Mutational analysis of human papillomavirus type 16 E6 demonstrates that p53 degradation is necessary for immortalization of mammary epithelial cells

Journal of Virology

Volumn 70, Issue 2, 1996, Pages 683-688

  Dalal, Sorab ^a   Gao, Qingshen ^a   Androphy, Elliot J ^a   Band, Vimla ^a,b  

^a TUFTS UNIVERSITY SCHOOL OF MEDICINE   (United States)

^b TUFTS MEDICAL CENTER   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

PROTEIN P53;

ARTICLE; BREAST EPITHELIUM; CARCINOGENESIS; CARCINOMA; CELL IMMORTALIZATION; CELL TRANSFORMATION; HUMAN; HUMAN CELL; PAPILLOMA VIRUS; PRIORITY JOURNAL; PROTEIN BINDING; PROTEIN DEGRADATION; TEMPERATURE SENSITIVITY; UTERINE CERVIX CANCER; VIRUS MUTATION;

EID: 0030050770     PISSN: 0022538X     EISSN: None     Source Type: Journal    
DOI: 10.1128/jvi.70.2.683-688.1996     Document Type: Article

References (39)

1. Androphy, E. J., N. L. Hubbert, J. T. Schiller, and D. R. Lowy. 1987. Identification of the HPV-16 E6 protein from transformed mouse cells and human cervical carcinoma cell lines. EMBO J. 6:989-992.
2. Band, V., S. Dalal, L. Delmolino, and E. J. Androphy. 1993. Enhanced degradation of p53 protein in HPV-6 and BPV-1 E6 immortalized human mammary epithelial cells. EMBO J. 12:1847-1852
3. Band, V., J. DeCaprio, L. Delmolino, V. Kulesa, and R. Sager. 1991. Loss of p53 protein in human papillomavirus type 16 E6-immortalized human mammary epithelial cells. J Virol 65:6671-6676.
4. Band, V., and R. Sager. 1989. Distinctive traits of normal and tumor-derived human mammary epithelial cells expressed in a medium that supports long-term growth of both cell types. Proc. Natl Acad. Sci. USA 86:1249-1253
5. Band, V., D. Zajchowski, V. Kulesa, and R. Sager. 1990. Human papillomavirus DNAs immortalize normal human mammary epithelial cells and reduce their growth factor requirements Proc Natl. Acad. Sci. USA 87:463-467.
6. Barbosa, M. S., and R. Schlegel. 1989. The E6 and E7 genes of HPV-18 are sufficient for inducing two-stage in vitro transformation of human keratinocytes. Oncogene 4:1529-1532.
7. Barbosa, M. S., W. C. Vass, D. R. Lowy, and J. T. Schiller. 1991. In vitro biological activities of the E6 and E7 genes vary among human papillomaviruses of different oncogenic potential. J. Virol. 65:292-298.
8. Bartek, J., R. Iggo, J. Gannon, and D. P. Lane. 1990. Genetic and immunochemical analysis of mutant p53 in human breast cancer cell lines. Int. J. Cancer 46:839-844.
9. Bedell, M. A., K. H. Jones, S. R. Grossman, and L. A. Laimins. 1989. Identification of human papillomavirus type 18 transforming genes in immortalized and primary cells. J Virol. 63:1247-1255.
10. Chen, J., C. E. Reid, V. Band, and E. J. Androphy. 1995. The papillomavirus E6 proteins interact with a novel calcium binding protein. Science 269:529-531
11. Crook, T., J. Tidy, and K. Vousden. 1991. Degradation of p53 can be targeted by HPV E6 sequences distinct from those required for p53 binding and trans-activation. Cell 67:547-556
12. Dalal S., V. Band, and E. J. Androphy. 1995. Unpublished data.
13. Delmolino, L., H. Band, and V. Band. 1993. Expression and stability of p53 protein in normal human mammary epithelial cells. Carcinogenesis 14:827-832.
14. Foster, S. A., G. W. Demers, B. G. Etscheid, and D. A. Galloway. 1994. The ability of human papillomavirus E6 proteins to target p53 for degradation in vivo correlates with their ability to abrogate actinomycin D-induced growth arrest. J Virol. 68:5698-5705,
15. Halbert, C. L., G. W. Demers, and D. A. Galloway. 1991. The E7 gene of human papillomavirus type 16 is sufficient for immortalization of human epithelial cells. J. Virol. 65:473-478.
16. Hawley-Nelson, P., K. H. Vousden, N. L. Hubbert, D. R. Lowy, and J. T. Schiller. 1989. HPV16 E6 and E7 proteins cooperate to immortalize human foreskin keratinocytes EMBO J. 8:3905-3910.
17. Hubbert, N. L., S. A. Sedman, and J. T. Schiller. 1992 Human papillomavirus type 16 E6 increases the degradation rate of p53 in human keratinocytes J. Virol. 66:6237-6241.
18. Huibregtse, J. M., M. Scheffner, and P. M. Howley. 1991. A cellular protein mediates association of p53 with the E6 oncoprotein of human papillomavirus types 16 or 18. EMBO J. 10:4129-4135.
