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. 2010 Oct 7;1(9):820–829. doi: 10.1007/s13238-010-0104-0

Nucleosome assembly and epigenetic inheritance

Mo Xu 1,2, Bing Zhu 2,
PMCID: PMC4875226  PMID: 21203924

Abstract

In eukaryotic cells, histones are packaged into octameric core particles with DNA wrapping around to form nucleosomes, which are the basic units of chromatin (Kornberg and Thomas, 1974). Multicellular organisms utilise chromatin marks to translate one single genome into hundreds of epigenomes for their corresponding cell types. Inheritance of epigenetic status is critical for the maintenance of gene expression profile during mitotic cell divisions (Allis et al., 2006). During S phase, canonical histones are deposited onto DNA in a replication-coupled manner (Allis et al., 2006). To understand how dividing cells overcome the dilution of epigenetic marks after chromatin duplication, DNA replication coupled (RC) nucleosome assembly has been of great interest. In this review, we focus on the potential influence of RC nucleosome assembly processes on the maintenance of epigenetic status.

Keywords: nucleosome assembly, epigenetic inheritance, DNA replication coupled

References

  1. Allfrey V.G., Mirsky A.E. Structural modifications of histones and their possible role in the regulation of RNA synthesis. Science. 1964;144:559. doi: 10.1126/science.144.3618.559. [DOI] [PubMed] [Google Scholar]
  2. Allis C.D., Jenuwein T., Reinberg D. In: Overviews and concepts. Epigenetics C.D. A., Jenuwein T., Reinberg D., editors. New York, USA: Higher Education Press and Springer-Verlag; 2006. pp. 23–56. [Google Scholar]
  3. Annunziato A.T. Split decision: what happens to nucleosomes during DNA replication? J Biol Chem. 2005;280:12065–12068. doi: 10.1074/jbc.R400039200. [DOI] [PubMed] [Google Scholar]
  4. Annunziato A.T., Seale R.L. Presence of nucleosomes within irregularly cleaved fragments of newly replicated chromatin. Nucleic Acids Res. 1984;12:6179–6196. doi: 10.1093/nar/12.15.6179. [DOI] [PMC free article] [PubMed] [Google Scholar]
  5. Bannister A.J., Zegerman P., Partridge J.F., Miska E.A., Thomas J. O., Allshire R.C., Kouzarides T. Selective recognition of methylated lysine 9 on histone H3 by the HP1 chromo domain. Nature. 2001;410:120–124. doi: 10.1038/35065138. [DOI] [PubMed] [Google Scholar]
  6. Barman H.K., Takami Y., Ono T., Nishijima H., Sanematsu F., Shibahara K., Nakayama T. Histone acetyltransferase 1 is dispensable for replication-coupled chromatin assembly but contributes to recover DNA damages created following replication blockage in vertebrate cells. Biochem Biophys Res Commun. 2006;345:1547–1557. doi: 10.1016/j.bbrc.2006.05.079. [DOI] [PubMed] [Google Scholar]
  7. Belotserkovskaya R., Oh S., Bondarenko V.A., Orphanides G., Studitsky V.M., Reinberg D. FACT facilitates transcription-dependent nucleosome alteration. Science. 2003;301:1090–1093. doi: 10.1126/science.1085703. [DOI] [PubMed] [Google Scholar]
  8. Benson L.J., Gu Y., Yakovleva T., Tong K., Barrows C., Strack C. L., Cook R.G., Mizzen C.A., Annunziato A.T. Modifications of H3 and H4 during chromatin replication, nucleosome assembly, and histone exchange. J Biol Chem. 2006;281:9287–9296. doi: 10.1074/jbc.M512956200. [DOI] [PubMed] [Google Scholar]
  9. Bonne-Andrea C., Wong M.L., Alberts B.M. In vitro replication through nucleosomes without histone displacement. Nature. 1990;343:719–726. doi: 10.1038/343719a0. [DOI] [PubMed] [Google Scholar]
  10. Brownell J.E., Zhou J., Ranalli T., Kobayashi R., Edmondson D.G., Roth S.Y., Allis C.D. Tetrahymena histone acetyltransferase A: a homolog to yeast Gcn5p linking histone acetylation to gene activation. Cell. 1996;84:843–851. doi: 10.1016/s0092-8674(00)81063-6. [DOI] [PubMed] [Google Scholar]
