Home LiteratureArticle Details
PMID: 16199876 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. Research Support, U.S. Gov't, P.H.S.

Domain-wide displacement of histones by activated heat shock factor occurs independently of Swi/Snf and is not correlated with RNA polymerase II density.

Molecular and cellular biology ·Vol. 25 ·No. 20 ·2005-10-00 ·Pages 8985-99

Zhao J, Herrera-Diaz J, Gross DS

Abstract

We show that histone-DNA interactions are disrupted across entire yeast heat shock genes upon their transcriptional activation. At HSP82, nucleosomal disassembly spans a domain of approximately 3 kb, beginning upstream of the promoter and extending through the transcribed region. A kinetic analysis reveals that histone H4 loses contact with DNA within 45 s of thermal upshift. Nucleosomal reassembly, prompted by temperature downshift, is also rapid, detectable within 60 s. Prior to their eviction, promoter-associated histones are transiently hyperacetylated, while those in the coding region are not. An upstream activation sequence mutation that weakens the binding of heat shock factor obviates domain-wide remodeling, while deletion of the TATA box that nearly abolishes transcription is permissive to 5'-end remodeling. The Swi/Snf complex is rapidly recruited to HSP82 upon heat shock. Nonetheless, domain-wide remodeling occurs efficiently in Swi/Snf mutants despite a sixfold reduction in transcription; it is also seen in gcn5Delta, set1Delta, and paf1Delta mutants. Contrary to current models, we demonstrate that a high density of RNA polymerase (Pol) is insufficient to elicit histone displacement. This finding suggests that histone eviction is modulated by factors that are not linked to elongating Pol II. It further suggests that histone depletion plays a causal role in mediating vigorous transcription in vivo and is not merely a consequence of it.

MeSH Terms
3' Untranslated Regions Acetylation Base Sequence Chromatin Assembly and Disassembly DNA, Fungal/genetics,metabolism Genes, Fungal HSP90 Heat-Shock Proteins/genetics,metabolism Heat-Shock Response Histones/metabolism Kinetics Nucleosomes/metabolism Open Reading Frames Promoter Regions, Genetic RNA Polymerase II/metabolism Saccharomyces cerevisiae/genetics,metabolism Saccharomyces cerevisiae Proteins/genetics,metabolism Transcription Factors/genetics,metabolism Transcription, Genetic
Chemicals
3' Untranslated Regions DNA, Fungal HSP82 protein, S cerevisiae HSP90 Heat-Shock Proteins Histones Nucleosomes Saccharomyces cerevisiae Proteins Transcription Factors RNA Polymerase II
Authors & Affiliations
3 authors, click to expand affiliations / ORCID
Zhao Jing
Department of Biochemistry and Molecular Biology, Louisiana State University Health Sciences Center, Shreveport, 71130-3932, USA.
Herrera-Diaz Jorge
Gross David S
References (93)
