Histone chaperones: an escort network regulating histone traffic (original) (raw)

• Kornberg, R.D. Structure of chromatin. Annu. Rev. Biochem. 46, 931–954 (1977).
  Article CAS PubMed Google Scholar
• Oudet, P., Gross-Bellard, M. & Chambon, P. Electron microscopic and biochemical evidence that chromatin structure is a repeating unit. Cell 4, 281–300 (1975).
  CAS PubMed Google Scholar
• Luger, K., Mader, A.W., Richmond, R.K., Sargent, D.F. & Richmond, T.J. Crystal structure of the nucleosome core particle at 2.8 Å resolution. Nature 389, 251–260 (1997).
  Article CAS PubMed Google Scholar
• Woodland, H.R. & Adamson, E.D. The synthesis and storage of histones during the oogenesis of Xenopus laevis. Dev. Biol. 57, 118–135 (1977).
  CAS PubMed Google Scholar
• Loyola, A. & Almouzni, G. Histone chaperones, a supporting role in the limelight. Biochim. Biophys. Acta 1677, 3–11 (2004).
  CAS PubMed Google Scholar
• Laskey, R.A., Mills, A.D. & Morris, N.R. Assembly of SV40 chromatin in a cell-free system from Xenopus eggs. Cell 10, 237–243 (1977).
  CAS PubMed Google Scholar
• Stillman, B. Chromatin assembly during SV40 DNA replication in vitro. Cell 45, 555–565 (1986).
  CAS PubMed Google Scholar
• Smith, S. & Stillman, B. Purification and characterization of CAF-I, a human cell factor required for chromatin assembly during DNA replication in vitro. Cell 58, 15–25 (1989).
  CAS PubMed Google Scholar
• Ray-Gallet, D. & Almouzni, G. DNA synthesis-dependent and -independent chromatin assembly pathways in Xenopus egg extracts. Methods Enzymol. 375, 117–131 (2004).
  CAS PubMed Google Scholar
• Quivy, J.P., Grandi, P. & Almouzni, G. Dimerization of the largest subunit of chromatin assembly factor 1: importance in vitro and during Xenopus early development. EMBO J. 20, 2015–2027 (2001).
  CAS PubMed PubMed Central Google Scholar
• Ray-Gallet, D. et al. HIRA is critical for a nucleosome assembly pathway independent of DNA synthesis. Mol. Cell 9, 1091–1100 (2002).
  CAS PubMed Google Scholar
• Mello, J.A. et al. Human Asf1 and CAF-1 interact and synergize in a repair-coupled nucleosome assembly pathway. EMBO Rep. 3, 329–334 (2002).
  CAS PubMed PubMed Central Google Scholar
• Ray-Gallet, D., Quivy, J.P., Sillje, H.W., Nigg, E.A. & Almouzni, G. The histone chaperone Asf1 is dispensable for direct de novo histone deposition in Xenopus egg extracts. Chromosoma 116, 487–496 (2007).
  CAS PubMed Google Scholar
• Polo, S.E. & Almouzni, G. Chromatin assembly: a basic recipe with various flavours. Curr. Opin. Genet. Dev. 16, 104–111 (2006).
  CAS PubMed Google Scholar
• Harata, M. et al. The nuclear actin-related protein of Saccharomyces cerevisiae, Act3p/Arp4, interacts with core histones. Mol. Biol. Cell 10, 2595–2605 (1999).
  CAS PubMed PubMed Central Google Scholar
• Luk, E. et al. Chz1, a nuclear chaperone for histone H2AZ. Mol. Cell 25, 357–368 (2007).
  CAS PubMed Google Scholar
• Loyola, A. & Almouzni, G. Marking histone H3 variants: how, when and why? Trends Biochem. Sci. 32, 425–433 (2007).
  CAS PubMed Google Scholar
• Tagami, H., Ray-Gallet, D., Almouzni, G. & Nakatani, Y. Histone H3.1 and H3.3 complexes mediate nucleosome assembly pathways dependent or independent of DNA synthesis. Cell 116, 51–61 (2004).
  CAS PubMed Google Scholar
• Richardson, R.T. et al. Characterization of the histone H1-binding protein, NASP, as a cell cycle-regulated somatic protein. J. Biol. Chem. 275, 30378–30386 (2000).
