1932

Abstract

Nucleosome dynamics and properties are central to all forms of genomic activities. Among the core histones, H3 variants play a pivotal role in modulating nucleosome structure and function. Here, we focus on the impact of H3 variants on various facets of development. The deposition of the replicative H3 variant following DNA replication is essential for the transmission of the epigenomic information encoded in posttranscriptional modifications. Through this process, replicative H3 maintains cell fate while, in contrast, the replacement H3.3 variant opposes cell differentiation during early embryogenesis. In later steps of development, H3.3 and specialized H3 variants are emerging as new, important regulators of terminal cell differentiation, including neurons and gametes. The specific pathways that regulate the dynamics of the deposition of H3.3 are paramount during reprogramming events that drive zygotic activation and the initiation of a new cycle of development.

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2020-11-23
2024-04-12
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Literature Cited

  1. 1. 
    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]
  2. 2. 
    Ait-Ahmed O, Bellon B, Capri M, Joblet C, Thomas-Delaage M 1992. The yemanuclein-α: a new Drosophila DNA binding protein specific for the oocyte nucleus. Mech. Dev. 37:69–80
    [Google Scholar]
  3. 3. 
    Akiyama T, Suzuki O, Matsuda J, Aoki F 2011. Dynamic replacement of histone H3 variants reprograms epigenetic marks in early mouse embryos. PLOS Genet 7:e1002279
    [Google Scholar]
  4. 4. 
    Alabert C, Barth TK, Reveron-Gomez N, Sidoli S, Schmidt A et al. 2015. Two distinct modes for propagation of histone PTMs across the cell cycle. Genes Dev 29:585–90
    [Google Scholar]
  5. 5. 
    Allan J, Mitchell T, Harborne N, Bohm L, Crane-Robinson C 1986. Roles of H1 domains in determining higher order chromatin structure and H1 location. J. Mol. Biol. 187:591–601
    [Google Scholar]
  6. 6. 
    Annunziato AT. 2015. The fork in the road: histone partitioning during DNA replication. Genes 6:353–71
    [Google Scholar]
  7. 7. 
    Balaji S, Iyer LM, Aravind L 2009. HPC2 and ubinuclein define a novel family of histone chaperones conserved throughout eukaryotes. Mol. Biosyst. 5:269–75
    [Google Scholar]
  8. 8. 
    Banaszynski LA, Wen D, Dewell S, Whitcomb SJ, Lin M et al. 2013. Hira-dependent histone H3.3 deposition facilitates PRC2 recruitment at developmental loci in ES cells. Cell 155:107–20
    [Google Scholar]
  9. 9. 
    Bano D, Piazzesi A, Salomoni P, Nicotera P 2017. The histone variant H3.3 claims its place in the crowded scene of epigenetics. Aging 9:602–14
    [Google Scholar]
  10. 10. 
    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]
  11. 11. 
    Bergamin E, Sarvan S, Malette J, Eram MS, Yeung S et al. 2017. Molecular basis for the methylation specificity of ATXR5 for histone H3. Nucleic Acids Res 45:6375–87
    [Google Scholar]
  12. 12. 
    Bintu L, Ishibashi T, Dangkulwanich M, Wu YY, Lubkowska L et al. 2012. Nucleosomal elements that control the topography of the barrier to transcription. Cell 151:738–49
    [Google Scholar]
  13. 13. 
    Blank TA, Becker PB. 1995. Electrostatic mechanism of nucleosome spacing. J. Mol. Biol. 252:305–13
    [Google Scholar]
  14. 14. 
    Bondarenko VA, Steele LM, Újvári A, Gaykalova DA, Kulaeva OI et al. 2006. Nucleosomes can form a polar barrier to transcript elongation by RNA polymerase II. Mol. Cell 24:469–79
    [Google Scholar]
  15. 15. 
    Bonisch C, Hake SB. 2012. Histone H2A variants in nucleosomes and chromatin: more or less stable. ? Nucleic Acids Res 40:10719–41
    [Google Scholar]
  16. 16. 
    Bonnefoy E, Orsi GA, Couble P, Loppin B 2007. The essential role of Drosophila HIRA for de novo assembly of paternal chromatin at fertilization. PLOS Genet 3:1991–2006
    [Google Scholar]
  17. 17. 
    Borg M, Berger F. 2015. Chromatin remodelling during male gametophyte development. Plant J 83:177–88
    [Google Scholar]
  18. 18. 
    Borg M, Jacob Y, Susaki D, LeBlanc C, Buendia D et al. 2020. Targeted reprogramming of H3K27me3 resets epigenetic memory in plant paternal chromatin. Nat. Cell Biol. 22:621–29
    [Google Scholar]
  19. 19. 
    Bowman JL, Kohchi T, Yamato KT, Jenkins J, Shu S et al. 2017. Insights into land plant evolution garnered from the Marchantia polymorpha genome. Cell 171:287–304.e15
    [Google Scholar]
  20. 20. 
    Braunschweig U, Hogan GJ, Pagie L, van Steensel B 2009. Histone H1 binding is inhibited by histone variant H3.3. EMBO J 28:3635–45
    [Google Scholar]
  21. 21. 
    Brykczynska U, Hisano M, Erkek S, Ramos L, Oakeley EJ et al. 2010. Repressive and active histone methylation mark distinct promoters in human and mouse spermatozoa. Nat. Struct. Mol. Biol. 17:679–87
    [Google Scholar]
  22. 22. 
    Buschbeck M, Hake SB. 2017. Variants of core histones and their roles in cell fate decisions, development and cancer. Nat. Rev. Mol. Cell Biol. 18:299–314
    [Google Scholar]
  23. 23. 
    Campbell AE, Shadle SC, Jagannathan S, Lim JW, Resnick R et al. 2018. NuRD and CAF-1-mediated silencing of the D4Z4 array is modulated by DUX4-induced MBD3L proteins. eLife 7:e31023
    [Google Scholar]
  24. 24. 
    Carter B, Bishop B, Ho KK, Huang R, Jia W et al. 2018. The chromatin remodelers PKL and PIE1 act in an epigenetic pathway that determines H3K27me3 homeostasis in Arabidopsis. Plant Cell 30:1337–52
    [Google Scholar]
  25. 25. 
