High-affinity DNA Binding by a Mot1p-TBP Complex: Implications for TAF-independent Transcription

Overview

Journal EMBO J

Specialties Biotechnology
Molecular Biology

Date 2003 Jun 14

PMID 12805227

Citations 26

Authors

Orlando H Gumbs

Allyson M Campbell

P Anthony Weil

Affiliations

Soon will be listed here.

Abstract

Yeast Mot1p, an abundant conserved member of the Snf2p-ATPase family of proteins, both dissociates TBP from DNA in vitro using the energy of ATP and represses gene transcription in vivo, yet paradoxically, loss of Mot1p function also leads to decreased transcription of certain genes. We conducted experiments utilizing fluorescently labeled DNA, TBP, fluorescence anisotropy spectroscopy and native gel electrophoresis to study Mot1p action. We have made a number of observations, the most intriguing being that a stable Mot1p-TBP complex has the ability to bind TATA DNA with high affinity, albeit with dramatically altered specificity. We propose that this altered TBP-DNA recognition is integral to Mot1p's ability to regulate transcription, and further postulate that the Mot1p-TBP complex delivers TBP to TAF-independent mRNA encoding genes.

Citing Articles

Structural convergence endows nuclear transport receptor Kap114p with a transcriptional repressor function toward TATA-binding protein.

Liao C, Wang Y, Pi W, Wang C, Wu Y, Chen W Nat Commun. 2023; 14(1):5518.

PMID: 37684250 PMC: 10491584. DOI: 10.1038/s41467-023-41206-9.

Karyopherin Kap114p-mediated trans-repression controls ribosomal gene expression under saline stress.

Liao C, Shankar S, Pi W, Chang C, Ahmed G, Chen W EMBO Rep. 2020; 21(7):e48324.

PMID: 32484313 PMC: 7332979. DOI: 10.15252/embr.201948324.

Conformational changes and catalytic inefficiency associated with Mot1-mediated TBP-DNA dissociation.

Heiss G, Ploetz E, Voith von Voithenberg L, Viswanathan R, Glaser S, Schluesche P Nucleic Acids Res. 2019; 47(6):2793-2806.

PMID: 30649478 PMC: 6451094. DOI: 10.1093/nar/gky1322.

Analyzing the Dynamics of Single TBP-DNA-NC2 Complexes Using Hidden Markov Models.

Zarrabi N, Schluesche P, Meisterernst M, Borsch M, Lamb D Biophys J. 2018; 115(12):2310-2326.

PMID: 30527334 PMC: 6302255. DOI: 10.1016/j.bpj.2018.11.015.

Molecular Mechanism of Mot1, a TATA-binding Protein (TBP)-DNA Dissociating Enzyme.

Viswanathan R, True J, Auble D J Biol Chem. 2016; 291(30):15714-26.

PMID: 27255709 PMC: 4957054. DOI: 10.1074/jbc.M116.730366.

References

van der Knaap J, van den Boom V, Kuipers J, Van Eijk M, van der Vliet P, Timmers H . The gene for human TATA-binding-protein-associated factor (TAFII) 170: structure, promoter and chromosomal localization. Biochem J. 2000; 345 Pt 3:521-7. PMC: 1220786. DOI: 10.1042/0264-6021:3450521. View

Li X, Virbasius A, Zhu X, Green M . Enhancement of TBP binding by activators and general transcription factors. Nature. 1999; 399(6736):605-9. DOI: 10.1038/21232. View

Li X, Bhaumik S, Green M . Distinct classes of yeast promoters revealed by differential TAF recruitment. Science. 2000; 288(5469):1242-4. DOI: 10.1126/science.288.5469.1242. View

Kuras L, Kosa P, Mencia M, Struhl K . TAF-Containing and TAF-independent forms of transcriptionally active TBP in vivo. Science. 2000; 288(5469):1244-8. DOI: 10.1126/science.288.5469.1244. View

Adamkewicz J, Mueller C, Hansen K, Prudhomme W, Thorner J . Purification and enzymic properties of Mot1 ATPase, a regulator of basal transcription in the yeast Saccharomyces cerevisiae. J Biol Chem. 2000; 275(28):21158-68. DOI: 10.1074/jbc.M002639200. View

