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PMID: 20211137 Published · ppublish English Journal Article Research Support, N.I.H., Extramural Research Support, Non-U.S. Gov't

Distinct factors control histone variant H3.3 localization at specific genomic regions.

Cell ·Vol. 140 ·No. 5 ·2010-03-05 ·Pages 678-91

Goldberg AD, Banaszynski LA, Noh KM, Lewis PW, Elsaesser SJ, Stadler S, Dewell S, Law M, Guo X, Li X, Wen D, Chapgier A, DeKelver RC, Miller JC, Lee YL, Boydston EA, Holmes MC, Gregory PD, Greally JM, Rafii S, Yang C, Scambler PJ, Garrick D, Gibbons RJ, Higgs DR, Cristea IM, Urnov FD, Zheng D, Allis CD

Abstract

The incorporation of histone H3 variants has been implicated in the epigenetic memory of cellular state. Using genome editing with zinc-finger nucleases to tag endogenous H3.3, we report genome-wide profiles of H3 variants in mammalian embryonic stem cells and neuronal precursor cells. Genome-wide patterns of H3.3 are dependent on amino acid sequence and change with cellular differentiation at developmentally regulated loci. The H3.3 chaperone Hira is required for H3.3 enrichment at active and repressed genes. Strikingly, Hira is not essential for localization of H3.3 at telomeres and many transcription factor binding sites. Immunoaffinity purification and mass spectrometry reveal that the proteins Atrx and Daxx associate with H3.3 in a Hira-independent manner. Atrx is required for Hira-independent localization of H3.3 at telomeres and for the repression of telomeric RNA. Our data demonstrate that multiple and distinct factors are responsible for H3.3 localization at specific genomic locations in mammalian cells.

MeSH Terms
Animals Binding Sites Cell Cycle Proteins/genetics,metabolism Embryonic Stem Cells/metabolism Genome Histone Chaperones/genetics,metabolism Histones/analysis,genetics,metabolism Mice Mice, Inbred C57BL Telomere/chemistry,metabolism Transcription Factors/genetics,metabolism Transcription Initiation Site
Chemicals
Cell Cycle Proteins Hira protein, mouse Histone Chaperones Histones Transcription Factors
Authors & Affiliations
29 authors, click to expand affiliations / ORCID
Goldberg Aaron D
Laboratory of Chromatin Biology and Epigenetics, The Rockefeller University, 1230 York Avenue, New York, NY 10065, USA.
Banaszynski Laura A
Noh Kyung-Min
Lewis Peter W
Elsaesser Simon J
Stadler Sonja
Dewell Scott
Law Martin
Guo Xingyi
Li Xuan
Wen Duancheng
Chapgier Ariane
DeKelver Russell C
Miller Jeffrey C
Lee Ya-Li
Boydston Elizabeth A
Holmes Michael C
Gregory Philip D
Greally John M
Rafii Shahin
Yang Chingwen
Scambler Peter J
Garrick David
Gibbons Richard J
Higgs Douglas R
Cristea Ileana M
Urnov Fyodor D
Zheng Deyou
Allis C David
References (70)
