Mapping the Initiator Binding Taf2 Subunit in the Structure of Hydrated Yeast TFIID

Overview

Journal Structure

Publisher Cell Press

Specialties Biochemistry
Biotechnology
Cell Biology
Molecular Biology

Date 2009 Mar 13

PMID 19278651

Citations 30

Authors

Gabor Papai

Manish K Tripathi

Christine Ruhlmann

Sebastiaan Werten

Corinne Crucifix

P Anthony Weil

Patrick Schultz

Affiliations

Soon will be listed here.

Abstract

The general transcription factor TFIID is a large multisubunit complex required for the transcription of most protein-encoding genes by RNA polymerase II. Taking advantage of a TFIID preparation partially depleted in the initiator-binding Taf2p subunit, we determined the conformational and biochemical variations of the complex by electron tomography and cryo-electron microscopy of single molecules. Image analysis revealed the extent of conformational flexibility of the complex and the selection of the most homogeneous TFIID subpopulation allowed us to determine an improved structural model at 23 Angstroms resolution. This study also identified two subpopulations of Taf2p-containing and Taf2p-depleted TFIID molecules. By comparing these two TFIID species we could infer the position of Taf2p, which was confirmed by immunolabeling using a subunit-specific antibody. Mapping the position of this crucial subunit in the vicinity of Taf1p and of TBP sheds new light on its role in promoter recognition.

Citing Articles

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References

Sanders S, Weil P . Identification of two novel TAF subunits of the yeast Saccharomyces cerevisiae TFIID complex. J Biol Chem. 2000; 275(18):13895-900. DOI: 10.1074/jbc.275.18.13895. View

Kastner B, Fischer N, Golas M, Sander B, Dube P, Boehringer D . GraFix: sample preparation for single-particle electron cryomicroscopy. Nat Methods. 2007; 5(1):53-5. DOI: 10.1038/nmeth1139. View

Verrijzer C, Chen J, Yokomori K, Tjian R . Binding of TAFs to core elements directs promoter selectivity by RNA polymerase II. Cell. 1995; 81(7):1115-25. DOI: 10.1016/s0092-8674(05)80016-9. View

Pettersen E, Goddard T, Huang C, Couch G, Greenblatt D, Meng E . UCSF Chimera--a visualization system for exploratory research and analysis. J Comput Chem. 2004; 25(13):1605-12. DOI: 10.1002/jcc.20084. View

Oelgeschlager T, Chiang C, Roeder R . Topology and reorganization of a human TFIID-promoter complex. Nature. 1996; 382(6593):735-8. DOI: 10.1038/382735a0. View

Mizzen C, Yang X, Kokubo T, Brownell J, Bannister A, Owen-Hughes T . The TAF(II)250 subunit of TFIID has histone acetyltransferase activity. Cell. 1996; 87(7):1261-70. DOI: 10.1016/s0092-8674(00)81821-8. View

van Heel M, Schatz M . Fourier shell correlation threshold criteria. J Struct Biol. 2005; 151(3):250-62. DOI: 10.1016/j.jsb.2005.05.009. View

Tasto J, Carnahan R, McDonald W, Gould K . Vectors and gene targeting modules for tandem affinity purification in Schizosaccharomyces pombe. Yeast. 2001; 18(7):657-62. DOI: 10.1002/yea.713. View

Brand M, Leurent C, Mallouh V, Tora L, Schultz P . Three-dimensional structures of the TAFII-containing complexes TFIID and TFTC. Science. 1999; 286(5447):2151-3. DOI: 10.1126/science.286.5447.2151. View

10.

Bai Y, Perez G, Beechem J, Weil P . Structure-function analysis of TAF130: identification and characterization of a high-affinity TATA-binding protein interaction domain in the N terminus of yeast TAF(II)130. Mol Cell Biol. 1997; 17(6):3081-93. PMC: 232161. DOI: 10.1128/MCB.17.6.3081. View

11.

Vermeulen M, Mulder K, Denissov S, Pijnappel W, Van Schaik F, Varier R . Selective anchoring of TFIID to nucleosomes by trimethylation of histone H3 lysine 4. Cell. 2007; 131(1):58-69. DOI: 10.1016/j.cell.2007.08.016. View

12.

Leurent C, Sanders S, Demeny M, Garbett K, Ruhlmann C, Anthony Weil P . Mapping key functional sites within yeast TFIID. EMBO J. 2004; 23(4):719-27. PMC: 381015. DOI: 10.1038/sj.emboj.7600111. View

13.

Leurent C, Sanders S, Ruhlmann C, Mallouh V, Anthony Weil P, Kirschner D . Mapping histone fold TAFs within yeast TFIID. EMBO J. 2002; 21(13):3424-33. PMC: 126091. DOI: 10.1093/emboj/cdf342. View

14.

Martinez E, Chiang C, Ge H, Roeder R . TATA-binding protein-associated factor(s) in TFIID function through the initiator to direct basal transcription from a TATA-less class II promoter. EMBO J. 1994; 13(13):3115-26. PMC: 395202. DOI: 10.1002/j.1460-2075.1994.tb06610.x. View

15.

Purnell B, Emanuel P, Gilmour D . TFIID sequence recognition of the initiator and sequences farther downstream in Drosophila class II genes. Genes Dev. 1994; 8(7):830-42. DOI: 10.1101/gad.8.7.830. View

16.

Mengus G, May M, Carre L, Chambon P, Davidson I . Human TAF(II)135 potentiates transcriptional activation by the AF-2s of the retinoic acid, vitamin D3, and thyroid hormone receptors in mammalian cells. Genes Dev. 1997; 11(11):1381-95. DOI: 10.1101/gad.11.11.1381. View

17.

Golas M, Sander B, Will C, Luhrmann R, Stark H . Major conformational change in the complex SF3b upon integration into the spliceosomal U11/U12 di-snRNP as revealed by electron cryomicroscopy. Mol Cell. 2005; 17(6):869-83. DOI: 10.1016/j.molcel.2005.02.016. View

18.

Hampsey M, Reinberg D . RNA polymerase II as a control panel for multiple coactivator complexes. Curr Opin Genet Dev. 1999; 9(2):132-9. DOI: 10.1016/S0959-437X(99)80020-3. View

19.

Leschziner A, Nogales E . Visualizing flexibility at molecular resolution: analysis of heterogeneity in single-particle electron microscopy reconstructions. Annu Rev Biophys Biomol Struct. 2007; 36:43-62. DOI: 10.1146/annurev.biophys.36.040306.132742. View

20.

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