Home LiteratureArticle Details
PMID: 15831453 Published · ppublish English Journal Article

Interdependent recruitment of SAGA and Srb mediator by transcriptional activator Gcn4p.

Molecular and cellular biology ·Vol. 25 ·No. 9 ·2005-05-00 ·Pages 3461-74

Qiu H, Hu C, Zhang F, Hwang GJ, Swanson MJ, Boonchird C, Hinnebusch AG

Abstract

Transcriptional activation by Gcn4p is enhanced by the coactivators SWI/SNF, SAGA, and Srb mediator, which stimulate recruitment of TATA binding protein (TBP) and polymerase II to target promoters. We show that wild-type recruitment of SAGA by Gcn4p is dependent on mediator but independent of SWI/SNF function at three different promoters. Recruitment of mediator is also independent of SWI/SNF but is enhanced by SAGA at a subset of Gcn4p target genes. Recruitment of all three coactivators to ARG1 is independent of the TATA element and preinitiation complex formation, whereas efficient recruitment of the general transcription factors requires the TATA box. We propose an activation pathway involving interdependent recruitment of SAGA and Srb mediator to the upstream activation sequence, enabling SWI/SNF recruitment and the binding of TBP and other general factors to the promoter. We also found that high-level recruitment of Tra1p and other SAGA subunits is independent of the Ada2p/Ada3p/Gcn5p histone acetyltransferase module but requires Spt3p in addition to subunits required for SAGA integrity. Thus, while Tra1p can bind directly to Gcn4p in vitro, it requires other SAGA subunits for efficient recruitment in vivo.

