1932

Abstract

The functional organization of eukaryotic DNA into chromatin uses histones as components of its building block, the nucleosome. Histone chaperones, which are proteins that escort histones throughout their cellular life, are key actors in all facets of histone metabolism; they regulate the supply and dynamics of histones at chromatin for its assembly and disassembly. Histone chaperones can also participate in the distribution of histone variants, thereby defining distinct chromatin landscapes of importance for genome function, stability, and cell identity. Here, we discuss our current knowledge of the known histone chaperones and their histone partners, focusing on histone H3 and its variants. We then place them into an escort network that distributes these histones in various deposition pathways. Through their distinct interfaces, we show how they affect dynamics during DNA replication, DNA damage, and transcription, and how they maintain genome integrity. Finally, we discuss the importance of histone chaperones during development and describe how misregulation of the histone flow can link to disease.

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2014-06-02
2024-06-14
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Literature Cited

  1. Kornberg RD.1.  1974. Chromatin structure: a repeating unit of histones and DNA. Science 184:868–71 [Google Scholar]
  2. Oudet P, Gross-Bellard M, Chambon P. 2.  1975. Electron microscopic and biochemical evidence that chromatin structure is a repeating unit. Cell 4:281–300 [Google Scholar]
  3. McGhee JD, Felsenfeld G. 3.  1980. Nucleosome structure. Annu. Rev. Biochem. 49:1115–56 [Google Scholar]
  4. Luger K, Mäder AW, Richmond RK, Sargent DF, Richmond TJ. 4.  1997. Crystal structure of the nucleosome core particle at 2.8 Å resolution. Nature 389:251–60 [Google Scholar]
  5. Kim UJ, Han M, Kayne P, Grunstein M. 5.  1988. Effects of histone H4 depletion on the cell cycle and transcription of Saccharomyces cerevisiae. EMBO J. 7:2211–19 [Google Scholar]
  6. Prado F, Aguilera A. 6.  2005. Partial depletion of histone H4 increases homologous recombination–mediated genetic instability. Mol. Cell. Biol. 25:1526–36 [Google Scholar]
  7. Meeks-Wagner D, Hartwell LH. 7.  1986. Normal stoichiometry of histone dimer sets is necessary for high fidelity of mitotic chromosome transmission. Cell 44:43–52 [Google Scholar]
  8. Groth A, Ray Gallet D, Quivy J-P, Lukas J, Bartek J, Almouzni G. 8.  2005. Human Asf1 regulates the flow of S phase histones during replicational stress. Mol. Cell 17:301–11 [Google Scholar]
  9. Laskey RA, Honda BM, Mills AD, Finch JT. 9.  1978. Nucleosomes are assembled by an acidic protein which binds histones and transfers them to DNA. Nature 275:416–20 [Google Scholar]
  10. Ellis RJ.10.  1990. The molecular chaperone concept. Semin. Cell Biol. 1:1–9 [Google Scholar]
  11. Felsenfeld G.11.  1978. Chromatin. Nature 271:115–22 [Google Scholar]
  12. Nelson T, Wiegand R, Brutlag D. 12.  1981. Ribonucleic acid and other polyanions facilitate chromatin assembly in vitro. Biochemistry 20:2594–601 [Google Scholar]
  13. Stein A.13.  1989. Reconstitution of chromatin from purified components. Methods Enzymol. 170:585–603 [Google Scholar]
  14. Stein A, Whitlock JP Jr, Bina M. 14.  1979. Acidic polypeptides can assemble both histones and chromatin in vitro at physiological ionic strength. Proc. Natl. Acad. Sci. USA 76:5000–4 [Google Scholar]
  15. Woodland HR, Adamson ED. 15.  1977. The synthesis and storage of histones during the oogenesis of Xenopus laevis. Dev. Biol. 57:118–35 [Google Scholar]
  16. Laskey RA, Mills AD, Morris NR. 16.  1977. Assembly of SV40 chromatin in a cell-free system from Xenopus eggs. Cell 10:237–43 [Google Scholar]
  17. Nelson T, Hsieh TS, Brutlag D. 17.  1979. Extracts of Drosophila embryos mediate chromatin assembly in vitro. Proc. Natl. Acad. Sci. USA 76:5510–14 [Google Scholar]
  18. Adamson ED, Woodland HR. 18.  1974. Histone synthesis in early amphibian development: histone and DNA syntheses are not co-ordinated. J. Mol. Biol. 88:263–85 [Google Scholar]
  19. Earnshaw WC, Honda BM, Laskey RA, Thomas JO. 19.  1980. Assembly of nucleosomes: the reaction involving X. laevis nucleoplasmin. Cell 21:373–83 [Google Scholar]
  20. Kleinschmidt JA, Franke WW. 20.  1982. Soluble acidic complexes containing histones H3 and H4 in nuclei of Xenopus laevis oocytes. Cell 29:799–809 [Google Scholar]
  21. Kleinschmidt JA, Fortkamp E, Krohne G, Zentgraf H, Franke WW. 21.  1985. Co-existence of two different types of soluble histone complexes in nuclei of Xenopus laevis oocytes. J. Biol. Chem. 260:1166–76 [Google Scholar]
  22. Kaufman DG, Almouzni G. 22.  2006. Chromatin assembly. DNA Replication and Human Disease ML DePamphilis 121–40 New York: Cold Spring Harb. Lab [Google Scholar]
  23. Gaume X, Monier K, Argoul F, Mongelard F, Bouvet P. 23.  2011. In vivo study of the histone chaperone activity of nucleolin by FRAP. Biochem. Res. Int. 12:1–15 [Google Scholar]
  24. Cong R, Das S, Douet J, Wong J, Buschbeck M. 24.  et al. 2013. macroH2A1 histone variant represses rDNA transcription. Nucleic Acids Res. 42:181–92 [Google Scholar]
  25. Ratnakumar K, Duarte LF, LeRoy G, Hasson D, Smeets D. 25.  et al. 2012. ATRX-mediated chromatin association of histone variant macroH2A1 regulates α-globin expression. Genes Dev. 26:433–38 [Google Scholar]
