Skip to main content
Molecular and Cellular Biology logoLink to Molecular and Cellular Biology
. 1992 Nov;12(11):5189–5196. doi: 10.1128/mcb.12.11.5189

TFIIA induces conformational changes in TFIID via interactions with the basic repeat.

D K Lee 1, J DeJong 1, S Hashimoto 1, M Horikoshi 1, R G Roeder 1
PMCID: PMC360452  PMID: 1406690

Abstract

DNA-binding studies with Saccharomyces cerevisiae TFIID point mutants indicated that TFIIA interacts with the basic repeat region of TFIID and induces structural changes. The latter was shown by the ability of TFIIA to compensate for TFIID point mutants defective for DNA binding. Interaction with TFIIA also rendered TFIID binding temperature independent, thus mimicking the effect of removing the nonconserved N terminus of TFIID. In addition, N-terminal truncation of the TFIID point mutants defective for DNA binding mimicked the ability of TFIIA to restore DNA binding of those mutants. Taken together, these results suggest that TFIIA enhances TFIID binding to DNA by eliminating an otherwise inhibitory effect of the nonconserved N terminus of TFIID. Furthermore, analyses of TFIID contact points on DNA and binding studies with TATA-containing oligonucleotide probes showed that TFIIA decreases the effect of sequences flanking the adenovirus major late TATA element on TFIID binding to DNA, suggesting a possible role of TFIIA in allowing TFIID to recognize a wider variety of promoters.

