Dynamics of Histone H3 Deposition In Vivo Reveal a Nucleosome Gap-Filling Mechanism for H3.3 to Maintain Chromatin Integrity

Molecular Cell

Volumn 44, Issue 6, 2011, Pages 928-941

  Ray Gallet, Dominique ^a,b   Woolfe, Adam ^a,b   Vassias, Isabelle ^a,b   Pellentz, Céline ^a,b   Lacoste, Nicolas ^a,b   Puri, Aastha ^c   Schultz, David C ^c   Pchelintsev, Nikolay A ^d   Adams, Peter D ^d   Jansen, Lars E T ^e   Almouzni, Geneviève ^a,b  

^a INSTITUT CURIE   (France)

^b CNRS   (France)

^c WISTAR INSTITUTE   (United States)

^d BEATSON INSTITUTE FOR CANCER RESEARCH   (United Kingdom)

^e INSTITUTO GULBENKIAN DE CIÊNCIA   (Portugal)

Author keywords

[No Author keywords available]

Indexed keywords

CHAPERONE; CHROMATIN ASSEMBLY FACTOR 1; HIRA PROTEIN; HISTONE H3; UNCLASSIFIED DRUG;

ARTICLE; CELL CYCLE; CHROMATIN IMMUNOPRECIPITATION; CHROMATIN STRUCTURE; COMPLEX FORMATION; CONTROLLED STUDY; DNA REPLICATION; FEMALE; HUMAN; HUMAN CELL; IN VIVO STUDY; MOLECULAR DYNAMICS; NUCLEOSOME; NUCLEOTIDE SEQUENCE; PROTEIN AGGREGATION; PROTEIN DEPLETION; PROTEIN DNA BINDING; REGULATORY SEQUENCE; SIGNAL TRANSDUCTION;

CELL CYCLE PROTEINS; CHROMATIN ASSEMBLY FACTOR-1; DEOXYRIBONUCLEASES; DNA REPLICATION; HELA CELLS; HISTONE CHAPERONES; HISTONES; HUMANS; MOLECULAR CHAPERONES; NUCLEOSOMES; RNA POLYMERASE II; TRANSCRIPTION FACTORS;

EID: 84255162049     PISSN: 10972765     EISSN: 10974164     Source Type: Journal    
DOI: 10.1016/j.molcel.2011.12.006     Document Type: Article

References (64)

