1887

Abstract

Cellular factors that bind to sequences in the human papillomavirus 16 (HPV-16) upstream regulatory region (URR) positively and negatively regulate the viral E6 and E7 oncogene promoter, P97. DNase I footprinting has revealed the binding of cellular proteins to two previously undetected elements overlapping and 3′ of the transcription-initiation site of the P97 promoter. Mutations within homologous motifs found in both of these elements abolished their negative function and the binding of the same cellular complex . This factor was identified as YY1 by complex mobility and binding specificity in comparison with vaccinia virus-expressed, purified recombinant YY1 protein and by antigenic reactivity with YY1 antisera. mutations in the ‘initiator’ YY1 site activated the P97 promoter and . P97 was also activated threefold by depletion of endogenous YY1 with wild-type, but not mutant, YY1 oligonucleotides from the IgH kappa E3′ enhancer. Furthermore, increasing concentrations of exogenous, purified recombinant YY1 repressed wild-type P97 transcript levels by up to threefold, but did not influence the P97 promoter mutated in the ‘initiator’ YY1 site. Thus, the promoter-proximal YY1 site was not necessary for correct transcription initiation at the P97 promoter, but was found to be required for downregulation of P97 transcription and . In contrast to other viral and cellular promoters, where YY1 is thought to function as a positive transcription-‘initiator’ factor, HPV-16 P97 transcription is downregulated by YY1 from a critical motif overlapping the transcription start site.

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2009-10-01
2021-10-18
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References

  1. Baritaki S., Sifakis S., Huerta-Yepez S., Neonakis I. K., Soufla G., Bonavida B., Spandidos D. A. 2007; Overexpression of VEGF and TGF- β 1 mRNA in Pap smears correlates with progression of cervical intraepithelial neoplasia to cancer: implication of YY1 in cervical tumorigenesis and HPV infection. Int J Oncol 31:69–79
    [Google Scholar]
  2. Bauknecht T., Angel P., Royer H. D., zur Hausen H. 1992; Identification of a negative regulatory domain in the human papillomavirus type 18 promoter: interaction with the transcriptional repressor YY1. EMBO J 11:4607–4617
    [Google Scholar]
  3. Boukamp P., Petrussevska R. T., Breitkreutz D., Hornung J., Markham A., Fusenig N. E. 1988; Normal keratinization in a spontaneously immortalized aneuploid human keratinocyte cell line. J Cell Biol 106:761–771 [CrossRef]
    [Google Scholar]
  4. Broyles S. S., Liu X., Zhu M., Kremer M. 1999; Transcription factor YY1 is a vaccinia virus late promoter activator. J Biol Chem 274:35662–35667 [CrossRef]
    [Google Scholar]
  5. Coull J. J., Romerio F., Sun J. M., Volker J. L., Galvin K. M., Davie J. R., Shi Y., Hansen U., Margolis D. M. 2000; The human factors YY1 and LSF repress the human immunodeficiency virus type 1 long terminal repeat via recruitment of histone deacetylase 1. J Virol 74:6790–6799 [CrossRef]
    [Google Scholar]
  6. Cripe T. P., Haugen T. H., Turk J. P., Tabatabai F., Schmid P. G., Dürst M., Gissmann L., Roman A., Turek L. P. 1987; 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 6:3745–3753
    [Google Scholar]
  7. Cripe T. P., Alderborn A., Anderson R. D., Parkkinen S., Bergman P., Haugen T. H., Pettersson U., Turek L. P. 1990; 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 2:450–463
    [Google Scholar]
  8. Cuthill S., Sibbet G. J., Campo M. S. 1993; Characterization of a nuclear factor, papilloma enhancer binding factor-1, that binds the long control region of human papillomavirus type 16 and contributes to enhancer activity. Mol Carcinog 8:96–104 [CrossRef]
    [Google Scholar]