70 references, click to expand
  1. Highly efficient endogenous human gene correction using designed zinc-finger nucleases.
    Nature. 2005 Jun 2;435(7042):646-51 PMID: 15806097
  2. Niche-independent symmetrical self-renewal of a mammalian tissue stem cell.
    PLoS Biol. 2005 Sep;3(9):e283 PMID: 16086633
  3. Genome-scale profiling of histone H3.3 replacement patterns.
    Nat Genet. 2005 Oct;37(10):1090-7 PMID: 16155569
  4. The histone H3.3 chaperone HIRA is essential for chromatin assembly in the male pronucleus.
    Nature. 2005 Oct 27;437(7063):1386-90 PMID: 16251970
  5. Fluorescent proteins as proteomic probes.
    Mol Cell Proteomics. 2005 Dec;4(12):1933-41 PMID: 16155292
  6. Histone H3.3 deposition at E2F-regulated genes is linked to transcription.
    EMBO Rep. 2006 Jan;7(1):66-71 PMID: 16258499
  7. Hyperdynamic plasticity of chromatin proteins in pluripotent embryonic stem cells.
    Dev Cell. 2006 Jan;10(1):105-16 PMID: 16399082
  8. Expression patterns and post-translational modifications associated with mammalian histone H3 variants.
    J Biol Chem. 2006 Jan 6;281(1):559-68 PMID: 16267050
  9. Distribution of histone H3.3 in hematopoietic cell lineages.
    Proc Natl Acad Sci U S A. 2006 Jan 17;103(3):574-9 PMID: 16407103
  10. A genome-wide analysis of CpG dinucleotides in the human genome distinguishes two distinct classes of promoters.
    Proc Natl Acad Sci U S A. 2006 Jan 31;103(5):1412-7 PMID: 16432200
  11. A bivalent chromatin structure marks key developmental genes in embryonic stem cells.
    Cell. 2006 Apr 21;125(2):315-26 PMID: 16630819
  12. Histone H3 variants and their potential role in indexing mammalian genomes: the "H3 barcode hypothesis".
    Proc Natl Acad Sci U S A. 2006 Apr 25;103(17):6428-35 PMID: 16571659
  13. Loss of Atrx affects trophoblast development and the pattern of X-inactivation in extraembryonic tissues.
    PLoS Genet. 2006 Apr;2(4):e58 PMID: 16628246
  14. Epigenetics: a landscape takes shape.
    Cell. 2007 Feb 23;128(4):635-8 PMID: 17320500
  15. The mammalian epigenome.
    Cell. 2007 Feb 23;128(4):669-81 PMID: 17320505
  16. Distinct and predictive chromatin signatures of transcriptional promoters and enhancers in the human genome.
    Nat Genet. 2007 Mar;39(3):311-8 PMID: 17277777
  17. Drosophila GAGA factor directs histone H3.3 replacement that prevents the heterochromatin spreading.
    Genes Dev. 2007 Mar 1;21(5):552-61 PMID: 17344416
  18. Histone replacement marks the boundaries of cis-regulatory domains.
    Science. 2007 Mar 9;315(5817):1408-11 PMID: 17347439
  19. Targeted gene addition into a specified location in the human genome using designed zinc finger nucleases.
    Proc Natl Acad Sci U S A. 2007 Feb 27;104(9):3055-60 PMID: 17360608
  20. Chromatin immunoprecipitation and microarray-based analysis of protein location.
    Nat Protoc. 2006;1(2):729-48 PMID: 17406303
  21. Telomeric repeat containing RNA and RNA surveillance factors at mammalian chromosome ends.
    Science. 2007 Nov 2;318(5851):798-801 PMID: 17916692
  22. Ring1-mediated ubiquitination of H2A restrains poised RNA polymerase II at bivalent genes in mouse ES cells.
    Nat Cell Biol. 2007 Dec;9(12):1428-35 PMID: 18037880
  23. Nucleosome destabilization in the epigenetic regulation of gene expression.
    Nat Rev Genet. 2008 Jan;9(1):15-26 PMID: 18059368
  24. Developmentally regulated transcription of mammalian telomeres by DNA-dependent RNA polymerase II.
    Nat Cell Biol. 2008 Feb;10(2):228-36 PMID: 18157120
  25. Dynamic regulation of nucleosome positioning in the human genome.
    Cell. 2008 Mar 7;132(5):887-98 PMID: 18329373
  26. Mutations in the chromatin-associated protein ATRX.
    Hum Mutat. 2008 Jun;29(6):796-802 PMID: 18409179
  27. Heritable targeted gene disruption in zebrafish using designed zinc-finger nucleases.
    Nat Biotechnol. 2008 Jun;26(6):702-8 PMID: 18500334
  28. Integration of external signaling pathways with the core transcriptional network in embryonic stem cells.
    Cell. 2008 Jun 13;133(6):1106-17 PMID: 18555785
  29. Combinatorial patterns of histone acetylations and methylations in the human genome.
    Nat Genet. 2008 Jul;40(7):897-903 PMID: 18552846
  30. Stem cell transcriptome profiling via massive-scale mRNA sequencing.
    Nat Methods. 2008 Jul;5(7):613-9 PMID: 18516046
  31. The epigenetics of rRNA genes: from molecular to chromosome biology.
    Annu Rev Cell Dev Biol. 2008;24:131-57 PMID: 18616426
  32. Progress and prospects: zinc-finger nucleases as gene therapy agents.
    Gene Ther. 2008 Nov;15(22):1463-8 PMID: 18784746
  33. H3.3/H2A.Z double variant-containing nucleosomes mark 'nucleosome-free regions' of active promoters and other regulatory regions.