93 references, click to expand
  1. Nucleosome remodeling induced by RNA polymerase II: loss of the H2A/H2B dimer during transcription.
    Mol Cell. 2002 Mar;9(3):541-52 PMID: 11931762
  2. Exchange of RNA polymerase II initiation and elongation factors during gene expression in vivo.
    Mol Cell. 2002 Apr;9(4):799-809 PMID: 11983171
  3. Dot1p modulates silencing in yeast by methylation of the nucleosome core.
    Cell. 2002 Jun 14;109(6):745-56 PMID: 12086673
  4. Histone variants and nucleosome deposition pathways.
    Mol Cell. 2002 Jun;9(6):1158-60 PMID: 12086613
  5. The histone variant H3.3 marks active chromatin by replication-independent nucleosome assembly.
    Mol Cell. 2002 Jun;9(6):1191-200 PMID: 12086617
  6. Active genes are tri-methylated at K4 of histone H3.
    Nature. 2002 Sep 26;419(6905):407-11 PMID: 12353038
  7. Function and selectivity of bromodomains in anchoring chromatin-modifying complexes to promoter nucleosomes.
    Cell. 2002 Nov 1;111(3):369-79 PMID: 12419247
  8. Deciphering the transcriptional histone acetylation code for a human gene.
    Cell. 2002 Nov 1;111(3):381-92 PMID: 12419248
  9. Transcriptional inhibition of genes with severe histone h3 hypoacetylation in the coding region.
    Mol Cell. 2002 Oct;10(4):925-33 PMID: 12419235
  10. Dynamic chromatin alterations triggered by natural and synthetic activation domains.
    J Biol Chem. 2003 Mar 7;278(10):7755-64 PMID: 12499367
  11. A multiplicity of coactivators is required by Gcn4p at individual promoters in vivo.
    Mol Cell Biol. 2003 Apr;23(8):2800-20 PMID: 12665580
  12. Targeted recruitment of Set1 histone methylase by elongating Pol II provides a localized mark and memory of recent transcriptional activity.
    Mol Cell. 2003 Mar;11(3):709-19 PMID: 12667453
  13. Independent recruitment in vivo by Gal4 of two complexes required for transcription.
    Mol Cell. 2003 May;11(5):1301-9 PMID: 12769853
  14. Localized recruitment of a chromatin-remodeling activity by an activator in vivo drives transcriptional elongation.
    Genes Dev. 2003 Jun 1;17(11):1392-401 PMID: 12782657
  15. Nucleosomes unfold completely at a transcriptionally active promoter.
    Mol Cell. 2003 Jun;11(6):1587-98 PMID: 12820971
  16. Histones are first hyperacetylated and then lose contact with the activated PHO5 promoter.
    Mol Cell. 2003 Jun;11(6):1599-607 PMID: 12820972
  17. Yeast heat shock factor contains separable transient and sustained response transcriptional activators.
    Cell. 1990 Aug 24;62(4):793-805 PMID: 2201452
  18. The yeast heat shock transcription factor contains a transcriptional activation domain whose activity is repressed under nonshock conditions.
    Cell. 1990 Aug 24;62(4):807-17 PMID: 2201453
  19. Genomic footprinting of the yeast HSP82 promoter reveals marked distortion of the DNA helix and constitutive occupancy of heat shock and TATA elements.
    J Mol Biol. 1990 Dec 5;216(3):611-31 PMID: 2175361
  20. Transcription-induced nucleosome 'splitting': an underlying structure for DNase I sensitive chromatin.
    EMBO J. 1991 Mar;10(3):607-15 PMID: 2001676
  21. Uncoupling gene activity from chromatin structure: promoter mutations can inactivate transcription of the yeast HSP82 gene without eliminating nucleosome-free regions.
    Proc Natl Acad Sci U S A. 1992 Oct 1;89(19):9166-70 PMID: 1409619
  22. Yeast SNF/SWI transcriptional activators and the SPT/SIN chromatin connection.
    Trends Genet. 1992 Nov;8(11):387-91 PMID: 1332230
  23. A direct link between core histone acetylation and transcriptionally active chromatin.
    EMBO J. 1988 May;7(5):1395-402 PMID: 3409869
  24. Nuclease hypersensitive sites in chromatin.
    Annu Rev Biochem. 1988;57:159-97 PMID: 3052270
  25. The formation and function of DNase I hypersensitive sites in the process of gene activation.
    J Biol Chem. 1988 Dec 25;263(36):19259-62 PMID: 3198625
  26. Basal-level expression of the yeast HSP82 gene requires a heat shock regulatory element.
    Mol Cell Biol. 1989 Nov;9(11):4789-98 PMID: 2689867
  27. Affinity chromatography of mammalian and yeast nucleosomes. Two modes of binding of transcriptionally active mammalian nucleosomes to organomercurial-agarose columns, and contrasting behavior of the active nucleosomes of yeast.
    J Biol Chem. 1990 Apr 5;265(10):5736-46 PMID: 2180934
  28. In vivo studies on the dynamics of histone-DNA interaction: evidence for nucleosome dissolution during replication and transcription and a low level of dissolution independent of both.
