Histone Chaperones in the Assembly and Disassembly of Chromatin

  • Briana K. Dennehey
  • Jessica Tyler


As we learned in the previous chapter, the eukaryotic genome exists in our cells as the nucleoprotein complex chromatin. A human cell contains approximately 40 million nucleosomes, which are the fundamental repeating units of chromatin. As expected for a highly conserved structure, such as that of the nucleosome, its assembly is tightly orchestrated. In this chapter, we learn how histone chaperone proteins help establish the formation of the nucleosomal structure from the core histones and DNA. One profound consequence of chromatin formation is blocked access of the cellular machineries that require intimate access to DNA for DNA replication, DNA repair and transcription. We present the current state of knowledge regarding how chromatin is locally disassembled to allow genomic processes to occur, and how it is then rapidly reassembled back into chromatin. As a whole, chromatin assembly not only enables the genome to be packaged to fit into our cells but also enables the regulation of all genomic functions through dynamic chromatin disassembly and reassembly.


Replication Fork Histone Variant Linker Histone Chromatin Assembly Histone Chaperone 
These keywords were added by machine and not by the authors. This process is experimental and the keywords may be updated as the learning algorithm improves.


  1. Abe T, Sugimura K, Hosono Y, Takami Y, Akita M, Yoshimura A, Tada S, Nakayama T, Murofushi H, Okumura K, Takeda S, Horikoshi M, Seki M, Enomoto T (2011) The histone chaperone facilitates chromatin transcription (FACT) protein maintains normal replication fork rates. J Biol Chem 286(35):30504–30512. doi: 10.1074/jbc.M111.264721, M111.264721 [pii]PubMedGoogle Scholar
  2. Adkins MW, Tyler JK (2006) Transcriptional activators are dispensable for transcription in the absence of Spt6-mediated chromatin reassembly of promoter regions. Mol Cell 21:405–416PubMedGoogle Scholar
  3. 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(5):657–666PubMedGoogle Scholar
  4. Adkins MW, Williams SK, Linger J, Tyler JK (2007) Chromatin disassembly from the PHO5 promoter is essential for the recruitment of the general transcription machinery and coactivators. Mol Cell Biol 27(18):6372–6382. doi: 10.1128/MCB.00981-07, MCB.00981-07 [pii]PubMedGoogle Scholar
  5. Ahmad K, Henikoff S (2002) The histone variant H3.3 marks active chromatin by replication-independent nucleosome assembly. Mol Cell 9(6):1191–1200PubMedGoogle Scholar
  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(10):8846–8852. doi: 10.1074/jbc.M210352200, M210352200 [pii]PubMedGoogle Scholar
  7. Alekseev OM, Widgren EE, Richardson RT, O’Rand MG (2005) Association of NASP with HSP90 in mouse spermatogenic cells: stimulation of ATPase activity and transport of linker histones into nuclei. J Biol Chem 280(4):2904–2911. doi: 10.1074/jbc.M410397200, M410397200 [pii]PubMedGoogle Scholar
  8. 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(20):17714–17721. doi: 10.1074/jbc.M111.223453, M111.223453 [pii]PubMedGoogle Scholar
  9. Andrews AJ, Chen X, Zevin A, Stargell LA, Luger K (2010) The histone chaperone Nap1 promotes nucleosome assembly by eliminating nonnucleosomal histone DNA interactions. Mol Cell 37(6):834–842. doi: 10.1016/j.molcel.2010.01.037, S1097-2765(10)00156-5 [pii]PubMedGoogle Scholar
  10. Banks DD, Gloss LM (2003) Equilibrium folding of the core histones: the H3-H4 tetramer is less stable than the H2A-H2B dimer. Biochemistry 42(22):6827–6839PubMedGoogle Scholar
  11. Barnhart MC, Kuich PH, Stellfox ME, Ward JA, Bassett EA, Black BE, Foltz DR (2011) HJURP is a CENP-A chromatin assembly factor sufficient to form a functional de novo kinetochore. J Cell Biol 194(2):229–243. doi: 10.1083/jcb.201012017, jcb.201012017 [pii]PubMedGoogle Scholar
  12. Bassett EA, DeNizio J, Barnhart-Dailey MC, Panchenko T, Sekulic N, Rogers DJ, Foltz DR, Black BE (2012) HJURP uses distinct CENP-A surfaces to recognize and to stabilize CENP-A/histone H4 for centromere assembly. Dev Cell 22(4):749–762. doi: 10.1016/j.devcel.2012.02.001, S1534-5807(12)00059-7 [pii]PubMedGoogle Scholar
  13. Baxevanis AD, Godfrey JE, Moudrianakis EN (1991) Associative behavior of the histone (H3-H4)2 tetramer: dependence on ionic environment. Biochemistry 30(36):8817–8823PubMedGoogle Scholar
  14. Belotserkovskaya R, Oh S, Bondarenko VA, Orphanides G, Studitsky VM, Reinberg D (2003) FACT facilitates transcription-dependent nucleosome alteration. Science 301(5636):1090–1093PubMedGoogle Scholar
  15. Biswas D, Yu Y, Prall M, Formosa T, Stillman DJ (2005) The yeast FACT complex has a role in transcriptional initiation. Mol Cell Biol 25(14):5812–5822PubMedGoogle Scholar
  16. Biswas D, Dutta-Biswas R, Mitra D, Shibata Y, Strahl BD, Formosa T, Stillman DJ (2006) Opposing roles for Set2 and yFACT in regulating TBP binding at promoters. EMBO J 25(19): 4479–4489PubMedGoogle Scholar
  17. Black BE, Foltz DR, Chakravarthy S, Luger K, Woods VL Jr, Cleveland DW (2004) Structural determinants for generating centromeric chromatin. Nature 430(6999):578–582. doi: 10.1038/nature02766, nature02766 [pii]PubMedGoogle Scholar
  18. Black BE, Jansen LE, Maddox PS, Foltz DR, Desai AB, Shah JV, Cleveland DW (2007) Centromere identity maintained by nucleosomes assembled with histone H3 containing the CENP-A targeting domain. Mol Cell 25(2):309–322. doi: 10.1016/j.molcel.2006.12.018, S1097-2765(06)00886-0 [pii]PubMedGoogle Scholar
  19. Bloom KS, Carbon J (1982) Yeast centromere DNA is in a unique and highly ordered structure in chromosomes and small circular minichromosomes. Cell 29(2):305–317, 0092-8674(82)90147-7 [pii]PubMedGoogle Scholar
  20. Bortvin A, Winston F (1996) Evidence that Spt6p controls chromatin structure by a direct interaction with histones. Science 272(5267):1473–1476PubMedGoogle Scholar
  21. Bui M, Dimitriadis EK, Hoischen C, An E, Quenet D, Giebe S, Nita-Lazar A, Diekmann S, Dalal Y (2012) Cell-cycle-dependent structural transitions in the human CENP-A nucleosome in vivo. Cell 150(2):317–326. doi: 10.1016/j.cell.2012.05.035, S0092-8674(12)00705-2 [pii]PubMedGoogle Scholar
  22. Burgess RJ, Zhou H, Han J, Zhang Z (2010) A role for Gcn5 in replication-coupled nucleosome assembly. Mol Cell 37(4):469–480. doi: 10.1016/j.molcel.2010.01.020, S1097-2765(10)00071-7 [pii]PubMedGoogle Scholar