  26. Angelov D, Bondarenko VA, Almagro S, Menoni H, Mongélard F. 26.  et al. 2006. Nucleolin is a histone chaperone with FACT-like activity and assists remodeling of nucleosomes. EMBO J. 25:1669–79 [Google Scholar]
  27. Stillman B, Gluzman Y. 27.  1985. Replication and supercoiling of simian virus 40 DNA in cell extracts from human cells. Mol. Cell. Biol. 5:2051–60 [Google Scholar]
  28. Stillman B.28.  1986. Chromatin assembly during SV40 DNA replication in vitro. Cell 45:555–65 [Google Scholar]
  29. Smith S, Stillman B. 29.  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]
  30. Quivy J-P, Grandi P, Almouzni G. 30.  2001. Dimerization of the largest subunit of chromatin assembly factor 1: importance in vitro and during Xenopus early development. EMBO J. 20:2015–27 [Google Scholar]
  31. De Koning L, Corpet A, Haber JE, Almouzni G. 31.  2007. Histone chaperones: an escort network regulating histone traffic. Nat. Struct. Mol. Biol. 14:997–1007 [Google Scholar]
  32. Dilworth SM, Black SJ, Laskey RA. 32.  1987. Two complexes that contain histones are required for nucleosome assembly in vitro: role of nucleoplasmin and N1 in Xenopus egg extracts. Cell 51:1009–18 [Google Scholar]
  33. Almouzni G, Mechali M. 33.  1988. Xenopus egg extracts: a model system for chromatin replication. Biochim. Biophys. Acta 951:443–50 [Google Scholar]
  34. Almouzni G, Mechali M. 34.  1988. Assembly of spaced chromatin involvement of ATP and DNA topoisomerase activity. EMBO J. 7:4355–65 [Google Scholar]
  35. Almouzni G, Mechali M. 35.  1988. Assembly of spaced chromatin promoted by DNA synthesis in extracts from Xenopus eggs. EMBO J. 7:665–72 [Google Scholar]
  36. Ray Gallet D, Almouzni G. 36.  2004. DNA synthesis–dependent and –independent chromatin assembly pathways in Xenopus egg extracts. Methods Enzymol. 375:117–31 [Google Scholar]
  37. Ray Gallet D, Quivy J-P, Scamps C, Martini EM-D, Lipinski M, Almouzni G. 37.  2002. HIRA is critical for a nucleosome assembly pathway independent of DNA synthesis. Mol. Cell 9:1091–100 [Google Scholar]
  38. Sharp JA, Fouts ET, Krawitz DC, Kaufman PD. 38.  2001. Yeast histone deposition protein Asf1p requires Hir proteins and PCNA for heterochromatic silencing. Curr. Biol. 11:463–73 [Google Scholar]
  39. Mello JA, Silljé HH, Roche DM, Kirschner DB, Nigg EA, Almouzni G. 39.  2002. Human Asf1 and CAF-1 interact and synergize in a repair-coupled nucleosome assembly pathway. EMBO Rep. 3:329–34 [Google Scholar]
  40. Polo SE, Roche D, Almouzni G. 40.  2006. New histone incorporation marks sites of UV repair in human cells. Cell 127:481–93 [Google Scholar]
  41. Szenker E, Ray Gallet D, Almouzni G. 41.  2011. The double face of the histone variant H3.3. Cell Res. 21:421–34 [Google Scholar]
  42. Filipescu D, Szenker E, Almouzni G. 42.  2013. Developmental roles of histone H3 variants and their chaperones. Trends Genet. 29:630–40 [Google Scholar]
  43. Boyarchuk E, Montes de Oca R, Almouzni G. 43.  2011. Cell cycle dynamics of histone variants at the centromere, a model for chromosomal landmarks. Curr. Opin. Cell Biol. 23:266–76 [Google Scholar]
  44. Vardabasso C, Hasson D, Ratnakumar K, Chung CY, Duarte LF, Bernstein E. 44.  2013. Histone variants: emerging players in cancer biology. Cell. Mol. Life Sci. 71:379–404 [Google Scholar]
  45. Tagami H, Ray Gallet D, Almouzni G, Nakatani Y. 45.  2004. Histone H3.1 and H3.3 complexes mediate nucleosome assembly pathways dependent or independent of DNA synthesis. Cell 116:51–61 [Google Scholar]
  46. Loyola A, Bonaldi T, Roche D, Imhof A, Almouzni G. 46.  2006. PTMs on H3 variants before chromatin assembly potentiate their final epigenetic state. Mol. Cell 24:309–16 [Google Scholar]
  47. Lewis PW, Elsässer SJ, Noh K-M, Stadler SC, Allis CD. 47.  2010. Daxx is an H3.3-specific histone chaperone and cooperates with ATRX in replication-independent chromatin assembly at telomeres. Proc. Natl. Acad. Sci. USA 107:14075–80 [Google Scholar]
  48. Dunleavy EM, Roche D, Tagami H, Lacoste N, Ray Gallet D. 48.  et al. 2009. HJURP is a cell-cycle-dependent maintenance and deposition factor of CENP-A at centromeres. Cell 137:485–97 [Google Scholar]
  49. Foltz DR, Jansen LE, Bailey AO, Yates JR 3rd, Bassett EA. 49.  et al. 2009. Centromere-specific assembly of CENP-A nucleosomes is mediated by HJURP. Cell 137:472–84 [Google Scholar]
  50. Richardson RT, Batova IN, Widgren EE, Zheng LX, Whitfield M. 50.  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]
  51. Campos EI, Fillingham J, Li G, Zheng H, Voigt P. 51.  et al. 2010. The program for processing newly synthesized histones H3.1 and H4. Nat. Struct. Mol. Biol. 17:1343–51 [Google Scholar]
  52. Cook AJL, Gurard-Levin ZA, Vassias I, Almouzni G. 52.  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]
  53. Shintomi K, Iwabuchi M, Saeki H, Ura K, Kishimoto T, Ohsumi K. 53.  2005. Nucleosome assembly protein 1 is a linker histone chaperone in Xenopus eggs. Proc. Natl. Acad. Sci. USA 102:8210–15 [Google Scholar]
  54. Keppler A, Gendreizig S, Gronemeyer T, Pick H, Vogel H, Johnsson K. 54.  2003. A general method for the covalent labeling of fusion proteins with small molecules in vivo. Nat. Biotechnol. 21:86–89 [Google Scholar]
