Skip to main content
Journal of Virology logoLink to Journal of Virology
. 1997 Nov;71(11):8832–8840. doi: 10.1128/jvi.71.11.8832-8840.1997

Transcription activities of human papillomavirus type 11 E6 promoter-proximal elements in raft and submerged cultures of foreskin keratinocytes.

W Zhao 1, L T Chow 1, T R Broker 1
PMCID: PMC192349  PMID: 9343243

Abstract

Human papillomaviruses (HPVs) replicate only in differentiated squamous epithelia in warts and in epithelial raft cultures grown at the medium-air interface. Virus-encoded and host transcription factors are thought to be responsible for repressing the viral enhancer and promoter located within the upstream regulatory region (URR) in the undifferentiated basal and parabasal cells while up-regulating their activities in the differentiated spinous cells. Using recombinant retroviruses, we acutely transduced neonatal foreskin keratinocytes (PHKs) with a lacZ reporter gene driven by the wild-type URR of the low-risk HPV type 11 or by a URR with individual mutations in seven promoter-proximal elements, some of which have not been characterized previously. Beta-galactosidase activities were detected in the submerged, proliferating PHKs and also in the differentiated spinous cells, but not in the steady-state proliferating basal cells, of stratified raft cultures. In particular, mutation of an Oct1, an Sp1, or a previously unknown promoter-proximal AP1 site severely reduced the reporter activity, whereas mutation of either of two NF1 sites flanking the Oct1 site had no effect. These results demonstrate changes in cellular transcription factor profiles under different culture conditions and begin to characterize the naturally differentiation-dependent activation of the URR. They provide one molecular explanation for the patterns of HPV expression in warts and help validate epithelial raft cultures as an important experimental system for genetic dissection of HPV regulatory elements.

Full Text

The Full Text of this article is available as a PDF (1.7 MB).

