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. 1997 Oct;71(10):8041–8047. doi: 10.1128/jvi.71.10.8041-8047.1997

Conserved interaction of the papillomavirus E2 transcriptional activator proteins with human and yeast TFIIB proteins.

J D Benson 1, R Lawande 1, P M Howley 1
PMCID: PMC192169  PMID: 9311902

Abstract

Papillomavirus early gene expression is regulated by the virus gene-encoded E2 proteins. The best-characterized E2 protein, encoded by bovine papillomavirus type 1 (BPV-1), has been shown to interact with basal transcription factor IIB (TFIIB) and the TATA binding protein basal transcription factor (N. M. Rank and P. F. Lambert, J. Virol. 69:6323-6334, 1995). We demonstrate that the potent E2 transcriptional activator protein encoded by a gene of human PV type 16 also interacts with TFIIB in vitro. Moreover, a direct comparison of domains within human TFIIB (hTFIIB) required for VP16 and BPV-1 E2 indicates that these acidic activators interact with hTFIIB in a qualitatively similar manner. Our mapping experiments identify hTFIIB interaction domains within the amino-terminal activation domain of BPV-1 E2. Finally, we demonstrate in vitro interaction between Saccharomyces cerevisiae TFIIB and BPV-1 E2, an observation that is consistent with the importance of the E2-TFIIB interaction for BPV-1 E2 transactivation in both systems.

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Selected References

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  1. Abroi A., Kurg R., Ustav M. Transcriptional and replicational activation functions in the bovine papillomavirus type 1 E2 protein are encoded by different structural determinants. J Virol. 1996 Sep;70(9):6169–6179. doi: 10.1128/jvi.70.9.6169-6179.1996. [DOI] [PMC free article] [PubMed] [Google Scholar]
  2. 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]
  3. Baniahmad A., Ha I., Reinberg D., Tsai S., Tsai M. J., O'Malley B. W. Interaction of human thyroid hormone receptor beta with transcription factor TFIIB may mediate target gene derepression and activation by thyroid hormone. Proc Natl Acad Sci U S A. 1993 Oct 1;90(19):8832–8836. doi: 10.1073/pnas.90.19.8832. [DOI] [PMC free article] [PubMed] [Google Scholar]
  4. Benson J. D., Howley P. M. Amino-terminal domains of the bovine papillomavirus type 1 E1 and E2 proteins participate in complex formation. J Virol. 1995 Jul;69(7):4364–4372. doi: 10.1128/jvi.69.7.4364-4372.1995. [DOI] [PMC free article] [PubMed] [Google Scholar]
  5. Blair W. S., Bogerd H., Cullen B. R. Genetic analysis indicates that the human foamy virus Bel-1 protein contains a transcription activation domain of the acidic class. J Virol. 1994 Jun;68(6):3803–3808. doi: 10.1128/jvi.68.6.3803-3808.1994. [DOI] [PMC free article] [PubMed] [Google Scholar]
  6. Breiding D. E., Grossel M. J., Androphy E. J. Genetic analysis of the bovine papillomavirus E2 transcriptional activation domain. Virology. 1996 Jul 1;221(1):34–43. doi: 10.1006/viro.1996.0350. [DOI] [PubMed] [Google Scholar]
  7. Brokaw J. L., Blanco M., McBride A. A. Amino acids critical for the functions of the bovine papillomavirus type 1 E2 transactivator. J Virol. 1996 Jan;70(1):23–29. doi: 10.1128/jvi.70.1.23-29.1996. [DOI] [PMC free article] [PubMed] [Google Scholar]