  55. Jansen LE, Black BE, Foltz DR, Cleveland DW. 55.  2007. Propagation of centromeric chromatin requires exit from mitosis. J. Cell Biol. 176:795–805 [Google Scholar]
  56. Mousson F, Lautrette A, Thuret J-Y, Agez M, Courbeyrette R. 56.  et al. 2005. Structural basis for the interaction of Asf1 with histone H3 and its functional implications. Proc. Natl. Acad. Sci. USA 102:5975–80 [Google Scholar]
  57. Park Y-J, Luger K. 57.  2006. The structure of nucleosome assembly protein 1. Proc. Natl. Acad. Sci. USA 103:1248–53 [Google Scholar]
  58. Belotserkovskaya R, Oh S, Bondarenko VA, Orphanides G, Studitsky VM, Reinberg D. 58.  2003. FACT facilitates transcription-dependent nucleosome alteration. Science 301:1090–93 [Google Scholar]
  59. Regnard C, Desbruyères E, Huet JC, Beauvallet C, Pernollet JC, Eddé B. 59.  2000. Polyglutamylation of nucleosome assembly proteins. J. Biol. Chem. 275:15969–76 [Google Scholar]
  60. Dutta S, Akey IV, Dingwall C, Hartman KL, Laue T. 60.  et al. 2001. The crystal structure of nucleoplasmin core: implications for histone binding and nucleosome assembly. Mol. Cell 8:841–53 [Google Scholar]
  61. Umehara T, Chimura T, Ichikawa N, Horikoshi M. 61.  2002. Polyanionic stretch-deleted histone chaperone cia1/Asf1p is functional both in vivo and in vitro. Genes Cells Devoted Mol. Cell. Mech. 7:59–73 [Google Scholar]
  62. Muto S, Senda M, Akai Y, Sato L, Suzuki T. 62.  et al. 2007. Relationship between the structure of SET/TAF-Iβ/INHAT and its histone chaperone activity. Proc. Natl. Acad. Sci. USA 104:4285–90 [Google Scholar]
  63. Namboodiri VM, Dutta S, Akey IV, Head JF, Akey CW. 63.  2003. The crystal structure of Drosophila NLP core provides insight into pentamer formation and histone binding. Structure 11:175–86 [Google Scholar]
  64. Park YJ, McBryant SJ, Luger K. 64.  2008. A β-hairpin comprising the nuclear localization sequence sustains the self-associated states of nucleosome assembly protein 1. J. Mol. Biol. 375:1076–85 [Google Scholar]
  65. Daganzo SM, Erzberger JP, Lam WM, Skordalakes E, Zhang R. 65.  et al. 2003. Structure and function of the conserved core of histone deposition protein Asf1. Curr. Biol. 13:2148–58 [Google Scholar]
  66. Kaufman PD, Kobayashi R, Kessler N, Stillman B. 66.  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]
  67. Verreault A, Kaufman PD, Kobayashi R, Stillman B. 67.  1996. Nucleosome assembly by a complex of CAF-1 and acetylated histones H3/H4. Cell 87:95–104 [Google Scholar]
  68. Natsume R, Eitoku M, Akai Y, Sano N, Horikoshi M, Senda T. 68.  2007. Structure and function of the histone chaperone CIA/ASF1 complexed with histones H3 and H4. Nature 446:338–41 [Google Scholar]
  69. Corpet A, Almouzni G. 69.  2009. Making copies of chromatin: the challenge of nucleosomal organization and epigenetic information. Trends Cell Biol. 19:29–41 [Google Scholar]
  70. English CM, Adkins MW, Carson JJ, Churchill ME, Tyler JK. 70.  2006. Structural basis for the histone chaperone activity of Asf1. Cell 127:495–508 [Google Scholar]
  71. Antczak AJ, Tsubota T, Kaufman PD, Berger JM. 71.  2006. Structure of the yeast histone H3–ASF1 interaction: implications for chaperone mechanism, species-specific interactions, and epigenetics. BMC Struct. Biol. 6:26 [Google Scholar]
  72. Malay AD, Umehara T, Matsubara-Malay K, Padmanabhan B, Yokoyama S. 72.  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]
  73. Abascal F, Corpet A, Gurard-Levin ZA, Juan D, Ochsenbein F. 73.  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]
  74. Elsässer SJ, Huang H, Lewis PW, Chin JW, Allis CD, Patel DJ. 74.  2012. DAXX envelops a histone H3.3–H4 dimer for H3.3-specific recognition. Nature 491:560–65 [Google Scholar]
  75. Hu H, Liu Y, Wang M, Fang J, Huang H. 75.  et al. 2011. Structure of a CENP-A-histone H4 heterodimer in complex with chaperone HJURP. Genes Dev. 25:901–6 [Google Scholar]
  76. Zhou Z, Feng H, Zhou B-R, Ghirlando R, Hu K. 76.  et al. 2011. Structural basis for recognition of centromere histone variant CenH3 by the chaperone Scm3. Nature 472:234–37 [Google Scholar]
  77. Bowman A, Ward R, Wiechens N, Singh V, El-Mkami H. 77.  et al. 2011. The histone chaperones Nap1 and Vps75 bind histones H3 and H4 in a tetrameric conformation. Mol. Cell 41:398–408 [Google Scholar]
  78. Lacoste N, Woolfe A, Tachiwana H, Villar Garea A, Barth T. 78.  et al. 2014. Mislocalization of the centromere histone variant CenH3/CENP-A in human cells depends on the chaperone DAXX. Mol. Cell 53:631–44 [Google Scholar]
  79. Hondele M, Stuwe T, Hassler M, Halbach F, Bowman A. 79.  et al. 2013. Structural basis of histone H2A–H2B recognition by the essential chaperone FACT. Nature 499:111–14 [Google Scholar]
  80. Hondele M, Ladurner AG. 80.  2011. The chaperone-histone partnership: for the greater good of histone traffic and chromatin plasticity. Curr. Opin. Struct. Biol. 21:698–708 [Google Scholar]
  81. Keck KM, Pemberton LF. 81.  2012. Histone chaperones link histone nuclear import and chromatin assembly. Biochim. Biophys. Acta 1819:277–89 [Google Scholar]
  82. Burgess RJ, Zhang Z. 82.  2013. Histone chaperones in nucleosome assembly and human disease. Nat. Struct. Mol. Biol. 20:14–22 [Google Scholar]
  83. Eitoku M, Sato L, Senda T, Horikoshi M. 83.  2008. Histone chaperones: 30 years from isolation to elucidation of the mechanisms of nucleosome assembly and disassembly. Cell. Mol. Life Sci. 65:414–44 [Google Scholar]
