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PMID: 12370284 Published · ppublish English Journal Article Research Support, U.S. Gov't, P.H.S.

Differential requirement of SAGA components for recruitment of TATA-box-binding protein to promoters in vivo.

Molecular and cellular biology ·Vol. 22 ·No. 21 ·2002-11-00 ·Pages 7365-71

Bhaumik SR, Green MR

Abstract

The multisubunit Saccharomyces cerevisiae SAGA (Spt-Ada-Gcn5-acetyltransferase) complex is required to activate transcription of a subset of RNA polymerase II-dependent genes. However, the contribution of each SAGA component to transcription activation is relatively unknown. Here, using a formaldehyde-based in vivo cross-linking and chromatin immunoprecipitation assay, we have systematically analyzed the role of SAGA components in the recruitment of TATA-box binding protein (TBP) to SAGA-dependent promoters. We show that recruitment of TBP is diminished at a number of SAGA-dependent promoters in ada1delta, spt7delta, and spt20delta null mutants, consistent with previous biochemical data suggesting that these components maintain the integrity of the SAGA complex. We also find that Spt3p is generally required for TBP binding to SAGA-dependent promoters, consistent with biochemical and genetic experiments, suggesting that Spt3p interacts with and recruits TBP to the core promoter. By contrast, Spt8p, which has been proposed to be required for the interaction between Spt3p and TBP, is required for TBP binding at only a subset of SAGA-dependent promoters. Ada2p and Ada3p are both required for TBP recruitment to Gcn5p-dependent promoters, supporting previous biochemical data that Ada2p and Ada3p are required for the histone acetyltransferase activity of Gcn5p. Finally, our results suggest that TBP-associated-factor components of SAGA are differentially required for TBP binding to SAGA-dependent promoters. In summary, we show that SAGA-dependent promoters require different combinations of SAGA components for TBP recruitment, revealing a complex combinatorial network for transcription activation in vivo.