  8. Buratowski S., Zhou H. Functional domains of transcription factor TFIIB. Proc Natl Acad Sci U S A. 1993 Jun 15;90(12):5633–5637. doi: 10.1073/pnas.90.12.5633. [DOI] [PMC free article] [PubMed] [Google Scholar]
  9. Choy B., Green M. R. Eukaryotic activators function during multiple steps of preinitiation complex assembly. Nature. 1993 Dec 9;366(6455):531–536. doi: 10.1038/366531a0. [DOI] [PubMed] [Google Scholar]
  10. Colgan J., Wampler S., Manley J. L. Interaction between a transcriptional activator and transcription factor IIB in vivo. Nature. 1993 Apr 8;362(6420):549–553. doi: 10.1038/362549a0. [DOI] [PubMed] [Google Scholar]
  11. Countryman J. K., Heston L., Gradoville L., Himmelfarb H., Serdy S., Miller G. Activation of the Epstein-Barr virus BMRF1 and BZLF1 promoters by ZEBRA in Saccharomyces cerevisiae. J Virol. 1994 Nov;68(11):7628–7633. doi: 10.1128/jvi.68.11.7628-7633.1994. [DOI] [PMC free article] [PubMed] [Google Scholar]
  12. Demeret C., Yaniv M., Thierry F. The E2 transcriptional repressor can compensate for Sp1 activation of the human papillomavirus type 18 early promoter. J Virol. 1994 Nov;68(11):7075–7082. doi: 10.1128/jvi.68.11.7075-7082.1994. [DOI] [PMC free article] [PubMed] [Google Scholar]
  13. Ferguson M. K., Botchan M. R. Genetic analysis of the activation domain of bovine papillomavirus protein E2: its role in transcription and replication. J Virol. 1996 Jul;70(7):4193–4199. doi: 10.1128/jvi.70.7.4193-4199.1996. [DOI] [PMC free article] [PubMed] [Google Scholar]
  14. Giri I., Yaniv M. Structural and mutational analysis of E2 trans-activating proteins of papillomaviruses reveals three distinct functional domains. EMBO J. 1988 Sep;7(9):2823–2829. doi: 10.1002/j.1460-2075.1988.tb03138.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  15. Goodrich J. A., Hoey T., Thut C. J., Admon A., Tjian R. Drosophila TAFII40 interacts with both a VP16 activation domain and the basal transcription factor TFIIB. Cell. 1993 Nov 5;75(3):519–530. doi: 10.1016/0092-8674(93)90386-5. [DOI] [PubMed] [Google Scholar]
  16. Ha I., Lane W. S., Reinberg D. Cloning of a human gene encoding the general transcription initiation factor IIB. Nature. 1991 Aug 22;352(6337):689–695. doi: 10.1038/352689a0. [DOI] [PubMed] [Google Scholar]
  17. Ha I., Roberts S., Maldonado E., Sun X., Kim L. U., Green M., Reinberg D. Multiple functional domains of human transcription factor IIB: distinct interactions with two general transcription factors and RNA polymerase II. Genes Dev. 1993 Jun;7(6):1021–1032. doi: 10.1101/gad.7.6.1021. [DOI] [PubMed] [Google Scholar]
  18. Ham J., Dostatni N., Arnos F., Yaniv M. Several different upstream promoter elements can potentiate transactivation by the BPV-1 E2 protein. EMBO J. 1991 Oct;10(10):2931–2940. doi: 10.1002/j.1460-2075.1991.tb07843.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  19. Hawley-Nelson P., Androphy E. J., Lowy D. R., Schiller J. T. The specific DNA recognition sequence of the bovine papillomavirus E2 protein is an E2-dependent enhancer. EMBO J. 1988 Feb;7(2):525–531. doi: 10.1002/j.1460-2075.1988.tb02841.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  20. 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]