  84. Alvarez F, Muñoz F, Schilcher P, Imhof A, Almouzni G, Loyola A. 84.  2011. Sequential establishment of marks on soluble histones H3 and H4. J. Biol. Chem. 286:17714–21 [Google Scholar]
  85. Mosammaparast N, Ewart CS, Pemberton LF. 85.  2002. A role for nucleosome assembly protein 1 in the nuclear transport of histones H2A and H2B. EMBO J. 21:6527–38 [Google Scholar]
  86. Welch JE, Zimmerman LJ, Joseph DR, O'Rand MG. 86.  1990. Characterization of a sperm-specific nuclear autoantigenic protein. I. Complete sequence and homology with the Xenopus protein, N1/N2. Biol. Reprod. 43:559–68 [Google Scholar]
  87. Alekseev OM, Bencic DC, Richardson RT, Widgren EE, O'Rand MG. 87.  2003. Overexpression of the Linker histone-binding protein tNASP affects progression through the cell cycle. J. Biol. Chem. 278:8846–52 [Google Scholar]
  88. Alekseev OM, Richardson RT, Pope MR, O'Rand MG. 88.  2005. Mass spectrometry identification of NASP binding partners in HeLa cells. Proteins 61:1–5 [Google Scholar]
  89. Finn RM, Browne K, Hodgson KC, Ausió J. 89.  2008. sNASP, a histone H1–specific eukaryotic chaperone dimer that facilitates chromatin assembly. Biophys. J. 95:1314–25 [Google Scholar]
  90. Wang H, Walsh STR, Parthun MR. 90.  2008. Expanded binding specificity of the human histone chaperone NASP. Nucleic Acids Res. 36:5763–72 [Google Scholar]
  91. Osakabe A, Tachiwana H, Matsunaga T, Shiga T, Nozawa RS. 91.  et al. 2010. Nucleosome formation activity of human somatic nuclear autoantigenic sperm protein (sNASP). J. Biol. Chem. 285:11913–21 [Google Scholar]
  92. Dunleavy EM, Pidoux AL, Monet M, Bonilla C, Richardson W. 92.  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]
  93. Ai X, Parthun MR. 93.  2004. The nuclear Hat1p/Hat2p complex: a molecular link between type B histone acetyltransferases and chromatin assembly. Mol. Cell 14:195–205 [Google Scholar]
  94. Gunjan A, Verreault A. 94.  2003. A Rad53 kinase–dependent surveillance mechanism that regulates histone protein levels in S. cerevisiae. Cell 115:537–49 [Google Scholar]
  95. Singh RK, Kabbaj MH, Paik J, Gunjan A. 95.  2009. Histone levels are regulated by phosphorylation and ubiquitylation-dependent proteolysis. Nat. Cell Biol. 11:925–33 [Google Scholar]
  96. Le S, Davis C, Konopka JB, Sternglanz R. 96.  1997. Two new S-phase-specific genes from Saccharomyces cerevisiae. Yeast 13:1029–42 [Google Scholar]
  97. Tyler JK, Adams CR, Chen SR, Kobayashi R, Kamakaka RT, Kadonaga JT. 97.  1999. The RCAF complex mediates chromatin assembly during DNA replication and repair. Nature 402:555–60 [Google Scholar]
  98. Munakata T, Adachi N, Yokoyama N, Kuzuhara T, Horikoshi M. 98.  2000. A human homologue of yeast anti-silencing factor has histone chaperone activity. Genes Cells Devoted Mol. Cell. Mech. 5:221–33 [Google Scholar]
  99. Umehara TT, Horikoshi MM. 99.  2003. Transcription initiation factor IID–interactive histone chaperone CIA-II implicated in mammalian spermatogenesis. J. Biol. Chem. 278:35660–67 [Google Scholar]
  100. Corpet A, De Koning L, Toedling J, Savignoni A, Berger F. 100.  et al. 2011. Asf1b, the necessary Asf1 isoform for proliferation, is predictive of outcome in breast cancer. EMBO J. 30:480–93 [Google Scholar]
  101. Tang Y, Poustovoitov MV, Zhao K, Garfinkel M, Canutescu A. 101.  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]
  102. Tamburini BA, Carson JJ, Adkins MW, Tyler JK. 102.  2005. Functional conservation and specialization among eukaryotic anti-silencing function 1 histone chaperones. Eukaryot. Cell 4:1583–90 [Google Scholar]
  103. Green EM, Antczak AJ, Bailey AO, Franco AA, Wu KJ. 103.  et al. 2005. Replication-independent histone deposition by the HIR complex and Asf1. Curr. Biol. 15:2044–49 [Google Scholar]
  104. Groth A, Corpet A, Cook AJ, Roche D, Bartek J. 104.  et al. 2007. Regulation of replication fork progression through histone supply and demand. Science 318:1928–31 [Google Scholar]
  105. Jasencakova Z, Scharf AN, Ask K, Corpet A, Imhof A. 105.  et al. 2010. Replication stress interferes with histone recycling and predeposition marking of new histones. Mol. Cell 37:736–43 [Google Scholar]
  106. Gaillard PH, Martini EM, Kaufman PD, Stillman B, Moustacchi E, Almouzni G. 106.  1996. Chromatin assembly coupled to DNA repair: a new role for chromatin assembly factor I. Cell 86:887–96 [Google Scholar]
  107. Moggs JG, Grandi P, Quivy J-P, Jónsson ZO, Hübscher U. 107.  et al. 2000. A CAF-1–PCNA–mediated chromatin assembly pathway triggered by sensing DNA damage. Mol. Cell. Biol. 20:1206–18 [Google Scholar]
  108. Shibahara K, Stillman B. 108.  1999. Replication-dependent marking of DNA by PCNA facilitates CAF-1-coupled inheritance of chromatin. Cell 96:575–85 [Google Scholar]
  109. Martini E, Roche DM, Marheineke K, Verreault A, Almouzni G. 109.  1998. Recruitment of phosphorylated chromatin assembly factor 1 to chromatin after UV irradiation of human cells. J. Cell Biol. 143:563–75 [Google Scholar]
  110. Gérard A, Koundrioukoff S, Ramillon V, Sergère J-C, Mailand N. 110.  et al. 2006. The replication kinase Cdc7–Dbf4 promotes the interaction of the p150 subunit of chromatin assembly factor 1 with proliferating cell nuclear antigen. EMBO Rep. 7:817–23 [Google Scholar]
