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:

Cross-regulation of histone modifications

Nature Structural & Molecular Biology volume 14, pages 1017–1024 (2007)Cite this article

Abstract

Histones undergo several different post-translational modifications that control a variety of physiological processes. These covalent modifications show substantial cross-regulation, providing a wealth of regulatory potential. New insights into the communication between modifications on histones have emerged in recent years. This review assesses the current understanding of cross-regulation of histone modifications and identifies future questions to be addressed in this field.

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

Access options

Buy this article

  • Purchase on Springer Link
  • Instant access to full article PDF
Buy now

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

Figure 1: Histone modification choices.
Figure 2: Cross-regulation of modifications in cis and in trans.
Figure 3: Cross-talk between lysine methylation and lysine acetylation.
Figure 4: Potential for additional cross-regulation in nonhistone and histone proteins.

Similar content being viewed by others

References

  1. Kornberg, R.D. Chromatin structure: a repeating unit of histones and DNA. Science 184, 868–871 (1974).

    Article  CAS  PubMed  Google Scholar 

  2. 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 

  3. Bühler, M. & Moazed, D. Transcription and RNA interference in heterochromatic gene silencing. Nat. Struct. Mol. Biol. 14, 1008–1016 (2007).

    Google Scholar 

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

    Article  CAS  PubMed  Google Scholar 

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

    CAS  PubMed  Google Scholar 

  6. 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).

    CAS  PubMed  PubMed Central  Google Scholar 

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

    CAS  PubMed  Google Scholar 

  8. Strahl, B.D. & Allis, C.D. The language of covalent histone modifications. Nature 403, 41–45 (2000).

    Article  CAS  PubMed  Google Scholar 

  9. Turner, B.M. Histone acetylation and an epigenetic code. Bioessays 22, 836–845 (2000).

    CAS  PubMed  Google Scholar 

  10. Hyland, E.M. et al. Insights into the role of histone H3 and histone H4 core modifiable residues in Saccharomyces cerevisiae. Mol. Cell. Biol. 25, 10060–10070 (2005).

    CAS  PubMed  PubMed Central  Google Scholar 

  11. Turner, B.M. Reading signals on the nucleosome with a new nomenclature for modified histones. Nat. Struct. Mol. Biol. 12, 110–112 (2005).

    CAS  PubMed  Google Scholar 

  12. Cuthbert, G.L. et al. Histone deimination antagonizes arginine methylation. Cell 118, 545–553 (2004).

    CAS  PubMed  Google Scholar 

  13. Nakayama, J., Rice, J.C., Strahl, B.D., Allis, C.D. & Grewal, S.I. Role of histone H3 lysine 9 methylation in epigenetic control of heterochromatin assembly. Science 292, 110–113 (2001).

    CAS  PubMed  Google Scholar 

  14. Rea, S. et al. Regulation of chromatin structure by site-specific histone H3 methyltransferases. Nature 406, 593–599 (2000).

    CAS  PubMed  Google Scholar 

  15. Hassan, Y.I. & Zempleni, J. Epigenetic regulation of chromatin structure and gene function by biotin. J. Nutr. 136, 1763–1765 (2006).

    CAS  PubMed  Google Scholar 

  16. Camporeale, G., Oommen, A.M., Griffin, J.B., Sarath, G. & Zempleni, J. K12-biotinylated histone H4 marks heterochromatin in human lymphoblastoma cells. J. Nutr. Biochem. published online, doi:10.1016/j.jnutbio.2006.12.014 (13 April 2007).

  17. 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).

    CAS  PubMed  PubMed Central  Google Scholar 

  18. 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 

  19. Aihara, H. et al. Nucleosomal histone kinase-1 phosphorylates H2A Thr 119 during mitosis in the early Drosophila embryo. Genes Dev. 18, 877–888 (2004).

    CAS  PubMed  PubMed Central  Google Scholar 

  20. Ivanovska, I., Khandan, T., Ito, T. & Orr-Weaver, T.L. A histone code in meiosis: the histone kinase, NHK-1, is required for proper chromosomal architecture in Drosophila oocytes. Genes Dev. 19, 2571–2582 (2005).

    CAS  PubMed  PubMed Central  Google Scholar 

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

    CAS  PubMed  PubMed Central  Google Scholar 

  22. Shin, J.A. et al. SUMO modification is involved in the maintenance of heterochromatin stability in fission yeast. Mol. Cell 19, 817–828 (2005).

