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:

Regulation of nucleosome dynamics by histone modifications

Abstract

Chromatin is a dynamic structure that must respond to myriad stimuli to regulate access to DNA, and chemical modification of histones is a major means by which the cell modulates nucleosome mobility and turnover. Histone modifications are linked to essentially every cellular process requiring DNA access, including transcription, replication and repair. Here we consider properties of the major types of histone modification in the context of their associated biological processes to view them in light of the cellular mechanisms that regulate nucleosome dynamics.

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: Cumulative charge neutralization as the predominant mechanism of transcriptional regulation by lysine acetylation.
Figure 2: Swi6-mediated chromatin stabilization.
Figure 3: Models for the establishment of distinct methylation states.
Figure 4: Model for maintenance of a histone modification through replication-independent nucleosome turnover.
Figure 5: Histone modifications as consequences of dynamic chromatin processes.

Similar content being viewed by others

References

  1. Woodcock, C.L. & Ghosh, R.P. Chromatin higher-order structure and dynamics. Cold Spring Harb. Perspect. Biol. 2, a000596 (2010).

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  2. Talbert, P.B. & Henikoff, S. Histone variants—ancient wrap artists of the epigenome. Nat. Rev. Mol. Cell Biol. 11, 264–275 (2010).

    Article  CAS  PubMed  Google Scholar 

  3. Hargreaves, D.C. & Crabtree, G.R. ATP-dependent chromatin remodeling: genetics, genomics and mechanisms. Cell Res. 21, 396–420 (2011).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  4. Allfrey, V.G., Faulkner, R. & Mirsky, A.E. Acetylation and methylation of histones and their possible role in the regulation of RNA synthesis. Proc. Natl. Acad. Sci. USA 51, 786–794 (1964). This paper describes methylation of histones and demonstrates the association of hyperacetylated histones with actively transcribed regions.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  5. Kouzarides, T. Chromatin modifications and their function. Cell 128, 693–705 (2007).

    Article  CAS  PubMed  Google Scholar 

  6. Tan, M. et al. Identification of 67 histone marks and histone lysine crotonylation as a new type of histone modification. Cell 146, 1016–1028 (2011). Nearly doubling the number of known histone modifications, this work highlights the diversity of sites and types of modification found on histones.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  7. Roudier, F. et al. Integrative epigenomic mapping defines four main chromatin states in Arabidopsis. EMBO J. 30, 1928–1938 (2011).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  8. Liu, C.L. et al. Single-nucleosome mapping of histone modifications in S. cerevisiae. PLoS Biol. 3, e328 (2005).

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  9. Wang, Z. et al. Combinatorial patterns of histone acetylations and methylations in the human genome. Nat. Genet. 40, 897–903 (2008).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  10. Mikkelsen, T.S. et al. Genome-wide maps of chromatin state in pluripotent and lineage-committed cells. Nature 448, 553–560 (2007).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  11. Kharchenko, P.V. et al. Comprehensive analysis of the chromatin landscape in Drosophila melanogaster. Nature 471, 480–485 (2011).

    Article  CAS  PubMed  Google Scholar 

  12. Zentner, G.E., Tesar, P.J. & Scacheri, P.C. Epigenetic signatures distinguish multiple classes of enhancers with distinct cellular functions. Genome Res. 21, 1273–1283 (2011).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  13. Rada-Iglesias, A. et al. A unique chromatin signature uncovers early developmental enhancers in humans. Nature 470, 279–283 (2011).

    Article  CAS  PubMed  Google Scholar 

  14. Phillips, D.M.P. The presence of acetyl groups in histones. Biochem. J. 87, 258–263 (1963).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  15. Pogo, B.G., Allfrey, V.G. & Mirsky, A.E. RNA synthesis and histone acetylation during the course of gene activation in lymphocytes. Proc. Natl. Acad. Sci. USA 55, 805–812 (1966).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  16. Hong, L., Schroth, G.P., Matthews, H.R., Yau, P. & Bradbury, E.M. Studies of the DNA binding properties of histone H4 amino terminus. Thermal denaturation studies reveal that acetylation markedly reduces the binding constant of the H4 “tail” to DNA. J. Biol. Chem. 268, 305–314 (1993).

