Multivalent engagement of chromatin modifications by linked binding modules (original) (raw)

• Cosgrove, M. S. Histone proteomics and the epigenetic regulation of nucleosome mobility. Expert Rev. Proteomics 4, 465–478 (2007). A recent overview of known histone PTMs as identified by mass spectrometry. It focuses on direct nucleosome-intrinsic effects of histone modifications and represents a nice catalogue of marks.
  CAS PubMed Google Scholar
• Clarkson, M. J., Wells, J. R., Gibson, F., Saint, R. & Tremethick, D. J. Regions of variant histone His2AvD required for Drosophila development. Nature 399, 694–697 (1999).
  CAS PubMed Google Scholar
• Bernstein, E. & Hake, S. B. The nucleosome: a little variation goes a long way. Biochem. Cell Biol. 84, 505–517 (2006).
  CAS PubMed Google Scholar
• Henikoff, S. & Ahmad, K. Assembly of variant histones into chromatin. Annu. Rev. Cell Dev. Biol. 21, 133–153 (2005). A definitive review on histone variants that describes the functional associations of variants with various stages of chromatin metabolism.
  CAS PubMed Google Scholar
• Pidoux, A. L. & Allshire, R. C. The role of heterochromatin in centromere function. Philos. Trans. R. Soc. Lond. B Biol. Sci. 360, 569–579 (2005).
  CAS PubMed PubMed Central Google Scholar
• Allis, C. D., Jenuwein, T. & Reinberg, D. Epigenetics (Cold Spring Harbor Laboratory Press, 2006).
  Google Scholar
• Sproul, D., Gilbert, N. & Bickmore, W. A. The role of chromatin structure in regulating the expression of clustered genes. Nature Rev. Genet. 6, 775–781 (2005).
  CAS PubMed Google Scholar
• Patterton, D. & Wolffe, A. P. Developmental roles for chromatin and chromosomal structure. Dev. Biol. 173, 2–13 (1996).
  CAS PubMed Google Scholar
• Barratt, M. J., Hazzalin, C. A., Cano, E. & Mahadevan, L. C. Mitogen-stimulated phosphorylation of histone H3 is targeted to a small hyperacetylation-sensitive fraction. Proc. Natl Acad. Sci. USA 91, 4781–4785 (1994).
  CAS PubMed PubMed Central Google Scholar
• 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
• Shi, Y. et al. Coordinated histone modifications mediated by a CtBP co-repressor complex. Nature 422, 735–738 (2003).
  CAS PubMed Google Scholar
• Bird, A. Perceptions of epigenetics. Nature 447, 396–398 (2007). A thoughtful examination of the meaning of the term epigenetics.
  CAS PubMed Google Scholar
• Goldberg, A. D., Allis, C. D. & Bernstein, E. Epigenetics: a landscape takes shape. Cell 128, 635–638 (2007).
  CAS PubMed Google Scholar
• Ptashne, M. On the use of the word 'epigenetic'. Curr. Biol. 17, R233–R236 (2007).
  CAS PubMed Google Scholar
• Klose, R. J. & Bird, A. P. Genomic DNA methylation: the mark and its mediators. Trends Biochem. Sci. 31, 89–97 (2006).
  CAS PubMed Google Scholar
• Berger, S. L. The complex language of chromatin regulation during transcription. Nature 447, 407–412 (2007).
  CAS PubMed Google Scholar
• Kouzarides, T. Chromatin modifications and their function. Cell 128, 693–705 (2007).
  CAS PubMed Google Scholar
• Strahl, B. D. & Allis, C. D. The language of covalent histone modifications. Nature 403, 41–45 (2000).
  CAS PubMed Google Scholar
• Huang, J. et al. Repression of p53 activity by Smyd2-mediated methylation. Nature 444, 629–632 (2006).
  Article CAS PubMed Google Scholar
• Seet, B. T., Dikic, I., Zhou, M. M. & Pawson, T. Reading protein modifications with interaction domains. Nature Rev. Mol. Cell Biol. 7, 473–483 (2006).
  CAS Google Scholar
• Yang, X. J. Multisite protein modification and intramolecular signaling. Oncogene 24, 1653–1662 (2005).
  CAS PubMed Google Scholar
• 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
• Birney, E. et al. Identification and analysis of functional elements in 1% of the human genome by the ENCODE pilot project. Nature 447, 799–816 (2007).
