Abstract
The binding of TATA-binding protein (TBP) to the TATA element is the first step in the initiation of RNA polymerase II transcription from many promoters in vitro. It has been proposed that upstream activator proteins stimulate transcription by recruiting TBP to the promoter, thus facilitating the assembly of a transcription complex. However, the role of activator proteins acting at this step to stimulate transcription in vivo remains largely speculative. To test whether recruitment of TBP to the promoter is sufficient for transcriptional activation in vivo, we constructed a hybrid protein containing TBP of the yeast Saccharomyces cerevisiae fused to the DNA-binding domain of GAL4. Our results show that TBP recruited by the GAL4 DNA-binding domain to promoters bearing a GAL4-binding site can interact with the TATA element and direct high levels of transcription. This finding indicates that binding of TBP to promoters in S. cerevisiae is a major rate-limiting step accelerated by upstream activator proteins.
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- Barberis A., Pearlberg J., Simkovich N., Farrell S., Reinagel P., Bamdad C., Sigal G., Ptashne M. Contact with a component of the polymerase II holoenzyme suffices for gene activation. Cell. 1995 May 5;81(3):359–368. doi: 10.1016/0092-8674(95)90389-5. [DOI] [PubMed] [Google Scholar]
- 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]
- Busby S., Ebright R. H. Promoter structure, promoter recognition, and transcription activation in prokaryotes. Cell. 1994 Dec 2;79(5):743–746. doi: 10.1016/0092-8674(94)90063-9. [DOI] [PubMed] [Google Scholar]
- Chatterjee S., Struhl K. Connecting a promoter-bound protein to TBP bypasses the need for a transcriptional activation domain. Nature. 1995 Apr 27;374(6525):820–822. doi: 10.1038/374820a0. [DOI] [PubMed] [Google Scholar]
- Chen J., Ding M., Pederson D. S. Binding of TFIID to the CYC1 TATA boxes in yeast occurs independently of upstream activating sequences. Proc Natl Acad Sci U S A. 1994 Dec 6;91(25):11909–11913. doi: 10.1073/pnas.91.25.11909. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 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]
- 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]
- Greenblatt J., Nodwell J. R., Mason S. W. Transcriptional antitermination. Nature. 1993 Jul 29;364(6436):401–406. doi: 10.1038/364401a0. [DOI] [PubMed] [Google Scholar]
- 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]
- Guarente L., Ptashne M. Fusion of Escherichia coli lacZ to the cytochrome c gene of Saccharomyces cerevisiae. Proc Natl Acad Sci U S A. 1981 Apr;78(4):2199–2203. doi: 10.1073/pnas.78.4.2199. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 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]
- 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]
- Hengartner C. J., Thompson C. M., Zhang J., Chao D. M., Liao S. M., Koleske A. J., Okamura S., Young R. A. Association of an activator with an RNA polymerase II holoenzyme. Genes Dev. 1995 Apr 15;9(8):897–910. doi: 10.1101/gad.9.8.897. [DOI] [PubMed] [Google Scholar]
- Hill J., Donald K. A., Griffiths D. E., Donald G. DMSO-enhanced whole cell yeast transformation. Nucleic Acids Res. 1991 Oct 25;19(20):5791–5791. doi: 10.1093/nar/19.20.5791. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 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]
- 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]
- Kim Y. J., Björklund S., Li Y., Sayre M. H., Kornberg R. D. A multiprotein mediator of transcriptional activation and its interaction with the C-terminal repeat domain of RNA polymerase II. Cell. 1994 May 20;77(4):599–608. doi: 10.1016/0092-8674(94)90221-6. [DOI] [PubMed] [Google Scholar]
- Klages N., Strubin M. Stimulation of RNA polymerase II transcription initiation by recruitment of TBP in vivo. Nature. 1995 Apr 27;374(6525):822–823. doi: 10.1038/374822a0. [DOI] [PubMed] [Google Scholar]
- Klein C., Struhl K. Increased recruitment of TATA-binding protein to the promoter by transcriptional activation domains in vivo. Science. 1994 Oct 14;266(5183):280–282. doi: 10.1126/science.7939664. [DOI] [PubMed] [Google Scholar]
- Koleske A. J., Young R. A. An RNA polymerase II holoenzyme responsive to activators. Nature. 1994 Mar 31;368(6470):466–469. doi: 10.1038/368466a0. [DOI] [PubMed] [Google Scholar]
