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Abstract

Nucleosomes compact and organize genetic material on a structural level. However, they also alter local chromatin accessibility through changes in their position, through the incorporation of histone variants, and through a vast array of histone posttranslational modifications. The dynamic nature of chromatin requires histone chaperones to process, deposit, and evict histones in different tissues and at different times in the cell cycle. This review focuses on the molecular details of canonical and variant H3–H4 histone chaperone pathways that lead to histone deposition on DNA as they are currently understood. Emphasis is placed on the most established pathways beginning with the folding, posttranslational modification, and nuclear import of newly synthesized H3–H4 histones. Next, we review the deposition of replication-coupled H3.1–H4 in S-phase and replication-independent H3.3–H4 via alternative histone chaperone pathways. Highly specialized histone chaperones overseeing the deposition of histone variants are also briefly discussed.

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2018-11-23
2024-03-28
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Literature Cited

  1. 1.  Abascal F, Corpet A, Gurard-Levin ZA, Juan D, Ochsenbein F et al. 2013. Subfunctionalization via adaptive evolution influenced by genomic context: the case of histone chaperones ASF1a and ASF1b. Mol. Biol. Evol. 30:1853–66
    [Google Scholar]
  2. 2.  Adkins MW, Howar SR, Tyler JK 2004. Chromatin disassembly mediated by the histone chaperone Asf1 is essential for transcriptional activation of the yeast PHO5 and PHO8 genes. Mol. Cell 14:657–66
    [Google Scholar]
  3. 3.  Agudelo Garcia PA, Hoover ME, Zhang P, Nagarajan P, Freitas MA, Parthun MR 2017. Identification of multiple roles for histone acetyltransferase 1 in replication-coupled chromatin assembly. Nucleic Acids Res 45:9319–35
    [Google Scholar]
  4. 4.  Ahmad K, Henikoff S 2002. The histone variant H3.3 marks active chromatin by replication-independent nucleosome assembly. Mol. Cell 9:1191–200
    [Google Scholar]
  5. 5.  Ai X, Parthun MR 2004. The nuclear Hat1p/Hat2p complex: a molecular link between type B histone acetyltransferases and chromatin assembly. Mol. Cell 14:195–205
    [Google Scholar]
  6. 6.  Alekseev OM, Bencic DC, Richardson RT, Widgren EE, O'Rand MG 2003. Overexpression of the linker histone-binding protein tNASP affects progression through the cell cycle. J. Biol. Chem. 278:8846–52
    [Google Scholar]
  7. 7.  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. 286:17714–21
    [Google Scholar]
  8. 8.  An S, Yoon J, Kim H, Song JJ, Cho US 2017. Structure-based nuclear import mechanism of histones H3 and H4 mediated by Kap123. eLife 6:e30244
    [Google Scholar]
  9. 9.  Annunziato AT 2005. Split decision: What happens to nucleosomes during DNA replication?. J. Biol. Chem. 280:12065–68
    [Google Scholar]
  10. 10.  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 31:2013–23
    [Google Scholar]
  11. 11.  Banumathy G, Somaiah N, Zhang R, Tang Y, Hoffmann J et al. 2009. 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. 29:758–70
    [Google Scholar]
  12. 12.  Barman HK, Takami Y, Ono T, Nishijima H, Sanematsu F et al. 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. 345:1547–57
    [Google Scholar]
  13. 13.  Belotserkovskaya R, Oh S, Bondarenko VA, Orphanides G, Studitsky VM, Reinberg D 2003. FACT facilitates transcription-dependent nucleosome alteration. Science 301:1090–93
    [Google Scholar]
  14. 14.  Benson LJ, Phillips JA, Gu Y, Parthun MR, Hoffman CS, Annunziato AT 2007. Properties of the type B histone acetyltransferase Hat1: H4 tail interaction, site preference, and involvement in DNA repair. J. Biol. Chem. 282:836–42
    [Google Scholar]
  15. 15.  Black BE, Foltz DR, Chakravarthy S, Luger K, Woods VL Jr., Cleveland DW 2004. Structural determinants for generating centromeric chromatin. Nature 430:578–82
    [Google Scholar]
  16. 16.  Black BE, Jansen LE, Maddox PS, Foltz DR, Desai AB et al. 2007. Centromere identity maintained by nucleosomes assembled with histone H3 containing the CENP-A targeting domain. Mol. Cell 25:309–22
