Skip to main content
PMC home page
Journal of Virology logoLink to Journal of Virology
. 1993 Jul;67(7):4296–4306. doi: 10.1128/jvi.67.7.4296-4306.1993

Identification and characterization of novel promoters in the genome of human papillomavirus type 18.

S Karlen 1, P Beard 1
PMCID: PMC237800  PMID: 8389929

Abstract

Most studies on the regulation of gene expression in human papillomaviruses (HPV) have focused on the promoter for the early genes E6 and E7. This promoter is located at the junction between the long control region and the E6 open reading frame. RNA mapping studies have suggested that additional promoters may exist in other parts of the genome. In this study, we used a combination of transcription in vitro and an analysis of RNA produced in vivo in transfected cells to identify three novel promoters in the genome of human papillomavirus type 18. These promoters are located in front of the E2 gene (P2598), within the E2 coding sequences (P3036), and at the end of the L2 open reading frame (P5600). They were active in HeLa cells, as shown by a chloramphenicol acetyltransferase assay. The activity of the P3036 promoter was stimulated by the bovine papillomavirus type 1 E2 protein.

Full text

PDF
4296

Images in this article

4298Image
on p.4298
4299Image
on p.4299
4299Image
on p.4299
4300Image
on p.4300
4300Image
on p.4300
4301Image
on p.4301
4301Image
on p.4301
4302Image
on p.4302