    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]
  26. 26. 
    Coleman-Derr D, Zilberman D. 2012. Deposition of histone variant H2A.Z within gene bodies regulates responsive genes. PLOS Genet 8:e1002988
    [Google Scholar]
  27. 27. 
    Das A, Smoak EM, Linares-Saldana R, Lampson MA, Black BE 2017. Centromere inheritance through the germline. Chromosoma 126:595–604
    [Google Scholar]
  28. 28. 
    Delaney K, Mailler J, Wenda JM, Gabus C, Steiner FA 2018. Differential expression of histone H3.3 genes and their role in modulating temperature stress response in Caenorhabditis elegans. . Genetics 209:551–65
    [Google Scholar]
  29. 29. 
    D'Ippolito RA, Minamino N, Rivera-Casas C, Cheema MS, Bai DL et al. 2019. Protamines from liverwort are produced by posttranslational cleavage and C-terminal di-aminopropanelation of several male germ-specific H1 histones. J. Biol. Chem. 294:16364–73
    [Google Scholar]
  30. 30. 
    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]
  31. 31. 
    Duc C, Benoit M, Detourne G, Simon L, Poulet A et al. 2017. Arabidopsis ATRX modulates H3.3 occupancy and fine-tunes gene expression. Plant Cell 29:1773–93
    [Google Scholar]
  32. 32. 
    Elsasser SJ, Huang H, Lewis PW, Chin JW, Allis CD, Patel DJ 2012. DAXX envelops a histone H3.3-H4 dimer for H3.3-specific recognition. Nature 491:560–65
    [Google Scholar]
  33. 33. 
    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]
  34. 34. 
    Erkek S, Hisano M, Liang CY, Gill M, Murr R et al. 2013. Molecular determinants of nucleosome retention at CpG-rich sequences in mouse spermatozoa. Nat. Struct. Mol. Biol. 20:868–75
    [Google Scholar]
  35. 35. 
    Fan JY, Gordon F, Luger K, Hansen JC, Tremethick DJ 2002. The essential histone variant H2A.Z regulates the equilibrium between different chromatin conformational states. Nat. Struct. Biol. 9:172–76
    [Google Scholar]
  36. 36. 
    Fan JY, Rangasamy D, Luger K, Tremethick DJ 2004. H2A.Z alters the nucleosome surface to promote HP1α-mediated chromatin fiber folding. Mol. Cell 16:655–61
    [Google Scholar]
  37. 37. 
    Fan Y, Nikitina T, Morin-Kensicki EM, Zhao J, Magnuson TR et al. 2003. H1 linker histones are essential for mouse development and affect nucleosome spacing in vivo. Mol. Cell. Biol. 23:4559–72
    [Google Scholar]
  38. 38. 
    Fang HT, El Farran CA, Xing QR, Zhang LF, Li H et al. 2018. Global H3.3 dynamic deposition defines its bimodal role in cell fate transition. Nat. Commun. 9:1537
    [Google Scholar]
  39. 39. 
    Filipescu D, Muller S, Almouzni G 2014. Histone H3 variants and their chaperones during development and disease: contributing to epigenetic control. Annu. Rev. Cell Dev. Biol. 30:615–46
    [Google Scholar]
  40. 40. 
    Filipescu D, Szenker E, Almouzni G 2013. Developmental roles of histone H3 variants and their chaperones. Trends Genet 29:630–40
    [Google Scholar]
  41. 41. 
    Fromental-Ramain C, Ramain P, Hamiche A 2017. The Drosophila DAXX-like protein (DLP) cooperates with ASF1 for H3.3 deposition and heterochromatin formation. Mol. Cell. Biol. 37:e00597–16
    [Google Scholar]
  42. 42. 
    Fukagawa T, Earnshaw WC. 2014. The centromere: chromatin foundation for the kinetochore machinery. Dev. Cell 30:496–508
    [Google Scholar]
  43. 43. 
    Gehre M, Bunina D, Sidoli S, Lubke MJ, Diaz N et al. 2020. Lysine 4 of histone H3.3 is required for embryonic stem cell differentiation, histone enrichment at regulatory regions and transcription accuracy. Nat. Genet. 52:273–82
    [Google Scholar]
  44. 44. 
    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]
  45. 45. 
    Gou L-T, Lim D-H, Ma W, Aubol BE, Hao Y et al. 2020. Initiation of parental genome reprogramming in fertilized oocyte by splicing kinase SRPK1-catalyzed protamine phosphorylation. Cell 180:1212–27.e14
    [Google Scholar]
  46. 46. 
    Green EM, Antczak AJ, Bailey AO, Franco AA, Wu KJ et al. 2005. Replication-independent histone deposition by the HIR complex and Asf1. Curr. Biol. 15:2044–49
    [Google Scholar]
  47. 47. 
    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]
  48. 48. 
    Gunesdogan U, Jackle H, Herzig A 2010. A genetic system to assess in vivo the functions of histones and histone modifications in higher eukaryotes. EMBO Rep 11:772–76
    [Google Scholar]
  49. 49. 
    Gurard-Levin ZA, Quivy JP, Almouzni G 2014. Histone chaperones: assisting histone traffic and nucleosome dynamics. Annu. Rev. Biochem. 83:487–517
    [Google Scholar]
  50. 50. 
    Hammond CM, Stromme CB, Huang H, Patel DJ, Groth A 2017. Histone chaperone networks shaping chromatin function. Nat. Rev. Mol. Cell Biol. 18:141–58
    [Google Scholar]
  51. 51. 
    Hammoud SS, Nix DA, Zhang H, Purwar J, Carrell DT, Cairns BR 2009. Distinctive chromatin in human sperm packages genes for embryo development. Nature 460:473–78
    [Google Scholar]
  52. 52. 
    Harada A, Maehara K, Ono Y, Taguchi H, Yoshioka K et al. 2018. Histone H3.3 sub-variant H3mm7 is required for normal skeletal muscle regeneration. Nat. Commun. 9:1400
    [Google Scholar]
  53. 53. 
    Hatanaka Y, Tsusaka T, Shimizu N, Morita K, Suzuki T et al. 2017. Histone H3 methylated at arginine 17 is essential for reprogramming the paternal genome in zygotes. Cell Rep 20:2756–65
    [Google Scholar]
  54. 54. 