    [Google Scholar]
  17. 17.  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. 282:20142–50
    [Google Scholar]
  18. 18.  Bowman A, Koide A, Goodman JS, Colling ME, Zinne D et al. 2017. sNASP and ASF1A function through both competitive and compatible modes of histone binding. Nucleic Acids Res 45:643–56
    [Google Scholar]
  19. 19.  Bowman A, Lercher L, Singh HR, Zinne D, Timinszky G et al. 2016. The histone chaperone sNASP binds a conserved peptide motif within the globular core of histone H3 through its TPR repeats. Nucleic Acids Res 44:3105–17
    [Google Scholar]
  20. 20.  Brennan LD, Forties RA, Patel SS, Wang MD 2016. DNA looping mediates nucleosome transfer. Nat. Commun. 7:13337
    [Google Scholar]
  21. 21.  Camahort R, Li B, Florens L, Swanson SK, Washburn MP, Gerton JL 2007. Scm3 is essential to recruit the histone H3 variant Cse4 to centromeres and to maintain a functional kinetochore. Mol. Cell 26:853–65
    [Google Scholar]
  22. 22.  Campos EI, Fillingham J, Li G, Zheng H, Voigt P et al. 2010. The program for processing newly synthesized histones H3.1 and H4. Nat. Struct. Mol. Biol. 17:1343–51
    [Google Scholar]
  23. 23.  Campos EI, Reinberg D 2009. Histones: annotating chromatin. Annu. Rev. Genet. 43:559–99
    [Google Scholar]
  24. 24.  Campos EI, Smits AH, Kang YH, Landry S, Escobar TM et al. 2015. Analysis of the Histone H3.1 interactome: a suitable chaperone for the right event. Mol. Cell 60:697–709
    [Google Scholar]
  25. 25.  Chang HW, Pandey M, Kulaeva OI, Patel SS, Studitsky VM 2016. Overcoming a nucleosomal barrier to replication. Sci. Adv. 2:e1601865
    [Google Scholar]
  26. 26.  Chen P, Zhao J, Wang Y, Wang M, Long H et al. 2013. H3.3 actively marks enhancers and primes gene transcription via opening higher-ordered chromatin. Genes Dev 27:2109–24
    [Google Scholar]
  27. 27.  Chow CM, Georgiou A, Szutorisz H, Maia e Silva A, Pombo A et al. 2005. Variant histone H3.3 marks promoters of transcriptionally active genes during mammalian cell division. EMBO Rep 6:354–60
    [Google Scholar]
  28. 28.  Cook AJ, Gurard-Levin ZA, Vassias I, Almouzni G 2011. A specific function for the histone chaperone NASP to fine-tune a reservoir of soluble H3-H4 in the histone supply chain. Mol. Cell 44:918–27
    [Google Scholar]
  29. 29.  Corpet A, De Koning L, Toedling J, Savignoni A, Berger F et al. 2011. Asf1b, the necessary Asf1 isoform for proliferation, is predictive of outcome in breast cancer. EMBO J 30:480–93
    [Google Scholar]
  30. 30.  Dahlin JL, Chen X, Walters MA, Zhang Z 2015. Histone-modifying enzymes, histone modifications and histone chaperones in nucleosome assembly: lessons learned from Rtt109 histone acetyltransferases. Crit. Rev. Biochem. Mol. Biol. 50:31–53
    [Google Scholar]
  31. 31.  Davey CA, Sargent DF, Luger K, Maeder AW, Richmond TJ 2002. Solvent mediated interactions in the structure of the nucleosome core particle at 1.9 Å resolution. J. Mol. Biol. 319:1097–113
    [Google Scholar]
  32. 32.  Dechassa ML, Wyns K, Luger K 2014. Scm3 deposits a (Cse4–H4)2 tetramer onto DNA through a Cse4–H4 dimer intermediate. Nucleic Acids Res 42:5532–42
    [Google Scholar]
  33. 33.  Dennehey BK, Noone S, Liu WH, Smith L, Churchill ME, Tyler JK 2013. The C terminus of the histone chaperone Asf1 cross-links to histone H3 in yeast and promotes interaction with histones H3 and H4. Mol. Cell. Biol. 33:605–21
    [Google Scholar]
  34. 34.  Dhayalan A, Tamas R, Bock I, Tattermusch A, Dimitrova E et al. 2011. The ATRX-ADD domain binds to H3 tail peptides and reads the combined methylation state of K4 and K9. Hum. Mol. Genet. 20:2195–203
    [Google Scholar]
  35. 35.  Donham DC II, Scorgie JK, Churchill ME 2011. The activity of the histone chaperone yeast Asf1 in the assembly and disassembly of histone H3/H4–DNA complexes. Nucleic Acids Res 39:5449–58
    [Google Scholar]
  36. 36.  Drane P, Ouararhni K, Depaux A, Shuaib M, Hamiche A 2010. The death-associated protein DAXX is a novel histone chaperone involved in the replication-independent deposition of H3.3. Genes Dev 24:1253–65
    [Google Scholar]