1. Ahmad K., Henikoff S. The histone variant H3.3 marks active chromatin by replication-independent nucleosome assembly. Mol. Cell 2002, 9:1191-1200.
2. Aït-Ahmed O., Bellon B., Capri M., Joblet C., Thomas-Delaage M. The yemanuclein-alpha: a new Drosophila DNA binding protein specific for the oocyte nucleus. Mech. Dev. 1992, 37:69-80.
3. Amin A.D., Vishnoi N., Prochasson P. A global requirement for the HIR complex in the assembly of chromatin. Biochim. Biophys. Acta 2011, in press. Published online July 23, 2011.
4. Anderson H.E., Kagansky A., Wardle J., Rappsilber J., Allshire R.C., Whitehall S.K. Silencing mediated by the Schizosaccharomyces pombe HIRA complex is dependent upon the Hpc2-like protein, Hip4. PLoS ONE 2010, 5:e13488.
5. Balaji S., Iyer L.M., Aravind L. HPC2 and ubinuclein define a novel family of histone chaperones conserved throughout eukaryotes. Mol. Biosyst. 2009, 5:269-275.
6. Banumathy G., Somaiah N., Zhang R., Tang Y., Hoffmann J., Andrake M., Ceulemans H., Schultz D., Marmorstein R., Adams P.D. Human UBN1 is an ortholog of yeast Hpc2p and has an essential role in the HIRA/ASF1a chromatin-remodeling pathway in senescent cells. Mol. Cell. Biol. 2009, 29:758-770.
7. Brookes E., Pombo A. Modifications of RNA polymerase II are pivotal in regulating gene expression states. EMBO Rep. 2009, 10:1213-1219.
8. Buratowski S. Progression through the RNA polymerase II CTD cycle. Mol. Cell 2009, 36:541-546.
9. Chen X., Xu H., Yuan P., Fang F., Huss M., Vega V.B., Wong E., Orlov Y.L., Zhang W., Jiang J., et al. Integration of external signaling pathways with the core transcriptional network in embryonic stem cells. Cell 2008, 133:1106-1117.
10. Core L.J., Lis J.T. Transcription regulation through promoter-proximal pausing of RNA polymerase II. Science 2008, 319:1791-1792.
11. Corpet A., Almouzni G. Making copies of chromatin: the challenge of nucleosomal organization and epigenetic information. Trends Cell Biol. 2009, 19:29-41.
12. Corpet A., De Koning L., Toedling J., Savignoni A., Berger F., Lemaître C., O'Sullivan R.J., Karlseder J., Barillot E., Asselain B., et al. Asf1b, the necessary Asf1 isoform for proliferation, is predictive of outcome in breast cancer. EMBO J. 2011, 30:480-493.
13. Creyghton M.P., Cheng A.W., Welstead G.G., Kooistra T., Carey B.W., Steine E.J., Hanna J., Lodato M.A., Frampton G.M., Sharp P.A., et al. Histone H3K27ac separates active from poised enhancers and predicts developmental state. Proc. Natl. Acad. Sci. USA 2010, 107:21931-21936.
14. Cui B., Liu Y., Gorovsky M.A. Deposition and function of histone H3 variants in Tetrahymena thermophila. Mol. Cell. Biol. 2006, 26:7719-7730.
15. De Koning L., Corpet A., Haber J.E., Almouzni G. Histone chaperones: an escort network regulating histone traffic. Nat. Struct. Mol. Biol. 2007, 14:997-1007.
16. Deal R.B., Henikoff J.G., Henikoff S. Genome-wide kinetics of nucleosome turnover determined by metabolic labeling of histones. Science 2010, 328:1161-1164.
17. Drané P., Ouararhni K., Depaux A., Shuaib M., Hamiche A. The death-associated protein DAXX is a novel histone chaperone involved in the replication-independent deposition of H3.3. Genes Dev. 2010, 24:1253-1265.
18. Dunleavy E.M., Almouzni G., Karpen G.H. H3.3 is deposited at centromeres in S phase as a placeholder for newly assembled CENP-A in G1 phase. Nucleus 2011, 2:1-12.
19. Elsaesser S.J., Allis C.D. HIRA and Daxx constitute two independent histone H3.3-containing predeposition complexes. Cold Spring Harb. Symp. Quant. Biol. 2010, 75:27-34.
20. Foltz D.R., Jansen L.E., Bailey A.O., Yates J.R., Bassett E.A., Wood S., Black B.E., Cleveland D.W. Centromere-specific assembly of CENP-a nucleosomes is mediated by HJURP. Cell 2009, 137:472-484.
21. Gaillard P.H., Martini E.M., Kaufman P.D., Stillman B., Moustacchi E., Almouzni G. Chromatin assembly coupled to DNA repair: a new role for chromatin assembly factor I. Cell 1996, 86:887-896.
22. Glover-Cutter K., Kim S., Espinosa J., Bentley D.L. RNA polymerase II pauses and associates with pre-mRNA processing factors at both ends of genes. Nat. Struct. Mol. Biol. 2008, 15:71-78.
