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PMID: 16880522 Published · ppublish English Journal Article Research Support, N.I.H., Extramural Research Support, Non-U.S. Gov't Research Support, U.S. Gov't, Non-P.H.S.

Isw1 functions in parallel with the NuA4 and Swr1 complexes in stress-induced gene repression.

Molecular and cellular biology ·Vol. 26 ·No. 16 ·2006-08-00 ·Pages 6117-29

Lindstrom KC, Vary JC, Parthun MR, Delrow J, Tsukiyama T

Abstract

The packaging of DNA into chromatin allows eukaryotic cells to organize and compact their genomes but also creates an environment that is generally repressive to nuclear processes that depend upon DNA accessibility. There are several classes of enzymes that modulate the primary structure of chromatin to regulate various DNA-dependent processes. The biochemical activities of the yeast Isw1 ATP-dependent chromatin-remodeling enzyme have been well characterized in vitro, but little is known about how these activities are utilized in vivo. In this work, we sought to discern genetic backgrounds that require Isw1 activity for normal growth. We identified a three-way genetic interaction among Isw1, the NuA4 histone acetyltransferase complex, and the Swr1 histone replacement complex. Transcription microarray analysis revealed parallel functions for these three chromatin-modifying factors in the regulation of TATA-containing genes, including the repression of a large number of stress-induced genes under normal growth conditions. In contrast to a recruitment-based model, we find that the NuA4 and Swr1 complexes act throughout the genome while only a specific subset of the genome shows alterations in transcription.

