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Reading Histone Modifications

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Fundamentals of Chromatin

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Abstract

Histone posttranslational modifications (PTM) constitute one of the most important signaling pathways in the eukaryotic nucleus. In this chapter, we will discuss the molecular mechanisms by which histone PTM are deciphered by chromatin regulators and the functional outcomes of reading this signaling system.

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References

  • Ali M et al (2012) Tandem PHD FIngers of MORF/MOZ acetyltransferases display selectivity for acetylated histone H3 and are required for the association with chromatin. J Mol Biol 424:328

    PubMed  CAS  Google Scholar 

  • Arita K et al (2012) Recognition of modification status on a histone H3 tail by linked histone reader modules of the epigenetic regulator UHRF1. Proc Natl Acad Sci USA 109:12950

    PubMed  CAS  Google Scholar 

  • Armache KJ, Garlick JD, Canzio D, Narlikar GJ, Kingston RE (2011) Structural basis of silencing: Sir3 BAH domain in complex with a nucleosome at 3.0 A resolution. Science 334:977

    PubMed  CAS  Google Scholar 

  • Asturias FJ, Chung WH, Kornberg RD, Lorch Y (2002) Structural analysis of the RSC chromatin-remodeling complex. Proc Natl Acad Sci USA 99:13477

    PubMed  CAS  Google Scholar 

  • Ballare C et al (2012) Phf19 links methylated Lys36 of histone H3 to regulation of polycomb activity. Nat Struct Mol Biol 19:1257

    PubMed  CAS  Google Scholar 

  • Bannister AJ et al (2001) Selective recognition of methylated lysine 9 on histone H3 by the HP1 chromo domain. Nature 410:120

    PubMed  CAS  Google Scholar 

  • Bartke T et al (2010) Nucleosome-interacting proteins regulated by DNA and histone methylation. Cell 143:470

    PubMed  CAS  Google Scholar 

  • Bell O et al (2010) Accessibility of the Drosophila genome discriminates PcG repression, H4K16 acetylation and replication timing. Nat Struct Mol Biol 17:894

    PubMed  CAS  Google Scholar 

  • Blackledge NP et al (2010) CpG islands recruit a histone H3 lysine 36 demethylase. Mol Cell 38:179

    PubMed  CAS  Google Scholar 

  • Botuyan MV et al (2006) Structural basis for the methylation state-specific recognition of histone H4-K20 by 53BP1 and Crb2 in DNA repair. Cell 127:1361

    PubMed  CAS  Google Scholar 

  • Brien GL et al (2012) Polycomb PHF19 binds H3K36me3 and recruits PRC2 and demethylase NO66 to embryonic stem cell genes during differentiation. Nat Struct Mol Biol 19:1273

    PubMed  CAS  Google Scholar 

  • Briggs SD et al (2002) Gene silencing: trans-histone regulatory pathway in chromatin. Nature 418:498

    PubMed  CAS  Google Scholar 

  • Bua DJ et al (2009) Epigenome microarray platform for proteome-wide dissection of chromatin-signaling networks. PLoS One 4:e6789

    PubMed  Google Scholar 

  • Buhler M, Gasser SM (2009) Silent chromatin at the middle and ends: lessons from yeasts. EMBO J 28:2149

    PubMed  Google Scholar 

  • Canzio D et al (2011) Chromodomain-mediated oligomerization of HP1 suggests a nucleosome-bridging mechanism for heterochromatin assembly. Mol Cell 41:67

    PubMed  CAS  Google Scholar 

  • Carey M, Li B, Workman JL (2006) RSC exploits histone acetylation to abrogate the nucleosomal block to RNA polymerase II elongation. Mol Cell 24:481

    PubMed  CAS  Google Scholar 

  • Carrozza MJ et al (2005a) Stable incorporation of sequence specific repressors Ash1 and Ume6 into the Rpd3L complex. Biochim Biophys Acta 1731:77

    PubMed  CAS  Google Scholar 

  • Carrozza MJ et al (2005b) Histone H3 methylation by Set2 directs deacetylation of coding regions by Rpd3S to suppress spurious intragenic transcription. Cell 123:581