  21. Hisatake K., Roeder R. G., Horikoshi M. Functional dissection of TFIIB domains required for TFIIB-TFIID-promoter complex formation and basal transcription activity. Nature. 1993 Jun 24;363(6431):744–747. doi: 10.1038/363744a0. [DOI] [PubMed] [Google Scholar]
  22. Hori R., Pyo S., Carey M. Protease footprinting reveals a surface on transcription factor TFIIB that serves as an interface for activators and coactivators. Proc Natl Acad Sci U S A. 1995 Jun 20;92(13):6047–6051. doi: 10.1073/pnas.92.13.6047. [DOI] [PMC free article] [PubMed] [Google Scholar]
  23. Ing N. H., Beekman J. M., Tsai S. Y., Tsai M. J., O'Malley B. W. Members of the steroid hormone receptor superfamily interact with TFIIB (S300-II). J Biol Chem. 1992 Sep 5;267(25):17617–17623. [PubMed] [Google Scholar]
  24. Kaelin W. G., Jr, Krek W., Sellers W. R., DeCaprio J. A., Ajchenbaum F., Fuchs C. S., Chittenden T., Li Y., Farnham P. J., Blanar M. A. Expression cloning of a cDNA encoding a retinoblastoma-binding protein with E2F-like properties. Cell. 1992 Jul 24;70(2):351–364. doi: 10.1016/0092-8674(92)90108-o. [DOI] [PubMed] [Google Scholar]
  25. Klemm R. D., Goodrich J. A., Zhou S., Tjian R. Molecular cloning and expression of the 32-kDa subunit of human TFIID reveals interactions with VP16 and TFIIB that mediate transcriptional activation. Proc Natl Acad Sci U S A. 1995 Jun 20;92(13):5788–5792. doi: 10.1073/pnas.92.13.5788. [DOI] [PMC free article] [PubMed] [Google Scholar]
  26. Kovelman R., Bilter G. K., Glezer E., Tsou A. Y., Barbosa M. S. Enhanced transcriptional activation by E2 proteins from the oncogenic human papillomaviruses. J Virol. 1996 Nov;70(11):7549–7560. doi: 10.1128/jvi.70.11.7549-7560.1996. [DOI] [PMC free article] [PubMed] [Google Scholar]
  27. Künzler M., Braus G. H., Georgiev O., Seipel K., Schaffner W. Functional differences between mammalian transcription activation domains at the yeast GAL1 promoter. EMBO J. 1994 Feb 1;13(3):641–645. doi: 10.1002/j.1460-2075.1994.tb06302.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  28. Lambert P. F., Dostatni N., McBride A. A., Yaniv M., Howley P. M., Arcangioli B. Functional analysis of the papilloma virus E2 trans-activator in Saccharomyces cerevisiae. Genes Dev. 1989 Jan;3(1):38–48. doi: 10.1101/gad.3.1.38. [DOI] [PubMed] [Google Scholar]
  29. 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]
  30. Li R., Knight J., Bream G., Stenlund A., Botchan M. Specific recognition nucleotides and their DNA context determine the affinity of E2 protein for 17 binding sites in the BPV-1 genome. Genes Dev. 1989 Apr;3(4):510–526. doi: 10.1101/gad.3.4.510. [DOI] [PubMed] [Google Scholar]
  31. Lin Y. S., Ha I., Maldonado E., Reinberg D., Green M. R. Binding of general transcription factor TFIIB to an acidic activating region. Nature. 1991 Oct 10;353(6344):569–571. doi: 10.1038/353569a0. [DOI] [PubMed] [Google Scholar]
  32. Lu H., Levine A. J. Human TAFII31 protein is a transcriptional coactivator of the p53 protein. Proc Natl Acad Sci U S A. 1995 May 23;92(11):5154–5158. doi: 10.1073/pnas.92.11.5154. [DOI] [PMC free article] [PubMed] [Google Scholar]