    CAS  PubMed  Google Scholar 

  23. Suka, N., Suka, Y., Carmen, A.A., Wu, J. & Grunstein, M. Highly specific antibodies determine histone acetylation site usage in yeast heterochromatin and euchromatin. Mol. Cell 8, 473–479 (2001).

    CAS  PubMed  Google Scholar 

  24. Ahn, S.H., Diaz, R.L., Grunstein, M. & Allis, C.D. Histone H2B deacetylation at lysine 11 is required for yeast apoptosis induced by phosphorylation of H2B at serine 10. Mol. Cell 24, 211–220 (2006).

    CAS  PubMed  Google Scholar 

  25. Cheung, W.L. et al. Apoptotic phosphorylation of histone H2B is mediated by mammalian sterile twenty kinase. Cell 113, 507–517 (2003).

    CAS  PubMed  Google Scholar 

  26. Thorne, A.W., Kmiciek, D., Mitchelson, K., Sautiere, P. & Crane-Robinson, C. Patterns of histone acetylation. Eur. J. Biochem. 193, 701–713 (1990).

    CAS  PubMed  Google Scholar 

  27. Shilatifard, A. Chromatin modifications by methylation and ubiquitination: implications in the regulation of gene expression. Annu. Rev. Biochem. 75, 243–269 (2006).

    CAS  PubMed  Google Scholar 

  28. Shahbazian, M.D., Zhang, K. & Grunstein, M. Histone H2B ubiquitylation controls processive methylation but not monomethylation by Dot1 and Set1. Mol. Cell 19, 271–277 (2005).

    CAS  PubMed  Google Scholar 

  29. Dehe, P.M. et al. Histone H3 lysine 4 mono-methylation does not require ubiquitination of histone H2B. J. Mol. Biol. 353, 477–484 (2005).

    CAS  PubMed  Google Scholar 

  30. Henry, K.W. et al. Transcriptional activation via sequential histone H2B ubiquitylation and deubiquitylation, mediated by SAGA-associated Ubp8. Genes Dev. 17, 2648–2663 (2003).

    CAS  PubMed  PubMed Central  Google Scholar 

  31. Nelson, C.J., Santos-Rosa, H. & Kouzarides, T. Proline isomerization of histone H3 regulates lysine methylation and gene expression. Cell 126, 905–916 (2006).

    CAS  PubMed  Google Scholar 

  32. Hsu, J.Y. et al. Mitotic phosphorylation of histone H3 is governed by Ipl1/aurora kinase and Glc7/PP1 phosphatase in budding yeast and nematodes. Cell 102, 279–291 (2000).

    CAS  PubMed  Google Scholar 

  33. Cheung, P. et al. Synergistic coupling of histone H3 phosphorylation and acetylation in response to epidermal growth factor stimulation. Mol. Cell 5, 905–915 (2000).

    CAS  PubMed  Google Scholar 

  34. Lo, W.S. et al. Phosphorylation of serine 10 in histone H3 is functionally linked in vitro and in vivo to Gcn5-mediated acetylation at lysine 14. Mol. Cell 5, 917–926 (2000).

    CAS  PubMed  Google Scholar 

  35. Edmondson, D.G. et al. Site-specific loss of acetylation upon phosphorylation of histone H3. J. Biol. Chem. 277, 29496–29502 (2002).

    CAS  PubMed  Google Scholar 

  36. Lee, D.Y., Northrop, J.P., Kuo, M.H. & Stallcup, M.R. Histone H3 lysine 9 methyltransferase G9a is a transcriptional coactivator for nuclear receptors. J. Biol. Chem. 281, 8476–8485 (2006).

    CAS  PubMed  Google Scholar 

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

    CAS  PubMed  Google Scholar 

  38. Lachner, M., O'Carroll, D., Rea, S., Mechtler, K. & Jenuwein, T. Methylation of histone H3 lysine 9 creates a binding site for HP1 proteins. Nature 410, 116–120 (2001).

    CAS  PubMed  Google Scholar 

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

    CAS  PubMed  Google Scholar 

  40. 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).

    CAS  PubMed  Google Scholar 

  41. Mateescu, B., England, P., Halgand, F., Yaniv, M. & Muchardt, C. Tethering of HP1 proteins to chromatin is relieved by phosphoacetylation of histone H3. EMBO Rep. 5, 490–496 (2004).