    PubMed  CAS  Google Scholar 

  • Chittuluru JR et al (2011) Structure and nucleosome interaction of the yeast NuA4 and Piccolo-NuA4 histone acetyltransferase complexes. Nat Struct Mol Biol 18:1196

    PubMed  CAS  Google Scholar 

  • Ciferri C et al (2012) Molecular architecture of human polycomb repressive complex 2. Elife 1:e00005

    PubMed  CAS  Google Scholar 

  • Cramer P, Bushnell DA, Kornberg RD (2001) Structural basis of transcription: RNA polymerase II at 2.8 angstrom resolution. Science 292:1863

    PubMed  CAS  Google Scholar 

  • Dang W, Bartholomew B (2007) Domain architecture of the catalytic subunit in the ISW2-nucleosome complex. Mol Cell Biol 27:8306

    PubMed  CAS  Google Scholar 

  • Davey CA, Sargent DF, Luger K, Maeder AW, Richmond TJ (2002) Solvent mediated interactions in the structure of the nucleosome core particle at 1.9 a resolution. J Mol Biol 319:1097

    PubMed  CAS  Google Scholar 

  • Davis JA, Takagi Y, Kornberg RD, Asturias FA (2002) Structure of the yeast RNA polymerase II holoenzyme: mediator conformation and polymerase interaction. Mol Cell 10:409

    PubMed  CAS  Google Scholar 

  • Dhalluin C et al (1999) Structure and ligand of a histone acetyltransferase bromodomain. Nature 399:491

    PubMed  CAS  Google Scholar 

  • Elsasser SJ et al (2012) DAXX envelops a histone H3.3-H4 dimer for H3.3-specific recognition. Nature 491:560

    PubMed  Google Scholar 

  • Ernst P, Wang J, Huang M, Goodman RH, Korsmeyer SJ (2001) MLL and CREB bind cooperatively to the nuclear coactivator CREB-binding protein. Mol Cell Biol 21:2249

    PubMed  CAS  Google Scholar 

  • Filion GJ et al (2010) Systematic protein location mapping reveals five principal chromatin types in Drosophila cells. Cell 143:212

    PubMed  CAS  Google Scholar 

  • Francis NJ, Kingston RE, Woodcock CL (2004) Chromatin compaction by a polycomb group protein complex. Science 306:1574

    PubMed  CAS  Google Scholar 

  • Francis NJ, Follmer NE, Simon MD, Aghia G, Butler JD (2009) Polycomb proteins remain bound to chromatin and DNA during DNA replication in vitro. Cell 137:110

    PubMed  CAS  Google Scholar 

  • Garske AL et al (2010) Combinatorial profiling of chromatin binding modules reveals multisite discrimination. Nat Chem Biol 6:283

    PubMed  CAS  Google Scholar 

  • Grob P et al (2006) Cryo-electron microscopy studies of human TFIID: conformational breathing in the integration of gene regulatory cues. Structure 14:511

    PubMed  CAS  Google Scholar 

  • Haldar S, Saini A, Nanda JS, Saini S, Singh J (2011) Role of Swi6/HP1 self-association-mediated recruitment of Clr4/Suv39 in establishment and maintenance of heterochromatin in fission yeast. J Biol Chem 286:9308

    PubMed  CAS  Google Scholar 

  • Hediger F, Gasser SM (2006) Heterochromatin protein 1: don’t judge the book by its cover! Curr Opin Genet Dev 16:143

    PubMed  CAS  Google Scholar 

  • Hickman MA, Froyd CA, Rusche LN (2011) Reinventing heterochromatin in budding yeasts: Sir2 and the origin recognition complex take center stage. Eukaryot Cell 10:1183

    PubMed  CAS  Google Scholar 

  • Hondele M, Ladurner AG (2011) The chaperone-histone partnership: for the greater good of histone traffic and chromatin plasticity. Curr Opin Struct Biol 21:698

    PubMed  CAS  Google Scholar 

  • Huh JW et al (2012) Multivalent di-nucleosome recognition enables the Rpd3S histone deacetylase complex to tolerate decreased H3K36 methylation levels. EMBO J 31:3564