  23. 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(6):853–865. doi: 10.1016/j.molcel.2007.05.013, S1097-2765(07)00314-0 [pii]PubMedGoogle Scholar
  24. Campos EI, Fillingham J, Li G, Zheng H, Voigt P, Kuo WH, Seepany H, Gao Z, Day LA, Greenblatt JF, Reinberg D (2010) The program for processing newly synthesized histones H3.1 and H4. Nat Struct Mol Biol 17(11):1343–1351. doi: 10.1038/nsmb.1911, nsmb.1911 [pii]PubMedGoogle Scholar
  25. Celic I, Masumoto H, Griffith WP, Meluh P, Cotter RJ, Boeke JD, Verreault A (2006) The sirtuins hst3 and Hst4p preserve genome integrity by controlling histone h3 lysine 56 deacetylation. Curr Biol 16(13):1280–1289PubMedGoogle Scholar
  26. Chang L, Loranger SS, Mizzen C, Ernst SG, Allis CD, Annunziato AT (1997) Histones in transit: cytosolic histone complexes and diacetylation of H4 during nucleosome assembly in human cells. Biochemistry 36(3):469–480PubMedGoogle Scholar
  27. Chen CC, Carson JJ, Feser J, Tamburini B, Zabaronick S, Linger J, Tyler JK (2008) Acetylated lysine 56 on histone H3 drives chromatin assembly after repair and signals for the completion of repair. Cell 134(2):231–243. doi: 10.1016/j.cell.2008.06.035, S0092-8674(08)00822-2 [pii]PubMedGoogle Scholar
  28. Cheung V, Chua G, Batada NN, Landry CR, Michnick SW, Hughes TR, Winston F (2008) Chromatin- and transcription-related factors repress transcription from within coding regions throughout the Saccharomyces cerevisiae genome. PLoS Biol 6(11):e277. doi: 10.1371/journal.pbio.0060277, 08-PLBI-RA-1993 [pii]PubMedGoogle Scholar
  29. Cole HA, Howard BH, Clark DJ (2011) The centromeric nucleosome of budding yeast is perfectly positioned and covers the entire centromere. Proc Natl Acad Sci USA 108(31):12687–12692. doi: 10.1073/pnas.1104978108, 1104978108 [pii]PubMedGoogle Scholar
  30. Cusick ME, DePamphilis ML, Wassarman PM (1984) Dispersive segregation of nucleosomes during replication of simian virus 40 chromosomes. J Mol Biol 178(2):249–271, 0022-2836(84)90143-8 [pii]PubMedGoogle Scholar
  31. Das C, Lucia MS, Hansen KC, Tyler JK (2009) CBP/p300-mediated acetylation of histone H3 on lysine 56. Nature 459(7243):113–117. doi: 10.1038/nature07861, nature07861 [pii]PubMedGoogle Scholar
  32. Dechassa ML, Wyns K, Li M, Hall MA, Wang MD, Luger K (2011) Structure and Scm3-mediated assembly of budding yeast centromeric nucleosomes. Nat Commun 2:313. doi: 10.1038/ncomms 1320, ncomms1320 [pii]
  33. Diffley JF (2011) Quality control in the initiation of eukaryotic DNA replication. Philos Trans R Soc Lond B Biol Sci 366(1584):3545–3553. doi: 10.1098/rstb.2011.0073, 366/1584/3545 [pii]PubMedGoogle Scholar
  34. Dion MF, Kaplan T, Kim M, Buratowski S, Friedman N, Rando OJ (2007) Dynamics of replication-independent histone turnover in budding yeast. Science 315(5817):1405–1408PubMedGoogle Scholar
  35. Donham DC 2nd, Scorgie JK, Churchill MEA (2011) The activity of the histone chaperone yeast Asf1 in the assembly and disassembly of histone H3/H4-DNA complexes. Nucleic Acids Res 39(13):5449–5458PubMedGoogle Scholar
  36. Dowell NL, Sperling AS, Mason MJ, Johnson RC (2010) Chromatin-dependent binding of the S. cerevisiae HMGB protein Nhp6A affects nucleosome dynamics and transcription. Genes Dev 24(18):2031–2042. doi: 10.1101/gad.1948910, 24/18/2031 [pii]PubMedGoogle Scholar
  37. 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(12):1253–1265. doi: 10.1101/gad.566910, gad.566910 [pii]PubMedGoogle Scholar
  38. Dunleavy EM, Pidoux AL, Monet M, Bonilla C, Richardson W, Hamilton GL, Ekwall K, McLaughlin PJ, Allshire RC (2007) A NASP (N1/N2)-related protein, Sim3, binds CENP-A and is required for its deposition at fission yeast centromeres. Mol Cell 28(6):1029–1044. doi: 10.1016/j.molcel.2007.10.010, S1097-2765(07)00692-2 [pii]PubMedGoogle Scholar
  39. Dunleavy EM, Roche D, Tagami H, Lacoste N, Ray-Gallet D, Nakamura Y, Daigo Y, Nakatani Y, Almouzni-Pettinotti G (2009) HJURP is a cell-cycle-dependent maintenance and deposition factor of CENP-A at centromeres. Cell 137(3):485–497. doi: 10.1016/j.cell.2009.02.040, S0092-8674(09)00254-2 [pii]PubMedGoogle Scholar
  40. Dunleavy EM, Almouzni G, Karpen GH (2011) H3.3 is deposited at centromeres in S phase as a placeholder for newly assembled CENP-A in G(1) phase. Nucleus 2(2):146–157. doi: 10.4161/nucl.2.2.15211, 1949-1034-2-2-10 [pii]PubMedGoogle Scholar
  41. Elsasser SJ, Huang H, Lewis PW, Chin JW, Allis CD, Patel DJ (2012) DAXX envelops an H3.3-H4 dimer for H3.3-specific recognition. Nature 491(7425):560–565. doi: 10.1038/nature11608, nature11608 [pii]PubMedGoogle Scholar
  42. English CM, Adkins MW, Carson JJ, Churchill ME, Tyler JK (2006) Structural basis for the histone chaperone activity of Asf1. Cell 127(3):495–508. doi: 10.1016/j.cell.2006.08.047, S0092-8674(06)01273-6 [pii]PubMedGoogle Scholar
  43. Fazly A, Li Q, Hu Q, Mer G, Horazdovsky B, Zhang Z (2012) Histone chaperone Rtt106 promotes nucleosome formation using (H3-H4)2 tetramers. J Biol Chem 287(14):10753–10760. doi: 10.1074/jbc.M112.347450, M112.347450 [pii]PubMedGoogle Scholar
  44. Finn RM, Browne K, Hodgson KC, Ausio J (2008) sNASP, a histone H1-specific eukaryotic chaperone dimer that facilitates chromatin assembly. Biophys J 95(3):1314–1325. doi: 10.1529/biophysj.108.130021, S0006-3495(08)70201-7 [pii]PubMedGoogle Scholar
  45. Fitzgerald-Hayes M, Clarke L, Carbon J (1982) Nucleotide sequence comparisons and functional analysis of yeast centromere DNAs. Cell 29(1):235–244, 0092-8674(82)90108-8 [pii]PubMedGoogle Scholar
  46. Floer M, Wang X, Prabhu V, Berrozpe G, Narayan S, Spagna D, Alvarez D, Kendall J, Krasnitz A, Stepansky A, Hicks J, Bryant GO, Ptashne M (2010) A RSC/nucleosome complex determines chromatin architecture and facilitates activator binding. Cell 141(3):407–418. doi: 10.1016/j.cell.2010.03.048, S0092-8674(10)00367-3 [pii]PubMedGoogle Scholar
  47. Franco AA, Lam WM, Burgers PM, Kaufman PD (2005) Histone deposition protein Asf1 maintains DNA replisome integrity and interacts with replication factor C. Genes Dev 19(11): 1365–1375PubMedGoogle Scholar
  48. Fujita Y, Hayashi T, Kiyomitsu T, Toyoda Y, Kokubu A, Obuse C, Yanagida M (2007) Priming of centromere for CENP-A recruitment by human hMis18alpha, hMis18beta, and M18BP1. Dev Cell 12(1):17–30. doi: 10.1016/j.devcel.2006.11.002, S1534-5807(06)00507-7 [pii]PubMedGoogle Scholar