  11. Chuang L.S., Ian H.I., Koh T.W., Ng H.H., Xu G., Li B.F. Human DNA-(cytosine-5) methyltransferase-PCNA complex as a target for p21WAF1. Science. 1997;277:1996–2000. doi: 10.1126/science.277.5334.1996. [DOI] [PubMed] [Google Scholar]
  12. Collins N., Poot R.A., Kukimoto I., García-Jiménez C., Dellaire G., Varga-Weisz P.D. An ACF1-ISWI chromatin-remodeling complex is required for DNA replication through heterochromatin. Nat Genet. 2002;32:627–632. doi: 10.1038/ng1046. [DOI] [PubMed] [Google Scholar]
  13. Cusick M.E., Herman T.M., DePamphilis M.L., Wassarman P. M. Structure of chromatin at deoxyribonucleic acid replication forks: prenucleosomal deoxyribonucleic acid is rapidly excised from replicating simian virus 40 chromosomes by micrococcal nuclease. Biochemistry. 1981;20:6648–6658. doi: 10.1021/bi00526a020. [DOI] [PubMed] [Google Scholar]
  14. Cusick M.E., DePamphilis M.L., Wassarman P.M. Dispersive segregation of nucleosomes during replication of simian virus 40 chromosomes. J Mol Biol. 1984;178:249–271. doi: 10.1016/0022-2836(84)90143-8. [DOI] [PubMed] [Google Scholar]
  15. Das C., Lucia M.S., Hansen K.C., Tyler J.K. CBP/p300-mediated acetylation of histone H3 on lysine 56. Nature. 2009;459:113–117. doi: 10.1038/nature07861. [DOI] [PMC free article] [PubMed] [Google Scholar]
  16. Eissenberg J.C. Divided loyalties: transdetermination and the genetics of tissue regeneration. Bioessays. 2006;28:574–577. doi: 10.1002/bies.20410. [DOI] [PubMed] [Google Scholar]
  17. Eissenberg J.C., James T.C., Foster-Hartnett D.M., Hartnett T., Ngan V., Elgin S.C. Mutation in a heterochromatin-specific chromosomal protein is associated with suppression of position-effect variegation in Drosophila melanogaster. Proc Natl Acad Sci U S A. 1990;87:9923–9927. doi: 10.1073/pnas.87.24.9923. [DOI] [PMC free article] [PubMed] [Google Scholar]
  18. English C.M., Maluf N.K., Tripet B., Churchill M.E., Tyler J.K. ASF1 binds to a heterodimer of histones H3 and H4: a twostep mechanism for the assembly of the H3–H4 heterotetramer on DNA. Biochemistry. 2005;44:13673–13682. doi: 10.1021/bi051333h. [DOI] [PMC free article] [PubMed] [Google Scholar]
  19. Enomoto S., Berman J. Chromatin assembly factor I contributes to the maintenance, but not the re-establishment, of silencing at the yeast silent mating loci. Genes Dev. 1998;12:219–232. doi: 10.1101/gad.12.2.219. [DOI] [PMC free article] [PubMed] [Google Scholar]
  20. Enomoto S., McCune-Zierath P.D., Gerami-Nejad M., Sanders M. A., Berman J. RLF2, a subunit of yeast chromatin assembly factor-I, is required for telomeric chromatin function in vivo. Genes Dev. 1997;11:358–370. doi: 10.1101/gad.11.3.358. [DOI] [PubMed] [Google Scholar]
  21. Espada J., Ballestar E., Fraga M.F., Villar-Garea A., Juarranz A., Stockert J.C., Robertson K.D., Fuks F., Esteller M. Human DNA methyltransferase 1 is required for maintenance of the histone H3 modification pattern. J Biol Chem. 2004;279:37175–37184. doi: 10.1074/jbc.M404842200. [DOI] [PubMed] [Google Scholar]
  22. Estève P.O., Chin H.G., Smallwood A., Feehery G.R., Gangisetty O., Karpf A.R., Carey M.F., Pradhan S. Direct interaction between DNMT1 and G9a coordinates DNA and histone methylation during replication. Genes Dev. 2006;20:3089–3103. doi: 10.1101/gad.1463706. [DOI] [PMC free article] [PubMed] [Google Scholar]
  23. Fotedar R., Roberts J.M. Multistep pathway for replication-dependent nucleosome assembly. Proc Natl Acad Sci U S A. 1989;86:6459–6463. doi: 10.1073/pnas.86.17.6459. [DOI] [PMC free article] [PubMed] [Google Scholar]
  24. Fowler E., Farb R., El-Saidy S. Distribution of the core histones H2A.H2B.H3 and H4 during cell replication. Nucleic Acids Res. 1982;10:735–748. doi: 10.1093/nar/10.2.735. [DOI] [PMC free article] [PubMed] [Google Scholar]
  25. Franco A.A., Lam W.M., Burgers P.M., Kaufman P.D. Histone deposition protein Asf1 maintains DNA replisome integrity and interacts with replication factor C. Genes Dev. 2005;19:1365–1375. doi: 10.1101/gad.1305005. [DOI] [PMC free article] [PubMed] [Google Scholar]