    PubMed  CAS  Google Scholar 

  • Huyen Y et al (2004) Methylated lysine 79 of histone H3 targets 53BP1 to DNA double-strand breaks. Nature 432:406

    PubMed  CAS  Google Scholar 

  • Jacobson RH, Ladurner AG, King DS, Tjian R (2000) Structure and function of a human TAFII250 double bromodomain module. Science 288:1422

    PubMed  CAS  Google Scholar 

  • Jenuwein T, Allis CD (2001) Translating the histone code. Science 293:1074

    PubMed  CAS  Google Scholar 

  • Ji Y et al (2010) The in vivo pattern of binding of RAG1 and RAG2 to antigen receptor loci. Cell 141:419

    PubMed  CAS  Google Scholar 

  • Jungmichel S, Stucki M (2010) MDC1: the art of keeping things in focus. Chromosoma 119:337

    PubMed  CAS  Google Scholar 

  • Kim T, Buratowski S (2009) Dimethylation of H3K4 by Set1 recruits the Set3 histone deacetylase complex to 5' transcribed regions. Cell 137:259

    PubMed  CAS  Google Scholar 

  • Kim J et al (2006) Tudor, MBT and chromo domains gauge the degree of lysine methylation. EMBO Rep 7:397

    PubMed  CAS  Google Scholar 

  • Kim D et al (2010) Corecognition of DNA and a methylated histone tail by the MSL3 chromodomain. Nat Struct Mol Biol 17:1027

    PubMed  CAS  Google Scholar 

  • Kim T, Xu Z, Clauder-Munster S, Steinmetz LM, Buratowski S (2012) Set3 HDAC mediates effects of overlapping noncoding transcription on gene induction kinetics. Cell 150:1158

    PubMed  CAS  Google Scholar 

  • Kumar GS et al (2012) Sequence requirements for combinatorial recognition of histone H3 by the MRG15 and Pf1 subunits of the Rpd3S/Sin3S corepressor complex. J Mol Biol 422:519

    PubMed  CAS  Google Scholar 

  • Lan F et al (2007) Recognition of unmethylated histone H3 lysine 4 links BHC80 to LSD1-mediated gene repression. Nature 448:718

    PubMed  CAS  Google Scholar 

  • Larschan E et al (2007) MSL complex is attracted to genes marked by H3K36 trimethylation using a sequence-independent mechanism. Mol Cell 28:121

    PubMed  CAS  Google Scholar 

  • Lee MG, Wynder C, Cooch N, Shiekhattar R (2005) An essential role for CoREST in nucleosomal histone 3 lysine 4 demethylation. Nature 437:432

    PubMed  CAS  Google Scholar 

  • Lee MG et al (2006) Functional interplay between histone demethylase and deacetylase enzymes. Mol Cell Biol 26:6395

    PubMed  CAS  Google Scholar 

  • Lee JS et al (2007a) Histone crosstalk between H2B monoubiquitination and H3 methylation mediated by COMPASS. Cell 131:1084

    PubMed  CAS  Google Scholar 

  • Lee MG et al (2007b) Demethylation of H3K27 regulates polycomb recruitment and H2A ubiquitination. Science 318:447

    PubMed  CAS  Google Scholar 

  • Leurent C et al (2002) Mapping histone fold TAFs within yeast TFIID. EMBO J 21:3424

    PubMed  CAS  Google Scholar 

  • Li B, Carey M, Workman JL (2007a) The role of chromatin during transcription. Cell 128:707

    PubMed  CAS  Google Scholar 

  • Li B et al (2007b) Combined action of PHD and chromo domains directs the Rpd3S HDAC to transcribed chromatin. Science 316:1050

    PubMed  CAS  Google Scholar 

  • Li Q et al (2008) Acetylation of histone H3 lysine 56 regulates replication-coupled nucleosome assembly. Cell 134:244

    PubMed  CAS  Google Scholar 

  • Li B et al (2009) Histone H3 lysine 36 dimethylation (H3K36me2) is sufficient to recruit the Rpd3s histone deacetylase complex and to repress spurious transcription. J Biol Chem 284:7970