Full text

PDF
5189

Images in this article

Selected References

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

  1. Buratowski S., Hahn S., Guarente L., Sharp P. A. Five intermediate complexes in transcription initiation by RNA polymerase II. Cell. 1989 Feb 24;56(4):549–561. doi: 10.1016/0092-8674(89)90578-3. [DOI] [PubMed] [Google Scholar]
  2. Cavallini B., Faus I., Matthes H., Chipoulet J. M., Winsor B., Egly J. M., Chambon P. Cloning of the gene encoding the yeast protein BTF1Y, which can substitute for the human TATA box-binding factor. Proc Natl Acad Sci U S A. 1989 Dec;86(24):9803–9807. doi: 10.1073/pnas.86.24.9803. [DOI] [PMC free article] [PubMed] [Google Scholar]
  3. Cavallini B., Huet J., Plassat J. L., Sentenac A., Egly J. M., Chambon P. A yeast activity can substitute for the HeLa cell TATA box factor. Nature. 1988 Jul 7;334(6177):77–80. doi: 10.1038/334077a0. [DOI] [PubMed] [Google Scholar]
  4. Conaway R. C., Conaway J. W. An RNA polymerase II transcription factor has an associated DNA-dependent ATPase (dATPase) activity strongly stimulated by the TATA region of promoters. Proc Natl Acad Sci U S A. 1989 Oct;86(19):7356–7360. doi: 10.1073/pnas.86.19.7356. [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. Cortes P., Flores O., Reinberg D. Factors involved in specific transcription by mammalian RNA polymerase II: purification and analysis of transcription factor IIA and identification of transcription factor IIJ. Mol Cell Biol. 1992 Jan;12(1):413–421. doi: 10.1128/mcb.12.1.413. [DOI] [PMC free article] [PubMed] [Google Scholar]
  7. Eisenmann D. M., Dollard C., Winston F. SPT15, the gene encoding the yeast TATA binding factor TFIID, is required for normal transcription initiation in vivo. Cell. 1989 Sep 22;58(6):1183–1191. doi: 10.1016/0092-8674(89)90516-3. [DOI] [PubMed] [Google Scholar]
  8. Fire A., Samuels M., Sharp P. A. Interactions between RNA polymerase II, factors, and template leading to accurate transcription. J Biol Chem. 1984 Feb 25;259(4):2509–2516. [PubMed] [Google Scholar]
  9. Flores O., Lu H., Reinberg D. Factors involved in specific transcription by mammalian RNA polymerase II. Identification and characterization of factor IIH. J Biol Chem. 1992 Feb 5;267(4):2786–2793. [PubMed] [Google Scholar]
  10. Gasch A., Hoffmann A., Horikoshi M., Roeder R. G., Chua N. H. Arabidopsis thaliana contains two genes for TFIID. Nature. 1990 Jul 26;346(6282):390–394. doi: 10.1038/346390a0. [DOI] [PubMed] [Google Scholar]
  11. Gerard M., Fischer L., Moncollin V., Chipoulet J. M., Chambon P., Egly J. M. Purification and interaction properties of the human RNA polymerase B(II) general transcription factor BTF2. J Biol Chem. 1991 Nov 5;266(31):20940–20945. [PubMed] [Google Scholar]
  12. 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]
  13. Hahn S., Buratowski S., Sharp P. A., Guarente L. Identification of a yeast protein homologous in function to the mammalian general transcription factor, TFIIA. EMBO J. 1989 Nov;8(11):3379–3382. doi: 10.1002/j.1460-2075.1989.tb08501.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  14. Hahn S., Buratowski S., Sharp P. A., Guarente L. Isolation of the gene encoding the yeast TATA binding protein TFIID: a gene identical to the SPT15 suppressor of Ty element insertions. Cell. 1989 Sep 22;58(6):1173–1181. doi: 10.1016/0092-8674(89)90515-1. [DOI] [PubMed] [Google Scholar]
  15. Hoey T., Dynlacht B. D., Peterson M. G., Pugh B. F., Tjian R. Isolation and characterization of the Drosophila gene encoding the TATA box binding protein, TFIID. Cell. 1990 Jun 29;61(7):1179–1186. doi: 10.1016/0092-8674(90)90682-5. [DOI] [PubMed] [Google Scholar]
  16. Hoffman A., Sinn E., Yamamoto T., Wang J., Roy A., Horikoshi M., Roeder R. G. Highly conserved core domain and unique N terminus with presumptive regulatory motifs in a human TATA factor (TFIID). Nature. 1990 Jul 26;346(6282):387–390. doi: 10.1038/346387a0. [DOI] [PubMed] [Google Scholar]
  17. Hoffmann A., Horikoshi M., Wang C. K., Schroeder S., Weil P. A., Roeder R. G. Cloning of the Schizosaccharomyces pombe TFIID gene reveals a strong conservation of functional domains present in Saccharomyces cerevisiae TFIID. Genes Dev. 1990 Jul;4(7):1141–1148. doi: 10.1101/gad.4.7.1141. [DOI] [PubMed] [Google Scholar]
