1887

Journal of General Virology

Volume 74, Issue 11

Trans-activation of the adenovirus E2 promoter by human papillomavirus type 16 E7 is mediated by retinoblastoma-dependent and -independent pathways Free

Abstract

In common with the adenovirus E1A and simian virus 40 large T oncoproteins, the E7 protein of human papillomavirus (HPV) type 16 interacts with the retinoblastoma (Rb) tumour suppressor protein (pRb). The functional importance of this interaction for HPV-16 E7 protein was investigated by analysis of the trans-activating function of E7 at the adenovirus E2 promoter in a set of breast tumour cell lines. Trans-activation by HPV-16 E7 in two pRb-deficient cell lines demonstrated that pRb is not essential for E7-mediated trans-activation, but reconstitution of Rb expression indicated the existence of an Rb-mediated pathway of E7 trans-activation. This pathway results from suppression by E7 of a trans-repressing function encoded by the Rb gene. The E7 protein is shown to be capable of interacting with the Rb-related protein p107. Furthermore, analysis of a fusion construct between the amino terminus of Rb and the carboxy terminus of p107 suggests that, in common with pRb, the p107 protein trans-represses the adenovirus E2 early promoter. Therefore it is proposed that the pRb-independent pathway of E7 trans-activation is a consequence of the suppression of trans-repression by p107.

  • Received:
  • Accepted:
  • Published Online:
© Journal of General Virology 1993
Loading

Article metrics loading...

/content/journal/jgv/10.1099/0022-1317-74-11-2479
1993-11-01
2021-10-24
Loading full text...

Full text loading...

/deliver/fulltext/jgv/74/11/JV0740112479.html?itemId=/content/journal/jgv/10.1099/0022-1317-74-11-2479&mimeType=html&fmt=ahah