  9. Flanagan J. R., Becker K. G., Ennist D. L., Gleason S. L., Driggers P. H., Levi B. Z., Appella E., Ozato K. 1992; Cloning of a negative transcription factor that binds to the upstream conserved region of Moloney murine leukemia virus. Mol Cell Biol 12:38–44
    [Google Scholar]
  10. Flores E. R., Lambert P. F. 1997; Evidence for a switch in the mode of human papillomavirus type 16 DNA replication during the viral life cycle. J Virol 71:7167–7179
    [Google Scholar]
  11. Galvin K. M., Shi Y. 1997; Multiple mechanisms of transcriptional repression by YY1. Mol Cell Biol 17:3723–3732
    [Google Scholar]
  12. Gloss B., Bernard H. U., Seedorf K., Klock G. 1987; The upstream regulatory region of the human papilloma virus-16 contains an E2 protein-independent enhancer which is specific for cervical carcinoma cells and regulated by glucocorticoid hormones. EMBO J 6:3735–3743
    [Google Scholar]
  13. Gordon S., Akopyan G., Garban H., Bonavida B. 2006; Transcription factor YY1: structure, function, and therapeutic implications in cancer biology. Oncogene 25:1125–1142 [CrossRef]
    [Google Scholar]
  14. Gualberto A., LePage D., Pons G., Mader S. L., Park K., Atchison M. L., Walsh K. 1992; Functional antagonism between YY1 and the serum response factor. Mol Cell Biol 12:4209–4214
    [Google Scholar]
  15. Guo B., Odgren P. R., Van Wijnen A. J., Last T. J., Nickerson J., Penman S., Lian J. B., Stein J. L., Stein G. S. 1995; The nuclear matrix protein NMP-1 is the transcription factor YY1. Proc Natl Acad Sci U S A 92:10526–10530 [CrossRef]
    [Google Scholar]
  16. Hebner C. M., Laimins L. A. 2006; Human papillomaviruses: basic mechanisms of pathogenesis and oncogenicity. Rev Med Virol 16:83–97 [CrossRef]
    [Google Scholar]
  17. Hubert W. G. 2005; Variant upstream regulatory region sequences differentially regulate human papillomavirus type 16 DNA replication throughout the viral life cycle. J Virol 79:5914–5922 [CrossRef]
    [Google Scholar]
  18. Inouye C. J., Seto E. 1994; Relief of YY1-induced transcriptional repression by protein–protein interaction with the nucleolar phosphoprotein B23. J Biol Chem 269:6506–6510
    [Google Scholar]
  19. 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. 1992; Transcriptional enhancer factor (TEF)-1 and its cell-specific co-activator activate human papillomavirus-16 E6 and E7 oncogene transcription in human keratinocytes and cervical carcinoma cells. EMBO J 11:2271–2281
    [Google Scholar]
  20. Lace M. J., Anson J. R., Thomas G. S., Turek L. P., Haugen T. H. 2008a; The E8–E2 gene product of human papillomavirus type 16 represses early transcription and replication but is dispensable for viral plasmid persistence in keratinocytes. J Virol 82:10841–10853 [CrossRef]
    [Google Scholar]
  21. Lace M. J., Anson J. R., Turek L. P., Haugen T. H. 2008b; Functional mapping of the human papillomavirus type 16 E1 cistron. J Virol 82:10724–10734 [CrossRef]
    [Google Scholar]
  22. Lace M. J., Isacson C., Anson J. R., Lörincz A. T., Wilczynski S. P., Haugen T. H., Turek L. P. 2009; Upstream regulatory region alterations found in human papillomavirus type 16 (HPV-16) isolates from cervical carcinomas increase transcription, ori function, and HPV immortalization capacity in culture. J Virol 83:7457–7466 [CrossRef]
    [Google Scholar]
  23. Lee T. C., Shi Y., Schwartz R. J. 1992; Displacement of BrdUrd-induced YY1 by serum response factor activates skeletal α -actin transcription in embryonic myoblasts. Proc Natl Acad Sci U S A 89:9814–9818 [CrossRef]
    [Google Scholar]
  24. Lee J. S., Galvin K. M., Shi Y. 1993; Evidence for physical interaction between the zinc-finger transcription factors YY1 and Sp1. Proc Natl Acad Sci U S A 90:6145–6149 [CrossRef]
    [Google Scholar]
  25. Lee J. S., Galvin K. M., See R. H., Eckner R., Livingston D., Moran E., Shi Y. 1995; Relief of YY1 transcriptional repression by adenovirus E1A is mediated by E1A-associated protein p300. Genes Dev 9:1188–1198 [CrossRef]