  49. Furuyama S, Biggins S (2007) Centromere identity is specified by a single centromeric nucleosome in budding yeast. Proc Natl Acad Sci USA 104(37):14706–14711. doi: 10.1073/pnas.0706985104, 0706985104 [pii]PubMedGoogle Scholar
  50. Furuyama T, Dalal Y, Henikoff S (2006) Chaperone-mediated assembly of centromeric chromatin in vitro. Proc Natl Acad Sci USA 103(16):6172–6177. doi: 10.1073/pnas.0601686103, 0601686103 [pii]PubMedGoogle Scholar
  51. Gaillard PH, Martini EM, Kaufman PD, Stillman B, Moustacchi E, Almouzni G (1996) Chromatin assembly coupled to DNA repair: a new role for chromatin assembly factor I. Cell 86(6):887–896PubMedGoogle Scholar
  52. Gambus A, Jones RC, Sanchez-Diaz A, Kanemaki M, van Deursen F, Edmondson RD, Labib K (2006) GINS maintains association of Cdc45 with MCM in replisome progression complexes at eukaryotic DNA replication forks. Nat Cell Biol 8(4):358–366. doi: 10.1038/ncb1382, ncb1382 [pii]PubMedGoogle Scholar
  53. Gao J, Zhu Y, Zhou W, Molinier J, Dong A, Shen WH (2012) NAP1 family histone chaperones are required for somatic homologous recombination in Arabidopsis. Plant Cell 24(4):1437–1447. doi: 10.1105/tpc.112.096792, tpc.112.096792 [pii]PubMedGoogle Scholar
  54. Gasser R, Koller T, Sogo JM (1996) The stability of nucleosomes at the replication fork. J Mol Biol 258(2):224–239PubMedGoogle Scholar
  55. Gkikopoulos T, Havas KM, Dewar H, Owen-Hughes T (2009) SWI/SNF and Asf1p cooperate to displace histones during induction of the saccharomyces cerevisiae HO promoter. Mol Cell Biol 29(15):4057–4066. doi: 10.1128/MCB.00400-09, MCB.00400-09 [pii]PubMedGoogle Scholar
  56. Goldberg AD, Banaszynski LA, Noh KM, Lewis PW, Elsaesser SJ, Stadler S, Dewell S, Law M, Guo X, Li X, Wen D, Chapgier A, DeKelver RC, Miller JC, Lee YL, Boydston EA, Holmes MC, Gregory PD, Greally JM, Rafii S, Yang C, Scambler PJ, Garrick D, Gibbons RJ, Higgs DR, Cristea IM, Urnov FD, Zheng D, Allis CD (2010) Distinct factors control histone variant H3.3 localization at specific genomic regions. Cell 140(5):678–691. doi: 10.1016/j.cell.2010.01.003, S0092-8674(10)00004-8 [pii]PubMedGoogle Scholar
  57. Gospodinov A, Vaissiere T, Krastev DB, Legube G, Anachkova B, Herceg Z (2011) Mammalian Ino80 mediates double-strand break repair through its role in DNA end strand resection. Mol Cell Biol 31(23):4735–4745. doi: 10.1128/MCB.06182-11, MCB.06182-11 [pii]PubMedGoogle Scholar
  58. 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(2):301–311PubMedGoogle Scholar
  59. Groth A, Corpet A, Cook AJ, Roche D, Bartek J, Lukas J, Almouzni G (2007) Regulation of replication fork progression through histone supply and demand. Science 318(5858):1928–1931. doi: 10.1126/science.1148992, 318/5858/1928 [pii]PubMedGoogle Scholar
  60. Guillemette B, Gaudreau L (2006) Reuniting the contrasting functions of H2A.Z. Biochem Cell Biol 84(4):528–535. doi: 10.1139/o06-077, o06-077 [pii]PubMedGoogle Scholar
  61. Hajra S, Ghosh SK, Jayaram M (2006) The centromere-specific histone variant Cse4p (CENP-A) is essential for functional chromatin architecture at the yeast 2-microm circle partitioning locus and promotes equal plasmid segregation. J Cell Biol 174(6):779–790. doi: 10.1083/jcb.200603042, jcb.200603042 [pii]PubMedGoogle Scholar
  62. Han J, Zhou H, Horazdovsky B, Zhang K, Xu RM, Zhang Z (2007) Rtt109 acetylates histone H3 lysine 56 and functions in DNA replication. Science 315(5812):653–655. doi: 10.1126/science.1133234, 315/5812/653 [pii]PubMedGoogle Scholar
  63. Han J, Li Q, McCullough L, Kettelkamp C, Formosa T, Zhang Z (2010) Ubiquitylation of FACT by the cullin-E3 ligase Rtt101 connects FACT to DNA replication. Genes Dev 24(14):1485–1490. doi: 10.1101/gad.1887310, 24/14/1485 [pii]PubMedGoogle Scholar
  64. Hatch CL, Bonner WM (1988) Sequence of cDNAs for mammalian H2A.Z, an evolutionarily diverged but highly conserved basal histone H2A isoprotein species. Nucleic Acids Res 16(3): 1113–1124PubMedGoogle Scholar
  65. 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(6):715–729. doi: 10.1016/j.cell.2004.09.002, S0092867404008323 [pii]PubMedGoogle Scholar
  66. Henikoff S, Henikoff JG (2012) “Point” centromeres of Saccharomyces harbor single centromere-specific nucleosomes. Genetics 190(4):1575–1577. doi: 10.1534/genetics.111.137711, genetics.111.137711 [pii]PubMedGoogle Scholar
  67. Heo K, Kim H, Choi SH, Choi J, Kim K, Gu J, Lieber MR, Yang AS, An W (2008) FACT-mediated exchange of histone variant H2AX regulated by phosphorylation of H2AX and ADP-ribosylation of Spt16. Mol Cell 30(1):86–97. doi: 10.1016/j.molcel.2008.02.029, S1097-2765(08)00206-2 [pii]PubMedGoogle Scholar
  68. Herman TM, DePamphilis ML, Wassarman PM (1981) Structure of chromatin at deoxyribonucleic acid replication forks: location of the first nucleosomes on newly synthesized simian virus 40 deoxyribonucleic acid. Biochemistry 20(3):621–630PubMedGoogle Scholar
  69. Ito T, Bulger M, Kobayashi R, Kadonaga JT (1996) Drosophila NAP-1 is a core histone chaperone that functions in ATP- facilitated assembly of regularly spaced nucleosomal arrays. Mol Cell Biol 16(6):3112–3124PubMedGoogle Scholar
  70. Ito T, Bulger M, Pazin MJ, Kobayashi R, Kadonaga JT (1997) ACF, an ISWI-containing and ATP-utilizing chromatin assembly and remodeling factor. Cell 90(1):145–155PubMedGoogle Scholar
  71. Izban MG, Luse DS (1991) Transcription on nucleosomal templates by RNA polymerase II in vitro: inhibition of elongation with enhancement of sequence-specific pausing. Genes Dev 5(4):683–696PubMedGoogle Scholar
  72. Jackson V (1987) Deposition of newly synthesized histones: new histones H2A and H2B do not deposit in the same nucleosome with new histones H3 and H4. Biochemistry 26(8): 2315–2325PubMedGoogle Scholar
  73. Jackson V (1988) Deposition of newly synthesized histones: hybrid nucleosomes are not tandemly arranged on daughter DNA strands. Biochemistry 27(6):2109–2120PubMedGoogle Scholar
  74. Jackson V, Chalkley R (1981) A new method for the isolation of replicative chromatin: selective deposition of histone on both new and old DNA. Cell 23(1):121–134PubMedGoogle Scholar
  75. Jamai A, Puglisi A, Strubin M (2009) Histone chaperone spt16 promotes redeposition of the original h3-h4 histones evicted by elongating RNA polymerase. Mol Cell 35(3):377–383. doi: 10.1016/j.molcel.2009.07.001, S1097-2765(09)00470-5 [pii]PubMedGoogle Scholar