    CAS  PubMed  PubMed Central  Google Scholar 

  42. Daujat, S., Zeissler, U., Waldmann, T., Happel, N. & Schneider, R. HP1 binds specifically to Lys26-methylated histone H1.4, whereas simultaneous Ser27 phosphorylation blocks HP1 binding. J. Biol. Chem. 280, 38090–38095 (2005).

    CAS  PubMed  Google Scholar 

  43. Czermin, B. et al. Physical and functional association of SU(VAR)3–9 and HDAC1 in Drosophila. EMBO Rep. 2, 915–919 (2001).

    CAS  PubMed  PubMed Central  Google Scholar 

  44. Vaute, O., Nicolas, E., Vandel, L. & Trouche, D. Functional and physical interaction between the histone methyl transferase Suv39H1 and histone deacetylases. Nucleic Acids Res. 30, 475–481 (2002).

    CAS  PubMed  PubMed Central  Google Scholar 

  45. Zhang, C.L., McKinsey, T.A. & Olson, E.N. Association of class II histone deacetylases with heterochromatin protein 1: potential role for histone methylation in control of muscle differentiation. Mol. Cell. Biol. 22, 7302–7312 (2002).

    CAS  PubMed  PubMed Central  Google Scholar 

  46. Wang, H. et al. Purification and functional characterization of a histone H3-lysine 4-specific methyltransferase. Mol. Cell 8, 1207–1217 (2001).

    CAS  PubMed  Google Scholar 

  47. Thomas, C.E., Kelleher, N.L. & Mizzen, C.A. Mass spectrometric characterization of human histone H3: a bird's eye view. J. Proteome Res. 5, 240–247 (2006).

    CAS  PubMed  Google Scholar 

  48. Johnson, L. et al. Mass spectrometry analysis of Arabidopsis histone H3 reveals distinct combinations of post-translational modifications. Nucleic Acids Res. 32, 6511–6518 (2004).

    CAS  PubMed  PubMed Central  Google Scholar 

  49. Zhang, K. et al. Differentiation between peptides containing acetylated or tri-methylated lysines by mass spectrometry: an application for determining lysine 9 acetylation and methylation of histone H3. Proteomics 4, 1–10 (2004).

    CAS  PubMed  Google Scholar 

  50. 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).

    CAS  PubMed  PubMed Central  Google Scholar 

  51. Vakoc, C.R., Mandat, S.A., Olenchock, B.A. & Blobel, G.A. Histone H3 lysine 9 methylation and HP1γ are associated with transcription elongation through mammalian chromatin. Mol. Cell 19, 381–391 (2005).

    CAS  PubMed  Google Scholar 

  52. Nishioka, K. et al. Set9, a novel histone H3 methyltransferase that facilitates transcription by precluding histone tail modifications required for heterochromatin formation. Genes Dev. 16, 479–489 (2002).

    CAS  PubMed  PubMed Central  Google Scholar 

  53. Nightingale, K.P. et al. Cross-talk between histone modifications in response to histone deacetylase inhibitors: MLL4 links histone H3 acetylation and histone H3K4 methylation. J. Biol. Chem. 282, 4408–4416 (2007).

    CAS  PubMed  Google Scholar 

  54. Martin, D.G., Grimes, D.E., Baetz, K. & Howe, L. Methylation of histone H3 mediates the association of the NuA3 histone acetyltransferase with chromatin. Mol. Cell. Biol. 26, 3018–3028 (2006).

    CAS  PubMed  PubMed Central  Google Scholar 

  55. Martin, D.G. et al. The Yng1p plant homeodomain finger is a methyl-histone binding module that recognizes lysine 4-methylated histone H3. Mol. Cell. Biol. 26, 7871–7879 (2006).

    CAS  PubMed  PubMed Central  Google Scholar 

  56. Taverna, S.D. et al. Yng1 PHD finger binding to H3 trimethylated at K4 promotes NuA3 HAT activity at K14 of H3 and transcription at a subset of targeted ORFs. Mol. Cell 24, 785–796 (2006).

    CAS  PubMed  PubMed Central  Google Scholar 

  57. Morillon, A., Karabetsou, N., Nair, A. & Mellor, J. Dynamic lysine methylation on histone H3 defines the regulatory phase of gene transcription. Mol. Cell 18, 723–734 (2005).

