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. 1992 Feb 1;89(3):1060–1064. doi: 10.1073/pnas.89.3.1060

Transcription factor TFIID induces DNA bending upon binding to the TATA element.

M Horikoshi 1, C Bertuccioli 1, R Takada 1, J Wang 1, T Yamamoto 1, R G Roeder 1
PMCID: PMC48385  PMID: 1736286

Abstract

The TATA box-binding factor TFIID plays a primary role in the process of transcription initiation by RNA polymerase II and its regulation by various gene-specific factors. Here we employ a permuted binding site/gel retardation assay with recombinant yeast and human TFIID to show that this factor induces DNA bending around the TATA element. These results are consistent with the presence of G + C-rich sequence elements flanking the consensus TATA element and led to the recently confirmed suggestion that TFIID interacts with the TATA element via the minor groove. They also raise the possibility that TFIID-induced bending might facilitate promoter interactions of other general factors in the preinitiation complex or interactions between general transcription factors and regulatory factors bound at upstream sites.

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Selected References

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

  1. Abmayr S. M., Workman J. L., Roeder R. G. The pseudorabies immediate early protein stimulates in vitro transcription by facilitating TFIID: promoter interactions. Genes Dev. 1988 May;2(5):542–553. doi: 10.1101/gad.2.5.542. [DOI] [PubMed] [Google Scholar]
  2. Bracco L., Kotlarz D., Kolb A., Diekmann S., Buc H. Synthetic curved DNA sequences can act as transcriptional activators in Escherichia coli. EMBO J. 1989 Dec 20;8(13):4289–4296. doi: 10.1002/j.1460-2075.1989.tb08615.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  3. 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]
  4. 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]
  5. 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]
  6. 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]
  7. 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]
  8. 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]
  9. Fikes J. D., Becker D. M., Winston F., Guarente L. Striking conservation of TFIID in Schizosaccharomyces pombe and Saccharomyces cerevisiae. Nature. 1990 Jul 19;346(6281):291–294. doi: 10.1038/346291a0. [DOI] [PubMed] [Google Scholar]
  10. Gartenberg M. R., Crothers D. M. DNA sequence determinants of CAP-induced bending and protein binding affinity. Nature. 1988 Jun 30;333(6176):824–829. doi: 10.1038/333824a0. [DOI] [PubMed] [Google Scholar]
  11. 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]
  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. Goodman S. D., Nash H. A. Functional replacement of a protein-induced bend in a DNA recombination site. Nature. 1989 Sep 21;341(6239):251–254. doi: 10.1038/341251a0. [DOI] [PubMed] [Google Scholar]
  14. Greenblatt J. Roles of TFIID in transcriptional initiation by RNA polymerase II. Cell. 1991 Sep 20;66(6):1067–1070. doi: 10.1016/0092-8674(91)90027-v. [DOI] [PubMed] [Google Scholar]
  15. 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]
  16. Hahn S., Buratowski S., Sharp P. A., Guarente L. Yeast TATA-binding protein TFIID binds to TATA elements with both consensus and nonconsensus DNA sequences. Proc Natl Acad Sci U S A. 1989 Aug;86(15):5718–5722. doi: 10.1073/pnas.86.15.5718. [DOI] [PMC free article] [PubMed] [Google Scholar]
  17. Hai T. W., Horikoshi M., Roeder R. G., Green M. R. Analysis of the role of the transcription factor ATF in the assembly of a functional preinitiation complex. Cell. 1988 Sep 23;54(7):1043–1051. doi: 10.1016/0092-8674(88)90119-5. [DOI] [PubMed] [Google Scholar]
  18. 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]
  19. 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]
  20. 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]
  21. Horikoshi M., Carey M. F., Kakidani H., Roeder R. G. Mechanism of action of a yeast activator: direct effect of GAL4 derivatives on mammalian TFIID-promoter interactions. Cell. 1988 Aug 26;54(5):665–669. doi: 10.1016/s0092-8674(88)80011-4. [DOI] [PubMed] [Google Scholar]
  22. 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]
