1887

Abstract

Binding of the human papillomavirus type 16 (HPV-16) E7 oncoprotein to the retinoblastoma protein (pRb) is thought to be involved in the cellular transformation mediated by HPV-16. Here we show that the E7 protein of the cottontail rabbit papillomavirus (CRPV) binds to the same C-terminal portion of human pRb as HPV-16 E7, and that both the CRPV and HPV-16 E7 proteins bind specifically through similar domains to rabbit pRb. Furthermore, a single amino acid substitution which reduces the binding of HPV-16 E7 to human pRb also abolishes binding of CRPV E7 to both human and rabbit pRb. The biochemical similarities observed between the HPV-16 and CRPV E7 proteins suggest that they are functionally conserved. These results further validate the use of CRPV as an animal model for the study of HPV-mediated disease.

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1993-01-01
2024-03-29
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References

  1. Baker CC, Phelps WC, Lindgren V, Braun MJ, Gonda MA, Howley PM. 1987; Structural and transcriptional analysis of human papillomavirus type 16 sequences in cervical carcinoma cell lines. Journal of Virology 61:962–971
    [Google Scholar]
  2. Barbosa MS, Wettstein FO. 1988; Identification and characterization of the CRPV E7 protein expressed in COS-7 cells. Virology 165:134–140
    [Google Scholar]
  3. Barbosa MS, Edmonds C, Fisher C, Schiller JT, Lowy DR, Vousden KH. 1990; The region of the HPV E7 oncoprotein homologous to adenovirus E1A and SV40 large T antigen contains separate domains for Rb binding and casein kinase II phosphorylation. EMBO Journal 9:153–160
    [Google Scholar]
  4. Brandsma JL, Yang ZH, Barthold SW, Johnson EA. 1991; Use of a rapid, efficient inoculation method to induce papillomas by cottontail rabbit papillomavirus DNA shows that the E7 gene is required. Proceedings of the National Academy of Sciences, U.S.A. 88:4816–4820
    [Google Scholar]
  5. Chellappan S, Kraus VB, Kroger B, Monger K, Howley PM, Phelps WC, Nevins JR. 1992; Adenovirus E1A, simian virus 40 tumor antigen, and human papillomavirus E7 protein share the capacity to disrupt the interaction between transcription factor E2F and the retinoblastoma gene product. Proceedings of the National Academy of Sciences, U.S.A. 89:4549–1553
    [Google Scholar]
  6. Chesters PM, McCance DJ. 1989; Human papillomavirus types 6 and 16 in cooperation with Ha-ras transform secondary rat embryo fibroblasts. Journal of General Virology 70:353–365
    [Google Scholar]
  7. Chesters PM, Vousden KH, Edmonds C, McCance DJ. 1990; Analysis of human papillomavirus type 16 open reading frame E7 immortalizing function in rat embryo fibroblast cells. Journal of General Virology 71:449–453
    [Google Scholar]
  8. Devereux J, Haeberli P, Smithies O. 1984; A comprehensive set of sequence analysis programs for the VAX. Nucleic Acids Research 12:387–395
    [Google Scholar]
  9. Dyson N, Duffy LA, Harlow E. 1989a; In vitro assays to detect the interaction of DNA tumor virus transforming proteins with the retinoblastoma protein. Cancer Cells 7:235–240
    [Google Scholar]
  10. Dyson N, Howley PM, Munger K, Harlow E. 1989b; The human papillomavirus 16 E7 oncoprotein is able to bind to the retinoblastoma gene product. Science 243:934–937
    [Google Scholar]