    PubMed  CAS  Google Scholar 

  • Lo SM et al (2012) A bridging model for persistence of a polycomb group protein complex through DNA replication in vitro. Mol Cell 46:784

    PubMed  CAS  Google Scholar 

  • Luco RF et al (2010) Regulation of alternative splicing by histone modifications. Science 327:996

    PubMed  CAS  Google Scholar 

  • Makde RD, England JR, Yennawar HP, Tan S (2010) Structure of RCC1 chromatin factor bound to the nucleosome core particle. Nature 467:562

    PubMed  CAS  Google Scholar 

  • Margueron R et al (2009) Role of the polycomb protein EED in the propagation of repressive histone marks. Nature 461:762

    PubMed  CAS  Google Scholar 

  • Martin C, Cao R, Zhang Y (2006) Substrate preferences of the EZH2 histone methyltransferase complex. J Biol Chem 281:8365

    PubMed  CAS  Google Scholar 

  • Martino F et al (2009) Reconstitution of yeast silent chromatin: multiple contact sites and O-AADPR binding load SIR complexes onto nucleosomes in vitro. Mol Cell 33:323

    PubMed  CAS  Google Scholar 

  • Mishima Y et al (2012) Hinge and chromoshadow of HP1alpha participate in recognition of K9 methylated histone H3 in nucleosomes. J Mol Biol 425:54–70

    PubMed  Google Scholar 

  • Moore SA, Ferhatoglu Y, Jia Y, Al-Jiab RA, Scott MJ (2010) Structural and biochemical studies on the chromo-barrel domain of male specific lethal 3 (MSL3) reveal a binding preference for mono- or dimethyllysine 20 on histone H4. J Biol Chem 285:40879

    PubMed  CAS  Google Scholar 

  • Munari F et al (2012) Methylation of lysine 9 in histone H3 directs alternative modes of highly dynamic interaction of heterochromatin protein hHP1beta with the nucleosome. J Biol Chem 287:33756

    PubMed  CAS  Google Scholar 

  • Musselman CA et al (2012a) Bivalent recognition of nucleosomes by the tandem PHD fingers of the CHD4 ATPase is required for CHD4-mediated repression. Proc Natl Acad Sci USA 109:787

    PubMed  CAS  Google Scholar 

  • Musselman CA et al (2012b) Molecular basis for H3K36me3 recognition by the Tudor domain of PHF1. Nat Struct Mol Biol 19:1266

    PubMed  CAS  Google Scholar 

  • Ng HH, Xu RM, Zhang Y, Struhl K (2002) Ubiquitination of histone H2B by Rad6 is required for efficient Dot1-mediated methylation of histone H3 lysine 79. J Biol Chem 277:34655

    PubMed  CAS  Google Scholar 

  • Oliver SS et al (2012) Multivalent recognition of histone tails by the PHD fingers of CHD5. Biochemistry 51:6534

    PubMed  CAS  Google Scholar 

  • Pasini D et al (2008) Coordinated regulation of transcriptional repression by the RBP2 H3K4 demethylase and polycomb-repressive complex 2. Gene Dev 22:1345

    PubMed  CAS  Google Scholar 

  • Pasini D et al (2010) JARID2 regulates binding of the Polycomb repressive complex 2 to target genes in ES cells. Nature 464:306

    PubMed  CAS  Google Scholar 

  • Peng JC et al (2009) Jarid2/Jumonji coordinates control of PRC2 enzymatic activity and target gene occupancy in pluripotent cells. Cell 139:1290

    PubMed  Google Scholar 

  • Qiu Y et al (2012) Combinatorial readout of unmodified H3R2 and acetylated H3K14 by the tandem PHD finger of MOZ reveals a regulatory mechanism for HOXA9 transcription. Gene Dev 26:1376

    PubMed  CAS  Google Scholar 

  • Richart AN, Brunner CI, Stott K, Murzina NV, Thomas JO (2012) Characterization of chromoshadow domain-mediated binding of heterochromatin protein 1alpha (HP1alpha) to histone H3. J Biol Chem 287:18730