    Biochemistry. 1990 Jan 23;29(3):719-31 PMID: 1692479
  29. 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
  30. Conditional silencing: the HMRE mating-type silencer exerts a rapidly reversible position effect on the yeast HSP82 heat shock gene.
    Mol Cell Biol. 1993 Feb;13(2):727-38 PMID: 8423797
  31. Cells in stress: transcriptional activation of heat shock genes.
    Science. 1993 Mar 5;259(5100):1409-10 PMID: 8451637
  32. Transcriptional silencing in yeast is associated with reduced nucleosome acetylation.
    Genes Dev. 1993 Apr;7(4):592-604 PMID: 8458576
  33. Chromatin structures and transcription of rDNA in yeast Saccharomyces cerevisiae.
    Nucleic Acids Res. 1993 May 25;21(10):2331-8 PMID: 8506130
  34. A critical role for heat shock transcription factor in establishing a nucleosome-free region over the TATA-initiation site of the yeast HSP82 heat shock gene.
    EMBO J. 1993 Oct;12(10):3931-45 PMID: 8404861
  35. Multiple protein-DNA interactions over the yeast HSC82 heat shock gene promoter.
    Nucleic Acids Res. 1995 May 25;23(10):1822-9 PMID: 7784189
  36. Msn2p, a zinc finger DNA-binding protein, is the transcriptional activator of the multistress response in Saccharomyces cerevisiae.
    Proc Natl Acad Sci U S A. 1996 Jun 11;93(12):5777-82 PMID: 8650168
  37. A new efficient gene disruption cassette for repeated use in budding yeast.
    Nucleic Acids Res. 1996 Jul 1;24(13):2519-24 PMID: 8692690
  38. Transcription-linked acetylation by Gcn5p of histones H3 and H4 at specific lysines.
    Nature. 1996 Sep 19;383(6597):269-72 PMID: 8805705
  39. Crystal structure of the nucleosome core particle at 2.8 A resolution.
    Nature. 1997 Sep 18;389(6648):251-60 PMID: 9305837
  40. Disruption of downstream chromatin directed by a transcriptional activator.
    Genes Dev. 1997 Dec 1;11(23):3116-21 PMID: 9389644
  41. Histones H3 and H4 are components of upstream activation factor required for the high-level transcription of yeast rDNA by RNA polymerase I.
