Recent advances in understanding the structure and function of general transcription factor TFIID

The general transcription factor TFIID is a macromolecular complex comprising the TATA-binding protein (TBP) and a set of 13–14 TBP associated factors (TAFs). This review discusses biochemical, genetic and electron microscopic data acquired over the past years that provide a model for the composition, organisation and assembly of TFIID. We also revisit ideas on how TFIID is recruited to the promoters of active and possibly repressed genes. Recent observations show that recognition of acetylated and methylated histone residues by structural domains in several TAFs plays an important role. Finally, we highlight several genetic studies suggesting that TFIID is required for initiation of transcription, but not for maintaining transcription once a promoter is in an active state.

[1]  Andrew J. Bannister,et al.  The TAFII250 Subunit of TFIID Has Histone Acetyltransferase Activity , 1996, Cell.

[2]  Y. Sancak,et al.  Tissue-Specific TAFs Counteract Polycomb to Turn on Terminal Differentiation , 2005, Science.

[3]  T. Furukawa,et al.  Genetic Dissection of hTAFII130 Defines a Hydrophobic Surface Required for Interaction with Glutamine-rich Activators* , 1999, The Journal of Biological Chemistry.

[4]  R. Roeder,et al.  Topology and reorganization of a human TFIID–promoter complex , 1996, Nature.

[5]  T. Margaritis,et al.  Dominant and redundant functions of TFIID involved in the regulation of hepatic genes. , 2008, Molecular cell.

[6]  Matthias Mann,et al.  Selective Anchoring of TFIID to Nucleosomes by Trimethylation of Histone H3 Lysine 4 , 2007, Cell.

[7]  R. Tjian,et al.  TAF4 nucleates a core subcomplex of TFIID and mediates activated transcription from a TATA-less promoter , 2006, Proceedings of the National Academy of Sciences.

[8]  K. Garbett,et al.  Molecular Characterization of Saccharomyces cerevisiae TFIID , 2002, Molecular and Cellular Biology.

[9]  J. T. Kadonaga,et al.  The RNA polymerase II core promoter - the gateway to transcription. , 2008, Current opinion in cell biology.

[10]  Steven L. Cohen,et al.  Structural similarity between TAFs and the heterotetrameric core of the histone octamer , 1996, Nature.

[11]  L. Tora,et al.  Mapping histone fold TAFs within yeast TFIID , 2002, The EMBO journal.

[12]  Robert Tjian,et al.  Human TAFII105 Is a Cell Type–Specific TFIID Subunit Related to hTAFII130 , 1996, Cell.

[13]  N. Tanese,et al.  Isoform-specific interaction of HP1 with human TAFII130 , 2002, Proceedings of the National Academy of Sciences of the United States of America.

[14]  J. T. Kadonaga,et al.  The RNA polymerase II core promoter. , 2003, Annual review of biochemistry.

[15]  Christin E Bland,et al.  Molecular and Genetic Characterization of a Taf1p Domain Essential for Yeast TFIID Assembly , 2004, Molecular and Cellular Biology.

[16]  M. G. Koerkamp,et al.  Cooperative action of NC2 and Mot1p to regulate TATA-binding protein function across the genome. , 2008, Genes & development.

[17]  P. Chambon,et al.  Human TAF(II)135 potentiates transcriptional activation by the AF-2s of the retinoic acid, vitamin D3, and thyroid hormone receptors in mammalian cells. , 1997, Genes & development.

[18]  L. Wallrath,et al.  The Heterochromatin Protein 1 family , 2006, Genome Biology.

[19]  S. Viville,et al.  RNA Polymerase II Transcription in Murine Cells Lacking the TATA Binding Protein , 2002, Science.

[20]  R. Tjian,et al.  A Glutamine-Rich Trail Leads to Transcription Factors , 2002, Science.

[21]  C. Romier,et al.  Functional Analysis of the TFIID-specific Yeast TAF4 (yTAFII48) Reveals an Unexpected Organization of Its Histone-fold Domain* , 2002, The Journal of Biological Chemistry.

[22]  I. Kanazawa,et al.  Expanded polyglutamine stretches interact with TAFII130, interfering with CREB-dependent transcription , 2000, Nature Genetics.

[23]  Robert Tjian,et al.  Structural changes in TAF4b-TFIID correlate with promoter selectivity. , 2008, Molecular cell.

[24]  J. Workman,et al.  Diverse functions of WD40 repeat proteins in histone recognition. , 2008, Genes & development.

[25]  P. Schultz,et al.  Mapping the initiator binding Taf2 subunit in the structure of hydrated yeast TFIID. , 2009, Structure.

[26]  M. Horikoshi,et al.  Identification of TFIID components required for transcriptional activation by upstream stimulatory factor. , 1993, The Journal of biological chemistry.

[27]  R. Tjian,et al.  TAFs revisited: more data reveal new twists and confirm old ideas. , 2000, Gene.

[28]  R. Tjian,et al.  Structure and function of a human TAFII250 double bromodomain module. , 2000, Science.

