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Chromatin Replication and Histone Dynamics

  • Constance Alabert
  • Zuzana Jasencakova
  • Anja GrothEmail author
Part of the Advances in Experimental Medicine and Biology book series (AEMB, volume 1042)

Abstract

Inheritance of the DNA sequence and its proper organization into chromatin is fundamental for genome stability and function. Therefore, how specific chromatin structures are restored on newly synthesized DNA and transmitted through cell division remains a central question to understand cell fate choices and self-renewal. Propagation of genetic information and chromatin-based information in cycling cells entails genome-wide disruption and restoration of chromatin, coupled with faithful replication of DNA. In this chapter, we describe how cells duplicate the genome while maintaining its proper organization into chromatin. We reveal how specialized replication-coupled mechanisms rapidly assemble newly synthesized DNA into nucleosomes, while the complete restoration of chromatin organization including histone marks is a continuous process taking place throughout the cell cycle. Because failure to reassemble nucleosomes at replication forks blocks DNA replication progression in higher eukaryotes and leads to genomic instability, we further underline the importance of the mechanistic link between DNA replication and chromatin duplication.

Keywords

DNA replication Nucleosome assembly Histone chaperone Histone recycling Chromatin Epigenetics 

References

  1. Abe T, Sugimura K, Hosono Y, Takami Y, Akita M, Yoshimura A, Tada S, Nakayama T, Murofushi H, Okumura K et al (2011) The histone chaperone facilitates chromatin transcription (FACT) protein maintains normal replication fork rates. J Biol Chem 286:30504–30512PubMedPubMedCentralCrossRefGoogle Scholar
  2. Alabert C, Groth A (2012) Chromatin replication and epigenome maintenance. Nat Rev Mol Cell Biol 13:153–167PubMedCrossRefGoogle Scholar
  3. Alabert C, Bukowski-Wills JC, Lee SB, Kustatscher G, Nakamura K, de Lima Alves F, Menard P, Mejlvang J, Rappsilber J, Groth A (2014) Nascent chromatin capture proteomics determines chromatin dynamics during DNA replication and identifies unknown fork components. Nat Cell Biol 16:281–293PubMedPubMedCentralCrossRefGoogle Scholar
  4. Alabert C, Barth TK, Reveron-Gomez N, Sidoli S, Schmidt A, Jensen ON, Imhof A, Groth A (2015) Two distinct modes for propagation of histone PTMs across the cell cycle. Genes Dev 29:585–590PubMedPubMedCentralCrossRefGoogle Scholar
  5. Almouzni G, Cedar H (2016) Maintenance of epigenetic information. Cold Spring Harb Perspect Biol 8:a019372PubMedCrossRefGoogle Scholar
  6. Alvarez F, Munoz F, Schilcher P, Imhof A, Almouzni G, Loyola A (2011) Sequential establishment of marks on soluble histones H3 and H4. J Biol Chem 286:17714–17721PubMedPubMedCentralCrossRefGoogle Scholar
  7. Andrews AJ, Chen X, Zevin A, Stargell LA, Luger K (2010) The histone chaperone Nap1 promotes nucleosome assembly by eliminating nonnucleosomal histone DNA interactions. Mol Cell 37:834–842PubMedPubMedCentralCrossRefGoogle Scholar
  8. Annunziato AT (2005) Split decision: what happens to nucleosomes during DNA replication? J Biol Chem 280:12065–12068PubMedCrossRefGoogle Scholar
  9. Annunziato AT (2013) Assembling chromatin: the long and winding road. Biochim Biophys Acta 1819:196–210PubMedCrossRefGoogle Scholar
  10. Annunziato AT, Seale RL (1983) Histone deacetylation is required for the maturation of newly replicated chromatin. J Biol Chem 258:12675–12684PubMedGoogle Scholar
  11. Ask K, Jasencakova Z, Menard P, Feng Y, Almouzni G, Groth A (2012) Codanin-1, mutated in the anaemic disease CDAI, regulates Asf1 function in S-phase histone supply. EMBO J 31:2013–2023PubMedPubMedCentralCrossRefGoogle Scholar
  12. Audergon PN, Catania S, Kagansky A, Tong P, Shukla M, Pidoux AL, Allshire RC (2015) Epigenetics. Restricted epigenetic inheritance of H3K9 methylation. Science 348:132–135PubMedPubMedCentralCrossRefGoogle Scholar
  13. Bancaud A, Conde e Silva N, Barbi M, Wagner G, Allemand JF, Mozziconacci J, Lavelle C, Croquette V, Victor JM, Prunell A et al (2006) Structural plasticity of single chromatin fibers revealed by torsional manipulation. Nat Struct Mol Biol 13:444–450PubMedCrossRefGoogle Scholar