  CAS PubMed Google Scholar
• Shintomi, K. et al. Nucleosome assembly protein-1 is a linker histone chaperone in Xenopus eggs. Proc. Natl. Acad. Sci. USA 102, 8210–8215 (2005).
  CAS PubMed PubMed Central Google Scholar
• Dutta, S. et al. The crystal structure of nucleoplasmin-core: implications for histone binding and nucleosome assembly. Mol. Cell 8, 841–853 (2001).
  CAS PubMed Google Scholar
• Mousson, F., Ochsenbein, F. & Mann, C. The histone chaperone Asf1 at the crossroads of chromatin and DNA checkpoint pathways. Chromosoma 116, 79–93 (2007).
  CAS PubMed Google Scholar
• Park, Y.J. & Luger, K. The structure of nucleosome assembly protein 1. Proc. Natl. Acad. Sci. USA 103, 1248–1253 (2006).
  CAS PubMed PubMed Central Google Scholar
• Belotserkovskaya, R. et al. FACT facilitates transcription-dependent nucleosome alteration. Science 301, 1090–1093 (2003).
  CAS PubMed Google Scholar
• Angelov, D. et al. Nucleolin is a histone chaperone with FACT-like activity and assists remodeling of nucleosomes. EMBO J. 25, 1669–1679 (2006).
  CAS PubMed PubMed Central Google Scholar
• Daganzo, S.M. et al. Structure and function of the conserved core of histone deposition protein Asf1. Curr. Biol. 13, 2148–2158 (2003).
  CAS PubMed Google Scholar
• Muto, S. et al. Relationship between the structure of SET/TAF-Iβ/INHAT and its histone chaperone activity. Proc. Natl. Acad. Sci. USA 104, 4285–4290 (2007).
  CAS PubMed PubMed Central Google Scholar
• Umehara, T., Chimura, T., Ichikawa, N. & Horikoshi, M. Polyanionic stretch-deleted histone chaperone cia1/Asf1p is functional both in vivo and in vitro. Genes Cells 7, 59–73 (2002).
  CAS PubMed Google Scholar
• Regnard, C. et al. Polyglutamylation of nucleosome assembly proteins. J. Biol. Chem. 275, 15969–15976 (2000).
  CAS PubMed Google Scholar
• Namboodiri, V.M., Dutta, S., Akey, I.V., Head, J.F. & Akey, C.W. The crystal structure of Drosophila NLP-core provides insight into pentamer formation and histone binding. Structure 11, 175–186 (2003).
  CAS PubMed Google Scholar
• Mousson, F. et al. Structural basis for the interaction of Asf1 with histone H3 and its functional implications. Proc. Natl. Acad. Sci. USA 102, 5975–5980 (2005).
  CAS PubMed PubMed Central Google Scholar
• DeSilva, H., Lee, K. & Osley, M.A. Functional dissection of yeast Hir1p, a WD repeat-containing transcriptional corepressor. Genetics 148, 657–667 (1998).
  CAS PubMed PubMed Central Google Scholar
• Kaufman, P.D., Kobayashi, R., Kessler, N. & Stillman, B. The p150 and p60 subunits of chromatin assembly factor I: a molecular link between newly synthesized histones and DNA replication. Cell 81, 1105–1114 (1995).
  CAS PubMed Google Scholar
• Verreault, A., Kaufman, P.D., Kobayashi, R. & Stillman, B. Nucleosome assembly by a complex of CAF-1 and acetylated histones H3/H4. Cell 87, 95–104 (1996).
  CAS PubMed Google Scholar
• Agez, M. et al. Structure of the histone chaperone ASF1 bound to the histone H3 C-terminal helix and functional insights. Structure 15, 191–199 (2007).
  CAS PubMed Google Scholar
• Antczak, A.J., Tsubota, T., Kaufman, P.D. & Berger, J.M. Structure of the yeast histone H3–ASF1 interaction: implications for chaperone mechanism, species-specific interactions, and epigenetics. BMC Struct. Biol. 6, 26 (2006).