19. Huibregtse, J. M., M. Scheffner, and P. M. Howley. 1993. Cloning and expression of the cDNA for E6-AP, a protein that mediates the interaction of the human papillomavirus E6 oncoprotein with p53. Mol. Cell. Biol. 13:775-784.
20. Leung, D. W., E. Chen, and D. V. Goeddel. 1988. A method for random mutagenesis of a defined DNA segment using a modified polymerase chain reaction. Techniques 5:11-18.
21. Liu, X., H. Band, Q. Gao, D. E. Wazer, Q. Chu, and V. Band. 1994. Tumor cell-specific loss of p53 protein in a unique in vitro model of human breast tumor progression Carcinogenesis 15:1969-1973.
22. Malkin, D., F. P. Li, L. C. Strong, J. F. Fraumeni, Jr., C. E. Nelson, D. H. Kim, J. Kassel, M. A. Gryka, F. Z. Bischoff, et al. 1990. Germ-line p53 mutations in a familial syndrome of breast cancer, sarcomas and other neoplasms. Science 250:1233-1238.
23. Miller, A. D., and G. J. Rosman. 1989. Improved retroviral vectors for gene transfer and expression. BioTechniques 7:980-990.
24. Munger, K., W. C. Phelps, V. Bubb, P. M. Howley, and S. R. 1989. The E6 and E7 genes of the human papillomavirus type 16 together are necessary and sufficient for transformation of primary human keratinocytes. J. Virol. 63:4417-4421.
25. Perez-Reyes, N., C. L. Halbert, P. P. Smith, E. P. Benditt, and J. K. McDougall. 1992. Immortalization of primary human smooth muscle cells. Proc. Natl. Acad. Sci. USA 89:1224-1228
26. Pim, D., A. Storey, M. Thomas, P. Massimi, and L. Banks. 1994. Mutational analysis of HPV-18 E6 identifies domains required for p53 degradation in vitro, abolition of p53 transactivation in vivo and immortalisation of primary BMK cells. Oncogene 9:1869-1876.
27. Runnebaum, I. B., M. Nagarajan, M. Bowman, D. Soto, and S. Sukumar. 1991. Mutations in p53 as potential molecular markers for human breast cancer. Proc. Natl Acad. Sci. USA 88:10657-10661.
28. Scheffner, M., J. M. Huibregtse, and P. M. Howley. 1994. Identification of a human ubiquitin-conjugating enzyme that mediates the E6-AP-dependent ubiquitination of p53 Proc. Natl. Acad. Sci. USA 91:8797-8801.
29. Scheffner, M., J. M. Huibregtse, R. D. Vierstra, and P. M. Howley. 1993. The HPV-16 E6 and E6-AP complex functions as a ubiquitin-protein ligase in the ubiquitination of p53. Cell 75:495-505.
30. Scheffner, M., K. Munger, J. M. Huibregtse, and P. M. Howley. 1992. Targeted degradation of the retinoblastoma protein by human papillomavirus E7-E6 fusion proteins. EMBO J. 11:2425-2431.
31. Scheffner, M., B. A. Werness, J. M. Huibregtse, A. J. Levine, and P. M. Howley. 1990 The E6 oncoprotein encoded by human papillomavirus types 16 and 18 promotes the degradation of p53 Cell 63:1129-1136.
32. Sedman, S. A., M. S. Barbosa, W. C. Vass, N. L. Hubbert, J. A. Haas, D. R. Lowy, and J. T. Schiller. 1991. The full-length E6 protein of human papillomavirus type 16 has transforming and trans-activating activities and cooperates with E7 to immortalize keratinocytes in culture J Virol 65:4860-4866.
33. Shay, J. W., G. Tomlinson, M. A. Piatyszek, and L. S. Gollahon. 1995. Spontaneous in vitro immortalization of breast epithelial cells from a patient with Li-Fraumeni syndrome. Mol. Cell. Biol. 15:425-432.
34. Srivastava, S., Z. Zou, K. Pirollo, W. Blattner, and E. H. Chang. 1990. Germ-line transmission of a mutated p53 gene in a cancer-prone family with Li-Fraumeni syndrome. Nature (London) 348:747-749
35. Wazer, D. E., Q. Chu, X. Liu, Q. Gao, H. Safaii, and V. Band. 1994. Loss of p53 protein during radiation transformation of primary human mammary epithelial cells. Mol. Cell. Biol. 14:2468-2478.
36. Wazer, D. E., X.-L. Liu, Q. Chu, Q. Gao, and V. Band. 1995. Immortalization of distinct human mammary epithelial cell types by human papillomavirus 16 E6 or E7. Proc Natl. Acad. Sci. USA 92:3687-3691.
37. Weis, K., G. Griffiths, and A. I. Lamond. 1994. The endoplasmic reticulum calcium-binding protein of 55 kDa is a novel EF-hand protein retained in the endoplasmic reticulum by a carboxyl-terminal His-Asp-Glu-Leu motif. J. Biol. Chem. 269:19142-19150.
38. Werness, B. A., A. J. Levine, and P. M. Howley. 1990. Association of human papillomavirus types 16 and 18 E6 proteins with p53. Science 248:76-79.
39. zur Hansen H. 1989. Papillomaviruses as carcinomaviruses, p. 1-26. In G. Klein (ed.), Advances in viral oncology. Raven Press, Ltd., New York.