  14. Bancaud A, Wagner G, Conde ESN, Lavelle C, Wong H, Mozziconacci J, Barbi M, Sivolob A, Le Cam E, Mouawad L et al (2007) Nucleosome chiral transition under positive torsional stress in single chromatin fibers. Mol Cell 27:135–147PubMedCrossRefGoogle Scholar
  15. Barman HK, Takami Y, Ono T, Nishijima H, Sanematsu F, Shibahara K, Nakayama T (2006) 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 345:1547–1557PubMedCrossRefGoogle Scholar
  16. Belotserkovskaya R, Reinberg D (2004) Facts about FACT and transcript elongation through chromatin. Curr Opin Genet Dev 14:139–146PubMedCrossRefGoogle Scholar
  17. Belotserkovskaya R, Oh S, Bondarenko VA, Orphanides G, Studitsky VM, Reinberg D (2003) FACT facilitates transcription-dependent nucleosome alteration. Science 301:1090–1093PubMedCrossRefGoogle Scholar
  18. Benson LJ, Gu Y, Yakovleva T, Tong K, Barrows C, Strack CL, Cook RG, Mizzen CA, Annunziato AT (2006) Modifications of H3 and H4 during chromatin replication, nucleosome assembly, and histone exchange. J Biol Chem 281:9287–9296PubMedCrossRefGoogle Scholar
  19. Blackwell JS Jr, Wilkinson ST, Mosammaparast N, Pemberton LF (2007) Mutational analysis of H3 and H4 N termini reveals distinct roles in nuclear import. J Biol Chem 282:20142–20150PubMedCrossRefGoogle Scholar
  20. Bowman A, Koide A, Goodman JS, Colling ME, Zinne D, Koide S, Ladurner AG (2017) sNASP and ASF1A function through both competitive and compatible modes of histone binding. Nucleic Acids Res 45:643–656PubMedCrossRefGoogle Scholar
  21. Burgess RJ, Zhou H, Han J, Zhang Z (2010) A role for Gcn5 in replication-coupled nucleosome assembly. Mol Cell 37:469–480PubMedPubMedCentralCrossRefGoogle Scholar
  22. Campos EI, Reinberg D (2010) New chaps in the histone chaperone arena. Genes Dev 24:1334–1338PubMedPubMedCentralCrossRefGoogle Scholar
  23. Chafin DR, Vitolo JM, Henricksen LA, Bambara RA, Hayes JJ (2000) Human DNA ligase I efficiently seals nicks in nucleosomes. EMBO J 19:5492–5501PubMedPubMedCentralCrossRefGoogle Scholar
  24. Clemente-Ruiz M, Prado F (2009) Chromatin assembly controls replication fork stability. EMBO Rep 10:790–796PubMedPubMedCentralCrossRefGoogle Scholar
  25. Clemente-Ruiz M, Gonzalez-Prieto R, Prado F (2011) Histone H3K56 acetylation, CAF1, and Rtt106 coordinate nucleosome assembly and stability of advancing replication forks. PLoS Genet 7:e1002376PubMedPubMedCentralCrossRefGoogle Scholar
  26. Collins N, Poot RA, Kukimoto I, Garcia-Jimenez C, Dellaire G, Varga-Weisz PD (2002) An ACF1-ISWI chromatin-remodeling complex is required for DNA replication through heterochromatin. Nat Genet 32:627–632PubMedCrossRefGoogle Scholar
  27. Contreras A, Hale TK, Stenoien DL, Rosen JM, Mancini MA, Herrera RE (2003) The dynamic mobility of histone H1 is regulated by cyclin/CDK phosphorylation. Mol Cell Biol 23:8626–8636PubMedPubMedCentralCrossRefGoogle Scholar
  28. D’Arcy S, Martin KW, Panchenko T, Chen X, Bergeron S, Stargell LA, Black BE, Luger K (2013) Chaperone Nap1 shields histone surfaces used in a nucleosome and can put H2A-H2B in an unconventional tetrameric form. Mol Cell 51:662–677PubMedCrossRefGoogle Scholar
  29. Dabin J, Fortuny A, Polo SE (2016) Epigenome maintenance in response to DNA damage. Mol Cell 62:712–727PubMedPubMedCentralCrossRefGoogle Scholar
  30. De Koning L, Corpet A, Haber JE, Almouzni G (2007) Histone chaperones: an escort network regulating histone traffic. Nat Struct Mol Biol 14:997–1007PubMedCrossRefGoogle Scholar
  31. Devbhandari S, Jiang J, Kumar C, Whitehouse I, Remus D (2017) Chromatin constrains the initiation and elongation of DNA replication. Mol Cell 65:131–141PubMedCrossRefGoogle Scholar
  32. Dileep V, Rivera-Mulia JC, Sima J, Gilbert DM (2015) Large-scale chromatin structure-function relationships during the cell cycle and development: insights from replication timing. Cold Spring Harb Symp Quant Biol 80:53–63PubMedCrossRefGoogle Scholar
  33. Driscoll R, Hudson A, Jackson SP (2007) Yeast Rtt109 promotes genome stability by acetylating histone H3 on lysine 56. Science 315:649–652PubMedPubMedCentralCrossRefGoogle Scholar
  34. Earp C, Rowbotham S, Merenyi G, Chabes A, Cha RS (2015) S phase block following MEC1ATR inactivation occurs without severe dNTP depletion. Biol Open 4:1739–1743PubMedPubMedCentralCrossRefGoogle Scholar