    Heaphy CM, de Wilde RF, Jiao Y, Klein AP, Edil BH et al. 2011. Altered telomeres in tumors with ATRX and DAXX mutations. Science 333:425
    [Google Scholar]
  55. 55. 
    Henikoff S, Ahmad K. 2005. Assembly of variant histones into chromatin. Annu. Rev. Cell Dev. Biol. 21:133–53
    [Google Scholar]
  56. 56. 
    Henikoff S, Smith MM. 2015. Histone variants and epigenetics. Cold Spring Harb. Perspect. Biol. 7:a019364
    [Google Scholar]
  57. 57. 
    Higo A, Kawashima T, Borg M, Zhao M, Lopez-Vidriero I et al. 2018. Transcription factor DUO1 generated by neo-functionalization is associated with evolution of sperm differentiation in plants. Nat. Commun. 9:5283
    [Google Scholar]
  58. 58. 
    Hodl M, Basler K. 2009. Transcription in the absence of histone H3.3. Curr. Biol. 19:1221–26
    [Google Scholar]
  59. 59. 
    Hodl M, Basler K. 2012. Transcription in the absence of histone H3.2 and H3K4 methylation. Curr. Biol. 22:2253–57
    [Google Scholar]
  60. 60. 
    Hoelper D, Huang H, Jain AY, Patel DJ, Lewis PW 2017. Structural and mechanistic insights into ATRX-dependent and -independent functions of the histone chaperone DAXX. Nat. Commun. 8:1193
    [Google Scholar]
  61. 61. 
    Hoghoughi N, Barral S, Vargas A, Rousseaux S, Khochbin S 2018. Histone variants: essential actors in male genome programming. J. Biochem. 163:97–103
    [Google Scholar]
  62. 62. 
    Horard B, Loppin B. 2015. Histone storage and deposition in the early Drosophila embryo. Chromosoma 124:163–75
    [Google Scholar]
  63. 63. 
    Horard B, Sapey-Triomphe L, Bonnefoy E, Loppin B 2018. ASF1 is required to load histones on the HIRA complex in preparation of paternal chromatin assembly at fertilization. Epigenet. Chromatin 11:19
    [Google Scholar]
  64. 64. 
    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]
  65. 65. 
    Ikeuchi M, Iwase A, Rymen B, Harashima H, Shibata M et al. 2015. PRC2 represses dedifferentiation of mature somatic cells in Arabidopsis. Nat. . Plants 1:15089
    [Google Scholar]
  66. 66. 
    Ingouff M, Hamamura Y, Gourgues M, Higashiyama T, Berger F 2007. Distinct dynamics of HISTONE3 variants between the two fertilization products in plants. Curr. Biol. 17:1032–37
    [Google Scholar]
  67. 67. 
    Ingouff M, Rademacher S, Holec S, Soljic L, Xin N et al. 2010. Zygotic resetting of the HISTONE 3 variant repertoire participates in epigenetic reprogramming in Arabidopsis. Curr. . Biol 20:2137–43
    [Google Scholar]
  68. 68. 
    Inoue A, Jiang L, Lu F, Suzuki T, Zhang Y 2017. Maternal H3K27me3 controls DNA methylation-independent imprinting. Nature 547:419–24
    [Google Scholar]
  69. 69. 
    Inoue A, Zhang Y. 2014. Nucleosome assembly is required for nuclear pore complex assembly in mouse zygotes. Nat. Struct. Mol. Biol. 21:609–16
    [Google Scholar]
  70. 70. 
    Ivanauskiene K, Delbarre E, McGhie JD, Kuntziger T, Wong LH, Collas P 2014. The PML-associated protein DEK regulates the balance of H3.3 loading on chromatin and is important for telomere integrity. Genome Res 24:1584–94
    [Google Scholar]
  71. 71. 
    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]
  72. 72. 
    Jacob Y, Bergamin E, Donoghue MT, Mongeon V, LeBlanc C et al. 2014. Selective methylation of histone H3 variant H3.1 regulates heterochromatin replication. Science 343:1249–53
    [Google Scholar]
  73. 73. 
    Jacob Y, Feng S, LeBlanc CA, Bernatavichute YV, Stroud H et al. 2009. ATXR5 and ATXR6 are H3K27 monomethyltransferases required for chromatin structure and gene silencing. Nat. Struct. Mol. Biol. 16:763–68
    [Google Scholar]
  74. 74. 
    Jang CW, Shibata Y, Starmer J, Yee D, Magnuson T 2015. Histone H3.3 maintains genome integrity during mammalian development. Genes Dev 29:1377–92
    [Google Scholar]
  75. 75. 
    Jarillo JA, Pineiro M. 2015. H2A.Z mediates different aspects of chromatin function and modulates flowering responses in Arabidopsis. Plant J 83:96–109
    [Google Scholar]
  76. 76. 
    Jenuwein T, Allis CD. 2001. Translating the histone code. Science 293:1074–80
    [Google Scholar]
  77. 77. 
    Jiang D, Berger F. 2017. DNA replication-coupled histone modification maintains Polycomb gene silencing in plants. Science 357:1146–49
    [Google Scholar]
  78. 78. 
    Jiang D, Berger F. 2017. Histone variants in plant transcriptional regulation. Biochim. Biophys. Acta Gene Regul. Mech. 1860:123–30
    [Google Scholar]
  79. 79. 
    Jin C, Felsenfeld G. 2007. Nucleosome stability mediated by histone variants H3.3 and H2A.Z. Genes Dev 21:1519–29
    [Google Scholar]
  80. 80. 
    Juhasz S, Elbakry A, Mathes A, Lobrich M 2018. ATRX promotes DNA repair synthesis and sister chromatid exchange during homologous recombination. Mol. Cell 71:11–24.e7
    [Google Scholar]
  81. 81. 
    Jullien J, Astrand C, Szenker E, Garrett N, Almouzni G, Gurdon JB 2012. HIRA dependent H3.3 deposition is required for transcriptional reprogramming following nuclear transfer to Xenopus oocytes. Epigenet. Chromatin 5:17
    [Google Scholar]
  82. 82. 