    CAS  PubMed  Google Scholar 

  17. Megee, P.C., Morgan, B.A. & Smith, M.M. Histone H4 and the maintenance of genome integrity. Genes Dev. 9, 1716–1727 (1995).

    Article  CAS  PubMed  Google Scholar 

  18. Dion, M.F., Altschuler, S.J., Wu, L.F. & Rando, O.J. Genomic characterization reveals a simple histone H4 acetylation code. Proc. Natl. Acad. Sci. USA 102, 5501–5506 (2005). This work shows that cumulative lysine charge neutralization is the predominant determinant of transcriptional effects mediated by histone H4 tail acetylation.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  19. Martin, A.M., Pouchnik, D.J., Walker, J.L. & Wyrick, J.J. Redundant roles for histone H3 N-terminal lysine residues in subtelomeric gene repression in Saccharomyces cerevisiae. Genetics 167, 1123–1132 (2004).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  20. Bell, S.P. & Dutta, A. DNA replication in eukaryotic cells. Annu. Rev. Biochem. 71, 333–374 (2002).

    Article  CAS  PubMed  Google Scholar 

  21. Unnikrishnan, A., Gafken, P.R. & Tsukiyama, T. Dynamic changes in histone acetylation regulate origins of DNA replication. Nat. Struct. Mol. Biol. 17, 430–437 (2010).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  22. Xu, Y. & Price, B.D. Chromatin dynamics and the repair of DNA double strand breaks. Cell Cycle 10, 261–267 (2011).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  23. Barth, T.K. & Imhof, A. Fast signals and slow marks: the dynamics of histone modifications. Trends Biochem. Sci. 35, 618–626 (2010).

    Article  CAS  PubMed  Google Scholar 

  24. Allis, C.D. et al. New nomenclature for chromatin-modifying enzymes. Cell 131, 633–636 (2007).

    Article  CAS  PubMed  Google Scholar 

  25. Wang, Z. et al. Genome-wide mapping of HATs and HDACs reveals distinct functions in active and inactive genes. Cell 138, 1019–1031 (2009).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  26. Waterborg, J.H. Dynamics of histone acetylation in vivo. A function for acetylation turnover? Biochem. Cell Biol. 80, 363–378 (2002).

    Article  CAS  PubMed  Google Scholar 

  27. Tamkun, J.W. et al. brahma: a regulator of Drosophila homeotic genes structurally related to the yeast transcriptional activator SNF2/SWI2. Cell 68, 561–572 (1992).

    Article  CAS  PubMed  Google Scholar 

  28. Zeng, L. & Zhou, M.-M. Bromodomain: an acetyl-lysine binding domain. FEBS Lett. 513, 124–128 (2002).

    Article  CAS  PubMed  Google Scholar 

  29. Corona, D.F.V., Clapier, C.R., Becker, P.B. & Tamkun, J.W. Modulation of ISWI function by site-specific histone acetylation. EMBO Rep. 3, 242–247 (2002).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  30. Shogren-Knaak, M. et al. Histone H4–K16 acetylation controls chromatin structure and protein interactions. Science 311, 844–847 (2006).

    Article  CAS  PubMed  Google Scholar 

  31. Clapier, C.R., Nightingale, K.P. & Becker, P.B. A critical epitope for substrate recognition by the nucleosome remodeling ATPase ISWI. Nucleic Acids Res. 30, 649–655 (2002).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  32. Olsen, C.A. Expansion of the lysine acylation landscape. Angew. Chem. Int. Ed. Engl. 51, 3755–3756 (2012).

    Article  CAS  PubMed  Google Scholar 

  33. Bedford, M.T. & Clarke, S.G. Protein arginine methylation in mammals: who, what, and why. Mol. Cell 33, 1–13 (2009).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  34. Hon, G.C., Hawkins, R.D. & Ren, B. Predictive chromatin signatures in the mammalian genome. Hum. Mol. Genet. 18, R195–R201 (2009).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  35. Lenstra, T.L. et al. The specificity and topology of chromatin interaction pathways in yeast. Mol. Cell 42, 536–549 (2011).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  36. Jiang, H. et al. Role for Dpy-30 in ES cell-fate specification by regulation of H3K4 methylation within bivalent domains. Cell 144, 513–525 (2011).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  37. Wagner, E.J. & Carpenter, P.B. Understanding the language of Lys36 methylation at histone H3. Nat. Rev. Mol. Cell Biol. 13, 115–126 (2012).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  38. Schmitges, F.W. et al. Histone methylation by PRC2 is inhibited by active chromatin marks. Mol. Cell 42, 330–341 (2011).