[29]  D. Moras,et al.  Crystal structure, biochemical and genetic characterization of yeast and E. cuniculi TAF(II)5 N-terminal domain: implications for TFIID assembly. , 2007, Journal of molecular biology.

[30]  L. Perletti,et al.  TAF4 inactivation in embryonic fibroblasts activates TGFβ signalling and autocrine growth , 2005, The EMBO journal.

[31]  W. Pijnappel,et al.  Dubbing SAGA unveils new epigenetic crosstalk. , 2008, Molecular cell.

[32]  L. Tora.  A unified nomenclature for TATA box binding protein (TBP)-associated factors (TAFs) involved in RNA polymerase II transcription. , 2002, Genes & development.

[33]  L. Kay,et al.  Solution Structure of a TBP–TAFII230 Complex Protein Mimicry of the Minor Groove Surface of the TATA Box Unwound by TBP , 1998, Cell.

[34]  M. Montminy,et al.  Chromatin-Dependent Cooperativity between Constitutive and Inducible Activation Domains in CREB , 2001, Molecular and Cellular Biology.

[35]  D. Page,et al.  Functional substitution for TAF(II)250 by a retroposed homolog that is expressed in human spermatogenesis. , 2002, Human molecular genetics.

[36]  Paolo Sassone-Corsi,et al.  The intracellular localisation of TAF7L, a paralogue of transcription factor TFIID subunit TAF7, is developmentally regulated during male germ-cell differentiation , 2003, Journal of Cell Science.

[37]  P. Chambon,et al.  Distinct TFIID complexes mediate the effect of different transcriptional activators. , 1993, The EMBO journal.

[38]  T. Oelgeschläger,et al.  Association of human TFIID–promoter complexes with silenced mitotic chromatin in vivo , 2002, Nature Cell Biology.

[39]  D. Metzger,et al.  TAF10 (TAFII30) Is Necessary for TFIID Stability and Early Embryogenesis in Mice , 2003, Molecular and Cellular Biology.

[40]  P. Grant,et al.  The SAGA continues: expanding the cellular role of a transcriptional co-activator complex , 2007, Oncogene.

[41]  S. Smale,et al.  Direct recognition of initiator elements by a component of the transcription factor IID complex. , 1994, Genes & development.

[42]  D. Singer,et al.  TAF7: a possible transcription initiation check-point regulator. , 2006, Proceedings of the National Academy of Sciences of the United States of America.

[43]  V. Rybin,et al.  The FACT Spt16 “peptidase” domain is a histone H3–H4 binding module , 2008, Proceedings of the National Academy of Sciences.

[44]  Rolf Boelens,et al.  Structural insight into the recognition of the H3K4me3 mark by the TFIID subunit TAF3. , 2008, Structure.

[45]  M. Brand,et al.  Three-dimensional structures of the TAFII-containing complexes TFIID and TFTC. , 1999, Science.

[46]  Michael R. Green,et al.  Yeast TAF IIS in a multisubunit complex required for activated transcription , 1994, Nature.

[47]  D. Moras,et al.  Crystal Structure of a Subcomplex of Human Transcription Factor TFIID Formed by TATA Binding Protein-associated Factors hTAF4 (hTAFII135) and hTAF12 (hTAFII20)* , 2002, The Journal of Biological Chemistry.

[48]  S K Burley,et al.  Biochemistry and structural biology of transcription factor IID (TFIID). , 1996, Annual review of biochemistry.

[49]  Martin S. Taylor,et al.  Genome-wide analysis of mammalian promoter architecture and evolution , 2006, Nature Genetics.

[50]  C. Verrijzer,et al.  DNA binding site selection by RNA polymerase II TAFs: a TAFII250–TAFII150 complex recognizes the Initiator , 1999, The EMBO journal.

[51]  Steven Hahn,et al.  Targets of the Gal4 Transcription Activator in Functional Transcription Complexes , 2005, Molecular and Cellular Biology.

[52]  Michael R. Green,et al.  Yeast TAFII145 Functions as a Core Promoter Selectivity Factor, Not a General Coactivator , 1997, Cell.

[53]  Jerry L. Workman,et al.  Crosstalk among Histone Modifications , 2008, Cell.

[54]  R. Lin,et al.  Global Transcriptional Repression in C. elegans Germline Precursors by Regulated Sequestration of TAF-4 , 2008, Cell.

[55]  Fang Yang,et al.  An abundance of X-linked genes expressed in spermatogonia , 2001, Nature Genetics.

[56]  Sean D. Taverna,et al.  How chromatin-binding modules interpret histone modifications: lessons from professional pocket pickers , 2007, Nature Structural &Molecular Biology.

[57]  R. Tjian,et al.  A glutamine-rich hydrophobic patch in transcription factor Sp1 contacts the dTAFII110 component of the Drosophila TFIID complex and mediates transcriptional activation. , 1994, Proceedings of the National Academy of Sciences of the United States of America.

[58]  D. Ledbetter,et al.  Complete cDNA sequence and chromosomal localization of mouse α1-antitrypsin , 1990 .

[59]  D. Poon,et al.  Immunopurification of yeast TATA-binding protein and associated factors. Presence of transcription factor IIIB transcriptional activity. , 1993, The Journal of biological chemistry.