    [Google Scholar]
  26. Lewis B. A., Tullis G., Seto E., Horikoshi N., Weinmann R., Shenk T. 1995; Adenovirus E1A proteins interact with the cellular YY1 transcription factor. J Virol 69:1628–1636
    [Google Scholar]
  27. Licht J. D., Ro M., English M. A., Grossel M., Hansen U. 1993; Selective repression of transcriptional activators at a distance by the Drosophila Krüppel protein. Proc Natl Acad Sci U S A 90:11361–11365 [CrossRef]
    [Google Scholar]
  28. Liu R., Baillie J., Sissons J. G. P., Sinclair J. H. 1994; The transcription factor YY1 binds to negative regulatory elements in the human cytomegalovirus major immediate early enhancer/promoter and mediates repression in non-permissive cells. Nucleic Acids Res 22:2453–2459 [CrossRef]
    [Google Scholar]
  29. Margolis D. M., Somasundaran M., Green M. R. 1994; Human transcription factor YY1 represses human immunodeficiency virus type 1 transcription and virion production. J Virol 68:905–910
    [Google Scholar]
  30. Martinez E., Chiang C. M., Ge H., Roeder R. G. 1994; TATA-binding protein-associated factor(s) in TFIID function through the initiator to direct basal transcription from a TATA-less class II promoter. EMBO J 13:3115–3126
    [Google Scholar]
  31. May M., Dong X. P., Beyer-Finkler E., Stubenrauch F., Fuchs P. G., Pfister H. 1994; The E6/E7 promoter of extrachromosomal HPV16 DNA in cervical cancers escapes from cellular repression by mutation of target sequences for YY1. EMBO J 13:1460–1466
    [Google Scholar]
  32. Meier V. S., Groner B. 1994; The nuclear factor YY1 participates in repression of the β -casein gene promoter in mammary epithelial cells and is counteracted by mammary gland factor during lactogenic hormone induction. Mol Cell Biol 14:128–137
    [Google Scholar]
  33. Mills L. K., Shi Y., Millette R. L. 1994; YY1 is the cellular factor shown previously to bind to regulatory regions of several leaky-late ( βγ , γ 1) genes of herpes simplex virus type 1. J Virol 68:1234–1238
    [Google Scholar]
  34. Montalvo E. A., Cottam M., Hill S., Wang Y. C. J. 1995; YY1 binds to and regulates cis -acting negative elements in the Epstein–Barr virus BZLF1 promoter. J Virol 69:4158–4165
    [Google Scholar]
  35. Moss B. 1991; Vaccinia virus: a tool for research and vaccine development. Science 252:1662–1667 [CrossRef]
    [Google Scholar]
  36. O'Connor M. J., Tan S. H., Tan C. H., Bernard H. U. 1996; YY1 represses human papillomavirus type 16 transcription by quenching AP-1 activity. J Virol 70:6529–6539
    [Google Scholar]
  37. Pajunk H. S., May C., Pfister H., Fuchs P. G. 1997; Regulatory interactions of transcription factor YY1 with control sequences of the E6 promoter of human papillomavirus type 8. J Gen Virol 78:3287–3295
    [Google Scholar]
  38. Palko L., Bass H. W., Beyrouthy M. J., Hurt M. M. 2004; The Yin Yang-1 (YY1) protein undergoes a DNA-replication-associated switch in localization from the cytoplasm to the nucleus at the onset of S phase. J Cell Sci 117:465–476
    [Google Scholar]
  39. Park K., Atchison M. L. 1991; Isolation of a candidate repressor/activator, NF-E1 (YY- 1, δ ), that binds to the immunoglobulin κ 3′ enhancer and the immunoglobulin heavy-chain μE1 site. Proc Natl Acad Sci U S A 88:9804–9808 [CrossRef]
    [Google Scholar]
  40. Psyrri A., DiMaio D. 2008; Human papillomavirus in cervical and head-and-neck cancer. Nat Clin Pract Oncol 5:24–31 [CrossRef]
    [Google Scholar]
  41. Ralph W. M. Jr, Liu K., Auborn K. J. 2006; CCAAT/enhancer-binding protein β represses human papillomavirus 11 upstream regulatory region expression through a promoter-proximal YY1-binding site. J Gen Virol 87:51–59 [CrossRef]
    [Google Scholar]
  42. Rezai-Zadeh N., Zhang X., Namour F., Fejer G., Wen Y. D., Yao Y. L., Gyory I., Wright K., Seto E. 2003; Targeted recruitment of a histone H4-specific methyltransferase by the transcription factor YY1. Genes Dev 17:1019–1029 [CrossRef]