    Kaneshiro KR, Rechtsteiner A, Strome S 2019. Sperm-inherited H3K27me3 impacts offspring transcription and development in C. elegans. Nat. Commun 10:1271
    [Google Scholar]
  83. 83. 
    Kireeva ML, Hancock B, Cremona GH, Walter W, Studitsky VM, Kashlev M 2005. Nature of the nucleosomal barrier to RNA polymerase II. Mol. Cell 18:97–108
    [Google Scholar]
  84. 84. 
    Kong Q, Banaszynski LA, Geng F, Zhang X, Zhang J et al. 2018. Histone variant H3.3-mediated chromatin remodeling is essential for paternal genome activation in mouse preimplantation embryos. J. Biol. Chem. 293:3829–38
    [Google Scholar]
  85. 85. 
    Kraushaar DC, Chen Z, Tang Q, Cui K, Zhang J, Zhao K 2018. The gene repressor complex NuRD interacts with the histone variant H3.3 at promoters of active genes. Genome Res 28:1646–55
    [Google Scholar]
  86. 86. 
    Kraushaar DC, Jin W, Maunakea A, Abraham B, Ha M, Zhao K 2013. Genome-wide incorporation dynamics reveal distinct categories of turnover for the histone variant H3.3. Genome Biol 14:R121
    [Google Scholar]
  87. 87. 
    Kujirai T, Horikoshi N, Sato K, Maehara K, Machida S et al. 2016. Structure and function of human histone H3.Y nucleosome. Nucleic Acids Res 44:6127–41 Erratum. 2017. Nucleic Acids Res. 45:3612
    [Google Scholar]
  88. 88. 
    Kujirai T, Horikoshi N, Xie Y, Taguchi H, Kurumizaka H 2017. Identification of the amino acid residues responsible for stable nucleosome formation by histone H3.Y. Nucleus 8:239–48
    [Google Scholar]
  89. 89. 
    Kursel LE, Malik HS. 2017. Recurrent gene duplication leads to diverse repertoires of centromeric histones in Drosophila species. Mol. Biol. Evol. 34:1445–62
    [Google Scholar]
  90. 90. 
    Law MJ, Lower KM, Voon HP, Hughes JR, Garrick D et al. 2010. ATR-X syndrome protein targets tandem repeats and influences allele-specific expression in a size-dependent manner. Cell 143:367–78
    [Google Scholar]
  91. 91. 
    Leatham-Jensen M, Uyehara CM, Strahl BD, Matera AG, Duronio RJ, McKay DJ 2019. Lysine 27 of replication-independent histone H3.3 is required for Polycomb target gene silencing but not for gene activation. PLOS Genet 15:e1007932
    [Google Scholar]
  92. 92. 
    Lee E, Iskow R, Yang L, Gokcumen O, Haseley P et al. 2012. Landscape of somatic retrotransposition in human cancers. Science 337:967–71
    [Google Scholar]
  93. 93. 
    Lee LR, Wengier DL, Bergmann DC 2019. Cell-type-specific transcriptome and histone modification dynamics during cellular reprogramming in the Arabidopsis stomatal lineage. PNAS 116:21914–24
    [Google Scholar]
  94. 94. 
    Lei B, Berger F. 2020. H2A Variants in Arabidopsis: versatile regulators of genome activity. Plant Commun 1:100015
    [Google Scholar]
  95. 95. 
    Lewis JD, Song Y, de Jong ME, Bagha SM, Ausio J 2003. A walk though vertebrate and invertebrate protamines. Chromosoma 111:473–82
    [Google Scholar]
  96. 96. 
    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]
  97. 97. 
    Lim CY, Reversade B, Knowles BB, Solter D 2013. Optimal histone H3 to linker histone H1 chromatin ratio is vital for mesodermal competence in Xenopus. . Development 140:853–60
    [Google Scholar]
  98. 98. 
    Lin CJ, Conti M, Ramalho-Santos M 2013. Histone variant H3.3 maintains a decondensed chromatin state essential for mouse preimplantation development. Development 140:3624–34
    [Google Scholar]
  99. 99. 
    Lin CJ, Koh FM, Wong P, Conti M, Ramalho-Santos M 2014. Hira-mediated H3.3 incorporation is required for DNA replication and ribosomal RNA transcription in the mouse zygote. Dev. Cell 30:268–79
    [Google Scholar]
  100. 100. 
    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]
  101. 101. 
    Long M, Sun X, Shi W, Yanru A, Leung STC et al. 2019. A novel histone H4 variant H4G regulates rDNA transcription in breast cancer. Nucleic Acids Res 47:8399–409
    [Google Scholar]
  102. 102. 
    Loppin B, Bonnefoy E, Anselme C, Laurencon A, Karr TL, Couble P 2005. The histone H3.3 chaperone HIRA is essential for chromatin assembly in the male pronucleus. Nature 437:1386–90
    [Google Scholar]
  103. 103. 
    Lovejoy CA, Li W, Reisenweber S, Thongthip S, Bruno J et al. 2012. Loss of ATRX, genome instability, and an altered DNA damage response are hallmarks of the alternative lengthening of telomeres pathway. PLOS Genet 8:e1002772
    [Google Scholar]
  104. 104. 
    Lowe BR, Maxham LA, Hamey JJ, Wilkins MR, Partridge JF 2019. Histone H3 mutations: an updated view of their role in chromatin deregulation and cancer. Cancers 11:660
    [Google Scholar]
  105. 105. 
    Lu L, Chen X, Qian S, Zhong X 2018. The plant-specific histone residue Phe41 is important for genome-wide H3.1 distribution. Nat. Commun. 9:630
    [Google Scholar]
  106. 106. 
    Luger K, Dechassa ML, Tremethick DJ 2012. New insights into nucleosome and chromatin structure: an ordered state or a disordered affair. ? Nat. Rev. Mol. Cell Biol. 13:436–47
    [Google Scholar]
  107. 107. 
    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]
  108. 108. 
    Maehara K, Harada A, Sato Y, Matsumoto M, Nakayama KI et al. 2015. Tissue-specific expression of histone H3 variants diversified after species separation. Epigenet. Chromatin 8:35
    [Google Scholar]
  109. 109. 