  35. Ejlassi-Lassallette A, Mocquard E, Arnaud MC, Thiriet C (2011) H4 replication-dependent diacetylation and Hat1 promote S-phase chromatin assembly in vivo. Mol Biol Cell 22:245–255PubMedPubMedCentralCrossRefGoogle Scholar
  36. English CM, Adkins MW, Carson JJ, Churchill ME, Tyler JK (2006) Structural basis for the histone chaperone activity of Asf1. Cell 127:495–508PubMedPubMedCentralCrossRefGoogle Scholar
  37. Fennessy RT, Owen-Hughes T (2016) Establishment of a promoter-based chromatin architecture on recently replicated DNA can accommodate variable inter-nucleosome spacing. Nucleic Acids Res 44:7189–7203PubMedPubMedCentralGoogle Scholar
  38. Foltman M, Evrin C, De Piccoli G, Jones RC, Edmondson RD, Katou Y, Nakato R, Shirahige K, Labib K (2013) Eukaryotic replisome components cooperate to process histones during chromosome replication. Cell Rep 3:892–904PubMedCrossRefGoogle Scholar
  39. Franco AA, Lam WM, Burgers PM, Kaufman PD (2005) Histone deposition protein Asf1 maintains DNA replisome integrity and interacts with replication factor C. Genes Dev 19:1365–1375PubMedPubMedCentralCrossRefGoogle Scholar
  40. Gambus A, Jones RC, Sanchez-Diaz A, Kanemaki M, van Deursen F, Edmondson RD, Labib K (2006) GINS maintains association of Cdc45 with MCM in replisome progression complexes at eukaryotic DNA replication forks. Nat Cell Biol 8:358–366PubMedCrossRefGoogle Scholar
  41. Gasser R, Koller T, Sogo JM (1996) The stability of nucleosomes at the replication fork. J Mol Biol 258:224–239PubMedCrossRefGoogle Scholar
  42. Gaydos LJ, Wang W, Strome S (2014) Gene repression. H3K27me and PRC2 transmit a memory of repression across generations and during development. Science 345:1515–1518PubMedPubMedCentralCrossRefGoogle Scholar
  43. Glowczewski L, Waterborg JH, Berman JG (2004) Yeast chromatin assembly complex 1 protein excludes nonacetylatable forms of histone H4 from chromatin and the nucleus. Mol Cell Biol 24:10180–10192PubMedPubMedCentralCrossRefGoogle Scholar
  44. Groth A, Lukas J, Nigg EA, Sillje HH, Wernstedt C, Bartek J, Hansen K (2003) Human tousled like kinases are targeted by an ATM- and Chk1-dependent DNA damage checkpoint. EMBO J 22:1676–1687PubMedPubMedCentralCrossRefGoogle Scholar
  45. Groth A, Corpet A, Cook AJ, Roche D, Bartek J, Lukas J, Almouzni G (2007) Regulation of replication fork progression through histone supply and demand. Science 318:1928–1931PubMedCrossRefGoogle Scholar
  46. Gunjan A, Verreault A (2003) A Rad53 kinase-dependent surveillance mechanism that regulates histone protein levels in S. cerevisiae. Cell 115:537–549PubMedCrossRefGoogle Scholar
  47. Gupta P, Zlatanova J, Tomschik M (2009) Nucleosome assembly depends on the torsion in the DNA molecule: a magnetic tweezers study. Biophys J 97:3150–3157PubMedPubMedCentralCrossRefGoogle Scholar
  48. Haigney A, Ricketts MD, Marmorstein R (2015) Dissecting the molecular roles of histone chaperones in histone acetylation by type B histone acetyltransferases (HAT-B). J Biol Chem 290:30648–30657PubMedPubMedCentralCrossRefGoogle Scholar
  49. Hammond CM, Sundaramoorthy R, Larance M, Lamond A, Stevens MA, El-Mkami H, Norman DG, Owen-Hughes T (2016) The histone chaperone Vps75 forms multiple oligomeric assemblies capable of mediating exchange between histone H3-H4 tetramers and Asf1-H3-H4 complexes. Nucleic Acids Res 44:6157–6172PubMedPubMedCentralCrossRefGoogle Scholar
  50. Hammond CM, Stromme CB, Huang H, Patel DJ, Groth A (2017) Histone chaperone networks shaping chromatin function. Nat Rev Mol Cell Biol 18:141–158PubMedPubMedCentralCrossRefGoogle Scholar
  51. Han M, Chang M, Kim UJ, Grunstein M (1987) Histone H2B repression causes cell-cycle-specific arrest in yeast: effects on chromosomal segregation, replication, and transcription. Cell 48:589–597PubMedCrossRefGoogle Scholar
  52. Han J, Zhou H, Horazdovsky B, Zhang K, Xu RM, Zhang Z (2007) Rtt109 acetylates histone H3 lysine 56 and functions in DNA replication. Science 315:653–655PubMedCrossRefGoogle Scholar
  53. Hoek M, Stillman B (2003) Chromatin assembly factor 1 is essential and couples chromatin assembly to DNA replication in vivo. Proc Natl Acad Sci U S A 100:12183–12188PubMedPubMedCentralCrossRefGoogle Scholar