    [Google Scholar]
  43. Riggs K. J., Saleque S., Wong K. K., Merrell K. T., Lee J. S., Shi Y., Calame K. 1993; Yin-yang 1 activates the c- myc promoter. Mol Cell Biol 13:7487–7495
    [Google Scholar]
  44. Roberts S. G. E., Green M. R. 1995; Transcription: dichotomous regulators. Nature 375:105–106 [CrossRef]
    [Google Scholar]
  45. Satyamoorthy K., Park K., Atchison M. L., Howe C. C. 1993; The intracisternal A-particle upstream element interacts with transcription factor YY1 to activate transcription: pleiotropic effects of YY1 on distinct DNA promoter elements. Mol Cell Biol 13:6621–6628
    [Google Scholar]
  46. Sauer F., Jäckle H. 1993; Dimerization and the control of transcription by Krüppel. Nature 364:454–457 [CrossRef]
    [Google Scholar]
  47. Schmidt M., Kedzia W., Gozdzicka-Jozefiak A. 2001; Intratype HPV16 sequence variation within LCR of isolates from asymptomatic carriers and cervical cancers. J Clin Virol 23:65–77 [CrossRef]
    [Google Scholar]
  48. Seto E., Shi Y., Shenk T. 1991; YY1 is an initiator sequence-binding protein that directs and activates transcription in vitro . Nature 354:241–245 [CrossRef]
    [Google Scholar]
  49. Seto E., Lewis B., Shenk T. 1993; Interaction between transcription factors Sp1 and YY1. Nature 365:462–464 [CrossRef]
    [Google Scholar]
  50. Shi Y., Seto E., Chang L. S., Shenk T. 1991; Transcriptional repression by YY1, a human GLI-Krüppel-related protein, and relief of repression by adenovirus E1A protein. Cell 67:377–388 [CrossRef]
    [Google Scholar]
  51. Shi Y., Lee J. S., Galvin K. M. 1997; Everything you have ever wanted to know about Yin Yang 1. Biochim Biophys Acta 1332F49–F66
    [Google Scholar]
  52. Shrivastava A., Saleque S., Kalpana G. V., Artandi S., Goff S. P., Calame K. 1993; Inhibition of transcriptional regulator Yin-Yang-1 by association with c-Myc. Science 262:1889–1892 [CrossRef]
    [Google Scholar]
  53. Soeda E., Ferran M. C., Baker C. C., McBride A. A. 2006; Repression of HPV16 early region transcription by the E2 protein. Virology 351:29–41 [CrossRef]
    [Google Scholar]
  54. Tan S. H., Baker C. C., Stunkel W., Bernard H. U. 2003; A transcriptional initiator overlaps with a conserved YY1 binding site in the long control region of human papillomavirus type 16. Virology 305:486–501 [CrossRef]
    [Google Scholar]
  55. TenHarmsel A., Austin R. J., Savenelli N., Biggin M. D. 1993; Cooperative binding at a distance by even-skipped protein correlates with repression and suggests a mechanism of silencing. Mol Cell Biol 13:2742–2752
    [Google Scholar]
  56. Thierry F. 2009; Transcriptional regulation of the papillomavirus oncogenes by cellular and viral transcription factors in cervical carcinoma. Virology 384:375–379 [CrossRef]
    [Google Scholar]
  57. Ushikai M., Lace M. J., Yamakawa Y., Kono M., Anson J., Ishiji T., Parkkinen S., Wicker N., Valentine M. E. other authors 1994; trans activation by the full-length E2 proteins of human papillomavirus type 16 and bovine papillomavirus type 1 in vitro and in vivo: cooperation with activation domains of cellular transcription factors. J Virol 68:6655–6666
    [Google Scholar]
  58. Weill L., Shestakova E., Bonnefoy E. 2003; Transcription factor YY1 binds to the murine beta interferon promoter and regulates its transcriptional capacity with a dual activator/repressor role. J Virol 77:2903–2914 [CrossRef]
    [Google Scholar]
  59. Xiao J. H., Davidson I., Matthes H., Garnier J. M., Chambon P. 1991; Cloning, expression, and transcriptional properties of the human enhancer factor TEF-1. Cell 65:551–568 [CrossRef]
    [Google Scholar]
  60. Yao Y. L., Yang W. M., Seto E. 2001; Regulation of transcription factor YY1 by acetylation and deacetylation. Mol Cell Biol 21:5979–5991 [CrossRef]
    [Google Scholar]
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