  26. Gambus A., Jones R.C., Sanchez-Diaz A., Kanemaki M., van Deursen F., Edmondson R.D., Labib K. GINS maintains association of Cdc45 with MCM in replisome progression complexes at eukaryotic DNA replication forks. Nat Cell Biol. 2006;8:358–366. doi: 10.1038/ncb1382. [DOI] [PubMed] [Google Scholar]
  27. Gasser R., Koller T., Sogo J.M. The stability of nucleosomes at the replication fork. J Mol Biol. 1996;258:224–239. doi: 10.1006/jmbi.1996.0245. [DOI] [PubMed] [Google Scholar]
  28. Groth A., Rocha W., Verreault A., Almouzni G. Chromatin challenges during DNA replication and repair. Cell. 2007;128:721–733. doi: 10.1016/j.cell.2007.01.030. [DOI] [PubMed] [Google Scholar]
  29. Groth A., Corpet A., Cook A.J., Roche D., Bartek J., Lukas J., Almouzni G. Regulation of replication fork progression through histone supply and demand. Science. 2007;318:1928–1931. doi: 10.1126/science.1148992. [DOI] [PubMed] [Google Scholar]
  30. Gruss C., Wu J., Koller T., Sogo J.M. Disruption of the nucleosomes at the replication fork. EMBO J. 1993;12:4533–4545. doi: 10.1002/j.1460-2075.1993.tb06142.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  31. Hadorn E. Transdetermination in cells. Sci Am. 1968;219:110–120. doi: 10.1038/scientificamerican1168-110. [DOI] [PubMed] [Google Scholar]
  32. Hake S.B., Allis C.D. Histone H3 variants and their potential role in indexing mammalian genomes: the “H3 barcode hypothesis”. Proc Natl Acad Sci U S A. 2006;103:6428–6435. doi: 10.1073/pnas.0600803103. [DOI] [PMC free article] [PubMed] [Google Scholar]
  33. Han J., Zhou H., Horazdovsky B., Zhang K., Xu R.M., Zhang Z. Rtt109 acetylates histone H3 lysine 56 and functions in DNA replication. Science. 2007;315:653–655. doi: 10.1126/science.1133234. [DOI] [PubMed] [Google Scholar]
  34. Hansen K.H., Bracken A.P., Pasini D., Dietrich N., Gehani S.S., Monrad A., Rappsilber J., Lerdrup M., Helin K. A model for transmission of the H3K27me3 epigenetic mark. Nat Cell Biol. 2008;10:1291–1300. doi: 10.1038/ncb1787. [DOI] [PubMed] [Google Scholar]
  35. Henderson D.S., Banga S.S., Grigliatti T.A., Boyd J.B. Mutagen sensitivity and suppression of position-effect variegation result from mutations in mus209, the Drosophila gene encoding PCNA. EMBO J. 1994;13:1450–1459. doi: 10.1002/j.1460-2075.1994.tb06399.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  36. Henikoff S., Ahmad K. Assembly of variant histones into chromatin. Annu Rev Cell Dev Biol. 2005;21:133–153. doi: 10.1146/annurev.cellbio.21.012704.133518. [DOI] [PubMed] [Google Scholar]
  37. Henikoff S., Furuyama T., Ahmad K. Histone variants, nucleosome assembly and epigenetic inheritance. Trends Genet. 2004;20:320–326. doi: 10.1016/j.tig.2004.05.004. [DOI] [PubMed] [Google Scholar]
  38. Hertel L., De Andrea M., Bellomo G., Santoro P., Landolfo S., Gariglio M. The HMG protein T160 colocalizes with DNA replication foci and is down-regulated during cell differentiation. Exp Cell Res. 1999;250:313–328. doi: 10.1006/excr.1999.4495. [DOI] [PubMed] [Google Scholar]
  39. Hoek M., Stillman B. Chromatin assembly factor 1 is essential and couples chromatin assembly to DNA replication in vivo. Proc Natl Acad Sci U S A. 2003;100:12183–12188. doi: 10.1073/pnas.1635158100. [DOI] [PMC free article] [PubMed] [Google Scholar]
  40. Huen M.S., Sy S.M., van Deursen J.M., Chen J. Direct interaction between SET8 and proliferating cell nuclear antigen couples H4-K20 methylation with DNA replication. J Biol Chem. 2008;283:11073–11077. doi: 10.1074/jbc.C700242200. [DOI] [PMC free article] [PubMed] [Google Scholar]
  41. Jackson V. Deposition of newly synthesized histones: new histones H2A and H2B do not deposit in the same nucleosome with new histones H3 and H4. Biochemistry. 1987;26:2315–2325. doi: 10.1021/bi00382a037. [DOI] [PubMed] [Google Scholar]