23. Goldberg A.D., Banaszynski L.A., Noh K.M., Lewis P.W., Elsaesser S.J., Stadler S., Dewell S., Law M., Guo X., Li X., et al. Distinct factors control histone variant H3.3 localization at specific genomic regions. Cell 2010, 140:678-691.
24. Groth A., Rocha W., Verreault A., Almouzni G. Chromatin challenges during DNA replication and repair. Cell 2007, 128:721-733.
25. Jansen L.E., Black B.E., Foltz D.R., Cleveland D.W. Propagation of centromeric chromatin requires exit from mitosis. J. Cell Biol. 2007, 176:795-805.
26. Jiao Y., Shi C., Edil B.H., de Wilde R.F., Klimstra D.S., Maitra A., Schulick R.D., Tang L.H., Wolfgang C.L., Choti M.A., et al. DAXX/ATRX, MEN1, and mTOR pathway genes are frequently altered in pancreatic neuroendocrine tumors. Science 2011, 331:1199-1203.
27. Jin C., Zang C., Wei G., Cui K., Peng W., Zhao K., Felsenfeld G. H3.3/H2A.Z double variant-containing nucleosomes mark 'nucleosome-free regions' of active promoters and other regulatory regions. Nat. Genet. 2009, 41:941-945.
28. Kaufman P.D., Rando O.J. Chromatin as a potential carrier of heritable information. Curr. Opin. Cell Biol. 2010, 22:284-290.
29. Keppler A., Gendreizig S., Gronemeyer T., Pick H., Vogel H., Johnsson K. A general method for the covalent labeling of fusion proteins with small molecules in vivo. Nat. Biotechnol. 2003, 21:86-89.
30. Kouzarides T. Chromatin modifications and their function. Cell 2007, 128:693-705.
31. Law M.J., Lower K.M., Voon H.P., Hughes J.R., Garrick D., Viprakasit V., Mitson M., De Gobbi M., Marra M., Morris A., et al. ATR-X syndrome protein targets tandem repeats and influences allele-specific expression in a size-dependent manner. Cell 2010, 143:367-378.
32. Lewis P.W., Elsaesser S.J., Noh K.M., Stadler S.C., Allis C.D. Daxx is an H3.3-specific histone chaperone and cooperates with ATRX in replication-independent chromatin assembly at telomeres. Proc. Natl. Acad. Sci. USA 2010, 107:14075-14080.
33. Loppin B., Bonnefoy E., Anselme C., Laurençon A., Karr T.L., Couble P. The histone H3.3 chaperone HIRA is essential for chromatin assembly in the male pronucleus. Nature 2005, 437:1386-1390.
34. Loyola A., Bonaldi T., Roche D., Imhof A., Almouzni G. PTMs on H3 variants before chromatin assembly potentiate their final epigenetic state. Mol. Cell 2006, 24:309-316.
35. Martini E., Roche D.M., Marheineke K., Verreault A., Almouzni G. Recruitment of phosphorylated chromatin assembly factor 1 to chromatin after UV irradiation of human cells. J. Cell Biol. 1998, 143:563-575.
36. Mattick J.S. Linc-ing Long noncoding RNAs and enhancer function. Dev. Cell 2010, 19:485-486.
37. Mello J.A., Moggs J.G., Almouzni G. Analysis of DNA repair and chromatin assembly in vitro using immobilized damaged DNA substrates. Methods Mol. Biol. 2004, 281:271-281.
38. Mito Y., Henikoff J.G., Henikoff S. Genome-scale profiling of histone H3.3 replacement patterns. Nat. Genet. 2005, 37:1090-1097.
39. Polo S.E., Almouzni G. Histone metabolic pathways and chromatin assembly factors as proliferation markers. Cancer Lett. 2005, 220:1-9.
40. Polo S.E., Roche D., Almouzni G. New histone incorporation marks sites of UV repair in human cells. Cell 2006, 127:481-493.
41. Polo S.E., Theocharis S.E., Grandin L., Gambotti L., Antoni G., Savignoni A., Asselain B., Patsouris E., Almouzni G. Clinical significance and prognostic value of chromatin assembly factor-1 overexpression in human solid tumours. Histopathology 2010, 57:716-724.
42. Prochasson P., Florens L., Swanson S.K., Washburn M.P., Workman J.L. The HIR corepressor complex binds to nucleosomes generating a distinct protein/DNA complex resistant to remodeling by SWI/SNF. Genes Dev. 2005, 19:2534-2539.
43. Rahl P.B., Lin C.Y., Seila A.C., Flynn R.A., McCuine S., Burge C.B., Sharp P.A., Young R.A. c-Myc regulates transcriptional pause release. Cell 2010, 141:432-445.
44. Rai T.S., Puri A., McBryan T., Hoffman J., Tang Y., Pchelintsev N.A., van Tuyn J., Marmorstein R., Schultz D.C., Adams P.D. Human CABIN1 is a functional member of the human HIRA/UBN1/ASF1a histone H3.3 chaperone complex. Mol. Cell. Biol. 2011, 31:4107-4118.