Selected References

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

  1. Androphy E. J., Lowy D. R., Schiller J. T. Bovine papillomavirus E2 trans-activating gene product binds to specific sites in papillomavirus DNA. Nature. 1987 Jan 1;325(6099):70–73. doi: 10.1038/325070a0. [DOI] [PubMed] [Google Scholar]
  2. Baker C. C., Howley P. M. Differential promoter utilization by the bovine papillomavirus in transformed cells and productively infected wart tissues. EMBO J. 1987 Apr;6(4):1027–1035. doi: 10.1002/j.1460-2075.1987.tb04855.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  3. Banks L., Spence P., Androphy E., Hubbert N., Matlashewski G., Murray A., Crawford L. Identification of human papillomavirus type 18 E6 polypeptide in cells derived from human cervical carcinomas. J Gen Virol. 1987 May;68(Pt 5):1351–1359. doi: 10.1099/0022-1317-68-5-1351. [DOI] [PubMed] [Google Scholar]
  4. Bauknecht T., Angel P., Royer H. D., zur Hausen H. Identification of a negative regulatory domain in the human papillomavirus type 18 promoter: interaction with the transcriptional repressor YY1. EMBO J. 1992 Dec;11(12):4607–4617. doi: 10.1002/j.1460-2075.1992.tb05563.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  5. Beard P., Nyfeler K. Transcription of Simian Virus 40 chromosomes in an extract of HeLa cells. EMBO J. 1982;1(1):9–14. doi: 10.1002/j.1460-2075.1982.tb01116.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  6. Ben-Hattar J., Beard P., Jiricny J. Cytosine methylation in CTF and Sp1 recognition sites of an HSV tk promoter: effects on transcription in vivo and on factor binding in vitro. Nucleic Acids Res. 1989 Dec 25;17(24):10179–10190. doi: 10.1093/nar/17.24.10179. [DOI] [PMC free article] [PubMed] [Google Scholar]
  7. Bernard B. A., Bailly C., Lenoir M. C., Darmon M., Thierry F., Yaniv M. The human papillomavirus type 18 (HPV18) E2 gene product is a repressor of the HPV18 regulatory region in human keratinocytes. J Virol. 1989 Oct;63(10):4317–4324. doi: 10.1128/jvi.63.10.4317-4324.1989. [DOI] [PMC free article] [PubMed] [Google Scholar]
  8. Briggs M. R., Kadonaga J. T., Bell S. P., Tjian R. Purification and biochemical characterization of the promoter-specific transcription factor, Sp1. Science. 1986 Oct 3;234(4772):47–52. doi: 10.1126/science.3529394. [DOI] [PubMed] [Google Scholar]
  9. Bucher P. Weight matrix descriptions of four eukaryotic RNA polymerase II promoter elements derived from 502 unrelated promoter sequences. J Mol Biol. 1990 Apr 20;212(4):563–578. doi: 10.1016/0022-2836(90)90223-9. [DOI] [PubMed] [Google Scholar]
  10. Chow L. T., Nasseri M., Wolinsky S. M., Broker T. R. Human papillomavirus types 6 and 11 mRNAs from genital condylomata acuminata. J Virol. 1987 Aug;61(8):2581–2588. doi: 10.1128/jvi.61.8.2581-2588.1987. [DOI] [PMC free article] [PubMed] [Google Scholar]
  11. Cole S. T., Danos O. Nucleotide sequence and comparative analysis of the human papillomavirus type 18 genome. Phylogeny of papillomaviruses and repeated structure of the E6 and E7 gene products. J Mol Biol. 1987 Feb 20;193(4):599–608. doi: 10.1016/0022-2836(87)90343-3. [DOI] [PubMed] [Google Scholar]
  12. Doerig C., Hirt B., Antonietti J. P., Beard P. Nonstructural protein of parvoviruses B19 and minute virus of mice controls transcription. J Virol. 1990 Jan;64(1):387–396. doi: 10.1128/jvi.64.1.387-396.1990. [DOI] [PMC free article] [PubMed] [Google Scholar]
  13. Dollard S. C., Wilson J. L., Demeter L. M., Bonnez W., Reichman R. C., Broker T. R., Chow L. T. Production of human papillomavirus and modulation of the infectious program in epithelial raft cultures. OFF. Genes Dev. 1992 Jul;6(7):1131–1142. doi: 10.1101/gad.6.7.1131. [DOI] [PubMed] [Google Scholar]
  14. Dostatni N., Lambert P. F., Sousa R., Ham J., Howley P. M., Yaniv M. The functional BPV-1 E2 trans-activating protein can act as a repressor by preventing formation of the initiation complex. Genes Dev. 1991 Sep;5(9):1657–1671. doi: 10.1101/gad.5.9.1657. [DOI] [PubMed] [Google Scholar]