  76. Jansen LE, Black BE, Foltz DR, Cleveland DW (2007) Propagation of centromeric chromatin requires exit from mitosis. J Cell Biol 176(6):795–805. doi: 10.1083/jcb.200701066, jcb.200701066 [pii]PubMedGoogle Scholar
  77. Jasencakova Z, Scharf AN, Ask K, Corpet A, Imhof A, Almouzni G, Groth A (2010) Replication stress interferes with histone recycling and predeposition marking of new histones. Mol Cell 37(5):736–743. doi: 10.1016/j.molcel.2010.01.033, S1097-2765(10)00118-8 [pii]PubMedGoogle Scholar
  78. Jin C, Felsenfeld G (2007) Nucleosome stability mediated by histone variants H3.3 and H2A.Z. Genes Dev 21(12):1519–1529. doi: 10.1101/gad.1547707, 21/12/1519 [pii]PubMedGoogle Scholar
  79. Jin C, Zang C, Wei G, Cui K, Peng W, Zhao K, Felsenfeld G (2009) H3.3/H2A.Z double variant-containing nucleosomes mark ‘nucleosome-free regions’ of active promoters and other regulatory regions. Nat Genet 41(8):941–945. doi: 10.1038/ng.409, ng.409 [pii]PubMedGoogle Scholar
  80. Kang B, Pu M, Hu G, Wen W, Dong Z, Zhao K, Stillman B, Zhang Z (2011) Phosphorylation of H4 Ser 47 promotes HIRA-mediated nucleosome assembly. Genes Dev 25(13):1359–1364. doi: 10.1101/gad.2055511, 25/13/1359 [pii]PubMedGoogle Scholar
  81. Kaplan CD, Laprade L, Winston F (2003) Transcription elongation factors repress transcription initiation from cryptic sites. Science 301(5636):1096–1099PubMedGoogle Scholar
  82. Katan-Khaykovich Y, Struhl K (2011) Splitting of H3-H4 tetramers at transcriptionally active genes undergoing dynamic histone exchange. Proc Natl Acad Sci USA 108(4):1296–1301. doi: 10.1073/pnas.1018308108, 1018308108 [pii]PubMedGoogle Scholar
  83. Kellogg DR, Kikuchi A, Fujii-Nakata T, Turck CW, Murray AW (1995) Members of the NAP/SET family of proteins interact specifically with B-type cyclins. J Cell Biol 130(3):661–673PubMedGoogle Scholar
  84. Kim HJ, Seol JH, Han JW, Youn HD, Cho EJ (2007) Histone chaperones regulate histone exchange during transcription. EMBO J 26(21):4467–4474. doi: 10.1038/sj.emboj.7601870, 7601870 [pii]PubMedGoogle Scholar
  85. Kireeva ML, Walter W, Tchernajenko V, Bondarenko V, Kashlev M, Studitsky VM (2002) Nucleosome remodeling induced by RNA polymerase II: loss of the H2A/H2B dimer during transcription. Mol Cell 9(3):541–552, S1097276502004720 [pii]PubMedGoogle Scholar
  86. Knezetic JA, Luse DS (1986) The presence of nucleosomes on a DNA template prevents initiation by RNA polymerase II in vitro. Cell 45(1):95–104, 0092-8674(86)90541-6 [pii]PubMedGoogle Scholar
  87. Kobor MS, Venkatasubrahmanyam S, Meneghini MD, Gin JW, Jennings JL, Link AJ, Madhani HD, Rine J (2004) A protein complex containing the conserved Swi2/Snf2-related ATPase Swr1p deposits histone variant H2A.Z into euchromatin. PLoS Biol 2(5):E131PubMedGoogle Scholar
  88. Korber P, Barbaric S, Luckenbach T, Schmid A, Schermer UJ, Blaschke D, Horz W (2006) The histone chaperone Asf1 increases the rate of histone eviction at the yeast PHO5 and PHO8 promoters. J Biol Chem 281(9):5539–5545PubMedGoogle Scholar
  89. Kunkel TA (2011) Balancing eukaryotic replication asymmetry with replication fidelity. Curr Opin Chem Biol 15(5):620–626. doi: 10.1016/j.cbpa.2011.07.025, S1367-5931(11)00132-3 [pii]PubMedGoogle Scholar
  90. Kuzuhara T, Horikoshi M (2004) A nuclear FK506-binding protein is a histone chaperone regulating rDNA silencing. Nat Struct Mol Biol 11(3):275–283. doi: 10.1038/nsmb733, nsmb733 [pii]PubMedGoogle Scholar
  91. Lankenau S, Barnickel T, Marhold J, Lyko F, Mechler BM, Lankenau DH (2003) Knockout targeting of the Drosophila nap1 gene and examination of DNA repair tracts in the recombination products. Genetics 163(2):611–623PubMedGoogle Scholar
  92. Laskey RA, Earnshaw WC (1980) Nucleosome assembly. Nature 286(5775):763–767PubMedGoogle Scholar
  93. 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(5679):416–420PubMedGoogle Scholar
  94. Le S, Davis C, Konopka JB, Sternglanz R (1997) Two new S-phase-specific genes from Saccharomyces cerevisiae. Yeast 13(11):1029–1042PubMedGoogle Scholar
  95. 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. Proc Natl Acad Sci USA 107(32):14075–14080. doi: 10.1073/pnas.1008850107, 1008850107 [pii]PubMedGoogle Scholar
  96. Li Q, Zhou H, Wurtele H, Davies B, Horazdovsky B, Verreault A, Zhang Z (2008) Acetylation of histone H3 lysine 56 regulates replication-coupled nucleosome assembly. Cell 134(2):244–255. doi: 10.1016/j.cell.2008.06.018, S0092-8674(08)00770-8 [pii]PubMedGoogle Scholar
  97. Lin LJ, Schultz MC (2011) Promoter regulation by distinct mechanisms of functional interplay between lysine acetylase Rtt109 and histone chaperone Asf1. Proc Natl Acad Sci USA 108(49): 19599–19604. doi: 10.1073/pnas.1111501108, 1111501108 [pii]PubMedGoogle Scholar
  98. Linger J, Tyler JK (2005) The yeast histone chaperone chromatin assembly factor 1 protects against double-strand DNA-damaging agents. Genetics 171(4):1513–1522PubMedGoogle Scholar
  99. 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 40:11229–11239. doi: 10.1093/nar/gks906, gks906 [pii]PubMedGoogle Scholar
  100. Lorch Y, LaPointe JW, Kornberg RD (1987) Nucleosomes inhibit the initiation of transcription but allow chain elongation with the displacement of histones. Cell 49(2):203–210, 0092-8674(87)90561-7 [pii]PubMedGoogle Scholar
  101. Lorch Y, Maier-Davis B, Kornberg RD (2006) Chromatin remodeling by nucleosome disassembly in vitro. Proc Natl Acad Sci USA 103(9):3090–3093PubMedGoogle Scholar
  102. Luciani JJ, Depetris D, Usson Y, Metzler-Guillemain C, Mignon-Ravix C, Mitchell MJ, Megarbane A, Sarda P, Sirma H, Moncla A, Feunteun J, Mattei MG (2006) PML nuclear bodies are highly organised DNA-protein structures with a function in heterochromatin remodelling at the G2 phase. J Cell Sci 119(Pt 12):2518–2531. doi: 10.1242/jcs.02965, jcs.02965 [pii]PubMedGoogle Scholar
  103. Luconi L, Araki Y, Erlemann S, Schiebel E (2011) The CENP-A chaperone Scm3 becomes enriched at kinetochores in anaphase independently of CENP-A incorporation. Cell Cycle 10(19):3369–3378. doi: 10.4161/cc.10.19.17663, 17663 [pii]PubMedGoogle Scholar
  104. Luger K, Mader AW, Richmond RK, Sargent DF, Richmond TJ (1997) Crystal structure of the nucleosome core particle at 2.8 A resolution. Nature 389(6648):251–260PubMedGoogle Scholar