  111. Keller C, Krude T. 111.  2000. Requirement of cyclin/Cdk2 and protein phosphatase 1 activity for chromatin assembly factor 1–dependent chromatin assembly during DNA synthesis. J. Biol. Chem. 275:35512–21 [Google Scholar]
  112. Ray Gallet D, Woolfe A, Vassias I, Pellentz C, Lacoste N. 112.  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]
  113. Quivy J-P, Gerard A, Cook AJ, Roche D, Almouzni G. 113.  2008. The HP1-p150/CAF-1 interaction is required for pericentric heterochromatin replication and S-phase progression in mouse cells. Nat. Struct. Mol. Biol. 15:972–79 [Google Scholar]
  114. Winkler DD, Zhou H, Dar MA, Zhang Z, Luger K. 114.  2012. Yeast CAF-1 assembles histone (H3–H4)2 tetramers prior to DNA deposition. Nucleic Acids Res. 40:10139–49 [Google Scholar]
  115. Kamakaka RT, Bulger M, Kaufman PD, Stillman B, Kadonaga JT. 115.  1996. Postreplicative chromatin assembly by Drosophila and human chromatin assembly factor 1. Mol. Cell. Biol. 16:810–17 [Google Scholar]
  116. Tyler JK, Bulger M, Kamakaka RT, Kobayashi R, Kadonaga JT. 116.  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]
  117. Tyler JK, Collins KA, Prasad-Sinha J, Amiott E, Bulger M. 117.  et al. 2001. Interaction between the Drosophila CAF-1 and ASF1 chromatin assembly factors. Mol. Cell. Biol. 21:6574–84 [Google Scholar]
  118. Kaya H, Shibahara KI, Taoka KI, Iwabuchi M, Stillman B, Araki T. 118.  2001. FASCIATA genes for chromatin assembly factor 1 in Arabidopsis maintain the cellular organization of apical meristems. Cell 104:131–42 [Google Scholar]
  119. Enomoto S, Berman J. 119.  1998. Chromatin assembly factor I contributes to the maintenance, but not the re-establishment, of silencing at the yeast silent mating loci. Genes Dev. 12:219–32 [Google Scholar]
  120. Kaufman PD, Kobayashi R, Stillman B. 120.  1997. Ultraviolet radiation sensitivity and reduction of telomeric silencing in Saccharomyces cerevisiae cells lacking chromatin assembly factor I. Genes Dev. 11:345–57 [Google Scholar]
  121. Prochasson P, Florens L, Swanson SK, Washburn MP, Workman JL. 121.  2005. The HIR corepressor complex binds to nucleosomes generating a distinct protein/DNA complex resistant to remodeling by SWI/SNF. Genes Dev. 19:2534–39 [Google Scholar]
  122. Sherwood PW, Tsang SV, Osley MA. 122.  1993. Characterization of HIR1 and HIR2, two genes required for regulation of histone gene transcription in Saccharomyces cerevisiae. Mol. Cell. Biol. 13:28–38 [Google Scholar]
  123. Sutton A, Bucaria J, Osley MA, Sternglanz R. 123.  2001. Yeast ASF1 protein is required for cell cycle regulation of histone gene transcription. Genetics 158:587–96 [Google Scholar]
  124. Xu H, Kim UJ, Schuster T, Grunstein M. 124.  1992. Identification of a new set of cell cycle–regulatory genes that regulate S-phase transcription of histone genes in Saccharomyces cerevisiae. Mol. Cell. Biol. 12:5249–59 [Google Scholar]
  125. Banumathy G, Somaiah N, Zhang R, Tang Y, Hoffmann J. 125.  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]
  126. Balaji S, Iyer LM, Aravind L. 126.  2009. HPC2 and ubinuclein define a novel family of histone chaperones conserved throughout eukaryotes. Mol. Biosyst. 5:269–75 [Google Scholar]
  127. Rai TS, Puri A, McBryan T, Hoffman J, Tang Y. 127.  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]
  128. Park PJ.128.  2009. ChIP-seq: advantages and challenges of a maturing technology. Nat. Rev. Genet. 10:669–80 [Google Scholar]
  129. Goldberg AD, Banaszynski LA, Noh K-M, Lewis PW, Elsässer SJ. 129.  et al. 2010. Distinct factors control histone variant H3.3 localization at specific genomic regions. Cell 140:678–91 [Google Scholar]
  130. Pchelintsev NA, McBryan T, Rai TS, van Tuyn J, Ray Gallet D. 130.  et al. 2013. Placing the HIRA histone chaperone complex in the chromatin landscape. Cell Rep. 3:1012–19 [Google Scholar]
  131. Drané P, Ouararhni K, Depaux A, Shuaib M, Hamiche A. 131.  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]
  132. Michod D, Bartesaghi S, Khelifi A, Bellodi C, Berliocchi L. 132.  et al. 2012. Calcium-dependent dephosphorylation of the histone chaperone DAXX regulates H3.3 loading and transcription upon neuronal activation. Neuron 74:122–35 [Google Scholar]
  133. Xue Y, Gibbons R, Yan Z, Yang D, McDowell TL. 133.  et al. 2003. The ATRX syndrome protein forms a chromatin-remodeling complex with Daxx and localizes in promyelocytic leukemia nuclear bodies. Proc. Natl. Acad. Sci. USA 100:10635–40 [Google Scholar]
  134. Clarke L, Carbon J. 134.  1980. Isolation of a yeast centromere and construction of functional small circular chromosomes. Nature 287:504–9 [Google Scholar]
  135. Black BE, Bassett EA. 135.  2008. The histone variant CENP-A and centromere specification. Curr. Opin. Cell Biol. 20:91–100 [Google Scholar]
  136. Kato T, Sato N, Hayama S, Yamabuki T, Ito T. 136.  et al. 2007. Activation of Holliday junction recognizing protein involved in the chromosomal stability and immortality of cancer cells. Cancer Res. 67:8544–53 [Google Scholar]
  137. Dunleavy EM, Almouzni G, Karpen GH. 137.  2011. H3.3 is deposited at centromeres in S phase as a placeholder for newly assembled CENP-A in G1 phase. Nucleus 2:146–57 [Google Scholar]
  138. Zasadzińska E, Barnhart-Dailey MC, Kuich PHJL, Foltz DR. 138.  2013. Dimerization of the CENP-A assembly factor HJURP is required for centromeric nucleosome deposition. EMBO J. 32:2113–24 [Google Scholar]