  15. Dostatni N., Thierry F., Yaniv M. A dimer of BPV-1 E2 containing a protease resistant core interacts with its DNA target. EMBO J. 1988 Dec 1;7(12):3807–3816. doi: 10.1002/j.1460-2075.1988.tb03265.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  16. Dynan W. S., Tjian R. Control of eukaryotic messenger RNA synthesis by sequence-specific DNA-binding proteins. 1985 Aug 29-Sep 4Nature. 316(6031):774–778. doi: 10.1038/316774a0. [DOI] [PubMed] [Google Scholar]
  17. Dynan W. S., Tjian R. The promoter-specific transcription factor Sp1 binds to upstream sequences in the SV40 early promoter. Cell. 1983 Nov;35(1):79–87. doi: 10.1016/0092-8674(83)90210-6. [DOI] [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. Garcia-Carranca A., Thierry F., Yaniv M. Interplay of viral and cellular proteins along the long control region of human papillomavirus type 18. J Virol. 1988 Nov;62(11):4321–4330. doi: 10.1128/jvi.62.11.4321-4330.1988. [DOI] [PMC free article] [PubMed] [Google Scholar]
  20. Gauthier J. M., Dostatni N., Lusky M., Yaniv M. Two DNA-bound E2 dimers are required for strong transcriptional activation and for cooperation with cellular factors in most cells. New Biol. 1991 May;3(5):498–509. [PubMed] [Google Scholar]
  21. Gius D., Grossman S., Bedell M. A., Laimins L. A. Inducible and constitutive enhancer domains in the noncoding region of human papillomavirus type 18. J Virol. 1988 Mar;62(3):665–672. doi: 10.1128/jvi.62.3.665-672.1988. [DOI] [PMC free article] [PubMed] [Google Scholar]
  22. Gloss B., Bernard H. U. The E6/E7 promoter of human papillomavirus type 16 is activated in the absence of E2 proteins by a sequence-aberrant Sp1 distal element. J Virol. 1990 Nov;64(11):5577–5584. doi: 10.1128/jvi.64.11.5577-5584.1990. [DOI] [PMC free article] [PubMed] [Google Scholar]
  23. Haugen T. H., Cripe T. P., Ginder G. D., Karin M., Turek L. P. Trans-activation of an upstream early gene promoter of bovine papilloma virus-1 by a product of the viral E2 gene. EMBO J. 1987 Jan;6(1):145–152. doi: 10.1002/j.1460-2075.1987.tb04732.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  24. Haugen T. H., Turek L. P., Mercurio F. M., Cripe T. P., Olson B. J., Anderson R. D., Seidl D., Karin M., Schiller J. Sequence-specific and general transcriptional activation by the bovine papillomavirus-1 E2 trans-activator require an N-terminal amphipathic helix-containing E2 domain. EMBO J. 1988 Dec 20;7(13):4245–4253. doi: 10.1002/j.1460-2075.1988.tb03322.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  25. 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]
  26. Heck D. V., Yee C. L., Howley P. M., Münger K. Efficiency of binding the retinoblastoma protein correlates with the transforming capacity of the E7 oncoproteins of the human papillomaviruses. Proc Natl Acad Sci U S A. 1992 May 15;89(10):4442–4446. doi: 10.1073/pnas.89.10.4442. [DOI] [PMC free article] [PubMed] [Google Scholar]
  27. Heike T., Miyatake S., Yoshida M., Arai K., Arai N. Bovine papilloma virus encoded E2 protein activates lymphokine genes through DNA elements, distinct from the consensus motif, in the long control region of its own genome. EMBO J. 1989 May;8(5):1411–1417. doi: 10.1002/j.1460-2075.1989.tb03522.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  28. Hen R., Sassone-Corsi P., Corden J., Gaub M. P., Chambon P. Sequences upstream from the T-A-T-A box are required in vivo and in vitro for efficient transcription from the adenovirus serotype 2 major late promoter. Proc Natl Acad Sci U S A. 1982 Dec;79(23):7132–7136. doi: 10.1073/pnas.79.23.7132. [DOI] [PMC free article] [PubMed] [Google Scholar]