  11. Edmonds C, Vousden KH. 1989; A point mutational analysis of human papillomavirus type 16 E7 protein. Journal of Virology 63:2650–2656
    [Google Scholar]
  12. Edmonds GM, Huber HE, Defeo-Jones D, Vuocolo G, Goodhart PJ, Maigetter RZ, Sanyal G, Oliff A, Heimbrook DC. 1992; Purification and characterization of a functionally homogeneous 60 kDa species of the retinoblastoma gene product. Journal of Biological Chemistry 267:7971–7974
    [Google Scholar]
  13. Ewen ME, Ludlow JW, Marsilio E, DeCaprio JA, Millikan RC, Cheng SH, Paucha E, Livingston DM. 1989; An N-terminal transformation-governing sequence of SV40 large T antigen contributes to the binding of both p110Rb and a second cellular protein, p120. Cell 58:257–267
    [Google Scholar]
  14. Gage JR, Meyers C, Wettstein FO. 1990; The E7 proteins of the nononcogenic human papillomavirus type 6B (HPV-6b) and of the oncogenic HPV-16 differ in retinoblastoma protein binding and other properties. Journal of Virology 64:723–730
    [Google Scholar]
  15. Halbert CL, Demers GW, Galloway DA. 1991; The E7 gene of human papillomavirus type 16 is sufficient for immortalization of human epithelial cells. Journal of Virology 65:473–478
    [Google Scholar]
  16. Hawley-Nelson P, Vousden KH, Hubbert NL, Lowy DR, Schiller JT. 1989; HPV 16 E6 and E7 proteins cooperate to immortalize human foreskin keratinocytes. EMBO Journal 8:3905–3910
    [Google Scholar]
  17. Inoue H, Kondoh G, Kamakura CR, Yutsudo M, Hakura A. 1991; Progression of rat embryo fibroblast cells immortalized with transforming genes of human papillomavirus type 16. Virology 180:191–198
    [Google Scholar]
  18. Jewers RJ, Hildebrandt P, Ludlow JW, Kell B, McCance DJ. 1992; Regions of human papillomavirus type 16 E7 oncoprotein required for immortalization of human keratinocytes. Journal of Virology 66:1329–1335
    [Google Scholar]
  19. Jones RE, Wegrzyn RJ, Patrick DR, Balishin NL, Vuocolo GA, Riemen MW, Defeo-Jones D, Garsky VM, Heimbrook DC, Oliff A. 1990; Identification of HPV-16 E7 peptides that are potent antagonists of E7 binding to the retinoblastoma suppressor protein. Journal of Biological Chemistry 265:12782–12785
    [Google Scholar]
  20. Jones RE, Heimbrook DC, Huber HE, Wegrzyn RJ, Rotberg NS, Stauffer KJ, Lumma PK, Garsky VM, Oliff A. 1992; Specific iV-methylations of HPV-16 E7 peptides alter binding to the retinoblastoma suppressor protein. Journal of Biological Chemistry 267:908–912
    [Google Scholar]
  21. Kanda T, Furuno A, Yoshiike K. 1988a; Human papillomavirus type 16 open reading frame E7 encodes a transforming gene for rat 3Y1 cells. Journal of Virology 62:610–613
    [Google Scholar]
  22. Kanda T, Watanabe S, Yoshiike K. 1988b; Immortalization of primary rat cells by human papillomavirus type 16 subgenomic DNA fragments controlled by the SV40 promoter. Virology 165:321–325
    [Google Scholar]
  23. McCance DJ, Kopan R, Fuchs E, Laimins LA. 1988; Human papillomavirus type 16 alters human epithelial cell differentiation in vitro. Proceedings of the National Academy of Sciences, U.S.A. 85:7169–7173
    [Google Scholar]
  24. Marshall CJ. 1991; Tumor suppressor genes. Cell 64:313–326
    [Google Scholar]
  25. Meyers C, Harry J, Lin YL, Wettstein FO. 1992; Identification of three transforming proteins encoded by cottontail rabbit papillomavirus. Journal of Virology 66:1655–1664
    [Google Scholar]