    Maheshwari S, Tan EH, West A, Franklin FC, Comai L, Chan SW 2015. Naturally occurring differences in CENH3 affect chromosome segregation in zygotic mitosis of hybrids. PLOS Genet 11:e1004970
    [Google Scholar]
  110. 110. 
    Malik HS, Henikoff S. 2003. Phylogenomics of the nucleosome. Nat. Struct. Biol. 10:882–91
    [Google Scholar]
  111. 111. 
    Malik HS, Henikoff S. 2009. Major evolutionary transitions in centromere complexity. Cell 138:1067–82
    [Google Scholar]
  112. 112. 
    Martire S, Gogate AA, Whitmill A, Tafessu A, Nguyen J et al. 2019. Phosphorylation of histone H3.3 at serine 31 promotes p300 activity and enhancer acetylation. Nat. Genet. 51:941–46
    [Google Scholar]
  113. 113. 
    Matsui T, Leung D, Miyashita H, Maksakova IA, Miyachi H et al. 2010. Proviral silencing in embryonic stem cells requires the histone methyltransferase ESET. Nature 464:927–31
    [Google Scholar]
  114. 114. 
    Maze I, Wenderski W, Noh KM, Bagot RC, Tzavaras N et al. 2015. Critical role of histone turnover in neuronal transcription and plasticity. Neuron 87:77–94
    [Google Scholar]
  115. 115. 
    McKay DJ, Klusza S, Penke TJ, Meers MP, Curry KP et al. 2015. Interrogating the function of metazoan histones using engineered gene clusters. Dev. Cell 32:373–86
    [Google Scholar]
  116. 116. 
    McKittrick E, Gafken PR, Ahmad K, Henikoff S 2004. Histone H3.3 is enriched in covalent modifications associated with active chromatin. PNAS 101:1525–30
    [Google Scholar]
  117. 117. 
    Mendiratta S, Gatto A, Almouzni G 2019. Histone supply: Multitiered regulation ensures chromatin dynamics throughout the cell cycle. J. Cell Biol. 218:39–54
    [Google Scholar]
  118. 118. 
    Milks KJ, Moree B, Straight AF 2009. Dissection of CENP-C-directed centromere and kinetochore assembly. Mol. Biol. Cell 20:4246–55
    [Google Scholar]
  119. 119. 
    Mito Y, Henikoff JG, Henikoff S 2007. Histone replacement marks the boundaries of cis-regulatory domains. Science 315:1408–11
    [Google Scholar]
  120. 120. 
    Montgomery SA, Tanizawa Y, Galik B, Wang N, Ito T et al. 2020. Chromatin organization in early land plants reveals an ancestral association between H3K27me3, transposons, and constitutive heterochromatin. Curr. Biol. 30:573–88.e7
    [Google Scholar]
  121. 121. 
    Moshkin YM, Armstrong JA, Maeda RK, Tamkun JW, Verrijzer P et al. 2002. Histone chaperone ASF1 cooperates with the Brahma chromatin-remodelling machinery. Genes Dev 16:2621–26
    [Google Scholar]
  122. 122. 
    Mousson F, Ochsenbein F, Mann C 2007. The histone chaperone Asf1 at the crossroads of chromatin and DNA checkpoint pathways. Chromosoma 116:79–93
    [Google Scholar]
  123. 123. 
    Muhire BM, Booker MA, Tolstorukov MY 2019. Non-neutral evolution of H3.3-encoding genes occurs without alterations in protein sequence. Sci. Rep. 9:8472
    [Google Scholar]
  124. 124. 
    Muller S, Almouzni G. 2014. A network of players in H3 histone variant deposition and maintenance at centromeres. Biochim. Biophys. Acta 1839:241–50
    [Google Scholar]
  125. 125. 
    Muller S, Almouzni G. 2017. Chromatin dynamics during the cell cycle at centromeres. Nat. Rev. Genet. 18:192–208
    [Google Scholar]
  126. 126. 
    Murphy PJ, Wu SF, James CR, Wike CL, Cairns BR 2018. Placeholder nucleosomes underlie germline-to-embryo DNA methylation reprogramming. Cell 172:993–1006.e13
    [Google Scholar]
  127. 127. 
    Nie X, Wang H, Li J, Holec S, Berger F 2014. The HIRA complex that deposits the histone H3.3 is conserved in Arabidopsis and facilitates transcriptional dynamics. Biol. Open 3:794–802
    [Google Scholar]
  128. 128. 
    Niikura Y, Kitagawa R, Kitagawa K 2016. The inheritance of centromere identity. Mol. Cell Oncol. 3:e1188226
    [Google Scholar]
  129. 129. 
    Ooi SL, Priess JR, Henikoff S 2006. Histone H3.3 variant dynamics in the germline of Caenorhabditis elegans. . PLOS Genet 2:e97
    [Google Scholar]
  130. 130. 
    Ors A, Papin C, Favier B, Roulland Y, Dalkara D et al. 2017. Histone H3.3 regulates mitotic progression in mouse embryonic fibroblasts. Biochem. Cell Biol. 95:491–99
    [Google Scholar]
  131. 131. 
    Orsi GA, Algazeery A, Meyer RE, Capri M, Sapey-Triomphe LM et al. 2013. Drosophila Yemanuclein and HIRA cooperate for de novo assembly of H3.3-containing nucleosomes in the male pronucleus. PLOS Genet 9:e1003285
    [Google Scholar]
  132. 132. 
    Otero S, Desvoyes B, Peiro R, Gutierrez C 2016. Histone H3 dynamics reveal domains with distinct proliferation potential in the Arabidopsis root. Plant Cell 28:1361–71
    [Google Scholar]
  133. 133. 
    Palmer DK, O'Day K, Margolis RL 1990. The centromere specific histone CENP-A is selectively retained in discrete foci in mammalian sperm nuclei. Chromosoma 100:32–36
    [Google Scholar]
  134. 134. 
    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 339:698–99
    [Google Scholar]
  135. 135. 
    Petricka JJ, Winter CM, Benfey PN 2012. Control of Arabidopsis root development. Annu. Rev. Plant Biol. 63:563–90
    [Google Scholar]
  136. 136. 
    Petryk N, Dalby M, Wenger A, Stromme CB, Strandsby A et al. 2018. MCM2 promotes symmetric inheritance of modified histones during DNA replication. Science 361:1389–92
    [Google Scholar]
  137. 137. 