    Article  CAS  PubMed  Google Scholar 

  39. Schwartz, Y.B. & Pirrotta, V. Polycomb silencing mechanisms and the management of genomic programmes. Nat. Rev. Genet. 8, 9–22 (2007).

    Article  CAS  PubMed  Google Scholar 

  40. Keogh, M.-C. et al. Cotranscriptional Set2 methylation of histone H3 lysine 36 recruits a repressive Rpd3 complex. Cell 123, 593–605 (2005).

    Article  CAS  PubMed  Google Scholar 

  41. Carrozza, M.J. et al. Histone H3 methylation by Set2 directs deacetylation of coding regions by Rpd3S to suppress spurious intragenic transcription. Cell 123, 581–592 (2005).

    Article  CAS  PubMed  Google Scholar 

  42. Li, B. et al. Infrequently transcribed long genes depend on the Set2/Rpd3S pathway for accurate transcription. Genes Dev. 21, 1422–1430 (2007).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  43. Drouin, S. et al. DSIF and RNA polymerase II CTD phosphorylation coordinate the recruitment of Rpd3S to actively transcribed genes. PLoS Genet. 6, e1001173 (2010).

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  44. Taverna, S.D., Li, H., Ruthenburg, A.J., Allis, C.D. & Patel, D.J. How chromatin-binding modules interpret histone modifications: lessons from professional pocket pickers. Nat. Struct. Mol. Biol. 14, 1025–1040 (2007).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  45. Fischle, W. et al. Molecular basis for the discrimination of repressive methyl-lysine marks in histone H3 by Polycomb and HP1 chromodomains. Genes Dev. 17, 1870–1881 (2003).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  46. Canzio, D. et al. Chromodomain-mediated oligomerization of HP1 suggests a nucleosome-bridging mechanism for heterochromatin assembly. Mol. Cell 41, 67–81 (2011). This work provides evidence that HP1 oligomerizes to stabilize nucleosomes as a component of heterochromatin formation.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  47. Venkatesh, S. et al. Set2 methylation of histone H3 lysine36 suppresses histone exchange on transcribed genes. Nature 489, 452–455 (2012).

    Article  CAS  PubMed  Google Scholar 

  48. Smolle, M. et al. Chromatin remodelers Isw1 and Chd1 maintain chromatin structure during transcription by preventing histone exchange. Nat. Struct. Mol. Biol. 19, 884–892 (2012).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  49. Maltby, V.E. et al. Histone H3 lysine 36 methylation targets the Isw1b remodeling complex to chromatin. Mol. Cell Biol. 32, 3479–3485 (2012).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  50. Briggs, S.D. et al. Gene silencing: trans-histone regulatory pathway in chromatin. Nature 418, 498 (2002).

    Article  CAS  PubMed  Google Scholar 

  51. Patnaik, D. et al. Substrate specificity and kinetic mechanism of mammalian G9a histone H3 methyltransferase. J. Biol. Chem. 279, 53248–53258 (2004).

    Article  CAS  PubMed  Google Scholar 

  52. Dillon, S., Zhang, X., Trievel, R. & Cheng, X. The SET-domain protein superfamily: protein lysine methyltransferases. Genome Biol. 6, 227 (2005).