Selected References

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

  1. Apt D., Chong T., Liu Y., Bernard H. U. Nuclear factor I and epithelial cell-specific transcription of human papillomavirus type 16. J Virol. 1993 Aug;67(8):4455–4463. doi: 10.1128/jvi.67.8.4455-4463.1993. [DOI] [PMC free article] [PubMed] [Google Scholar]
  2. Auborn K. J., Steinberg B. M. A key DNA-protein interaction determines the function of the 5'URR enhancer in human papillomavirus type 11. Virology. 1991 Mar;181(1):132–138. doi: 10.1016/0042-6822(91)90477-s. [DOI] [PubMed] [Google Scholar]
  3. 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]
  4. Bernard H. U., Apt D. Transcriptional control and cell type specificity of HPV gene expression. Arch Dermatol. 1994 Feb;130(2):210–215. [PubMed] [Google Scholar]
  5. Butz K., Hoppe-Seyler F. Transcriptional control of human papillomavirus (HPV) oncogene expression: composition of the HPV type 18 upstream regulatory region. J Virol. 1993 Nov;67(11):6476–6486. doi: 10.1128/jvi.67.11.6476-6486.1993. [DOI] [PMC free article] [PubMed] [Google Scholar]
  6. Chan W. K., Klock G., Bernard H. U. Progesterone and glucocorticoid response elements occur in the long control regions of several human papillomaviruses involved in anogenital neoplasia. J Virol. 1989 Aug;63(8):3261–3269. doi: 10.1128/jvi.63.8.3261-3269.1989. [DOI] [PMC free article] [PubMed] [Google Scholar]
  7. Cheng S., Schmidt-Grimminger D. C., Murant T., Broker T. R., Chow L. T. Differentiation-dependent up-regulation of the human papillomavirus E7 gene reactivates cellular DNA replication in suprabasal differentiated keratinocytes. Genes Dev. 1995 Oct 1;9(19):2335–2349. doi: 10.1101/gad.9.19.2335. [DOI] [PubMed] [Google Scholar]
  8. Chin M. T., Broker T. R., Chow L. T. Identification of a novel constitutive enhancer element and an associated binding protein: implications for human papillomavirus type 11 enhancer regulation. J Virol. 1989 Jul;63(7):2967–2976. doi: 10.1128/jvi.63.7.2967-2976.1989. [DOI] [PMC free article] [PubMed] [Google Scholar]
  9. Chin M. T., Hirochika R., Hirochika H., Broker T. R., Chow L. T. Regulation of human papillomavirus type 11 enhancer and E6 promoter by activating and repressing proteins from the E2 open reading frame: functional and biochemical studies. J Virol. 1988 Aug;62(8):2994–3002. doi: 10.1128/jvi.62.8.2994-3002.1988. [DOI] [PMC free article] [PubMed] [Google Scholar]
  10. Chong T., Apt D., Gloss B., Isa M., Bernard H. U. The enhancer of human papillomavirus type 16: binding sites for the ubiquitous transcription factors oct-1, NFA, TEF-2, NF1, and AP-1 participate in epithelial cell-specific transcription. J Virol. 1991 Nov;65(11):5933–5943. doi: 10.1128/jvi.65.11.5933-5943.1991. [DOI] [PMC free article] [PubMed] [Google Scholar]
  11. Chong T., Chan W. K., Bernard H. U. Transcriptional activation of human papillomavirus 16 by nuclear factor I, AP1, steroid receptors and a possibly novel transcription factor, PVF: a model for the composition of genital papillomavirus enhancers. Nucleic Acids Res. 1990 Feb 11;18(3):465–470. doi: 10.1093/nar/18.3.465. [DOI] [PMC free article] [PubMed] [Google Scholar]
  12. 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]
  13. Cripe T. P., Alderborn A., Anderson R. D., Parkkinen S., Bergman P., Haugen T. H., Pettersson U., Turek L. P. Transcriptional activation of the human papillomavirus-16 P97 promoter by an 88-nucleotide enhancer containing distinct cell-dependent and AP-1-responsive modules. New Biol. 1990 May;2(5):450–463. [PubMed] [Google Scholar]
  14. Cripe T. P., Haugen T. H., Turk J. P., Tabatabai F., Schmid P. G., 3rd, Dürst M., Gissmann L., Roman A., Turek L. P. Transcriptional regulation of the human papillomavirus-16 E6-E7 promoter by a keratinocyte-dependent enhancer, and by viral E2 trans-activator and repressor gene products: implications for cervical carcinogenesis. EMBO J. 1987 Dec 1;6(12):3745–3753. doi: 10.1002/j.1460-2075.1987.tb02709.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  15. Dent C. L., McIndoe G. A., Latchman D. S. The constitutively expressed octamer binding protein OTF-1 and a novel octamer binding protein expressed specifically in cervical cells bind to an octamer-related sequence in the human papillomavirus 16 enhancer. Nucleic Acids Res. 1991 Aug 25;19(16):4531–4535. doi: 10.1093/nar/19.16.4531. [DOI] [PMC free article] [PubMed] [Google Scholar]