45. Ray-Gallet D., Almouzni G. Nucleosome dynamics and histone variants. Essays Biochem. 2010, 48:75-87.
46. Ray-Gallet D., Quivy J.P., Scamps C., Martini E.M., Lipinski M., Almouzni G. HIRA is critical for a nucleosome assembly pathway independent of DNA synthesis. Mol. Cell 2002, 9:1091-1100.
47. Rugg-Gunn P.J., Cox B.J., Ralston A., Rossant J. Distinct histone modifications in stem cell lines and tissue lineages from the early mouse embryo. Proc. Natl. Acad. Sci. USA 2010, 107:10783-10790.
48. Sakai A., Schwartz B.E., Goldstein S., Ahmad K. Transcriptional and developmental functions of the H3.3 histone variant in Drosophila. Curr. Biol. 2009, 19:1816-1820.
49. Santenard A., Ziegler-Birling C., Koch M., Tora L., Bannister A.J., Torres-Padilla M.E. Heterochromatin formation in the mouse embryo requires critical residues of the histone variant H3.3. Nat. Cell Biol. 2010, 12:853-862.
50. Sawatsubashi S., Murata T., Lim J., Fujiki R., Ito S., Suzuki E., Tanabe M., Zhao Y., Kimura S., Fujiyama S., et al. A histone chaperone, DEK, transcriptionally coactivates a nuclear receptor. Genes Dev. 2010, 24:159-170.
51. Shah J.V., Botvinick E., Bonday Z., Furnari F., Berns M., Cleveland D.W. Dynamics of centromere and kinetochore proteins; implications for checkpoint signaling and silencing. Curr. Biol. 2004, 14:942-952.
52. Sims R.J., Belotserkovskaya R., Reinberg D. Elongation by RNA polymerase II: the short and long of it. Genes Dev. 2004, 18:2437-2468.
53. Smith S., Stillman B. Purification and characterization of CAF-I, a human cell factor required for chromatin assembly during DNA replication in vitro. Cell 1989, 58:15-25.
54. Stock J.K., Giadrossi S., Casanova M., Brookes E., Vidal M., Koseki H., Brockdorff N., Fisher A.G., Pombo A. Ring1-mediated ubiquitination of H2A restrains poised RNA polymerase II at bivalent genes in mouse ES cells. Nat. Cell Biol. 2007, 9:1428-1435.
55. Szenker E., Ray-Gallet D., Almouzni G. The double face of the histone variant H3.3. Cell Res. 2011, 21:421-434.
56. Tagami H., Ray-Gallet D., Almouzni G., Nakatani Y. Histone H3.1 and H3.3 complexes mediate nucleosome assembly pathways dependent or independent of DNA synthesis. Cell 2004, 116:51-61.
57. Talbert P.B., Henikoff S. Histone variants-ancient wrap artists of the epigenome. Nat. Rev. Mol. Cell Biol. 2010, 11:264-275.
58. Torres-Padilla M.E., Bannister A.J., Hurd P.J., Kouzarides T., Zernicka-Goetz M. Dynamic distribution of the replacement histone variant H3.3 in the mouse oocyte and preimplantation embryos. Int. J. Dev. Biol. 2006, 50:455-461.
59. van der Heijden G.W., Dieker J.W., Derijck A.A., Muller S., Berden J.H., Braat D.D., van der Vlag J., de Boer P. Asymmetry in histone H3 variants and lysine methylation between paternal and maternal chromatin of the early mouse zygote. Mech. Dev. 2005, 122:1008-1022.
60. von Lindern M., Fornerod M., van Baal S., Jaegle M., de Wit T., Buijs A., Grosveld G. The translocation (6;9), associated with a specific subtype of acute myeloid leukemia, results in the fusion of two genes, dek and can, and the expression of a chimeric, leukemia-specific dek-can mRNA. Mol. Cell. Biol. 1992, 12:1687-1697.
61. Wirbelauer C., Bell O., Schübeler D. Variant histone H3.3 is deposited at sites of nucleosomal displacement throughout transcribed genes while active histone modifications show a promoter-proximal bias. Genes Dev. 2005, 19:1761-1766.
62. Wong L.H., Ren H., Williams E., McGhie J., Ahn S., Sim M., Tam A., Earle E., Anderson M.A., Mann J., Choo K.H. Histone H3.3 incorporation provides a unique and functionally essential telomeric chromatin in embryonic stem cells. Genome Res. 2009, 19:404-414.
63. Wong L.H., McGhie J.D., Sim M., Anderson M.A., Ahn S., Hannan R.D., George A.J., Morgan K.A., Mann J.R., Choo K.H. ATRX interacts with H3.3 in maintaining telomere structural integrity in pluripotent embryonic stem cells. Genome Res. 2010, 20:351-360.
64. Wu R.S., Tsai S., Bonner W.M. Patterns of histone variant synthesis can distinguish G0 from G1 cells. Cell 1982, 31:367-374.