  37. 37.  Dunleavy EM, Pidoux AL, Monet M, Bonilla C, Richardson W et al. 2007. A NASP (N1/N2)-related protein, Sim3, binds CENP-A and is required for its deposition at fission yeast centromeres. Mol. Cell 28:1029–44
    [Google Scholar]
  38. 38.  Dunleavy EM, Roche D, Tagami H, Lacoste N, Ray-Gallet D et al. 2009. HJURP is a cell-cycle-dependent maintenance and deposition factor of CENP-A at centromeres. Cell 137:485–97
    [Google Scholar]
  39. 39.  Elsaesser SJ, Allis CD 2010. HIRA and Daxx constitute two independent histone H3.3-containing predeposition complexes. Cold Spring Harb. Symp. Quant. Biol. 75:27–34
    [Google Scholar]
  40. 40.  Elsasser SJ, Noh KM, Diaz N, Allis CD, Banaszynski LA 2015. Histone H3.3 is required for endogenous retroviral element silencing in embryonic stem cells. Nature 522:240–44
    [Google Scholar]
  41. 41.  English CM, Adkins MW, Carson JJ, Churchill ME, Tyler JK 2006. Structural basis for the histone chaperone activity of Asf1. Cell 127:495–508
    [Google Scholar]
  42. 42.  Eustermann S, Yang JC, Law MJ, Amos R, Chapman LM et al. 2011. Combinatorial readout of histone H3 modifications specifies localization of ATRX to heterochromatin. Nat. Struct. Mol. Biol. 18:777–82
    [Google Scholar]
  43. 43.  Foltman M, Evrin C, De Piccoli G, Jones RC, Edmondson RD et al. 2013. Eukaryotic replisome components cooperate to process histones during chromosome replication. Cell Rep 3:892–904
    [Google Scholar]
  44. 44.  Foltz DR, Jansen LE, Bailey AO, Yates JR3rd, Bassett EA et al. 2009. Centromere-specific assembly of CENP-a nucleosomes is mediated by HJURP. Cell 137:472–84
    [Google Scholar]
  45. 45.  Foltz DR, Jansen LE, Black BE, Bailey AO, Yates JR III, Cleveland DW 2006. The human CENP-A centromeric nucleosome-associated complex. Nat. Cell Biol. 8:458–69
    [Google Scholar]
  46. 46.  Formosa T 2012. The role of FACT in making and breaking nucleosomes. Biochim. Biophys. Acta 1819:247–55
    [Google Scholar]
  47. 47.  Franklin SG, Zweidler A 1977. Non-allelic variants of histones 2a, 2b and 3 in mammals. Nature 266:273–75
    [Google Scholar]
  48. 48.  Fujita Y, Hayashi T, Kiyomitsu T, Toyoda Y, Kokubu A et al. 2007. Priming of centromere for CENP-A recruitment by human hMis18α, hMis18β, and M18BP1. Dev. Cell 12:17–30
    [Google Scholar]
  49. 49.  Gambus A, Jones RC, Sanchez-Diaz A, Kanemaki M, van Deursen F et al. 2006. GINS maintains association of Cdc45 with MCM in replisome progression complexes at eukaryotic DNA replication forks. Nat. Cell Biol. 8:358–66
    [Google Scholar]
  50. 50.  Garg J, Lambert JP, Karsou A, Marquez S, Nabeel-Shah S et al. 2013. Conserved Asf1–importin β physical interaction in growth and sexual development in the ciliate Tetrahymena thermophila. J. Proteom. 94:311–26
    [Google Scholar]
  51. 51.  Goldberg AD, Banaszynski LA, Noh KM, Lewis PW, Elsaesser SJ et al. 2010. Distinct factors control histone variant H3.3 localization at specific genomic regions. Cell 140:678–91
    [Google Scholar]
  52. 52.  Greiner M, Caesar S, Schlenstedt G 2004. The histones H2A/H2B and H3/H4 are imported into the yeast nucleus by different mechanisms. Eur. J. Cell Biol. 83:511–20
    [Google Scholar]
  53. 53.  Groth A, Corpet A, Cook AJ, Roche D, Bartek J et al. 2007. Regulation of replication fork progression through histone supply and demand. Science 318:1928–31
    [Google Scholar]
  54. 54.  Groth A, Ray-Gallet D, Quivy JP, Lukas J, Bartek J, Almouzni G 2005. Human Asf1 regulates the flow of S phase histones during replicational stress. Mol. Cell 17:301–11
    [Google Scholar]
  55. 55.  Gurard-Levin ZA, Quivy JP, Almouzni G 2014. Histone chaperones: assisting histone traffic and nucleosome dynamics. Annu. Rev. Biochem. 83:487–517
    [Google Scholar]
  56. 56.  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. 290:30648–57
    [Google Scholar]
  57. 57.  Hake SB, Allis CD 2006. Histone H3 variants and their potential role in indexing mammalian genomes: the “H3 barcode hypothesis. .” PNAS 103:6428–35
    [Google Scholar]
  58. 58.  Hammond CM, Stromme CB, Huang H, Patel DJ, Groth A 2017. Histone chaperone networks shaping chromatin function. Nat. Rev. Mol. Cell Biol. 18:141–58
    [Google Scholar]