MeSH Terms
Acetyltransferases/physiology DNA-Binding Proteins/genetics,metabolism,physiology Gene Expression Regulation, Fungal/genetics,physiology Histone Acetyltransferases Promoter Regions, Genetic/genetics Protein Kinases/genetics,metabolism,physiology RNA Polymerase II/metabolism Saccharomyces cerevisiae/genetics,physiology Saccharomyces cerevisiae Proteins/genetics,metabolism,physiology TATA-Box Binding Protein/metabolism Trans-Activators/genetics,metabolism,physiology Transcription Factors/genetics,metabolism Transcription, Genetic/genetics,physiology
Chemicals
ADA2 protein, S cerevisiae DNA-Binding Proteins NGG1 protein, S cerevisiae SPT3 protein, S cerevisiae Saccharomyces cerevisiae Proteins TATA-Box Binding Protein TRA1 protein, S cerevisiae Trans-Activators Transcription Factors Acetyltransferases Histone Acetyltransferases Protein Kinases RNA Polymerase II
Authors & Affiliations
7 authors, click to expand affiliations / ORCID
Qiu Hongfang
Laboratory of Gene Regulation and Development, National Institute of Child Health & Human Development/NIH, Building 6A, Bethesda, MD 20892, USA.
Hu Cuihua
Zhang Fan
Hwang Gwo Jiunn
Swanson Mark J
Boonchird Cheunchit
Hinnebusch Alan G
References (72)
72 references, click to expand
  1. A multiplicity of coactivators is required by Gcn4p at individual promoters in vivo.
    Mol Cell Biol. 2003 Apr;23(8):2800-20 PMID: 12665580
  2. Independent recruitment in vivo by Gal4 of two complexes required for transcription.
    Mol Cell. 2003 May;11(5):1301-9 PMID: 12769853
  3. Gcn4 occupancy of open reading frame regions results in the recruitment of chromatin-modifying complexes but not the mediator complex.
    EMBO Rep. 2003 Sep;4(9):872-6 PMID: 12949586
  4. Targeting activity is required for SWI/SNF function in vivo and is accomplished through two partially redundant activator-interaction domains.
    Mol Cell. 2003 Oct;12(4):983-90 PMID: 14580348
  5. Recruitment of SWI/SNF by Gcn4p does not require Snf2p or Gcn5p but depends strongly on SWI/SNF integrity, SRB mediator, and SAGA.
    Mol Cell Biol. 2003 Dec;23(23):8829-45 PMID: 14612422
  6. Association of the Mediator complex with enhancers of active genes.
    Proc Natl Acad Sci U S A. 2003 Nov 25;100(24):13887-91 PMID: 14623974
  7. In vivo target of a transcriptional activator revealed by fluorescence resonance energy transfer.
    Genes Dev. 2004 Feb 1;18(3):333-43 PMID: 14871930
  8. An array of coactivators is required for optimal recruitment of TATA binding protein and RNA polymerase II by promoter-bound Gcn4p.
    Mol Cell Biol. 2004 May;24(10):4104-17 PMID: 15121833
  9. A multisubunit complex associated with the RNA polymerase II CTD and TATA-binding protein in yeast.
    Cell. 1993 Jul 2;73(7):1361-75 PMID: 8324825
  10. ADA3: a gene, identified by resistance to GAL4-VP16, with properties similar to and different from those of ADA2.
    Mol Cell Biol. 1993 Oct;13(10):5981-9 PMID: 8413201
  11. A multiprotein mediator of transcriptional activation and its interaction with the C-terminal repeat domain of RNA polymerase II.
    Cell. 1994 May 20;77(4):599-608 PMID: 8187178
  12. The transcriptional activator GCN4 contains multiple activation domains that are critically dependent on hydrophobic amino acids.
    Mol Cell Biol. 1995 Mar;15(3):1220-33 PMID: 7862116
  13. Characterization of physical interactions of the putative transcriptional adaptor, ADA2, with acidic activation domains and TATA-binding protein.
    J Biol Chem. 1995 Aug 18;270(33):19337-44 PMID: 7642611
  14. Identification of seven hydrophobic clusters in GCN4 making redundant contributions to transcriptional activation.
    Mol Cell Biol. 1996 Oct;16(10):5557-71 PMID: 8816468
  15. Identification of native complexes containing the yeast coactivator/repressor proteins NGG1/ADA3 and ADA2.
    J Biol Chem. 1997 Feb 28;272(9):5571-8 PMID: 9038164
  16. In vivo requirement of activator-specific binding targets of mediator.
    Mol Cell Biol. 2000 Dec;20(23):8709-19 PMID: 11073972
  17. Structure and ligand of a histone acetyltransferase bromodomain.
    Nature. 1999 Jun 3;399(6735):491-6 PMID: 10365964