  54. Hondele M, Stuwe T, Hassler M, Halbach F, Bowman A, Zhang ET, Nijmeijer B, Kotthoff C, Rybin V, Amlacher S et al (2013) Structural basis of histone H2A-H2B recognition by the essential chaperone FACT. Nature 499:111–114PubMedCrossRefGoogle Scholar
  55. Huang H, Stromme CB, Saredi G, Hodl M, Strandsby A, Gonzalez-Aguilera C, Chen S, Groth A, Patel DJ (2015) A unique binding mode enables MCM2 to chaperone histones H3-H4 at replication forks. Nat Struct Mol Biol 22:618–626PubMedPubMedCentralCrossRefGoogle Scholar
  56. Huggins CF, Chafin DR, Aoyagi S, Henricksen LA, Bambara RA, Hayes JJ (2002) Flap endonuclease 1 efficiently cleaves base excision repair and DNA replication intermediates assembled into nucleosomes. Mol Cell 10:1201–1211PubMedCrossRefGoogle Scholar
  57. Iida T, Araki H (2004) Noncompetitive counteractions of DNA polymerase epsilon and ISW2/yCHRAC for epigenetic inheritance of telomere position effect in Saccharomyces cerevisiae. Mol Cell Biol 24:217–227PubMedPubMedCentralCrossRefGoogle Scholar
  58. Ishimi Y, Komamura-Kohno Y, Arai K, Masai H (2001) Biochemical activities associated with mouse Mcm2 protein. J Biol Chem 276:42744–42752PubMedCrossRefGoogle Scholar
  59. Jackson V (1987) Deposition of newly synthesized histones: new histones H2A and H2B do not deposit in the same nucleosome with new histones H3 and H4. Biochemistry 26:2315–2325PubMedCrossRefGoogle Scholar
  60. Jackson V (1990) 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 29:719–731PubMedCrossRefGoogle Scholar
  61. Jasencakova Z, Scharf AN, Ask K, Corpet A, Imhof A, Almouzni G, Groth A (2010) Replication stress interferes with histone recycling and predeposition marking of new histones. Mol Cell 37:736–743PubMedCrossRefGoogle Scholar
  62. Katan-Khaykovich Y, Struhl K (2011) Splitting of H3-H4 tetramers at transcriptionally active genes undergoing dynamic histone exchange. Proc Natl Acad Sci U S A 108:1296–1301PubMedPubMedCentralCrossRefGoogle Scholar
  63. Kim UJ, Han M, Kayne P, Grunstein M (1988) Effects of histone H4 depletion on the cell cycle and transcription of Saccharomyces cerevisiae. EMBO J 7:2211–2219PubMedPubMedCentralGoogle Scholar
  64. Kim D, Setiaputra D, Jung T, Chung J, Leitner A, Yoon J, Aebersold R, Hebert H, Yip CK, Song JJ (2016) Molecular architecture of yeast chromatin assembly factor 1. Sci Rep 6:26702PubMedPubMedCentralCrossRefGoogle Scholar
  65. Kleff S, Andrulis ED, Anderson CW, Sternglanz R (1995) Identification of a gene encoding a yeast histone H4 acetyltransferase. J Biol Chem 270:24674–24677PubMedCrossRefGoogle Scholar
  66. Klimovskaia IM, Young C, Stromme CB, Menard P, Jasencakova Z, Mejlvang J, Ask K, Ploug M, Nielsen ML, Jensen ON et al (2014) Tousled-like kinases phosphorylate Asf1 to promote histone supply during DNA replication. Nat Commun 5:3394PubMedPubMedCentralCrossRefGoogle Scholar
  67. Krause DR, Jonnalagadda JC, Gatei MH, Sillje HH, Zhou BB, Nigg EA, Khanna K (2003) Suppression of Tousled-like kinase activity after DNA damage or replication block requires ATM, NBS1 and Chk1. Oncogene 22:5927–5937PubMedCrossRefGoogle Scholar
  68. Kubota T, Katou Y, Nakato R, Shirahige K, Donaldson AD (2015) Replication-coupled PCNA unloading by the Elg1 complex occurs genome-wide and requires Okazaki fragment ligation. Cell Rep 12:774–787PubMedPubMedCentralCrossRefGoogle Scholar
  69. Kurat CF, Yeeles JT, Patel H, Early A, Diffley JF (2017) Chromatin controls DNA replication origin selection, lagging-strand synthesis, and replication fork rates. Mol Cell 65:117–130PubMedPubMedCentralCrossRefGoogle Scholar
  70. Lee HS, Lee SA, Hur SK, Seo JW, Kwon J (2014) Stabilization and targeting of INO80 to replication forks by BAP1 during normal DNA synthesis. Nat Commun 5:5128PubMedCrossRefGoogle Scholar
  71. Li Q, Zhou H, Wurtele H, Davies B, Horazdovsky B, Verreault A, Zhang Z (2008) Acetylation of histone H3 lysine 56 regulates replication-coupled nucleosome assembly. Cell 134:244–255PubMedPubMedCentralCrossRefGoogle Scholar
  72. Liu WH, Roemer SC, Zhou Y, Shen ZJ, Dennehey BK, Balsbaugh JL, Liddle JC, Nemkov T, Ahn NG, Hansen KC, et al (2016) The Cac1 subunit of histone chaperone CAF-1 organizes CAF-1-H3/H4 architecture and tetramerizes histones. Elife 5:e18023Google Scholar
