Skip to main content

Thank you for visiting nature.com. You are using a browser version with limited support for CSS. To obtain the best experience, we recommend you use a more up to date browser (or turn off compatibility mode in Internet Explorer). In the meantime, to ensure continued support, we are displaying the site without styles and JavaScript.

  • Review Article
  • Published:

Histone chaperones: an escort network regulating histone traffic

An Erratum to this article was published on 01 December 2007

Abstract

In eukaryotes, DNA is organized into chromatin in a dynamic manner that enables it to be accessed for processes such as transcription and repair. Histones, the chief protein component of chromatin, must be assembled, replaced or exchanged to preserve or change this organization according to cellular needs. Histone chaperones are key actors during histone metabolism. Here we classify known histone chaperones and discuss how they build a network to escort histone proteins. Molecular interactions with histones and their potential specificity or redundancy are also discussed in light of chaperone structural properties. The multiplicity of histone chaperone partners, including histone modifiers, nucleosome remodelers and cell-cycle regulators, is relevant to their coordination with key cellular processes. Given the current interest in chromatin as a source of epigenetic marks, we address the potential contributions of histone chaperones to epigenetic memory and genome stability.

This is a preview of subscription content, access via your institution

Access options

Buy this article

Prices may be subject to local taxes which are calculated during checkout

Figure 1: Classification of histone chaperones in multiple organisms.
Figure 2: Asf1 histone chaperone structure and function.
Figure 3: Asf1 is an example of a histone chaperone within a network of binding partners.
Figure 4: Histone chaperones mediate histone dynamics during transcription elongation.
Figure 5: Chromatin rearrangements and histone chaperone activities during DSB repair in S.cerevisiae.

Similar content being viewed by others

References

  1. Kornberg, R.D. Structure of chromatin. Annu. Rev. Biochem. 46, 931–954 (1977).

    Article  CAS  PubMed  Google Scholar 

  2. 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 

  3. 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 

  4. 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 

  5. Loyola, A. & Almouzni, G. Histone chaperones, a supporting role in the limelight. Biochim. Biophys. Acta 1677, 3–11 (2004).

    CAS  PubMed  Google Scholar 

  6. 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 

  7. Stillman, B. Chromatin assembly during SV40 DNA replication in vitro. Cell 45, 555–565 (1986).

    CAS  PubMed  Google Scholar 

  8. 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 

  9. 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 

  10. 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 

  11. 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 

  12. 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 

  13. 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 

  14. 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 

  15. 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 

  16. Luk, E. et al. Chz1, a nuclear chaperone for histone H2AZ. Mol. Cell 25, 357–368 (2007).

    CAS  PubMed  Google Scholar 

  17. Loyola, A. & Almouzni, G. Marking histone H3 variants: how, when and why? Trends Biochem. Sci. 32, 425–433 (2007).

    CAS  PubMed  Google Scholar 

  18. 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 

  19. 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 

  20. 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 

  21. 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 

  22. 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 

  23. 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 

  24. Belotserkovskaya, R. et al. FACT facilitates transcription-dependent nucleosome alteration. Science 301, 1090–1093 (2003).

    CAS  PubMed  Google Scholar 

  25. 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 

  26. 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 

  27. 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 

  28. 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 

  29. Regnard, C. et al. Polyglutamylation of nucleosome assembly proteins. J. Biol. Chem. 275, 15969–15976 (2000).

    CAS  PubMed  Google Scholar 

  30. 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 

  31. 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 

  32. 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 

  33. 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 

  34. 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 

  35. 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 

  36. 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 

  37. 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 

  38. 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 

  39. 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 

  40. 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 

  41. 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 

  42. 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 

  43. 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 

  44. 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 

  45. 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 

  46. Han, J. et al. Rtt109 acetylates histone H3 lysine 56 and functions in DNA replication. Science 315, 653–655 (2007).

    CAS  PubMed  Google Scholar 

  47. 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 

  48. 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 

  49. 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 

  50. 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 

  51. 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 

  52. 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 

  53. 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 

  54. 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 

  55. 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 

  56. 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 

  57. 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 

  58. 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 

  59. 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 

  60. 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 

  61. 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 

  62. 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 

  63. Groth, A., Rocha, W., Verreault, A. & Almouzni, G. Chromatin challenges during DNA replication and repair. Cell 128, 721–733 (2007).