  18. Enhancement of TBP binding by activators and general transcription factors.
    Nature. 1999 Jun 10;399(6736):605-9 PMID: 10376604
  19. Binding of TBP to promoters in vivo is stimulated by activators and requires Pol II holoenzyme.
    Nature. 1999 Jun 10;399(6736):609-13 PMID: 10376605
  20. Functional characterization of the S. cerevisiae genome by gene deletion and parallel analysis.
    Science. 1999 Aug 6;285(5429):901-6 PMID: 10436161
  21. NuA4, an essential transcription adaptor/histone H4 acetyltransferase complex containing Esa1p and the ATM-related cofactor Tra1p.
    EMBO J. 1999 Sep 15;18(18):5108-19 PMID: 10487762
  22. The ADA complex is a distinct histone acetyltransferase complex in Saccharomyces cerevisiae.
    Mol Cell Biol. 1999 Oct;19(10):6621-31 PMID: 10490601
  23. Transcriptional activation by Gcn4p involves independent interactions with the SWI/SNF complex and the SRB/mediator.
    Mol Cell. 1999 Oct;4(4):657-64 PMID: 10549298
  24. Role of covalent modifications of histones in regulating gene expression.
    Gene. 1999 Nov 15;240(1):1-12 PMID: 10564807
  25. Evidence for a mediator cycle at the initiation of transcription.
    Proc Natl Acad Sci U S A. 1997 Jun 10;94(12):6075-8 PMID: 9177171
  26. General transcription factors for RNA polymerase II.
    Prog Nucleic Acid Res Mol Biol. 1997;56:327-46 PMID: 9187058
  27. 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
  28. Yeast Gal11 and transcription factor IIE function through a common pathway in transcriptional regulation.
    J Biol Chem. 1997 Dec 19;272(51):32663-9 PMID: 9405484
  29. The Gcn4p activation domain interacts specifically in vitro with RNA polymerase II holoenzyme, TFIID, and the Adap-Gcn5p coactivator complex.
    Mol Cell Biol. 1998 Mar;18(3):1711-24 PMID: 9488488
  30. Transcriptional activators direct histone acetyltransferase complexes to nucleosomes.
    Nature. 1998 Jul 30;394(6692):498-502 PMID: 9697775
  31. 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
  32. 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
  33. Expanded lysine acetylation specificity of Gcn5 in native complexes.
    J Biol Chem. 1999 Feb 26;274(9):5895-900 PMID: 10026213
  34. Ordered recruitment of transcription and chromatin remodeling factors to a cell cycle- and developmentally regulated promoter.
    Cell. 1999 Apr 30;97(3):299-311 PMID: 10319811
  35. The structural basis for the recognition of acetylated histone H4 by the bromodomain of histone acetyltransferase gcn5p.
    EMBO J. 2000 Nov 15;19(22):6141-9 PMID: 11080160
  36. Functional connections between mediator components and general transcription factors of Saccharomyces cerevisiae.
    J Biol Chem. 2000 Nov 24;275(47):37251-6 PMID: 10973956
  37. 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
  38. 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
  39. The Gcn5 bromodomain co-ordinates nucleosome remodelling.
    Nature. 2000 Mar 23;404(6776):414-7 PMID: 10746732
  40. Distinct classes of yeast promoters revealed by differential TAF recruitment.
    Science. 2000 May 19;288(5469):1242-4 PMID: 10817999
  41. Structure and function of a human TAFII250 double bromodomain module.
    Science. 2000 May 26;288(5470):1422-5 PMID: 10827952
  42. The Swi/Snf family nucleosome-remodeling complexes and transcriptional control.
    Trends Genet. 2000 Aug;16(8):345-51 PMID: 10904263
  43. Mediator of transcriptional regulation.
    Annu Rev Biochem. 2000;69:729-49 PMID: 10966474
  44. Global role for chromatin remodeling enzymes in mitotic gene expression.
    Cell. 2000 Sep 1;102(5):587-98 PMID: 11007477
  45. Solution structure and acetyl-lysine binding activity of the GCN5 bromodomain.
    J Mol Biol. 2000 Dec 1;304(3):355-70 PMID: 11090279
  46. Gcn4 activator targets Gcn5 histone acetyltransferase to specific promoters independently of transcription.
    Mol Cell. 2000 Dec;6(6):1309-20 PMID: 11163205
  47. The yeast mediator.
    Mol Cells. 2001 Apr 30;11(2):129-36 PMID: 11355691
  48. Transcriptional profiling shows that Gcn4p is a master regulator of gene expression during amino acid starvation in yeast.
    Mol Cell Biol. 2001 Jul;21(13):4347-68 PMID: 11390663