    CAS  PubMed  Google Scholar 

  58. Govind, C.K., Zhang, F., Qiu, H., Hofmeyer, K. & Hinnebusch, A.G. Gcn5 promotes acetylation, eviction, and methylation of nucleosomes in transcribed coding regions. Mol. Cell 25, 31–42 (2007).

    CAS  PubMed  Google Scholar 

  59. Milne, T.A. et al. MLL targets SET domain methyltransferase activity to Hox gene promoters. Mol. Cell 10, 1107–1117 (2002).

    CAS  PubMed  Google Scholar 

  60. Pray-Grant, M.G., Daniel, J.A., Schieltz, D., Yates, J.R. III & Grant, P.A. Chd1 chromodomain links histone H3 methylation with SAGA- and SLIK-dependent acetylation. Nature 433, 434–438 (2005).

    CAS  PubMed  Google Scholar 

  61. Sims, R.J. III et al. Human but not yeast CHD1 binds directly and selectively to histone H3 methylated at lysine 4 via its tandem chromodomains. J. Biol. Chem. 280, 41789–41792 (2005).

    CAS  PubMed  Google Scholar 

  62. Dou, Y. et al. Physical association and coordinate function of the H3 K4 methyltransferase MLL1 and the H4 K16 acetyltransferase MOF. Cell 121, 873–885 (2005).

    CAS  PubMed  Google Scholar 

  63. Shi, X. et al. ING2 PHD domain links histone H3 lysine 4 methylation to active gene repression. Nature 442, 96–99 (2006).

    CAS  PubMed  PubMed Central  Google Scholar 

  64. Hazzalin, C.A. & Mahadevan, L.C. Dynamic acetylation of all lysine 4-methylated histone H3 in the mouse nucleus: analysis at c-fos and c-jun. PLoS Biol. 3, e393 (2005).

    PubMed  PubMed Central  Google Scholar 

  65. Lee, M.G., Norman, J., Shilatifard, A. & Shiekhattar, R. Physical and functional association of a trimethyl H3K4 demethylase and Ring6a/MBLR, a polycomb-like protein. Cell 128, 877–887 (2007).

    CAS  PubMed  Google Scholar 

  66. Schuettengruber, B., Chourrout, D., Vervoort, M., Leblanc, B. & Cavalli, G. Genome regulation by polycomb and trithorax proteins. Cell 128, 735–745 (2007).

    CAS  PubMed  Google Scholar 

  67. Lee, M.G., Wynder, C., Cooch, N. & Shiekhattar, R. An essential role for CoREST in nucleosomal histone 3 lysine 4 demethylation. Nature 437, 432–435 (2005).

    CAS  PubMed  Google Scholar 

  68. Shi, Y.J. et al. Regulation of LSD1 histone demethylase activity by its associated factors. Mol. Cell 19, 857–864 (2005).

    CAS  PubMed  Google Scholar 

  69. Lee, M.G. et al. Functional interplay between histone demethylase and deacetylase enzymes. Mol. Cell. Biol. 26, 6395–6402 (2006).

    CAS  PubMed  PubMed Central  Google Scholar 

  70. Joshi, A.A. & Struhl, K. Eaf3 chromodomain interaction with methylated H3–K36 links histone deacetylation to Pol II elongation. Mol. Cell 20, 971–978 (2005).

    CAS  PubMed  Google Scholar 

  71. Keogh, M.C. et al. Cotranscriptional set2 methylation of histone H3 lysine 36 recruits a repressive Rpd3 complex. Cell 123, 593–605 (2005).

    CAS  PubMed  Google Scholar 

  72. 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).

    CAS  PubMed  Google Scholar 

  73. Brown, M.A., Sims, R.J. III, Gottlieb, P.D. & Tucker, P.W. Identification and characterization of Smyd2: a split SET/MYND domain-containing histone H3 lysine 36-specific methyltransferase that interacts with the Sin3 histone deacetylase complex. Mol. Cancer 5, 26 (2006).

    PubMed  PubMed Central  Google Scholar 

  74. Tompa, R. & Madhani, H.D. Histone H3 lysine 36 methylation antagonizes silencing in Saccharomyces cerevisiae independently of the Rpd3S histone deacetylase complex. Genetics 175, 585–593 (2007).

