Expression of a viral oncoprotein during mammary gland development alters cell fate and function: Induction of p53-independent apoptosis is followed by impaired milk protein production in surviving cells

Cell Growth and Differentiation

Volumn 7, Issue 1, 1996, Pages 3-11

  Li, Minglin ^a   Hu, Jiadi ^a   Heermeier, Kathrin ^b   Hennighausen, Lothar ^b   Furth, Priscilla A ^a  

^a UNIVERSITY OF MARYLAND SCHOOL OF MEDICINE   (United States)

^b NATIONAL INSTITUTE OF DIABETES AND DIGESTIVE AND KIDNEY DISEASES   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

MILK PROTEIN; ONCOPROTEIN; PROTEIN P53; RNA; TUMOR MARKER; VIRUS LARGE T ANTIGEN; VIRUS PROTEIN;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL TISSUE; APOPTOSIS; ARTICLE; BREAST EPITHELIUM; BREAST TUMOR; CELL CYCLE; CELL DEATH; CONTROLLED STUDY; DEVELOPMENTAL GENETICS; GENE EXPRESSION REGULATION; LACTATION DISORDER; MOUSE; NONHUMAN; PREGNANCY; PRIORITY JOURNAL; PROMOTER REGION; PROTEIN SYNTHESIS; TRANSGENIC MOUSE;

ANIMALS; ANIMALS, SUCKLING; ANTIGENS, POLYOMAVIRUS TRANSFORMING; APOPTOSIS; BASE SEQUENCE; BCL-2-ASSOCIATED X PROTEIN; BCL-X PROTEIN; BLOTTING, NORTHERN; CELL DIFFERENTIATION; CELL TRANSFORMATION, NEOPLASTIC; CELL TRANSFORMATION, VIRAL; EPITHELIUM; FEMALE; GENE EXPRESSION REGULATION, VIRAL; IMMUNOHISTOCHEMISTRY; LACTATION; MAMMARY GLANDS, ANIMAL; MICE; MICE, TRANSGENIC; MILK PROTEINS; ONCOGENE PROTEINS, VIRAL; PREGNANCY; PROTO-ONCOGENE PROTEINS; PROTO-ONCOGENE PROTEINS C-BCL-2; RNA, MESSENGER; TRANSGENES; TUMOR MARKERS, BIOLOGICAL; TUMOR SUPPRESSOR PROTEIN P53;

ANIMALIA; MUS MUSCULUS;

EID: 0030050224     PISSN: 10449523     EISSN: None     Source Type: Journal    
DOI: None     Document Type: Article

References (36)