  105. Luk E, Vu ND, Patteson K, Mizuguchi G, Wu WH, Ranjan A, Backus J, Sen S, Lewis M, Bai Y, Wu C (2007) Chz1, a nuclear chaperone for histone H2AZ. Mol Cell 25(3):357–368. doi: 10.1016/j.molcel.2006.12.015, S1097-2765(06)00883-5 [pii]PubMedGoogle Scholar
  106. Maddox PS, Oegema K, Desai A, Cheeseman IM (2004) “Holo”er than thou: chromosome segregation and kinetochore function in C. elegans. Chromosome Res 12(6):641–653. doi: 10.1023/B:CHRO.0000036588.42225.2f, 5381345 [pii]PubMedGoogle Scholar
  107. Maddox PS, Hyndman F, Monen J, Oegema K, Desai A (2007) Functional genomics identifies a Myb domain-containing protein family required for assembly of CENP-A chromatin. J Cell Biol 176(6):757–763. doi: 10.1083/jcb.200701065, jcb.200701065 [pii]PubMedGoogle Scholar
  108. 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(20):14022–14031PubMedGoogle Scholar
  109. Marques M, Laflamme L, Gervais AL, Gaudreau L (2010) Reconciling the positive and negative roles of histone H2A.Z in gene transcription. Epigenetics 5(4):267–272, 11520 [pii]PubMedGoogle Scholar
  110. Mason PB, Struhl K (2003) The FACT complex travels with elongating RNA polymerase II and is important for the fidelity of transcriptional initiation in vivo. Mol Cell Biol 23(22):8323–8333PubMedGoogle Scholar
  111. Masumoto H, Hawke D, Kobayashi R, Verreault A (2005) A role for cell-cycle-regulated histone H3 lysine 56 acetylation in the DNA damage response. Nature 436(7048):294–298PubMedGoogle Scholar
  112. McCullough L, Rawlins R, Olsen A, Xin H, Stillman DJ, Formosa T (2011) Insight into the mechanism of nucleosome reorganization from histone mutants that suppress defects in the FACT histone chaperone. Genetics 188(4):835–846. doi: 10.1534/genetics.111.128769, genetics.111.128769 [pii]PubMedGoogle Scholar
  113. McKnight SL, Miller OL Jr (1977) Electron microscopic analysis of chromatin replication in the cellular blastoderm Drosophila melanogaster embryo. Cell 12(3):795–804, 0092-8674(77)90278-1 [pii]PubMedGoogle Scholar
  114. Mellone BG, Grive KJ, Shteyn V, Bowers SR, Oderberg I, Karpen GH (2011) Assembly of Drosophila centromeric chromatin proteins during mitosis. PLoS Genet 7(5):e1002068. doi: 10.1371/journal.pgen.1002068, PGENETICS-D-10-00429 [pii]PubMedGoogle Scholar
  115. Mills AD, Laskey RA, Black P, De Robertis EM (1980) An acidic protein which assembles nucleosomes in vitro is the most abundant protein in Xenopus oocyte nuclei. J Mol Biol 139(3):561–568, 0022-2836(80)90148-5 [pii]PubMedGoogle Scholar
  116. Mishra PK, Au WC, Choy JS, Kuich PH, Baker RE, Foltz DR, Basrai MA (2011) Misregulation of Scm3p/HJURP causes chromosome instability in Saccharomyces cerevisiae and human cells. PLoS Genet 7(9):e1002303. doi: 10.1371/journal.pgen.1002303, PGENETICS-D-11-00568 [pii]PubMedGoogle Scholar
  117. Mito Y, Henikoff JG, Henikoff S (2005) Genome-scale profiling of histone H3.3 replacement patterns. Nat Genet 37(10):1090–1097PubMedGoogle Scholar
  118. Mito Y, Henikoff JG, Henikoff S (2007) Histone replacement marks the boundaries of cis-regulatory domains. Science 315(5817):1408–1411. doi: 10.1126/science.1134004, 315/5817/1408 [pii]PubMedGoogle Scholar
  119. Mizuguchi G, Shen X, Landry J, Wu WH, Sen S, Wu C (2003) ATP-driven exchange of histone H2AZ variant catalyzed by SWR1 chromatin remodeling complex. Science 303(5656):343–348PubMedGoogle Scholar
  120. Moggs JG, Grandi P, Quivy JP, Jonsson ZO, Hubscher U, Becker PB, Almouzni G (2000) A CAF-1-PCNA-mediated chromatin assembly pathway triggered by sensing DNA damage. Mol Cell Biol 20(4):1206–1218PubMedGoogle Scholar
  121. Morillo-Huesca M, Maya D, Munoz-Centeno MC, Singh RK, Oreal V, Reddy GU, Liang D, Geli V, Gunjan A, Chavez S (2010) FACT prevents the accumulation of free histones evicted from transcribed chromatin and a subsequent cell cycle delay in G1. PLoS Genet 6(5):e1000964. doi: 10.1371/journal.pgen.1000964 PubMedGoogle Scholar
  122. Morrison AJ, Highland J, Krogan NJ, Arbel-Eden A, Greenblatt JF, Haber JE, Shen X (2004) INO80 and gamma-H2AX interaction links ATP-dependent chromatin remodeling to DNA damage repair. Cell 119(6):767–775. doi: 10.1016/j.cell.2004.11.037, S0092867404011055 [pii]PubMedGoogle Scholar
  123. Mosammaparast N, Jackson KR, Guo Y, Brame CJ, Shabanowitz J, Hunt DF, Pemberton LF (2001) Nuclear import of histone H2A and H2B is mediated by a network of karyopherins. J Cell Biol 153(2):251–262PubMedGoogle Scholar
  124. Mosammaparast N, Ewart CS, Pemberton LF (2002a) A role for nucleosome assembly protein 1 in the nuclear transport of histones H2A and H2B. EMBO J 21(23):6527–6538PubMedGoogle Scholar
  125. Mosammaparast N, Guo Y, Shabanowitz J, Hunt DF, Pemberton LF (2002b) Pathways mediating the nuclear import of histones H3 and H4 in yeast. J Biol Chem 277(1):862–868. doi: 10.1074/jbc.M106845200, M106845200 [pii]PubMedGoogle Scholar
  126. Murzina N, Verreault A, Laue E, Stillman B (1999) Heterochromatin dynamics in mouse cells: interaction between chromatin assembly factor 1 and HP1 proteins. Mol Cell 4(4):529–540PubMedGoogle Scholar
  127. Nabatiyan A, Krude T (2004) Silencing of chromatin assembly factor 1 in human cells leads to cell death and loss of chromatin assembly during DNA synthesis. Mol Cell Biol 24(7):2853–2862PubMedGoogle Scholar
  128. Nair DM, Ge Z, Mersfelder EL, Parthun MR (2011) Genetic interactions between POB3 and the acetylation of newly synthesized histones. Curr Genet 57(4):271–286. doi: 10.1007/s00294-011-0347-1 PubMedGoogle Scholar
  129. Nakayama T, Nishioka K, Dong YX, Shimojima T, Hirose S (2007) Drosophila GAGA factor directs histone H3.3 replacement that prevents the heterochromatin spreading. Genes Dev 21(5):552–561. doi: 10.1101/gad.1503407, 21/5/552 [pii]PubMedGoogle Scholar
  130. 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(7133):338–341. doi: 10.1038/nature05613, nature05613 [pii]PubMedGoogle Scholar
  131. Neumann H, Hancock SM, Buning R, Routh A, Chapman L, Somers J, Owen-Hughes T, van Noort J, Rhodes D, Chin JW (2009) A method for genetically installing site-specific acetylation in recombinant histones defines the effects of H3 K56 acetylation. Mol Cell 36(1): 153–163. doi: 10.1016/j.molcel.2009.07.027, S1097-2765(09)00582-6 [pii]PubMedGoogle Scholar
  132. Okuhara K, Ohta K, Seo H, Shioda M, Yamada T, Tanaka Y, Dohmae N, Seyama Y, Shibata T, Murofushi H (1999) A DNA unwinding factor involved in DNA replication in cell-free extracts of Xenopus eggs. Curr Biol 9(7):341–350, S0960-9822(99)80160-2 [pii]PubMedGoogle Scholar
