Skip to main content
PMC home page
Journal of Virology logoLink to Journal of Virology
. 1993 Feb;67(2):716–725. doi: 10.1128/jvi.67.2.716-725.1993

Papillomavirus E7 protein binding to the retinoblastoma protein is not required for viral induction of warts.

D Defeo-Jones 1, G A Vuocolo 1, K M Haskell 1, M G Hanobik 1, D M Kiefer 1, E M McAvoy 1, M Ivey-Hoyle 1, J L Brandsma 1, A Oliff 1, R E Jones 1
PMCID: PMC237423  PMID: 8380462

Abstract

Human papillomaviruses (HPVs) are the etiologic agents responsible for benign epithelial proliferative disorders including genital warts and are a contributory factor in the pathogenesis of cervical cancer. HPVs demonstrate strict species and cell-type specificity, which is manifested by the inability of these viruses to induce disease in any species other than humans. The natural history of HPV infection in humans is closely mimicked by cottontail rabbit papillomavirus (CRPV) infection in domestic laboratory rabbits. The CRPV E7 gene is known to play an essential role in virus-mediated induction of papillomas. We now show by mutational analysis that the CRPV E7 protein's biochemical and biological properties, including binding to the retinoblastoma suppressor protein (pRB), transcription factor E2F transactivation of the adenovirus E2 promoter, disruption of pRB-E2F complexes, and cellular transformation as measured by growth in soft agar, mimic those of the HPV E7 protein. Intradermal injection of CRPV DNA lacking E7 gene sequences critical for the binding of the CRPV E7 protein to pRB induced papillomas in rabbits. These studies indicate that E7 protein binding to pRB is not required in the molecular pathogenesis of virally induced warts and suggest that other properties intrinsic to the E7 protein are necessary for papilloma formation.

Full text

PDF
716

Images in this article

719Image
on p.719
720Image
on p.720
721Image
on p.721
722Image
on p.722

Selected References

These references are in PubMed. This may not be the complete list of references from this article.