1. Pan, H., and Griep, A. E. Altered cell cycle regulation in the lens of HPV-16 E6 or E7 transgenic mice: implications for tumor suppressor gene function in development. Genes & Dev., 8: 1285-1299, 1994.
2. Fromm, L , Shawlot, W., Gunning, K., Butel, S. S., and Overbeek, P. A. The retinoblastoma protein-binding region of simian virus 40 large T antigen alters cell cycle regulation in lenses of transgenic mice. Mol. Cell. Biol., 14: 6743-6754, 1994.
3. Bryce, D. M., Liu, Q., Khoo, W., Tsui, L-C., and Brutman, M. L. Progressive and regressive fate of lens tumors correlates with subtle differences in transgene expression in α-crystallin -SV40 T antigen transgenic mice Oncogene, 8: 1611-1620, 1993.
4. Symonds, H., Krall, L., Remington, L., Saenz-Robles, M., Lowe, S., Jacks, T., and Van Dyke, T. p53-dependent apoptosis suppresses tumor growth and progression in vivo. Cell, 78: 703-711, 1994.
5. Tzeng, Y-J., Guhl, E., Graessmann, M., and Graessmann, A. Breast cancer formation in transgenic animals induced by the whey acidic protein SV40 T antigen (WAP-SV-T) hybrid gene. Oncogene, 8: 1965-1971, 1993.
6. Topper, Y. J., and Freeman, C. S. Multiple hormone interactions in the developmental biology of the mammary gland. Physiol. Rev., 60: 1049-1056, 1980.
7. Robinson, G., McKnight, R. A, Smith, G. H., and Hennighausen, L. Mammary epithelial cells undergo secretory differentiation in cycling virgins but require pregnancy for the establishment of terminal differentiation. Development (Camb.), 121: 2079-2090, 1995.
8. Russo, I. H., Tewari, M., and Russo, J. Morphology and development of the rat mammary gland. In: T. C. Jones, V. Mohr, and R. D. Hunt (eds.), Integument and Mammary Glands, pp. 233-252. Berlin: Springer-Verlag 1989.
9. Daniel, C. W., and Silberstein, G. B. The mammary gland: development, regulation and function. New York: Plenum Publishing Corp., 1987
10. Korsmeyer, S J Bcl-2 initiates a new category of oncogenes: regulators of cell death. Blood, 80: 879-886, 1992.
11. Li, M., Hu, J. Heermeier, K., Hennighausen, L., and Furth, P A. Apoptosis and remodeling of mammary gland tissue during involution proceeds through p53-independent pathways. Cell Growth & Differ 7: 13-20, 1996.
12. Hennighausen, L. G., and Sippel, A. E. Characterization and cloning of the mRNAs specific for the lactating mouse mammary gland. Eur. J. Biochem., 125: 131-141, 1982.
13. Morrison, B., and Leder, P. Neu and ras initiate murine mammary tumors that share genetic markers generally absent in c-myc and int-2 initiated tumors Oncogene, 9: 3417-3426, 1994.
14. Daniel, C. W., and Robinson, S. D. Regulation of mammary growth and function by TGF-β. Mol. Reprod. Dev., 32: 145-151, 1992.
15. Binas, B., Spitzer, E., Zschiefche, W., Erdmann, B., Kurtz, S., Muller, P., Niemann, C., Blenau, W., and Grosse, R. Hormonal induction of functional differentiation and mammary-derived growth inhibitor expression in cultured mouse mammary gland explants. In Vitro Cell. Dev Biol., 28A: 625-634, 1992.
16. Merlo, G. R., Basolo, F., Fiore, L., Duboc, L., and Hynes, N. E. p53-dependent and p53-independent activation of apoptosis in mammary epithelial cells reveals a survival function of EGF and insulin J. Cell Biol., 128: 1185-1196, 1995.
17. Strasser, A , Harris, A. W , Jacks, T., and Cory, S. DNA damage can Induce apoptosis in proliferating lymphoid cells via p53-independent mechanisms inhibitable by bcl-2. Cell, 79: 329-339, 1994.
18. Sedlak, T. W., Zoltan, N O., Yang, E., Wang, K., Boise, L. H., Thompson, C. B., and Korsmeyer, S. J. Multiple Bcl-2 family members demonstrate selective dimenzation with Bax Proc. Natl. Acad. Sci. USA, 92: 7834-7838, 1995
19. Oltvai, Z. N., and Korsmeyer, S. J. Checkpoints of dueling dimers foil death wishes. Cell, 79: 189-192, 1994.
20. Oltvai, Z. N., Milliman, L. L., and Korsmeyer, S. Bcl-2 heterodimerizes in vivo with a conserved homolog, bax, that accelerates programmed cell death. Cell, 74: 609-619, 1993.
21. Boise, L. H., Gonzalez-Garcia, M., Postema, C. E., Ding, L., Lindsten, T , Turka, L. A., Mao, X., Nunez, G., and Thompson, C. A. bcl-x, a bcl-2 related gene that functions as a dominant regulator of apoptotic cell death. Cell, 74: 597-608, 1993.
22. Gonzalez-Garcia, M., Perez-Ballestero, R., Ding, L., Buan, L., Boise, L., Thompson, C., and Nunez, G. Bcl-xL is the major bcl-x mRNA form expressed during murine development and its product localizes to mitochondria. Development (Camb.), 120: 3033-3042, 1994.
23. Miyashita, T , and Reed, J. C. Tumor suppressor p53 is a direct transcriptional activator of the human bax gene. Cell, 80: 293-299, 1995.
24. Schneider, J. W., Gu, W., Zhu, L., Mahdavi, W., and Nadal-Ginard, B. Reversal of terminal differentiation mediated by p107 in Rb-/- muscle cells. Science (Washington DC), 264: 1467-1471, 1994.
25. Furth, P. A., St. Onge, L., Boger, H., Gruss, P., Gossen, M., Kistner, A., Bujard, H., and Hennighausen, L. Temporal control of gene expression in transgenic mice by a tetracycline responsive promoter in transgenic mice. Proc. Natl. Acad. Sci. USA, 91: 9302-9306, 1994.
26. Hennighausen, L., Wall, R. J., Tillmann, U., Li, M., and Furth, P. A. Conditional gene expression in secretory tissues and skin of transgenic mice using the MMTV-LTR and the tetracycline responsive system. J. Cell. Biochem., 59: 463-472, 1995.
27. Basola, F., Fiore, L., Ciardiello, F., Calvo, S., Fontanini, G., Conaldi, P. G , and Toniolo, A. Response of normal and oncogene-transformed human mammary epithelial cells to transforming growth factor β1 (TGF-β1): lack of growth-inhibitory effect on cells expressing the simian virus 40 large-T antigen. Int. J. Cancer, 56: 736-742, 1994.
28. Franch, H. A., Shay, J. W., Alpern, R. J., and Preisig, P. A. Involvement of pRb family in TGFβ-dependent epithelial cell hypertrophy. J. Cell Biol., 129: 245-254, 1995.
29. Schwarz, J. K., Bassing, C. H., Kovesdi, I., Datto, M. B., Blazing, M., George, S., Wang, X-F., and Nevins, J. R. Expression of the E2F1 transcription factor overcomes type β transforming growth factor-mediated growth suppression Proc. Natl. Acad. Sci. USA, 92: 483-487, 1995.
30. Adamczewski, J. P., Gannon, J. V., and Hunt, T. Simian vims 40 large T antigen associates with cyclin A and p33cdk2. J. Virol., 67: 6551-6557, 1993.
31. Wang, W. B., Bikel, I., Marsilio, E., Newsome, D., and Livingston, D. M. Transrepression of RNA polymerase II promoters by the simian virus 40 small T antigen. J. Virol., 68: 6180-6187, 1994.
32. Rajan, P., Swaminathan, S., Zhu, J., Cole, C. N., Barber, G., Tevethia, M. J., and Thimmapaya, B. A novel translational regulation function for the simian virus large-T antigen gene. J. Virol., 69: 785-795, 1995.
33. Gilinger, G., and Alwine, J. C. Transcriptional activation by simian virus 40 large T antigen: requirements for simple promoter constructs containing either TATA or initiator elements with variable upstream factor binding sites. J. Virol., 67: 6682-6688, 1993.
34. Rice, P. W., and Cole, C. N. Efficient transcriptional activation of many simple modular promoters by simian virus 40 large T antigen. J. Virol., 67: 6689-6697, 1993.
35. Shamay, A., Pursel, V. G., Wilkinson, E., Wall, R. J., and Hennighausen, L. Expression of the whey acidic protein in transgenic pigs impairs mammary development. Transgenic Res., 1: 124-132, 1992.
36. Chomczynski, P., and Sacchi, N. Single step method of RNA isolation by acid guanidinium thiocyanate-phenol-chloroform extraction. Anal. Biochem., 162: 156-159, 1987.