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PMID: 17158748 Published · ppublish English Journal Article Research Support, Non-U.S. Gov't

The histone variant mH2A1.1 interferes with transcription by down-regulating PARP-1 enzymatic activity.

Genes & development ·Vol. 20 ·No. 23 ·2006-12-01 ·Pages 3324-36

Ouararhni K, Hadj-Slimane R, Ait-Si-Ali S, Robin P, Mietton F, Harel-Bellan A, Dimitrov S, Hamiche A

Abstract

The histone variant mH2A is believed to be involved in transcriptional repression, but how it exerts its function remains elusive. By using chromatin immunoprecipitation and tandem affinity immunopurification of the mH2A1.1 nucleosome complex, we identified numerous genes with promoters containing mH2A1.1 nucleosomes. In particular, the promoters of the inducible Hsp70.1 and Hsp70.2 genes, but not that of the constitutively expressed Hsp70.8, were highly enriched in mH2A1.1. PARP-1 was identified as a part of the mH2A1.1 nucleosome complex and was found to be associated with the Hsp70.1 promoter. A specific interaction between mH2A1.1 and PARP-1 was demonstrated and found to be associated with inactivation of PARP-1 enzymatic activity. Heat shock released both mH2A1.1 and PARP-1 from the Hsp70.1 promoter and activated PARP-1 automodification activity. The data we present point to a novel mechanism for control of Hsp70.1 gene transcription. mH2A1.1 recruits PARP-1 to the promoter, thereby inactivating it. Upon heat shock, the Hsp70.1 promoter-bound PARP-1 is released to activate transcription through ADP-ribosylation of other Hsp70.1 promoter-bound proteins.