  59. 59.  Han J, Zhou H, Li Z, Xu RM, Zhang Z 2007. Acetylation of lysine 56 of histone H3 catalyzed by RTT109 and regulated by ASF1 is required for replisome integrity. J. Biol. Chem. 282:28587–96
    [Google Scholar]
  60. 60.  Hayashi R, Goto Y, Tanaka R, Oonogi K, Hisasue M, Yoshida K 2007. Transcriptional regulation of human chromatin assembly factor ASF1. DNA Cell Biol 26:91–99
    [Google Scholar]
  61. 61.  Hayashi T, Fujita Y, Iwasaki O, Adachi Y, Takahashi K, Yanagida M 2004. Mis16 and Mis18 are required for CENP-A loading and histone deacetylation at centromeres. Cell 118:715–29
    [Google Scholar]
  62. 62.  Henikoff S, Smith MM 2015. Histone variants and epigenetics. Cold Spring Harb. Perspect. Biol. 7:a019364
    [Google Scholar]
  63. 63.  Hsieh FK, Kulaeva OI, Patel SS, Dyer PN, Luger K et al. 2013. Histone chaperone FACT action during transcription through chromatin by RNA polymerase II. PNAS 110:7654–59
    [Google Scholar]
  64. 64.  Hu H, Liu Y, Wang M, Fang J, Huang H et al. 2011. Structure of a CENP-A-histone H4 heterodimer in complex with chaperone HJURP. Genes Dev 25:901–6
    [Google Scholar]
  65. 65.  Huang C, Zhang Z, Xu M, Li Y, Li Z et al. 2013. H3.3-H4 tetramer splitting events feature cell-type specific enhancers. PLOS Genet 9:e1003558
    [Google Scholar]
  66. 66.  Huang H, Stromme CB, Saredi G, Hodl M, Strandsby A et al. 2015. A unique binding mode enables MCM2 to chaperone histones H3–H4 at replication forks. Nat. Struct. Mol. Biol. 22:618–26
    [Google Scholar]
  67. 67.  Ishimi Y, Komamura Y, You Z, Kimura H 1998. Biochemical function of mouse minichromosome maintenance 2 protein. J. Biol. Chem. 273:8369–75
    [Google Scholar]
  68. 68.  Ishimi Y, Komamura-Kohno Y, Arai K, Masai H 2001. Biochemical activities associated with mouse Mcm2 protein. J. Biol. Chem. 276:42744–52
    [Google Scholar]
  69. 69.  Iwase S, Xiang B, Ghosh S, Ren T, Lewis PW et al. 2011. ATRX ADD domain links an atypical histone methylation recognition mechanism to human mental-retardation syndrome. Nat. Struct. Mol. Biol. 18:769–76
    [Google Scholar]
  70. 70.  Jackson V, Shires A, Tanphaichitr N, Chalkley R 1976. Modifications to histones immediately after synthesis. J. Mol. Biol. 104:471–83
    [Google Scholar]
  71. 71.  Jansen LE, Black BE, Foltz DR, Cleveland DW 2007. Propagation of centromeric chromatin requires exit from mitosis. J. Cell Biol. 176:795–805
    [Google Scholar]
  72. 72.  Jasencakova Z, Scharf AN, Ask K, Corpet A, Imhof A et al. 2010. Replication stress interferes with histone recycling and predeposition marking of new histones. Mol. Cell 37:736–43
    [Google Scholar]
  73. 73.  Jin C, Zang C, Wei G, Cui K, Peng W et al. 2009. H3.3/H2A.Z double variant-containing nucleosomes mark ‘nucleosome-free regions’ of active promoters and other regulatory regions. Nat. Genet. 41:941–45
    [Google Scholar]
  74. 74.  Kadyrova LY, Rodriges Blanko E, Kadyrov FA 2013. Human CAF-1-dependent nucleosome assembly in a defined system. Cell Cycle 12:3286–97
    [Google Scholar]
  75. 75.  Kang YH, Galal WC, Farina A, Tappin I, Hurwitz J 2012. Properties of the human Cdc45/Mcm2-7/GINS helicase complex and its action with DNA polymerase ε in rolling circle DNA synthesis. PNAS 109:6042–47
    [Google Scholar]
  76. 76.  Kaufman PD, Kobayashi R, Kessler N, Stillman B 1995. The p150 and p60 subunits of chromatin assembly factor I: a molecular link between newly synthesized histones and DNA replication. Cell 81:1105–14
    [Google Scholar]
  77. 77.  Kelly TJ, Qin S, Gottschling DE, Parthun MR 2000. Type B histone acetyltransferase Hat1p participates in telomeric silencing. Mol. Cell. Biol. 20:7051–58
    [Google Scholar]
  78. 78.  Kemble DJ, McCullough LL, Whitby FG, Formosa T, Hill CP 2015. FACT disrupts nucleosome structure by binding H2A-H2B with conserved peptide motifs. Mol. Cell 60:294–306
    [Google Scholar]
  79. 79.  Kemble DJ, Whitby FG, Robinson H, McCullough LL, Formosa T, Hill CP 2013. Structure of the Spt16 middle domain reveals functional features of the histone chaperone FACT. J. Biol. Chem. 288:10188–94
    [Google Scholar]
  80. 80.  Kim D, Setiaputra D, Jung T, Chung J, Leitner A et al. 2016. Molecular architecture of yeast chromatin assembly factor 1. Sci. Rep. 6:26702