    Nat Genet. 2009 Aug;41(8):941-5 PMID: 19633671
  34. Transcription in the absence of histone H3.3.
    Curr Biol. 2009 Jul 28;19(14):1221-6 PMID: 19523831
  35. Chd1 regulates open chromatin and pluripotency of embryonic stem cells.
    Nature. 2009 Aug 13;460(7257):863-8 PMID: 19587682
  36. The XNP remodeler targets dynamic chromatin in Drosophila.
    Proc Natl Acad Sci U S A. 2009 Aug 25;106(34):14472-7 PMID: 19706533
  37. TERRA: telomeric repeat-containing RNA.
    EMBO J. 2009 Sep 2;28(17):2503-10 PMID: 19629047
  38. Transcriptional and developmental functions of the H3.3 histone variant in Drosophila.
    Curr Biol. 2009 Nov 17;19(21):1816-20 PMID: 19781938
  39. Genome-wide maps of chromatin state in pluripotent and lineage-committed cells.
    Nature. 2007 Aug 2;448(7153):553-60 PMID: 17603471
  40. CHD1 motor protein is required for deposition of histone variant H3.3 into chromatin in vivo.
    Science. 2007 Aug 24;317(5841):1087-90 PMID: 17717186
  41. Marking histone H3 variants: how, when and why?
    Trends Biochem Sci. 2007 Sep;32(9):425-33 PMID: 17764953
  42. The essential role of Drosophila HIRA for de novo assembly of paternal chromatin at fertilization.
    PLoS Genet. 2007 Oct;3(10):1991-2006 PMID: 17967064
  43. H2AZ is enriched at polycomb complex target genes in ES cells and is necessary for lineage commitment.
    Cell. 2008 Nov 14;135(4):649-61 PMID: 18992931
  44. Telomeres acquire embryonic stem cell characteristics in induced pluripotent stem cells.
    Cell Stem Cell. 2009 Feb 6;4(2):141-54 PMID: 19200803
  45. Genome-wide profiling of salt fractions maps physical properties of chromatin.
    Genome Res. 2009 Mar;19(3):460-9 PMID: 19088306
  46. Histone H3.3 incorporation provides a unique and functionally essential telomeric chromatin in embryonic stem cells.
    Genome Res. 2009 Mar;19(3):404-14 PMID: 19196724
  47. Dynamic histone variant exchange accompanies gene induction in T cells.
    Mol Cell Biol. 2009 Apr;29(7):1972-86 PMID: 19158270
  48. Chromatin signature reveals over a thousand highly conserved large non-coding RNAs in mammals.
    Nature. 2009 Mar 12;458(7235):223-7 PMID: 19182780
  49. Inducible deposition of the histone variant H3.3 in interferon-stimulated genes.
    J Biol Chem. 2009 May 1;284(18):12217-25 PMID: 19244243
  50. Four histone variants mark the boundaries of polycistronic transcription units in Trypanosoma brucei.
    Genes Dev. 2009 May 1;23(9):1063-76 PMID: 19369410
  51. Chromatin-based transcriptional punctuation.
    Genes Dev. 2009 May 1;23(9):1037-41 PMID: 19417102
  52. Mammalian telomeres resemble fragile sites and require TRF1 for efficient replication.
    Cell. 2009 Jul 10;138(1):90-103 PMID: 19596237
  53. A unifying model for the selective regulation of inducible transcription by CpG islands and nucleosome remodeling.
    Cell. 2009 Jul 10;138(1):114-28 PMID: 19596239
  54. Resolving the composition of protein complexes using a MALDI LTQ Orbitrap.
    J Am Soc Mass Spectrom. 2010 Jan;21(1):34-46 PMID: 19822444
  55. ATRX interacts with H3.3 in maintaining telomere structural integrity in pluripotent embryonic stem cells.
    Genome Res. 2010 Mar;20(3):351-60 PMID: 20110566
  56. Histone chaperones: an escort network regulating histone traffic.
    Nat Struct Mol Biol. 2007 Nov;14(11):997-1007 PMID: 17984962