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  53. Banerjee, T. & Chakravarti, D. A peek into the complex realm of histone phosphorylation. Mol. Cell Biol. 31, 4858–4873 (2011).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  54. Mirsky, A.E., Silverman, B. & Panda, N.C. Blocking by histones of accessibility to DNA in chromatin: addition of histones. Proc. Natl. Acad. Sci. USA 69, 3243–3246 (1972).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  55. North, J.A. et al. Phosphorylation of histone H3(T118) alters nucleosome dynamics and remodeling. Nucleic Acids Res. 39, 6465–6474 (2011). This work shows that histone core phosphorylation can influence nucleosome sliding and histone-DNA interactions.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  56. Paull, T.T. et al. A critical role for histone H2AX in recruitment of repair factors to nuclear foci after DNA damage. Curr. Biol. 10, 886–895 (2000).

    Article  CAS  PubMed  Google Scholar 

  57. Talbert, P. et al. A unified phylogeny-based nomenclature for histone variants. Epigenetics Chromatin 5, 7 (2012).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  58. Kusch, T. et al. Acetylation by Tip60 is required for selective histone variant exchange at DNA lesions. Science 306, 2084–2087 (2004).

    Article  CAS  PubMed  Google Scholar 

  59. Green, G.R. & Poccia, D.L. Phosphorylation of sea urchin sperm H1 and H2B histones precedes chromatin decondensation and H1 exchange during pronuclear formation. Dev. Biol. 108, 235–245 (1985).

    Article  CAS  PubMed  Google Scholar 

  60. Hirota, T., Lipp, J.J., Toh, B.-H. & Peters, J.-M. Histone H3 serine 10 phosphorylation by Aurora B causes HP1 dissociation from heterochromatin. Nature 438, 1176–1180 (2005). The work in refs. 60 and 61 shows that H3S10 phosphorylation adjacent to H3K9me3 displaces HP1 from chromatin—the first example of a histone tail phospho-methyl switch.

    Article  CAS  PubMed  Google Scholar 

  61. Fischle, W. et al. Regulation of HP1-chromatin binding by histone H3 methylation and phosphorylation. Nature 438, 1116–1122 (2005).

    Article  CAS  PubMed  Google Scholar 

  62. Gehani, S.S. et al. Polycomb group protein displacement and gene activation through MSK-dependent H3K27me3S28 phosphorylation. Mol. Cell 39, 886–900 (2010).

    Article  CAS  PubMed  Google Scholar 

  63. Hassa, P.O., Haenni, S.S., Elser, M. & Hottiger, M.O. Nuclear ADP-ribosylation reactions in mammalian cells: where are we today and where are we going? Microbiol. Mol. Biol. Rev. 70, 789–829 (2006).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  64. Messner, S. & Hottiger, M.O. Histone ADP-ribosylation in DNA repair, replication and transcription. Trends Cell Biol. 21, 534–542 (2011).

    Article  CAS  PubMed  Google Scholar 

  65. Petesch, S.J. & Lis, J.T. Activator-induced spread of poly(ADP-ribose) polymerase promotes nucleosome loss at Hsp70. Mol. Cell 45, 64–74 (2012).

    Article  CAS  PubMed  Google Scholar 

  66. Sakabe, K., Wang, Z. & Hart, G.W. β-N-acetylglucosamine (O-GlcNAc) is part of the histone code. Proc. Natl. Acad. Sci. USA 107, 19915–19920 (2010).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  67. Zhang, S., Roche, K., Nasheuer, H.-P. & Lowndes, N.F. Modification of histones by sugar β-N-acetylglucosamine (GlcNAc) occurs on multiple residues, including histone H3 serine 10, and is cell cycle–regulated. J. Biol. Chem. 286, 37483–37495 (2011).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  68. Fujiki, R. et al. GlcNAcylation of histone H2B facilitates its monoubiquitination. Nature 480, 557–560 (2011).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  69. Fleming, A.B., Kao, C.-F., Hillyer, C., Pikaart, M. & Osley, M.A. H2B ubiquitylation plays a role in nucleosome dynamics during transcription elongation. Mol. Cell 31, 57–66 (2008).

