DNA binding site selection by RNA polymerase II TAFs: a TAFII250–TAFII150 complex recognizes the Initiator

Basal transcription factor TFIID comprises the TATA‐box‐binding protein, TBP, and associated factors, the TAFIIs. Previous studies have implicated TAFII250 and TAFII150 in core promoter selectivity of RNA polymerase II. Here, we have used a random DNA binding site selection procedure to identify target sequences for these TAFs. Individually, neither TAFII250 nor TAFII150 singles out a clearly constrained DNA sequence. However, a TAFII250–TAFII150 complex selects sequences that match the Initiator (Inr) consensus. When in a trimeric complex with TBP, these TAFs select Inr sequences at the appropriate distance from the TATA‐box. Point mutations that inhibit binding of the TAFII250–TAFII150 complex also impair Inr function in reconstituted basal transcription reactions, underscoring the functional relevance of Inr recognition by TAFs. Surprisingly, the precise DNA sequence at the start site of transcription influences transcriptional regulation by the upstream activator Sp1. Finally, we found that TAFII150 specifically binds to four‐way junction DNA, suggesting that promoter binding by TFIID may involve recognition of DNA structure as well as primary sequence. Taken together, our results establish that TAFII250 and TAFII150 bind the Inr directly and that Inr recognition can determine the responsiveness of a promoter to an activator

[1]  R. Tjian,et al.  Binding of TAFs to core elements directs promoter selectivity by RNA polymerase II , 1995, Cell.

[2]  John J. Cullen,et al.  Interactive effects of ozone depletion and vertical mixing on photosynthesis of Antarctic phytoplankton , 1998, Nature.

[3]  R. Dikstein,et al.  TAFII105 mediates activation of anti‐apoptotic genes by NF‐κB , 1998 .

[4]  Winship Herr,et al.  Basal promoter elements as a selective determinant of transcriptional activator function , 1995, Nature.

[5]  T Lagrange,et al.  The general transcription factors of RNA polymerase II. , 1996, Genes & development.

[6]  R. Roeder,et al.  Interaction of a gene-specific transcription factor with the adenovirus major late promoter upstream of the TATA box region , 1985, Cell.

[7]  S. Jackson,et al.  Sequence-specific DNA binding by the S. shibatae TFIIB homolog, TFB, and its effect on promoter strength. , 1998, Molecular cell.

[8]  X. Jacq,et al.  Human TAFII30 is present in a distinct TFIID complex and is required for transcriptional activation by the estrogen receptor , 1994, Cell.

[9]  S. Smale,et al.  Transcription initiation from TATA-less promoters within eukaryotic protein-coding genes. , 1997, Biochimica et biophysica acta.

[10]  R. Roeder,et al.  TATA‐binding protein‐associated factor(s) in TFIID function through the initiator to direct basal transcription from a TATA‐less class II promoter. , 1994, The EMBO journal.

[11]  M. Horikoshi,et al.  A downstream initiation element required for efficient TATA box binding and in vitro function of TFIID , 1990, Nature.

[12]  R. Tjian,et al.  Reconstitution of TATA-binding protein-associated factor/TATA-binding protein complexes for in vitro transcription. , 1996, Methods in enzymology.

[13]  S. Hahn.  The Role of TAFs in RNA Polymerase II Transcription , 1998, Cell.

[14]  A. Hoffmann,et al.  Considerations of transcriptional control mechanisms: do TFIID-core promoter complexes recapitulate nucleosome-like functions? , 1997, Proceedings of the National Academy of Sciences of the United States of America.

[15]  M. Brand,et al.  Function of TAFII-containing complex without TBP in transcription by RNA polymerase II , 1998, Nature.

[16]  M. Horikoshi,et al.  Drosophila 230-kD TFIID subunit, a functional homolog of the human cell cycle gene product, negatively regulates DNA binding of the TATA box-binding subunit of TFIID. , 1993, Genes & development.

[17]  S. Smale,et al.  CIF150, a Human Cofactor for Transcription Factor IID-Dependent Initiator Function , 1998, Molecular and Cellular Biology.

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

[19]  J. Thorner,et al.  Mot1, a global repressor of RNA polymerase II transcription, inhibits TBP binding to DNA by an ATP-dependent mechanism. , 1994, Genes & development.

[20]  D. Landsman,et al.  AT-hook motifs identified in a wide variety of DNA-binding proteins. , 1998, Nucleic acids research.

[21]  Qiang Zhou,et al.  Holo-TFIID supports transcriptional stimulation by diverse activators and from a TATA-less promoter. , 1992, Genes & development.

[22]  Masami Horikoshi,et al.  Transcription factor ATF interacts with the TATA factor to facilitate establishment of a preinitiation complex , 1988, Cell.

[23]  Robert Tjian,et al.  Transcription Properties of a Cell Type–Specific TATA-Binding Protein, TRF , 1997, Cell.

[24]  T Lagrange,et al.  New core promoter element in RNA polymerase II-dependent transcription: sequence-specific DNA binding by transcription factor IIB. , 1998, Genes & development.

[25]  J. Wang,et al.  Initiator sequences direct downstream promoter binding by human transcription factor IID. , 1993, Biochimica et biophysica acta.

[26]  D. Gilmour,et al.  Protein/DNA crosslinking of a TFIID complex reveals novel interactions downstream of the transcription start. , 1994, Nucleic acids research.

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

[28]  R. Tjian,et al.  TAFs and TFIIA mediate differential utilization of the tandem Adh promoters , 1995, Cell.

[29]  P. Emanuel,et al.  Transcription factor TFIID recognizes DNA sequences downstream of the TATA element in the Hsp70 heat shock gene. , 1993, Proceedings of the National Academy of Sciences of the United States of America.