References

  1. Bagchi S., Weinmann R., Raychaudhuri P. 1991; The retinoblastoma protein copurifies with E2F-I, an ElA-regulated inhibitor of the transcription factor E2F. Cell 65:1063–1072
     [Google Scholar]
  2. Baker C. C., Phelps W. C., Lindgren V., Braun M. J., Gonda M. A., Howley P. M. 1987; Structural and transcriptional analysis of human papillomavirus type 16 sequences in cervical carcinoma cell lines. Journal of Virology 61:962–971
     [Google Scholar]
  3. Baker S. J., Fearon E. R., Nigro J. M., Hamilton S. R., Preisinger A. C., Jessup J. M., van Tuinen P., Ledbetter D. H., Barker D. F., Nakamura Y., White R., Vogelstein B. 1989; Chromosome 17 deletions and p53 gene mutations in colorectal carcinomas. Science 244:217–221
     [Google Scholar]
  4. Barbosa M. S., Edmonds C., Fisher C., Schiller J. T., Lowy D. R., Vousden K. H. 1990; The region of the HPV E7 oncoprotein homologous to adenovirus Ela and SV40 large T antigen contains separate domains for Rb binding and casein kinase II phosphorylation. EMBO Journal 9:153–160
     [Google Scholar]
  5. Chellappan S. P., Hiebert S., Mudryj M., Horowitz J. M., Nevins J. R. 1991; The E2F transcription factor is a cellular target for the RB protein. Cell 65:1053–1061
     [Google Scholar]
  6. Chittenden T., Livingston D. M., Kaelin W. J. 1991; The T/ElA-binding domain of the retinoblastoma product can interact selectively with a sequence-specific DNA-binding protein. Cell 65:1073–1082
     [Google Scholar]
  7. Choo K. B., Chong K. Y. 1993; Absence of mutation in the p53 and the retinoblastoma susceptibility genes in primary cervical carcinomas. Virology 193:1042–1046
     [Google Scholar]
  8. Crook T., Storey A., Almond N., Osborn K., Crawford L. 1988; Human papillomavirus type 16 cooperates with activated ras and fos oncogenes in the hormone-dependent transformation of primary mouse cells. Proceedings of the National Academy of Sciences, U.S.A 85:8820–8824
     [Google Scholar]
  9. De Villiers E.-M. 1989; Heterogeneity of the human papillomavirus group. Journal of Virology 63:4898–4903
     [Google Scholar]
  10. Dyson N., Howley P. M., Munger K., Harlow E. 1989; The human papilloma virus-16 E7 oncoprotein is able to bind to the retinoblastoma gene product. Science 243:934–937
     [Google Scholar]
  11. Edmonds C., Vousden K. H. 1989; A point mutational analysis of human papillomavirus type 16 E7 protein. Journal of Virology 63:2650–2656
     [Google Scholar]
  12. Ewen M. E., Xing Y. G., Lawrence J. B., Livingston D. M. 1991; Molecular cloning, chromosomal mapping, and expression of the cDNA for pl07, a retinoblastoma gene product-related protein. Cell 66:1155–1164
     [Google Scholar]
  13. Ewen M. E., Faha B., Harlow E., Livingston D. M. 1992; Interaction of p107 with cyclin A independent of complex formation with viral oncoproteins. Science 255:85–87
     [Google Scholar]
  14. Friend S. H., Horowitz J. M., Gerber M. R., Wang X. F., Bogenmann E., Li F. P., Weinberg R. A. 1987; Deletions of a DNA sequence in retinoblastomas and mesenchymal tumors: organization of the sequence and its encoded protein. Proceedings of the National Academy of Sciences, U,. S,. A 84:9059–9063 erratum 85, 2234
    [Google Scholar]
  15. Helin K., Lees J. A., Vidal M., Dyson N., Harlow E., Fattaey A. 1992; A cDNA encoding a pRB-binding protein with properties of the transcription factor E2F. Cell 70:337–350
     [Google Scholar]
  16. Hudson J. B., Bedell M. A., McCance D. J., Laiminis L. A. 1990; Immortalization and altered differentiation of human keratinocytes in vitro by the E6 and E7 open reading frames of human papillomavirus type 18. Journal of Virology 64:519–526
     [Google Scholar]
  17. Johnson M. A., Blomfield P. I., Bevan I. S., Woodman C. B. J., Young L. S. 1990; Analysis of human papillomavirus type 16 E6-E7 transcription in cervical carcinomas and normal cervical epithelium using the polymerase chain reaction. Journal of General Virology 71:1473–1479
     [Google Scholar]
  18. Kaelin W. J. Jr, Krek W., Sellers W. R., DeCaprio J. A., Ajchenbaum F., Fuchs C. S., Chittenden T., Li Y., Farnham P. J., Blanar M. A., Livingston D. M., Flemington E. K. 1992; Expression cloning of a cDNA encoding a retinoblastomabinding protein with E2F-like properties. Cell 70:351–364
     [Google Scholar]
  19. Kovesdi I., Reichel R., Nevins J. R. 1986; Identification of a cellular transcription factor involved in E1A trans-activation. Cell 45:219–228
     [Google Scholar]
  20. Ma J., Ptashne M. 1988; Converting a eukaryotic transcriptional inhibitor into an activator. Cell 55:443–146
     [Google Scholar]
  21. Martin K. J., Lillie J. W., Green M. R. 1990; Evidence for interaction of different eukaryotic transcriptional activators with distinct cellular targets. Nature, London 346:147–152
     [Google Scholar]
  22. Moran E., Zerler B., Harrison T. M., Mathews M. B. 1986; Identification of separate domains in the adenovirus El A gene for immortalization activity and the activation of virus early genes. Molecular and Cellular Biology 6:3470–3480
     [Google Scholar]
  23. Munger K., Werness B. A., Dyson N., Phelps W. C., Harlow E., Howley P. M. 1989; Complex formation of human papillomavirus E7 proteins with the retinoblastoma tumor suppressor gene product. EMBO Journal 8:4099–4105
     [Google Scholar]