  16. DiLorenzo T. P., Steinberg B. M. Differential regulation of human papillomavirus type 6 and 11 early promoters in cultured cells derived from laryngeal papillomas. J Virol. 1995 Nov;69(11):6865–6872. doi: 10.1128/jvi.69.11.6865-6872.1995. [DOI] [PMC free article] [PubMed] [Google Scholar]
  17. Dollard S. C., Broker T. R., Chow L. T. Regulation of the human papillomavirus type 11 E6 promoter by viral and host transcription factors in primary human keratinocytes. J Virol. 1993 Mar;67(3):1721–1726. doi: 10.1128/jvi.67.3.1721-1726.1993. [DOI] [PMC free article] [PubMed] [Google Scholar]
  18. Dollard S. C., Chow L. T., Kreider J. W., Broker T. R., Lill N. L., Howett M. K. Characterization of an HPV type 11 isolate propagated in human foreskin implants in nude mice. Virology. 1989 Jul;171(1):294–297. doi: 10.1016/0042-6822(89)90542-4. [DOI] [PubMed] [Google Scholar]
  19. 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]
  20. Dong G., Broker T. R., Chow L. T. Human papillomavirus type 11 E2 proteins repress the homologous E6 promoter by interfering with the binding of host transcription factors to adjacent elements. J Virol. 1994 Feb;68(2):1115–1127. doi: 10.1128/jvi.68.2.1115-1127.1994. [DOI] [PMC free article] [PubMed] [Google Scholar]
  21. 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]
  22. Dürst M., Glitz D., Schneider A., zur Hausen H. Human papillomavirus type 16 (HPV 16) gene expression and DNA replication in cervical neoplasia: analysis by in situ hybridization. Virology. 1992 Jul;189(1):132–140. doi: 10.1016/0042-6822(92)90688-l. [DOI] [PubMed] [Google Scholar]
  23. Fisher C., Byers M. R., Iadarola M. J., Powers E. A. Patterns of epithelial expression of Fos protein suggest important role in the transition from viable to cornified cell during keratinization. Development. 1991 Feb;111(2):253–258. doi: 10.1242/dev.111.2.253. [DOI] [PubMed] [Google Scholar]
  24. Frattini M. G., Lim H. B., Laimins L. A. In vitro synthesis of oncogenic human papillomaviruses requires episomal genomes for differentiation-dependent late expression. Proc Natl Acad Sci U S A. 1996 Apr 2;93(7):3062–3067. doi: 10.1073/pnas.93.7.3062. [DOI] [PMC free article] [PubMed] [Google Scholar]
  25. 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]
  26. 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]
  27. Gloss B., Chong T., Bernard H. U. Numerous nuclear proteins bind the long control region of human papillomavirus type 16: a subset of 6 of 23 DNase I-protected segments coincides with the location of the cell-type-specific enhancer. J Virol. 1989 Mar;63(3):1142–1152. doi: 10.1128/jvi.63.3.1142-1152.1989. [DOI] [PMC free article] [PubMed] [Google Scholar]
  28. Gloss B., Yeo-Gloss M., Meisterenst M., Rogge L., Winnacker E. L., Bernard H. U. Clusters of nuclear factor I binding sites identify enhancers of several papillomaviruses but alone are not sufficient for enhancer function. Nucleic Acids Res. 1989 May 11;17(9):3519–3533. doi: 10.1093/nar/17.9.3519. [DOI] [PMC free article] [PubMed] [Google Scholar]
  29. 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]
  30. 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]
  31. Hoppe-Seyler F., Butz K. Activation of human papillomavirus type 18 E6-E7 oncogene expression by transcription factor Sp1. Nucleic Acids Res. 1992 Dec 25;20(24):6701–6706. doi: 10.1093/nar/20.24.6701. [DOI] [PMC free article] [PubMed] [Google Scholar]
  32. Hoppe-Seyler F., Butz K. Cellular control of human papillomavirus oncogene transcription. Mol Carcinog. 1994 Jul;10(3):134–141. doi: 10.1002/mc.2940100304. [DOI] [PubMed] [Google Scholar]
  33. 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]
