Abstract
Activator-dependent recruitment of TFIID initiates formation of the transcriptional preinitiation complex. TFIID binds core promoter DNA elements and directs the assembly of other general transcription factors, leading to binding of RNA polymerase II and activation of RNA synthesis. How TATA box-binding protein (TBP) and the TBP-associated factors (TAFs) are assembled into a functional TFIID complex with promoter recognition and coactivator activities in vivo remains unknown. Here, we use RNAi to knock down specific TFIID subunits in Drosophila tissue culture cells to determine which subunits are most critical for maintaining stability of TFIID in vivo. Contrary to expectations, we find that TAF4 rather than TBP or TAF1 plays the most critical role in maintaining stability of the complex. Our analysis also indicates that TAF5, TAF6, TAF9, and TAF12 play key roles in stability of the complex, whereas TBP, TAF1, TAF2, and TAF11 contribute very little to complex stability. Based on our results, we propose that holo-TFIID comprises a stable core subcomplex containing TAF4, TAF5, TAF6, TAF9, and TAF12 decorated with peripheral subunits TAF1, TAF2, TAF11, and TBP. Our initial functional studies indicate a specific and significant role for TAF1 and TAF4 in mediating transcription from a TATA-less, downstream core promoter element (DPE)-containing promoter, whereas a TATA-containing, DPE-less promoter was far less dependent on these subunits. In contrast to both TAF1 and TAF4, RNAi knockdown of TAF5 had little effect on transcription from either class of promoter. These studies significantly alter previous models for the assembly, structure, and function of TFIID.
MeSH Terms
Animals
Cell Line
Drosophila Proteins/genetics,metabolism
Drosophila melanogaster/physiology
Enzyme Stability
Gene Expression Regulation
Humans
Macromolecular Substances
Models, Molecular
Protein Subunits/genetics,metabolism
RNA Interference
TATA Box
TATA-Binding Protein Associated Factors/genetics,metabolism
Transcription Factor TFIID/genetics,metabolism
Transcription, Genetic
Chemicals
Drosophila Proteins
Macromolecular Substances
Protein Subunits
TATA-Binding Protein Associated Factors
Taf4 protein, Drosophila
Transcription Factor TFIID
Authors & Affiliations
3 authors, click to expand affiliations / ORCID
Wright Kevin J
Department of Molecular and Cell Biology and Howard Hughes Medical Institute, University of California, Berkeley, 16 Barker Hall, CA 94720, USA.
Marr Michael T
Tjian Robert
References (29)
29 references, click to expand
-
Developmental regulation of transcription by a tissue-specific TAF homolog.
Genes Dev. 2001 Apr 15;15(8):1021-30
PMID: 11316795
-
Region of yeast TAF 130 required for TFIID to associate with promoters.
Mol Cell Biol. 2001 Feb;21(4):1145-54
PMID: 11158301
-
RNA interference of gene expression (RNAi) in cultured Drosophila cells.
Sci STKE. 2001 Aug 14;2001(95):pl1
PMID: 11752672
-
Molecular characterization of Saccharomyces cerevisiae TFIID.
Mol Cell Biol. 2002 Aug;22(16):6000-13
PMID: 12138208
-
Two Drosophila Ada2 homologues function in different multiprotein complexes.
Mol Cell Biol. 2003 May;23(9):3305-19
PMID: 12697829
-
Mapping key functional sites within yeast TFIID.
EMBO J. 2004 Feb 25;23(4):719-27
PMID: 14765106
-
Identification and distinct regulation of yeast TATA box-containing genes.
Cell. 2004 Mar 5;116(5):699-709
PMID: 15006352
-
Testis-specific TAF homologs collaborate to control a tissue-specific transcription program.
Development. 2004 Nov;131(21):5297-308
PMID: 15456720
-
The TATA-binding protein and associated factors are integral components of the RNA polymerase I transcription factor, SL1.
Cell. 1992 Mar 6;68(5):965-76
PMID: 1547496
-
Molecular cloning and functional analysis of Drosophila TAF110 reveal properties expected of coactivators.
Cell. 1993 Jan 29;72(2):247-60
PMID: 7678780
-
Largest subunit of Drosophila transcription factor IID directs assembly of a complex containing TBP and a coactivator.
Nature. 1993 Apr 8;362(6420):511-7
PMID: 8464492
-
The dTAFII80 subunit of Drosophila TFIID contains beta-transducin repeats.
Nature. 1993 May 13;363(6425):176-9
PMID: 8483503
-
Drosophila TAFII40 interacts with both a VP16 activation domain and the basal transcription factor TFIIB.
Cell. 1993 Nov 5;75(3):519-30
PMID: 8221891
-
Drosophila TAFII150: similarity to yeast gene TSM-1 and specific binding to core promoter DNA.
Science. 1994 May 13;264(5161):933-41
PMID: 8178153
-
Structure and function of transcriptional activation domains.
Curr Opin Genet Dev. 1995 Apr;5(2):190-6
PMID: 7613088
-
Human TAFII 105 is a cell type-specific TFIID subunit related to hTAFII130.
Cell. 1996 Oct 4;87(1):137-46
PMID: 8858156
-
Molecular cloning and analysis of two subunits of the human TFIID complex: hTAFII130 and hTAFII100.
Proc Natl Acad Sci U S A. 1996 Nov 26;93(24):13611-6
PMID: 8942982
-
The downstream core promoter element, DPE, is conserved from Drosophila to humans and is recognized by TAFII60 of Drosophila.
Genes Dev. 1997 Nov 15;11(22):3020-31
PMID: 9367984
-
Function of TAF(II)-containing complex without TBP in transcription by RNA polymerase II.
Nature. 1998 May 14;393(6681):187-91
PMID: 9603525
-
Histone-like TAFs within the PCAF histone acetylase complex.
Cell. 1998 Jul 10;94(1):35-44
PMID: 9674425
-
A subset of TAF(II)s are integral components of the SAGA complex required for nucleosome acetylation and transcriptional stimulation.
Cell. 1998 Jul 10;94(1):45-53
PMID: 9674426
-
Coactivator cross-talk specifies transcriptional output.
Genes Dev. 2006 Jun 1;20(11):1458-69
PMID: 16751183
-
Three-dimensional structures of the TAFII-containing complexes TFIID and TFTC.
Science. 1999 Dec 10;286(5447):2151-3
PMID: 10591645
-
Three-dimensional structure of the human TFIID-IIA-IIB complex.
Science. 1999 Dec 10;286(5447):2153-6
PMID: 10591646
-
TAFs revisited: more data reveal new twists and confirm old ideas.
Gene. 2000 Jan 25;242(1-2):1-13
PMID: 10721692
-
A TRF1:BRF complex directs Drosophila RNA polymerase III transcription.
Cell. 2000 May 26;101(5):459-69
PMID: 10850489
-
Assembly of partial TFIID complexes in mammalian cells reveals distinct activities associated with individual TATA box-binding protein-associated factors.
J Biol Chem. 2000 Sep 22;275(38):29847-56
PMID: 10896937
-
Orchestrated response: a symphony of transcription factors for gene control.
Genes Dev. 2000 Oct 15;14(20):2551-69
PMID: 11040209
-
Enhancer-promoter specificity mediated by DPE or TATA core promoter motifs.
Genes Dev. 2001 Oct 1;15(19):2515-9
PMID: 11581157