[60]  Karine Prat,et al.  Prediction of the general transcription factors associated with RNA polymerase II in Plasmodium falciparum: conserved features and differences relative to other eukaryotes , 2005, BMC Genomics.

[61]  Steven Hahn,et al.  A transcription reinitiation intermediate that is stabilized by activator , 2000, Nature.

[62]  D. Metzger,et al.  Mammalian TAFII30 is required for cell cycle progression and specific cellular differentiation programmes , 1999, The EMBO journal.

[63]  I. Davidson.  The genetics of TBP and TBP-related factors. , 2003, Trends in biochemical sciences.

[64]  S. Takada,et al.  Structural analysis and dimerization potential of the human TAF5 subunit of TFIID , 2007, Proceedings of the National Academy of Sciences.

[65]  D. Singer,et al.  TAFII55 binding to TAFII250 inhibits its acetyltransferase activity , 2001, Proceedings of the National Academy of Sciences of the United States of America.

[66]  M. Brand,et al.  The TFIID Components Human TAFII140 andDrosophila BIP2 (TAFII155) Are Novel Metazoan Homologues of Yeast TAFII47 Containing a Histone Fold and a PHD Finger , 2001, Molecular and Cellular Biology.

[67]  Nathan L. Vanderford,et al.  The TBP–PP2A mitotic complex bookmarks genes by preventing condensin action , 2008, Nature Cell Biology.

[68]  J. Reese,et al.  Analysis of TAF90 Mutants Displaying Allele-Specific and Broad Defects in Transcription , 2001, Molecular and Cellular Biology.

[69]  Boris Lenhard,et al.  Mammalian RNA polymerase II core promoters: insights from genome-wide studies , 2007, Nature Reviews Genetics.

[70]  D. Metzger,et al.  TAF10 is required for the establishment of skin barrier function in foetal, but not in adult mouse epidermis. , 2005, Developmental biology.

[71]  Yeast homologues of higher eukaryotic TFIID subunits , 1996 .

[72]  J. Workman,et al.  The heterochromatin protein 1 (HP1) family: put away a bias toward HP1. , 2008, Molecules and cells.

[73]  D. Moras,et al.  Human TAFII28 and TAFII18 Interact through a Histone Fold Encoded by Atypical Evolutionary Conserved Motifs Also Found in the SPT3 Family , 1998, Cell.

[74]  C. Romier,et al.  The histone fold is a key structural motif of transcription factor TFIID. , 2001, Trends in biochemical sciences.

[75]  P. Lijnzaad,et al.  Genome-wide location of the coactivator mediator: Binding without activation and transient Cdk8 interaction on DNA. , 2006, Molecular cell.

[76]  R. Tjian,et al.  Isolation of coactivators associated with the TATA-binding protein that mediate transcriptional activation , 1991, Cell.

[77]  Pawel A Penczek,et al.  Cryo-electron microscopy studies of human TFIID: conformational breathing in the integration of gene regulatory cues. , 2006, Structure.

[78]  L. Tora,et al.  Mapping key functional sites within yeast TFIID , 2004, The EMBO journal.

[79]  D. Singer,et al.  TFIID component TAF7 functionally interacts with both TFIIH and P-TEFb , 2008, Proceedings of the National Academy of Sciences.

[80]  S. Burley.  The TATA box binding protein. , 1996, Current opinion in structural biology.

[81]  K. Garbett,et al.  Yeast TFIID Serves as a Coactivator for Rap1p by Direct Protein-Protein Interaction , 2006, Molecular and Cellular Biology.

[82]  R. Tjian,et al.  Assembly of recombinant TFIID reveals differential coactivator requirements for distinct transcriptional activators , 1994, Cell.

[83]  James T Kadonaga,et al.  The DPE, a core promoter element for transcription by RNA polymerase II , 2002, Experimental & Molecular Medicine.

[84]  Martin T. Suchorolski,et al.  Testis-specific TAF homologs collaborate to control a tissue-specific transcription program , 2004, Development.

[85]  R. Roeder,et al.  Positive and Negative TAFII Functions That Suggest a Dynamic TFIID Structure and Elicit Synergy with TRAPs in Activator-Induced Transcription , 2001, Molecular and Cellular Biology.

[86]  Làszlò Tora,et al.  SAGA unveiled. , 2005, Trends in biochemical sciences.

[87]  R. Tjian,et al.  Three-dimensional structure of the human TFIID-IIA-IIB complex. , 1999, Science.

[88]  S. Buratowski,et al.  Structure and function of the TFIID complex. , 2004, Advances in protein chemistry.

[89]  Yang Shi,et al.  Distinct requirements for C.elegans TAFIIs in early embryonic transcription , 2001, The EMBO journal.

[90]  Ting-Yi Lin,et al.  Developmental regulation of transcription by a tissue-specific TAF homolog. , 2001, Genes & development.

[91]  C. Chiang,et al.  The General Transcription Machinery and General Cofactors , 2006, Critical reviews in biochemistry and molecular biology.