  33. Manet E., Allera C., Gruffat H., Mikaelian I., Rigolet A., Sergeant A. The acidic activation domain of the Epstein-Barr virus transcription factor R interacts in vitro with both TBP and TFIIB and is cell-specifically potentiated by a proline-rich region. Gene Expr. 1993;3(1):49–59. [PMC free article] [PubMed] [Google Scholar]
  34. 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]
  35. McBride A. A., Romanczuk H., Howley P. M. The papillomavirus E2 regulatory proteins. J Biol Chem. 1991 Oct 5;266(28):18411–18414. [PubMed] [Google Scholar]
  36. McBride A. A., Schlegel R., Howley P. M. The carboxy-terminal domain shared by the bovine papillomavirus E2 transactivator and repressor proteins contains a specific DNA binding activity. EMBO J. 1988 Feb;7(2):533–539. doi: 10.1002/j.1460-2075.1988.tb02842.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  37. Mohr I. J., Clark R., Sun S., Androphy E. J., MacPherson P., Botchan M. R. Targeting the E1 replication protein to the papillomavirus origin of replication by complex formation with the E2 transactivator. Science. 1990 Dec 21;250(4988):1694–1699. doi: 10.1126/science.2176744. [DOI] [PubMed] [Google Scholar]
  38. Moore P. A., Ruben S. M., Rosen C. A. Conservation of transcriptional activation functions of the NF-kappa B p50 and p65 subunits in mammalian cells and Saccharomyces cerevisiae. Mol Cell Biol. 1993 Mar;13(3):1666–1674. doi: 10.1128/mcb.13.3.1666. [DOI] [PMC free article] [PubMed] [Google Scholar]
  39. Morrissey L. C., Barsoum J., Androphy E. J. Trans activation by the bovine papillomavirus E2 protein in Saccharomyces cerevisiae. J Virol. 1989 Oct;63(10):4422–4425. doi: 10.1128/jvi.63.10.4422-4425.1989. [DOI] [PMC free article] [PubMed] [Google Scholar]
  40. Moskaluk C., Bastia D. The E2 "gene" of bovine papillomavirus encodes an enhancer-binding protein. Proc Natl Acad Sci U S A. 1987 Mar;84(5):1215–1218. doi: 10.1073/pnas.84.5.1215. [DOI] [PMC free article] [PubMed] [Google Scholar]
  41. Pinto I., Ware D. E., Hampsey M. The yeast SUA7 gene encodes a homolog of human transcription factor TFIIB and is required for normal start site selection in vivo. Cell. 1992 Mar 6;68(5):977–988. doi: 10.1016/0092-8674(92)90040-j. [DOI] [PubMed] [Google Scholar]
  42. Ponticelli A. S., Pardee T. S., Struhl K. The glutamine-rich activation domains of human Sp1 do not stimulate transcription in Saccharomyces cerevisiae. Mol Cell Biol. 1995 Feb;15(2):983–988. doi: 10.1128/mcb.15.2.983. [DOI] [PMC free article] [PubMed] [Google Scholar]
  43. Privalsky M. L., Sharif M., Yamamoto K. R. The viral erbA oncogene protein, a constitutive repressor in animal cells, is a hormone-regulated activator in yeast. Cell. 1990 Dec 21;63(6):1277–1286. doi: 10.1016/0092-8674(90)90423-c. [DOI] [PubMed] [Google Scholar]
  44. Ptashne M., Gann A. Transcriptional activation by recruitment. Nature. 1997 Apr 10;386(6625):569–577. doi: 10.1038/386569a0. [DOI] [PubMed] [Google Scholar]
  45. Rank N. M., Lambert P. F. Bovine papillomavirus type 1 E2 transcriptional regulators directly bind two cellular transcription factors, TFIID and TFIIB. J Virol. 1995 Oct;69(10):6323–6334. doi: 10.1128/jvi.69.10.6323-6334.1995. [DOI] [PMC free article] [PubMed] [Google Scholar]
  46. Regier J. L., Shen F., Triezenberg S. J. Pattern of aromatic and hydrophobic amino acids critical for one of two subdomains of the VP16 transcriptional activator. Proc Natl Acad Sci U S A. 1993 Feb 1;90(3):883–887. doi: 10.1073/pnas.90.3.883. [DOI] [PMC free article] [PubMed] [Google Scholar]