  1. Bagchi S., Weinmann R., Raychaudhuri P. The retinoblastoma protein copurifies with E2F-I, an E1A-regulated inhibitor of the transcription factor E2F. Cell. 1991 Jun 14;65(6):1063–1072. doi: 10.1016/0092-8674(91)90558-g. [DOI] [PubMed] [Google Scholar]
  2. Bandara L. R., La Thangue N. B. Adenovirus E1a prevents the retinoblastoma gene product from complexing with a cellular transcription factor. Nature. 1991 Jun 6;351(6326):494–497. doi: 10.1038/351494a0. [DOI] [PubMed] [Google Scholar]
  3. Banks L., Edmonds C., Vousden K. H. Ability of the HPV16 E7 protein to bind RB and induce DNA synthesis is not sufficient for efficient transforming activity in NIH3T3 cells. Oncogene. 1990 Sep;5(9):1383–1389. [PubMed] [Google Scholar]
  4. Barbosa M. S., Edmonds C., Fisher C., Schiller J. T., Lowy D. R., Vousden K. H. 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 J. 1990 Jan;9(1):153–160. doi: 10.1002/j.1460-2075.1990.tb08091.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  5. Barbosa M. S., Lowy D. R., Schiller J. T. Papillomavirus polypeptides E6 and E7 are zinc-binding proteins. J Virol. 1989 Mar;63(3):1404–1407. doi: 10.1128/jvi.63.3.1404-1407.1989. [DOI] [PMC free article] [PubMed] [Google Scholar]
  6. Barbosa M. S., Vass W. C., Lowy D. R., Schiller J. T. In vitro biological activities of the E6 and E7 genes vary among human papillomaviruses of different oncogenic potential. J Virol. 1991 Jan;65(1):292–298. doi: 10.1128/jvi.65.1.292-298.1991. [DOI] [PMC free article] [PubMed] [Google Scholar]
  7. Bedell M. A., Jones K. H., Grossman S. R., Laimins L. A. Identification of human papillomavirus type 18 transforming genes in immortalized and primary cells. J Virol. 1989 Mar;63(3):1247–1255. doi: 10.1128/jvi.63.3.1247-1255.1989. [DOI] [PMC free article] [PubMed] [Google Scholar]
  8. Bedell M. A., Jones K. H., Laimins L. A. The E6-E7 region of human papillomavirus type 18 is sufficient for transformation of NIH 3T3 and rat-1 cells. J Virol. 1987 Nov;61(11):3635–3640. doi: 10.1128/jvi.61.11.3635-3640.1987. [DOI] [PMC free article] [PubMed] [Google Scholar]
  9. Brandsma J. L., Yang Z. H., Barthold S. W., Johnson E. A. Use of a rapid, efficient inoculation method to induce papillomas by cottontail rabbit papillomavirus DNA shows that the E7 gene is required. Proc Natl Acad Sci U S A. 1991 Jun 1;88(11):4816–4820. doi: 10.1073/pnas.88.11.4816. [DOI] [PMC free article] [PubMed] [Google Scholar]
  10. Cao L., Faha B., Dembski M., Tsai L. H., Harlow E., Dyson N. Independent binding of the retinoblastoma protein and p107 to the transcription factor E2F. Nature. 1992 Jan 9;355(6356):176–179. doi: 10.1038/355176a0. [DOI] [PubMed] [Google Scholar]
  11. Chellappan S. P., Hiebert S., Mudryj M., Horowitz J. M., Nevins J. R. The E2F transcription factor is a cellular target for the RB protein. Cell. 1991 Jun 14;65(6):1053–1061. doi: 10.1016/0092-8674(91)90557-f. [DOI] [PubMed] [Google Scholar]
  12. Chen S., Paucha E. Identification of a region of simian virus 40 large T antigen required for cell transformation. J Virol. 1990 Jul;64(7):3350–3357. doi: 10.1128/jvi.64.7.3350-3357.1990. [DOI] [PMC free article] [PubMed] [Google Scholar]
  13. Chesters P. M., McCance D. J. Human papillomavirus types 6 and 16 in cooperation with Ha-ras transform secondary rat embryo fibroblasts. J Gen Virol. 1989 Feb;70(Pt 2):353–365. doi: 10.1099/0022-1317-70-2-353. [DOI] [PubMed] [Google Scholar]