    [Google Scholar]
  81. 81.  Kleff S, Andrulis ED, Anderson CW, Sternglanz R 1995. Identification of a gene encoding a yeast histone H4 acetyltransferase. J. Biol. Chem. 270:24674–77
    [Google Scholar]
  82. 82.  Krohne G 1985. Immunological identification of the karyophilic, histone-binding proteins N1 and N2 in somatic cells and oocytes of diverse amphibia. Exp. Cell Res. 158:205–22
    [Google Scholar]
  83. 83.  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 65:117–30
    [Google Scholar]
  84. 84.  Laskey RA, Honda BM, Mills AD, Finch JT 1978. Nucleosomes are assembled by an acidic protein which binds histones and transfers them to DNA. Nature 275:416–20
    [Google Scholar]
  85. 85.  Laskey RA, Kearsey SE, Mechali M, Dingwall C, Mills AD et al. 1985. Chromosome replication in early Xenopus embryos. Cold Spring Harb. Symp. Quant. Biol. 50:657–63
    [Google Scholar]
  86. 86.  Lechner MS, Schultz DC, Negorev D, Maul GG, Rauscher FJ III 2005. The mammalian heterochromatin protein 1 binds diverse nuclear proteins through a common motif that targets the chromoshadow domain. Biochem. Biophys. Res. Commun. 331:929–37
    [Google Scholar]
  87. 87.  Levy MA, Kernohan KD, Jiang Y, Berube NG 2015. ATRX promotes gene expression by facilitating transcriptional elongation through guanine-rich coding regions. Hum. Mol. Genet. 24:1824–35
    [Google Scholar]
  88. 88.  Lewis PW, Elsaesser SJ, Noh KM, Stadler SC, Allis CD 2010. Daxx is an H3.3-specific histone chaperone and cooperates with ATRX in replication-independent chromatin assembly at telomeres. PNAS 107:14075–80
    [Google Scholar]
  89. 89.  Li Q, Zhou H, Wurtele H, Davies B, Horazdovsky B et al. 2008. Acetylation of histone H3 lysine 56 regulates replication-coupled nucleosome assembly. Cell 134:244–55
    [Google Scholar]
  90. 90.  Ling X, Harkness TA, Schultz MC, Fisher-Adams G, Grunstein M 1996. Yeast histone H3 and H4 amino termini are important for nucleosome assembly in vivo and in vitro: redundant and position-independent functions in assembly but not in gene regulation. Genes Dev 10:686–99
    [Google Scholar]
  91. 91.  Liu CP, Xiong C, Wang M, Yu Z, Yang N et al. 2012. Structure of the variant histone H3.3-H4 heterodimer in complex with its chaperone DAXX. Nat. Struct. Mol. Biol. 19:1287–92
    [Google Scholar]
  92. 92.  Liu WH, Roemer SC, Port AM, Churchill ME 2012. CAF-1-induced oligomerization of histones H3/H4 and mutually exclusive interactions with Asf1 guide H3/H4 transitions among histone chaperones and DNA. Nucleic Acids Res 40:11229–39
    [Google Scholar]
  93. 93.  Liu WH, Roemer SC, Zhou Y, Shen ZJ, Dennehey BK et al. 2016. The Cac1 subunit of histone chaperone CAF-1 organizes CAF-1-H3/H4 architecture and tetramerizes histones. eLife 5:e10823
    [Google Scholar]
  94. 94.  Louie AJ, Dixon GH 1972. Synthesis, acetylation, and phosphorylation of histone IV and its binding to DNA during spermatogenesis in trout. PNAS 69:1975–79
    [Google Scholar]
  95. 95.  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 24:309–16
    [Google Scholar]
  96. 96.  Luger K, Mader AW, Richmond RK, Sargent DF, Richmond TJ 1997. Crystal structure of the nucleosome core particle at 2.8 Å resolution. Nature 389:251–60
    [Google Scholar]
  97. 97.  Ma XJ, Wu J, Altheim BA, Schultz MC, Grunstein M 1998. Deposition-related sites K5/K12 in histone H4 are not required for nucleosome deposition in yeast. PNAS 95:6693–98
    [Google Scholar]
  98. 98.  Madamba EV, Berthet EB, Francis NJ 2017. Inheritance of histones H3 and H4 during DNA replication in vitro. Cell Rep 21:1361–74
    [Google Scholar]
  99. 99.  Maksimov V, Nakamura M, Wildhaber T, Nanni P, Ramstrom M et al. 2016. The H3 chaperone function of NASP is conserved in Arabidopsis. Plant J 88:425–36
    [Google Scholar]
  100. 100.  Malay AD, Umehara T, Matsubara-Malay K, Padmanabhan B, Yokoyama S 2008. Crystal structures of fission yeast histone chaperone Asf1 complexed with the Hip1 B-domain or the Cac2 C terminus. J. Biol. Chem. 283:14022–31
    [Google Scholar]
  101. 101.  Malik HS, Henikoff S 2003. Phylogenomics of the nucleosome. Nat. Struct. Biol. 10:882–91
    [Google Scholar]
