Home LiteratureArticle Details
PMID: 17030999 Published · ppublish English Journal Article Research Support, N.I.H., Extramural

SWI/SNF displaces SAGA-acetylated nucleosomes.

Eukaryotic cell ·Vol. 5 ·No. 10 ·2006-10-00 ·Pages 1738-47

Chandy M, Gutiérrez JL, Prochasson P, Workman JL

Abstract

SWI/SNF is a well-characterized chromatin remodeling complex that remodels chromatin by sliding nucleosomes in cis and/or displacing nucleosomes in trans. The latter mechanism has the potential to remove promoter nucleosomes, allowing access to transcription factors and RNA polymerase. In vivo, histone acetylation often precedes apparent nucleosome loss; therefore, we sought to determine whether nucleosomes containing acetylated histones could be displaced by the SWI/SNF chromatin remodeling complex. We found that SAGA-acetylated histones were lost from an immobilized nucleosome array when treated with the SWI/SNF complex. When the nucleosome array was acetylated by SAGA in the presence of bound transcription activators, it generated a peak of acetylation surrounding the activator binding sites. Subsequent SWI/SNF treatment suppressed this acetylation peak. Immunoblots indicated that SWI/SNF preferentially displaced acetylated histones from the array relative to total histones. Moreover, the Swi2/Snf2 bromodomain, an acetyl-lysine binding domain, played a role in the displacement of acetylated histones. These data indicate that targeted histone acetylation by the SAGA complex predisposes promoter nucleosomes for displacement by the SWI/SNF complex.