    Piazzesi A, Papic D, Bertan F, Salomoni P, Nicotera P, Bano D 2016. Replication-independent histone variant H3.3 controls animal lifespan through the regulation of pro-longevity transcriptional programs. Cell Rep 17:987–96
    [Google Scholar]
  138. 138. 
    Postberg J, Forcob S, Chang WJ, Lipps HJ 2010. The evolutionary history of histone H3 suggests a deep eukaryotic root of chromatin modifying mechanisms. BMC Evol. Biol. 10:259
    [Google Scholar]
  139. 139. 
    Rai TS, Puri A, McBryan T, Hoffman J, Tang Y et al. 2011. Human CABIN1 is a functional member of the human HIRA/UBN1/ASF1a histone H3.3 chaperone complex. Mol. Cell. Biol. 31:4107–18
    [Google Scholar]
  140. 140. 
    Ramirez-Parra E, Gutierrez C. 2007. The many faces of chromatin assembly factor 1. Trends Plant Sci 12:570–76
    [Google Scholar]
  141. 141. 
    Rathke C, Baarends WM, Awe S, Renkawitz-Pohl R 2014. Chromatin dynamics during spermiogenesis. Biochim. Biophys. Acta 1839:155–68
    [Google Scholar]
  142. 142. 
    Ravi M, Chan SW. 2010. Haploid plants produced by centromere-mediated genome elimination. Nature 464:615–18
    [Google Scholar]
  143. 143. 
    Raychaudhuri N, Dubruille R, Orsi GA, Bagheri HC, Loppin B, Lehner CF 2012. Transgenerational propagation and quantitative maintenance of paternal centromeres depends on Cid/Cenp-A presence in Drosophila sperm. PLOS Biol 10:e1001434
    [Google Scholar]
  144. 144. 
    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]
  145. 145. 
    Ray-Gallet D, Ricketts MD, Sato Y, Gupta K, Boyarchuk E et al. 2018. Functional activity of the H3.3 histone chaperone complex HIRA requires trimerization of the HIRA subunit. Nat. Commun. 9:3103
    [Google Scholar]
  146. 146. 
    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]
  147. 147. 
    Resnick R, Wong CJ, Hamm DC, Bennett SR, Skene PJ et al. 2019. DUX4-induced histone variants H3.X and H3.Y mark DUX4 target genes for expression. Cell Rep 29:1812–20.e5
    [Google Scholar]
  148. 148. 
    Reveron-Gomez N, Gonzalez-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]
  149. 149. 
    Ricketts MD, Dasgupta N, Fan J, Han J, Gerace M et al. 2019. The HIRA histone chaperone complex subunit UBN1 harbors H3/H4- and DNA-binding activity. J. Biol. Chem. 294:9239–59
    [Google Scholar]
  150. 150. 
    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]
  151. 151. 
    Rowe HM, Jakobsson J, Mesnard D, Rougemont J, Reynard S et al. 2010. KAP1 controls endogenous retroviruses in embryonic stem cells. Nature 463:237–40
    [Google Scholar]
  152. 152. 
    Rudnizky S, Bavly A, Malik O, Pnueli L, Melamed P, Kaplan A 2016. H2A.Z controls the stability and mobility of nucleosomes to regulate expression of the LH genes. Nat. Commun. 7:12958
    [Google Scholar]
  153. 153. 
    Sadic D, Schmidt K, Groh S, Kondofersky I, Ellwart J et al. 2015. Atrx promotes heterochromatin formation at retrotransposons. EMBO Rep 16:836–50
    [Google Scholar]
  154. 154. 
    Sakai A, Schwartz BE, Goldstein S, Ahmad K 2009. Transcriptional and developmental functions of the H3.3 histone variant in Drosophila. . Curr. Biol 19:1816–20
    [Google Scholar]
  155. 155. 
    Santenard A, Ziegler-Birling C, Koch M, Tora L, Bannister AJ, Torres-Padilla ME 2010. Heterochromatin formation in the mouse embryo requires critical residues of the histone variant H3.3. Nat. Cell Biol. 12:853–62
    [Google Scholar]
  156. 156. 
    Sawatsubashi S, Murata T, Lim J, Fujiki R, Ito S et al. 2010. A histone chaperone, DEK, transcriptionally coactivates a nuclear receptor. Genes Dev 24:159–70
    [Google Scholar]
  157. 157. 
    Schenk R, Jenke A, Zilbauer M, Wirth S, Postberg J 2011. H3.5 is a novel hominid-specific histone H3 variant that is specifically expressed in the seminiferous tubules of human testes. Chromosoma 120:275–85
    [Google Scholar]
  158. 158. 
    Schlissel G, Rine J. 2019. The nucleosome core particle remembers its position through DNA replication and RNA transcription. PNAS 116:20605–11
    [Google Scholar]
  159. 159. 
    Schneiderman JI, Orsi GA, Hughes KT, Loppin B, Ahmad K 2012. Nucleosome-depleted chromatin gaps recruit assembly factors for the H3.3 histone variant. PNAS 109:4819721–26
    [Google Scholar]
  160. 160. 
    Schneiderman JI, Sakai A, Goldstein S, Ahmad K 2009. The XNP remodeler targets dynamic chromatin in Drosophila. . PNAS 106:3414472–77
    [Google Scholar]
  161. 161. 
    Schultz RM. 2002. The molecular foundations of the maternal to zygotic transition in the preimplantation embryo. Hum. Reprod. Update 8:323–31
    [Google Scholar]
  162. 162. 
    Schulz LL, Tyler JK. 2006. The histone chaperone ASF1 localizes to active DNA replication forks to mediate efficient DNA replication. FASEB J 20:488–90
    [Google Scholar]
  163. 163. 
    Sequeira-Mendes J, Araguez I, Peiro R, Mendez-Giraldez R, Zhang X et al. 2014. The functional topography of the Arabidopsis genome is organized in a reduced number of linear motifs of chromatin states. Plant Cell 26:2351–66
    [Google Scholar]
  164. 164. 