  102. 102.  Mattiroli F, D'Arcy S, Luger K 2015. The right place at the right time: chaperoning core histone variants. EMBO Rep 16:1454–66
    [Google Scholar]
  103. 103.  Mattiroli F, Gu Y, Balsbaugh JL, Ahn NG, Luger K 2017. The Cac2 subunit is essential for productive histone binding and nucleosome assembly in CAF-1. Sci. Rep. 7:46274
    [Google Scholar]
  104. 104.  Mattiroli F, Gu Y, Yadav T, Balsbaugh JL, Harris MR et al. 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:e22799
    [Google Scholar]
  105. 105.  Mejlvang J, Feng Y, Alabert C, Neelsen KJ, Jasencakova Z et al. 2014. New histone supply regulates replication fork speed and PCNA unloading. J. Cell Biol. 204:29–43
    [Google Scholar]
  106. 106.  Mito Y, Henikoff JG, Henikoff S 2005. Genome-scale profiling of histone H3.3 replacement patterns. Nat. Genet. 37:1090–97
    [Google Scholar]
  107. 107.  Mizuguchi G, Xiao H, Wisniewski J, Smith MM, Wu C 2007. Nonhistone Scm3 and histones CenH3-H4 assemble the core of centromere-specific nucleosomes. Cell 129:1153–64
    [Google Scholar]
  108. 108.  Mosammaparast N, Guo Y, Shabanowitz J, Hunt DF, Pemberton LF 2002. Pathways mediating the nuclear import of histones H3 and H4 in yeast. J. Biol. Chem. 277:862–68
    [Google Scholar]
  109. 109.  Moyer SE, Lewis PW, Botchan MR 2006. Isolation of the Cdc45/Mcm2–7/GINS (CMG) complex, a candidate for the eukaryotic DNA replication fork helicase. PNAS 103:10236–41
    [Google Scholar]
  110. 110.  Muller S, Almouzni G 2017. Chromatin dynamics during the cell cycle at centromeres. Nat. Rev. Genet. 18:192–208
    [Google Scholar]
  111. 111.  Murzina NV, Pei XY, Zhang W, Sparkes M, Vicente-Garcia J et al. 2008. Structural basis for the recognition of histone H4 by the histone-chaperone RbAp46. Structure 16:1077–85
    [Google Scholar]
  112. 112.  Nabeel-Shah S, Ashraf K, Pearlman RE, Fillingham J 2014. Molecular evolution of NASP and conserved histone H3/H4 transport pathway. BMC Evol. Biol. 14:139
    [Google Scholar]
  113. 113.  Nagarajan P, Ge Z, Sirbu B, Doughty C, Agudelo Garcia PA et al. 2013. Histone acetyl transferase 1 is essential for mammalian development, genome stability, and the processing of newly synthesized histones H3 and H4. PLOS Genet 9:e1003518
    [Google Scholar]
  114. 114.  Nardi IK, Zasadzińska E, Stellfox ME, Knippler CM, Foltz DR 2016. Licensing of centromeric chromatin assembly through the Mis18α-Mis18β heterotetramer. Mol. Cell 61:774–87
    [Google Scholar]
  115. 115.  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 446:338–41
    [Google Scholar]
  116. 116.  Niikura Y, Kitagawa R, Ogi H, Abdulle R, Pagala V, Kitagawa K 2015. CENP-A K124 ubiquitylation is required for CENP-A deposition at the centromere. Dev. Cell 32:589–603
    [Google Scholar]
  117. 117.  Osakabe A, Tachiwana H, Matsunaga T, Shiga T, Nozawa RS et al. 2010. Nucleosome formation activity of human somatic nuclear autoantigenic sperm protein (sNASP). J. Biol. Chem. 285:11913–21
    [Google Scholar]
  118. 118.  Park YJ, Luger K 2008. Histone chaperones in nucleosome eviction and histone exchange. Curr. Opin. Struct. Biol. 18:282–89
    [Google Scholar]
  119. 119.  Parthun MR 2012. Histone acetyltransferase 1: more than just an enzyme?. Biochim. Biophys. Acta 1819:256–63
    [Google Scholar]
  120. 120.  Parthun MR, Widom J, Gottschling DE 1996. The major cytoplasmic histone acetyltransferase in yeast: links to chromatin replication and histone metabolism. Cell 87:85–94
    [Google Scholar]
  121. 121.  Poveda A, Pamblanco M, Tafrov S, Tordera V, Sternglanz R, Sendra R 2004. Hif1 is a component of yeast histone acetyltransferase B, a complex mainly localized in the nucleus. J. Biol. Chem. 279:16033–43
    [Google Scholar]
  122. 122.  Pradhan SK, Su T, Yen L, Jacquet K, Huang C et al. 2016. EP400 deposits H3.3 into promoters and enhancers during gene activation. Mol. Cell 61:27–38
    [Google Scholar]
  123. 123.  Qin S, Parthun MR 2002. Histone H3 and the histone acetyltransferase Hat1p contribute to DNA double-strand break repair. Mol. Cell. Biol. 22:8353–65
    [Google Scholar]
  124. 124.  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 9:1091–100
    [Google Scholar]