MeSH Terms
Acetylation Chromosomal Proteins, Non-Histone/metabolism HeLa Cells Histones/metabolism Humans Multiprotein Complexes/metabolism Nucleosomes/metabolism Transcription Factors/metabolism Yeasts/metabolism
Chemicals
Chromosomal Proteins, Non-Histone Histones Multiprotein Complexes Nucleosomes SWI-SNF-B chromatin-remodeling complex Transcription Factors
Authors & Affiliations
4 authors, click to expand affiliations / ORCID
Chandy Mark
Stowers Institute for Medical Research, 1000 E 50th St., Kansas City, MO 64110, USA.
Gutiérrez José L
Prochasson Philippe
Workman Jerry L
References (61)
61 references, click to expand
  1. A generic protein purification method for protein complex characterization and proteome exploration.
    Nat Biotechnol. 1999 Oct;17(10):1030-2 PMID: 10504710
  2. Persistent site-specific remodeling of a nucleosome array by transient action of the SWI/SNF complex.
    Science. 1996 Jul 26;273(5274):513-6 PMID: 8662543
  3. RSC, an essential, abundant chromatin-remodeling complex.
    Cell. 1996 Dec 27;87(7):1249-60 PMID: 8980231
  4. 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
  5. Transcriptional activators direct histone acetyltransferase complexes to nucleosomes.
    Nature. 1998 Jul 30;394(6692):498-502 PMID: 9697775
  6. Linker histones stabilize the intrinsic salt-dependent folding of nucleosomal arrays: mechanistic ramifications for higher-order chromatin folding.
    Biochemistry. 1998 Oct 20;37(42):14776-87 PMID: 9778352
  7. Dissecting the regulatory circuitry of a eukaryotic genome.
    Cell. 1998 Nov 25;95(5):717-28 PMID: 9845373
  8. Histone octamer transfer by a chromatin-remodeling complex.
    Cell. 1999 Feb 5;96(3):389-92 PMID: 10025404
  9. The bromodomain of Gcn5p interacts in vitro with specific residues in the N terminus of histone H4.
    J Mol Biol. 1999 Mar 19;287(1):1-7 PMID: 10074402
  10. 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
  11. Evidence for histone eviction in trans upon induction of the yeast PHO5 promoter.
    Mol Cell Biol. 2004 Dec;24(24):10965-74 PMID: 15572697
  12. Specific contributions of histone tails and their acetylation to the mechanical stability of nucleosomes.
    J Mol Biol. 2005 Feb 11;346(1):135-46 PMID: 15663933
  13. Function of a eukaryotic transcription activator during the transcription cycle.
    Mol Cell. 2005 Apr 29;18(3):369-78 PMID: 15866178
  14. A decade of histone acetylation: marking eukaryotic chromosomes with specific codes.
    J Biochem. 2005 Dec;138(6):647-62 PMID: 16428293
  15. SWI/SNF binding to the HO promoter requires histone acetylation and stimulates TATA-binding protein recruitment.
    Mol Cell Biol. 2006 Jun;26(11):4095-110 PMID: 16705163
  16. Activation domain-mediated targeting of the SWI/SNF complex to promoters stimulates transcription from nucleosome arrays.
    Mol Cell. 1999 Oct;4(4):649-55 PMID: 10549297
  17. 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
  18. Whole-genome expression analysis of snf/swi mutants of Saccharomyces cerevisiae.
    Proc Natl Acad Sci U S A. 2000 Mar 28;97(7):3364-9 PMID: 10725359
  19. Analysis of nucleosome disruption by ATP-driven chromatin remodeling complexes.
    Methods Mol Biol. 1999;119:319-31 PMID: 10804522
  20. Structure and function of a human TAFII250 double bromodomain module.
    Science. 2000 May 26;288(5470):1422-5 PMID: 10827952
  21. Distribution of acetylated histones resulting from Gal4-VP16 recruitment of SAGA and NuA4 complexes.
    EMBO J. 2000 Jun 1;19(11):2629-40 PMID: 10835360
  22. p300-mediated acetylation facilitates the transfer of histone H2A-H2B dimers from nucleosomes to a histone chaperone.
    Genes Dev. 2000 Aug 1;14(15):1899-907 PMID: 10921904
  23. Octamer transfer and creation of stably remodeled nucleosomes by human SWI-SNF and its isolated ATPases.
    Mol Cell Biol. 2000 Sep;20(17):6380-9 PMID: 10938115
  24. 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
  25. Solution structure and acetyl-lysine binding activity of the GCN5 bromodomain.
    J Mol Biol. 2000 Dec 1;304(3):355-70 PMID: 11090279
  26. Gcn4 activator targets Gcn5 histone acetyltransferase to specific promoters independently of transcription.
    Mol Cell. 2000 Dec;6(6):1309-20 PMID: 11163205
  27. Histone acetyltransferase complexes stabilize swi/snf binding to promoter nucleosomes.
    Cell. 2001 Mar 23;104(6):817-27 PMID: 11290320
  28. Recruitment of HAT complexes by direct activator interactions with the ATM-related Tra1 subunit.
    Science. 2001 Jun 22;292(5525):2333-7 PMID: 11423663
  29. A transient histone hyperacetylation signal marks nucleosomes for remodeling at the PHO8 promoter in vivo.
    Mol Cell. 2001 Mar;7(3):529-38 PMID: 11463378
  30. Promoter targeting of chromatin-modifying complexes.
    Front Biosci. 2001 Sep 1;6:D1054-64 PMID: 11532604
  31. Transcription activator interactions with multiple SWI/SNF subunits.