    CAS  PubMed  Google Scholar 

  64. 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 

  65. Li, B., Carey, M. & Workman, J.L. The role of chromatin during transcription. Cell 128, 707–719 (2007).

    CAS  PubMed  Google Scholar 

  66. Workman, J.L. Nucleosome displacement in transcription. Genes Dev. 20, 2009–2017 (2006).

    CAS  PubMed  Google Scholar 

  67. 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 

  68. 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 

  69. 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 

  70. 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 

  71. 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 

  72. 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 

  73. 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 

  74. 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 

  75. 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 

  76. 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 

  77. 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 

  78. 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 

  79. 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 

  80. 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 

  81. 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 

  82. 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 

  83. 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 

  84. 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 

  85. 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 

  86. 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 

  87. 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 

  88. 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 

  89. 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 

  90. Dion, M.F. et al. Dynamics of replication-independent histone turnover in budding yeast. Science 315, 1405–1408 (2007).

    CAS  PubMed  Google Scholar 

  91. 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 

  92. 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 

  93. 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 

  94. 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 

  95. 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 

  96. 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 

  97. 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 

  98. 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 

  99. 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 

  100. Bao, Y. & Shen, X. Chromatin remodeling in DNA double-strand break repair. Curr. Opin. Genet. Dev. 17, 126–131 (2007).

    CAS  PubMed  Google Scholar 

  101. Altaf, M., Saksouk, N. & Cote, J. Histone modifications in response to DNA damage. Mutat. Res. 618, 81–90 (2007).

    CAS  PubMed  Google Scholar 

  102. 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 

  103. 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 

  104. 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 

  105. 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 

  106. 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 

  107. 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 

  108. 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 

  109. 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 

  110. 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 

  111. 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 

  112. 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 

  113. 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 

  114. 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 

  115. 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 

  116. 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 

  117. 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 

  118. 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 

  119. 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 

  120. 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 

  121. 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 

  122. 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 

  123. 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 

  124. 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 

  125. 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 

  126. 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 

  127. 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 

  128. 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 

  129. 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 

  130. 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 

  131. 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 

  132. 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 

  133. 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 

  134. 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 

  135. Wang, G.S. et al. Transcriptional modification by a CASK-interacting nucleosome assembly protein. Neuron 42, 113–128 (2004).

    CAS  PubMed  Google Scholar 

  136. 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 

  137. 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 

  138. 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 

  139. 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 

  140. 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 

Download references

Acknowledgements

We thank E. Dunleavy, D. Ray-Gallet and A. Gérard for their input. The authors are supported by Cancéropôle Ile-de-France (L.D.K. and G.A.); Université Paris 6 (A.C.); the Ligue Nationale contre le Cancer (Equipe labellisée la Ligue); the Commissariat à l'Energie Atomique (LRC no. 26), European Contract RTN (HPRN-CT-2002-00238), Network of Excellence Epigenome (LSHG-CT-2004-503433), Action Concertée Interface Physique-Chimie-Biologie (04393), the Agence Nationale de la Recherche (NT05-4-422267 and PCV06-142302), and Programme Incitatif et Collaboratif (PIC) Rétinoblastome (G.A.); and US National Institutes of Health grants GM61766 and GM20056 (J.E.H.). J.E.H. received a Mayent-Rotschild sabbatical fellowship from the Institut Curie. We apologize to authors whose work has not been cited because of limited space.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Geneviève Almouzni.

Rights and permissions

Reprints and permissions

About this article

Cite this article

De Koning, L., Corpet, A., Haber, J. et al. Histone chaperones: an escort network regulating histone traffic. Nat Struct Mol Biol 14, 997–1007 (2007). https://doi.org/10.1038/nsmb1318

Download citation

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1038/nsmb1318

This article is cited by

Search

Quick links

Nature Briefing

Sign up for the Nature Briefing newsletter — what matters in science, free to your inbox daily.

Get the most important science stories of the day, free in your inbox. Sign up for Nature Briefing