  139. Bernad R, Sánchez P, Rivera T, Rodríguez-Corsino M, Boyarchuk E. 139.  et al. 2011. Xenopus HJURP and condensin II are required for CENP-A assembly. J. Cell Biol. 192:569–82 [Google Scholar]
  140. Stoler S, Rogers K, Weitze S, Morey L, Fitzgerald-Hayes M, Baker RE. 140.  2007. Scm3, an essential Saccharomyces cerevisiae centromere protein required for G2/M progression and Cse4 localization. Proc. Natl. Acad. Sci. USA 104:10571–76 [Google Scholar]
  141. Erhardt S, Mellone BG, Betts CM, Zhang W, Karpen GH, Straight AF. 141.  2008. Genome-wide analysis reveals a cell cycle–dependent mechanism controlling centromere propagation. J. Cell Biol. 183:805–18 [Google Scholar]
  142. Kaufman PD, Cohen JL, Osley MA. 142.  1998. Hir proteins are required for position-dependent gene silencing in Saccharomyces cerevisiae in the absence of chromatin assembly factor I. Mol. Cell. Biol. 18:4793–806 [Google Scholar]
  143. Sharp JA, Franco AA, Osley MA, Kaufman PD. 143.  2002. Chromatin assembly factor I and Hir proteins contribute to building functional kinetochores in S. cerevisiae. Genes Dev. 16:85–100 [Google Scholar]
  144. Haber JE, Braberg H, Wu Q, Alexander R, Haase J. 144.  et al. 2013. Systematic triple-mutant analysis uncovers functional connectivity between pathways involved in chromosome regulation. Cell Rep. 3:2168–78 [Google Scholar]
  145. Murzina N, Verreault A, Laue E, Stillman B. 145.  1999. Heterochromatin dynamics in mouse cells: interaction between chromatin assembly factor 1 and HP1 proteins. Mol. Cell 4:529–40 [Google Scholar]
  146. Loyola A, Tagami H, Bonaldi T, Roche D, Quivy J-P. 146.  et al. 2009. The HP1α–CAF1–SetDB1–containing complex provides H3K9me1 for Suv39-mediated K9me3 in pericentric heterochromatin. EMBO Rep. 10:769–75 [Google Scholar]
  147. Wong LH, Ren H, Williams E, McGhie J, Ahn S. 147.  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]
  148. Ask K, Jasencakova Z, Menard P, Feng Y, Almouzni G, Groth A. 148.  2012. Codanin-1, mutated in the anaemic disease CDAI, regulates Asf1 function in S-phase histone supply. EMBO J. 31:2013–23 [Google Scholar]
  149. Kaufman PD, Almouzni G. 149.  2000. DNA replication, nucleotide excision repair, and nucleosome assembly. Chromatin Structure and Gene Expression SCR Elgin, JL Workman 24–48 Oxford, UK: Oxford Univ. Press [Google Scholar]
  150. Alabert C, Groth A. 150.  2012. Chromatin replication and epigenome maintenance. Nat. Rev. Mol. Cell Biol. 13:153–67 [Google Scholar]
  151. Prior CP, Cantor CR, Johnson EM, Allfrey VG. 151.  1980. Incorporation of exogenous pyrene-labeled histone into Physarum chromatin: a system for studying changes in nucleosomes assembled in vivo. Cell 20:597–608 [Google Scholar]
  152. Jackson DA, Cook PR. 152.  1987. The nucleoskeleton: active site of transcription and replication. Haematol. Blood Transfus. 31:299–303 [Google Scholar]
  153. Jackson V.153.  1988. Deposition of newly synthesized histones: Hybrid nucleosomes are not tandemly arranged on daughter DNA strands. Biochemistry 27:2109–20 [Google Scholar]
  154. Annunziato AT.154.  1989. Inhibitors of topoisomerases I and II arrest DNA replication, but do not prevent nucleosome assembly in vivo. J. Cell Sci. 93:Part 4593–603 [Google Scholar]
  155. Yamasu K, Senshu T. 155.  1990. Conservative segregation of tetrameric units of H3 and H4 histones during nucleosome replication. J. Biochem. 107:15–20 [Google Scholar]
  156. Kass SU, Wolffe AP. 156.  1998. DNA methylation, nucleosomes and the inheritance of chromatin structure and function. Novartis Found. Symp. 214:22–50 [Google Scholar]
  157. McKittrick E, Gafken PR, Ahmad K, Henikoff S. 157.  2004. Histone H3.3 is enriched in covalent modifications associated with active chromatin. Proc. Natl. Acad. Sci. USA 101:1525–30 [Google Scholar]
  158. Xu M, Long C, Chen X, Huang C, Chen S, Zhu B. 158.  2010. Partitioning of histone H3–H4 tetramers during DNA replication–dependent chromatin assembly. Science 328:94–98 [Google Scholar]
  159. Huang C, Zhang Z, Xu M, Li Y, Li Z. 159.  et al. 2013. H3.3–H4 tetramer splitting events feature cell-type specific enhancers. PLoS Genet. 9:e1003558 [Google Scholar]
  160. Nakatani Y, Ray Gallet D, Quivy J-P, Tagami H, Almouzni G. 160.  2004. Two distinct nucleosome assembly pathways: dependent or independent of DNA synthesis promoted by histone H3.1 and H3.3 complexes. Cold Spring Harb. Symp. Quant. Biol. 69:273–80 [Google Scholar]
  161. Formosa T.161.  2012. The role of FACT in making and breaking nucleosomes. Biochim. Biophys. Acta 1819:247–55 [Google Scholar]
  162. Winkler DD, Muthurajan UM, Hieb AR, Luger K. 162.  2011. Histone chaperone FACT coordinates nucleosome interaction through multiple synergistic binding events. J. Biol. Chem. 286:41883–92 [Google Scholar]
  163. Gambus A, Jones RC, Sanchez-Diaz A, Kanemaki M, van Deursen F. 163.  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]
  164. Tan BC, Chien CT, Hirose S, Lee SC. 164.  2006. Functional cooperation between FACT and MCM helicase facilitates initiation of chromatin DNA replication. EMBO J. 25:3975–85 [Google Scholar]
  165. VanDemark AP, Blanksma M, Ferris E, Heroux A, Hill CP, Formosa T. 165.  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 22:363–74 [Google Scholar]