    Article  CAS  PubMed  Google Scholar 

  70. Batta, K., Zhang, Z., Yen, K., Goffman, D.B. & Pugh, B.F. Genome-wide function of H2B ubiquitylation in promoter and genic regions. Genes Dev. 25, 2254–2265 (2011).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  71. Lee, J.-S. et al. Codependency of H2B monoubiquitination and nucleosome reassembly on Chd1. Genes Dev. 26, 914–919 (2012).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  72. Chandrasekharan, M.B., Huang, F. & Sun, Z.-W. Ubiquitination of histone H2B regulates chromatin dynamics by enhancing nucleosome stability. Proc. Natl. Acad. Sci. USA 106, 16686–16691 (2009).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  73. Fierz, B. et al. Histone H2B ubiquitylation disrupts local and higher-order chromatin compaction. Nat. Chem. Biol. 7, 113–119 (2011).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  74. Moyal, L. et al. Requirement of ATM-dependent monoubiquitylation of histone H2B for timely repair of DNA double-strand breaks. Mol. Cell 41, 529–542 (2011).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  75. Wang, H. et al. Role of histone H2A ubiquitination in Polycomb silencing. Nature 431, 873–878 (2004).

    Article  CAS  PubMed  Google Scholar 

  76. Zhou, W. et al. Histone H2A monoubiquitination represses transcription by inhibiting RNA polymerase II transcriptional elongation. Mol. Cell 29, 69–80 (2008).

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  77. Shiio, Y. & Eisenman, R.N. Histone sumoylation is associated with transcriptional repression. Proc. Natl. Acad. Sci. USA 100, 13225–13230 (2003).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  78. Nathan, D. et al. Histone sumoylation is a negative regulator in Saccharomyces cerevisiae and shows dynamic interplay with positive-acting histone modifications. Genes Dev. 20, 966–976 (2006).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  79. Lee, J.-S. et al. Histone crosstalk between H2B monoubiquitination and H3 methylation mediated by COMPASS. Cell 131, 1084–1096 (2007).

    Article  CAS  PubMed  Google Scholar 

  80. Henikoff, S. Nucleosome destabilization in the epigenetic regulation of gene expression. Nat. Rev. Genet. 9, 15–26 (2008).

    Article  CAS  PubMed  Google Scholar 

  81. Szenker, E., Ray-Gallet, D. & Almouzni, G. The double face of the histone variant H3.3. Cell Res. 21, 421–434 (2011).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  82. 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).

    Article  CAS  PubMed  Google Scholar 

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

    Article  CAS  PubMed  Google Scholar 

  84. Deal, R.B., Henikoff, J.G. & Henikoff, S. Genome-wide kinetics of nucleosome turnover determined by metabolic labeling of histones. Science 328, 1161–1164 (2010).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  85. modENCODE Consortium. Identification of functional elements and regulatory circuits by Drosophila modENCODE. Science 330, 1787–1797 (2010).

  86. Gerstein, M.B. et al. Integrative analysis of the Caenorhabditis elegans genome by the modENCODE Project. Science 330, 1775–1787 (2010).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  87. McKittrick, E., Gafken, P.R., Ahmad, K. & Henikoff, S. Histone H3.3 is enriched in covalent modifications associated with active chromatin. Proc. Natl. Acad. Sci. USA 101, 1525–1530 (2004).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

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

    Article  CAS  PubMed  Google Scholar 

  89. Henikoff, S., McKittrick, E. & Ahmad, K. Epigenetics, histone H3 variants and the inheritance of chromatin states. Cold Spring Harb. Symp. Quant. Biol. 69, 235–243 (2004).

    Article  CAS  PubMed  Google Scholar 

  90. Gossett, A.J. & Lieb, J.D. In vivo effects of histone H3 depletion on nucleosome occupancy and position in Saccharomyces cerevisiae. PLoS Genet. 8, e1002771 (2012). This work demonstrates preferential loss of acetylated nucleosomes upon histone H3 depletion in vivo.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  91. Aagaard, L. et al. Functional mammalian homologues of the Drosophila PEV-modifier Su(var)3–9 encode centromere-associated proteins which complex with the heterochromatin component M31. EMBO J. 18, 1923–1938 (1999).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  92. Bannister, A.J. et al. Selective recognition of methylated lysine 9 on histone H3 by the HP1 chromo domain. Nature 410, 120–124 (2001).

    Article  CAS  PubMed  Google Scholar 

  93. Eustermann, S. et al. Combinatorial readout of histone H3 modifications specifies localization of ATRX to heterochromatin. Nat. Struct. Mol. Biol. 18, 777–782 (2011).