    Shaytan AK, Landsman D, Panchenko AR 2015. Nucleosome adaptability conferred by sequence and structural variations in histone H2A-H2B dimers. Curr. Opin. Struct. Biol. 32:48–57
    [Google Scholar]
  165. 165. 
    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]
  166. 166. 
    Shindo Y, Amodeo AA. 2019. Dynamics of free and chromatin-bound histone H3 during early embryogenesis. Curr. Biol. 29:359–66.e4
    [Google Scholar]
  167. 167. 
    Shiraishi K, Shindo A, Harada A, Kurumizaka H, Kimura H et al. 2018. Roles of histone H3.5 in human spermatogenesis and spermatogenic disorders. Andrology 6:158–65
    [Google Scholar]
  168. 168. 
    Shu H, Nakamura M, Siretskiy A, Borghi L, Moraes I et al. 2014. Arabidopsis replacement histone variant H3.3 occupies promoters of regulated genes. Genome Biol 15:R62
    [Google Scholar]
  169. 169. 
    Sims RJ 3rd, Reinberg D 2008. Is there a code embedded in proteins that is based on post-translational modifications. ? Nat. Rev. Mol. Cell Biol. 9:815–20
    [Google Scholar]
  170. 170. 
    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]
  171. 171. 
    Stroud H, Greenberg MV, Feng S, Bernatavichute YV, Jacobsen SE 2013. Comprehensive analysis of silencing mutants reveals complex regulation of the Arabidopsis methylome. Cell 152:352–64
    [Google Scholar]
  172. 172. 
    Stroud H, Hale CJ, Feng S, Caro E, Jacob Y et al. 2012. DNA methyltransferases are required to induce heterochromatic re-replication in Arabidopsis. PLOS Genet 8:e1002808
    [Google Scholar]
  173. 173. 
    Stroud H, Otero S, Desvoyes B, Ramirez-Parra E, Jacobsen SE, Gutierrez C 2012. Genome-wide analysis of histone H3.1 and H3.3 variants in Arabidopsis thaliana. . PNAS 109:5370–75
    [Google Scholar]
  174. 174. 
    Subramanian V, Fields PA, Boyer LA 2015. H2A.Z: a molecular rheostat for transcriptional control. F1000Prime Rep 7:01
    [Google Scholar]
  175. 175. 
    Szenker E, Lacoste N, Almouzni G 2012. A developmental requirement for HIRA-dependent H3.3 deposition revealed at gastrulation in Xenopus. . Cell Rep 1:730–40
    [Google Scholar]
  176. 176. 
    Tabuchi TM, Rechtsteiner A, Jeffers TE, Egelhofer TA, Murphy CT, Strome S 2018. Caenorhabditis elegans sperm carry a histone-based epigenetic memory of both spermatogenesis and oogenesis. Nat. Commun. 9:4310
    [Google Scholar]
  177. 177. 
    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]
  178. 178. 
    Taguchi H, Xie Y, Horikoshi N, Maehara K, Harada A et al. 2017. Crystal structure and characterization of novel human histone H3 variants, H3.6, H3.7, and H3.8. Biochemistry 56:2184–96
    [Google Scholar]
  179. 179. 
    Talbert PB, Ahmad K, Almouzni G, Ausio J, Berger F et al. 2012. A unified phylogeny-based nomenclature for histone variants. Epigenet. Chromatin 5:7
    [Google Scholar]
  180. 180. 
    Talbert PB, Henikoff S. 2017. Histone variants on the move: substrates for chromatin dynamics. Nat. Rev. Mol. Cell Biol. 18:115–26
    [Google Scholar]
  181. 181. 
    Tian Q, Wang XF, Xie SM, Yin Y, Zhou LQ 2020. H3.3 impedes zygotic transcriptional program activated by Dux. Biochem. Biophys. Res. Commun. 522:422–27
    [Google Scholar]
  182. 182. 
    Tie CH, Fernandes L, Conde L, Robbez-Masson L, Sumner RP et al. 2018. KAP1 regulates endogenous retroviruses in adult human cells and contributes to innate immune control. EMBO Rep 19:e45000
    [Google Scholar]
  183. 183. 
    Tran V, Lim C, Xie J, Chen X 2012. Asymmetric division of Drosophila male germline stem cell shows asymmetric histone distribution. Science 338:679–82
    [Google Scholar]
  184. 184. 
    Tvardovskiy A, Schwammle V, Kempf SJ, Rogowska-Wrzesinska A, Jensen ON 2017. Accumulation of histone variant H3.3 with age is associated with profound changes in the histone methylation landscape. Nucleic Acids Res 45:9272–89
    [Google Scholar]
  185. 185. 
    Udugama M, Sanij E, Voon HPJ, Son J, Hii L et al. 2018. Ribosomal DNA copy loss and repeat instability in ATRX-mutated cancers. PNAS 115:4737–42
    [Google Scholar]
  186. 186. 
    Ueda J, Harada A, Urahama T, Machida S, Maehara K et al. 2017. Testis-specific histone variant H3t gene is essential for entry into spermatogenesis. Cell Rep 18:593–600
    [Google Scholar]
  187. 187. 
    Urahama T, Harada A, Maehara K, Horikoshi N, Sato K et al. 2016. Histone H3.5 forms an unstable nucleosome and accumulates around transcription start sites in human testis. Epigenet. Chromatin 9:2
    [Google Scholar]
  188. 188. 
    van der Heijden GW, Derijck AA, Posfai E, Giele M, Pelczar P et al. 2007. Chromosome-wide nucleosome replacement and H3.3 incorporation during mammalian meiotic sex chromosome inactivation. Nat. Genet. 39:251–58
    [Google Scholar]
  189. 189. 
    Venkatesh S, Workman JL. 2015. Histone exchange, chromatin structure and the regulation of transcription. Nat. Rev. Mol. Cell Biol. 16:178–89
    [Google Scholar]
  190. 190. 
    Voon HP, Hughes JR, Rode C, De La Rosa-Velazquez 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]
  191. 191. 
    Waidmann S, Kusenda B, Mayerhofer J, Mechtler K, Jonak C 2014. A DEK domain-containing protein modulates chromatin structure and function in Arabidopsis. . Plant Cell 26:4328–44
    [Google Scholar]
  192. 192. 