  42. Jackson V. 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;29:719–731. doi: 10.1021/bi00455a019. [DOI] [PubMed] [Google Scholar]
  43. Jackson V., Chalkley R. Histone segregation on replicating chromatin. Biochemistry. 1985;24:6930–6938. doi: 10.1021/bi00345a027. [DOI] [PubMed] [Google Scholar]
  44. Jasencakova Z., Scharf A.N., Ask K., Corpet A., Imhof A., Almouzni G., Groth A. Replication stress interferes with histone recycling and predeposition marking of new histones. Mol Cell. 2010;37:736–743. doi: 10.1016/j.molcel.2010.01.033. [DOI] [PubMed] [Google Scholar]
  45. Jenuwein T., Allis C.D. Translating the histone code. Science. 2001;293:1074–1080. doi: 10.1126/science.1063127. [DOI] [PubMed] [Google Scholar]
  46. Jørgensen S., Elvers I., Trelle M.B., Menzel T., Eskildsen M., Jensen O.N., Helleday T., Helin K., Sørensen C.S. The histone methyltransferase SET8 is required for S-phase progression. J Cell Biol. 2007;179:1337–1345. doi: 10.1083/jcb.200706150. [DOI] [PMC free article] [PubMed] [Google Scholar]
  47. Kaufman P.D., Kobayashi R., Kessler N., Stillman B. The p150 and p60 subunits of chromatin assembly factor I: a molecular link between newly synthesized histones and DNA replication. Cell. 1995;81:1105–1114. doi: 10.1016/s0092-8674(05)80015-7. [DOI] [PubMed] [Google Scholar]
  48. Kaufman P.D., Kobayashi R., Stillman B. Ultraviolet radiation sensitivity and reduction of telomeric silencing in Saccharomyces cerevisiae cells lacking chromatin assembly factor-I. Genes Dev. 1997;11:345–357. doi: 10.1101/gad.11.3.345. [DOI] [PubMed] [Google Scholar]
  49. Kaya H., Shibahara K.I., Taoka K.I., Iwabuchi M., Stillman B., Araki T. FASCIATA genes for chromatin assembly factor-1 in arabidopsis maintain the cellular organization of apical meristems. Cell. 2001;104:131–142. doi: 10.1016/s0092-8674(01)00197-0. [DOI] [PubMed] [Google Scholar]
  50. Kornberg R.D., Thomas J.O. Chromatin structure; oligomers of the histones. Science. 1974;184:865–868. doi: 10.1126/science.184.4139.865. [DOI] [PubMed] [Google Scholar]
  51. Krude T., Knippers R. Transfer of nucleosomes from parental to replicated chromatin. Mol Cell Biol. 1991;11:6257–6267. doi: 10.1128/mcb.11.12.6257. [DOI] [PMC free article] [PubMed] [Google Scholar]
  52. Lachner M., O’Carroll D., Rea S., Mechtler K., Jenuwein T. Methylation of histone H3 lysine 9 creates a binding site for HP1 proteins. Nature. 2001;410:116–120. doi: 10.1038/35065132. [DOI] [PubMed] [Google Scholar]
  53. Leonhardt H., Page A.W., Weier H.U., Bestor T.H. A targeting sequence directs DNA methyltransferase to sites of DNA replication in mammalian nuclei. Cell. 1992;71:865–873. doi: 10.1016/0092-8674(92)90561-p. [DOI] [PubMed] [Google Scholar]
  54. LeRoy G., Orphanides G., Lane W.S., Reinberg D. Requirement of RSF and FACT for transcription of chromatin templates in vitro. Science. 1998;282:1900–1904. doi: 10.1126/science.282.5395.1900. [DOI] [PubMed] [Google Scholar]
  55. Li Q., Zhou H., Wurtele H., Davies B., Horazdovsky B., Verreault A., Zhang Z. Acetylation of histone H3 lysine 56 regulates replication-coupled nucleosome assembly. Cell. 2008;134:244–255. doi: 10.1016/j.cell.2008.06.018. [DOI] [PMC free article] [PubMed] [Google Scholar]
  56. Luger K., Mäder A.W., Richmond R.K., Sargent D.F., Richmond T.J. Crystal structure of the nucleosome core particle at 2.8 A resolution. Nature. 1997;389:251–260. doi: 10.1038/38444. [DOI] [PubMed] [Google Scholar]
  57. Margueron R., Justin N., Ohno K., Sharpe M.L., Son J., Drury W.J., 3rd, Voigt P., Martin S.R., Taylor W.R., De Marco V., et al. Role of the polycomb protein EED in the propagation of repressive histone marks. Nature. 2009;461:762–767. doi: 10.1038/nature08398. [DOI] [PMC free article] [PubMed] [Google Scholar]