  73. Liu S, Xu Z, Leng H, Zheng P, Yang J, Chen K, Feng J, Li Q (2017) RPA binds histone H3-H4 and functions in DNA replication-coupled nucleosome assembly. Science 355:415–420PubMedCrossRefGoogle Scholar
  74. Loyola A, Bonaldi T, Roche D, Imhof A, Almouzni G (2006) PTMs on H3 variants before chromatin assembly potentiate their final epigenetic state. Mol Cell 24:309–316PubMedCrossRefGoogle Scholar
  75. Loyola A, Tagami H, Bonaldi T, Roche D, Quivy JP, Imhof A, Nakatani Y, Dent SY, Almouzni G (2009) The HP1alpha-CAF1-SetDB1-containing complex provides H3K9me1 for Suv39-mediated K9me3 in pericentric heterochromatin. EMBO Rep 10:769–775PubMedPubMedCentralCrossRefGoogle Scholar
  76. Marzluff WF, Wagner EJ, Duronio RJ (2008) Metabolism and regulation of canonical histone mRNAs: life without a poly(A) tail. Nat Rev Genet 9:843–854PubMedPubMedCentralCrossRefGoogle Scholar
  77. Masumoto H, Hawke D, Kobayashi R, Verreault A (2005) A role for cell-cycle-regulated histone H3 lysine 56 acetylation in the DNA damage response. Nature 436:294–298PubMedCrossRefGoogle Scholar
  78. Mattiroli F, Gu Y, Yadav T, Balsbaugh JL, Harris MR, Findlay ES, Liu Y, Radebaugh CA, Stargell LA, Ahn NG, Whitehouse I, Luger K (2017) DNA-mediated association of two histone-bound complexes of yeast Chromatin Assembly Factor-1 (CAF-1) drives tetrasome assembly in the wake of DNA replication. elife 6:e22799PubMedPubMedCentralCrossRefGoogle Scholar
  79. McCullough L, Connell Z, Petersen C, Formosa T (2015) The abundant histone chaperones Spt6 and FACT collaborate to assemble, inspect, and maintain chromatin structure in Saccharomyces cerevisiae. Genetics 201:1031–1045PubMedPubMedCentralCrossRefGoogle Scholar
  80. McKnight SL, Miller OL Jr (1977) Electron microscopic analysis of chromatin replication in the cellular blastoderm Drosophila melanogaster embryo. Cell 12:795–804PubMedCrossRefGoogle Scholar
  81. Meeks-Wagner D, Hartwell LH (1986) Normal stoichiometry of histone dimer sets is necessary for high fidelity of mitotic chromosome transmission. Cell 44:43–52PubMedCrossRefGoogle Scholar
  82. Mejlvang J, Feng Y, Alabert C, Neelsen KJ, Jasencakova Z, Zhao X, Lees M, Sandelin A, Pasero P, Lopes M et al (2014) New histone supply regulates replication fork speed and PCNA unloading. J Cell Biol 204:29–43PubMedPubMedCentralCrossRefGoogle Scholar
  83. Mello JA, Sillje HH, Roche DM, Kirschner DB, Nigg EA, Almouzni G (2002) Human Asf1 and CAF-1 interact and synergize in a repair-coupled nucleosome assembly pathway. EMBO Rep 3:329–334PubMedPubMedCentralCrossRefGoogle Scholar
  84. Moggs JG, Grandi P, Quivy JP, Jonsson ZO, Hubscher U, Becker PB, Almouzni G (2000) A CAF-1-PCNA-mediated chromatin assembly pathway triggered by sensing DNA damage. Mol Cell Biol 20:1206–1218PubMedPubMedCentralCrossRefGoogle Scholar
  85. Myung K, Pennaneach V, Kats ES, Kolodner RD (2003) Saccharomyces cerevisiae chromatin-assembly factors that act during DNA replication function in the maintenance of genome stability. Proc Natl Acad Sci U S A 100:6640–6645PubMedPubMedCentralCrossRefGoogle Scholar
  86. Narlikar GJ, Sundaramoorthy R, Owen-Hughes T (2013) Mechanisms and functions of ATP-dependent chromatin-remodeling enzymes. Cell 154:490–503PubMedPubMedCentralCrossRefGoogle Scholar
  87. Natsume R, Eitoku M, Akai Y, Sano N, Horikoshi M, Senda T (2007) Structure and function of the histone chaperone CIA/ASF1 complexed with histones H3 and H4. Nature 446:338–341PubMedCrossRefGoogle Scholar
  88. Nelson DM, Ye X, Hall C, Santos H, Ma T, Kao GD, Yen TJ, Harper JW, Adams PD (2002) Coupling of DNA synthesis and histone synthesis in S phase independent of cyclin/cdk2 activity. Mol Cell Biol 22:7459–7472PubMedPubMedCentralCrossRefGoogle Scholar
  89. Orphanides G, Wu WH, Lane WS, Hampsey M, Reinberg D (1999) The chromatin-specific transcription elongation factor FACT comprises human SPT16 and SSRP1 proteins. Nature 400:284–288PubMedCrossRefGoogle Scholar
  90. Parthun MR, Widom J, Gottschling DE (1996) The major cytoplasmic histone acetyltransferase in yeast: links to chromatin replication and histone metabolism. Cell 87:85–94PubMedCrossRefGoogle Scholar
