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PMID: 15057269 Published · ppublish English Comparative Study Journal Article Research Support, Non-U.S. Gov't

Spt3 and Mot1 cooperate in nucleosome remodeling independently of TBP recruitment.

The EMBO journal ·Vol. 23 ·No. 9 ·2004-05-05 ·Pages 1943-8

Topalidou I, Papamichos-Chronakis M, Thireos G, Tzamarias D

Abstract

We have investigated the requirements for nucleosome remodeling upon transcriptional induction of the GAL1 promoter. We found that remodeling was dependent on two SAGA complex components, Gcn5 and Spt3. The involvement of the latter was surprising as its function has been suggested to be directly involved in TATA-binding protein (TBP) recruitment. We demonstrated that this novel function was in fact independent of TBP recruitment and this was further validated using a Gal4-driven synthetic promoter. Most importantly, we showed that the involvement of Spt3 in chromatin remodeling was independent of transcription, as it was also observed for a nonpromoter nucleosome located next to an activator-binding site. In an effort to explore how the Spt3 function was elicited, we found that Mot1, an ATPase of the Snf2 family that genetically interacts with Spt3, was also required for nucleosome remodeling independently of TBP recruitment. Interestingly enough, Spt3 and Mot1 were recruited on the GAL1 promoter as well as on the nonpromoter site in an interdependent manner. These findings show that the two proteins cooperate in nucleosomal transactions.