  133. Orphanides G, Wu WH, Lane WS, Hampsey M, Reinberg D (1999) The chromatin-specific transcription elongation factor FACT comprises human SPT16 and SSRP1 proteins. Nature 400(6741):284–288PubMedGoogle Scholar
  134. Osley MA (1991) The regulation of histone synthesis in the cell cycle. Annu Rev Biochem 60:827–861PubMedGoogle Scholar
  135. Park YJ, Chodaparambil JV, Bao Y, McBryant SJ, Luger K (2005) Nucleosome assembly protein 1 exchanges histone H2A-H2B dimers and assists nucleosome sliding. J Biol Chem 280(3): 1817–1825. doi: 10.1074/jbc.M411347200, M411347200 [pii]PubMedGoogle Scholar
  136. Pearson CG, Yeh E, Gardner M, Odde D, Salmon ED, Bloom K (2004) Stable kinetochore-microtubule attachment constrains centromere positioning in metaphase. Curr Biol 14(21): 1962–1967. doi: 10.1016/j.cub.2004.09.086, S0960982204007493 [pii]PubMedGoogle Scholar
  137. Pidoux AL, Choi ES, Abbott JK, Liu X, Kagansky A, Castillo AG, Hamilton GL, Richardson W, Rappsilber J, He X, Allshire RC (2009) Fission yeast Scm3: A CENP-A receptor required for integrity of subkinetochore chromatin. Mol Cell 33(3):299–311. doi: 10.1016/j.molcel.2009.01.019, S1097-2765(09)00063-X [pii]PubMedGoogle Scholar
  138. Polo SE, Roche D, Almouzni G (2006) New histone incorporation marks sites of UV repair in human cells. Cell 127(3):481–493PubMedGoogle Scholar
  139. Quivy JP, Gerard A, Cook AJ, Roche D, Almouzni G (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(9):972–979PubMedGoogle Scholar
  140. Ransom M, Williams SK, Dechassa ML, Das C, Linger J, Adkins M, Liu C, Bartholomew B, Tyler JK (2009) FACT and the proteasome promote promoter chromatin disassembly and transcriptional initiation. J Biol Chem 284(35):23461–23471. doi: 10.1074/jbc.M109.019562, M109.019562 [pii]PubMedGoogle Scholar
  141. Ray-Gallet D, Quivy JP, Sillje HW, Nigg EA, Almouzni G (2007) The histone chaperone Asf1 is dispensable for direct de novo histone deposition in Xenopus egg extracts. Chromosoma 116(5):487–496. doi: 10.1007/s00412-007-0112-x PubMedGoogle Scholar
  142. Ray-Gallet D, Woolfe A, Vassias I, Pellentz C, Lacoste N, Puri A, Schultz DC, Pchelintsev NA, Adams PD, Jansen LE, Almouzni G (2011) Dynamics of histone H3 deposition in vivo reveal a nucleosome gap-filling mechanism for H3.3 to maintain chromatin integrity. Mol Cell 44(6):928–941. doi: 10.1016/j.molcel.2011.12.006, S1097-2765(11)00945-2 [pii]PubMedGoogle Scholar
  143. Recht J, Tsubota T, Tanny JC, Diaz RL, Berger JM, Zhang X, Garcia BA, Shabanowitz J, Burlingame AL, Hunt DF, Kaufman PD, Allis CD (2006) Histone chaperone Asf1 is required for histone H3 lysine 56 acetylation, a modification associated with S phase in mitosis and meiosis. Proc Natl Acad Sci USA 103(18):6988–6993. doi: 10.1073/pnas.0601676103, 0601676103 [pii]PubMedGoogle Scholar
  144. Reese BE, Bachman KE, Baylin SB, Rountree MR (2003) The methyl-CpG binding protein MBD1 interacts with the p150 subunit of chromatin assembly factor 1. Mol Cell Biol 23(9):3226–3236PubMedGoogle Scholar
  145. Rhoades AR, Ruone S, Formosa T (2004) Structural features of nucleosomes reorganized by yeast FACT and its HMG box component, Nhp6. Mol Cell Biol 24(9):3907–3917PubMedGoogle Scholar
  146. Robinson KM, Schultz MC (2003) Replication-independent assembly of nucleosome arrays in a novel yeast chromatin reconstitution system involves antisilencing factor Asf1p and chromodomain protein Chd1p. Mol Cell Biol 23(22):7937–7946PubMedGoogle Scholar
  147. Rufiange A, Jacques PE, Bhat W, Robert F, Nourani A (2007) Genome-wide replication-independent histone H3 exchange occurs predominantly at promoters and implicates H3 K56 acetylation and Asf1. Mol Cell 27(3):393–405PubMedGoogle Scholar
  148. Sanematsu F, Takami Y, Barman HK, Fukagawa T, Ono T, Shibahara KI, Nakayama T (2006) Asf1 is required for viability and chromatin assembly during DNA replication in vertebrate cells. J Biol Chem 281(19):13817–13827PubMedGoogle Scholar
  149. Santisteban MS, Kalashnikova T, Smith MM (2000) Histone H2A.Z regulats transcription and is partially redundant with nucleosome remodeling complexes. Cell 103(3):411–422PubMedGoogle Scholar
  150. Santisteban MS, Hang M, Smith MM (2011) Histone variant H2A.Z and RNA polymerase II transcription elongation. Mol Cell Biol 31(9):1848–1860. doi: 10.1128/MCB.01346-10, MCB.01346-10 [pii]PubMedGoogle Scholar
  151. Sarraf SA, Stancheva I (2004) Methyl-CpG binding protein MBD1 couples histone H3 methylation at lysine 9 by SETDB1 to DNA replication and chromatin assembly. Mol Cell 15(4):595–605PubMedGoogle Scholar
  152. Saunders A, Werner J, Andrulis ED, Nakayama T, Hirose S, Reinberg D, Lis JT (2003) Tracking FACT and the RNA polymerase II elongation complex through chromatin in vivo. Science 301(5636):1094–1096PubMedGoogle Scholar
  153. Scharf AN, Barth TK, Imhof A (2009) Establishment of histone modifications after chromatin assembly. Nucleic Acids Res 37(15):5032–5040. doi: 10.1093/nar/gkp518, gkp518 [pii]PubMedGoogle Scholar
  154. Schermer UJ, Korber P, Horz W (2005) Histones are incorporated in trans during reassembly of the yeast PHO5 promoter. Mol Cell 19(2):279–285PubMedGoogle Scholar
  155. Schittenhelm RB, Althoff F, Heidmann S, Lehner CF (2010) Detrimental incorporation of excess Cenp-A/Cid and Cenp-C into Drosophila centromeres is prevented by limiting amounts of the bridging factor Cal1. J Cell Sci 123(Pt 21):3768–3779. doi: 10.1242/jcs.067934, jcs.067934 [pii]PubMedGoogle Scholar
  156. Schlaeger EJ, Knippers R (1979) DNA-histone interaction in the vicinity of replication points. Nucleic Acids Res 6(2):645–656PubMedGoogle Scholar
  157. Schlesinger MB, Formosa T (2000) POB3 is required for both transcription and replication in the yeast Saccharomyces cerevisiae. Genetics 155(4):1593–1606PubMedGoogle Scholar
  158. Schneider J, Bajwa P, Johnson FC, Bhaumik SR, Shilatifard A (2006) Rtt109 is required for proper H3K56 acetylation: a chromatin mark associated with the elongating RNA polymerase II. J Biol Chem 281(49):37270–37274PubMedGoogle Scholar
  159. Schuh M, Lehner CF, Heidmann S (2007) Incorporation of Drosophila CID/CENP-A and CENP-C into centromeres during early embryonic anaphase. Curr Biol 17(3):237–243. doi: 10.1016/j.cub.2006.11.051, S0960-9822(06)02569-3 [pii]PubMedGoogle Scholar