MeSH Terms
Acetyltransferases/metabolism Adaptor Proteins, Signal Transducing Chromatin/genetics,metabolism DNA-Binding Proteins/genetics,metabolism,physiology Dose-Response Relationship, Drug Formaldehyde/pharmacology Fungal Proteins/genetics,metabolism,physiology Gene Expression Regulation, Fungal Genes, Fungal Histone Acetyltransferases Mutation Polymerase Chain Reaction Precipitin Tests Promoter Regions, Genetic Protein Binding Protein Kinases Saccharomyces cerevisiae/genetics,metabolism Saccharomyces cerevisiae Proteins/physiology TATA-Box Binding Protein Temperature Time Factors Trans-Activators/physiology Transcription Factors/genetics,metabolism,physiology Transcription, Genetic Transcriptional Activation
Chemicals
ADA2 protein, S cerevisiae Adaptor Proteins, Signal Transducing Chromatin DNA-Binding Proteins Fungal Proteins HFI1 protein, S cerevisiae NGG1 protein, S cerevisiae SPT20 protein, S cerevisiae SPT3 protein, S cerevisiae SPT7 protein, S cerevisiae SPT8 protein, S cerevisiae Saccharomyces cerevisiae Proteins TATA-Box Binding Protein Trans-Activators Transcription Factors Formaldehyde Acetyltransferases GCN5 protein, S cerevisiae Histone Acetyltransferases Protein Kinases
Authors & Affiliations
2 authors, click to expand affiliations / ORCID
Bhaumik Sukesh R
Howard Hughes Medical Institute, Programs in Gene Expression and Function and Molecular Medicine, University of Massachusetts Medical School, Worcester, Massachusetts 01605, USA.
Green Michael R
References (41)
41 references, click to expand
  1. The Spt components of SAGA facilitate TBP binding to a promoter at a post-activator-binding step in vivo.
    Genes Dev. 1999 Nov 15;13(22):2940-5 PMID: 10580001
  2. The SAGA of Spt proteins and transcriptional analysis in yeast: past, present, and future.
    Cold Spring Harb Symp Quant Biol. 1998;63:553-61 PMID: 10384320
  3. Inhibition of TATA-binding protein function by SAGA subunits Spt3 and Spt8 at Gcn4-activated promoters.
    Mol Cell Biol. 2000 Jan;20(2):634-47 PMID: 10611242
  4. The many HATs of transcription coactivators.
    Trends Biochem Sci. 2000 Jan;25(1):15-9 PMID: 10637607
  5. TBP-associated factors (TAFIIs): multiple, selective transcriptional mediators in common complexes.
    Trends Biochem Sci. 2000 Feb;25(2):59-63 PMID: 10664584
  6. TAFs revisited: more data reveal new twists and confirm old ideas.
    Gene. 2000 Jan 25;242(1-2):1-13 PMID: 10721692
  7. Distinct classes of yeast promoters revealed by differential TAF recruitment.
    Science. 2000 May 19;288(5469):1242-4 PMID: 10817999
  8. TAF-Containing and TAF-independent forms of transcriptionally active TBP in vivo.
    Science. 2000 May 19;288(5469):1244-8 PMID: 10818000
  9. Redundant roles for the TFIID and SAGA complexes in global transcription.
    Nature. 2000 Jun 8;405(6787):701-4 PMID: 10864329
  10. Recruitment of HAT complexes by direct activator interactions with the ATM-related Tra1 subunit.
    Science. 2001 Jun 22;292(5525):2333-7 PMID: 11423663
  11. SAGA is an essential in vivo target of the yeast acidic activator Gal4p.
    Genes Dev. 2001 Aug 1;15(15):1935-45 PMID: 11485988
  12. The S. cerevisiae SAGA complex functions in vivo as a coactivator for transcriptional activation by Gal4.
    Genes Dev. 2001 Aug 1;15(15):1946-56 PMID: 11485989
  13. Histone acetyltransferases.
    Annu Rev Biochem. 2001;70:81-120 PMID: 11395403
  14. Role of the Ada2 and Ada3 transcriptional coactivators in histone acetylation.
    J Biol Chem. 2002 Mar 8;277(10):7989-95 PMID: 11773077
  15. Distinct mutations in yeast TAF(II)25 differentially affect the composition of TFIID and SAGA complexes as well as global gene expression patterns.
    Mol Cell Biol. 2002 May;22(9):3178-93 PMID: 11940675
  16. A unified nomenclature for TATA box binding protein (TBP)-associated factors (TAFs) involved in RNA polymerase II transcription.
    Genes Dev. 2002 Mar 15;16(6):673-5 PMID: 11963920
  17. Promoter specificity of basal transcription factors.
    Cell. 1992 Mar 20;68(6):1135-44 PMID: 1547507
  18. SPT3 interacts with TFIID to allow normal transcription in Saccharomyces cerevisiae.