  PubMed PubMed Central Google Scholar
• English, C.M., Adkins, M.W., Carson, J.J., Churchill, M.E. & Tyler, J.K. Structural basis for the histone chaperone activity of Asf1. Cell 127, 495–508 (2006).
  CAS PubMed PubMed Central Google Scholar
• Natsume, R. et al. Structure and function of the histone chaperone CIA/ASF1 complexed with histones H3 and H4. Nature 446, 338–341 (2007).
  CAS PubMed Google Scholar
• English, C.M., Maluf, N.K., Tripet, B., Churchill, M.E. & Tyler, J.K. ASF1 binds to a heterodimer of histones H3 and H4: a two-step mechanism for the assembly of the H3–H4 heterotetramer on DNA. Biochemistry 44, 13673–13682 (2005).
  CAS PubMed Google Scholar
• Schwabish, M.A. & Struhl, K. Asf1 mediates histone eviction and deposition during elongation by RNA polymerase II. Mol. Cell 22, 415–422 (2006).
  CAS PubMed Google Scholar
• Adkins, M.W., Howar, S.R. & Tyler, J.K. Chromatin disassembly mediated by the histone chaperone Asf1 is essential for transcriptional activation of the yeast PHO5 and PHO8 genes. Mol. Cell 14, 657–666 (2004).
  CAS PubMed Google Scholar
• Tamburini, B.A., Carson, J.J., Adkins, M.W. & Tyler, J.K. Functional conservation and specialization among eukaryotic anti-silencing function 1 histone chaperones. Eukaryot. Cell 4, 1583–1590 (2005).
  CAS PubMed PubMed Central Google Scholar
• Tang, Y. et al. Structure of a human ASF1a-HIRA complex and insights into specificity of histone chaperone complex assembly. Nat. Struct. Mol. Biol. 13, 921–929 (2006).
  CAS PubMed PubMed Central Google Scholar
• Sillje, H.H. & Nigg, E.A. Identification of human Asf1 chromatin assembly factors as substrates of Tousled-like kinases. Curr. Biol. 11, 1068–1073 (2001).
  CAS PubMed Google Scholar
• Driscoll, R., Hudson, A. & Jackson, S.P. Yeast Rtt109 promotes genome stability by acetylating histone H3 on lysine 56. Science 315, 649–652 (2007).
  CAS PubMed PubMed Central Google Scholar
• Han, J. et al. Rtt109 acetylates histone H3 lysine 56 and functions in DNA replication. Science 315, 653–655 (2007).
  CAS PubMed Google Scholar
• Tsubota, T. et al. Histone H3–K56 acetylation is catalyzed by histone chaperone-dependent complexes. Mol. Cell 25, 703–712 (2007).
  CAS PubMed PubMed Central Google Scholar
• Adkins, M.W., Carson, J.J., English, C.M., Ramey, C.J. & Tyler, J.K. The histone chaperone anti-silencing function 1 stimulates the acetylation of newly synthesized histone H3 in S-phase. J. Biol. Chem. 282, 1334–1340 (2007).
  CAS PubMed Google Scholar
• Recht, J. et al. 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, 6988–6993 (2006).
  CAS PubMed PubMed Central Google Scholar
• Schneider, J., Bajwa, P., Johnson, F.C., Bhaumik, S.R. & Shilatifard, A. Rtt109 is required for proper H3K56 acetylation: a chromatin mark associated with the elongating RNA polymerase II. J. Biol. Chem. 281, 37270–37274 (2006).
  CAS PubMed Google Scholar
• Xhemalce, B. et al. Regulation of histone H3 lysine 56 acetylation in Schizosaccharomyces pombe. J. Biol. Chem. 282, 15040–15047 (2007).
  CAS PubMed Google Scholar
• Morris, S.A. et al. Identification of histone H3 lysine 36 acetylation as a highly conserved histone modification. J. Biol. Chem. 282, 7632–7640 (2007).
  CAS PubMed Google Scholar
• Lorain, S. et al. Core histones and HIRIP3, a novel histone-binding protein, directly interact with WD repeat protein HIRA. Mol. Cell. Biol. 18, 5546–5556 (1998).
  CAS PubMed PubMed Central Google Scholar
• Sharp, J.A., Fouts, E.T., Krawitz, D.C. & Kaufman, P.D. Yeast histone deposition protein Asf1p requires Hir proteins and PCNA for heterochromatic silencing. Curr. Biol. 11, 463–473 (2001).