MeSH Terms
Adenosine Triphosphatases Chromatin Assembly and Disassembly/physiology Chromatin Immunoprecipitation DNA Helicases/metabolism DNA-Binding Proteins/metabolism Gene Expression Histone Acetyltransferases Nucleosomes/metabolism Plasmids/genetics Promoter Regions, Genetic/genetics Protein Kinases/metabolism Saccharomyces cerevisiae Proteins/genetics,metabolism TATA-Binding Protein Associated Factors/metabolism Transcription Factors/genetics Yeasts
Chemicals
DNA-Binding Proteins GAL4 protein, S cerevisiae Nucleosomes SPT3 protein, S cerevisiae Saccharomyces cerevisiae Proteins TATA-Binding Protein Associated Factors Transcription Factors GCN5 protein, S cerevisiae Histone Acetyltransferases Protein Kinases Adenosine Triphosphatases MOT1 protein, S cerevisiae DNA Helicases
Authors & Affiliations
4 authors, click to expand affiliations / ORCID
Topalidou Irini
Institute of Molecular Biology and Biotechnology, FORTH, Crete, Greece.
Papamichos-Chronakis Manolis
Thireos George
Tzamarias Dimitris
References (37)
37 references, click to expand
  1. A histone fold TAF octamer within the yeast TFIID transcriptional coactivator.
    Nat Struct Biol. 2001 Aug;8(8):695-700 PMID: 11473260
  2. Histones are first hyperacetylated and then lose contact with the activated PHO5 promoter.
    Mol Cell. 2003 Jun;11(6):1599-607 PMID: 12820972
  3. 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
  4. Histone acetyltransferases.
    Annu Rev Biochem. 2001;70:81-120 PMID: 11395403
  5. Role of the Ada2 and Ada3 transcriptional coactivators in histone acetylation.
    J Biol Chem. 2002 Mar 8;277(10):7989-95 PMID: 11773077
  6. The SANT domain of Ada2 is required for normal acetylation of histones by the yeast SAGA complex.
    J Biol Chem. 2002 Mar 8;277(10):8178-86 PMID: 11777910
  7. Mot1 activates and represses transcription by direct, ATPase-dependent mechanisms.
    Proc Natl Acad Sci U S A. 2002 Mar 5;99(5):2666-71 PMID: 11880621
  8. 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
  9. Post-TATA binding protein recruitment clearance of Gcn5-dependent histone acetylation within promoter nucleosomes.
    Mol Cell Biol. 2003 Nov;23(21):7809-17 PMID: 14560024
  10. 5' untranslated sequences are required for the translational control of a yeast regulatory gene.
    Proc Natl Acad Sci U S A. 1984 Aug;81(16):5096-100 PMID: 6433345
  11. The SPT3 gene is required for normal transcription of Ty elements in S. cerevisiae.
    Cell. 1984 Dec;39(3 Pt 2):675-82 PMID: 6096019
  12. SPT3 interacts with TFIID to allow normal transcription in Saccharomyces cerevisiae.
    Genes Dev. 1992 Jul;6(7):1319-31 PMID: 1628834
  13. GAL4 disrupts a repressing nucleosome during activation of GAL1 transcription in vivo.
    Genes Dev. 1993 May;7(5):857-69 PMID: 8491382
  14. Multiple mechanisms provide rapid and stringent glucose repression of GAL gene expression in Saccharomyces cerevisiae.
    Mol Cell Biol. 1994 Jun;14(6):3834-41 PMID: 8196626
  15. 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
  16. Mot1, a global repressor of RNA polymerase II transcription, inhibits TBP binding to DNA by an ATP-dependent mechanism.
    Genes Dev. 1994 Aug 15;8(16):1920-34 PMID: 7958867
  17. Genetic evidence for the interaction of the yeast transcriptional co-activator proteins GCN5 and ADA2.
    Mol Gen Genet. 1995 Mar 20;246(6):723-8 PMID: 7898440
  18. The NOT, SPT3, and MOT1 genes functionally interact to regulate transcription at core promoters.
    Mol Cell Biol. 1996 Dec;16(12):6668-76 PMID: 8943321
  19. Evidence that Spt3 functionally interacts with Mot1, TFIIA, and TATA-binding protein to confer promoter-specific transcriptional control in Saccharomyces cerevisiae.
    Mol Cell Biol. 1997 Jan;17(1):287-95 PMID: 8972209
  20. Saccharomyces cerevisiae BUR6 encodes a DRAP1/NC2alpha homolog that has both positive and negative roles in transcription in vivo.
    Mol Cell Biol. 1997 Apr;17(4):2057-65 PMID: 9121454
  21. Molecular analysis of the SNF2/SWI2 protein family member MOT1, an ATP-driven enzyme that dissociates TATA-binding protein from DNA.
    Mol Cell Biol. 1997 Aug;17(8):4842-51 PMID: 9234740
  22. Nucleosome transactions on the promoters of the yeast GAL and PHO genes.
    J Biol Chem. 1997 Oct 24;272(43):26795-8 PMID: 9341105
  23. Regulation of gene expression by TBP-associated proteins.
    Genes Dev. 1998 May 15;12(10):1398-408 PMID: 9585500
  24. 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
  25. 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
  26. 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
  27. The Gcn5 bromodomain co-ordinates nucleosome remodelling.
    Nature. 2000 Mar 23;404(6776):414-7 PMID: 10746732
  28. Redundant roles for the TFIID and SAGA complexes in global transcription.
    Nature. 2000 Jun 8;405(6787):701-4 PMID: 10864329
  29. SPT genes: key players in the regulation of transcription, chromatin structure and other cellular processes.
    J Biochem. 2001 Feb;129(2):185-91 PMID: 11173517
  30. Recruitment of HAT complexes by direct activator interactions with the ATM-related Tra1 subunit.
    Science. 2001 Jun 22;292(5525):2333-7 PMID: 11423663
  31. Cti6, a PHD domain protein, bridges the Cyc8-Tup1 corepressor and the SAGA coactivator to overcome repression at GAL1.
    Mol Cell. 2002 Jun;9(6):1297-305 PMID: 12086626
  32. Mot1p is essential for TBP recruitment to selected promoters during in vivo gene activation.
    EMBO J. 2002 Oct 1;21(19):5173-83 PMID: 12356733
  33. Differential requirement of SAGA components for recruitment of TATA-box-binding protein to promoters in vivo.
    Mol Cell Biol. 2002 Nov;22(21):7365-71 PMID: 12370284
  34. Mot1 associates with transcriptionally active promoters and inhibits association of NC2 in Saccharomyces cerevisiae.
    Mol Cell Biol. 2002 Dec;22(23):8122-34 PMID: 12417716
  35. Multiple mechanistically distinct functions of SAGA at the PHO5 promoter.
    Mol Cell Biol. 2003 May;23(10):3468-76 PMID: 12724405
  36. Nucleosomes unfold completely at a transcriptionally active promoter.
    Mol Cell. 2003 Jun;11(6):1587-98 PMID: 12820971
  37. SAGA is an essential in vivo target of the yeast acidic activator Gal4p.
    Genes Dev. 2001 Aug 1;15(15):1935-45 PMID: 11485988
Article Info
Journal
The EMBO journal
Abbr.
EMBO J
ISSN
0261-4189
Published
2004-05-05
Epub
2004-00-01
Pages
1943-8
Language
English
Region
England
NLM ID
8208664
PMCID
PMC404319
Subset
IM
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