  CAS PubMed Google Scholar
• Brinkman, A. B. et al. Histone modification patterns associated with the human X chromosome. EMBO Rep. 7, 628–634 (2006).
  CAS PubMed PubMed Central Google Scholar
• Guenther, M. G., Levine, S. S., Boyer, L. A., Jaenisch, R. & Young, R. A. A chromatin landmark and transcription initiation at most promoters in human cells. Cell 130, 77–88 (2007). This study reports widespread abortive transcriptional initiation and the appearance of H3K4me3 at nearly every coding gene in ES cells.
  CAS PubMed PubMed Central Google Scholar
• Mikkelsen, T. S. et al. Genome-wide maps of chromatin state in pluripotent and lineage-committed cells. Nature 448, 553–560 (2007). A genome-wide profiling of chromatin states in stem cells as they differentiate, describing the first use of allele-specific ChIP. This work also represents the first direct comparison of ChIP-chip and ChIP-seq approaches.
  CAS PubMed PubMed Central Google Scholar
• Garcia, B. A., Shabanowitz, J. & Hunt, D. F. Characterization of histones and their post-translational modifications by mass spectrometry. Curr. Opin. Chem. Biol. 11, 66–73 (2007).
  CAS PubMed Google Scholar
• Cosgrove, M. S., Boeke, J. D. & Wolberger, C. Regulated nucleosome mobility and the histone code. Nature Struct. Mol. Biol. 11, 1037–1043 (2004).
  CAS Google Scholar
• Garcia-Ramirez, M., Rocchini, C. & Ausio, J. Modulation of chromatin folding by histone acetylation. J. Biol. Chem. 270, 17923–17928 (1995).
  CAS PubMed Google Scholar
• Tse, C., Sera, T., Wolffe, A. P. & Hansen, J. C. Disruption of higher-order folding by core histone acetylation dramatically enhances transcription of nucleosomal arrays by RNA polymerase III. Mol. Cell. Biol. 18, 4629–4638 (1998).
  CAS PubMed PubMed Central Google Scholar
• Shogren-Knaak, M. et al. Histone H4-K16 acetylation controls chromatin structure and protein interactions. Science 311, 844–847 (2006).
  CAS PubMed Google Scholar
• Jenuwein, T. & Allis, C. D. Translating the histone code. Science 293, 1074–1080 (2001).
  CAS PubMed Google Scholar
• Francis, N. J., Kingston, R. E. & Woodcock, C. L. Chromatin compaction by a polycomb group protein complex. Science 306, 1574–1577 (2004).
  CAS PubMed Google Scholar
• Zhao, T., Heyduk, T., Allis, C. D. & Eissenberg, J. C. Heterochromatin protein 1 binds to nucleosomes and DNA in vitro. J. Biol. Chem. 275, 28332–28338 (2000).
  CAS PubMed Google Scholar
• Nielsen, A. L. et al. Heterochromatin formation in mammalian cells: interaction between histones and HP1 proteins. Mol. Cell 7, 729–739 (2001).
  CAS PubMed Google Scholar
• Vermeulen, M. et al. Selective anchoring of TFIID to nucleosomes by trimethylation of histone H3 lysine 4. Cell 131, 58–69 (2007).
  CAS PubMed Google Scholar
• Dhalluin, C. et al. Structure and ligand of a histone acetyltransferase bromodomain. Nature 399, 491–496 (1999).
  CAS PubMed Google Scholar
• Ruthenburg, A. J., Allis, C. D. & Wysocka, J. Methylation of lysine 4 on histone H3: intricacy of writing and reading a single epigenetic mark. Mol. Cell 25, 15–30 (2007). A review that evaluates the biology and biophysics of H3K4 methylation and recognition, with an emphasis on structure and function.
  CAS PubMed Google Scholar
• 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. Nature Struct. Mol. Biol. 14, 1025–1040 (2007). A recent and comprehensive enumeration of chromatin-binding module structures in complex with modified histones, coupled to the attendant biology of these interactions.
  CAS Google Scholar
• Li, B., Carey, M. & Workman, J. L. The role of chromatin during transcription. Cell 128, 707–719 (2007).
  CAS PubMed Google Scholar
• 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
• van Attikum, H. & Gasser, S. M. The histone code at DNA breaks: a guide to repair? Nature Rev. Mol. Cell Biol. 6, 757–765 (2005).
  CAS Google Scholar
• Ahn, S. H. et al. Sterile 20 kinase phosphorylates histone H2B at serine 10 during hydrogen peroxide-induced apoptosis in S. cerevisiae. Cell 120, 25–36 (2005).