  49. Recruitment of HAT complexes by direct activator interactions with the ATM-related Tra1 subunit.
    Science. 2001 Jun 22;292(5525):2333-7 PMID: 11423663
  50. SAGA is an essential in vivo target of the yeast acidic activator Gal4p.
    Genes Dev. 2001 Aug 1;15(15):1935-45 PMID: 11485988
  51. 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
  52. A triad of subunits from the Gal11/tail domain of Srb mediator is an in vivo target of transcriptional activator Gcn4p.
    Mol Cell Biol. 2004 Aug;24(15):6871-86 PMID: 15254252
  53. Molecular architecture of the S. cerevisiae SAGA complex.
    Mol Cell. 2004 Jul 23;15(2):199-208 PMID: 15260971
  54. Targeting of Swi/Snf to the yeast GAL1 UAS G requires the Mediator, TAF IIs, and RNA polymerase II.
    EMBO J. 2004 Oct 13;23(20):4040-50 PMID: 15385957
  55. Import of proteins into mitochondria. Extramitochondrial pools and post-translational import of mitochondrial protein precursors in vivo.
    J Biol Chem. 1982 Nov 10;257(21):13062-7 PMID: 6215406
  56. New yeast-Escherichia coli shuttle vectors constructed with in vitro mutagenized yeast genes lacking six-base pair restriction sites.
    Gene. 1988 Dec 30;74(2):527-34 PMID: 3073106
  57. Complex formation by positive and negative translational regulators of GCN4.
    Mol Cell Biol. 1991 Jun;11(6):3217-28 PMID: 2038327
  58. 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
  59. Two distinct yeast transcriptional activators require the function of the GCN5 protein to promote normal levels of transcription.
    EMBO J. 1992 Nov;11(11):4145-52 PMID: 1396595
  60. Mediator, not holoenzyme, is directly recruited to the heat shock promoter by HSF upon heat shock.
    Mol Cell. 2001 Jul;8(1):9-19 PMID: 11511356
  61. The Swi5 activator recruits the Mediator complex to the HO promoter without RNA polymerase II.
    Genes Dev. 2001 Sep 15;15(18):2457-69 PMID: 11562354
  62. The structural and functional organization of the yeast mediator complex.
    J Biol Chem. 2001 Nov 9;276(45):42003-10 PMID: 11555651
  63. Transcriptional coactivator complexes.
    Annu Rev Biochem. 2001;70:475-501 PMID: 11395415
  64. Transcription activator interactions with multiple SWI/SNF subunits.
    Mol Cell Biol. 2002 Mar;22(6):1615-25 PMID: 11865042
  65. Role of the Ada2 and Ada3 transcriptional coactivators in histone acetylation.
    J Biol Chem. 2002 Mar 8;277(10):7989-95 PMID: 11773077
  66. Coactivators in transcription initiation: here are your orders.
    Curr Opin Genet Dev. 2002 Apr;12(2):149-55 PMID: 11893487
  67. Cooperation between complexes that regulate chromatin structure and transcription.
    Cell. 2002 Feb 22;108(4):475-87 PMID: 11909519
  68. Exchange of RNA polymerase II initiation and elongation factors during gene expression in vivo.
    Mol Cell. 2002 Apr;9(4):799-809 PMID: 11983171
  69. Proteomics of the eukaryotic transcription machinery: identification of proteins associated with components of yeast TFIID by multidimensional mass spectrometry.
    Mol Cell Biol. 2002 Jul;22(13):4723-38 PMID: 12052880
  70. Analysis of Spt7 function in the Saccharomyces cerevisiae SAGA coactivator complex.
    Mol Cell Biol. 2002 Aug;22(15):5367-79 PMID: 12101232
  71. Function and selectivity of bromodomains in anchoring chromatin-modifying complexes to promoter nucleosomes.
    Cell. 2002 Nov 1;111(3):369-79 PMID: 12419247
  72. SWI/SNF-dependent chromatin remodeling of RNR3 requires TAF(II)s and the general transcription machinery.
    Genes Dev. 2003 Feb 15;17(4):502-15 PMID: 12600943
Article Info
Journal
Molecular and cellular biology
Abbr.
Mol Cell Biol
ISSN
0270-7306
Published
2005-05-00
Pages
3461-74
Language
English
Region
United States
NLM ID
8109087
PMCID
PMC1084306
Subset
IM
Analysis Services
Analysis Services

Contact

No. 2 Wenbo Road, Zhangqiu District, Jinan, Shandong

Qilu Normal University · Genelibs Bioinformatics Lab

750 Shunhua Rd, Jinan

2F, Bldg F, University Science Park

Tel: 0531-88819269

WeChat Official Account

Follow our WeChat subscription account for real-time updates and the latest in medical and biological research.


Business Email

E-mail: product@genelibs.com