  125. 125.  Ray-Gallet D, Woolfe A, Vassias I, Pellentz C, Lacoste N 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 44:928–41
    [Google Scholar]
  126. 125a.  Reverón-Gómez N, González-Aguilera C, Stewart-Morgan KR, Petryk N, Flury V et al. 2018. Accurate recycling of parental histones reproduces the histone modification landscape during DNA replication. Mol. Cell 72:239–49.e5
    [Google Scholar]
  127. 126.  Richardson RT, Batova IN, Widgren EE, Zheng LX, Whitfield M et al. 2000. Characterization of the histone H1-binding protein, NASP, as a cell cycle-regulated somatic protein. J. Biol. Chem. 275:30378–86
    [Google Scholar]
  128. 127.  Richet N, Liu D, Legrand P, Velours C, Corpet A 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 43:1905–17
    [Google Scholar]
  129. 128.  Ricketts MD, Frederick B, Hoff H, Tang Y, Schultz DC et al. 2015. Ubinuclein-1 confers histone H3.3-specific-binding by the HIRA histone chaperone complex. Nat. Commun. 6:7711
    [Google Scholar]
  130. 129.  Rivera C, Saavedra F, Alvarez F, Diaz-Celis C, Ugalde V et al. 2015. Methylation of histone H3 lysine 9 occurs during translation. Nucleic Acids Res 43:9097–106
    [Google Scholar]
  131. 130.  Ruiz-Carrillo A, Wangh LJ, Allfrey VG 1975. Processing of newly synthesized histone molecules. Science 190:117–28
    [Google Scholar]
  132. 131.  Saavedra F, Rivera C, Rivas E, Merino P, Garrido D et al. 2017. PP32 and SET/TAF-Iβ proteins regulate the acetylation of newly synthesized histone H4. Nucleic Acids Res 45:11700–10
    [Google Scholar]
  133. 132.  Sarai N, Nimura K, Tamura T, Kanno T, Patel MC et al. 2013. WHSC1 links transcription elongation to HIRA-mediated histone H3.3 deposition. EMBO J 32:2392–406
    [Google Scholar]
  134. 133.  Sauer PV, Timm J, Liu D, Sitbon D, Boeri-Erba E et al. 2017. Insights into the molecular architecture and histone H3-H4 deposition mechanism of yeast Chromatin assembly factor 1. eLife 6:e23474
    [Google Scholar]
  135. 134.  Scorgie JK, Donham DC III, Churchill ME 2012. Analysis of histone chaperone antisilencing function 1 interactions. Methods Enzymol 512:223–41
    [Google Scholar]
  136. 135.  Shibahara K, Stillman B 1999. Replication-dependent marking of DNA by PCNA facilitates CAF-1-coupled inheritance of chromatin. Cell 96:575–85
    [Google Scholar]
  137. 136.  Shibahara K, Verreault A, Stillman B 2000. The N-terminal domains of histones H3 and H4 are not necessary for chromatin assembly factor-1-mediated nucleosome assembly onto replicated DNA in vitro. PNAS 97:7766–71
    [Google Scholar]
  138. 137.  Shuaib M, Ouararhni K, Dimitrov S, Hamiche A 2010. HJURP binds CENP-A via a highly conserved N-terminal domain and mediates its deposition at centromeres. PNAS 107:1349–54
    [Google Scholar]
  139. 138.  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 25:1320–27
    [Google Scholar]
  140. 139.  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 58:15–25
    [Google Scholar]
  141. 140.  Sobel RE, Cook RG, Perry CA, Annunziato AT, Allis CD 1995. Conservation of deposition-related acetylation sites in newly synthesized histones H3 and H4. PNAS 92:1237–41
    [Google Scholar]
  142. 141.  Song JJ, Garlick JD, Kingston RE 2008. Structural basis of histone H4 recognition by p55. Genes Dev 22:1313–18
    [Google Scholar]
  143. 142.  Soniat M, Cagatay T, Chook YM 2016. Recognition elements in the histone H3 and H4 tails for seven different importins. J. Biol. Chem. 291:21171–83
    [Google Scholar]
  144. 143.  Stoler S, Rogers K, Weitze S, Morey L, Fitzgerald-Hayes M, Baker RE 2007. Scm3, an essential Saccharomyces cerevisiae centromere protein required for G2/M progression and Cse4 localization. PNAS 104:10571–76
    [Google Scholar]
  145. 144.  Tachiwana H, Osakabe A, Shiga T, Miya Y, Kimura H et al. 2011. Structures of human nucleosomes containing major histone H3 variants. Acta Crystallogr. Sect. D 67:578–83
    [Google Scholar]
  146. 145.  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 116:51–61
    [Google Scholar]
  147. 146.  Tan BC, Chien CT, Hirose S, Lee SC 2006. Functional cooperation between FACT and MCM helicase facilitates initiation of chromatin DNA replication. EMBO J 25:3975–85
    [Google Scholar]