  CAS PubMed Google Scholar
• 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
• Baylin, S. B. & Ohm, J. E. Epigenetic gene silencing in cancer — a mechanism for early oncogenic pathway addiction? Nature Rev. Cancer 6, 107–116 (2006).
  CAS Google Scholar
• Wang, G. G., Allis, C. D. & Chi, P. Chromatin remodeling and cancer, part I: covalent histone modifications. Trends Mol. Med. 13, 363–372 (2007).
  CAS PubMed Google Scholar
• Jaenisch, R. & Bird, A. Epigenetic regulation of gene expression: how the genome integrates intrinsic and environmental signals. Nature Genet. 33 Suppl, 245–254 (2003).
  CAS PubMed Google Scholar
• Lan, F. et al. A histone H3 lysine 27 demethylase regulates animal posterior development. Nature 449, 689–694 (2007).
  CAS PubMed Google Scholar
• Swigut, T. & Wysocka, J. H3K27 demethylases, at long last. Cell 131, 29–32 (2007).
  CAS PubMed Google Scholar
• Turner, B. M. Histone acetylation and an epigenetic code. Bioessays 22, 836–845 (2000).
  CAS PubMed Google Scholar
• Li, H. et al. Molecular basis for site-specific read-out of histone H3K4me3 by the BPTF PHD finger of NURF. Nature 442, 91–95 (2006). Reports the first structure of a mixed two-effector module (one of each binding-domain type), as well as the first structures of the PHD fingers in complex with H3K4me3-binding modules.
  CAS PubMed PubMed Central Google Scholar
• Pena, P. V. et al. Molecular mechanism of histone H3K4me3 recognition by plant homeodomain of ING2. Nature 442, 100–103 (2006).
  CAS PubMed PubMed Central Google Scholar
• 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
• Wysocka, J. et al. A PHD finger of NURF couples histone H3 lysine 4 trimethylation with chromatin remodelling. Nature 442, 86–90 (2006).
  CAS PubMed Google Scholar
• Becker, P. B. Gene regulation: a finger on the mark. Nature 442, 31–32 (2006).
  CAS PubMed Google Scholar
• Henikoff, S. Histone modifications: combinatorial complexity or cumulative simplicity? Proc. Natl Acad. Sci. USA 102, 5308–5309 (2005).
  CAS PubMed PubMed Central Google Scholar
• Ptashne, M. & Gann, A. Transcriptional activation by recruitment. Nature 386, 569 (1997).
  CAS PubMed Google Scholar
• Hassan, A. H. et al. Selective recognition of acetylated histones by bromodomains in transcriptional co-activators. Biochem. J. 402, 125–133 (2007).
  CAS PubMed PubMed Central Google Scholar
• Krishnamurthy, V. M., Estroff, L. M. & Whitesides, G. M. in Fragment-based Approaches in Drug Discovery (eds Jahnke, W. & Erlanson, D. A.) 11–53 (Wiley-VCH, Weinheim, 2006). A comprehensive review of the thermodynamics of multivalency.
  Google Scholar
• Mammen, M., Choi, S.-K. & Whitesides, G. M. Polyvalent interactions in biological systems: implications for design and use of multivalent ligands and inhibitors. Angew. Chem. Int. Ed. Engl. 37, 2754–2794 (1998). This review is an exhaustive enumeration of examples of multivalency from the literature of chemistry and biology.
  PubMed Google Scholar
• Jencks, W. P. On the attribution and additivity of binding energies. Proc. Natl Acad. Sci. USA 78, 4046–4050 (1981).
  CAS PubMed PubMed Central Google Scholar
• Lee, Y. C. et al. Binding of synthetic oligosaccharides to the hepatic Gal/GalNAc lectin. Dependence on fine structural features. J. Biol. Chem. 258, 199–202 (1983).
  CAS PubMed Google Scholar
• Turner, B. M. Defining an epigenetic code. Nature Cell Biol. 9, 2–6 (2007).
  CAS PubMed Google Scholar
• Fraser, P. & Bickmore, W. Nuclear organization of the genome and the potential for gene regulation. Nature 447, 413–417 (2007). A wonderful review of chromatin territories by two of the key experts on in vivo chromatin structural organization.
  CAS PubMed Google Scholar
• Hecht, A. & Grunstein, M. Mapping DNA interaction sites of chromosomal proteins using immunoprecipitation and polymerase chain reaction. Methods Enzymol. 304, 399–414 (1999).