    Mol Cell Biol. 2002 Mar;22(6):1615-25 PMID: 11865042
  32. Bromodomain: an acetyl-lysine binding domain.
    FEBS Lett. 2002 Feb 20;513(1):124-8 PMID: 11911891
  33. Genome-wide location and regulated recruitment of the RSC nucleosome-remodeling complex.
    Genes Dev. 2002 Apr 1;16(7):806-19 PMID: 11937489
  34. Analysis of Spt7 function in the Saccharomyces cerevisiae SAGA coactivator complex.
    Mol Cell Biol. 2002 Aug;22(15):5367-79 PMID: 12101232
  35. Function and selectivity of bromodomains in anchoring chromatin-modifying complexes to promoter nucleosomes.
    Cell. 2002 Nov 1;111(3):369-79 PMID: 12419247
  36. Structural analysis of the yeast SWI/SNF chromatin remodeling complex.
    Nat Struct Biol. 2003 Feb;10(2):141-5 PMID: 12524530
  37. Different sensitivities of bromodomain factors 1 and 2 to histone H4 acetylation.
    Mol Cell. 2003 Feb;11(2):353-63 PMID: 12620224
  38. Effect of DNA length and H4 acetylation on the thermal stability of reconstituted nucleosome particles.
    Biochem Biophys Res Commun. 2003 Mar 21;302(4):885-91 PMID: 12646255
  39. Multiple mechanistically distinct functions of SAGA at the PHO5 promoter.
    Mol Cell Biol. 2003 May;23(10):3468-76 PMID: 12724405
  40. Nucleosomes unfold completely at a transcriptionally active promoter.
    Mol Cell. 2003 Jun;11(6):1587-98 PMID: 12820971
  41. Histones are first hyperacetylated and then lose contact with the activated PHO5 promoter.
    Mol Cell. 2003 Jun;11(6):1599-607 PMID: 12820972
  42. 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
  43. A genome-wide housekeeping role for TFIID and a highly regulated stress-related role for SAGA in Saccharomyces cerevisiae.
    Mol Cell. 2004 Feb 27;13(4):573-85 PMID: 14992726
  44. Tandem bromodomains in the chromatin remodeler RSC recognize acetylated histone H3 Lys14.
    EMBO J. 2004 Mar 24;23(6):1348-59 PMID: 15014446
  45. Differential targeting of two distinct SWI/SNF-related Drosophila chromatin-remodeling complexes.
    Mol Cell Biol. 2004 Apr;24(8):3077-88 PMID: 15060132
  46. Structure and ligand of a histone acetyltransferase bromodomain.
    Nature. 1999 Jun 3;399(6735):491-6 PMID: 10365964
  47. Nucleosome mobilization catalysed by the yeast SWI/SNF complex.
    Nature. 1999 Aug 19;400(6746):784-7 PMID: 10466730
  48. Recruitment of the SWI/SNF chromatin remodeling complex by transcriptional activators.
    Genes Dev. 1999 Sep 15;13(18):2369-74 PMID: 10500094
  49. Removal of promoter nucleosomes by disassembly rather than sliding in vivo.
    Mol Cell. 2004 Jun 4;14(5):667-73 PMID: 15175161
  50. Evidence for nucleosome depletion at active regulatory regions genome-wide.
    Nat Genet. 2004 Aug;36(8):900-5 PMID: 15247917
  51. Global position and recruitment of HATs and HDACs in the yeast genome.
    Mol Cell. 2004 Oct 22;16(2):199-209 PMID: 15494307
  52. Proteomic analysis of chromatin-modifying complexes in Saccharomyces cerevisiae identifies novel subunits.
    Biochem Soc Trans. 2004 Dec;32(Pt 6):899-903 PMID: 15506919
  53. GAL4 derivatives function alone and synergistically with mammalian activators in vitro.
    Cell. 1988 Aug 26;54(5):659-64 PMID: 3044607
  54. A positive role for histone acetylation in transcription factor access to nucleosomal DNA.
    Cell. 1993 Jan 15;72(1):73-84 PMID: 8422685
  55. Effects of histone acetylation, ubiquitination and variants on nucleosome stability.
    Biochem J. 1993 Dec 15;296 ( Pt 3):737-44 PMID: 8280071
  56. A multisubunit complex containing the SWI1/ADR6, SWI2/SNF2, SWI3, SNF5, and SNF6 gene products isolated from yeast.
    Proc Natl Acad Sci U S A. 1994 Mar 1;91(5):1950-4 PMID: 8127913
  57. Stimulation of GAL4 derivative binding to nucleosomal DNA by the yeast SWI/SNF complex.
    Science. 1994 Jul 1;265(5168):53-60 PMID: 8016655
  58. Nucleosome disruption and enhancement of activator binding by a human SW1/SNF complex.
    Nature. 1994 Aug 11;370(6489):477-81 PMID: 8047169
  59. Facilitated binding of TATA-binding protein to nucleosomal DNA.
    Nature. 1994 Aug 11;370(6489):481-5 PMID: 8047170
  60. DNA-binding properties of the yeast SWI/SNF complex.
    Nature. 1996 Feb 29;379(6568):844-7 PMID: 8587611
  61. Remodeling the chromatin structure of a nucleosome array by transcription factor-targeted trans-displacement of histones.
    EMBO J. 1996 Sep 2;15(17):4702-12 PMID: 8887561
Article Info
Journal
Eukaryotic cell
Abbr.
Eukaryot Cell
ISSN
1535-9778
DOI
10.1128/EC.00165-06
Published
2006-10-00
Pages
1738-47
Language
English
Region
United States
NLM ID
101130731
PMCID
PMC1595347
Subset
IM
Grants
NIGMS NIH HHS · R37 GM047867 · United States
External Links
PubMed source DOI: 10.1128/EC.00165-06 PMC Full Text View journal details
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

Copyright © 2026.Genelibs Jinan Honghui Biotechnology Co., Ltd. 鲁ICP备20007159号-2