  CAS PubMed Google Scholar
• Zhang, R. et al. Formation of MacroH2A-containing senescence-associated heterochromatin foci and senescence driven by ASF1a and HIRA. Dev. Cell 8, 19–30 (2005).
  CAS PubMed Google Scholar
• Tyler, J.K. et al. Interaction between the Drosophila CAF-1 and ASF1 chromatin assembly factors. Mol. Cell. Biol. 21, 6574–6584 (2001).
  CAS PubMed PubMed Central Google Scholar
• Sanematsu, F. et al. Asf1 is required for viability and chromatin assembly during DNA replication in vertebrate cells. J. Biol. Chem. 281, 13817–13827 (2006).
  CAS PubMed Google Scholar
• Emili, A., Schieltz, D.M., Yates, J.R., III & Hartwell, L.H. Dynamic interaction of DNA damage checkpoint protein Rad53 with chromatin assembly factor Asf1. Mol. Cell 7, 13–20 (2001).
  CAS PubMed Google Scholar
• Hu, F., Alcasabas, A.A. & Elledge, S.J. Asf1 links Rad53 to control of chromatin assembly. Genes Dev. 15, 1061–1066 (2001).
  CAS PubMed PubMed Central Google Scholar
• Gunjan, A. & Verreault, A.A. Rad53 kinase-dependent surveillance mechanism that regulates histone protein levels in S. cerevisiae. Cell 115, 537–549 (2003).
  CAS PubMed Google Scholar
• Groth, A. et al. Human Asf1 regulates the flow of S phase histones during replicational stress. Mol. Cell 17, 301–311 (2005).
  CAS PubMed Google Scholar
• Polo, S.E. & Almouzni, G. Histone metabolic pathways and chromatin assembly factors as proliferation markers. Cancer Lett. 220, 1–9 (2005).
  CAS PubMed Google Scholar
• Groth, A., Rocha, W., Verreault, A. & Almouzni, G. Chromatin challenges during DNA replication and repair. Cell 128, 721–733 (2007).
  CAS PubMed Google Scholar
• Kulaeva, O.I., Gaykalova, D.A. & Studitsky, V.M. Transcription through chromatin by RNA polymerase II: histone displacement and exchange. Mutat. Res. 618, 116–129 (2007).
  CAS PubMed PubMed Central Google Scholar
• Li, B., Carey, M. & Workman, J.L. The role of chromatin during transcription. Cell 128, 707–719 (2007).
  CAS PubMed Google Scholar
• Workman, J.L. Nucleosome displacement in transcription. Genes Dev. 20, 2009–2017 (2006).
  CAS PubMed Google Scholar
• Krogan, N.J. et al. RNA polymerase II elongation factors of Saccharomyces cerevisiae: a targeted proteomics approach. Mol. Cell. Biol. 22, 6979–6992 (2002).
  CAS PubMed PubMed Central Google Scholar
• Bhaumik, S.R., Smith, E. & Shilatifard, A. Covalent modifications of histones during development and disease pathogenesis. Nat. Struct. Mol. Biol. 14, 1008–1016 (2007).
  CAS PubMed Google Scholar
• Masumoto, H., Hawke, D., Kobayashi, R. & Verreault, A. A role for cell-cycle-regulated histone H3 lysine 56 acetylation in the DNA damage response. Nature 436, 294–298 (2005).
  CAS PubMed Google Scholar
• Xu, F., Zhang, K. & Grunstein, M. Acetylation in histone H3 globular domain regulates gene expression in yeast. Cell 121, 375–385 (2005).
  CAS PubMed Google Scholar
• Han, J., Zhou, H., Li, Z., Xu, R.M. & Zhang, Z. The Rtt109-Vps75 histone acetyltransferase complex acetylates non-nucleosomal histone H3. J. Biol. Chem. 282, 14158–14164 (2007).
  CAS PubMed Google Scholar
• Duina, A.A. et al. Evidence that the localization of the elongation factor Spt16 across transcribed genes is dependent upon histone H3 integrity in Saccharomyces cerevisiae. Genetics 177, 101–112 (2007).