  CAS PubMed Google Scholar
• Bernstein, B. E. et al. Methylation of histone H3 Lys 4 in coding regions of active genes. Proc. Natl Acad. Sci. USA 99, 8695–8700 (2002).
  CAS PubMed PubMed Central Google Scholar
• Robyr, D. et al. Microarray deacetylation maps determine genome-wide functions for yeast histone deacetylases. Cell 109, 437–446 (2002).
  CAS PubMed Google Scholar
• Barski, A. et al. High-resolution profiling of histone methylations in the human genome. Cell 129, 823–837 (2007). The first systematic application of ChIP-seq methodology to histone PTMs reports numerous histone modifications and their correlations to chromatin states. A comparison of different methylation states at the same Lys residue is also described.
  CAS PubMed Google Scholar
• Bernstein, B. E. et al. Genomic maps and comparative analysis of histone modifications in human and mouse. Cell 120, 169–181 (2005).
  CAS PubMed Google Scholar
• Wade, P. A., Pruss, D. & Wolffe, A. P. Histone acetylation: chromatin in action. Trends Biochem. Sci. 22, 128–132 (1997).
  CAS PubMed Google Scholar
• Kurdistani, S. K., Tavazoie, S. & Grunstein, M. Mapping global histone acetylation patterns to gene expression. Cell 117, 721–733 (2004).
  CAS PubMed Google Scholar
• Schubeler, D. et al. The histone modification pattern of active genes revealed through genome-wide chromatin analysis of a higher eukaryote. Genes Dev. 18, 1263–1271 (2004).
  PubMed PubMed Central Google Scholar
• Johnson, E. M., Sterner, R. & Allfrey, V. G. Altered nucleosomes of active nucleolar chromatin contain accessible histone H3 in its hyperacetylated forms. J. Biol. Chem. 262, 6943–6946 (1987).
  CAS PubMed Google Scholar
• Ura, K., Kurumizaka, H., Dimitrov, S., Almouzni, G. & Wolffe, A. P. Histone acetylation: influence on transcription, nucleosome mobility and positioning, and linker histone-dependent transcriptional repression. EMBO J. 16, 2096–2107 (1997).
  CAS PubMed PubMed Central Google Scholar
• Wang, X. & Hayes, J. J. Site-specific binding affinities within the H2B tail domain indicate specific effects of lysine acetylation. J. Biol. Chem. 282, 23867–32876 (2007).
  Google Scholar
• Jacobson, R. H., Ladurner, A. G., King, D. S. & Tjian, R. Structure and function of a human TAFII250 double bromodomain module. Science 288, 1422–1425 (2000). Reports the first dual histone-binding module structure, and represents a landmark study indicating cooperative binding by two bromodomains of multiply acetylated histone substrates.
  CAS PubMed Google Scholar
• Kasten, M. et al. Tandem bromodomains in the chromatin remodeler RSC recognize acetylated histone H3 Lys14. EMBO J. 23, 1348–1359 (2004).
  CAS PubMed PubMed Central Google Scholar
• Ladurner, A. G., Inouye, C., Jain, R. & Tjian, R. Bromodomains mediate an acetyl-histone encoded antisilencing function at heterochromatin boundaries. Mol. Cell 11, 365–376 (2003).
  CAS PubMed Google Scholar
• Mujtaba, S. et al. Structural mechanism of the bromodomain of the coactivator CBP in p53 transcriptional activation. Mol. Cell 13, 251–263 (2004).
  CAS PubMed Google Scholar
• Mujtaba, S., Zeng, L. & Zhou, M. M. Structure and acetyl-lysine recognition of the bromodomain. Oncogene 26, 5521–5527 (2007).
  CAS PubMed Google Scholar
• Mellor, J. Dynamic nucleosomes and gene transcription. Trends Genet. 22, 320–329 (2006).
  CAS PubMed Google Scholar
• Huang, Y., Fang, J., Bedford, M. T., Zhang, Y. & Xu, R. M. Recognition of histone H3 lysine-4 methylation by the double tudor domain of JMJD2A. Science 312, 748–751 (2006).
  CAS PubMed Google Scholar
• Klose, R. J. et al. The transcriptional repressor JHDM3A demethylates trimethyl histone H3 lysine 9 and lysine 36. Nature 442, 312–316 (2006).