  91. Pengelly AR, Copur O, Jackle H, Herzig A, Muller J (2013) A histone mutant reproduces the phenotype caused by loss of histone-modifying factor Polycomb. Science 339:698–699PubMedCrossRefGoogle Scholar
  92. Perry CA, Annunziato AT (1989) Influence of histone acetylation on the solubility, H1 content and DNase I sensitivity of newly assembled chromatin. Nucleic Acids Res 17:4275–4291PubMedPubMedCentralCrossRefGoogle Scholar
  93. Pesavento JJ, Bullock CR, LeDuc RD, Mizzen CA, Kelleher NL (2008) Combinatorial modification of human histone H4 quantitated by two-dimensional liquid chromatography coupled with top down mass spectrometry. J Biol Chem 283:14927–14937PubMedPubMedCentralCrossRefGoogle Scholar
  94. Pinheiro I, Margueron R, Shukeir N, Eisold M, Fritzsch C, Richter FM, Mittler G, Genoud C, Goyama S, Kurokawa M et al (2012) Prdm3 and Prdm16 are H3K9me1 methyltransferases required for mammalian heterochromatin integrity. Cell 150:948–960PubMedCrossRefGoogle Scholar
  95. Poot RA, Bozhenok L, van den Berg DL, Steffensen S, Ferreira F, Grimaldi M, Gilbert N, Ferreira J, Varga-Weisz PD (2004) The Williams syndrome transcription factor interacts with PCNA to target chromatin remodelling by ISWI to replication foci. Nat Cell Biol 6:1236–1244PubMedCrossRefGoogle Scholar
  96. Prado F, Aguilera A (2005) Partial depletion of histone H4 increases homologous recombination-mediated genetic instability. Mol Cell Biol 25:1526–1536PubMedPubMedCentralCrossRefGoogle Scholar
  97. Prado F, Cortes-Ledesma F, Aguilera A (2004) The absence of the yeast chromatin assembly factor Asf1 increases genomic instability and sister chromatid exchange. EMBO Rep 5:497–502PubMedPubMedCentralCrossRefGoogle Scholar
  98. Prior CP, Cantor CR, Johnson EM, Allfrey VG (1980) Incorporation of exogenous pyrene-labeled histone into Physarum chromatin: a system for studying changes in nucleosomes assembled in vivo. Cell 20:597–608PubMedCrossRefGoogle Scholar
  99. Radman-Livaja M, Verzijlbergen KF, Weiner A, van Welsem T, Friedman N, Rando OJ, van Leeuwen F (2011) Patterns and mechanisms of ancestral histone protein inheritance in budding yeast. PLoS Biol 9:e1001075PubMedPubMedCentralCrossRefGoogle Scholar
  100. Ragunathan K, Jih G, Moazed D (2015) Epigenetics. Epigenetic inheritance uncoupled from sequence-specific recruitment. Science 348:1258699PubMedCrossRefGoogle Scholar
  101. Ramachandran S, Henikoff S (2016) Transcriptional regulators compete with nucleosomes post-replication. Cell 165:580–592PubMedPubMedCentralCrossRefGoogle Scholar
  102. Ray-Gallet D, Quivy JP, Scamps C, Martini EM, Lipinski M, Almouzni G (2002) HIRA is critical for a nucleosome assembly pathway independent of DNA synthesis. Mol Cell 9:1091–1100PubMedCrossRefGoogle Scholar
  103. Ray-Gallet D, Woolfe A, Vassias I, Pellentz C, Lacoste N, Puri A, Schultz DC, Pchelintsev NA, Adams PD, Jansen LE et al (2011) Dynamics of histone H3 deposition in vivo reveal a nucleosome gap-filling mechanism for H3.3 to maintain chromatin integrity. Mol Cell 44:928–941PubMedCrossRefGoogle Scholar
  104. Richet N, Liu D, Legrand P, Velours C, Corpet A, Gaubert A, Bakail M, Moal-Raisin G, Guerois R, Compper C et al (2015) Structural insight into how the human helicase subunit MCM2 may act as a histone chaperone together with ASF1 at the replication fork. Nucleic Acids Res 43:1905–1917PubMedPubMedCentralCrossRefGoogle Scholar
  105. Rivera C, Saavedra F, Alvarez F, Diaz-Celis C, Ugalde V, Li J, Forne I, Gurard-Levin ZA, Almouzni G, Imhof A et al (2015) Methylation of histone H3 lysine 9 occurs during translation. Nucleic Acids Res 43:9097–9106PubMedPubMedCentralCrossRefGoogle Scholar
  106. Saredi G, Huang H, Hammond CM, Alabert C, Bekker-Jensen S, Forne I, Reveron-Gomez N, Foster BM, Mlejnkova L, Bartke T et al (2016) H4K20me0 marks post-replicative chromatin and recruits the TONSL-MMS22L DNA repair complex. Nature 534:714–718PubMedPubMedCentralCrossRefGoogle Scholar
  107. Sauer PV, Timm J, Liu D, Sitbon D, Boeri-Erba E, Velours C, Mucke N, Langowski J, Ochsenbein F, Almouzni G, Panne D (2017) Insights into the molecular architecture and histone H3-H4 deposition mechanism of yeast Chromatin assembly factor 1. elife 6:e23474PubMedPubMedCentralCrossRefGoogle Scholar
  108. Scharf AN, Barth TK, Imhof A (2009) Establishment of histone modifications after chromatin assembly. Nucleic Acids Res 37:5032–5040PubMedPubMedCentralCrossRefGoogle Scholar