  58. Martin C., Zhang Y. Mechanisms of epigenetic inheritance. Curr Opin Cell Biol. 2007;19:266–272. doi: 10.1016/j.ceb.2007.04.002. [DOI] [PubMed] [Google Scholar]
  59. Marzluff W.F., Wagner E.J., Duronio R.J. Metabolism and regulation of canonical histone mRNAs: life without a poly(A) tail. Nat Rev Genet. 2008;9:843–854. doi: 10.1038/nrg2438. [DOI] [PMC free article] [PubMed] [Google Scholar]
  60. Masumoto H., Hawke D., Kobayashi R., Verreault A. A role for cell-cycle-regulated histone H3 lysine 56 acetylation in the DNA damage response. Nature. 2005;436:294–298. doi: 10.1038/nature03714. [DOI] [PubMed] [Google Scholar]
  61. McKnight S.L., Miller O.L., Jr Electron microscopic analysis of chromatin replication in the cellular blastoderm Drosophila melanogaster embryo. Cell. 1977;12:795–804. doi: 10.1016/0092-8674(77)90278-1. [DOI] [PubMed] [Google Scholar]
  62. Meijsing S.H., Ehrenhofer-Murray A.E. The silencing complex SAS-I links histone acetylation to the assembly of repressed chromatin by CAF-I and Asf1 in Saccharomyces cerevisiae. Genes Dev. 2001;15:3169–3182. doi: 10.1101/gad.929001. [DOI] [PMC free article] [PubMed] [Google Scholar]
  63. Milutinovic S., Zhuang Q., Szyf M. Proliferating cell nuclear antigen associates with histone deacetylase activity, integrating DNA replication and chromatin modification. J Biol Chem. 2002;277:20974–20978. doi: 10.1074/jbc.M202504200. [DOI] [PubMed] [Google Scholar]
  64. Moggs J.G., Grandi P., Quivy J.P., Jónsson Z.O., Hübscher U., Becker P.B., Almouzni G. A CAF-1-PCNA-mediated chromatin assembly pathway triggered by sensing DNA damage. Mol Cell Biol. 2000;20:1206–1218. doi: 10.1128/mcb.20.4.1206-1218.2000. [DOI] [PMC free article] [PubMed] [Google Scholar]
  65. Monson E.K., de Bruin D., Zakian V.A. The yeast Cac1 protein is required for the stable inheritance of transcriptionally repressed chromatin at telomeres. Proc Natl Acad Sci U S A. 1997;94:13081–13086. doi: 10.1073/pnas.94.24.13081. [DOI] [PMC free article] [PubMed] [Google Scholar]
  66. Mosammaparast N., Shi Y. Reversal of histone methylation: biochemical and molecular mechanisms of histone demethylases. Annu Rev Biochem. 2010;79:155–179. doi: 10.1146/annurev.biochem.78.070907.103946. [DOI] [PubMed] [Google Scholar]
  67. Nabatiyan A., Krude T. Silencing of chromatin assembly factor 1 in human cells leads to cell death and loss of chromatin assembly during DNA synthesis. Mol Cell Biol. 2004;24:2853–2862. doi: 10.1128/MCB.24.7.2853-2862.2004. [DOI] [PMC free article] [PubMed] [Google Scholar]
  68. Nakatani Y., Ray-Gallet D., Quivy J.P., Tagami H., Almouzni G. Two distinct nucleosome assembly pathways: dependent or independent of DNA synthesis promoted by histone H3.1 and H3.3 complexes. Cold Spring Harb Symp Quant Biol. 2004;69:273–280. doi: 10.1101/sqb.2004.69.273. [DOI] [PubMed] [Google Scholar]
  69. Nakayama J., Rice J.C., Strahl B.D., Allis C.D., Grewal S.I. Role of histone H3 lysine 9 methylation in epigenetic control of heterochromatin assembly. Science. 2001;292:110–113. doi: 10.1126/science.1060118. [DOI] [PubMed] [Google Scholar]
  70. Natsume R., Eitoku M., Akai Y., Sano N., Horikoshi M., Senda T. Structure and function of the histone chaperone CIA/ASF1 complexed with histones H3 and H4. Nature. 2007;446:338–341. doi: 10.1038/nature05613. [DOI] [PubMed] [Google Scholar]
  71. Neumann H., Hancock S.M., Buning R., Routh A., Chapman L., Somers J., Owen-Hughes T., van Noort J., Rhodes D., Chin J.W. A method for genetically installing site-specific acetylation in recombinant histones defines the effects of H3 K56 acetylation. Mol Cell. 2009;36:153–163. doi: 10.1016/j.molcel.2009.07.027. [DOI] [PMC free article] [PubMed] [Google Scholar]
  72. Orphanides G., LeRoy G., Chang C.H., Luse D.S., Reinberg D. FACT, a factor that facilitates transcript elongation through nucleosomes. Cell. 1998;92:105–116. doi: 10.1016/s0092-8674(00)80903-4. [DOI] [PubMed] [Google Scholar]