Pugh B . Control of gene expression through regulation of the TATA-binding protein. Gene. 2000; 255(1):1-14. DOI: 10.1016/s0378-1119(00)00288-2. View

Darst R, Wang D, Auble D . MOT1-catalyzed TBP-DNA disruption: uncoupling DNA conformational change and role of upstream DNA. EMBO J. 2001; 20(8):2028-40. PMC: 125425. DOI: 10.1093/emboj/20.8.2028. View

Adamkewicz J, Hansen K, Prudhomme W, Davis J, Thorner J . High affinity interaction of yeast transcriptional regulator, Mot1, with TATA box-binding protein (TBP). J Biol Chem. 2001; 276(15):11883-94. DOI: 10.1074/jbc.M010665200. View

Bhaumik S, Green M . SAGA is an essential in vivo target of the yeast acidic activator Gal4p. Genes Dev. 2001; 15(15):1935-45. PMC: 312746. DOI: 10.1101/gad.911401. View

10.

Larschan E, Winston F . The S. cerevisiae SAGA complex functions in vivo as a coactivator for transcriptional activation by Gal4. Genes Dev. 2001; 15(15):1946-56. PMC: 312753. DOI: 10.1101/gad.911501. View

11.

Andrade M, Petosa C, ODonoghue S, Muller C, Bork P . Comparison of ARM and HEAT protein repeats. J Mol Biol. 2001; 309(1):1-18. DOI: 10.1006/jmbi.2001.4624. View

12.

Pereira L, van der Knaap J, van den Boom V, van den Heuvel F, Timmers H . TAF(II)170 interacts with the concave surface of TATA-binding protein to inhibit its DNA binding activity. Mol Cell Biol. 2001; 21(21):7523-34. PMC: 99923. DOI: 10.1128/MCB.21.21.7523-7534.2001. View

13.

Banik U, Beechem J, Klebanow E, Schroeder S, Weil P . Fluorescence-based analyses of the effects of full-length recombinant TAF130p on the interaction of TATA box-binding protein with TATA box DNA. J Biol Chem. 2001; 276(52):49100-9. DOI: 10.1074/jbc.M109246200. View

14.

Dasgupta A, Darst R, Martin K, Afshari C, Auble D . Mot1 activates and represses transcription by direct, ATPase-dependent mechanisms. Proc Natl Acad Sci U S A. 2002; 99(5):2666-71. PMC: 122405. DOI: 10.1073/pnas.052397899. View

15.

Tora L . A unified nomenclature for TATA box binding protein (TBP)-associated factors (TAFs) involved in RNA polymerase II transcription. Genes Dev. 2002; 16(6):673-5. DOI: 10.1101/gad.976402. View

16.

Mencia M, Moqtaderi Z, Geisberg J, Kuras L, Struhl K . Activator-specific recruitment of TFIID and regulation of ribosomal protein genes in yeast. Mol Cell. 2002; 9(4):823-33. DOI: 10.1016/s1097-2765(02)00490-2. View

17.

Sanders S, Jennings J, Canutescu A, Link A, Anthony Weil P . Proteomics of the eukaryotic transcription machinery: identification of proteins associated with components of yeast TFIID by multidimensional mass spectrometry. Mol Cell Biol. 2002; 22(13):4723-38. PMC: 133885. DOI: 10.1128/MCB.22.13.4723-4738.2002. View

18.

Sanders S, Garbett K, Anthony Weil P . Molecular characterization of Saccharomyces cerevisiae TFIID. Mol Cell Biol. 2002; 22(16):6000-13. PMC: 133964. DOI: 10.1128/MCB.22.16.6000-6013.2002. View

19.

Li X, Bhaumik S, Zhu X, Li L, Shen W, Dixit B . Selective recruitment of TAFs by yeast upstream activating sequences. Implications for eukaryotic promoter structure. Curr Biol. 2002; 12(14):1240-4. DOI: 10.1016/s0960-9822(02)00932-6. View

20.

Andrau J, van Oevelen C, van Teeffelen H, Anthony Weil P, Holstege F, Timmers H . Mot1p is essential for TBP recruitment to selected promoters during in vivo gene activation. EMBO J. 2002; 21(19):5173-83. PMC: 129025. DOI: 10.1093/emboj/cdf485. View