  109. Seale RL, Simpson RT (1975) Effects of cycloheximide on chromatin biosynthesis. J Mol Biol 94:479–501PubMedCrossRefGoogle Scholar
  110. Shibahara K, Stillman B (1999) Replication-dependent marking of DNA by PCNA facilitates CAF-1-coupled inheritance of chromatin. Cell 96:575–585PubMedCrossRefGoogle Scholar
  111. Shundrovsky A, Smith CL, Lis JT, Peterson CL, Wang MD (2006) Probing SWI/SNF remodeling of the nucleosome by unzipping single DNA molecules. Nat Struct Mol Biol 13:549–554PubMedCrossRefGoogle Scholar
  112. Sillje HH, Nigg EA (2001) Identification of human Asf1 chromatin assembly factors as substrates of Tousled-like kinases. Curr Biol 11:1068–1073PubMedCrossRefGoogle Scholar
  113. Sillje HH, Takahashi K, Tanaka K, Van Houwe G, Nigg EA (1999) Mammalian homologues of the plant Tousled gene code for cell-cycle-regulated kinases with maximal activities linked to ongoing DNA replication. EMBO J 18:5691–5702PubMedPubMedCentralCrossRefGoogle Scholar
  114. Sirbu BM, Couch FB, Feigerle JT, Bhaskara S, Hiebert SW, Cortez D (2011) Analysis of protein dynamics at active, stalled, and collapsed replication forks. Genes Dev 25:1320–1327PubMedPubMedCentralCrossRefGoogle Scholar
  115. Smith S, Stillman B (1989) Purification and characterization of CAF-I, a human cell factor required for chromatin assembly during DNA replication in vitro. Cell 58:15–25PubMedCrossRefGoogle Scholar
  116. Smith S, Stillman B (1991) Stepwise assembly of chromatin during DNA replication in vitro. EMBO J 10:971–980PubMedPubMedCentralGoogle Scholar
  117. Smith DJ, Whitehouse I (2012) Intrinsic coupling of lagging-strand synthesis to chromatin assembly. Nature 483:434–438PubMedPubMedCentralCrossRefGoogle Scholar
  118. Sobel RE, Cook RG, Perry CA, Annunziato AT, Allis CD (1995) Conservation of deposition-related acetylation sites in newly synthesized histones H3 and H4. Proc Natl Acad Sci U S A 92:1237–1241PubMedPubMedCentralCrossRefGoogle Scholar
  119. Sogo JM, Stahl H, Koller T, Knippers R (1986) Structure of replicating simian virus 40 minichromosomes. The replication fork, core histone segregation and terminal structures. J Mol Biol 189:189–204PubMedCrossRefGoogle Scholar
  120. Straube K, Blackwell JS Jr, Pemberton LF (2010) Nap1 and Chz1 have separate Htz1 nuclear import and assembly functions. Traffic 11:185–197PubMedCrossRefGoogle Scholar
  121. Stuwe T, Hothorn M, Lejeune E, Rybin V, Bortfeld M, Scheffzek K, Ladurner AG (2008) The FACT Spt16 “peptidase” domain is a histone H3-H4 binding module. Proc Natl Acad Sci U S A 105:8884–8889PubMedPubMedCentralCrossRefGoogle Scholar
  122. Svikovic S, Sale JE (2016) The effects of replication stress on S phase histone management and epigenetic memory. J Mol Biol 429:2011–2029PubMedCrossRefGoogle Scholar
  123. Tagami H, Ray-Gallet D, Almouzni G, Nakatani Y (2004) Histone H3.1 and H3.3 complexes mediate nucleosome assembly pathways dependent or independent of DNA synthesis. Cell 116:51–61PubMedCrossRefGoogle Scholar
  124. Talbert PB, Henikoff S (2017) Histone variants on the move: substrates for chromatin dynamics. Nat Rev Mol Cell Biol 18:115–126PubMedCrossRefGoogle Scholar
  125. Tan BC, Chien CT, Hirose S, Lee SC (2006) Functional cooperation between FACT and MCM helicase facilitates initiation of chromatin DNA replication. EMBO J 25:3975–3985PubMedPubMedCentralCrossRefGoogle Scholar
  126. Tang Y, Poustovoitov MV, Zhao K, Garfinkel M, Canutescu A, Dunbrack R, Adams PD, Marmorstein R (2006) Structure of a human ASF1a-HIRA complex and insights into specificity of histone chaperone complex assembly. Nat Struct Mol Biol 13:921–929PubMedPubMedCentralCrossRefGoogle Scholar
  127. Teves SS, Henikoff S (2014) DNA torsion as a feedback mediator of transcription and chromatin dynamics. Nucleus 5:211–218PubMedPubMedCentralCrossRefGoogle Scholar
  128. Tsubota T, Berndsen CE, Erkmann JA, Smith CL, Yang L, Freitas MA, Denu JM, Kaufman PD (2007) Histone H3-K56 acetylation is catalyzed by histone chaperone-dependent complexes. Mol Cell 25:703–712PubMedPubMedCentralCrossRefGoogle Scholar
  129. Tsunaka Y, Fujiwara Y, Oyama T, Hirose S, Morikawa K (2016) Integrated molecular mechanism directing nucleosome reorganization by human FACT. Genes Dev 30:673–686PubMedPubMedCentralCrossRefGoogle Scholar