  73. Papamichos-Chronakis M., Peterson C.L. The Ino80 chromatin-remodeling enzyme regulates replisome function and stability. Nat Struct Mol Biol. 2008;15:338–345. [Google Scholar]
  74. Paul J., Gilmour R.S. Organ-specific restriction of transcription in mammalian chromatin. J Mol Biol. 1968;34:305–316. doi: 10.1016/0022-2836(68)90255-6. [DOI] [PubMed] [Google Scholar]
  75. Pesavento J.J., Yang H., Kelleher N.L., Mizzen C.A. Certain and progressive methylation of histone H4 at lysine 20 during the cell cycle. Mol Cell Biol. 2008;28:468–486. doi: 10.1128/MCB.01517-07. [DOI] [PMC free article] [PubMed] [Google Scholar]
  76. Peters A.H., O’Carroll D., Scherthan H., Mechtler K., Sauer S., Schöfer C., Weipoltshammer K., Pagani M., Lachner M., Kohlmaier A., et al. Loss of the Suv39h histone methyltransferases impairs mammalian heterochromatin and genome stability. Cell. 2001;107:323–337. doi: 10.1016/s0092-8674(01)00542-6. [DOI] [PubMed] [Google Scholar]
  77. Poot R.A., Bozhenok L., van den Berg D.L., Steffensen S., Ferreira F., Grimaldi M., Gilbert N., Ferreira J., Varga-Weisz P.D. The Williams syndrome transcription factor interacts with PCNA to target chromatin remodelling by ISWI to replication foci. Nat Cell Biol. 2004;6:1236–1244. doi: 10.1038/ncb1196. [DOI] [PubMed] [Google Scholar]
  78. Pospelov V., Russev G., Vassilev L., Tsanev R. Nucleosome segregation in chromatin replicated in the presence of cycloheximide. J Mol Biol. 1982;156:79–91. doi: 10.1016/0022-2836(82)90460-0. [DOI] [PubMed] [Google Scholar]
  79. Prior C.P., Cantor C.R., Johnson E.M., Allfrey V.G. Incorporation of exogenous pyrene-labeled histone into Physarum chromatin: a system for studying changes in nucleosomes assembled in vivo. Cell. 1980;20:597–608. doi: 10.1016/0092-8674(80)90306-2. [DOI] [PubMed] [Google Scholar]
  80. Probst A.V., Dunleavy E., Almouzni G. Epigenetic inheritance during the cell cycle. Nat Rev Mol Cell Biol. 2009;10:192–206. doi: 10.1038/nrm2640. [DOI] [PubMed] [Google Scholar]
  81. Randall S.K., Kelly T.J. The fate of parental nucleosomes during SV40 DNA replication. J Biol Chem. 1992;267:14259–14265. [PubMed] [Google Scholar]
  82. Rea S., Eisenhaber F., O’Carroll D., Strahl B.D., Sun Z.W., Schmid M., Opravil S., Mechtler K., Ponting C.P., Allis C.D., et al. Regulation of chromatin structure by site-specific histone H3 methyltransferases. Nature. 2000;406:593–599. doi: 10.1038/35020506. [DOI] [PubMed] [Google Scholar]
  83. Recht J., Tsubota T., Tanny J.C., Diaz R.L., Berger J.M., Zhang X., Garcia B.A., Shabanowitz J., Burlingame A.L., Hunt D.F., et al. Histone chaperone Asf1 is required for histone H3 lysine 56 acetylation, a modification associated with S phase in mitosis and meiosis. Proc Natl Acad Sci U S A. 2006;103:6988–6993. doi: 10.1073/pnas.0601676103. [DOI] [PMC free article] [PubMed] [Google Scholar]
  84. Reese B.E., Bachman K.E., Baylin S.B., Rountree M.R. The methyl-CpG binding protein MBD1 interacts with the p150 subunit of chromatin assembly factor 1. Mol Cell Biol. 2003;23:3226–3236. doi: 10.1128/MCB.23.9.3226-3236.2003. [DOI] [PMC free article] [PubMed] [Google Scholar]
  85. Riley D., Weintraub H. Conservative segregation of parental histones during replication in the presence of cycloheximide. Proc Natl Acad Sci U S A. 1979;76:328–332. doi: 10.1073/pnas.76.1.328. [DOI] [PMC free article] [PubMed] [Google Scholar]
  86. Sarraf S.A., Stancheva I. Methyl-CpG binding protein MBD1 couples histone H3 methylation at lysine 9 by SETDB1 to DNA replication and chromatin assembly. Mol Cell. 2004;15:595–605. doi: 10.1016/j.molcel.2004.06.043. [DOI] [PubMed] [Google Scholar]
  87. Scharf A.N., Barth T.K., Imhof A. Establishment of histone modifications after chromatin assembly. Nucleic Acids Res. 2009;37:5032–5040. doi: 10.1093/nar/gkp518. [DOI] [PMC free article] [PubMed] [Google Scholar]