  CAS PubMed PubMed Central Google Scholar
• Adkins, M.W. & Tyler, J.K. Transcriptional activators are dispensable for transcription in the absence of Spt6-mediated chromatin reassembly of promoter regions. Mol. Cell 21, 405–416 (2006).
  CAS PubMed Google Scholar
• Kaplan, C.D., Laprade, L. & Winston, F. Transcription elongation factors repress transcription initiation from cryptic sites. Science 301, 1096–1099 (2003).
  CAS PubMed Google Scholar
• Cairns, B.R. Chromatin remodeling: insights and intrigue from single-molecule studies. Nat. Struct. Mol. Biol. 14, 989–996 (2007).
  CAS PubMed PubMed Central Google Scholar
• Saha, A., Wittmeyer, J. & Cairns, B.R. Chromatin remodelling: the industrial revolution of DNA around histones. Nat. Rev. Mol. Cell Biol. 7, 437–447 (2006).
  CAS PubMed Google Scholar
• Raisner, R.M. et al. Histone variant H2A.Z marks the 5′ ends of both active and inactive genes in euchromatin. Cell 123, 233–248 (2005).
  CAS PubMed PubMed Central Google Scholar
• Thiriet, C. & Hayes, J.J. Replication-independent core histone dynamics at transcriptionally active loci in vivo. Genes Dev. 19, 677–682 (2005).
  CAS PubMed PubMed Central Google Scholar
• Levchenko, V., Jackson, B. & Jackson, V. Histone release during transcription: displacement of the two H2A–H2B dimers in the nucleosome is dependent on different levels of transcription-induced positive stress. Biochemistry 44, 5357–5372 (2005).
  CAS PubMed Google Scholar
• Chen, H., Li, B. & Workman, J.L. A histone-binding protein, nucleoplasmin, stimulates transcription factor binding to nucleosomes and factor-induced nucleosome disassembly. EMBO J. 13, 380–390 (1994).
  CAS PubMed PubMed Central Google Scholar
• Walter, P.P., Owen-Hughes, T.A., Cote, J. & Workman, J.L. 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, 6178–6187 (1995).
  CAS PubMed PubMed Central Google Scholar
• Orphanides, G., LeRoy, G., Chang, C.H., Luse, D.S. & Reinberg, D. FACT, a factor that facilitates transcript elongation through nucleosomes. Cell 92, 105–116 (1998).
  CAS PubMed Google Scholar
• Orphanides, G., Wu, W.H., Lane, W.S., Hampsey, M. & Reinberg, D. The chromatin-specific transcription elongation factor FACT comprises human SPT16 and SSRP1 proteins. Nature 400, 284–288 (1999).
  CAS PubMed Google Scholar
• Ito, T., Ikehara, T., Nakagawa, T., Kraus, W.L. & Muramatsu, M. p300-mediated acetylation facilitates the transfer of histone H2A–H2B dimers from nucleosomes to a histone chaperone. Genes Dev. 14, 1899–1907 (2000).
  CAS PubMed PubMed Central Google Scholar
• Swaminathan, V., Kishore, A.H., Febitha, K.K. & Kundu, T.K. Human histone chaperone nucleophosmin enhances acetylation-dependent chromatin transcription. Mol. Cell. Biol. 25, 7534–7545 (2005).
  CAS PubMed PubMed Central Google Scholar
• Zlatanova, J., Seebart, C. & Tomschik, M. Nap1: taking a closer look at a juggler protein of extraordinary skills. FASEB J. 21, 1294–1310 (2007).
  CAS PubMed Google Scholar
• Korber, P. et al. The histone chaperone Asf1 increases the rate of histone eviction at the yeast PHO5 and PHO8 promoters. J. Biol. Chem. 281, 5539–5545 (2006).
  CAS PubMed Google Scholar
• Owen-Hughes, T. & Workman, J.L. Remodeling the chromatin structure of a nucleosome array by transcription factor-targeted trans-displacement of histones. EMBO J. 15, 4702–4712 (1996).
  CAS PubMed PubMed Central Google Scholar
• Jamai, A., Imoberdorf, R.M. & Strubin, M. Continuous histone H2B and transcription-dependent histone H3 exchange in yeast cells outside of replication. Mol. Cell 25, 345–355 (2007).