  29. Hermonat P. L., Spalholz B. A., Howley P. M. The bovine papillomavirus P2443 promoter is E2 trans-responsive: evidence for E2 autoregulation. EMBO J. 1988 Sep;7(9):2815–2822. doi: 10.1002/j.1460-2075.1988.tb03137.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  30. Higgins G. D., Uzelin D. M., Phillips G. E., McEvoy P., Marin R., Burrell C. J. Transcription patterns of human papillomavirus type 16 in genital intraepithelial neoplasia: evidence for promoter usage within the E7 open reading frame during epithelial differentiation. J Gen Virol. 1992 Aug;73(Pt 8):2047–2057. doi: 10.1099/0022-1317-73-8-2047. [DOI] [PubMed] [Google Scholar]
  31. Hirochika H., Hirochika R., Broker T. R., Chow L. T. Functional mapping of the human papillomavirus type 11 transcriptional enhancer and its interaction with the trans-acting E2 proteins. Genes Dev. 1988 Jan;2(1):54–67. doi: 10.1101/gad.2.1.54. [DOI] [PubMed] [Google Scholar]
  32. Hoppe-Seyler F., Butz K., zur Hausen H. Repression of the human papillomavirus type 18 enhancer by the cellular transcription factor Oct-1. J Virol. 1991 Oct;65(10):5613–5618. doi: 10.1128/jvi.65.10.5613-5618.1991. [DOI] [PMC free article] [PubMed] [Google Scholar]
  33. Hubbert N. L., Sedman S. A., Schiller J. T. Human papillomavirus type 16 E6 increases the degradation rate of p53 in human keratinocytes. J Virol. 1992 Oct;66(10):6237–6241. doi: 10.1128/jvi.66.10.6237-6241.1992. [DOI] [PMC free article] [PubMed] [Google Scholar]
  34. Hummel M., Hudson J. B., Laimins L. A. Differentiation-induced and constitutive transcription of human papillomavirus type 31b in cell lines containing viral episomes. J Virol. 1992 Oct;66(10):6070–6080. doi: 10.1128/jvi.66.10.6070-6080.1992. [DOI] [PMC free article] [PubMed] [Google Scholar]
  35. Jones K. A., Kadonaga J. T., Luciw P. A., Tjian R. Activation of the AIDS retrovirus promoter by the cellular transcription factor, Sp1. Science. 1986 May 9;232(4751):755–759. doi: 10.1126/science.3008338. [DOI] [PubMed] [Google Scholar]
  36. Lambert P. F., Spalholz B. A., Howley P. M. A transcriptional repressor encoded by BPV-1 shares a common carboxy-terminal domain with the E2 transactivator. Cell. 1987 Jul 3;50(1):69–78. doi: 10.1016/0092-8674(87)90663-5. [DOI] [PubMed] [Google Scholar]
  37. Lechner M. S., Mack D. H., Finicle A. B., Crook T., Vousden K. H., Laimins L. A. Human papillomavirus E6 proteins bind p53 in vivo and abrogate p53-mediated repression of transcription. EMBO J. 1992 Aug;11(8):3045–3052. doi: 10.1002/j.1460-2075.1992.tb05375.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  38. Letovsky J., Dynan W. S. Measurement of the binding of transcription factor Sp1 to a single GC box recognition sequence. Nucleic Acids Res. 1989 Apr 11;17(7):2639–2653. doi: 10.1093/nar/17.7.2639. [DOI] [PMC free article] [PubMed] [Google Scholar]
  39. Li R., Knight J. D., Jackson S. P., Tjian R., Botchan M. R. Direct interaction between Sp1 and the BPV enhancer E2 protein mediates synergistic activation of transcription. Cell. 1991 May 3;65(3):493–505. doi: 10.1016/0092-8674(91)90467-d. [DOI] [PubMed] [Google Scholar]
  40. Luckow B., Schütz G. CAT constructions with multiple unique restriction sites for the functional analysis of eukaryotic promoters and regulatory elements. Nucleic Acids Res. 1987 Jul 10;15(13):5490–5490. doi: 10.1093/nar/15.13.5490. [DOI] [PMC free article] [PubMed] [Google Scholar]
  41. Mack D. H., Laimins L. A. A keratinocyte-specific transcription factor, KRF-1, interacts with AP-1 to activate expression of human papillomavirus type 18 in squamous epithelial cells. Proc Natl Acad Sci U S A. 1991 Oct 15;88(20):9102–9106. doi: 10.1073/pnas.88.20.9102. [DOI] [PMC free article] [PubMed] [Google Scholar]
  42. Manley J. L., Fire A., Cano A., Sharp P. A., Gefter M. L. DNA-dependent transcription of adenovirus genes in a soluble whole-cell extract. Proc Natl Acad Sci U S A. 1980 Jul;77(7):3855–3859. doi: 10.1073/pnas.77.7.3855. [DOI] [PMC free article] [PubMed] [Google Scholar]
  43. McBride A. A., Byrne J. C., Howley P. M. E2 polypeptides encoded by bovine papillomavirus type 1 form dimers through the common carboxyl-terminal domain: transactivation is mediated by the conserved amino-terminal domain. Proc Natl Acad Sci U S A. 1989 Jan;86(2):510–514. doi: 10.1073/pnas.86.2.510. [DOI] [PMC free article] [PubMed] [Google Scholar]