  57. High-resolution profiling of histone methylations in the human genome.
    Cell. 2007 May 18;129(4):823-37 PMID: 17512414
  58. A chromatin landmark and transcription initiation at most promoters in human cells.
    Cell. 2007 Jul 13;130(1):77-88 PMID: 17632057
  59. Targeted mutagenesis of the Hira gene results in gastrulation defects and patterning abnormalities of mesoendodermal derivatives prior to early embryonic lethality.
    Mol Cell Biol. 2002 Apr;22(7):2318-28 PMID: 11884616
  60. HIRA is critical for a nucleosome assembly pathway independent of DNA synthesis.
    Mol Cell. 2002 May;9(5):1091-100 PMID: 12049744
  61. The histone variant H3.3 marks active chromatin by replication-independent nucleosome assembly.
    Mol Cell. 2002 Jun;9(6):1191-200 PMID: 12086617
  62. Signalling, cell cycle and pluripotency in embryonic stem cells.
    Trends Cell Biol. 2002 Sep;12(9):432-8 PMID: 12220864
  63. The ATRX syndrome protein forms a chromatin-remodeling complex with Daxx and localizes in promyelocytic leukemia nuclear bodies.
    Proc Natl Acad Sci U S A. 2003 Sep 16;100(19):10635-40 PMID: 12953102
  64. Histone H3.1 and H3.3 complexes mediate nucleosome assembly pathways dependent or independent of DNA synthesis.
    Cell. 2004 Jan 9;116(1):51-61 PMID: 14718166
  65. From silencing to gene expression: real-time analysis in single cells.
    Cell. 2004 Mar 5;116(5):683-98 PMID: 15006351
  66. A novel transcription regulatory complex containing death domain-associated protein and the ATR-X syndrome protein.
    J Biol Chem. 2004 May 7;279(19):20369-77 PMID: 14990586
  67. Purification and characterization of CAF-I, a human cell factor required for chromatin assembly during DNA replication in vitro.
    Cell. 1989 Jul 14;58(1):15-25 PMID: 2546672
  68. Conservation of the human telomere sequence (TTAGGG)n among vertebrates.
    Proc Natl Acad Sci U S A. 1989 Sep;86(18):7049-53 PMID: 2780561
  69. ATRX encodes a novel member of the SNF2 family of proteins: mutations point to a common mechanism underlying the ATR-X syndrome.
    Hum Mol Genet. 1996 Dec;5(12):1899-907 PMID: 8968741
  70. Transcriptional activation triggers deposition and removal of the histone variant H3.3.
    Genes Dev. 2005 Apr 1;19(7):804-14 PMID: 15774717
Article Info
Journal
Cell
Abbr.
Cell
ISSN
1097-4172
Published
2010-03-05
Pages
678-91
Language
English
Region
United States
NLM ID
0413066
PMCID
PMC2885838
Subset
IM
Grants
NIDA NIH HHS · DP1 DA026192 · United States
NIDA NIH HHS · DP1 DA026192-01 · United States
British Heart Foundation · United Kingdom
NIDA NIH HHS · DP1DA026192 · United States
NIGMS NIH HHS · GM07739 · United States
NIGMS NIH HHS · R37 GM053512-30 · United States
Biotechnology and Biological Sciences Research Council · BB/E009603/1 · United Kingdom
Medical Research Council · MC_U137961147 · United Kingdom
NCRR NIH HHS · RR022220 · United States
NCRR NIH HHS · P41 RR000862 · United States
NCRR NIH HHS · U54 RR022220 · United States
Howard Hughes Medical Institute · United States
NIGMS NIH HHS · R37 GM053512 · United States
NIGMS NIH HHS · GM53512 · United States
NCRR NIH HHS · RR00862 · United States
NIGMS NIH HHS · GM53122 · United States
NIGMS NIH HHS · T32 GM007739 · United States
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