  34. Ishiji T., Lace M. J., Parkkinen S., Anderson R. D., Haugen T. H., Cripe T. P., Xiao J. H., Davidson I., Chambon P., Turek L. P. Transcriptional enhancer factor (TEF)-1 and its cell-specific co-activator activate human papillomavirus-16 E6 and E7 oncogene transcription in keratinocytes and cervical carcinoma cells. EMBO J. 1992 Jun;11(6):2271–2281. doi: 10.1002/j.1460-2075.1992.tb05286.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  35. Jang S. I., Steinert P. M., Markova N. G. Activator protein 1 activity is involved in the regulation of the cell type-specific expression from the proximal promoter of the human profilaggrin gene. J Biol Chem. 1996 Sep 27;271(39):24105–24114. doi: 10.1074/jbc.271.39.24105. [DOI] [PubMed] [Google Scholar]
  36. Kemler I., Schaffner W. Octamer transcription factors and the cell type-specificity of immunoglobulin gene expression. FASEB J. 1990 Mar;4(5):1444–1449. doi: 10.1096/fasebj.4.5.2407588. [DOI] [PubMed] [Google Scholar]
  37. Klock G., Gloss B., Bernard H. U. Constitutive and steroid hormone regulated transcriptional enhancer elements in the genome of the human papilloma virus type 16, which is associated with neoplasia of the cervix. Cancer Detect Prev. 1988;12(1-6):23–29. [PubMed] [Google Scholar]
  38. 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]
  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. Lu B., Rothnagel J. A., Longley M. A., Tsai S. Y., Roop D. R. Differentiation-specific expression of human keratin 1 is mediated by a composite AP-1/steroid hormone element. J Biol Chem. 1994 Mar 11;269(10):7443–7449. [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. Markowitz D., Goff S., Bank A. Construction and use of a safe and efficient amphotropic packaging cell line. Virology. 1988 Dec;167(2):400–406. [PubMed] [Google Scholar]
  43. May M., Dong X. P., Beyer-Finkler E., Stubenrauch F., Fuchs P. G., Pfister H. The E6/E7 promoter of extrachromosomal HPV16 DNA in cervical cancers escapes from cellular repression by mutation of target sequences for YY1. EMBO J. 1994 Mar 15;13(6):1460–1466. doi: 10.1002/j.1460-2075.1994.tb06400.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  44. 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]
  45. Miller A. D., Rosman G. J. Improved retroviral vectors for gene transfer and expression. Biotechniques. 1989 Oct;7(9):980-2, 984-6, 989-90. [PMC free article] [PubMed] [Google Scholar]
  46. Morris P. J., Dent C. L., Ring C. J., Latchman D. S. The octamer binding site in the HPV16 regulatory region produces opposite effects on gene expression in cervical and non-cervical cells. Nucleic Acids Res. 1993 Feb 25;21(4):1019–1023. doi: 10.1093/nar/21.4.1019. [DOI] [PMC free article] [PubMed] [Google Scholar]
  47. O'Connor M. J., Tan S. H., Tan C. H., Bernard H. U. YY1 represses human papillomavirus type 16 transcription by quenching AP-1 activity. J Virol. 1996 Oct;70(10):6529–6539. doi: 10.1128/jvi.70.10.6529-6539.1996. [DOI] [PMC free article] [PubMed] [Google Scholar]
  48. O'Connor M., Bernard H. U. Oct-1 activates the epithelial-specific enhancer of human papillomavirus type 16 via a synergistic interaction with NFI at a conserved composite regulatory element. Virology. 1995 Feb 20;207(1):77–88. doi: 10.1006/viro.1995.1053. [DOI] [PubMed] [Google Scholar]
  49. 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]
  50. Parker J. N., Zhao W., Askins K. J., Broker T. R., Chow L. T. Mutational analyses of differentiation-dependent human papillomavirus type 18 enhancer elements in epithelial raft cultures of neonatal foreskin keratinocytes. Cell Growth Differ. 1997 Jul;8(7):751–762. [PubMed] [Google Scholar]
  51. Romanczuk H., Thierry F., Howley P. M. Mutational analysis of cis elements involved in E2 modulation of human papillomavirus type 16 P97 and type 18 P105 promoters. J Virol. 1990 Jun;64(6):2849–2859. doi: 10.1128/jvi.64.6.2849-2859.1990. [DOI] [PMC free article] [PubMed] [Google Scholar]
  52. Rutberg S. E., Saez E., Glick A., Dlugosz A. A., Spiegelman B. M., Yuspa S. H. Differentiation of mouse keratinocytes is accompanied by PKC-dependent changes in AP-1 proteins. Oncogene. 1996 Jul 4;13(1):167–176. [PubMed] [Google Scholar]