  44. Melton D. A., Krieg P. A., Rebagliati M. R., Maniatis T., Zinn K., Green M. R. Efficient in vitro synthesis of biologically active RNA and RNA hybridization probes from plasmids containing a bacteriophage SP6 promoter. Nucleic Acids Res. 1984 Sep 25;12(18):7035–7056. doi: 10.1093/nar/12.18.7035. [DOI] [PMC free article] [PubMed] [Google Scholar]
  45. Meyers C., Frattini M. G., Hudson J. B., Laimins L. A. Biosynthesis of human papillomavirus from a continuous cell line upon epithelial differentiation. Science. 1992 Aug 14;257(5072):971–973. doi: 10.1126/science.1323879. [DOI] [PubMed] [Google Scholar]
  46. 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]
  47. Nasseri M., Hirochika R., Broker T. R., Chow L. T. A human papilloma virus type 11 transcript encoding an E1--E4 protein. Virology. 1987 Aug;159(2):433–439. doi: 10.1016/0042-6822(87)90482-x. [DOI] [PubMed] [Google Scholar]
  48. Offord E. A., Beard P. A member of the activator protein 1 family found in keratinocytes but not in fibroblasts required for transcription from a human papillomavirus type 18 promoter. J Virol. 1990 Oct;64(10):4792–4798. doi: 10.1128/jvi.64.10.4792-4798.1990. [DOI] [PMC free article] [PubMed] [Google Scholar]
  49. Palermo-Dilts D. A., Broker T. R., Chow L. T. Human papillomavirus type 1 produces redundant as well as polycistronic mRNAs in plantar warts. J Virol. 1990 Jun;64(6):3144–3149. doi: 10.1128/jvi.64.6.3144-3149.1990. [DOI] [PMC free article] [PubMed] [Google Scholar]
  50. Pfister H. Biology and biochemistry of papillomaviruses. Rev Physiol Biochem Pharmacol. 1984;99:111–181. doi: 10.1007/BFb0027716. [DOI] [PubMed] [Google Scholar]
  51. Prakash S. S., Horwitz B. H., Zibello T., Settleman J., DiMaio D. Bovine papillomavirus E2 gene regulates expression of the viral E5 transforming gene. J Virol. 1988 Oct;62(10):3608–3613. doi: 10.1128/jvi.62.10.3608-3613.1988. [DOI] [PMC free article] [PubMed] [Google Scholar]
  52. Roggenbuck B., Larsen P. M., Fey S. J., Bartsch D., Gissmann L., Schwarz E. Human papillomavirus type 18 E6*, E6, and E7 protein synthesis in cell-free translation systems and comparison of E6 and E7 in vitro translation products to proteins immunoprecipitated from human epithelial cells. J Virol. 1991 Sep;65(9):5068–5072. doi: 10.1128/jvi.65.9.5068-5072.1991. [DOI] [PMC free article] [PubMed] [Google Scholar]
  53. Scheffner M., Werness B. A., Huibregtse J. M., Levine A. J., Howley P. M. The E6 oncoprotein encoded by human papillomavirus types 16 and 18 promotes the degradation of p53. Cell. 1990 Dec 21;63(6):1129–1136. doi: 10.1016/0092-8674(90)90409-8. [DOI] [PubMed] [Google Scholar]
  54. Schneider-Gädicke A., Schwarz E. Different human cervical carcinoma cell lines show similar transcription patterns of human papillomavirus type 18 early genes. EMBO J. 1986 Sep;5(9):2285–2292. doi: 10.1002/j.1460-2075.1986.tb04496.x. [DOI] [PMC free article] [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. Seedorf K., Oltersdorf T., Krämmer G., Röwekamp W. Identification of early proteins of the human papilloma viruses type 16 (HPV 16) and type 18 (HPV 18) in cervical carcinoma cells. EMBO J. 1987 Jan;6(1):139–144. doi: 10.1002/j.1460-2075.1987.tb04731.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  57. Smale S. T., Baltimore D. The "initiator" as a transcription control element. Cell. 1989 Apr 7;57(1):103–113. doi: 10.1016/0092-8674(89)90176-1. [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. Spalholz B. A., Vande Pol S. B., Howley P. M. Characterization of the cis elements involved in basal and E2-transactivated expression of the bovine papillomavirus P2443 promoter. J Virol. 1991 Feb;65(2):743–753. doi: 10.1128/jvi.65.2.743-753.1991. [DOI] [PMC free article] [PubMed] [Google Scholar]