  CAS PubMed Google Scholar
• Li, B. et al. Combined action of PHD and chromo domains directs the Rpd3S HDAC to transcribed chromatin. Science 316, 1050–1054 (2007). An important example of multivalent binding capacity that is combinatorially assembled into chromatin-modification complexes.
  CAS PubMed Google Scholar
• Berndsen, C. E. et al. Nucleosome recognition by the Piccolo NuA4 histone acetyltransferase complex. Biochemistry 46, 2091–2099 (2007).
  CAS PubMed Google Scholar
• Kim, Y. C., Grable, J. C., Love, R., Greene, P. J. & Rosenberg, J. M. Refinement of _Eco_RI endonuclease crystal structure: a revised protein chain tracing. Science 249, 1307–1309 (1990).
  CAS PubMed Google Scholar
• Rao, J., Lahiri, J., Isaacs, L., Weis, R. M. & Whitesides, G. M. A trivalent system from vancomycin.D-ala-D-Ala with higher affinity than avidin.biotin. Science 280, 708–711 (1998). A landmark study in multivalency that demonstrates the enormous gain in overall affinity by systematic comparison of monovalent and trivalent vancomycin molecules.
  CAS PubMed Google Scholar
• Khorasanizadeh, S. The nucleosome: from genomic organization to genomic regulation. Cell 116, 259–272 (2004).
  CAS PubMed Google Scholar
• Martinez-Campa, C. et al. Precise nucleosome positioning and the TATA box dictate requirements for the histone H4 tail and the bromodomain factor Bdf1. Mol. Cell 15, 69–81 (2004).
  CAS PubMed Google Scholar
• Matangkasombut, O. & Buratowski, S. Different sensitivities of bromodomain factors 1 and 2 to histone H4 acetylation. Mol. Cell 11, 353–363 (2003).
  CAS PubMed Google Scholar
• Lindroth, A. M. et al. Dual histone H3 methylation marks at lysines 9 and 27 required for interaction with CHROMOMETHYLASE3. EMBO J. 23, 4286–4296 (2004).
  CAS PubMed Google Scholar
• Fischle, W. et al. Regulation of HP1–chromatin binding by histone H3 methylation and phosphorylation. Nature 438, 1116–1122 (2005).
  CAS PubMed Google Scholar
• 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
• 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
• 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
• Shi, X. et al. Proteome-wide analysis in Saccharomyces cerevisiae identifies several PHD fingers as novel direct and selective binding modules of histone H3 methylated at either lysine 4 or lysine 36. J. Biol. Chem. 282, 2450–2455 (2007).
  CAS PubMed Google Scholar
• You, A., Tong, J. K., Grozinger, C. M. & Schreiber, S. L. CoREST is an integral component of the CoREST–human histone deacetylase complex. Proc. Natl Acad. Sci. USA 98, 1454–1458 (2001).
  CAS PubMed PubMed Central Google Scholar
• Verreault, A., Kaufman, P. D., Kobayashi, R. & Stillman, B. Nucleosomal DNA regulates the core-histone-binding subunit of the human Hat1 acetyltransferase. Curr. Biol. 8, 96–108 (1998).
  CAS PubMed Google Scholar
• Yang, M. et al. Structural basis for CoREST-dependent demethylation of nucleosomes by the human LSD1 histone demethylase. Mol. Cell 23, 377–387 (2006).
  CAS PubMed Google Scholar
• 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
• Lan, F. et al. Recognition of unmethylated histone H3 lysine 4 links BHC80 to LSD1-mediated gene repression. Nature 448, 718–722 (2007).
  CAS PubMed PubMed Central Google Scholar
• Ooi, S. K. et al. DNMT3L connects unmethylated lysine 4 of histone H3 to de novo methylation of DNA. Nature 448, 714–717 (2007).
  CAS PubMed PubMed Central Google Scholar
• Barak, O. et al. Isolation of human NURF: a regulator of Engrailed gene expression. EMBO J. 22, 6089–6100 (2003).
  CAS PubMed PubMed Central Google Scholar
• 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).
  CAS PubMed PubMed Central Google Scholar
• Vandemark, A. P. et al. Autoregulation of the RSC4 tandem bromodomain by GCN5 acetylation. Mol. Cell 27, 817–828 (2007).
  CAS PubMed PubMed Central Google Scholar
• Segal, E. et al. A genomic code for nucleosome positioning. Nature 442, 772–778 (2006).
