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Berkeley MCELLBI 140 - Distinct factors control histone variant H3.3 localization at specific genomic regions

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Accepted ManuscriptTitle: Distinct factors control histone variant H3.3 localizationat specific genomic regionsAuthors: Aaron D. Goldberg, Laura A. Banaszynski,Kyung-Min Noh, Peter W. Lewis, Simon J. Elsaesser, SonjaStadler, Scott Dewell, Martin Law, Xingyi Guo, Xuan Li,Duancheng Wen, Ariane Chapgier, Russell C. DeKelver,Jeffrey C. Miller, Ya-Li Lee, Elizabeth A. Boydston, MichaelC. Holmes, Philip D. Gregory, John M. Greally, Shahin Rafii,Chingwen Yang, Peter J. Scambler, David Garrick, Richard J.Gibbons, Douglas R. Higgs, Ileana M. Cristea, Fyodor D.Urnov, Deyou Zheng, C. David AllisPII: S0092-8674(10)00004-8DOI: 10.1016/j.cell.2010.01.003Reference: CELL/4956Published in: CellReceived date: 9 September 2009Revised date: 23 November 2009Accepted date: 31 December 2009Cite this article as: Goldberg AD, Banaszynski LA, Noh K-M, Lewis PW, ElsaesserSJ, Stadler S, Dewell S, Law M, Guo X, Li X, Wen D, Chapgier A, DeKelver RC,Miller JC, Lee Y-L, Boydston EA, Holmes MC, Gregory PD, Greally JM, Rafii S, YangC, Scambler PJ, Garrick D, Gibbons RJ, Higgs DR, Cristea IM, Urnov FD, Zheng D,Allis C D, Distinct factors control histone variant H3.3 localization at specific genomicregions, Cell, doi:10.1016/j.cell.2010.01.003This is a PDF file of an unedited manuscript that has been accepted for publication.As a service to our customers we are providing this early version of the manuscript.The manuscript will undergo copyediting, typesetting, and review of the resulting proofbefore it is published in its final citable form. Please note that during the productionprocess errors may be discovered which could affect the content, and all legal disclaimersthat apply to the journal pertain.© 2010 Elsevier Inc. All rights reserved.1Distinct factors control histone variant H3.3 localization at specific genomic regions Aaron D. Goldberg1, Laura A. Banaszynski1#, Kyung-Min Noh1#, Peter W. Lewis1, Simon J. Elsaesser1, Sonja Stadler1, Scott Dewell2, Martin Law4, Xingyi Guo11, Xuan Li3, Duancheng Wen5,6,7, Ariane Chapgier8, Russell C. DeKelver9, Jeffrey C. Miller9, Ya-Li Lee9, Elizabeth A. Boydston9, Michael C. Holmes9, Philip D. Gregory9, John M. Greally12,13, Shahin Rafii5,6,7, Chingwen Yang3, Peter J. Scambler8, David Garrick4, Richard J. Gibbons4, Douglas R. Higgs4, Ileana M. Cristea10, Fyodor D. Urnov9, Deyou Zheng11,13,14*, C. David Allis1* 1Laboratory of Chromatin Biology, 2Genomics Resource Center, 3Gene Targeting Resource Center, The Rockefeller University, 1230 York Avenue, New York, NY 10065, USA. 4MRC Molecular Haematology Unit, Weatherall Institute of Molecular Medicine, John Radcliffe Hospital, Headington, Oxford OX3 9DS, UK. 5Howard Hughes Medical Institute, 6Ansary Stem Cell Institute, 7Department of Genetic Medicine, Weill Cornell Medical College, New York, NY 10065, USA. 8Molecular Medicine Unit, Institute of Child Health, 30 Guilford Street, London WC1N 1EH, UK. 9Sangamo BioSciences, Inc. Pt. Richmond Tech Center 501, Canal Blvd, Suite A100 Richmond, CA 94804, USA. 10Department of Molecular Biology, Princeton University, Princeton, NJ 08544, USA. 11Department of Neurology, 12Department of Medicine, 13Department of Genetics, and 14Department of Neuroscience, Albert Einstein College of Medicine, Bronx, NY 10461, USA. #These authors contributed equally. *Contact: [email protected], [email protected] 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 (ES) 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. Introduction Genetic and biochemical evidence have recently converged to connect epigenetic mechanisms at the level of chromatin (Bernstein et al., 2007; Goldberg et al., 2007; Henikoff, 2008). In addition to nucleosome remodeling and covalent modifications, eukaryotic cells generate variation in chromatin by the introduction of variant histone proteins (Henikoff, 2008). Mammalian cells express three major types of non-centromeric histone H3 variants, H3.1, H3.2, and H3.3 (Hake and Allis, 2006; Hake et al., 2006). Although histone H3.3 differs from H3.2 and H3.1 at only 4 or 5 amino acids (Figure S1A), H3.3 is specifically enriched at transcriptionally active genes and regulatory elements in non-pluripotent cells (Ahmad and Henikoff, 2002; Jin et al., 2009; Mito et al., 2005, 2007).3 Histone H3.3 is incorporated into chromatin in both a replication-coupled (RC) and replication-independent (RI) manner, while the incorporation of H3.2 is coupled to replication (Ahmad and Henikoff, 2002; De Koning et al., 2007). The histone chaperone CAF-1 is found in a complex with H3.1, and mediates RC nucleosome assembly (Smith and Stillman, 1989; Tagami et al., 2004). In contrast, the histone chaperone Hira has been found in a complex with H3.3, and mediates RI nucleosome assembly (Ray-Gallet et al., 2002; Tagami et al., 2004). Hira has been implicated in H3.3-specific deposition and chromatin assembly (Loyola and Almouzni, 2007). Although Hira is required for chromatin assembly and H3.3 deposition in the male pronucleus of Drosophila, Hira is not required for global H3.3 deposition in Drosophila embryos or adult cells, suggesting that alternate pathways may mediate H3.3 nucleosome assembly (Bonnefoy et al., 2007; Loppin et al., 2005). Indeed, the chromatin remodeling factor CHD1 was shown to physically associate with Hira, and has been suggested to work with Hira to mediate H3.3 incorporation into chromatin in Drosophila (Konev et al., 2007). In Drosophila, both Hira and H3.3 are required for fertility and for transcriptional regulation of specific genes, but not for


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Berkeley MCELLBI 140 - Distinct factors control histone variant H3.3 localization at specific genomic regions

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