  53. Sanes J. R., Rubenstein J. L., Nicolas J. F. Use of a recombinant retrovirus to study post-implantation cell lineage in mouse embryos. EMBO J. 1986 Dec 1;5(12):3133–3142. doi: 10.1002/j.1460-2075.1986.tb04620.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  54. Seto E., Lewis B., Shenk T. Interaction between transcription factors Sp1 and YY1. Nature. 1993 Sep 30;365(6445):462–464. doi: 10.1038/365462a0. [DOI] [PubMed] [Google Scholar]
  55. Sibbet G. J., Campo M. S. Multiple interactions between cellular factors and the non-coding region of human papillomavirus type 16. J Gen Virol. 1990 Nov;71(Pt 11):2699–2707. doi: 10.1099/0022-1317-71-11-2699. [DOI] [PubMed] [Google Scholar]
  56. Sibbet G. J., Cuthill S., Campo M. S. The enhancer in the long control region of human papillomavirus type 16 is up-regulated by PEF-1 and down-regulated by Oct-1. J Virol. 1995 Jul;69(7):4006–4011. doi: 10.1128/jvi.69.7.4006-4011.1995. [DOI] [PMC free article] [PubMed] [Google Scholar]
  57. Stenlund A., Botchan M. R. The E2 trans-activator can act as a repressor by interfering with a cellular transcription factor. Genes Dev. 1990 Jan;4(1):123–136. doi: 10.1101/gad.4.1.123. [DOI] [PubMed] [Google Scholar]
  58. Stoler M. H., Broker T. R. In situ hybridization detection of human papillomavirus DNAs and messenger RNAs in genital condylomas and a cervical carcinoma. Hum Pathol. 1986 Dec;17(12):1250–1258. doi: 10.1016/s0046-8177(86)80569-x. [DOI] [PubMed] [Google Scholar]
  59. 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]
  60. Tan S. H., Leong L. E., Walker P. A., Bernard H. U. The human papillomavirus type 16 E2 transcription factor binds with low cooperativity to two flanking sites and represses the E6 promoter through displacement of Sp1 and TFIID. J Virol. 1994 Oct;68(10):6411–6420. doi: 10.1128/jvi.68.10.6411-6420.1994. [DOI] [PMC free article] [PubMed] [Google Scholar]
  61. 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]
  62. 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]
  63. Wang H., Liu K., Yuan F., Berdichevsky L., Taichman L. B., Auborn K. C/EBPbeta is a negative regulator of human papillomavirus type 11 in keratinocytes. J Virol. 1996 Jul;70(7):4839–4844. doi: 10.1128/jvi.70.7.4839-4844.1996. [DOI] [PMC free article] [PubMed] [Google Scholar]
  64. Welter J. F., Crish J. F., Agarwal C., Eckert R. L. Fos-related antigen (Fra-1), junB, and junD activate human involucrin promoter transcription by binding to proximal and distal AP1 sites to mediate phorbol ester effects on promoter activity. J Biol Chem. 1995 May 26;270(21):12614–12622. doi: 10.1074/jbc.270.21.12614. [DOI] [PubMed] [Google Scholar]
  65. Welter J. F., Eckert R. L. Differential expression of the fos and jun family members c-fos, fosB, Fra-1, Fra-2, c-jun, junB and junD during human epidermal keratinocyte differentiation. Oncogene. 1995 Dec 21;11(12):2681–2687. [PubMed] [Google Scholar]
  66. Wilson J. L., Dollard S. C., Chow L. T., Broker T. R. Epithelial-specific gene expression during differentiation of stratified primary human keratinocyte cultures. Cell Growth Differ. 1992 Aug;3(8):471–483. [PubMed] [Google Scholar]
  67. Xiao J. H., Davidson I., Macchi M., Rosales R., Vigneron M., Staub A., Chambon P. In vitro binding of several cell-specific and ubiquitous nuclear proteins to the GT-I motif of the SV40 enhancer. Genes Dev. 1987 Oct;1(8):794–807. doi: 10.1101/gad.1.8.794. [DOI] [PubMed] [Google Scholar]
  68. Yukawa K., Butz K., Yasui T., Kikutani H., Hoppe-Seyler F. Regulation of human papillomavirus transcription by the differentiation-dependent epithelial factor Epoc-1/skn-1a. J Virol. 1996 Jan;70(1):10–16. doi: 10.1128/jvi.70.1.10-16.1996. [DOI] [PMC free article] [PubMed] [Google Scholar]
  69. zur Hausen H., de Villiers E. M. Human papillomaviruses. Annu Rev Microbiol. 1994;48:427–447. doi: 10.1146/annurev.mi.48.100194.002235. [DOI] [PubMed] [Google Scholar]

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

RESOURCES