    CAS  PubMed  PubMed Central  Google Scholar 

  75. Sims, J.K., Houston, S.I., Magazinnik, T. & Rice, J.C. A trans-tail histone code defined by monomethylated H4 Lys-20 and H3 Lys-9 demarcates distinct regions of silent chromatin. J. Biol. Chem. 281, 12760–12766 (2006).

    CAS  PubMed  Google Scholar 

  76. Yin, Y. et al. SET8 recognizes the sequence RHRK20VLRDN within the N terminus of histone H4 and mono-methylates lysine 20. J. Biol. Chem. 280, 30025–30031 (2005).

    CAS  PubMed  Google Scholar 

  77. Fingerman, I.M., Li, H.C. & Briggs, S.D. A charge-based interaction between histone H4 and Dot1 is required for H3K79 methylation and telomere silencing: identification of a new trans-histone pathway. Genes Dev. 21, 2018–2029 (2007).

    CAS  PubMed  PubMed Central  Google Scholar 

  78. Nishioka, K. et al. PR-Set7 is a nucleosome-specific methyltransferase that modifies lysine 20 of histone H4 and is associated with silent chromatin. Mol. Cell 9, 1201–1213 (2002).

    CAS  PubMed  Google Scholar 

  79. Kourmouli, N. et al. Heterochromatin and tri-methylated lysine 20 of histone H4 in animals. J. Cell Sci. 117, 2491–2501 (2004).

    CAS  PubMed  Google Scholar 

  80. Sarg, B., Helliger, W., Talasz, H., Koutzamani, E. & Lindner, H.H. Histone H4 hyperacetylation precludes histone H4 lysine 20 trimethylation. J. Biol. Chem. 279, 53458–53464 (2004).

    CAS  PubMed  Google Scholar 

  81. Talasz, H., Lindner, H.H., Sarg, B. & Helliger, W. Histone H4-lysine 20 monomethylation is increased in promoter and coding regions of active genes and correlates with hyperacetylation. J. Biol. Chem. 280, 38814–38822 (2005).

    CAS  PubMed  Google Scholar 

  82. Wang, H. et al. Methylation of histone H4 at arginine 3 facilitating transcriptional activation by nuclear hormone receptor. Science 293, 853–857 (2001).

    CAS  PubMed  Google Scholar 

  83. Strahl, B.D. et al. Methylation of histone H4 at arginine 3 occurs in vivo and is mediated by the nuclear receptor coactivator PRMT1. Curr. Biol. 11, 996–1000 (2001).

    CAS  PubMed  Google Scholar 

  84. Yu, M.C., Lamming, D.W., Eskin, J.A., Sinclair, D.A. & Silver, P.A. The role of protein arginine methylation in the formation of silent chromatin. Genes Dev. 20, 3249–3254 (2006).

    CAS  PubMed  PubMed Central  Google Scholar 

  85. Fabbrizio, E. et al. Negative regulation of transcription by the type II arginine methyltransferase PRMT5. EMBO Rep. 3, 641–645 (2002).

    CAS  PubMed  PubMed Central  Google Scholar 

  86. Pal, S. et al. mSin3A/histone deacetylase 2- and PRMT5-containing Brg1 complex is involved in transcriptional repression of the Myc target gene cad. Mol. Cell. Biol. 23, 7475–7487 (2003).

    CAS  PubMed  PubMed Central  Google Scholar 

  87. Le Guezennec, X. et al. MBD2/NuRD and MBD3/NuRD, two distinct complexes with different biochemical and functional properties. Mol. Cell. Biol. 26, 843–851 (2006).

    CAS  PubMed  PubMed Central  Google Scholar 

  88. Zhang, K. et al. Histone acetylation and deacetylation: identification of acetylation and methylation sites of HeLa histone H4 by mass spectrometry. Mol. Cell. Proteomics 1, 500–508 (2002).

    CAS  PubMed  Google Scholar 

  89. Utley, R.T., Lacoste, N., Jobin-Robitaille, O., Allard, S. & Cote, J. Regulation of NuA4 histone acetyltransferase activity in transcription and DNA repair by phosphorylation of histone H4. Mol. Cell. Biol. 25, 8179–8190 (2005).