  47. Roberts S. G., Ha I., Maldonado E., Reinberg D., Green M. R. Interaction between an acidic activator and transcription factor TFIIB is required for transcriptional activation. Nature. 1993 Jun 24;363(6431):741–744. doi: 10.1038/363741a0. [DOI] [PubMed] [Google Scholar]
  48. Sakai H., Yasugi T., Benson J. D., Dowhanick J. J., Howley P. M. Targeted mutagenesis of the human papillomavirus type 16 E2 transactivation domain reveals separable transcriptional activation and DNA replication functions. J Virol. 1996 Mar;70(3):1602–1611. doi: 10.1128/jvi.70.3.1602-1611.1996. [DOI] [PMC free article] [PubMed] [Google Scholar]
  49. Schärer E., Iggo R. Mammalian p53 can function as a transcription factor in yeast. Nucleic Acids Res. 1992 Apr 11;20(7):1539–1545. doi: 10.1093/nar/20.7.1539. [DOI] [PMC free article] [PubMed] [Google Scholar]
  50. Sharp P. A. Gene transcription. TFIIB or not TFIIB? Nature. 1991 May 2;351(6321):16–18. doi: 10.1038/351016d0. [DOI] [PubMed] [Google Scholar]
  51. Smith C. A., Bates P., Rivera-Gonzalez R., Gu B., DeLuca N. A. ICP4, the major transcriptional regulatory protein of herpes simplex virus type 1, forms a tripartite complex with TATA-binding protein and TFIIB. J Virol. 1993 Aug;67(8):4676–4687. doi: 10.1128/jvi.67.8.4676-4687.1993. [DOI] [PMC free article] [PubMed] [Google Scholar]
  52. Spalholz B. A., Lambert P. F., Yee C. L., Howley P. M. Bovine papillomavirus transcriptional regulation: localization of the E2-responsive elements of the long control region. J Virol. 1987 Jul;61(7):2128–2137. doi: 10.1128/jvi.61.7.2128-2137.1987. [DOI] [PMC free article] [PubMed] [Google Scholar]
  53. Stanway C. A., Sowden M. P., Wilson L. E., Kingsman A. J., Kingsman S. M. Efficient activation of transcription in yeast by the BPV1 E2 protein. Nucleic Acids Res. 1989 Mar 25;17(6):2187–2196. doi: 10.1093/nar/17.6.2187. [DOI] [PMC free article] [PubMed] [Google Scholar]
  54. Stargell L. A., Struhl K. Mechanisms of transcriptional activation in vivo: two steps forward. Trends Genet. 1996 Aug;12(8):311–315. doi: 10.1016/0168-9525(96)10028-7. [DOI] [PubMed] [Google Scholar]
  55. Steger G., Ham J., Lefebvre O., Yaniv M. The bovine papillomavirus 1 E2 protein contains two activation domains: one that interacts with TBP and another that functions after TBP binding. EMBO J. 1995 Jan 16;14(2):329–340. doi: 10.1002/j.1460-2075.1995.tb07007.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  56. 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]
  57. Thut C. J., Chen J. L., Klemm R., Tjian R. p53 transcriptional activation mediated by coactivators TAFII40 and TAFII60. Science. 1995 Jan 6;267(5194):100–104. doi: 10.1126/science.7809597. [DOI] [PubMed] [Google Scholar]
  58. Xu X., Prorock C., Ishikawa H., Maldonado E., Ito Y., Gélinas C. Functional interaction of the v-Rel and c-Rel oncoproteins with the TATA-binding protein and association with transcription factor IIB. Mol Cell Biol. 1993 Nov;13(11):6733–6741. doi: 10.1128/mcb.13.11.6733. [DOI] [PMC free article] [PubMed] [Google Scholar]

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