  18. Horikoshi M., Bertuccioli C., Takada R., Wang J., Yamamoto T., Roeder R. G. Transcription factor TFIID induces DNA bending upon binding to the TATA element. Proc Natl Acad Sci U S A. 1992 Feb 1;89(3):1060–1064. doi: 10.1073/pnas.89.3.1060. [DOI] [PMC free article] [PubMed] [Google Scholar]
  19. Horikoshi M., Hai T., Lin Y. S., Green M. R., Roeder R. G. Transcription factor ATF interacts with the TATA factor to facilitate establishment of a preinitiation complex. Cell. 1988 Sep 23;54(7):1033–1042. doi: 10.1016/0092-8674(88)90118-3. [DOI] [PubMed] [Google Scholar]
  20. Horikoshi M., Wang C. K., Fujii H., Cromlish J. A., Weil P. A., Roeder R. G. Cloning and structure of a yeast gene encoding a general transcription initiation factor TFIID that binds to the TATA box. Nature. 1989 Sep 28;341(6240):299–303. doi: 10.1038/341299a0. [DOI] [PubMed] [Google Scholar]
  21. 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]
  22. 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]
  23. Horikoshi N., Maguire K., Kralli A., Maldonado E., Reinberg D., Weinmann R. Direct interaction between adenovirus E1A protein and the TATA box binding transcription factor IID. Proc Natl Acad Sci U S A. 1991 Jun 15;88(12):5124–5128. doi: 10.1073/pnas.88.12.5124. [DOI] [PMC free article] [PubMed] [Google Scholar]
  24. Kao C. C., Lieberman P. M., Schmidt M. C., Zhou Q., Pei R., Berk A. J. Cloning of a transcriptionally active human TATA binding factor. Science. 1990 Jun 29;248(4963):1646–1650. doi: 10.1126/science.2194289. [DOI] [PubMed] [Google Scholar]
  25. Lee D. K., Horikoshi M., Roeder R. G. Interaction of TFIID in the minor groove of the TATA element. Cell. 1991 Dec 20;67(6):1241–1250. doi: 10.1016/0092-8674(91)90300-n. [DOI] [PubMed] [Google Scholar]
  26. Lee W. S., Kao C. C., Bryant G. O., Liu X., Berk A. J. Adenovirus E1A activation domain binds the basic repeat in the TATA box transcription factor. Cell. 1991 Oct 18;67(2):365–376. doi: 10.1016/0092-8674(91)90188-5. [DOI] [PubMed] [Google Scholar]
  27. 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]
  28. Maldonado E., Ha I., Cortes P., Weis L., Reinberg D. Factors involved in specific transcription by mammalian RNA polymerase II: role of transcription factors IIA, IID, and IIB during formation of a transcription-competent complex. Mol Cell Biol. 1990 Dec;10(12):6335–6347. doi: 10.1128/mcb.10.12.6335. [DOI] [PMC free article] [PubMed] [Google Scholar]
  29. Meisterernst M., Roeder R. G. Family of proteins that interact with TFIID and regulate promoter activity. Cell. 1991 Nov 1;67(3):557–567. doi: 10.1016/0092-8674(91)90530-c. [DOI] [PubMed] [Google Scholar]
  30. Meisterernst M., Roy A. L., Lieu H. M., Roeder R. G. Activation of class II gene transcription by regulatory factors is potentiated by a novel activity. Cell. 1991 Sep 6;66(5):981–993. doi: 10.1016/0092-8674(91)90443-3. [DOI] [PubMed] [Google Scholar]
  31. Muhich M. L., Iida C. T., Horikoshi M., Roeder R. G., Parker C. S. cDNA clone encoding Drosophila transcription factor TFIID. Proc Natl Acad Sci U S A. 1990 Dec;87(23):9148–9152. doi: 10.1073/pnas.87.23.9148. [DOI] [PMC free article] [PubMed] [Google Scholar]
  32. Nakajima N., Horikoshi M., Roeder R. G. Factors involved in specific transcription by mammalian RNA polymerase II: purification, genetic specificity, and TATA box-promoter interactions of TFIID. Mol Cell Biol. 1988 Oct;8(10):4028–4040. doi: 10.1128/mcb.8.10.4028. [DOI] [PMC free article] [PubMed] [Google Scholar]
  33. 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]
  34. 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]
  35. Ptashne M., Gann A. A. Activators and targets. Nature. 1990 Jul 26;346(6282):329–331. doi: 10.1038/346329a0. [DOI] [PubMed] [Google Scholar]
  36. Ranish J. A., Hahn S. The yeast general transcription factor TFIIA is composed of two polypeptide subunits. J Biol Chem. 1991 Oct 15;266(29):19320–19327. [PubMed] [Google Scholar]