  166. Wittmeyer J, Formosa T. 166.  1997. The Saccharomyces cerevisiae DNA polymerase α catalytic subunit interacts with Cdc68/Spt16 and with Pob3, a protein similar to an HMG1-like protein. Mol. Cell. Biol. 17:4178–90 [Google Scholar]
  167. Abe T, Sugimura K, Hosono Y, Takami Y, Akita M. 167.  et al. 2011. The histone chaperone facilitates chromatin transcription (FACT) protein maintains normal replication fork rates. J. Biol. Chem. 286:30504–12 [Google Scholar]
  168. Soria G, Polo SE, Almouzni G. 168.  2012. Prime, repair, restore: the active role of chromatin in the DNA damage response. Mol. Cell 46:722–34 [Google Scholar]
  169. Adam S, Polo SE. 169.  2012. Chromatin dynamics during nucleotide excision repair: histones on the move. Int. J. Mol. Sci. 13:11895–911 [Google Scholar]
  170. Smerdon MJ.170.  1991. DNA repair and the role of chromatin structure. Curr. Opin. Cell Biol. 3:422–28 [Google Scholar]
  171. Baldeyron C, Soria G, Roche D, Cook AJ, Almouzni G. 171.  2011. HP1α recruitment to DNA damage by p150CAF-1 promotes homologous recombination repair. J. Cell Biol. 193:81–95 [Google Scholar]
  172. Soria G, Almouzni G. 172.  2013. Differential contribution of HP1 proteins to DNA end resection and homology-directed repair. Cell Cycle 12:422–29 [Google Scholar]
  173. Rogakou EP, Boon C, Redon C, Bonner WM. 173.  1999. Megabase chromatin domains involved in DNA double-strand breaks in vivo. J. Cell Biol. 146:905–16 [Google Scholar]
  174. Fillingham J, Keogh MC, Krogan NJ. 174.  2006. γH2AX and its role in DNA double-strand break repair. Biochem. Cell Biol. 84:568–77 [Google Scholar]
  175. Adam S, Polo SE, Almouzni G. 175.  2013. Transcription recovery after DNA damage requires chromatin priming by the H3.3 histone chaperone HIRA. Cell 155:94–106 [Google Scholar]
  176. Dinant C, Ampatziadis-Michailidis G, Lans H, Tresini M, Lagarou A. 176.  et al. 2013. Enhanced chromatin dynamics by FACT promotes transcriptional restart after UV-induced DNA damage. Mol. Cell 51:469–79 [Google Scholar]
  177. Boeger H, Griesenbeck J, Kornberg RD. 177.  2008. Nucleosome retention and the stochastic nature of promoter chromatin remodeling for transcription. Cell 133:716–26 [Google Scholar]
  178. Boeger H, Griesenbeck J, Strattan JS, Kornberg RD. 178.  2004. Removal of promoter nucleosomes by disassembly rather than sliding in vivo. Mol. Cell 14:667–73 [Google Scholar]
  179. Kornberg RD, Lorch Y. 179.  2002. Chromatin and transcription: Where do we go from here?. Curr. Opin. Genet. Dev. 12:249–51 [Google Scholar]
  180. Kulaeva OI, Gaykalova DA, Studitsky VM. 180.  2007. Transcription through chromatin by RNA polymerase II: histone displacement and exchange. Mutat. Res. 618:116–29 [Google Scholar]
  181. Smolle M, Venkatesh S, Gogol MM, Li H, Zhang Y. 181.  et al. 2012. Chromatin remodelers Isw1 and Chd1 maintain chromatin structure during transcription by preventing histone exchange. Nat. Struct. Mol. Biol. 19:884–92 [Google Scholar]
  182. Venkatesh S, Smolle M, Li H, Gogol MM, Saint M. 182.  et al. 2012. Set2 methylation of histone H3 lysine 36 suppresses histone exchange on transcribed genes. Nature 489:452–55 [Google Scholar]
  183. Owen-Hughes T, Workman JL. 183.  1996. Remodeling the chromatin structure of a nucleosome array by transcription factor–targeted trans-displacement of histones. EMBO J. 15:4702–12 [Google Scholar]
  184. Chen H, Li B, Workman JL. 184.  1994. A histone-binding protein, nucleoplasmin, stimulates transcription factor binding to nucleosomes and factor-induced nucleosome disassembly. EMBO J. 13:380–90 [Google Scholar]
  185. Walter PP, Owen-Hughes TA, Côté J, Workman JL. 185.  1995. Stimulation of transcription factor binding and histone displacement by nucleosome assembly protein 1 and nucleoplasmin requires disruption of the histone octamer. Mol. Cell. Biol. 15:6178–87 [Google Scholar]
  186. Schwabish MA, Struhl K. 186.  2006. Asf1 mediates histone eviction and deposition during elongation by RNA polymerase II. Mol. Cell 22:415–22 [Google Scholar]
  187. Kaplan CD, Laprade L, Winston F. 187.  2003. Transcription elongation factors repress transcription initiation from cryptic sites. Science 301:1096–99 [Google Scholar]
  188. Endoh M, Zhu W, Hasegawa J, Watanabe H, Kim DK. 188.  et al. 2004. Human Spt6 stimulates transcription elongation by RNA polymerase II in vitro. Mol. Cell. Biol. 24:3324–36 [Google Scholar]
  189. Chimura T, Kuzuhara T, Horikoshi M. 189.  2002. Identification and characterization of CIA/ASF1 as an interactor of bromodomains associated with TFIID. Proc. Natl. Acad. Sci. USA 99:9334–39 [Google Scholar]
  190. Simic R, Lindstrom DL, Tran HG, Roinick KL, Costa PJ. 190.  et al. 2003. Chromatin remodeling protein Chd1 interacts with transcription elongation factors and localizes to transcribed genes. EMBO J. 22:1846–56 [Google Scholar]
  191. Houlard M, Berlivet S, Probst AV, Quivy J-P, Héry P. 191.  et al. 2006. CAF-1 is essential for heterochromatin organization in pluripotent embryonic cells. PLoS Genet. 2:e181 [Google Scholar]
  192. Roberts C, Sutherland HF, Farmer H, Kimber W, Halford S. 192.  et al. 2002. Targeted mutagenesis of the Hira gene results in gastrulation defects and patterning abnormalities of mesoendodermal derivatives prior to early embryonic lethality. Mol. Cell. Biol. 22:2318–28 [Google Scholar]