  88. Schlesinger M.B., Formosa T. POB3 is required for both transcription and replication in the yeast Saccharomyces cerevisiae. Genetics. 2000;155:1593–1606. doi: 10.1093/genetics/155.4.1593. [DOI] [PMC free article] [PubMed] [Google Scholar]
  89. Schotta G., Ebert A., Krauss V., Fischer A., Hoffmann J., Rea S., Jenuwein T., Dorn R., Reuter G. Central role of Drosophila SU(VAR)3-9 in histone H3-K9 methylation and heterochromatic gene silencing. EMBO J. 2002;21:1121–1131. doi: 10.1093/emboj/21.5.1121. [DOI] [PMC free article] [PubMed] [Google Scholar]
  90. Schulz L.L., Tyler J.K. The histone chaperone ASF1 localizes to active DNA replication forks to mediate efficient DNA replication. FASEB J. 2006;20:488–490. doi: 10.1096/fj.05-5020fje. [DOI] [PubMed] [Google Scholar]
  91. Schwartz Y.B., Pirrotta V. Polycomb silencing mechanisms and the management of genomic programmes. Nat Rev Genet. 2007;8:9–22. doi: 10.1038/nrg1981. [DOI] [PubMed] [Google Scholar]
  92. Seale R.L. Studies on the mode of segregation of histone nu bodies during replication in HeLa cells. Cell. 1976;9:423–429. doi: 10.1016/0092-8674(76)90087-8. [DOI] [PubMed] [Google Scholar]
  93. Seidman M.M., Levine A.J., Weintraub H. The asymmetric segregation of parental nucleosomes during chrosome replication. Cell. 1979;18:439–449. doi: 10.1016/0092-8674(79)90063-1. [DOI] [PubMed] [Google Scholar]
  94. Shahbazian M.D., Grunstein M. Functions of sitespecific histone acetylation and deacetylation. Annu Rev Biochem. 2007;76:75–100. doi: 10.1146/annurev.biochem.76.052705.162114. [DOI] [PubMed] [Google Scholar]
  95. Shibahara K., Stillman B. Replication-dependent marking of DNA by PCNA facilitates CAF-1-coupled inheritance of chromatin. Cell. 1999;96:575–585. doi: 10.1016/s0092-8674(00)80661-3. [DOI] [PubMed] [Google Scholar]
  96. Shilatifard A. Chromatin modifications by methylation and ubiquitination: implications in the regulation of gene expression. Annu Rev Biochem. 2006;75:243–269. doi: 10.1146/annurev.biochem.75.103004.142422. [DOI] [PubMed] [Google Scholar]
  97. 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. doi: 10.1016/0092-8674(89)90398-x. [DOI] [PubMed] [Google Scholar]
  98. Sobel R.E., Cook R.G., Perry C.A., Annunziato A.T., Allis C.D. Conservation of deposition-related acetylation sites in newly synthesized histones H3 and H4. Proc Natl Acad Sci U S A. 1995;92:1237–1241. doi: 10.1073/pnas.92.4.1237. [DOI] [PMC free article] [PubMed] [Google Scholar]
  99. Sogo J.M., Stahl H., Koller T., Knippers R. Structure of replicating simian virus 40 minichromosomes. The replication fork, core histone segregation and terminal structures. J Mol Biol. 1986;189:189–204. doi: 10.1016/0022-2836(86)90390-6. [DOI] [PubMed] [Google Scholar]
  100. Sporbert A., Gahl A., Ankerhold R., Leonhardt H., Cardoso M. C. DNA polymerase clamp shows little turnover at established replication sites but sequential de novo assembly at adjacent origin clusters. Mol Cell. 2002;10:1355–1365. doi: 10.1016/s1097-2765(02)00729-3. [DOI] [PubMed] [Google Scholar]
  101. Stewart M.D., Li J., Wong J. Relationship between histone H3 lysine 9 methylation, transcription repression, and heterochromatin protein 1 recruitment. Mol Cell Biol. 2005;25:2525–2538. doi: 10.1128/MCB.25.7.2525-2538.2005. [DOI] [PMC free article] [PubMed] [Google Scholar]
  102. Stuwe T., Hothorn M., Lejeune E., Rybin V., Bortfeld M., Scheffzek K., Ladurner A.G. The FACT Spt16 “peptidase“ domain is a histone H3–H4 binding module. Proc Natl Acad Sci U S A. 2008;105:8884–8889. doi: 10.1073/pnas.0712293105. [DOI] [PMC free article] [PubMed] [Google Scholar]
  103. Sugasawa K., Ishimi Y., Eki T., Hurwitz J., Kikuchi A., Hanaoka F. Nonconservative segregation of parental nucleosomes during simian virus 40 chromosome replication in vitro. Proc Natl Acad Sci U S A. 1992;89:1055–1059. doi: 10.1073/pnas.89.3.1055. [DOI] [PMC free article] [PubMed] [Google Scholar]