  23. 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]
  24. 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]
  25. 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]
  26. Ingles C. J., Shales M., Cress W. D., Triezenberg S. J., Greenblatt J. Reduced binding of TFIID to transcriptionally compromised mutants of VP16. Nature. 1991 Jun 13;351(6327):588–590. doi: 10.1038/351588a0. [DOI] [PubMed] [Google Scholar]
  27. Inostroza J., Flores O., Reinberg D. Factors involved in specific transcription by mammalian RNA polymerase II. Purification and functional analysis of general transcription factor IIE. J Biol Chem. 1991 May 15;266(14):9304–9308. [PubMed] [Google Scholar]
  28. 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]
  29. Kato H., Horikoshi M., Roeder R. G. Repression of HIV-1 transcription by a cellular protein. Science. 1991 Mar 22;251(5000):1476–1479. doi: 10.1126/science.2006421. [DOI] [PubMed] [Google Scholar]
  30. 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]
  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. Nash H. A. Bending and supercoiling of DNA at the attachment site of bacteriophage lambda. Trends Biochem Sci. 1990 Jun;15(6):222–227. doi: 10.1016/0968-0004(90)90034-9. [DOI] [PubMed] [Google Scholar]
  34. 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]
  35. 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]
  36. 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]
  37. Roy A. L., Meisterernst M., Pognonec P., Roeder R. G. Cooperative interaction of an initiator-binding transcription initiation factor and the helix-loop-helix activator USF. Nature. 1991 Nov 21;354(6350):245–248. doi: 10.1038/354245a0. [DOI] [PubMed] [Google Scholar]
  38. 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]
  39. 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]
  40. 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]
  41. Smale S. T., Baltimore D. The "initiator" as a transcription control element. Cell. 1989 Apr 7;57(1):103–113. doi: 10.1016/0092-8674(89)90176-1. [DOI] [PubMed] [Google Scholar]
  42. Solomon M. J., Strauss F., Varshavsky A. A mammalian high mobility group protein recognizes any stretch of six A.T base pairs in duplex DNA. Proc Natl Acad Sci U S A. 1986 Mar;83(5):1276–1280. doi: 10.1073/pnas.83.5.1276. [DOI] [PMC free article] [PubMed] [Google Scholar]
  43. 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]
  44. Studier F. W., Rosenberg A. H., Dunn J. J., Dubendorff J. W. Use of T7 RNA polymerase to direct expression of cloned genes. Methods Enzymol. 1990;185:60–89. doi: 10.1016/0076-6879(90)85008-c. [DOI] [PubMed] [Google Scholar]
  45. 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]
  46. Travers A. A. DNA conformation and protein binding. Annu Rev Biochem. 1989;58:427–452. doi: 10.1146/annurev.bi.58.070189.002235. [DOI] [PubMed] [Google Scholar]
  47. 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]
  48. Workman J. L., Abmayr S. M., Cromlish W. A., Roeder R. G. Transcriptional regulation by the immediate early protein of pseudorabies virus during in vitro nucleosome assembly. Cell. 1988 Oct 21;55(2):211–219. doi: 10.1016/0092-8674(88)90044-x. [DOI] [PubMed] [Google Scholar]
  49. Workman J. L., Roeder R. G., Kingston R. E. An upstream transcription factor, USF (MLTF), facilitates the formation of preinitiation complexes during in vitro chromatin assembly. EMBO J. 1990 Apr;9(4):1299–1308. doi: 10.1002/j.1460-2075.1990.tb08239.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  50. Workman J. L., Taylor I. C., Kingston R. E. Activation domains of stably bound GAL4 derivatives alleviate repression of promoters by nucleosomes. Cell. 1991 Feb 8;64(3):533–544. doi: 10.1016/0092-8674(91)90237-s. [DOI] [PubMed] [Google Scholar]
  51. Wu H. M., Crothers D. M. The locus of sequence-directed and protein-induced DNA bending. Nature. 1984 Apr 5;308(5959):509–513. doi: 10.1038/308509a0. [DOI] [PubMed] [Google Scholar]
  52. Yang C. C., Nash H. A. The interaction of E. coli IHF protein with its specific binding sites. Cell. 1989 Jun 2;57(5):869–880. doi: 10.1016/0092-8674(89)90801-5. [DOI] [PubMed] [Google Scholar]
  53. 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]

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