  160. Schulz LL, Tyler JK (2006) The histone chaperone ASF1 localizes to active DNA replication forks to mediate efficient DNA replication. FASEB J 20(3):488–490PubMedGoogle Scholar
  161. Schwabish MA, Struhl K (2006) Asf1 mediates histone eviction and deposition during elongation by RNA polymerase II. Mol Cell 22(3):415–422PubMedGoogle Scholar
  162. Schwartz BE, Ahmad K (2005) Transcriptional activation triggers deposition and removal of the histone variant H3.3. Genes Dev 19(7):804–814PubMedGoogle Scholar
  163. Seale RL (1975) Assembly of DNA and protein during replication in HeLa cells. Nature 255(5505):247–249PubMedGoogle Scholar
  164. Seale RL (1976) Studies on the mode of segregation of histone nu bodies during replication in HeLa cells. Cell 9(3):423–429, 0092-8674(76)90087-8 [pii]PubMedGoogle Scholar
  165. Senshu T, Fukuda M, Ohashi M (1978) Preferential association of newly synthesized H3 and H4 histones with newly replicated DNA. J Biochem 84(4):985–988PubMedGoogle Scholar
  166. Shelby RD, Monier K, Sullivan KF (2000) Chromatin assembly at kinetochores is uncoupled from DNA replication. J Cell Biol 151(5):1113–1118PubMedGoogle Scholar
  167. Shibahara K, Stillman B (1999) Replication-dependent marking of DNA by PCNA facilitates CAF-1-coupled inheritance of chromatin. Cell 96(4):575–585PubMedGoogle Scholar
  168. Shimko JC, North JA, Bruns AN, Poirier MG, Ottesen JJ (2011) Preparation of fully synthetic histone H3 reveals that acetyl-lysine 56 facilitates protein binding within nucleosomes. J Mol Biol 408(2):187–204. doi: 10.1016/j.jmb.2011.01.003, S0022-2836(11)00020-9 [pii]PubMedGoogle Scholar
  169. Shimojima T, Okada M, Nakayama T, Ueda H, Okawa K, Iwamatsu A, Handa H, Hirose S (2003) Drosophila FACT contributes to Hox gene expression through physical and functional interactions with GAGA factor. Genes Dev 17(13):1605–1616. doi: 10.1101/gad.1086803, 1086803 [pii]PubMedGoogle Scholar
  170. Shintomi K, Iwabuchi M, Saeki H, Ura K, Kishimoto T, Ohsumi K (2005) Nucleosome assembly protein-1 is a linker histone chaperone in Xenopus eggs. Proc Natl Acad Sci USA 102(23): 8210–8215. doi: 10.1073/pnas.0500822102, 0500822102 [pii]PubMedGoogle Scholar
  171. Shivaraju M, Unruh JR, Slaughter BD, Mattingly M, Berman J, Gerton JL (2012) Cell-cycle-coupled structural oscillation of centromeric nucleosomes in yeast. Cell 150(2):304–316. doi: 10.1016/j.cell.2012.05.034, S0092-8674(12)00704-0 [pii]PubMedGoogle Scholar
  172. 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. Proc Natl Acad Sci USA 107(4):1349–1354. doi: 10.1073/pnas.0913709107, 0913709107 [pii]PubMedGoogle Scholar
  173. Silva AC, Xu X, Kim HS, Fillingham J, Kislinger T, Mennella TA, Keogh MC (2012) The replication-independent histone H3-H4 chaperones HIR, ASF1, and RTT106 co-operate to maintain promoter fidelity. J Biol Chem 287(3):1709–1718. doi: 10.1074/jbc.M111.316489, M111.316489 [pii]PubMedGoogle Scholar
  174. Singer MS, Kahana A, Wolf AJ, Meisinger LL, Peterson SE, Goggin C, Mahowald M, Gottschling DE (1998) Identification of high-copy disruptors of telomeric silencing in Saccharomyces cerevisiae. Genetics 150(2):613–632PubMedGoogle Scholar
  175. Smerdon MJ (1991) DNA repair and the role of chromatin structure. Curr Opin Cell Biol 3(3): 422–428PubMedGoogle Scholar
  176. 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(1):15–25PubMedGoogle Scholar
  177. Smith PA, Jackson V, Chalkley R (1984) Two-stage maturation process for newly replicated chromatin. Biochemistry 23(7):1576–1581PubMedGoogle Scholar
  178. Sogo JM, Stahl H, Koller T, Knippers R (1986) Structure of replicating simian virus 40 minichromosomes. The replication fork, core histone segregation and terminal structures. J Mol Biol 189(1):189–204PubMedGoogle Scholar
  179. Stephens GE, Slawson EE, Craig CA, Elgin SC (2005) Interaction of heterochromatin protein 2 with HP1 defines a novel HP1-binding domain. Biochemistry 44(40):13394–13403. doi: 10.1021/bi051006+ PubMedGoogle Scholar
  180. Stephens GE, Xiao H, Lankenau DH, Wu C, Elgin SC (2006) Heterochromatin protein 2 interacts with Nap-1 and NURF: a link between heterochromatin-induced gene silencing and the chromatin remodeling machinery in Drosophila. Biochemistry 45(50):14990–14999. doi: 10.1021/bi060983y PubMedGoogle Scholar
  181. 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. Proc Natl Acad Sci USA 104(25):10571–10576. doi: 10.1073/pnas.0703178104, 0703178104 [pii]PubMedGoogle Scholar
  182. Straube K, Blackwell JS Jr, Pemberton LF (2010) Nap1 and Chz1 have separate Htz1 nuclear import and assembly functions. Traffic 11(2):185–197. doi: 10.1111/j.1600-0854.2009.01010.x, TRA1010 [pii]PubMedGoogle Scholar
  183. Su D, Hu Q, Li Q, Thompson JR, Cui G, Fazly A, Davies BA, Botuyan MV, Zhang Z, Mer G (2012) Structural basis for recognition of H3K56-acetylated histone H3-H4 by the chaperone Rtt106. Nature 483(7387):104–107. doi: 10.1038/nature10861, nature10861 [pii]PubMedGoogle Scholar
  184. 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(1):51–61PubMedGoogle Scholar
  185. Takahata S, Yu Y, Stillman DJ (2009) FACT and Asf1 regulate nucleosome dynamics and coactivator binding at the HO promoter. Mol Cell 34(4):405–415. doi: 10.1016/j.molcel.2009.04.010, S1097-2765(09)00239-1 [pii]PubMedGoogle Scholar
  186. Takami Y, Ono T, Fukagawa T, Shibahara K, Nakayama T (2007) Essential role of chromatin assembly factor-1-mediated rapid nucleosome assembly for DNA replication and cell division in vertebrate cells. Mol Biol Cell 18(1):129–141. doi: 10.1091/mbc.E06-05-0426, E06-05-0426 [pii]PubMedGoogle Scholar
  187. Takayama Y, Sato H, Saitoh S, Ogiyama Y, Masuda F, Takahashi K (2008) Biphasic incorporation of centromeric histone CENP-A in fission yeast. Mol Biol Cell 19(2):682–690. doi: 10.1091/mbc.E07-05-0504, E07-05-0504 [pii]PubMedGoogle Scholar
  188. 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(17):3975–3985. doi: 10.1038/sj.emboj.7601271, 7601271 [pii]PubMedGoogle Scholar
  189. Tang J, Wu S, Liu H, Stratt R, Barak OG, Shiekhattar R, Picketts DJ, Yang X (2004) A novel transcription regulatory complex containing death domain-associated protein and the ATR-X syndrome protein. J Biol Chem 279(19):20369–20377. doi: 10.1074/jbc.M401321200, M401321200 [pii]PubMedGoogle Scholar