    Article  CAS  PubMed  Google Scholar 

  94. Goldberg, A.D. et al. Distinct factors control histone variant H3.3 localization at specific genomic regions. Cell 140, 678–691 (2010).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  95. Xu, M. et al. Partitioning of histone H3–H4 tetramers during DNA replication–dependent chromatin assembly. Science 328, 94–98 (2010).

    Article  CAS  PubMed  Google Scholar 

  96. Zhu, B. & Reinberg, D. Epigenetic inheritance: uncontested? Cell Res. 21, 435–441 (2011).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

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

    Article  CAS  PubMed  Google Scholar 

  98. Huen, M.S.Y., Sy, S.M.-H., van Deursen, J.M. & Chen, J. Direct interaction between SET8 and proliferating cell nuclear antigen couples H4–K20 methylation with DNA replication. J. Biol. Chem. 283, 11073–11077 (2008).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  99. Petruk, S. et al. TrxG and PcG proteins but not methylated histones remain associated with DNA through replication. Cell 150, 922–933 (2012).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  100. Lo, S.M. et al. A bridging model for persistence of a polycomb group protein complex through DNA replication in vitro. Mol. Cell 46, 784–796 (2012).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  101. Huff, J.T., Plocik, A.M., Guthrie, C. & Yamamoto, K.R. Reciprocal intronic and exonic histone modification regions in humans. Nat. Struct. Mol. Biol. 17, 1495–1499 (2010).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  102. Ernst, J. et al. Mapping and analysis of chromatin state dynamics in nine human cell types. Nature 473, 43–49 (2011).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  103. Henikoff, S. & Shilatifard, A. Histone modification: cause or cog? Trends Genet. 27, 389–396 (2011).

    Article  CAS  PubMed  Google Scholar 

  104. Kundaje, A. et al. Ubiquitous heterogeneity and asymmetry of the chromatin environment at regulatory elements. Genome Res. 22, 1735–1747 (2012). This work shows that there are notably few patterns of histone modifications around transcription factor binding sites in the human genome.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  105. Sims, R.J. III, Mandal, S.S. & Reinberg, D. Recent highlights of RNA-polymerase-II-mediated transcription. Curr. Opin. Cell Biol. 16, 263–271 (2004).

    Article  CAS  PubMed  Google Scholar 

  106. Buro, L., Chipumuro, E. & Henriksen, M. Menin and RNF20 recruitment is associated with dynamic histone modifications that regulate signal transducer and activator of transcription 1 (STAT1)-activated transcription of the interferon regulatory factor 1 gene (IRF1). Epigenetics Chromatin 3, 16 (2010).

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  107. Li, Y. et al. The histone modifications governing TFF1 transcription mediated by estrogen receptor. J. Biol. Chem. 286, 13925–13936 (2011).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  108. Aygün, O. & Grewal, S.I.S. Assembly and functions of heterochromatin in the fission yeast genome. Cold Spring Harb. Symp. Quant. Biol. 75, 259–267 (2010).

    Article  PubMed  Google Scholar 

  109. Wang, K.C. et al. A long noncoding RNA maintains active chromatin to coordinate homeotic gene expression. Nature 472, 120–124 (2011).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  110. Cosgrove, M.S., Boeke, J.D. & Wolberger, C. Regulated nucleosome mobility and the histone code. Nat. Struct. Mol. Biol. 11, 1037–1043 (2004).

    Article  CAS  PubMed  Google Scholar 

Download references

Acknowledgements

We thank S. Kasanathan and P. Talbert for helpful comments on the manuscript. Work in our laboratory is supported by US National Institutes of Health grants 5U01 HG004274, U54 CA143862 and R01 ES020116 and by the Howard Hughes Medical Institute.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Steven Henikoff.

Ethics declarations

Competing interests

The authors declare no competing financial interests.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Zentner, G., Henikoff, S. Regulation of nucleosome dynamics by histone modifications. Nat Struct Mol Biol 20, 259–266 (2013). https://doi.org/10.1038/nsmb.2470

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1038/nsmb.2470

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