    CAS  PubMed  PubMed Central  Google Scholar 

  90. Bode, A.M. & Dong, Z. Post-translational modification of p53 in tumorigenesis. Nat. Rev. Cancer 4, 793–805 (2004).

    CAS  PubMed  Google Scholar 

  91. Xirodimas, D.P., Saville, M.K., Bourdon, J.C., Hay, R.T. & Lane, D.P. Mdm2-mediated NEDD8 conjugation of p53 inhibits its transcriptional activity. Cell 118, 83–97 (2004).

    CAS  PubMed  Google Scholar 

  92. Huang, J. et al. Repression of p53 activity by Smyd2-mediated methylation. Nature 444, 629–632 (2006).

    CAS  PubMed  Google Scholar 

  93. Youmell, M., Park, S.J., Basu, S. & Price, B.D. Regulation of the p53 protein by protein kinase C alpha and protein kinase C zeta. Biochem. Biophys. Res. Commun. 245, 514–518 (1998).

    CAS  PubMed  Google Scholar 

  94. Chuikov, S. et al. Regulation of p53 activity through lysine methylation. Nature 432, 353–360 (2004).

    CAS  PubMed  Google Scholar 

  95. Liu, L. et al. p53 sites acetylated in vitro by PCAF and p300 are acetylated in vivo in response to DNA damage. Mol. Cell. Biol. 19, 1202–1209 (1999).

    CAS  PubMed  PubMed Central  Google Scholar 

  96. Zhang, K. et al. The Set1 methyltransferase opposes Ipl1 aurora kinase functions in chromosome segregation. Cell 122, 723–734 (2005).

    CAS  PubMed  PubMed Central  Google Scholar 

  97. Cheeseman, I.M. et al. Phospho-regulation of kinetochore-microtubule attachments by the Aurora kinase Ipl1p. Cell 111, 163–172 (2002).

    CAS  PubMed  Google Scholar 

  98. Grégoire, S. et al. Control of MEF2 transcriptional activity by coordinated phosphorylation and sumoylation. J. Biol. Chem. 281, 4423–4433 (2006).

    PubMed  Google Scholar 

  99. Grégoire, S. & Yang, X. Association with class IIa histone deacetylases upregulates the sumoylation of MEF2 transcription factors. Mol. Cell Biol. 25, 2273–2287 (2005).

    PubMed  PubMed Central  Google Scholar 

  100. Shalizi, A. et al. A calcium-regulated MEF2 sumoylation switch controls postsynaptic differentiation. Science 311, 1012–1017 (2006).

    CAS  PubMed  Google Scholar 

  101. Moore, J.D., Yazgan, O., Ataian, Y. & Krebs, J.E. Diverse roles for histone H2A modifications in DNA damage response pathways in yeast. Genetics 176, 15–25 (2006).

    PubMed  Google Scholar 

  102. Taverna, S.D. et al. Long-distance combinatorial linkage between methylation and acetylation on histone H3 N termini. Proc. Natl. Acad. Sci. USA 104, 2086–2091 (2007).

    CAS  PubMed  PubMed Central  Google Scholar 

  103. Bernstein, B.E. et al. A bivalent chromatin structure marks key developmental genes in embryonic stem cells. Cell 125, 315–326 (2006).

    CAS  PubMed  Google Scholar 

Download references

Acknowledgements

We thank A. Loyola and R. Chosed for critical comments and suggestions. J.A.L. is supported in part by a fellowship by the American Legion Auxiliary. Aspects of this work were supported by US National Institutes of Health grant GM067718 and a grant from the Robert A. Welch Foundation (G1371) to S.Y.R.D. We apologize to colleagues whose work was not cited owing to space limitations.

Author information

Authors and Affiliations

  1. Department of Biochemistry and Molecular Biology and Center for Epigenetics, Program in Genes and Development, University of Texas M. D. Anderson Cancer Center, Houston, 77030, Texas, USA

    John A Latham & Sharon Y R Dent

  2. Formerly known as Sharon Y. Roth.,

    Sharon Y R Dent

Authors
  1. John A Latham
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Sharon Y R Dent
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Sharon Y R Dent.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Latham, J., Dent, S. Cross-regulation of histone modifications. Nat Struct Mol Biol 14, 1017–1024 (2007). https://doi.org/10.1038/nsmb1307

Download citation

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1038/nsmb1307

This article is cited by

Search

Advanced 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