  130. Tyler JK, Adams CR, Chen SR, Kobayashi R, Kamakaka RT, Kadonaga JT (1999) The RCAF complex mediates chromatin assembly during DNA replication and repair. Nature 402:555–560PubMedCrossRefGoogle Scholar
  131. Tyler JK, Collins KA, Prasad-Sinha J, Amiott E, Bulger M, Harte PJ, Kobayashi R, Kadonaga JT (2001) Interaction between the Drosophila CAF-1 and ASF1 chromatin assembly factors. Mol Cell Biol 21:6574–6584PubMedPubMedCentralCrossRefGoogle Scholar
  132. VanDemark AP, Blanksma M, Ferris E, Heroux A, Hill CP, Formosa T (2006) 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 22:363–374PubMedCrossRefGoogle Scholar
  133. Vasseur P, Tonazzini S, Ziane R, Camasses A, Rando OJ, Radman-Livaja M (2016) Dynamics of nucleosome positioning maturation following genomic replication. Cell Rep 16:2651–2665PubMedPubMedCentralCrossRefGoogle Scholar
  134. Verreault A, Kaufman PD, Kobayashi R, Stillman B (1996) Nucleosome assembly by a complex of CAF-1 and acetylated histones H3/H4. Cell 87:95–104PubMedCrossRefGoogle Scholar
  135. Vincent JA, Kwong TJ, Tsukiyama T (2008) ATP-dependent chromatin remodeling shapes the DNA replication landscape. Nat Struct Mol Biol 15:477–484PubMedPubMedCentralCrossRefGoogle Scholar
  136. Wang H, Wang M, Yang N, Xu RM (2015) Structure of the quaternary complex of histone H3-H4 heterodimer with chaperone ASF1 and the replicative helicase subunit MCM2. Protein Cell 6:693–697PubMedPubMedCentralCrossRefGoogle Scholar
  137. Weintraub H (1972) A possible role for histone in the synthesis of DNA. Nature 240:449–453PubMedCrossRefGoogle Scholar
  138. Wittmeyer J, Joss L, Formosa T (1999) Spt16 and Pob3 of Saccharomyces cerevisiae form an essential, abundant heterodimer that is nuclear, chromatin-associated, and copurifies with DNA polymerase alpha. Biochemistry 38:8961–8971PubMedCrossRefGoogle Scholar
  139. Xu M, Long C, Chen X, Huang C, Chen S, Zhu B (2010) Partitioning of histone H3-H4 tetramers during DNA replication-dependent chromatin assembly. Science 328:94–98PubMedCrossRefGoogle Scholar
  140. Xu M, Wang W, Chen S, Zhu B (2011) A model for mitotic inheritance of histone lysine methylation. EMBO Rep 13:60–67PubMedPubMedCentralCrossRefGoogle Scholar
  141. Yamasu K, Senshu T (1990) Conservative segregation of tetrameric units of H3 and H4 histones during nucleosome replication. J Biochem 107:15–20PubMedCrossRefGoogle Scholar
  142. Yang J, Zhang X, Feng J, Leng H, Li S, Xiao J, Liu S, Xu Z, Xu J, Li D et al (2016) The histone chaperone FACT contributes to DNA replication-coupled nucleosome assembly. Cell Rep 16:3414PubMedCrossRefGoogle Scholar
  143. Ye X, Franco AA, Santos H, Nelson DM, Kaufman PD, Adams PD (2003) Defective S phase chromatin assembly causes DNA damage, activation of the S phase checkpoint, and S phase arrest. Mol Cell 11:341–351PubMedCrossRefGoogle Scholar
  144. Zee BM, Britton LM, Wolle D, Haberman DM, Garcia BA (2012) Origins and formation of histone methylation across the human cell cycle. Mol Cell Biol 32:2503–2514PubMedPubMedCentralCrossRefGoogle Scholar
  145. Zeman MK, Cimprich KA (2014) Causes and consequences of replication stress. Nat Cell Biol 16:2–9PubMedPubMedCentralCrossRefGoogle Scholar
  146. Zhang W, Tyl M, Ward R, Sobott F, Maman J, Murthy AS, Watson AA, Fedorov O, Bowman A, Owen-Hughes T et al (2013) Structural plasticity of histones H3-H4 facilitates their allosteric exchange between RbAp48 and ASF1. Nat Struct Mol Biol 20:29–35PubMedCrossRefGoogle Scholar
  147. Zhou Y, Wang TS (2004) A coordinated temporal interplay of nucleosome reorganization factor, sister chromatin cohesion factor, and DNA polymerase alpha facilitates DNA replication. Mol Cell Biol 24:9568–9579PubMedPubMedCentralCrossRefGoogle Scholar

Copyright information

© Springer Nature Singapore Pte Ltd. 2017

Authors and Affiliations

  • Constance Alabert
    • 1
  • Zuzana Jasencakova
    • 2
  • Anja Groth
    • 2
    Email author
  1. 1.Centre for Gene Regulation and Expression, School of Life SciencesUniversity of DundeeDundeeUK
  2. 2.Biotech Research and Innovation Centre (BRIC), Health and Medical FacultyUniversity of CopenhagenCopenhagenDenmark

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