  193. Garrick D, Sharpe JA, Arkell R, Dobbie L, Smith AJ. 193.  et al. 2006. Loss of Atrx affects trophoblast development and the pattern of X-inactivation in extraembryonic tissues. PLoS Genet. 2:e58 [Google Scholar]
  194. Michaelson JS, Bader D, Kuo F, Kozak C, Leder P. 194.  1999. Loss of Daxx, a promiscuously interacting protein, results in extensive apoptosis in early mouse development. Genes Dev. 13:1918–23 [Google Scholar]
  195. Hartford SA, Luo Y, Southard TL, Min IM, Lis JT, Schimenti JC. 195.  2011. Minichromosome maintenance helicase paralog MCM9 is dispensible for DNA replication but functions in germ-line stem cells and tumor suppression. Proc. Natl. Acad. Sci. USA 108:17702–7 [Google Scholar]
  196. Loppin B, Bonnefoy E, Anselme C, Laurençon A, Karr TL, Couble P. 196.  2005. The histone H3.3 chaperone HIRA is essential for chromatin assembly in the male pronucleus. Nature 437:1386–90 [Google Scholar]
  197. Bonnefoy E, Orsi GA, Couble P, Loppin B. 197.  2007. The essential role of Drosophila HIRA for de novo assembly of paternal chromatin at fertilization. PLoS Genet. 3:1991–2006 [Google Scholar]
  198. Szenker E, Lacoste N, Almouzni G. 198.  2012. A developmental requirement for HIRA-dependent H3.3 deposition revealed at gastrulation in Xenopus. Cell Rep. 1:730–40 [Google Scholar]
  199. Jullien J, Astrand C, Szenker E, Garrett N, Almouzni G, Gurdon JB. 199.  2012. HIRA dependent H3.3 deposition is required for transcriptional reprogramming following nuclear transfer to Xenopus oocytes. Epigenet. Chromatin 5:17 [Google Scholar]
  200. Lewis PW, Muller MM, Koletsky MS, Cordero F, Lin S. 200.  et al. 2013. Inhibition of PRC2 activity by a gain-of-function H3 mutation found in pediatric glioblastoma. Science 340:857–61 [Google Scholar]
  201. Almouzni G, Corpet A. 201.  2011. ASF1b as a prognosis marker and therapeutic target in human cancer. US patent no. 20130149320 [Google Scholar]
  202. Robinson PJ, Bushnell DA, Trnka MJ, Burlingame AL, Kornberg RD. 202.  2012. Structure of the mediator head module bound to the carboxy-terminal domain of RNA polymerase II. Proc. Natl. Acad. Sci. USA 109:17931–35 [Google Scholar]
  203. Sobel RE, Cook RG, Perry CA, Annunziato AT, Allis CD. 203.  1995. Conservation of deposition-related acetylation sites in newly synthesized histones H3 and H4. Proc. Natl. Acad. Sci. USA 92:1237–41 [Google Scholar]
  204. Huang S, Zhou H, Katzmann D, Hochstrasser M, Atanasova E, Zhang Z. 204.  2005. Rtt106p is a histone chaperone involved in heterochromatin-mediated silencing. Proc. Natl. Acad. Sci. USA 38:13410–15 [Google Scholar]
  205. Bortvin A, Winston F. 205.  1996. Evidence that Spt6p controls chromatin structure by a direct interaction with histones. Science 272:1473–76 [Google Scholar]
  206. Luk E, Vu N, Patteson K, Mizuguchi G, Wu W. 206.  et al. 2007. Chz1, a nuclear chaperone for histone H2AZ. Mol. Cell 5:357–68 [Google Scholar]
  207. Harata M, Oma Y, Mizuno S, Jiang YW, Sillman DJ. 207.  et al. 1999. The nuclear actin–related protein of Saccharomyces cerevisiae, Act3p/Arp4, interacts with core histones. Mol. Biol. Cell 10:2595–605 [Google Scholar]
  208. Shen X, Ranallo R, Choi E, Wu C. 208.  2003. Involvement of actin-related proteins in ATP-dependent chromatin remodeling. Mol. Cell 12:147–55 [Google Scholar]
  209. Okuwaki M, Matsumoto K, Tsujimoto M, Nagata K. 209.  2001. Function of nucleophosmin/B23, a nuclear acidic protein, as a histone chaperone. FEBS Lett. 506:272–76 [Google Scholar]
  210. Rouguelle C, Avner P. 210.  1996. Cloning and characterization of a murine brain specific gene Bpx and its human homologue lying within the Xic region. Hum. Mol. Genet. 5:41–49 [Google Scholar]
  211. Okuwaki M, Nagata K. 211.  1998. Template activating factor 1 remodels the chromatin structure and stimulates transcription from the chromatin template. J. Biol. Chem. 273:34511–18 [Google Scholar]
  212. Wang GS, Hong CJ, Yen TY, Huang HY, Ou Y. 212.  et al. 2004. Transcriptional modification by a CASK-interacting nucleosome assembly protein. Neuron 42:113–28 [Google Scholar]
  213. Selth L, Svejstrup JQ. 213.  2007. Vps75, a new yeast member of the NAP histone chaperone family. J. Biol. Chem. 282:12358–62 [Google Scholar]
  214. Loyola A, LeRoy G, Wang YH, Reinberg D. 214.  2001. Reconstitution of recombinant chromatin establishes a requirement for histone-tail modifications during chromatin assembly and transcription. Genes Dev. 15:2837–51 [Google Scholar]
  215. Peterson CL, Zhao Y, Chait BT. 215.  1998. Subunits of the yeast SWI/SNF complex are members of the actin-related protein (ARP) family. J. Biol. Chem. 273:23641–44 [Google Scholar]
  216. Ito T, Bulger M, Pazin MJ, Kobayashi R, Kadonaga JT. 216.  1997. ACF, an ISWI-containing and ATP-utilizing chromatin assembly and remodeling factor. Cell 90:145–55 [Google Scholar]
  217. Sawatsubashi S, Murata T, Lim J, Fujiki R, Ito S. 217.  et al. 2010. A histone chaperone, DEK, transcriptionally coactivates a nuclear receptor. Genes Dev. 24:159–70 [Google Scholar]
  218. Kashiwaba S, Kitahashi K, Watanabe T, Onoda F, Ohtsu M, Murakami Y. 218.  2010. The mammalian INO80 complex is recruited to DNA damage sites in an ARP8 dependent manner. Biochem. Biophys. Res. Commun. 402:619–25 [Google Scholar]
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