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. 1995 Jan;15(1):534–539. doi: 10.1128/mcb.15.1.534

The yeast TATA-binding protein (TBP) core domain assembles with human TBP-associated factors into a functional TFIID complex.

Q Zhou 1, A J Berk 1
PMCID: PMC232007  PMID: 7799963

Abstract

In mammalian and Drosophila cells, the central RNA polymerase II general transcription factor TFIID is a multisubunit complex containing the TATA-binding protein (TBP) and TBP-associated factors (TAFs) bound to the conserved TBP carboxy-terminal core domain. TBP also associates with alternative TAFs in these cells to form general transcription factors required for initiation by RNA polymerases I and III. Although extracts of human HeLa cells contain little TBP that is not associated with TAFs, free TBP is readily isolated from yeast cell extracts. However, recent studies indicate that yeast TBP can also interact with other yeast polypeptides to form multiprotein complexes. We established stable human HeLa cell lines expressing yeast TBP and several yeast-human TBP hybrids to study TBP-TAF interactions. We found that the yeast TBP core domain assembles with a complete set of human TAFs into a stable TFIID complex that can support activated transcription in vitro. The fact that the yeast TBP core, which differs from human TBP core in approximately 20% of its amino acid residues, has the structural features required to form a stable complex with human TAFs implies that Saccharomyces cerevisiae probably contains TAFs that are structurally and functionally analogous to human TAFs. Surprisingly, the non-conserved amino terminus of yeast TBP inhibited association between the yeast core domain and human TAFs.