  CAS PubMed PubMed Central Google Scholar
• 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
• Dodd, I. B., Micheelsen, M. A., Sneppen, K. & Thon, G. Theoretical analysis of epigenetic cell memory by nucleosome modification. Cell 129, 813–822 (2007).
  CAS PubMed Google Scholar
• Schreiber, S. L. & Bernstein, B. E. Signaling network model of chromatin. Cell 111, 771–778 (2002).
  CAS PubMed Google Scholar
• Filippova, G. N. et al. An exceptionally conserved transcriptional repressor, CTCF, employs different combinations of zinc fingers to bind diverged promoter sequences of avian and mammalian c-myc oncogenes. Mol. Cell. Biol. 16, 2802–2813 (1996).
  CAS PubMed PubMed Central Google Scholar
• Zubarev, R. A. et al. Electron capture dissociation for structural characterization of multiply charged protein cations. Anal. Chem. 72, 563–573 (2000).
  CAS PubMed Google Scholar
• Mikesh, L. M. et al. The utility of ETD mass spectrometry in proteomic analysis. Biochim. Biophys. Acta 1764, 1811–1822 (2006).
  CAS PubMed PubMed Central Google Scholar
• Chicoine, L. G., Schulman, I. G., Richman, R., Cook, R. G. & Allis, C. D. Nonrandom utilization of acetylation sites in histones isolated from Tetrahymena. Evidence for functionally distinct H4 acetylation sites. J. Biol. Chem. 261, 1071–1076 (1986).
  CAS PubMed Google Scholar
• Shechter, D., Dormann, H. L., Allis, C. D. & Hake, S. B. Extraction, purification and analysis of histones. Nature Protoc. 2, 1445–1457 (2007).
  CAS Google Scholar
• Metivier, R. et al. Transcriptional complexes engaged by apo-estrogen receptor-α isoforms have divergent outcomes. EMBO J. 23, 3653–3666 (2004).
  CAS PubMed PubMed Central Google Scholar
• Shang, Y., Hu, X., DiRenzo, J., Lazar, M. A. & Brown, M. Cofactor dynamics and sufficiency in estrogen receptor-regulated transcription. Cell 103, 843–852 (2000).
  CAS PubMed Google Scholar
• Dawson, P. E., Muir, T. W., Clark-Lewis, I. & Kent, S. B. Synthesis of proteins by native chemical ligation. Science 266, 776–779 (1994).
  CAS PubMed Google Scholar
• Shogren-Knaak, M. A. & Peterson, C. L. Creating designer histones by native chemical ligation. Methods Enzymol. 375, 62–76 (2004).
  CAS PubMed Google Scholar
• Chatterjee, C., McGinty, R. K., Pellois, J. P. & Muir, T. W. Auxiliary-mediated site-specific peptide ubiquitylation. Angew. Chem. Int. Ed. Engl. 46, 2814–2818 (2007).
  CAS PubMed Google Scholar
• Simon, M. D. et al. The site-specific installation of methyl-lysine analogs into recombinant histones. Cell 128, 1003–1012 (2007).
  CAS PubMed PubMed Central Google Scholar
• Dorigo, B., Schalch, T., Bystricky, K. & Richmond, T. J. Chromatin fiber folding: requirement for the histone H4 N-terminal tail. J. Mol. Biol. 327, 85–96 (2003).
  CAS PubMed Google Scholar
• 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
• Xiao, H. et al. Dual functions of largest NURF subunit NURF301 in nucleosome sliding and transcription factor interactions. Mol. Cell 8, 531–543 (2001).
  CAS PubMed Google Scholar
• Turner, B. M. Cellular memory and the histone code. Cell 111, 285–291 (2002).
  CAS PubMed Google Scholar
• 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
• Garcia, B. A. et al. Modifications of human histone H3 variants during mitosis. Biochemistry 44, 13202–13213 (2005).
  CAS PubMed Google Scholar
• Daujat, S. et al. Crosstalk between CARM1 methylation and CBP acetylation on histone H3. Curr. Biol. 12, 2090–2097 (2002).
  CAS PubMed Google Scholar
• Loyola, A., Bonaldi, T., Roche, D., Imhof, A. & Almouzni, G. PTMs on H3 variants before chromatin assembly potentiate their final epigenetic state. Mol. Cell 24, 309–316 (2006).
  CAS PubMed Google Scholar
• Lindroth, A. M. et al. Requirement of CHROMOMETHYLASE3 for maintenance of CpXpG methylation. Science 292, 2077–2080 (2001).
  CAS PubMed Google Scholar
• 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