MeSH Terms
Acetylation Acetyltransferases/deficiency,metabolism Adenosine Triphosphatases/deficiency,metabolism Chromatin Assembly and Disassembly/genetics DNA-Binding Proteins/deficiency,metabolism Down-Regulation/drug effects Gene Expression Regulation, Fungal/drug effects Genome, Fungal/genetics Histone Acetyltransferases Histones/metabolism Lysine/metabolism Microbial Sensitivity Tests Mutation/genetics Promoter Regions, Genetic/genetics Protein Transport Saccharomyces cerevisiae/cytology,drug effects,enzymology Saccharomyces cerevisiae Proteins/metabolism Sirolimus/pharmacology Transcription Factors/metabolism Transcription, Genetic
Chemicals
DNA-Binding Proteins Histones MSN2 protein, S cerevisiae Saccharomyces cerevisiae Proteins Transcription Factors Acetyltransferases Histone Acetyltransferases NuA4 protein, S cerevisiae Adenosine Triphosphatases ISW1 protein, S cerevisiae Swr1 protein, S cerevisiae Lysine Sirolimus
Authors & Affiliations
5 authors, click to expand affiliations / ORCID
Lindstrom Kimberly C
Division of Basic Sciences, Fred Hutchinson Cancer Research Center, Seattle, WA 98109, USA.
Vary Jay C
Parthun Mark R
Delrow Jeffrey
Tsukiyama Toshio
References (64)
64 references, click to expand
  1. Multiple links between the NuA4 histone acetyltransferase complex and epigenetic control of transcription.
    Mol Cell. 2000 Jun;5(6):927-37 PMID: 10911987
  2. Genomic expression programs in the response of yeast cells to environmental changes.
    Mol Biol Cell. 2000 Dec;11(12):4241-57 PMID: 11102521
  3. A chromatin remodelling complex involved in transcription and DNA processing.
    Nature. 2000 Aug 3;406(6795):541-4 PMID: 10952318
  4. Type B histone acetyltransferase Hat1p participates in telomeric silencing.
    Mol Cell Biol. 2000 Oct;20(19):7051-8 PMID: 10982821
  5. Coordinate regulation of yeast ribosomal protein genes is associated with targeted recruitment of Esa1 histone acetylase.
    Mol Cell. 2000 Dec;6(6):1297-307 PMID: 11163204
  6. The yeast NuA4 and Drosophila MSL complexes contain homologous subunits important for transcription regulation.
    J Biol Chem. 2001 Feb 2;276(5):3484-91 PMID: 11036083
  7. A Bayesian framework for the analysis of microarray expression data: regularized t -test and statistical inferences of gene changes.
    Bioinformatics. 2001 Jun;17(6):509-19 PMID: 11395427
  8. Translating the histone code.
    Science. 2001 Aug 10;293(5532):1074-80 PMID: 11498575
  9. The p400 complex is an essential E1A transformation target.
    Cell. 2001 Aug 10;106(3):297-307 PMID: 11509179
  10. Widespread collaboration of Isw2 and Sin3-Rpd3 chromatin remodeling complexes in transcriptional repression.
    Mol Cell Biol. 2001 Oct;21(19):6450-60 PMID: 11533234
  11. Cooperation between complexes that regulate chromatin structure and transcription.
    Cell. 2002 Feb 22;108(4):475-87 PMID: 11909519
  12. The in vivo functions of ATP-dependent chromatin-remodelling factors.
    Nat Rev Mol Cell Biol. 2002 Jun;3(6):422-9 PMID: 12042764
  13. Ordered recruitment: gene-specific mechanism of transcription activation.
    Mol Cell. 2002 Aug;10(2):227-36 PMID: 12191469
  14. Acetylation of histone H4 by Esa1 is required for DNA double-strand break repair.
    Nature. 2002 Sep 26;419(6905):411-5 PMID: 12353039
  15. NuA4 subunit Yng2 function in intra-S-phase DNA damage response.
    Mol Cell Biol. 2002 Dec;22(23):8215-25 PMID: 12417725
  16. Yeast Isw1p forms two separable complexes in vivo.
    Mol Cell Biol. 2003 Jan;23(1):80-91 PMID: 12482963
  17. Conserved histone variant H2A.Z protects euchromatin from the ectopic spread of silent heterochromatin.
    Cell. 2003 Mar 7;112(5):725-36 PMID: 12628191
  18. Histone acetylation and deacetylation in yeast.
    Nat Rev Mol Cell Biol. 2003 Apr;4(4):276-84 PMID: 12671650
  19. Functional consequences of histone modifications.
    Curr Opin Genet Dev. 2003 Apr;13(2):154-60 PMID: 12672492
  20. Yeast enhancer of polycomb defines global Esa1-dependent acetylation of chromatin.
    Genes Dev. 2003 Jun 1;17(11):1415-28 PMID: 12782659
  21. The diverse functions of histone acetyltransferase complexes.
    Trends Genet. 2003 Jun;19(6):321-9 PMID: 12801725
  22. Yaf9, a novel NuA4 histone acetyltransferase subunit, is required for the cellular response to spindle stress in yeast.
    Mol Cell Biol. 2003 Sep;23(17):6086-102 PMID: 12917332
  23. FunSpec: a web-based cluster interpreter for yeast.
    BMC Bioinformatics. 2002 Nov 13;3:35 PMID: 12431279
  24. Isw1 chromatin remodeling ATPase coordinates transcription elongation and termination by RNA polymerase II.
    Cell. 2003 Nov 14;115(4):425-35 PMID: 14622597
  25. The nuclear actin-related protein Act3p/Arp4p of Saccharomyces cerevisiae is involved in transcription regulation of stress genes.
    Mol Microbiol. 2003 Nov;50(4):1155-71 PMID: 14622406
  26. Chromatin remodeling in vivo: evidence for a nucleosome sliding mechanism.
    Mol Cell. 2003 Nov;12(5):1333-40 PMID: 14636590
  27. A Snf2 family ATPase complex required for recruitment of the histone H2A variant Htz1.
    Mol Cell. 2003 Dec;12(6):1565-76 PMID: 14690608
  28. Eaf3 regulates the global pattern of histone acetylation in Saccharomyces cerevisiae.
    Mol Cell Biol. 2004 Jan;24(2):757-64 PMID: 14701747
  29. ATP-driven exchange of histone H2AZ variant catalyzed by SWR1 chromatin remodeling complex.
    Science. 2004 Jan 16;303(5656):343-8 PMID: 14645854
  30. 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
  31. Identification and distinct regulation of yeast TATA box-containing genes.
    Cell. 2004 Mar 5;116(5):699-709 PMID: 15006352