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Selected References

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  1. Berger S. L., Cress W. D., Cress A., Triezenberg S. J., Guarente L. Selective inhibition of activated but not basal transcription by the acidic activation domain of VP16: evidence for transcriptional adaptors. Cell. 1990 Jun 29;61(7):1199–1208. doi: 10.1016/0092-8674(90)90684-7. [DOI] [PubMed] [Google Scholar]
  2. Boyer T. G., Berk A. J. Functional interaction of adenovirus E1A with holo-TFIID. Genes Dev. 1993 Sep;7(9):1810–1823. doi: 10.1101/gad.7.9.1810. [DOI] [PubMed] [Google Scholar]
  3. Buratowski S., Hahn S., Sharp P. A., Guarente L. Function of a yeast TATA element-binding protein in a mammalian transcription system. Nature. 1988 Jul 7;334(6177):37–42. doi: 10.1038/334037a0. [DOI] [PubMed] [Google Scholar]
  4. Chasman D. I., Flaherty K. M., Sharp P. A., Kornberg R. D. Crystal structure of yeast TATA-binding protein and model for interaction with DNA. Proc Natl Acad Sci U S A. 1993 Sep 1;90(17):8174–8178. doi: 10.1073/pnas.90.17.8174. [DOI] [PMC free article] [PubMed] [Google Scholar]
  5. Cormack B. P., Strubin M., Ponticelli A. S., Struhl K. Functional differences between yeast and human TFIID are localized to the highly conserved region. Cell. 1991 Apr 19;65(2):341–348. doi: 10.1016/0092-8674(91)90167-w. [DOI] [PubMed] [Google Scholar]
  6. 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]
  7. Dynlacht B. D., Hoey T., Tjian R. Isolation of coactivators associated with the TATA-binding protein that mediate transcriptional activation. Cell. 1991 Aug 9;66(3):563–576. doi: 10.1016/0092-8674(81)90019-2. [DOI] [PubMed] [Google Scholar]
  8. Field J., Nikawa J., Broek D., MacDonald B., Rodgers L., Wilson I. A., Lerner R. A., Wigler M. Purification of a RAS-responsive adenylyl cyclase complex from Saccharomyces cerevisiae by use of an epitope addition method. Mol Cell Biol. 1988 May;8(5):2159–2165. doi: 10.1128/mcb.8.5.2159. [DOI] [PMC free article] [PubMed] [Google Scholar]
  9. Gill G., Tjian R. A highly conserved domain of TFIID displays species specificity in vivo. Cell. 1991 Apr 19;65(2):333–340. doi: 10.1016/0092-8674(91)90166-v. [DOI] [PubMed] [Google Scholar]
  10. Giniger E., Ptashne M. Transcription in yeast activated by a putative amphipathic alpha helix linked to a DNA binding unit. Nature. 1987 Dec 17;330(6149):670–672. doi: 10.1038/330670a0. [DOI] [PubMed] [Google Scholar]
  11. Hernandez N. TBP, a universal eukaryotic transcription factor? Genes Dev. 1993 Jul;7(7B):1291–1308. doi: 10.1101/gad.7.7b.1291. [DOI] [PubMed] [Google Scholar]
  12. Horikoshi M., Wang C. K., Fujii H., Cromlish J. A., Weil P. A., Roeder R. G. Purification of a yeast TATA box-binding protein that exhibits human transcription factor IID activity. Proc Natl Acad Sci U S A. 1989 Jul;86(13):4843–4847. doi: 10.1073/pnas.86.13.4843. [DOI] [PMC free article] [PubMed] [Google Scholar]
  13. Horikoshi M., Yamamoto T., Ohkuma Y., Weil P. A., Roeder R. G. Analysis of structure-function relationships of yeast TATA box binding factor TFIID. Cell. 1990 Jun 29;61(7):1171–1178. doi: 10.1016/0092-8674(90)90681-4. [DOI] [PubMed] [Google Scholar]
  14. Keaveney M., Berkenstam A., Feigenbutz M., Vriend G., Stunnenberg H. G. Residues in the TATA-binding protein required to mediate a transcriptional response to retinoic acid in EC cells. Nature. 1993 Oct 7;365(6446):562–566. doi: 10.1038/365562a0. [DOI] [PubMed] [Google Scholar]
  15. Kelleher R. J., 3rd, Flanagan P. M., Kornberg R. D. A novel mediator between activator proteins and the RNA polymerase II transcription apparatus. Cell. 1990 Jun 29;61(7):1209–1215. doi: 10.1016/0092-8674(90)90685-8. [DOI] [PubMed] [Google Scholar]
  16. Kim J. L., Nikolov D. B., Burley S. K. Co-crystal structure of TBP recognizing the minor groove of a TATA element. Nature. 1993 Oct 7;365(6446):520–527. doi: 10.1038/365520a0. [DOI] [PubMed] [Google Scholar]
  17. Kim Y., Geiger J. H., Hahn S., Sigler P. B. Crystal structure of a yeast TBP/TATA-box complex. Nature. 1993 Oct 7;365(6446):512–520. doi: 10.1038/365512a0. [DOI] [PubMed] [Google Scholar]
  18. Lieberman P. M., Schmidt M. C., Kao C. C., Berk A. J. Two distinct domains in the yeast transcription factor IID and evidence for a TATA box-induced conformational change. Mol Cell Biol. 1991 Jan;11(1):63–74. doi: 10.1128/mcb.11.1.63. [DOI] [PMC free article] [PubMed] [Google Scholar]
  19. Lillie J. W., Green M. R. Transcription activation by the adenovirus E1a protein. Nature. 1989 Mar 2;338(6210):39–44. doi: 10.1038/338039a0. [DOI] [PubMed] [Google Scholar]