  CAS PubMed Google Scholar
• Dion, M.F. et al. Dynamics of replication-independent histone turnover in budding yeast. Science 315, 1405–1408 (2007).
  CAS PubMed Google Scholar
• Formosa, T. et al. Defects in SPT16 or POB3 (yFACT) in Saccharomyces cerevisiae cause dependence on the Hir/Hpc pathway: polymerase passage may degrade chromatin structure. Genetics 162, 1557–1571 (2002).
  CAS PubMed PubMed Central Google Scholar
• Schermer, U.J., Korber, P. & Horz, W. Histones are incorporated in trans during reassembly of the yeast PHO5 promoter. Mol. Cell 19, 279–285 (2005).
  CAS PubMed Google Scholar
• Endoh, M. et al. Human Spt6 stimulates transcription elongation by RNA polymerase II in vitro. Mol. Cell. Biol. 24, 3324–3336 (2004).
  CAS PubMed PubMed Central Google Scholar
• Chimura, T., Kuzuhara, T. & Horikoshi, M. Identification and characterization of CIA/ASF1 as an interactor of bromodomains associated with TFIID. Proc. Natl. Acad. Sci. USA 99, 9334–9339 (2002).
  CAS PubMed PubMed Central Google Scholar
• Simic, R. et al. Chromatin remodeling protein Chd1 interacts with transcription elongation factors and localizes to transcribed genes. EMBO J. 22, 1846–1856 (2003).
  CAS PubMed PubMed Central Google Scholar
• Konev, A.Y. et al. CHD1 motor protein is required for deposition of histone variant H3.3 into chromatin in vivo. Science 317, 1087–1090 (2007).
  CAS PubMed PubMed Central Google Scholar
• Brickner, D.G. et al. H2A.Z-mediatedlocalization of genes at the nuclear periphery confers epigenetic memory of previous transcriptional state. PLoS Biol. 5, e81 (2007).
  PubMed PubMed Central Google Scholar
• Leno, G.H., Mills, A.D., Philpott, A. & Laskey, R.A. Hyperphosphorylation of nucleoplasmin facilitates Xenopus sperm decondensation at fertilization. J. Biol. Chem. 271, 7253–7256 (1996).
  CAS PubMed Google Scholar
• Downs, J.A., Nussenzweig, M.C. & Nussenzweig, A. Chromatin dynamics and the preservation of genetic information. Nature 447, 951–958 (2007).
  CAS PubMed Google Scholar
• Bao, Y. & Shen, X. Chromatin remodeling in DNA double-strand break repair. Curr. Opin. Genet. Dev. 17, 126–131 (2007).
  CAS PubMed Google Scholar
• Altaf, M., Saksouk, N. & Cote, J. Histone modifications in response to DNA damage. Mutat. Res. 618, 81–90 (2007).
  CAS PubMed Google Scholar
• Osley, M.A., Tsukuda, T. & Nickoloff, J.A. ATP-dependent chromatin remodeling factors and DNA damage repair. Mutat. Res. 618, 65–80 (2007).
  CAS PubMed PubMed Central Google Scholar
• Rodrigue, A. et al. Interplay between human DNA repair proteins at a unique double-strand break in vivo. EMBO J. 25, 222–231 (2006).
  CAS PubMed PubMed Central Google Scholar
• Soutoglou, E. et al. Positional stability of single double-strand breaks in mammalian cells. Nat. Cell Biol. 9, 675–682 (2007).
  CAS PubMed PubMed Central Google Scholar
• Berkovich, E., Monnat, R.J. Jr. & Kastan, M.B. Roles of ATM and NBS1 in chromatin structure modulation and DNA double-strand break repair. Nat. Cell Biol. 9, 683–690 (2007).
  CAS PubMed Google Scholar
• Rogakou, E.P., Boon, C., Redon, C. & Bonner, W.M. Megabase chromatin domains involved in DNA double-strand breaks in vivo. J. Cell Biol. 146, 905–916 (1999).
  CAS PubMed PubMed Central Google Scholar
• Fillingham, J., Keogh, M.C. & Krogan, N.J. GammaH2AX and its role in DNA double-strand break repair. Biochem. Cell Biol. 84, 568–577 (2006).