  32. A new class of C. elegans synMuv genes implicates a Tip60/NuA4-like HAT complex as a negative regulator of Ras signaling.
    Dev Cell. 2004 Apr;6(4):563-76 PMID: 15068795
  33. A protein complex containing the conserved Swi2/Snf2-related ATPase Swr1p deposits histone variant H2A.Z into euchromatin.
    PLoS Biol. 2004 May;2(5):E131 PMID: 15045029
  34. Chromatin dynamics at DNA replication, transcription and repair.
    Eur J Biochem. 2004 Jun;271(12):2335-49 PMID: 15182349
  35. Regulation of chromosome stability by the histone H2A variant Htz1, the Swr1 chromatin remodeling complex, and the histone acetyltransferase NuA4.
    Proc Natl Acad Sci U S A. 2004 Sep 14;101(37):13513-8 PMID: 15353583
  36. The Yaf9 component of the SWR1 and NuA4 complexes is required for proper gene expression, histone H4 acetylation, and Htz1 replacement near telomeres.
    Mol Cell Biol. 2004 Nov;24(21):9424-36 PMID: 15485911
  37. The genetic control of direct-repeat recombination in Saccharomyces: the effect of rad52 and rad1 on mitotic recombination at GAL10, a transcriptionally regulated gene.
    Genetics. 1989 Dec;123(4):725-38 PMID: 2693208
  38. Evolution of the SNF2 family of proteins: subfamilies with distinct sequences and functions.
    Nucleic Acids Res. 1995 Jul 25;23(14):2715-23 PMID: 7651832
  39. A new efficient gene disruption cassette for repeated use in budding yeast.
    Nucleic Acids Res. 1996 Jul 1;24(13):2519-24 PMID: 8692690
  40. Nuclear localization of the C2H2 zinc finger protein Msn2p is regulated by stress and protein kinase A activity.
    Genes Dev. 1998 Feb 15;12(4):586-97 PMID: 9472026
  41. A suppressor of two essential checkpoint genes identifies a novel protein that negatively affects dNTP pools.
    Mol Cell. 1998 Sep;2(3):329-40 PMID: 9774971
  42. Cluster analysis and display of genome-wide expression patterns.
    Proc Natl Acad Sci U S A. 1998 Dec 8;95(25):14863-8 PMID: 9843981
  43. Characterization of the imitation switch subfamily of ATP-dependent chromatin-remodeling factors in Saccharomyces cerevisiae.
    Genes Dev. 1999 Mar 15;13(6):686-97 PMID: 10090725
  44. Three new dominant drug resistance cassettes for gene disruption in Saccharomyces cerevisiae.
    Yeast. 1999 Oct;15(14):1541-53 PMID: 10514571
  45. ATP-dependent chromatin remodeling.
    Curr Top Dev Biol. 2005;65:115-48 PMID: 15642381
  46. Histone variants: deviants?
    Genes Dev. 2005 Feb 1;19(3):295-310 PMID: 15687254
  47. Characterization of the yeast trimeric-SAS acetyltransferase complex.
    J Biol Chem. 2005 Mar 25;280(12):11987-94 PMID: 15659401
  48. The mammalian YL1 protein is a shared subunit of the TRRAP/TIP60 histone acetyltransferase and SRCAP complexes.
    J Biol Chem. 2005 Apr 8;280(14):13665-70 PMID: 15647280
  49. Genomic characterization reveals a simple histone H4 acetylation code.
    Proc Natl Acad Sci U S A. 2005 Apr 12;102(15):5501-6 PMID: 15795371
  50. Dynamic lysine methylation on histone H3 defines the regulatory phase of gene transcription.
    Mol Cell. 2005 Jun 10;18(6):723-34 PMID: 15949446
  51. Genome-wide map of nucleosome acetylation and methylation in yeast.
    Cell. 2005 Aug 26;122(4):517-27 PMID: 16122420
  52. Single-nucleosome mapping of histone modifications in S. cerevisiae.
    PLoS Biol. 2005 Oct;3(10):e328 PMID: 16122352
  53. Assembly of variant histones into chromatin.
    Annu Rev Cell Dev Biol. 2005;21:133-53 PMID: 16212490
  54. Genome-wide dynamics of Htz1, a histone H2A variant that poises repressed/basal promoters for activation through histone loss.
    Cell. 2005 Oct 21;123(2):219-31 PMID: 16239141
  55. Histone variant H2A.Z marks the 5' ends of both active and inactive genes in euchromatin.
    Cell. 2005 Oct 21;123(2):233-48 PMID: 16239142
  56. Preferential occupancy of histone variant H2AZ at inactive promoters influences local histone modifications and chromatin remodeling.
    Proc Natl Acad Sci U S A. 2005 Dec 20;102(51):18385-90 PMID: 16344463
  57. The Saccharomyces cerevisiae histone H2A variant Htz1 is acetylated by NuA4.
    Genes Dev. 2006 Mar 15;20(6):660-5 PMID: 16543219
  58. Telomeric heterochromatin boundaries require NuA4-dependent acetylation of histone variant H2A.Z in Saccharomyces cerevisiae.
    Genes Dev. 2006 Mar 15;20(6):700-10 PMID: 16543222
  59. Acetylation of H2AZ Lys 14 is associated with genome-wide gene activity in yeast.
    Genes Dev. 2006 Mar 15;20(6):711-22 PMID: 16543223
  60. Histones and histone modifications.
    Curr Biol. 2004 Jul 27;14(14):R546-51 PMID: 15268870
  61. Recruitment of the NuA4 complex poises the PHO5 promoter for chromatin remodeling and activation.
    EMBO J. 2004 Jul 7;23(13):2597-607 PMID: 15175650
  62. Histone H2A.Z regulats transcription and is partially redundant with nucleosome remodeling complexes.
    Cell. 2000 Oct 27;103(3):411-22 PMID: 11081628
  63. The Isw2 chromatin remodeling complex represses early meiotic genes upon recruitment by Ume6p.
    Cell. 2000 Oct 27;103(3):423-33 PMID: 11081629
  64. Direct physical and functional interaction of the NuA4 complex components Yaf9p and Swc4p.
    Eukaryot Cell. 2004 Aug;3(4):976-83 PMID: 15302830
Article Info
Journal
Molecular and cellular biology
Abbr.
Mol Cell Biol
ISSN
0270-7306
Published
2006-08-00
Pages
6117-29
Language
English
Region
United States
NLM ID
8109087
PMCID
PMC1592817
Subset
IM
Grants
NIGMS NIH HHS · R01 GM058465 · United States
NIGMS NIH HHS · R01 GM062970 · United States
NIGMS NIH HHS · GM58465 · United States
NIGMS NIH HHS · GM62970 · United States
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