, S. Imreh, G. Klein, and K. G. Wiman. 1995. The EBV-encoded LMP1 protein inhibits p53-triggered apoptosis but not growth arrest. Oncogene 11:1027-1031.
39. Rao, L., M. Debbas, P. Sabbatini, D. Hockenbery, S. Korsmeyer, and E. White. 1992. The adenovirus E1A proteins induce apoptosis, which is inhibited by the E1B 19-kDa and Bcl-2 proteins. Proc. Natl. Acad. Sci. USA 89:7742-7746.
40. Rosai, J. 1993. Principles of oncologic pathology, p. 228-237. In V. T. DeVita, S. Hellman, and S. A. Rosenberg (ed.), Cancer: principles & practice of oncology, 4th ed. J. B. Lippincott Co., Philadelphia, Pa.
41. Sala, A., I. casella, L. Grasso, T. Bellon, J. C. Reed, T. Miyashita, and C. Peschle. 1996. Apoptotic response to oncogenic stimuli: cooperative and antagonistic interactions between c-myb and the growth suppressor p53. Cancer Res. 56:1991-1996.
42. Shan, B., and W.-H. Lee. 1994. Deregulated expression of E2F-1 induces S-phase entry and leads to apoptosis. Mol. Cell. Biol. 14:8166-8173.
43. Shaw, P., R. Bovey, S. Tardy, R. Sahli, B. Sordat, and J. Costa. 1992. Induction of apoptosis by wild-type p53 in a human colon tumor-derived cell line. Proc. Natl. Acad. Sc. USA 89:4495-1499.
44. Sinn, E., W. Muller, P. Pattengale, I. Tepler, R. Wallace, and P. Leder. 1987. Coexpression of MMTV/v-Ha-ras and MMTV/c-myc genes in transgenic mice: synergistic action of oncogenes in vivo. Cell 49:465-475.
45. Stewart, T. A., P. K. Pattengale, and P. Leder. 1984. Spontaneous mammary adenocarcinomas in transgenic mice that carry and express MTV/myc fusion genes. Cell 38:627-637.
46. Symonds, H., L. Krall, L. Remington, M. Saenz-Robles, S. Lowe, T. Jacks, and T. Van Dyke. 1994. p53-dependent apoptosis suppresses tumor growth and progression in vivo. Cell 78:703-711.
47. Thor, A. D., D. H. Moore, S. M. Edgerton, E. S. Kawasaki, E. Reihsaus, H. T. Lyneh, J. N. Marcus, L. Schwartz, L. Chen, B. H. Mayall, and H. S. Smith. 1992. Accumulation of p53 tumor suppressor gene protein: an independent marker of prognosis in breast cancers. J. Natl. Cancer Inst. 84:845-855.
48. Toffoli, G., C. Doglioni, C. Cernigoi, S. Frustaci, T. Perin, B. Canal, and M. Boiocchi. 1994. p53 overexpression in human soft tissue sarcomas: relation to biological aggressiveness. Ann. Oncol. 5:167-172.
49. Wagner, A. J., J. M. Kokontis, and N. Hay. 1994. Myc-mediated apoptosis requires wild-type p53 in a manner independent of cell cycle arrest and the ability of p53 to induce p21/wafl/cipl. Genes Dev. 8:2817-2830.
50. Winer, B. J. 1971. Statistical principles in experimental design. McGraw-Hill Book Co., New York, N.Y.
51. Wyllie, A. H., K. A. Rose, R. G. Morris, C. M. Steel, E. Foster, and D. A. Spandidos. 1987. Rodent fibroblast tumours expressing human myc and ras genes: growth, metastasis, and endogenous oncogenc expression. Br. J. Cancer 56:251-259.
52. Xiao-Qiang, Q., D. M. Livingstone, W. G. Daelin, and P. D. Adams. 1994. Deregulated transcription factor E2F-1 expression leads to S-phase entry and p53-mediated apoptosis. Proc. Natl. Acad. Sci. USA 91:10918-10922.
53. Yin, Y., M. A. Tainsky, F. Z. Bischoff, L. C. Strong, and G. M. Wahl. 1992. Wild-type p53 restores cell cycle control and inhibits gene amplification in cells with mutant p53 alleles. Cell 70:937-948.
54. Yonish-Rouach, E., D. Resnitzky, J. Lotem, L. Sachs, A. Kimchi, and M. Oren. 1991. Wild-type p53 induces apoptosis of myeloid leukaemic cells that is inhibited by interleukin-6. Nature 352:345-347.