  14. Chittenden T., Livingston D. M., Kaelin W. G., Jr The T/E1A-binding domain of the retinoblastoma product can interact selectively with a sequence-specific DNA-binding protein. Cell. 1991 Jun 14;65(6):1073–1082. doi: 10.1016/0092-8674(91)90559-h. [DOI] [PubMed] [Google Scholar]
  15. Crook T., Storey A., Almond N., Osborn K., Crawford L. Human papillomavirus type 16 cooperates with activated ras and fos oncogenes in the hormone-dependent transformation of primary mouse cells. Proc Natl Acad Sci U S A. 1988 Dec;85(23):8820–8824. doi: 10.1073/pnas.85.23.8820. [DOI] [PMC free article] [PubMed] [Google Scholar]
  16. DeCaprio J. A., Ludlow J. W., Figge J., Shew J. Y., Huang C. M., Lee W. H., Marsilio E., Paucha E., Livingston D. M. SV40 large tumor antigen forms a specific complex with the product of the retinoblastoma susceptibility gene. Cell. 1988 Jul 15;54(2):275–283. doi: 10.1016/0092-8674(88)90559-4. [DOI] [PubMed] [Google Scholar]
  17. Dignam J. D., Lebovitz R. M., Roeder R. G. Accurate transcription initiation by RNA polymerase II in a soluble extract from isolated mammalian nuclei. Nucleic Acids Res. 1983 Mar 11;11(5):1475–1489. doi: 10.1093/nar/11.5.1475. [DOI] [PMC free article] [PubMed] [Google Scholar]
  18. Dyson N., Howley P. M., Münger K., Harlow E. The human papilloma virus-16 E7 oncoprotein is able to bind to the retinoblastoma gene product. Science. 1989 Feb 17;243(4893):934–937. doi: 10.1126/science.2537532. [DOI] [PubMed] [Google Scholar]
  19. Edmonds C., Vousden K. H. A point mutational analysis of human papillomavirus type 16 E7 protein. J Virol. 1989 Jun;63(6):2650–2656. doi: 10.1128/jvi.63.6.2650-2656.1989. [DOI] [PMC free article] [PubMed] [Google Scholar]
  20. Edwards G. M., Huber H. E., DeFeo-Jones D., Vuocolo G., Goodhart P. J., Maigetter R. Z., Sanyal G., Oliff A., Heimbrook D. C. Purification and characterization of a functionally homogeneous 60-kDa species of the retinoblastoma gene product. J Biol Chem. 1992 Apr 25;267(12):7971–7974. [PubMed] [Google Scholar]
  21. Egan C., Jelsma T. N., Howe J. A., Bayley S. T., Ferguson B., Branton P. E. Mapping of cellular protein-binding sites on the products of early-region 1A of human adenovirus type 5. Mol Cell Biol. 1988 Sep;8(9):3955–3959. doi: 10.1128/mcb.8.9.3955. [DOI] [PMC free article] [PubMed] [Google Scholar]
  22. Gissmann L., Wolnik L., Ikenberg H., Koldovsky U., Schnürch H. G., zur Hausen H. Human papillomavirus types 6 and 11 DNA sequences in genital and laryngeal papillomas and in some cervical cancers. Proc Natl Acad Sci U S A. 1983 Jan;80(2):560–563. doi: 10.1073/pnas.80.2.560. [DOI] [PMC free article] [PubMed] [Google Scholar]
  23. Gorman C. M., Moffat L. F., Howard B. H. Recombinant genomes which express chloramphenicol acetyltransferase in mammalian cells. Mol Cell Biol. 1982 Sep;2(9):1044–1051. doi: 10.1128/mcb.2.9.1044. [DOI] [PMC free article] [PubMed] [Google Scholar]
  24. Gown A. M., Vogel A. M. Monoclonal antibodies to human intermediate filament proteins. II. Distribution of filament proteins in normal human tissues. Am J Pathol. 1984 Feb;114(2):309–321. [PMC free article] [PubMed] [Google Scholar]
  25. Halbert C. L., Demers G. W., Galloway D. A. The E6 and E7 genes of human papillomavirus type 6 have weak immortalizing activity in human epithelial cells. J Virol. 1992 Apr;66(4):2125–2134. doi: 10.1128/jvi.66.4.2125-2134.1992. [DOI] [PMC free article] [PubMed] [Google Scholar]