  CAS PubMed Google Scholar
• Bewersdorf, J., Bennett, B.T. & Knight, K.L. H2AX chromatin structures and their response to DNA damage revealed by 4Pi microscopy. Proc. Natl. Acad. Sci. USA 103, 18137–18142 (2006).
  CAS PubMed PubMed Central Google Scholar
• Kent, N.A., Chambers, A.L. & Downs, J.A. Dual chromatin-remodelling roles for RSC during DNA double-strand break induction and repair at the yeast MAT locus. J. Biol. Chem. 282, 27693–27701 (2007).
  CAS PubMed Google Scholar
• Kim, J.A., Kruhlak, M., Dotiwala, F., Nussenzweig, A. & Haber, J.E. Heterochromatin is refractory to gamma-H2AX modification in yeast and mammals. J. Cell Biol. 178, 209–218 (2007).
  CAS PubMed PubMed Central Google Scholar
• Downs, J.A. et al. Binding of chromatin-modifying activities to phosphorylated histone H2A at DNA damage sites. Mol. Cell 16, 979–990 (2004).
  CAS PubMed Google Scholar
• Morrison, A.J. et al. INO80 and gamma-H2AX interaction links ATP-dependent chromatin remodeling to DNA damage repair. Cell 119, 767–775 (2004).
  CAS PubMed Google Scholar
• Shen, X., Ranallo, R., Choi, E. & Wu, C. Involvement of actin-related proteins in ATP-dependent chromatin remodeling. Mol. Cell 12, 147–155 (2003).
  CAS PubMed Google Scholar
• van Attikum, H., Fritsch, O., Hohn, B. & Gasser, S.M. Recruitment of the INO80 complex by H2A phosphorylation links ATP-dependent chromatin remodeling with DNA double-strand break repair. Cell 119, 777–788 (2004).
  CAS PubMed Google Scholar
• Qin, S. & Parthun, M.R. Recruitment of the type B histone acetyltransferase Hat1p to chromatin is linked to DNA double-strand breaks. Mol. Cell. Biol. 26, 3649–3658 (2006).
  CAS PubMed PubMed Central Google Scholar
• Parthun, M.R., Widom, J. & Gottschling, D.E. The major cytoplasmic histone acetyltransferase in yeast: links to chromatin replication and histone metabolism. Cell 87, 85–94 (1996).
  CAS PubMed Google Scholar
• Tamburini, B.A. & Tyler, J.K. Localized histone acetylation and deacetylation triggered by the homologous recombination pathway of double-strand DNA repair. Mol. Cell. Biol. 25, 4903–4913 (2005).
  CAS PubMed PubMed Central Google Scholar
• Chowdhury, D. et al. gamma-H2AX dephosphorylation by protein phosphatase 2A facilitates DNA double-strand break repair. Mol. Cell 20, 801–809 (2005).
  CAS PubMed Google Scholar
• Keogh, M.C. et al. A phosphatase complex that dephosphorylates gammaH2AX regulates DNA damage checkpoint recovery. Nature 439, 497–501 (2006).
  CAS PubMed Google Scholar
• Cheung, W.L. et al. Phosphorylation of histone H4 serine 1 during DNA damage requires casein kinase II in S. cerevisiae. Curr. Biol. 15, 656–660 (2005).
  CAS PubMed Google Scholar
• Papamichos-Chronakis, M., Krebs, J.E. & Peterson, C.L. Interplay between Ino80 and Swr1 chromatin remodeling enzymes regulates cell cycle checkpoint adaptation in response to DNA damage. Genes Dev. 20, 2437–2449 (2006).
  CAS PubMed PubMed Central Google Scholar
• Squatrito, M., Gorrini, C. & Amati, B. Tip60 in DNA damage response and growth control: many tricks in one HAT. Trends Cell Biol. 16, 433–442 (2006).
  CAS PubMed Google Scholar
• Shim, E.Y., Ma, J.L., Oum, J.H., Yanez, Y. & Lee, S.E. The yeast chromatin remodeler RSC complex facilitates end joining repair of DNA double-strand breaks. Mol. Cell. Biol. 25, 3934–3944 (2005).