  60. Spalholz B. A., Yang Y. C., Howley P. M. Transactivation of a bovine papilloma virus transcriptional regulatory element by the E2 gene product. Cell. 1985 Aug;42(1):183–191. doi: 10.1016/s0092-8674(85)80114-8. [DOI] [PubMed] [Google Scholar]
  61. Stenlund A., Zabielski J., Ahola H., Moreno-Lopez J., Pettersson U. Messenger RNAs from the transforming region of bovine papilloma virus type I. J Mol Biol. 1985 Apr 20;182(4):541–554. doi: 10.1016/0022-2836(85)90240-2. [DOI] [PubMed] [Google Scholar]
  62. Stoler M. H., Wolinsky S. M., Whitbeck A., Broker T. R., Chow L. T. Differentiation-linked human papillomavirus types 6 and 11 transcription in genital condylomata revealed by in situ hybridization with message-specific RNA probes. Virology. 1989 Sep;172(1):331–340. doi: 10.1016/0042-6822(89)90135-9. [DOI] [PubMed] [Google Scholar]
  63. Stubenrauch F., Malejczyk J., Fuchs P. G., Pfister H. Late promoter of human papillomavirus type 8 and its regulation. J Virol. 1992 Jun;66(6):3485–3493. doi: 10.1128/jvi.66.6.3485-3493.1992. [DOI] [PMC free article] [PubMed] [Google Scholar]
  64. Tack L. C., Beard P. Both trans-acting factors and chromatin structure are involved in the regulation of transcription from the early and late promoters in simian virus 40 chromosomes. J Virol. 1985 Apr;54(1):207–218. doi: 10.1128/jvi.54.1.207-218.1985. [DOI] [PMC free article] [PubMed] [Google Scholar]
  65. Tan S. H., Gloss B., Bernard H. U. During negative regulation of the human papillomavirus-16 E6 promoter, the viral E2 protein can displace Sp1 from a proximal promoter element. Nucleic Acids Res. 1992 Jan 25;20(2):251–256. doi: 10.1093/nar/20.2.251. [DOI] [PMC free article] [PubMed] [Google Scholar]
  66. Thierry F., Dostatni N., Arnos F., Yaniv M. Cooperative activation of transcription by bovine papillomavirus type 1 E2 can occur over a large distance. Mol Cell Biol. 1990 Aug;10(8):4431–4437. doi: 10.1128/mcb.10.8.4431. [DOI] [PMC free article] [PubMed] [Google Scholar]
  67. Thierry F., Heard J. M., Dartmann K., Yaniv M. Characterization of a transcriptional promoter of human papillomavirus 18 and modulation of its expression by simian virus 40 and adenovirus early antigens. J Virol. 1987 Jan;61(1):134–142. doi: 10.1128/jvi.61.1.134-142.1987. [DOI] [PMC free article] [PubMed] [Google Scholar]
  68. Thierry F., Spyrou G., Yaniv M., Howley P. Two AP1 sites binding JunB are essential for human papillomavirus type 18 transcription in keratinocytes. J Virol. 1992 Jun;66(6):3740–3748. doi: 10.1128/jvi.66.6.3740-3748.1992. [DOI] [PMC free article] [PubMed] [Google Scholar]
  69. Thierry F., Yaniv M. The BPV1-E2 trans-acting protein can be either an activator or a repressor of the HPV18 regulatory region. EMBO J. 1987 Nov;6(11):3391–3397. doi: 10.1002/j.1460-2075.1987.tb02662.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  70. Vaillancourt P., Nottoli T., Choe J., Botchan M. R. The E2 transactivator of bovine papillomavirus type 1 is expressed from multiple promoters. J Virol. 1990 Aug;64(8):3927–3937. doi: 10.1128/jvi.64.8.3927-3937.1990. [DOI] [PMC free article] [PubMed] [Google Scholar]
  71. Vousden K. H. Human papillomaviruses and cervical carcinoma. Cancer Cells. 1989 Oct;1(2):43–50. [PubMed] [Google Scholar]
  72. Werness B. A., Levine A. J., Howley P. M. Association of human papillomavirus types 16 and 18 E6 proteins with p53. Science. 1990 Apr 6;248(4951):76–79. doi: 10.1126/science.2157286. [DOI] [PubMed] [Google Scholar]
  73. Wettstein F. O., Barbosa M. S., Nasseri M. Identification of the major cottontail rabbit papillomavirus late RNA cap site and mapping and quantitation of an E2 and minor E6 coding mRNA in papillomas and carcinomas. Virology. 1987 Aug;159(2):321–328. doi: 10.1016/0042-6822(87)90470-3. [DOI] [PubMed] [Google Scholar]
  74. Yang Y. C., Okayama H., Howley P. M. Bovine papillomavirus contains multiple transforming genes. Proc Natl Acad Sci U S A. 1985 Feb;82(4):1030–1034. doi: 10.1073/pnas.82.4.1030. [DOI] [PMC free article] [PubMed] [Google Scholar]
  75. 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