  26. Hawley-Nelson P., Vousden K. H., Hubbert N. L., Lowy D. R., Schiller J. T. HPV16 E6 and E7 proteins cooperate to immortalize human foreskin keratinocytes. EMBO J. 1989 Dec 1;8(12):3905–3910. doi: 10.1002/j.1460-2075.1989.tb08570.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  27. Hiebert S. W., Blake M., Azizkhan J., Nevins J. R. Role of E2F transcription factor in E1A-mediated trans activation of cellular genes. J Virol. 1991 Jul;65(7):3547–3552. doi: 10.1128/jvi.65.7.3547-3552.1991. [DOI] [PMC free article] [PubMed] [Google Scholar]
  28. Hudson J. B., Bedell M. A., McCance D. J., Laiminis L. A. Immortalization and altered differentiation of human keratinocytes in vitro by the E6 and E7 open reading frames of human papillomavirus type 18. J Virol. 1990 Feb;64(2):519–526. doi: 10.1128/jvi.64.2.519-526.1990. [DOI] [PMC free article] [PubMed] [Google Scholar]
  29. Jewers R. J., Hildebrandt P., Ludlow J. W., Kell B., McCance D. J. Regions of human papillomavirus type 16 E7 oncoprotein required for immortalization of human keratinocytes. J Virol. 1992 Mar;66(3):1329–1335. doi: 10.1128/jvi.66.3.1329-1335.1992. [DOI] [PMC free article] [PubMed] [Google Scholar]
  30. Jones R. E., Heimbrook D. C., Huber H. E., Wegrzyn R. J., Rotberg N. S., Stauffer K. J., Lumma P. K., Garsky V. M., Oliff A. Specific N-methylations of HPV-16 E7 peptides alter binding to the retinoblastoma suppressor protein. J Biol Chem. 1992 Jan 15;267(2):908–912. [PubMed] [Google Scholar]
  31. Jones R. E., Wegrzyn R. J., Patrick D. R., Balishin N. L., Vuocolo G. A., Riemen M. W., Defeo-Jones D., Garsky V. M., Heimbrook D. C., Oliff A. Identification of HPV-16 E7 peptides that are potent antagonists of E7 binding to the retinoblastoma suppressor protein. J Biol Chem. 1990 Aug 5;265(22):12782–12785. [PubMed] [Google Scholar]
  32. Kanda T., Furuno A., Yoshiike K. Human papillomavirus type 16 open reading frame E7 encodes a transforming gene for rat 3Y1 cells. J Virol. 1988 Feb;62(2):610–613. doi: 10.1128/jvi.62.2.610-613.1988. [DOI] [PMC free article] [PubMed] [Google Scholar]
  33. Kopan R., Traska G., Fuchs E. Retinoids as important regulators of terminal differentiation: examining keratin expression in individual epidermal cells at various stages of keratinization. J Cell Biol. 1987 Jul;105(1):427–440. doi: 10.1083/jcb.105.1.427. [DOI] [PMC free article] [PubMed] [Google Scholar]
  34. Kreider J. W., Bartlett G. L. The Shope papilloma-carcinoma complex of rabbits: a model system of neoplastic progression and spontaneous regression. Adv Cancer Res. 1981;35:81–110. doi: 10.1016/s0065-230x(08)60909-4. [DOI] [PubMed] [Google Scholar]
  35. Matlashewski G., Schneider J., Banks L., Jones N., Murray A., Crawford L. Human papillomavirus type 16 DNA cooperates with activated ras in transforming primary cells. EMBO J. 1987 Jun;6(6):1741–1746. doi: 10.1002/j.1460-2075.1987.tb02426.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  36. Meyers C., Harry J., Lin Y. L., Wettstein F. O. Identification of three transforming proteins encoded by cottontail rabbit papillomavirus. J Virol. 1992 Mar;66(3):1655–1664. doi: 10.1128/jvi.66.3.1655-1664.1992. [DOI] [PMC free article] [PubMed] [Google Scholar]