  26. Moran E. 1988; A region of SV40 large T antigen can substitute for a transforming domain of the adenovirus E1 A products. Nature, London 334:168–170
    [Google Scholar]
  27. Munger K, Phelps WC, Bubb V, Howley PM, Schlegel R. 1989a; The E6 and E7 genes of human papillomavirus type 16 together are necessary and sufficient for transformation of primary human keratinocytes. Journal of Virology 63:4417–4421
    [Google Scholar]
  28. Munger K, Werness BA, Dyson N, Phelps WC, Harlow E, Howley PM. 1989b; Complex formation of human papillomavirus E7 proteins with the retinoblastoma tumor suppressor gene product. EMBO Journal 8:4099–4105
    [Google Scholar]
  29. Phelps WC, Yee CL, Munger K, Howley PM. 1988; The human papillomavirus type 16 E7 gene encodes transactivation and transformation functions similar to those of adenovirus E1A. Cell 53:539–547
    [Google Scholar]
  30. Phelps WC, Bagchi S, Barnes JA, Raychaudhuri P, Kraus V, Munger K, Howley PM, Nevins JR. 1991; Analysis of trans activation by human papillomavirus type 16 E7 and adenovirus 12S E1 A suggests a common mechanism. Journal of Virology 65:6922–6930
    [Google Scholar]
  31. Pirisi L, Yasumoto S, Feller M, Doniger J, DiPaolo JA. 1987; Transformation of human fibroblasts and keratinocytes with human papillomavirus type 16 DNA. Journal of Virology 61:1061–1066
    [Google Scholar]
  32. Scheffner M, Munger K, Byrne JC, Howley PM. 1991; The state of the p53 and retinoblastoma genes in human cervical carcinoma cell lines. Proceedings of the National Academy of Sciences, U.S.A. 88:5523–5527
    [Google Scholar]
  33. Scheffner M, Munger K, Huibregtse JM, Howley PM. 1992; Targeted degradation of the retinoblastoma protein by human papillomavirus E7-E6 fusion proteins. EMBO Journal 11:2425–2431
    [Google Scholar]
  34. Schwarz E, Freese UK, Gissmann L, Mayer W, Roggenbuck B, Stremlau A, zur Hausen H. 1985; Structure and transcription of human papillomavirus sequences in cervical carcinoma cells. Nature, London 341:111–114
    [Google Scholar]
  35. Smotkin D, Wettstein FO. 1986; Transcription of human papillomavirus type 16 early genes in cervical cancer and a cervical cancer derived cell line and identification of the E7 protein. Proceedings of the National Academy of Sciences, U.S.A. 83:4680–4684
    [Google Scholar]
  36. Storey A, Pim D, Murray A, Osborn K, Banks L, Crawford L. 1988; Comparison of the in vivo transforming activities of human papillomavirus types. EMBO Journal 7:1815–1820
    [Google Scholar]
  37. Vousden KH, Doniger J, DiPaolo JA, Lowy DR. 1988; The E7 open reading frame of human papillomavirus type 16 encodes a transforming gene. Oncogene Research 3:167–175
    [Google Scholar]
  38. Weinberg RA. 1991; Tumor suppressor genes. Science 254:1138–1153
    [Google Scholar]
  39. Wettstein FO. 1987; Cottontail rabbit (Shope) papillomaviruses. In The Papovaviridae vol 2 pp 167–186Edited by Salzman NP, Howley PM. New York & London: Plenum Press;
    [Google Scholar]
  40. Yasumoto S, Burkhardt AL, Doniger J, DiPaolo JA. 1986; Human papillomavirus type 16 DNA-induced malignant transformation of NIH3T3 cells. Journal of Virology 57:572–577
    [Google Scholar]
  41. zur Hausen H. 1991a; Human papillomaviruses in the pathogenesis of anogenital cancer. Virology 184:9–13
    [Google Scholar]
  42. zur Hausen H. 1991b; Viruses in human cancers. Science 254:1167–1173
    [Google Scholar]
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