  CAS PubMed PubMed Central Google Scholar
• Chai, B., Huang, J., Cairns, B.R. & Laurent, B.C. Distinct roles for the RSC and Swi/Snf ATP-dependent chromatin remodelers in DNA double-strand break repair. Genes Dev. 19, 1656–1661 (2005).
  CAS PubMed PubMed Central Google Scholar
• Polo, S.E., Roche, D. & Almouzni, G. New histone incorporation marks sites of UV repair in human cells. Cell 127, 481–493 (2006).
  CAS PubMed Google Scholar
• Tyler, J.K. et al. The RCAF complex mediates chromatin assembly during DNA replication and repair. Nature 402, 555–560 (1999).
  CAS PubMed Google Scholar
• Kuzuhara, T. & Horikoshi, M. A nuclear FK506-binding protein is a histone chaperone regulating rDNA silencing. Nat. Struct. Mol. Biol. 11, 275–283 (2004).
  CAS PubMed Google Scholar
• Kleinschmidt, J.A., Fortkamp, E., Krohne, G., Zentgraf, H. & Franke, W.W. Co-existence of two different types of soluble histone complexes in nuclei of Xenopus laevis oocytes. J. Biol. Chem. 260, 1166–1176 (1985).
  CAS PubMed Google Scholar
• Bortvin, A. & Winston, F. Evidence that Spt6p controls chromatin structure by a direct interaction with histones. Science 272, 1473–1476 (1996).
  CAS PubMed Google Scholar
• Huang, S. et al. Rtt106p is a histone chaperone involved in heterochromatin-mediated silencing. Proc. Natl. Acad. Sci. USA 102, 13410–13415 (2005).
  CAS PubMed PubMed Central Google Scholar
• Laskey, R.A., Honda, B.M., Mills, A.D. & Finch, J.T. Nucleosomes are assembled by an acidic protein which binds histones and transfers them to DNA. Nature 275, 416–420 (1978).
  CAS PubMed Google Scholar
• Okuwaki, M., Matsumoto, K., Tsujimoto, M. & Nagata, K. Function of nucleophosmin/B23, a nucleolar acidic protein, as a histone chaperone. FEBS Lett. 506, 272–276 (2001).
  CAS PubMed Google Scholar
• Rougeulle, C. & Avner, P. Cloning and characterization of a murine brain specific gene Bpx and its human homologue lying within the Xic candidate region. Hum. Mol. Genet. 5, 41–49 (1996).
  CAS PubMed Google Scholar
• Okuwaki, M. & Nagata, K. Template activating factor-I remodels the chromatin structure and stimulates transcription from the chromatin template. J. Biol. Chem. 273, 34511–34518 (1998).
  CAS PubMed Google Scholar
• Wang, G.S. et al. Transcriptional modification by a CASK-interacting nucleosome assembly protein. Neuron 42, 113–128 (2004).
  CAS PubMed Google Scholar
• Selth, L. & Svejstrup, J.Q. Vps75, a new yeast member of the NAP histone chaperone family. J. Biol. Chem. 282, 12358–12362 (2007).
  CAS PubMed Google Scholar
• Ai, X. & Parthun, M.R. The nuclear Hat1p/Hat2p complex: a molecular link between type B histone acetyltransferases and chromatin assembly. Mol. Cell 14, 195–205 (2004).
  CAS PubMed Google Scholar
• Loyola, A., LeRoy, G., Wang, Y.H. & Reinberg, D. Reconstitution of recombinant chromatin establishes a requirement for histone-tail modifications during chromatin assembly and transcription. Genes Dev. 15, 2837–2851 (2001).
  CAS PubMed PubMed Central Google Scholar
• Peterson, C.L., Zhao, Y. & Chait, B.T. Subunits of the yeast SWI/SNF complex are members of the actin-related protein (ARP) family. J. Biol. Chem. 273, 23641–23644 (1998).
  CAS PubMed Google Scholar
• Ito, T., Bulger, M., Pazin, M.J., Kobayashi, R. & Kadonaga, J.T. ACF, an ISWI-containing and ATP-utilizing chromatin assembly and remodeling factor. Cell 90, 145–155 (1997).
  CAS PubMed Google Scholar