  37. Meyers C., Wettstein F. O. The late region differentially regulates the in vitro transformation by cottontail rabbit papillomavirus DNA in different cell types. Virology. 1991 Apr;181(2):637–646. doi: 10.1016/0042-6822(91)90897-k. [DOI] [PubMed] [Google Scholar]
  38. Mincheva A., Gissmann L., zur Hausen H. Chromosomal integration sites of human papillomavirus DNA in three cervical cancer cell lines mapped by in situ hybridization. Med Microbiol Immunol. 1987;176(5):245–256. doi: 10.1007/BF00190531. [DOI] [PubMed] [Google Scholar]
  39. Münger K., Phelps W. C., Bubb V., Howley P. M., Schlegel R. The E6 and E7 genes of the human papillomavirus type 16 together are necessary and sufficient for transformation of primary human keratinocytes. J Virol. 1989 Oct;63(10):4417–4421. doi: 10.1128/jvi.63.10.4417-4421.1989. [DOI] [PMC free article] [PubMed] [Google Scholar]
  40. Münger K., Werness B. A., Dyson N., Phelps W. C., Harlow E., Howley P. M. Complex formation of human papillomavirus E7 proteins with the retinoblastoma tumor suppressor gene product. EMBO J. 1989 Dec 20;8(13):4099–4105. doi: 10.1002/j.1460-2075.1989.tb08594.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  41. Münger K., Yee C. L., Phelps W. C., Pietenpol J. A., Moses H. L., Howley P. M. Biochemical and biological differences between E7 oncoproteins of the high- and low-risk human papillomavirus types are determined by amino-terminal sequences. J Virol. 1991 Jul;65(7):3943–3948. doi: 10.1128/jvi.65.7.3943-3948.1991. [DOI] [PMC free article] [PubMed] [Google Scholar]
  42. Nasseri M., Gage J. R., Lorincz A., Wettstein F. O. Human papillomavirus type 16 immortalized cervical keratinocytes contain transcripts encoding E6, E7, and E2 initiated at the P97 promoter and express high levels of E7. Virology. 1991 Sep;184(1):131–140. doi: 10.1016/0042-6822(91)90829-z. [DOI] [PubMed] [Google Scholar]
  43. Nasseri M., Meyers C., Wettstein F. O. Genetic analysis of CRPV pathogenesis: the L1 open reading frame is dispensable for cellular transformation but is required for papilloma formation. Virology. 1989 May;170(1):321–325. doi: 10.1016/0042-6822(89)90388-7. [DOI] [PubMed] [Google Scholar]
  44. Needleman S. B., Wunsch C. D. A general method applicable to the search for similarities in the amino acid sequence of two proteins. J Mol Biol. 1970 Mar;48(3):443–453. doi: 10.1016/0022-2836(70)90057-4. [DOI] [PubMed] [Google Scholar]
  45. Patrick D. R., Zhang K., Defeo-Jones D., Vuocolo G. R., Maigetter R. Z., Sardana M. K., Oliff A., Heimbrook D. C. Characterization of functional HPV-16 E7 protein produced in Escherichia coli. J Biol Chem. 1992 Apr 5;267(10):6910–6915. [PubMed] [Google Scholar]
  46. Phelps W. C., Bagchi S., Barnes J. A., Raychaudhuri P., Kraus V., Münger K., Howley P. M., Nevins J. R. Analysis of trans activation by human papillomavirus type 16 E7 and adenovirus 12S E1A suggests a common mechanism. J Virol. 1991 Dec;65(12):6922–6930. doi: 10.1128/jvi.65.12.6922-6930.1991. [DOI] [PMC free article] [PubMed] [Google Scholar]
  47. Phelps W. C., Münger K., Yee C. L., Barnes J. A., Howley P. M. Structure-function analysis of the human papillomavirus type 16 E7 oncoprotein. J Virol. 1992 Apr;66(4):2418–2427. doi: 10.1128/jvi.66.4.2418-2427.1992. [DOI] [PMC free article] [PubMed] [Google Scholar]
  48. Phelps W. C., Yee C. L., Münger K., Howley P. M. The human papillomavirus type 16 E7 gene encodes transactivation and transformation functions similar to those of adenovirus E1A. Cell. 1988 May 20;53(4):539–547. doi: 10.1016/0092-8674(88)90570-3. [DOI] [PubMed] [Google Scholar]