    Proc Natl Acad Sci U S A. 1997 Dec 9;94(25):13458-62 PMID: 9391047
  42. Histone acetyltransferase activity of yeast Gcn5p is required for the activation of target genes in vivo.
    Genes Dev. 1998 Mar 1;12(5):627-39 PMID: 9499399
  43. Histone acetylation facilitates RNA polymerase II transcription of the Drosophila hsp26 gene in chromatin.
    EMBO J. 1998 May 15;17(10):2865-76 PMID: 9582280
  44. Transcriptional activation independent of TFIIH kinase and the RNA polymerase II mediator in vivo.
    Nature. 1998 May 28;393(6683):389-92 PMID: 9620805
  45. Transcriptional activators direct histone acetyltransferase complexes to nucleosomes.
    Nature. 1998 Jul 30;394(6692):498-502 PMID: 9697775
  46. Activated transcription independent of the RNA polymerase II holoenzyme in budding yeast.
    Genes Dev. 1998 Aug 15;12(16):2510-21 PMID: 9716404
  47. 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
  48. The histone H3-like TAF is broadly required for transcription in yeast.
    Mol Cell. 1998 Nov;2(5):675-82 PMID: 9844639
  49. Cooperative binding of heat shock factor to the yeast HSP82 promoter in vivo and in vitro.
    Mol Cell Biol. 1999 Mar;19(3):1627-39 PMID: 10022851
  50. Cell cycle-regulated histone acetylation required for expression of the yeast HO gene.
    Genes Dev. 1999 Jun 1;13(11):1412-21 PMID: 10364158
  51. Epitope tagging of yeast genes using a PCR-based strategy: more tags and improved practical routines.
    Yeast. 1999 Jul;15(10B):963-72 PMID: 10407276
  52. Evidence for eviction and rapid deposition of histones upon transcriptional elongation by RNA polymerase II.
    Mol Cell Biol. 2004 Dec;24(23):10111-7 PMID: 15542822
  53. Changes in genomewide occupancy of core transcriptional regulators during heat stress.
    Proc Natl Acad Sci U S A. 2004 Nov 30;101(48):16843-8 PMID: 15548603
  54. Replication-independent core histone dynamics at transcriptionally active loci in vivo.
    Genes Dev. 2005 Mar 15;19(6):677-82 PMID: 15769942
  55. Identification of a novel class of target genes and a novel type of binding sequence of heat shock transcription factor in Saccharomyces cerevisiae.
    J Biol Chem. 2005 Mar 25;280(12):11911-9 PMID: 15647283
  56. Transcriptional activation triggers deposition and removal of the histone variant H3.3.
    Genes Dev. 2005 Apr 1;19(7):804-14 PMID: 15774717
  57. Function of a eukaryotic transcription activator during the transcription cycle.
    Mol Cell. 2005 Apr 29;18(3):369-78 PMID: 15866178
  58. Altered nucleosome occupancy and histone H3K4 methylation in response to 'transcriptional stress'.
    EMBO J. 2005 Jul 6;24(13):2379-90 PMID: 15944735
  59. Methylation of histone H3 K4 mediates association of the Isw1p ATPase with chromatin.
    Mol Cell. 2003 Nov;12(5):1325-32 PMID: 14636589
  60. ATP-driven exchange of histone H2AZ variant catalyzed by SWR1 chromatin remodeling complex.
    Science. 2004 Jan 16;303(5656):343-8 PMID: 14645854
  61. Activation of the Saccharomyces cerevisiae heat shock transcription factor under glucose starvation conditions by Snf1 protein kinase.
    J Biol Chem. 2004 Feb 13;279(7):5169-76 PMID: 14612437
  62. In vivo target of a transcriptional activator revealed by fluorescence resonance energy transfer.
    Genes Dev. 2004 Feb 1;18(3):333-43 PMID: 14871930
  63. Transcription through chromatin: understanding a complex FACT.
    Biochim Biophys Acta. 2004 Mar 15;1677(1-3):87-99 PMID: 15020050
  64. 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
  65. The Paf1 complex has functions independent of actively transcribing RNA polymerase II.
    Mol Cell. 2004 May 21;14(4):447-56 PMID: 15149594
  66. Genome-wide analysis of the biology of stress responses through heat shock transcription factor.
    Mol Cell Biol. 2004 Jun;24(12):5249-56 PMID: 15169889
  67. The histone modification pattern of active genes revealed through genome-wide chromatin analysis of a higher eukaryote.
    Genes Dev. 2004 Jun 1;18(11):1263-71 PMID: 15175259
  68. Chromatin disassembly mediated by the histone chaperone Asf1 is essential for transcriptional activation of the yeast PHO5 and PHO8 genes.
    Mol Cell. 2004 Jun 4;14(5):657-66 PMID: 15175160
  69. Evidence for nucleosome depletion at active regulatory regions genome-wide.
    Nat Genet. 2004 Aug;36(8):900-5 PMID: 15247917
  70. Elongation by RNA polymerase II: the short and long of it.
    Genes Dev. 2004 Oct 15;18(20):2437-68 PMID: 15489290
  71. Evidence for distinct mechanisms facilitating transcript elongation through chromatin in vivo.
    EMBO J. 2004 Oct 27;23(21):4243-52 PMID: 15457216
  72. Chromosomal subunits in active genes have an altered conformation.
    Science. 1976 Sep 3;193(4256):848-56 PMID: 948749
  73. Selective digestion of transcriptionally active ovalbumin genes from oviduct nuclei.
    Proc Natl Acad Sci U S A. 1976 Nov;73(11):3966-70 PMID: 1069279
  74. DNA associated with hyperacetylated histone is preferentially digested by DNase I.
    Nucleic Acids Res. 1978 Jun;5(6):1863-76 PMID: 673837
  75. The histone core complex: an octamer assembled by two sets of protein-protein interactions.
    Biochemistry. 1978 Nov 14;17(23):4955-64 PMID: 718868
  76. Eukaryotic RNA polymerase II binds to nucleosome cores from transcribed genes.
    Nature. 1983 Feb 10;301(5900):482-8 PMID: 6823327
  77. Reversible changes in nucleosome structure and histone H3 accessibility in transcriptionally active and inactive states of rDNA chromatin.