  24. Murthy S. C., Bhat G. P., Thimmappaya B. 1985; Adenovirus EIIA early promoter: transcriptional control elements and induction by the viral pre-early EIA gene, which appears to be sequence independent. Proceedings of the National Academy of Sciences, U,. S,. A 82:2230–2234
     [Google Scholar]
  25. Pagano M., Durst M., Joswig S., Draetta G., Jansen D. P. 1992; Binding of the human E2F transcription factor to the retinoblastoma protein but not to cyclin A is abolished in HPV-16-immortalized cells. Oncogene 7:1681–1686
     [Google Scholar]
  26. Phelps W. C., Yee C. L., Munger K., Howley P. M. 1988; The human papillomavirus type 16 E7 gene encodes transactivation and transformation functions similar to those of adenovirus EIA. Cell 53:539–547
     [Google Scholar]
  27. Phelps W. C., Bagchi S., Barnes J. A., Raychaudhuri P., Kraus V., Munger K., Howley P. M., Nevins J. R. 1991; Analysis of transactivation by human papillomavirus type 16 E7 and adenovirus 12S EIA suggests a common mechanism. Journal of Virology 65:6922–6930
     [Google Scholar]
  28. Qin X. Q., Chittenden T., Livingston D. M., Kaelin W. J. 1992; Identification of a growth suppression domain within the retinoblastoma gene product. Genes and Development 6:953–964
     [Google Scholar]
  29. Robbins P. D., Horowitz J. M., Mulligan R. C. 1990; Negative regulation of human c-fos expression by the retinoblastoma gene product. Nature, London 346:668–671 erratum 351, 419
    [Google Scholar]
  30. Scheffner M., Werness B. A., Huibregtse J. M., Levine A. J., Howley P. M. 1990; The E6 oncoprotein encoded by human papillomavirus types 16 and 18 promotes the degradation of p53. Cell 63:1129–1136
     [Google Scholar]
  31. Schneider J. F., Fisher F., Goding C. R., Jones N. C. 1987; Mutational analysis of the adenovirus Ela gene: the role of transcriptional regulation in transformation. EMBO Journal 6:2053–2060
     [Google Scholar]
  32. Schwartz J. K., Devoto S. H., Smith E. J., Chellappan S. P., Jakoi L., Nevins J. R. 1993; Interactions of the pl07 and Rb proteins with E2F during the cell proliferation response. EMBO Journal 12:1013–1020
     [Google Scholar]
  33. Shirodkar S., Ewen M., DeCaprio J. A., Morgan J., Livingston D. M., Chittendon T. 1992; The transcription factor E2F interacts with the retinoblastoma product and a pl07-cyclin A complex in a cell cycle-regulated manner. Cell 68:157–166
     [Google Scholar]
  34. Storey A., Pim D., Murray A., Osborn K., Banks L., Crawford L. 1988; Comparison of the in vitro transforming activities of human papillomavirus types. EMBO Journal 7:1815–1820
     [Google Scholar]
  35. Storey A., Almond N., Osborn K., Crawford L. 1990; Mutations of the human papillomavirus type 16 E7 gene that affect transformation, transactivation and phosphorylation by the E7 protein. Journal of General Virology 71:965–970
     [Google Scholar]
  36. Takahashi T., Nau M. M., Chiba I., Birrer M. J., Rosenberg R. K., Vinocour M., Levitt M., Pass H., Oazdar A. F., Minna J. D. 1989; p53: a frequent target for genetic abnormalities in lung cancer. Science 246:491–494
     [Google Scholar]
  37. T’Ang A., Varley J. M., Chakraborty S., Murphree A. L., Fung Y. K. 1988; Structural rearrangement of the retinoblastoma gene in human breast carcinoma. Science 242:263–266
     [Google Scholar]
  38. Templeton D. J., Park S. H., Lanier L., Weinberg R. A. 1991; Nonfunctional mutants of the retinoblastoma protein are characterized by defects in phosphorylation, viral oncoprotein association, and nuclear tethering. Proceedings of the National Academy of Sciences, U,. S,. A 88:3033–3037
     [Google Scholar]
  39. Watanabe S., Kanda T., Yoshiike K. 1989; Human papillomavirus type 16 transformation of primary human embryonic fibroblasts requires expression of open reading frames E6 and E7. Journal of Virology 63:965–969
     [Google Scholar]
  40. Watanabe S., Kanda T., Sato H., Furuno A., Yoshiike K. 1990; Mutational analysis of human papillomavirus type 16 E7 functions. Journal of Virology 64:207–214
     [Google Scholar]
  41. Weintraub S. J., Prater C. A., Dean D. C. 1992; Retinoblastoma protein switches the E2F site from positive to negative element. Nature, London 358:259–261
     [Google Scholar]
  42. Werness B. A., Levine A. J., Howley P. M. 1990; Association of human papillomavirus types 16 and 18 E6 proteins with p53. Science 248:76–79
     [Google Scholar]
  43. Yokota J., Akiyama T., Fung Y. K., Benedict W. F., Namba Y., Hanaoka M., Wada M., Terasaki T., Shimosato Y., Sugimura T., Terada M. 1988; Altered expression of the retinoblastoma (RB) gene in small-cell carcinoma of the lung. Oncogene 3:471–475
     [Google Scholar]
http://instance.metastore.ingenta.com/content/journal/jgv/10.1099/0022-1317-74-11-2479
Loading
Trans-activation of the adenovirus E2 promoter by human papillomavirus type 16 E7 is mediated by retinoblastoma-dependent and -independent pathways
J. Gen. Virol. 74, 2479 (1993); https://doi.org/10.1099/0022-1317-74-11-2479
/content/journal/jgv/10.1099/0022-1317-74-11-2479
/content/journal/jgv/10.1099/0022-1317-74-11-2479
Loading

Data & Media loading...

Most cited this month Most Cited RSS feed

This is a required field
Please enter a valid email address
Approval was a Success
Invalid data
An Error Occurred
Approval was partially successful, following selected items could not be processed due to error