  104. Taddei A., Roche D., Sibarita J.B., Turner B.M., Almouzni G. Duplication and maintenance of heterochromatin domains. J Cell Biol. 1999;147:1153–1166. doi: 10.1083/jcb.147.6.1153. [DOI] [PMC free article] [PubMed] [Google Scholar]
  105. 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. doi: 10.1016/s0092-8674(03)01064-x. [DOI] [PubMed] [Google Scholar]
  106. Takami Y., Ono T., Fukagawa T., Shibahara K., Nakayama T. Essential role of chromatin assembly factor-1-mediated rapid nucleosome assembly for DNA replication and cell division in vertebrate cells. Mol Biol Cell. 2007;18:129–141. doi: 10.1091/mbc.E06-05-0426. [DOI] [PMC free article] [PubMed] [Google Scholar]
  107. Tan B.C., Chien C.T., Hirose S., Lee S.C. Functional cooperation between FACT and MCM helicase facilitates initiation of chromatin DNA replication. EMBO J. 2006;25:3975–3985. doi: 10.1038/sj.emboj.7601271. [DOI] [PMC free article] [PubMed] [Google Scholar]
  108. Tsubota T., Berndsen C.E., Erkmann J.A., Smith C.L., Yang L., Freitas M.A., Denu J.M., Kaufman P.D. Histone H3-K56 acetylation is catalyzed by histone chaperone-dependent complexes. Mol Cell. 2007;25:703–712. doi: 10.1016/j.molcel.2007.02.006. [DOI] [PMC free article] [PubMed] [Google Scholar]
  109. VanDemark A.P., Blanksma M., Ferris E., Heroux A., Hill C.P., Formosa T. The structure of the yFACT Pob3-M domain, its interaction with the DNA replication factor RPA, and a potential role in nucleosome deposition. Mol Cell. 2006;22:363–374. doi: 10.1016/j.molcel.2006.03.025. [DOI] [PubMed] [Google Scholar]
  110. Verreault A., Kaufman P.D., Kobayashi R., Stillman B. Nucleosome assembly by a complex of CAF-1 and acetylated histones H3/H4. Cell. 1996;87:95–104. doi: 10.1016/s0092-8674(00)81326-4. [DOI] [PubMed] [Google Scholar]
  111. Vincent J.A., Kwong T.J., Tsukiyama T. ATP-dependent chromatin remodeling shapes the DNA replication landscape. Nat Struct Mol Biol. 2008;15:477–484. doi: 10.1038/nsmb.1419. [DOI] [PMC free article] [PubMed] [Google Scholar]
  112. Volpe T.A., Kidner C., Hall I.M., Teng G., Grewal S.I., Martienssen R.A. Regulation of heterochromatic silencing and histone H3 lysine-9 methylation by RNAi. Science. 2002;297:1833–1837. doi: 10.1126/science.1074973. [DOI] [PubMed] [Google Scholar]
  113. Xie W., Song C., Young N.L., Sperling A.S., Xu F., Sridharan R., Conway A.E., Garcia B.A., Plath K., Clark A.T., et al. Histone h3 lysine 56 acetylation is linked to the core transcriptional network in human embryonic stem cells. Mol Cell. 2009;33:417–427. doi: 10.1016/j.molcel.2009.02.004. [DOI] [PMC free article] [PubMed] [Google Scholar]
  114. Xu M., Long C., Chen X., Huang C., Chen S., Zhu B. Partitioning of histone H3-H4 tetramers during DNA replicationdependent chromatin assembly. Science. 2010;328:94–98. doi: 10.1126/science.1178994. [DOI] [PubMed] [Google Scholar]
  115. Yamasu K., Senshu T. Conservative segregation of tetrameric units of H3 and H4 histones during nucleosome replication. J Biochem. 1990;107:15–20. doi: 10.1093/oxfordjournals.jbchem.a122999. [DOI] [PubMed] [Google Scholar]
  116. Ye X., Franco A.A., Santos H., Nelson D.M., Kaufman P.D., Adams P.D. Defective S phase chromatin assembly causes DNA damage, activation of the S phase checkpoint, and S phase arrest. Mol Cell. 2003;11:341–351. doi: 10.1016/s1097-2765(03)00037-6. [DOI] [PubMed] [Google Scholar]
  117. Zee B.M., Levin R.S., Xu B., LeRoy G., Wingreen N.S., Garcia B.A. In vivo residue-specific histone methylation dynamics. J Biol Chem. 2010;285:3341–3350. doi: 10.1074/jbc.M109.063784. [DOI] [PMC free article] [PubMed] [Google Scholar]
  118. Zhang Z., Shibahara K., Stillman B. PCNA connects DNA replication to epigenetic inheritance in yeast. Nature. 2000;408:221–225. doi: 10.1038/35041601. [DOI] [PubMed] [Google Scholar]

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