  20. Muller A. J., Young J. C., Pendergast A. M., Pondel M., Landau N. R., Littman D. R., Witte O. N. BCR first exon sequences specifically activate the BCR/ABL tyrosine kinase oncogene of Philadelphia chromosome-positive human leukemias. Mol Cell Biol. 1991 Apr;11(4):1785–1792. doi: 10.1128/mcb.11.4.1785. [DOI] [PMC free article] [PubMed] [Google Scholar]
  21. Nikolov D. B., Hu S. H., Lin J., Gasch A., Hoffmann A., Horikoshi M., Chua N. H., Roeder R. G., Burley S. K. Crystal structure of TFIID TATA-box binding protein. Nature. 1992 Nov 5;360(6399):40–46. doi: 10.1038/360040a0. [DOI] [PubMed] [Google Scholar]
  22. Peterson M. G., Tanese N., Pugh B. F., Tjian R. Functional domains and upstream activation properties of cloned human TATA binding protein. Science. 1990 Jun 29;248(4963):1625–1630. doi: 10.1126/science.2363050. [DOI] [PubMed] [Google Scholar]
  23. Poon D., Schroeder S., Wang C. K., Yamamoto T., Horikoshi M., Roeder R. G., Weil P. A. The conserved carboxy-terminal domain of Saccharomyces cerevisiae TFIID is sufficient to support normal cell growth. Mol Cell Biol. 1991 Oct;11(10):4809–4821. doi: 10.1128/mcb.11.10.4809. [DOI] [PMC free article] [PubMed] [Google Scholar]
  24. Poon D., Weil P. A. Immunopurification of yeast TATA-binding protein and associated factors. Presence of transcription factor IIIB transcriptional activity. J Biol Chem. 1993 Jul 25;268(21):15325–15328. [PubMed] [Google Scholar]
  25. Reddy P., Hahn S. Dominant negative mutations in yeast TFIID define a bipartite DNA-binding region. Cell. 1991 Apr 19;65(2):349–357. doi: 10.1016/0092-8674(91)90168-x. [DOI] [PubMed] [Google Scholar]
  26. Schmidt M. C., Kao C. C., Pei R., Berk A. J. Yeast TATA-box transcription factor gene. Proc Natl Acad Sci U S A. 1989 Oct;86(20):7785–7789. doi: 10.1073/pnas.86.20.7785. [DOI] [PMC free article] [PubMed] [Google Scholar]
  27. Strubin M., Struhl K. Yeast and human TFIID with altered DNA-binding specificity for TATA elements. Cell. 1992 Feb 21;68(4):721–730. doi: 10.1016/0092-8674(92)90147-5. [DOI] [PubMed] [Google Scholar]
  28. Takada R., Nakatani Y., Hoffmann A., Kokubo T., Hasegawa S., Roeder R. G., Horikoshi M. Identification of human TFIID components and direct interaction between a 250-kDa polypeptide and the TATA box-binding protein (TFIID tau). Proc Natl Acad Sci U S A. 1992 Dec 15;89(24):11809–11813. doi: 10.1073/pnas.89.24.11809. [DOI] [PMC free article] [PubMed] [Google Scholar]
  29. Tanese N., Pugh B. F., Tjian R. Coactivators for a proline-rich activator purified from the multisubunit human TFIID complex. Genes Dev. 1991 Dec;5(12A):2212–2224. doi: 10.1101/gad.5.12a.2212. [DOI] [PubMed] [Google Scholar]
  30. Timmers H. T., Meyers R. E., Sharp P. A. Composition of transcription factor B-TFIID. Proc Natl Acad Sci U S A. 1992 Sep 1;89(17):8140–8144. doi: 10.1073/pnas.89.17.8140. [DOI] [PMC free article] [PubMed] [Google Scholar]
  31. Verrijzer C. P., Yokomori K., Chen J. L., Tjian R. Drosophila TAFII150: similarity to yeast gene TSM-1 and specific binding to core promoter DNA. Science. 1994 May 13;264(5161):933–941. doi: 10.1126/science.8178153. [DOI] [PubMed] [Google Scholar]
  32. Weinzierl R. O., Dynlacht B. D., Tjian R. Largest subunit of Drosophila transcription factor IID directs assembly of a complex containing TBP and a coactivator. Nature. 1993 Apr 8;362(6420):511–517. doi: 10.1038/362511a0. [DOI] [PubMed] [Google Scholar]
  33. Yokomori K., Chen J. L., Admon A., Zhou S., Tjian R. Molecular cloning and characterization of dTAFII30 alpha and dTAFII30 beta: two small subunits of Drosophila TFIID. Genes Dev. 1993 Dec;7(12B):2587–2597. doi: 10.1101/gad.7.12b.2587. [DOI] [PubMed] [Google Scholar]
  34. Zhou Q. A., Schmidt M. C., Berk A. J. Requirement for acidic amino acid residues immediately N-terminal to the conserved domain of Saccharomyces cerevisiae TFIID. EMBO J. 1991 Jul;10(7):1843–1852. doi: 10.1002/j.1460-2075.1991.tb07710.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  35. Zhou Q., Boyer T. G., Berk A. J. Factors (TAFs) required for activated transcription interact with TATA box-binding protein conserved core domain. Genes Dev. 1993 Feb;7(2):180–187. doi: 10.1101/gad.7.2.180. [DOI] [PubMed] [Google Scholar]
  36. Zhou Q., Lieberman P. M., Boyer T. G., Berk A. J. Holo-TFIID supports transcriptional stimulation by diverse activators and from a TATA-less promoter. Genes Dev. 1992 Oct;6(10):1964–1974. doi: 10.1101/gad.6.10.1964. [DOI] [PubMed] [Google Scholar]

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