  190. Tang Y, Poustovoitov MV, Zhao K, Garfinkel M, Canutescu A, Dunbrack R, Adams PD, Marmorstein R (2006) Structure of a human ASF1a-HIRA complex and insights into specificity of histone chaperone complex assembly. Nat Struct Mol Biol 13(10):921–929PubMedGoogle Scholar
  191. Torigoe SE, Urwin DL, Ishii H, Smith DE, Kadonaga JT (2011) Identification of a rapidly formed nonnucleosomal histone-DNA intermediate that is converted into chromatin by ACF. Mol Cell 43(4):638–648. doi: 10.1016/j.molcel.2011.07.017, S1097-2765(11)00541-7 [pii]PubMedGoogle Scholar
  192. Tsubota T, Berndsen CE, Erkmann JA, Smith CL, Yang L, Freitas MA, Denu JM, Kaufman PD (2007) Histone H3-K56 acetylation is catalyzed by histone chaperone-dependent complexes. Mol Cell 25(5):703–712PubMedGoogle Scholar
  193. Tsukiyama T, Wu C (1995) Purification and properties of an ATP-dependent nucleosome remodeling factor. Cell 83(6):1011–1020PubMedGoogle Scholar
  194. Tyler JK (2002) Chromatin assembly. Cooperation between histone chaperones and ATP-dependent nucleosome remodeling machines. Eur J Biochem 269(9):2268–2274PubMedGoogle Scholar
  195. 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(6761): 555–560PubMedGoogle Scholar
  196. van Attikum H, Fritsch O, Hohn B, Gasser SM (2004) Recruitment of the INO80 complex by H2A phosphorylation links ATP-dependent chromatin remodeling with DNA double-strand break repair. Cell 119(6):777–788PubMedGoogle Scholar
  197. VanDemark AP, Blanksma M, Ferris E, Heroux A, Hill CP, Formosa T (2006) The structure of the yFACT Pob3-M domain, its interaction with the DNA replication factor RPA, and a potential role in nucleosome deposition. Mol Cell 22(3):363–374. doi: 10.1016/j.molcel.2006.03.025, S1097-2765(06)00191-2 [pii]PubMedGoogle Scholar
  198. Venkatesh S, Smolle M, Li H, Gogol MM, Saint M, Kumar S, Natarajan K, Workman JL (2012) Set2 methylation of histone H3 lysine 36 suppresses histone exchange on transcribed genes. Nature 489(7416):452–455. doi: 10.1038/nature11326, nature11326 [pii]PubMedGoogle Scholar
  199. Vermaak D, Hayden HS, Henikoff S (2002) Centromere targeting element within the histone fold domain of Cid. Mol Cell Biol 22(21):7553–7561PubMedGoogle Scholar
  200. 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(2):660–669. doi: 10.1093/nar/gkr781, gkr781 [pii]PubMedGoogle Scholar
  201. Weber CM, Henikoff JG, Henikoff S (2010) H2A.Z nucleosomes enriched over active genes are homotypic. Nat Struct Mol Biol 17(12):1500–1507. doi: 10.1038/nsmb.1926, nsmb.1926 [pii]PubMedGoogle Scholar
  202. Williams SK, Truong D, Tyler JK (2008) Acetylation in the globular core of histone H3 on lysine-56 promotes chromatin disassembly during transcriptional activation. Proc Natl Acad Sci USA 105(26):9000–9005. doi: 10.1073/pnas.0800057105, 0800057105 [pii]PubMedGoogle Scholar
  203. Williams JS, Hayashi T, Yanagida M, Russell P (2009) Fission yeast Scm3 mediates stable assembly of Cnp1/CENP-A into centromeric chromatin. Mol Cell 33(3):287–298. doi: 10.1016/j.molcel.2009.01.017, S1097-2765(09)00061-6 [pii]PubMedGoogle Scholar
  204. Winkler DD, Muthurajan UM, Hieb AR, Luger K (2011) Histone chaperone FACT coordinates nucleosome interaction through multiple synergistic binding events. J Biol Chem 286(48): 41883–41892. doi: 10.1074/jbc.M111.301465, M111.301465 [pii]PubMedGoogle Scholar
  205. Winkler DD, Zhou H, Dar MA, Zhang Z, Luger K (2012) Yeast CAF-1 assembles histone (H3-H4)2 tetramers prior to DNA deposition. Nucleic Acids Res. doi: 10.1093/nar/gks812, gks812 [pii]Google Scholar
  206. Wittmeyer J, Formosa T (1997) The Saccharomyces cerevisiae DNA polymerase alpha catalytic subunit interacts with Cdc68/Spt16 and with Pob3, a protein similar to an HMG1-like protein. Mol Cell Biol 17(7):4178–4190PubMedGoogle Scholar
  207. Wong LH, McGhie JD, Sim M, Anderson MA, Ahn S, Hannan RD, George AJ, Morgan KA, Mann JR, Choo KH (2010) ATRX interacts with H3.3 in maintaining telomere structural integrity in pluripotent embryonic stem cells. Genome Res 20(3):351–360. doi: 10.1101/gr.101477.109, gr.101477.109 [pii]PubMedGoogle Scholar
  208. Xiao H, Mizuguchi G, Wisniewski J, Huang Y, Wei D, Wu C (2011) Nonhistone Scm3 binds to AT-rich DNA to organize atypical centromeric nucleosome of budding yeast. Mol Cell 43(3): 369–380. doi: 10.1016/j.molcel.2011.07.009, S1097-2765(11)00531-4 [pii]PubMedGoogle Scholar
  209. Xin H, Takahata S, Blanksma M, McCullough L, Stillman DJ, Formosa T (2009) yFACT induces global accessibility of nucleosomal DNA without H2A-H2B displacement. Mol Cell 35(3): 365–376. doi: 10.1016/j.molcel.2009.06.024, S1097-2765(09)00462-6 [pii]PubMedGoogle Scholar
  210. Xu F, Zhang K, Grunstein M (2005) Acetylation in histone H3 globular domain regulates gene expression in yeast. Cell 121(3):375–385PubMedGoogle Scholar
  211. 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(5974):94–98. doi: 10.1126/ science.1178994, 328/5974/94 [pii]Google Scholar
  212. Xu Y, Ayrapetov MK, Xu C, Gursoy-Yuzugullu O, Hu Y, Price BD (2012) Histone H2A.Z controls a critical chromatin remodeling step required for DNA double-strand break repair. Mol Cell 48(5):723–733. doi: 10.1016/j.molcel.2012.09.026, S1097-2765(12)00826-X [pii]PubMedGoogle Scholar
  213. Xue Y, Gibbons R, Yan Z, Yang D, McDowell TL, Sechi S, Qin J, Zhou S, Higgs D, Wang W (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(19): 10635–10640. doi: 10.1073/pnas.1937626100, 1937626100 [pii]PubMedGoogle Scholar
  214. Zhang H, Han J, Kang B, Burgess R, Zhang Z (2012) Human histone acetyltransferase 1 protein preferentially acetylates H4 histone molecules in H3.1-H4 over H3.3-H4. J Biol Chem 287(9):6573–6581. doi: 10.1074/jbc.M111.312637, M111.312637 [pii]PubMedGoogle Scholar
  215. Zhou Z, Feng H, Zhou BR, Ghirlando R, Hu K, Zwolak A, Miller Jenkins LM, Xiao H, Tjandra N, Wu C, Bai Y (2011) Structural basis for recognition of centromere histone variant CenH3 by the chaperone Scm3. Nature 472(7342):234–237. doi: 10.1038/nature09854, nature09854 [pii]PubMedGoogle Scholar
  216. Zunder RM, Antczak AJ, Berger JM, Rine J (2012) Two surfaces on the histone chaperone Rtt106 mediate histone binding, replication, and silencing. Proc Natl Acad Sci USA 109(3):E144–E153. doi: 10.1073/pnas.1119095109, 1119095109 [pii]PubMedGoogle Scholar

Copyright information

© Springer Science+Business Media New York 2014

Authors and Affiliations

  1. 1.Department of Biochemistry and Molecular BiologyMD Anderson Cancer CenterHoustonUSA

Personalised recommendations