  148. 147.  Tang J, Wu S, Liu H, Stratt R, Barak OG et al. 2004. A novel transcription regulatory complex containing death domain-associated protein and the ATR-X syndrome protein. J. Biol. Chem. 279:20369–77
    [Google Scholar]
  149. 148.  Tang Y, Poustovoitov MV, Zhao K, Garfinkel M, Canutescu A et al. 2006. Structure of a human ASF1a–HIRA complex and insights into specificity of histone chaperone complex assembly. Nat. Struct. Mol. Biol. 13:921–29
    [Google Scholar]
  150. 149.  Tsunaka Y, Fujiwara Y, Oyama T, Hirose S, Morikawa K 2016. Integrated molecular mechanism directing nucleosome reorganization by human FACT. Genes Dev 30:673–86
    [Google Scholar]
  151. 150.  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 402:555–60
    [Google Scholar]
  152. 151.  Tyler JK, Bulger M, Kamakaka RT, Kobayashi R, Kadonaga JT 1996. The p55 subunit of Drosophila chromatin assembly factor 1 is homologous to a histone deacetylase-associated protein. Mol. Cell. Biol. 16:6149–59
    [Google Scholar]
  153. 152.  Urban MK, Zweidler A 1983. Changes in nucleosomal core histone variants during chicken development and maturation. Dev. Biol. 95:421–28
    [Google Scholar]
  154. 153.  Verreault A, Kaufman PD, Kobayashi R, Stillman B 1998. Nucleosomal DNA regulates the core-histone-binding subunit of the human Hat1 acetyltransferase. Curr. Biol. 8:96–108
    [Google Scholar]
  155. 154.  Voon HP, Hughes JR, Rode C, De La Rosa-Velázquez IA, Jenuwein T et al. 2015. ATRX plays a key role in maintaining silencing at interstitial heterochromatic loci and imprinted genes. Cell Rep 11:405–18
    [Google Scholar]
  156. 155.  Wang H, Ge Z, Walsh ST, Parthun MR 2012. The human histone chaperone sNASP interacts with linker and core histones through distinct mechanisms. Nucleic Acids Res 40:660–69
    [Google Scholar]
  157. 156.  Wang H, Walsh ST, Parthun MR 2008. Expanded binding specificity of the human histone chaperone NASP. Nucleic Acids Res 36:5763–72
    [Google Scholar]
  158. 157.  Winkler DD, Muthurajan UM, Hieb AR, Luger K 2011. Histone chaperone FACT coordinates nucleosome interaction through multiple synergistic binding events. J. Biol. Chem. 286:41883–92
    [Google Scholar]
  159. 158.  Wong LH, Ren H, Williams E, McGhie J, Ahn S et al. 2009. Histone H3.3 incorporation provides a unique and functionally essential telomeric chromatin in embryonic stem cells. Genome Res 19:404–14
    [Google Scholar]
  160. 159.  Wu RS, Tsai S, Bonner WM 1982. Patterns of histone variant synthesis can distinguish G0 from G1 cells. Cell 31:367–74
    [Google Scholar]
  161. 160.  Xu F, Zhang K, Grunstein M 2005. Acetylation in histone H3 globular domain regulates gene expression in yeast. Cell 121:375–85
    [Google Scholar]
  162. 161.  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 328:94–98
    [Google Scholar]
  163. 162.  Xue Y, Gibbons R, Yan Z, Yang D, McDowell TL et al. 2003. The ATRX syndrome protein forms a chromatin-remodeling complex with Daxx and localizes in promyelocytic leukemia nuclear bodies. PNAS 100:10635–40
    [Google Scholar]
  164. 163.  Yoon J, Kim SJ, An S, Cho S, Leitner A et al. 2018. Integrative structural investigation on the architecture of human Importin4_histone H3/H4_Asf1a complex and its histone H3 tail binding. J. Mol. Biol. 430:822–41
    [Google Scholar]
  165. 164.  Yu Z, Zhou X, Wang W, Deng W, Fang J et al. 2015. Dynamic phosphorylation of CENP-A at Ser68 orchestrates its cell-cycle-dependent deposition at centromeres. Dev. Cell 32:68–81
    [Google Scholar]
  166. 165.  Zasadzińska E, Barnhart-Dailey MC, Kuich PH, Foltz DR 2013. Dimerization of the CENP-A assembly factor HJURP is required for centromeric nucleosome deposition. EMBO J 32:2113–24
    [Google Scholar]
  167. 166.  Zhang H, Gan H, Wang Z, Lee JH, Zhou H et al. 2017. RPA interacts with HIRA and regulates H3.3 deposition at gene regulatory elements in mammalian cells. Mol. Cell 65:272–84
    [Google Scholar]
  168. 167.  Zhang K, Gao Y, Li J, Burgess R, Han J et al. 2016. A DNA binding winged helix domain in CAF-1 functions with PCNA to stabilize CAF-1 at replication forks. Nucleic Acids Res 44:5083–94
    [Google Scholar]
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