  37. Ranish J. A., Lane W. S., Hahn S. Isolation of two genes that encode subunits of the yeast transcription factor IIA. Science. 1992 Feb 28;255(5048):1127–1129. doi: 10.1126/science.1546313. [DOI] [PubMed] [Google Scholar]
  38. 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]
  39. Reinberg D., Horikoshi M., Roeder R. G. Factors involved in specific transcription in mammalian RNA polymerase II. Functional analysis of initiation factors IIA and IID and identification of a new factor operating at sequences downstream of the initiation site. J Biol Chem. 1987 Mar 5;262(7):3322–3330. [PubMed] [Google Scholar]
  40. Roeder R. G. The complexities of eukaryotic transcription initiation: regulation of preinitiation complex assembly. Trends Biochem Sci. 1991 Nov;16(11):402–408. doi: 10.1016/0968-0004(91)90164-q. [DOI] [PubMed] [Google Scholar]
  41. Samuels M., Sharp P. A. Purification and characterization of a specific RNA polymerase II transcription factor. J Biol Chem. 1986 Feb 15;261(5):2003–2013. [PubMed] [Google Scholar]
  42. Sawadogo M., Roeder R. G. Interaction of a gene-specific transcription factor with the adenovirus major late promoter upstream of the TATA box region. Cell. 1985 Nov;43(1):165–175. doi: 10.1016/0092-8674(85)90021-2. [DOI] [PubMed] [Google Scholar]
  43. Sawadogo M., Sentenac A. RNA polymerase B (II) and general transcription factors. Annu Rev Biochem. 1990;59:711–754. doi: 10.1146/annurev.bi.59.070190.003431. [DOI] [PubMed] [Google Scholar]
  44. 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]
  45. Schmidt M. C., Zhou Q., Berk A. J. Sp1 activates transcription without enhancing DNA-binding activity of the TATA box factor. Mol Cell Biol. 1989 Aug;9(8):3299–3307. doi: 10.1128/mcb.9.8.3299. [DOI] [PMC free article] [PubMed] [Google Scholar]
  46. Starr D. B., Hawley D. K. TFIID binds in the minor groove of the TATA box. Cell. 1991 Dec 20;67(6):1231–1240. doi: 10.1016/0092-8674(91)90299-e. [DOI] [PubMed] [Google Scholar]
  47. Stringer K. F., Ingles C. J., Greenblatt J. Direct and selective binding of an acidic transcriptional activation domain to the TATA-box factor TFIID. Nature. 1990 Jun 28;345(6278):783–786. doi: 10.1038/345783a0. [DOI] [PubMed] [Google Scholar]
  48. Sumimoto H., Ohkuma Y., Yamamoto T., Horikoshi M., Roeder R. G. Factors involved in specific transcription by mammalian RNA polymerase II: identification of general transcription factor TFIIG. Proc Natl Acad Sci U S A. 1990 Dec;87(23):9158–9162. doi: 10.1073/pnas.87.23.9158. [DOI] [PMC free article] [PubMed] [Google Scholar]
  49. Tamura T., Sumita K., Fujino I., Aoyama A., Horikoshi M., Hoffmann A., Roeder R. G., Muramatsu M., Mikoshiba K. Striking homology of the 'variable' N-terminal as well as the 'conserved core' domains of the mouse and human TATA-factors (TFIID). Nucleic Acids Res. 1991 Jul 25;19(14):3861–3865. doi: 10.1093/nar/19.14.3861. [DOI] [PMC free article] [PubMed] [Google Scholar]
  50. Usuda Y., Kubota A., Berk A. J., Handa H. Affinity purification of transcription factor IIA from HeLa cell nuclear extracts. EMBO J. 1991 Aug;10(8):2305–2310. doi: 10.1002/j.1460-2075.1991.tb07767.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  51. Van Dyke M. W., Roeder R. G., Sawadogo M. Physical analysis of transcription preinitiation complex assembly on a class II gene promoter. Science. 1988 Sep 9;241(4871):1335–1338. doi: 10.1126/science.3413495. [DOI] [PubMed] [Google Scholar]
  52. Van Dyke M. W., Sawadogo M., Roeder R. G. Stability of transcription complexes on class II genes. Mol Cell Biol. 1989 Jan;9(1):342–344. doi: 10.1128/mcb.9.1.342. [DOI] [PMC free article] [PubMed] [Google Scholar]
  53. Yamamoto T., Horikoshi M., Wang J., Hasegawa S., Weil P. A., Roeder R. G. A bipartite DNA binding domain composed of direct repeats in the TATA box binding factor TFIID. Proc Natl Acad Sci U S A. 1992 Apr 1;89(7):2844–2848. doi: 10.1073/pnas.89.7.2844. [DOI] [PMC free article] [PubMed] [Google Scholar]
  54. 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]

Articles from Molecular and Cellular Biology are provided here courtesy of Taylor & Francis

RESOURCES