[30]  R. Young,et al.  Regulation of gene expression by TBP-associated proteins. , 1998, Genes & development.

[31]  I. Arkhipova,et al.  Promoter elements in Drosophila melanogaster revealed by sequence analysis. , 1995, Genetics.

[32]  R. Conaway,et al.  Role of core promoter structure in assembly of the RNA polymerase II preinitiation complex. A common pathway for formation of preinitiation intermediates at many TATA and TATA-less promoters. , 1994, The Journal of biological chemistry.

[33]  M. Bianchi,et al.  Interaction of a protein from rat liver nuclei with cruciform DNA. , 1988, The EMBO journal.

[34]  S. Smale,et al.  Core promoter specificities of the Sp1 and VP16 transcriptional activation domains , 1995, Molecular and cellular biology.

[35]  M. Levine,et al.  Different core promoters possess distinct regulatory activities in the Drosophila embryo. , 1998, Genes & development.

[36]  D. Baltimore,et al.  The “initiator” as a transcription control element , 1989, Cell.

[37]  D. Reinberg,et al.  Accurate positioning of RNA polymerase II on a natural TATA-less promoter is independent of TATA-binding-protein-associated factors and initiator-binding proteins , 1997, Molecular and cellular biology.

[38]  R. Roeder,et al.  Novel Cofactors and TFIIA Mediate Functional Core Promoter Selectivity by the Human TAFII150-Containing TFIID Complex , 1998, Molecular and Cellular Biology.

[39]  C. Verrijzer,et al.  CIF, an essential cofactor for TFIID-dependent initiator function. , 1996, Genes & development.

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

[41]  Michael Hampsey,et al.  Molecular Genetics of the RNA Polymerase II General Transcriptional Machinery , 1998, Microbiology and Molecular Biology Reviews.

[42]  T. Burke,et al.  Drosophila TFIID binds to a conserved downstream basal promoter element that is present in many TATA-box-deficient promoters. , 1996, Genes & development.

[43]  S. Elgin,et al.  UV cross-linking identifies four polypeptides that require the TATA box to bind to the Drosophila hsp70 promoter , 1990, Molecular and cellular biology.

[44]  Jeffrey A. Lefstin,et al.  Allosteric effects of DNA on transcriptional regulators , 1998, Nature.

[45]  R. Tjian,et al.  TAFs mediate transcriptional activation and promoter selectivity. , 1996, Trends in biochemical sciences.

[46]  R. Roeder,et al.  The role of general initiation factors in transcription by RNA polymerase II. , 1996, Trends in biochemical sciences.

[47]  D. Reinberg,et al.  Transcription: Why are TAFs essential? , 1997, Current Biology.

[48]  R. Tjian,et al.  An interplay between TATA box-binding protein and transcription factors IIE and IIA modulates DNA binding and transcription. , 1998, Proceedings of the National Academy of Sciences of the United States of America.

[49]  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.

[50]  R. Treisman,et al.  A sensitive method for the determination of protein-DNA binding specificities. , 1990, Nucleic acids research.

[51]  M. Biggin,et al.  Purification of the Drosophila RNA polymerase II general transcription factors. , 1996, Proceedings of the National Academy of Sciences of the United States of America.

[52]  J. Sambrook,et al.  Molecular Cloning: A Laboratory Manual , 2001 .

[53]  J. T. Kadonaga.  Assembly and disassembly of the Drosophila RNA polymerase II complex during transcription. , 1990, The Journal of biological chemistry.

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

[55]  R. Tjian,et al.  Drosophila TAFII150: similarity to yeast gene TSM-1 and specific binding to core promoter DNA. , 1994, Science.

[56]  T. Burke,et al.  The downstream core promoter element, DPE, is conserved from Drosophila to humans and is recognized by TAFII60 of Drosophila. , 1997, Genes & development.

[57]  F. Robert,et al.  Wrapping of promoter DNA around the RNA polymerase II initiation complex induced by TFIIF. , 1998, Molecular cell.

[58]  N. Hernandez,et al.  TBP, a universal eukaryotic transcription factor? , 1993, Genes & development.

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

[60]  D. Reinberg,et al.  The initiator directs the assembly of a transcription factor IID-dependent transcription complex. , 1991, Proceedings of the National Academy of Sciences of the United States of America.

[61]  P. Emanuel,et al.  TFIID sequence recognition of the initiator and sequences farther downstream in Drosophila class II genes. , 1994, Genes & development.

[62]  R. Tjian,et al.  TAFII250-dependent transcription of cyclin A is directed by ATF activator proteins. , 1997, Genes & development.

[63]  S. Burley,et al.  TATA Box Mimicry by TFIID Autoinhibition of Pol II Transcription , 1998, Cell.

[64]  R. Roeder,et al.  Core promoter-specific function of a mutant transcription factor TFIID defective in TATA-box binding. , 1995, Proceedings of the National Academy of Sciences of the United States of America.

[65]  Robert Tjian,et al.  The transcriptional cofactor complex CRSP is required for activity of the enhancer-binding protein Sp1 , 1999, Nature.

[66]  Maria Raquel Aires-Barros,et al.  Purification of a , 1999 .

[67]  S. Smale,et al.  Mechanism of synergy between TATA and initiator: synergistic binding of TFIID following a putative TFIIA-induced isomerization. , 1997, Genes & development.

[68]  M. Carey,et al.  Assembly of the isomerized TFIIA--TFIID--TATA ternary complex is necessary and sufficient for gene activation. , 1996, Genes & development.

[69]  R. Gentz,et al.  Cloning of the cDNA for the TATA-binding protein-associated factorII170 subunit of transcription factor B-TFIID reveals homology to global transcription regulators in yeast and Drosophila. , 1997, Proceedings of the National Academy of Sciences of the United States of America.