- Kumar A., Grimes B., Logan M., Wedgwood S., Williamson H., Hayward R. S. A hybrid sigma subunit directs RNA polymerase to a hybrid promoter in Escherichia coli. J Mol Biol. 1995 Mar 10;246(5):563–571. doi: 10.1016/s0022-2836(05)80105-6. [DOI] [PubMed] [Google Scholar]
- Li W. Z., Sherman F. Two types of TATA elements for the CYC1 gene of the yeast Saccharomyces cerevisiae. Mol Cell Biol. 1991 Feb;11(2):666–676. doi: 10.1128/mcb.11.2.666. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 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]
- Mitchell P. J., Tjian R. Transcriptional regulation in mammalian cells by sequence-specific DNA binding proteins. Science. 1989 Jul 28;245(4916):371–378. doi: 10.1126/science.2667136. [DOI] [PubMed] [Google Scholar]
- Rasmussen E. B., Lis J. T. In vivo transcriptional pausing and cap formation on three Drosophila heat shock genes. Proc Natl Acad Sci U S A. 1993 Sep 1;90(17):7923–7927. doi: 10.1073/pnas.90.17.7923. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Roberts J. W. Phage lambda and the regulation of transcription termination. Cell. 1988 Jan 15;52(1):5–6. doi: 10.1016/0092-8674(88)90523-5. [DOI] [PubMed] [Google Scholar]
- Rougvie A. E., Lis J. T. The RNA polymerase II molecule at the 5' end of the uninduced hsp70 gene of D. melanogaster is transcriptionally engaged. Cell. 1988 Sep 9;54(6):795–804. doi: 10.1016/s0092-8674(88)91087-2. [DOI] [PubMed] [Google Scholar]
- Simon J. A., Lis J. T. A germline transformation analysis reveals flexibility in the organization of heat shock consensus elements. Nucleic Acids Res. 1987 Apr 10;15(7):2971–2988. doi: 10.1093/nar/15.7.2971. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 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]
- 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]
- Swaffield J. C., Melcher K., Johnston S. A. A highly conserved ATPase protein as a mediator between acidic activation domains and the TATA-binding protein. Nature. 1995 Mar 2;374(6517):88–91. doi: 10.1038/374088a0. [DOI] [PubMed] [Google Scholar]
- Thompson C. M., Koleske A. J., Chao D. M., Young R. A. A multisubunit complex associated with the RNA polymerase II CTD and TATA-binding protein in yeast. Cell. 1993 Jul 2;73(7):1361–1375. doi: 10.1016/0092-8674(93)90362-t. [DOI] [PubMed] [Google Scholar]
- Tjian R., Maniatis T. Transcriptional activation: a complex puzzle with few easy pieces. Cell. 1994 Apr 8;77(1):5–8. doi: 10.1016/0092-8674(94)90227-5. [DOI] [PubMed] [Google Scholar]
- Usheva A., Maldonado E., Goldring A., Lu H., Houbavi C., Reinberg D., Aloni Y. Specific interaction between the nonphosphorylated form of RNA polymerase II and the TATA-binding protein. Cell. 1992 May 29;69(5):871–881. doi: 10.1016/0092-8674(92)90297-p. [DOI] [PubMed] [Google Scholar]
- Wang W., Gralla J. D., Carey M. The acidic activator GAL4-AH can stimulate polymerase II transcription by promoting assembly of a closed complex requiring TFIID and TFIIA. Genes Dev. 1992 Sep;6(9):1716–1727. doi: 10.1101/gad.6.9.1716. [DOI] [PubMed] [Google Scholar]
- 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]
- Xiao H., Friesen J. D., Lis J. T. A highly conserved domain of RNA polymerase II shares a functional element with acidic activation domains of upstream transcription factors. Mol Cell Biol. 1994 Nov;14(11):7507–7516. doi: 10.1128/mcb.14.11.7507. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Xiao H., Lis J. T., Xiao H., Greenblatt J., Friesen J. D. The upstream activator CTF/NF1 and RNA polymerase II share a common element involved in transcriptional activation. Nucleic Acids Res. 1994 Jun 11;22(11):1966–1973. doi: 10.1093/nar/22.11.1966. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Xiao H., Pearson A., Coulombe B., Truant R., Zhang S., Regier J. L., Triezenberg S. J., Reinberg D., Flores O., Ingles C. J. Binding of basal transcription factor TFIIH to the acidic activation domains of VP16 and p53. Mol Cell Biol. 1994 Oct;14(10):7013–7024. doi: 10.1128/mcb.14.10.7013. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Zawel L., Reinberg D. Initiation of transcription by RNA polymerase II: a multi-step process. Prog Nucleic Acid Res Mol Biol. 1993;44:67–108. doi: 10.1016/s0079-6603(08)60217-2. [DOI] [PubMed] [Google Scholar]