    Genes Dev. 1992 Jul;6(7):1319-31 PMID: 1628834
  19. Genetic isolation of ADA2: a potential transcriptional adaptor required for function of certain acidic activation domains.
    Cell. 1992 Jul 24;70(2):251-65 PMID: 1638630
  20. The Saccharomyces cerevisiae SPT8 gene encodes a very acidic protein that is functionally related to SPT3 and TATA-binding protein.
    Genetics. 1994 Jul;137(3):647-57 PMID: 8088510
  21. Functional similarity and physical association between GCN5 and ADA2: putative transcriptional adaptors.
    EMBO J. 1994 Oct 17;13(20):4807-15 PMID: 7957049
  22. ADA3, a putative transcriptional adaptor, consists of two separable domains and interacts with ADA2 and GCN5 in a trimeric complex.
    Mol Cell Biol. 1995 Mar;15(3):1203-9 PMID: 7862114
  23. Tetrahymena histone acetyltransferase A: a homolog to yeast Gcn5p linking histone acetylation to gene activation.
    Cell. 1996 Mar 22;84(6):843-51 PMID: 8601308
  24. Structural and functional analysis of yeast putative adaptors. Evidence for an adaptor complex in vivo.
    J Biol Chem. 1996 Mar 1;271(9):5237-45 PMID: 8617808
  25. SPT20/ADA5 encodes a novel protein functionally related to the TATA-binding protein and important for transcription in Saccharomyces cerevisiae.
    Mol Cell Biol. 1996 Jun;16(6):3206-13 PMID: 8649431
  26. Histone acetyltransferase activity and interaction with ADA2 are critical for GCN5 function in vivo.
    EMBO J. 1997 Feb 3;16(3):555-65 PMID: 9034338
  27. ADA1, a novel component of the ADA/GCN5 complex, has broader effects than GCN5, ADA2, or ADA3.
    Mol Cell Biol. 1997 Jun;17(6):3220-8 PMID: 9154821
  28. Yeast Gcn5 functions in two multisubunit complexes to acetylate nucleosomal histones: characterization of an Ada complex and the SAGA (Spt/Ada) complex.
    Genes Dev. 1997 Jul 1;11(13):1640-50 PMID: 9224714
  29. Essential functional interactions of SAGA, a Saccharomyces cerevisiae complex of Spt, Ada, and Gcn5 proteins, with the Snf/Swi and Srb/mediator complexes.
    Genetics. 1997 Oct;147(2):451-65 PMID: 9335585
  30. A SAGA of histone acetylation and gene expression.
    Trends Genet. 1997 Nov;13(11):427-9 PMID: 9385836
  31. Critical residues for histone acetylation by Gcn5, functioning in Ada and SAGA complexes, are also required for transcriptional function in vivo.
    Genes Dev. 1998 Mar 1;12(5):640-53 PMID: 9499400
  32. Identification and analysis of homologues of Saccharomyces cerevisiae Spt3 suggest conserved functional domains.
    Yeast. 1998 Mar 30;14(5):409-17 PMID: 9559549
  33. Regulation of gene expression by TBP-associated proteins.
    Genes Dev. 1998 May 15;12(10):1398-408 PMID: 9585500
  34. 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
  35. The SAGA unfolds: convergence of transcription regulators in chromatin-modifying complexes.
    Trends Cell Biol. 1998 May;8(5):193-7 PMID: 9695838
  36. Characterization of a human homologue of the Saccharomyces cerevisiae transcription factor spt3 (SUPT3H).
    Genomics. 1998 Oct 1;53(1):90-6 PMID: 9787080
  37. Broad, but not universal, transcriptional requirement for yTAFII17, a histone H3-like TAFII present in TFIID and SAGA.
    Mol Cell. 1998 Nov;2(5):653-61 PMID: 9844637
  38. Histone-like TAFs are essential for transcription in vivo.
    Mol Cell. 1998 Nov;2(5):663-73 PMID: 9844638
  39. yTAFII61 has a general role in RNA polymerase II transcription and is required by Gcn4p to recruit the SAGA coactivator complex.
    Mol Cell. 1998 Nov;2(5):683-92 PMID: 9844640
  40. Functional organization of the yeast SAGA complex: distinct components involved in structural integrity, nucleosome acetylation, and TATA-binding protein interaction.
    Mol Cell Biol. 1999 Jan;19(1):86-98 PMID: 9858534
  41. Transcriptional activation in yeast cells lacking transcription factor IIA.
    Genetics. 1999 Dec;153(4):1573-81 PMID: 10581267
Article Info
Journal
Molecular and cellular biology
Abbr.
Mol Cell Biol
ISSN
0270-7306
Published
2002-11-00
Pages
7365-71
Language
English
Region
United States
NLM ID
8109087
PMCID
PMC135674
Subset
IM
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