    Cell. 1983 Oct;34(3):1033-42 PMID: 6313204
  78. Complete sequence of the heat shock-inducible HSP90 gene of Saccharomyces cerevisiae.
    J Biol Chem. 1984 May 10;259(9):5745-51 PMID: 6325446
  79. Sharp boundaries demarcate the chromatin structure of a yeast heat-shock gene.
    J Mol Biol. 1987 Jan 5;193(1):71-80 PMID: 3295258
  80. Deposition of newly synthesized histones: hybrid nucleosomes are not tandemly arranged on daughter DNA strands.
    Biochemistry. 1988 Mar 22;27(6):2109-20 PMID: 3378048
  81. Transcriptional activation in yeast cells lacking transcription factor IIA.
    Genetics. 1999 Dec;153(4):1573-81 PMID: 10581267
  82. SIR repression of a yeast heat shock gene: UAS and TATA footprints persist within heterochromatin.
    EMBO J. 1999 Dec 15;18(24):7041-55 PMID: 10601026
  83. The language of covalent histone modifications.
    Nature. 2000 Jan 6;403(6765):41-5 PMID: 10638745
  84. Mammalian SWI-SNF complexes contribute to activation of the hsp70 gene.
    Mol Cell Biol. 2000 Apr;20(8):2839-51 PMID: 10733587
  85. Cell cycle-dependent binding of yeast heat shock factor to nucleosomes.
    Mol Cell Biol. 2000 Sep;20(17):6435-48 PMID: 10938121
  86. Dynamic association of capping enzymes with transcribing RNA polymerase II.
    Genes Dev. 2000 Oct 1;14(19):2435-40 PMID: 11018011
  87. Hsf1p and Msn2/4p cooperate in the expression of Saccharomyces cerevisiae genes HSP26 and HSP104 in a gene- and stress type-dependent manner.
    Mol Microbiol. 2001 Mar;39(6):1523-32 PMID: 11260469
  88. Histone acetylation at promoters is differentially affected by specific activators and repressors.
    Mol Cell Biol. 2001 Apr;21(8):2726-35 PMID: 11283252
  89. Transitions in histone acetylation reveal boundaries of three separately regulated neighboring loci.
    EMBO J. 2001 May 1;20(9):2224-35 PMID: 11331588
  90. Silenced chromatin is permissive to activator binding and PIC recruitment.
    Cell. 2001 May 4;105(3):403-14 PMID: 11348596
  91. Translating the histone code.
    Science. 2001 Aug 10;293(5532):1074-80 PMID: 11498575
  92. Histone acetylation: a switch between repressive and permissive chromatin. Second in review series on chromatin dynamics.
    EMBO Rep. 2002 Mar;3(3):224-9 PMID: 11882541
  93. Dynamics of global histone acetylation and deacetylation in vivo: rapid restoration of normal histone acetylation status upon removal of activators and repressors.
    Genes Dev. 2002 Mar 15;16(6):743-52 PMID: 11914279
Article Info
Journal
Molecular and cellular biology
Abbr.
Mol Cell Biol
ISSN
0270-7306
DOI
10.1128/MCB.25.20.8985-8999.2005
Published
2005-10-00
Pages
8985-99
Language
English
Region
United States
NLM ID
8109087
PMCID
PMC1265789
Subset
IM
Grants
NIGMS NIH HHS · R01 GM045842 · United States
NIGMS NIH HHS · GM45842 · United States
External Links
PubMed source DOI: 10.1128/MCB.25.20.8985-8999.2005 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