  49. Pietenpol J. A., Stein R. W., Moran E., Yaciuk P., Schlegel R., Lyons R. M., Pittelkow M. R., Münger K., Howley P. M., Moses H. L. TGF-beta 1 inhibition of c-myc transcription and growth in keratinocytes is abrogated by viral transforming proteins with pRB binding domains. Cell. 1990 Jun 1;61(5):777–785. doi: 10.1016/0092-8674(90)90188-k. [DOI] [PubMed] [Google Scholar]
  50. Raychaudhuri P., Rooney R., Nevins J. R. Identification of an E1A-inducible cellular factor that interacts with regulatory sequences within the adenovirus E4 promoter. EMBO J. 1987 Dec 20;6(13):4073–4081. doi: 10.1002/j.1460-2075.1987.tb02753.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  51. Rikitake Y., Moran E. DNA-binding properties of the E1A-associated 300-kilodalton protein. Mol Cell Biol. 1992 Jun;12(6):2826–2836. doi: 10.1128/mcb.12.6.2826. [DOI] [PMC free article] [PubMed] [Google Scholar]
  52. SYVERTON J. T. The pathogenesis of the rabbit papilloma-to-carcinoma sequence. Ann N Y Acad Sci. 1952 Jul 10;54(6):1126–1140. doi: 10.1111/j.1749-6632.1952.tb39983.x. [DOI] [PubMed] [Google Scholar]
  53. Saiki R. K., Gelfand D. H., Stoffel S., Scharf S. J., Higuchi R., Horn G. T., Mullis K. B., Erlich H. A. Primer-directed enzymatic amplification of DNA with a thermostable DNA polymerase. Science. 1988 Jan 29;239(4839):487–491. doi: 10.1126/science.2448875. [DOI] [PubMed] [Google Scholar]
  54. Sato H., Furuno A., Yoshiike K. Expression of human papillomavirus type 16 E7 gene induces DNA synthesis of rat 3Y1 cells. Virology. 1989 Jan;168(1):195–199. doi: 10.1016/0042-6822(89)90423-6. [DOI] [PubMed] [Google Scholar]
  55. Schwarz E., Freese U. K., Gissmann L., Mayer W., Roggenbuck B., Stremlau A., zur Hausen H. Structure and transcription of human papillomavirus sequences in cervical carcinoma cells. Nature. 1985 Mar 7;314(6006):111–114. doi: 10.1038/314111a0. [DOI] [PubMed] [Google Scholar]
  56. Sedman S. A., Barbosa M. S., Vass W. C., Hubbert N. L., Haas J. A., Lowy D. R., Schiller J. T. 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. 1991 Sep;65(9):4860–4866. doi: 10.1128/jvi.65.9.4860-4866.1991. [DOI] [PMC free article] [PubMed] [Google Scholar]
  57. Smith J. A., Pease L. G. Reverse turns in peptides and proteins. CRC Crit Rev Biochem. 1980;8(4):315–399. doi: 10.3109/10409238009105470. [DOI] [PubMed] [Google Scholar]
  58. Smotkin D., Prokoph H., Wettstein F. O. Oncogenic and nononcogenic human genital papillomaviruses generate the E7 mRNA by different mechanisms. J Virol. 1989 Mar;63(3):1441–1447. doi: 10.1128/jvi.63.3.1441-1447.1989. [DOI] [PMC free article] [PubMed] [Google Scholar]
  59. Smotkin D., Wettstein F. O. The major human papillomavirus protein in cervical cancers is a cytoplasmic phosphoprotein. J Virol. 1987 May;61(5):1686–1689. doi: 10.1128/jvi.61.5.1686-1689.1987. [DOI] [PMC free article] [PubMed] [Google Scholar]
  60. Smotkin D., Wettstein F. O. Transcription of human papillomavirus type 16 early genes in a cervical cancer and a cancer-derived cell line and identification of the E7 protein. Proc Natl Acad Sci U S A. 1986 Jul;83(13):4680–4684. doi: 10.1073/pnas.83.13.4680. [DOI] [PMC free article] [PubMed] [Google Scholar]