    Wang H, Jiang D, Axelsson E, Lorkovic ZJ, Montgomery S et al. 2018. LHP1 interacts with ATRX through plant-specific domains at specific loci targeted by PRC2. Mol. Plant 11:1038–52
    [Google Scholar]
  193. 193. 
    Wang Y, Long H, Yu J, Dong L, Wassef M et al. 2018. Histone variants H2A.Z and H3.3 coordinately regulate PRC2-dependent H3K27me3 deposition and gene expression regulation in mES cells. BMC Biol 16:107
    [Google Scholar]
  194. 194. 
    Weber CM, Ramachandran S, Henikoff S 2014. Nucleosomes are context-specific, H2A.Z-modulated barriers to RNA polymerase. Mol. Cell 53:819–30
    [Google Scholar]
  195. 195. 
    Wiedemann SM, Mildner SN, Bonisch C, Israel L, Maiser A et al. 2010. Identification and characterization of two novel primate-specific histone H3 variants, H3.X and H3.Y. J. Cell Biol. 190:777–91
    [Google Scholar]
  196. 196. 
    Wilkins AS. 2010. The enemy within: an epigenetic role of retrotransposons in cancer initiation. Bioessays 32:856–65
    [Google Scholar]
  197. 197. 
    Witt O, Albig W, Doenecke D 1996. Testis-specific expression of a novel human H3 histone gene. Exp. Cell Res. 229:301–6
    [Google Scholar]
  198. 198. 
    Wollmann H, Holec S, Alden K, Clarke ND, Jacques PE, Berger F 2012. Dynamic deposition of histone variant H3.3 accompanies developmental remodeling of the Arabidopsis transcriptome. PLOS Genet 8:e1002658
    [Google Scholar]
  199. 199. 
    Wollmann H, Stroud H, Yelagandula R, Tarutani Y, Jiang D et al. 2017. The histone H3 variant H3.3 regulates gene body DNA methylation in Arabidopsis thaliana. . Genome Biol 18:94
    [Google Scholar]
  200. 200. 
    Wooten M, Ranjan R, Chen X 2020. Asymmetric histone inheritance in asymmetrically dividing stem cells. Trends Genet 36:30–43
    [Google Scholar]
  201. 201. 
    Wooten M, Snedeker J, Nizami ZF, Yang X, Ranjan R et al. 2019. Asymmetric histone inheritance via strand-specific incorporation and biased replication fork movement. Nat. Struct. Mol. Biol. 26:732–43
    [Google Scholar]
  202. 202. 
    Wu SF, Zhang H, Cairns BR 2011. Genes for embryo development are packaged in blocks of multivalent chromatin in zebrafish sperm. Genome Res 21:578–89
    [Google Scholar]
  203. 203. 
    Xia W, Jiao J. 2017. Histone variant H3.3 orchestrates neural stem cell differentiation in the developing brain. Cell Death Differ 24:1548–63
    [Google Scholar]
  204. 204. 
    Xie J, Wooten M, Tran V, Chen BC, Pozmanter C et al. 2015. Histone H3 threonine phosphorylation regulates asymmetric histone inheritance in the Drosophila male germline. Cell 163:920–33
    [Google Scholar]
  205. 205. 
    Xiong C, Wen Z, Yu J, Chen J, Liu CP et al. 2018. UBN1/2 of HIRA complex is responsible for recognition and deposition of H3.3 at cis-regulatory elements of genes in mouse ES cells. BMC Biol 16:110
    [Google Scholar]
  206. 206. 
    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]
  207. 207. 
    Yan A, Borg M, Berger F, Chen Z 2020. The atypical histone variant H3.15 promotes callus formation in Arabidopsis thaliana. . Development 147:dev184895
    [Google Scholar]
  208. 208. 
    Yoshida K, Muratani M, Araki H, Miura F, Suzuki T et al. 2018. Mapping of histone-binding sites in histone replacement-completed spermatozoa. Nat. Commun. 9:3885
    [Google Scholar]
  209. 209. 
    Yu R, Wang X, Moazed D 2018. Epigenetic inheritance mediated by coupling of RNAi and histone H3K9 methylation. Nature 558:615–19
    [Google Scholar]
  210. 210. 
    Yuan W, Wu T, Fu H, Dai C, Wu H et al. 2012. Dense chromatin activates Polycomb repressive complex 2 to regulate H3 lysine 27 methylation. Science 337:971–75
    [Google Scholar]
  211. 211. 
    Zhang W, Zhang X, Xue Z, Li Y, Ma Q et al. 2019. Probing the function of metazoan histones with a systematic library of H3 and H4 mutants. Dev. Cell 48:406–19.e5
    [Google Scholar]
  212. 212. 
    Zhao P, Zhou X, Shen K, Liu Z, Cheng T et al. 2019. Two-step maternal-to-zygotic transition with two-phase parental genome contributions. Dev. Cell 49:882–93.e5
    [Google Scholar]
  213. 213. 
    Zhao ZK, Li W, Wang MY, Zhou L, Wang JL, Wang YF 2011. The role of HIRA and maternal histones in sperm nucleus decondensation in the gibel carp and color crucian carp. Mol. Reprod. Dev. 78:139–47
    [Google Scholar]
  214. 214. 
    Zheng H, Huang B, Zhang B, Xiang Y, Du Z et al. 2016. Resetting epigenetic memory by reprogramming of histone modifications in mammals. Mol. Cell 63:1066–79
    [Google Scholar]
  215. 215. 
    Zhu R, Iwabuchi M, Ohsumi K 2017. The WD40 domain of HIRA is essential for RI-nucleosome assembly in Xenopus egg extracts. Cell Struct. Funct. 42:37–48
    [Google Scholar]
  216. 216. 
    Zilberman D, Coleman-Derr D, Ballinger T, Henikoff S 2008. Histone H2A.Z and DNA methylation are mutually antagonistic chromatin marks. Nature 456:125–29
    [Google Scholar]
  217. 217. 
    Zink LM, Delbarre E, Eberl HC, Keilhauer EC, Bonisch C et al. 2017. H3.Y discriminates between HIRA and DAXX chaperone complexes and reveals unexpected insights into human DAXX-H3.3-H4 binding and deposition requirements. Nucleic Acids Res 45:5691–706
    [Google Scholar]
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