MeSH Terms
Chromatin/genetics,physiology Cloning, Molecular DNA Primers Gene Expression Regulation, Enzymologic Genetic Variation HSP70 Heat-Shock Proteins/genetics,metabolism HSP72 Heat-Shock Proteins/genetics,metabolism HeLa Cells Histones/genetics,isolation & purification,metabolism Humans Nucleosomes/physiology Poly (ADP-Ribose) Polymerase-1 Poly(ADP-ribose) Polymerases/genetics,metabolism Polymerase Chain Reaction RNA, Small Interfering/genetics Transcription, Genetic
Chemicals
Chromatin DNA Primers HSP70 Heat-Shock Proteins HSP72 Heat-Shock Proteins HSPA2 protein, human Histones Nucleosomes RNA, Small Interfering PARP1 protein, human Poly (ADP-Ribose) Polymerase-1 Poly(ADP-ribose) Polymerases
Authors & Affiliations
8 authors, click to expand affiliations / ORCID
Ouararhni Khalid
Laboratoire Epigénétique et Cancer, Centre National de la Recherche Scientifique FRE 2944, 94801 Villejuif, France.
Hadj-Slimane Réda
Ait-Si-Ali Slimane
Robin Philippe
Mietton Flore
Harel-Bellan Annick
Dimitrov Stefan
Hamiche Ali
References (38)
38 references, click to expand
  1. Cell cycle-dependent recruitment of HDAC-1 correlates with deacetylation of histone H4 on an Rb-E2F target promoter.
    EMBO Rep. 2001 Sep;2(9):794-9 PMID: 11520855
  2. Histone H2A variants and the inactive X chromosome: identification of a second macroH2A variant.
    Hum Mol Genet. 2001 May 1;10(10):1101-13 PMID: 11331621
  3. Chromatin loosening by poly(ADP)-ribose polymerase (PARP) at Drosophila puff loci.
    Science. 2003 Jan 24;299(5606):560-2 PMID: 12543974
  4. The histone variant macroH2A interferes with transcription factor binding and SWI/SNF nucleosome remodeling.
    Mol Cell. 2003 Apr;11(4):1033-41 PMID: 12718888
  5. PARP goes transcription.
    Cell. 2003 Jun 13;113(6):677-83 PMID: 12809599
  6. The crystal structure of AF1521 a protein from Archaeoglobus fulgidus with homology to the non-histone domain of macroH2A.
    J Mol Biol. 2003 Jul 11;330(3):503-11 PMID: 12842467
  7. Inactivating chromosomes: a macro domain that minimizes transcription.
    Mol Cell. 2003 Jul;12(1):1-3 PMID: 12887886
  8. Phylogenomics of the nucleosome.
    Nat Struct Biol. 2003 Nov;10(11):882-91 PMID: 14583738
  9. Immunoaffinity purification of mammalian protein complexes.
    Methods Enzymol. 2003;370:430-44 PMID: 14712665
  10. The PARP superfamily.
    Bioessays. 2004 Aug;26(8):882-93 PMID: 15273990
  11. Structure and expression of a human gene coding for a 71 kd heat shock 'cognate' protein.
    Nucleic Acids Res. 1987 Jul 10;15(13):5181-97 PMID: 3037489
  12. MacroH2A, a core histone containing a large nonhistone region.
    Science. 1992 Sep 4;257(5075):1398-400 PMID: 1529340
  13. Developmental and tissue expression patterns of histone macroH2A1 subtypes.
    J Cell Biochem. 1997 Apr;65(1):107-13 PMID: 9138085
  14. A hitchhiker's guide to the human Hsp70 family.
    Cell Stress Chaperones. 1996 Apr;1(1):23-8 PMID: 9222585
  15. Crystal structure of the nucleosome core particle at 2.8 A resolution.
    Nature. 1997 Sep 18;389(6648):251-60 PMID: 9305837
  16. A novel function of poly(ADP-ribosyl)ation: silencing of RNA polymerase II-dependent transcription.
    Biochemistry. 1998 Feb 10;37(6):1465-9 PMID: 9484215
  17. Evolutionary conservation of histone macroH2A subtypes and domains.
    Nucleic Acids Res. 1998 Jun 15;26(12):2837-42 PMID: 9611225
  18. Histone macroH2A1 is concentrated in the inactive X chromosome of female mammals.
    Nature. 1998 Jun 11;393(6685):599-601 PMID: 9634239
  19. Messenger RNAs encoding mouse histone macroH2A1 isoforms are expressed at similar levels in male and female cells and result from alternative splicing.
    Nucleic Acids Res. 1999 Sep 15;27(18):3685-9 PMID: 10471737
  20. Dynamic relocation of epigenetic chromatin markers reveals an active role of constitutive heterochromatin in the transition from proliferation to quiescence.
    J Cell Sci. 2004 Dec 1;117(Pt 25):6153-62 PMID: 15564378
  21. Multiple spatially distinct types of facultative heterochromatin on the human inactive X chromosome.
    Proc Natl Acad Sci U S A. 2004 Dec 14;101(50):17450-5 PMID: 15574503
  22. The ways of PARP.
    Cell. 2004 Dec 17;119(6):735-6 PMID: 15607968
  23. Activating the PARP-1 sensor component of the groucho/ TLE1 corepressor complex mediates a CaMKinase IIdelta-dependent neurogenic gene activation pathway.
    Cell. 2004 Dec 17;119(6):815-29 PMID: 15607978
  24. Transcriptional activation triggers deposition and removal of the histone variant H3.3.
    Genes Dev. 2005 Apr 1;19(7):804-14 PMID: 15774717
  25. Variant histone H3.3 marks promoters of transcriptionally active genes during mammalian cell division.
    EMBO Rep. 2005 Apr;6(4):354-60 PMID: 15776021
  26. Beyond the Xi: macroH2A chromatin distribution and post-translational modification in an avian system.
    J Biol Chem. 2005 Apr 22;280(16):16437-45 PMID: 15718235
  27. The macro domain is an ADP-ribose binding module.
    EMBO J. 2005 Jun 1;24(11):1911-20 PMID: 15902274
  28. Splicing regulates NAD metabolite binding to histone macroH2A.
    Nat Struct Mol Biol. 2005 Jul;12(7):624-5 PMID: 15965484
  29. Structural characterization of the histone variant macroH2A.
    Mol Cell Biol. 2005 Sep;25(17):7616-24 PMID: 16107708
  30. Poly(ADP-ribosyl)ation by PARP-1: 'PAR-laying' NAD+ into a nuclear signal.
    Genes Dev. 2005 Sep 1;19(17):1951-67 PMID: 16140981
  31. Mechanism of polymerase II transcription repression by the histone variant macroH2A.
    Mol Cell Biol. 2006 Feb;26(3):1156-64 PMID: 16428466
  32. MACROH2A2, a new member of the MARCOH2A core histone family.
    J Biol Chem. 2001 Jun 15;276(24):21776-84 PMID: 11262398
  33. A biochemical genomics approach for identifying genes by the activity of their products.
    Science. 1999 Nov 5;286(5442):1153-5 PMID: 10550052
  34. Characterization of the Saccharomyces cerevisiae cyclic nucleotide phosphodiesterase involved in the metabolism of ADP-ribose 1",2"-cyclic phosphate.
    Nucleic Acids Res. 2000 Apr 15;28(8):1676-83 PMID: 10734185
  35. Histone macroH2A1 is concentrated in the inactive X chromosome of female preimplantation mouse embryos.
    Development. 2000 Jun;127(11):2283-9 PMID: 10804171
  36. Dynamic relocalization of histone MacroH2A1 from centrosomes to inactive X chromosomes during X inactivation.
    J Cell Biol. 2000 Sep 4;150(5):1189-98 PMID: 10974005
  37. Structure and mechanism of activity of the cyclic phosphodiesterase of Appr>p, a product of the tRNA splicing reaction.
    EMBO J. 2000 Nov 15;19(22):6207-17 PMID: 11080166
  38. Cell cycle-dependent localization of macroH2A in chromatin of the inactive X chromosome.
    J Cell Biol. 2002 Jun 24;157(7):1113-23 PMID: 12082075
Article Info
Journal
Genes & development
Abbr.
Genes Dev
ISSN
0890-9369
Published
2006-12-01
Pages
3324-36
Language
English
Region
United States
NLM ID
8711660
PMCID
PMC1686608
Subset
IM
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