  61. Stirdivant S. M., Huber H. E., Patrick D. R., Defeo-Jones D., McAvoy E. M., Garsky V. M., Oliff A., Heimbrook D. C. Human papillomavirus type 16 E7 protein inhibits DNA binding by the retinoblastoma gene product. Mol Cell Biol. 1992 May;12(5):1905–1914. doi: 10.1128/mcb.12.5.1905. [DOI] [PMC free article] [PubMed] [Google Scholar]
  62. Storey A., Almond N., Osborn K., Crawford L. Mutations of the human papillomavirus type 16 E7 gene that affect transformation, transactivation and phosphorylation by the E7 protein. J Gen Virol. 1990 Apr;71(Pt 4):965–970. doi: 10.1099/0022-1317-71-4-965. [DOI] [PubMed] [Google Scholar]
  63. Storey A., Osborn K., Crawford L. Co-transformation by human papillomavirus types 6 and 11. J Gen Virol. 1990 Jan;71(Pt 1):165–171. doi: 10.1099/0022-1317-71-1-165. [DOI] [PubMed] [Google Scholar]
  64. Storey A., Pim D., Murray A., Osborn K., Banks L., Crawford L. Comparison of the in vitro transforming activities of human papillomavirus types. EMBO J. 1988 Jun;7(6):1815–1820. doi: 10.1002/j.1460-2075.1988.tb03013.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  65. Sundström C., Nilsson K. Establishment and characterization of a human histiocytic lymphoma cell line (U-937). Int J Cancer. 1976 May 15;17(5):565–577. doi: 10.1002/ijc.2910170504. [DOI] [PubMed] [Google Scholar]
  66. Tanaka A., Noda T., Yajima H., Hatanaka M., Ito Y. Identification of a transforming gene of human papillomavirus type 16. J Virol. 1989 Mar;63(3):1465–1469. doi: 10.1128/jvi.63.3.1465-1469.1989. [DOI] [PMC free article] [PubMed] [Google Scholar]
  67. Vousden K. H., Doniger J., DiPaolo J. A., Lowy D. R. The E7 open reading frame of human papillomavirus type 16 encodes a transforming gene. Oncogene Res. 1988 Sep;3(2):167–175. [PubMed] [Google Scholar]
  68. Watanabe S., Kanda T., Yoshiike K. Human papillomavirus type 16 transformation of primary human embryonic fibroblasts requires expression of open reading frames E6 and E7. J Virol. 1989 Feb;63(2):965–969. doi: 10.1128/jvi.63.2.965-969.1989. [DOI] [PMC free article] [PubMed] [Google Scholar]
  69. Watanabe S., Yoshiike K. Transformation of rat 3Y1 cells by human papillomavirus type-18 DNA. Int J Cancer. 1988 Jun 15;41(6):896–900. doi: 10.1002/ijc.2910410622. [DOI] [PubMed] [Google Scholar]
  70. Whang Y., Silberklang M., Morgan A., Munshi S., Lenny A. B., Ellis R. W., Kieff E. Expression of the Epstein-Barr virus gp350/220 gene in rodent and primate cells. J Virol. 1987 Jun;61(6):1796–1807. doi: 10.1128/jvi.61.6.1796-1807.1987. [DOI] [PMC free article] [PubMed] [Google Scholar]
  71. Whyte P., Buchkovich K. J., Horowitz J. M., Friend S. H., Raybuck M., Weinberg R. A., Harlow E. Association between an oncogene and an anti-oncogene: the adenovirus E1A proteins bind to the retinoblastoma gene product. Nature. 1988 Jul 14;334(6178):124–129. doi: 10.1038/334124a0. [DOI] [PubMed] [Google Scholar]
  72. Yee A. S., Raychaudhuri P., Jakoi L., Nevins J. R. The adenovirus-inducible factor E2F stimulates transcription after specific DNA binding. Mol Cell Biol. 1989 Feb;9(2):578–585. doi: 10.1128/mcb.9.2.578. [DOI] [PMC free article] [PubMed] [Google Scholar]
  73. de Villiers E. M. Heterogeneity of the human papillomavirus group. J Virol. 1989 Nov;63(11):4898–4903. doi: 10.1128/jvi.63.11.4898-4903.1989. [DOI] [PMC free article] [PubMed] [Google Scholar]

Articles from Journal of Virology are provided here courtesy of American Society for Microbiology (ASM)

RESOURCES