    PubMed  CAS  Google Scholar 

  • Ruthenburg AJ, Li H, Patel DJ, Allis CD (2007) Multivalent engagement of chromatin modifications by linked binding modules. Nat Rev Mol Cell Biol 8:983

    PubMed  CAS  Google Scholar 

  • Ruthenburg AJ et al (2011) Recognition of a mononucleosomal histone modification pattern by BPTF via multivalent interactions. Cell 145:692

    PubMed  CAS  Google Scholar 

  • Schmitges FW et al (2011) Histone methylation by PRC2 is inhibited by active chromatin marks. Mol Cell 42:330

    PubMed  CAS  Google Scholar 

  • Schotta G et al (2002) Central role of Drosophila SU(VAR)3-9 in histone H3-K9 methylation and heterochromatic gene silencing. EMBO J 21:1121

    PubMed  CAS  Google Scholar 

  • Shen X et al (2009) Jumonji modulates polycomb activity and self-renewal versus differentiation of stem cells. Cell 139:1303

    PubMed  Google Scholar 

  • Shen Z et al (2010) A WD-repeat protein stabilizes ORC binding to chromatin. Mol Cell 40:99

    PubMed  CAS  Google Scholar 

  • Shindo H et al (2012) PHD finger of the SUMO ligase Siz/PIAS family in rice reveals specific binding for methylated histone H3 at lysine 4 and arginine 2. FEBS Lett 586:1783

    PubMed  CAS  Google Scholar 

  • Smith CL, Horowitz-Scherer R, Flanagan JF, Woodcock CL, Peterson CL (2003) Structural analysis of the yeast SWI/SNF chromatin remodeling complex. Nat Struct Biol 10:141

    PubMed  CAS  Google Scholar 

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

    PubMed  CAS  Google Scholar 

  • Stucki M et al (2005) MDC1 directly binds phosphorylated histone H2AX to regulate cellular responses to DNA double-strand breaks. Cell 123:1213

    PubMed  CAS  Google Scholar 

  • Su D et al (2012) Structural basis for recognition of H3K56-acetylated histone H3-H4 by the chaperone Rtt106. Nature 483:104

    PubMed  CAS  Google Scholar 

  • Sun ZW, Allis CD (2002) Ubiquitination of histone H2B regulates H3 methylation and gene silencing in yeast. Nature 418:104

    PubMed  CAS  Google Scholar 

  • Sural TH et al (2008) The MSL3 chromodomain directs a key targeting step for dosage compensation of the Drosophila melanogaster X chromosome. Nat Struct Mol Biol 15:1318

    PubMed  CAS  Google Scholar 

  • Tan M et al (2011) Identification of 67 histone marks and histone lysine crotonylation as a new type of histone modification. Cell 146:1016

    PubMed  CAS  Google Scholar 

  • Tsai WW et al (2010) TRIM24 links a non-canonical histone signature to breast cancer. Nature 468:927

    PubMed  CAS  Google Scholar 

  • van Ingen H et al (2008) Structural insight into the recognition of the H3K4me3 mark by the TFIID subunit TAF3. Structure 16:1245

    PubMed  Google Scholar 

  • Venkatesh S et al (2012) Set2 methylation of histone H3 lysine 36 suppresses histone exchange on transcribed genes. Nature 489:452

    PubMed  CAS  Google Scholar 

  • Vermeulen M et al (2007) Selective anchoring of TFIID to nucleosomes by trimethylation of histone H3 lysine 4. Cell 131:58

    PubMed  CAS  Google Scholar 

  • Vermeulen M et al (2010) Quantitative interaction proteomics and genome-wide profiling of epigenetic histone marks and their readers. Cell 142:967

    PubMed  CAS  Google Scholar 

  • Vogelauer M, Rubbi L, Lucas I, Brewer BJ, Grunstein M (2002) Histone acetylation regulates the time of replication origin firing. Mol Cell 10:1223

    PubMed  CAS  Google Scholar 

  • Voigt P et al (2012) Asymmetrically modified nucleosomes. Cell 151:181

    PubMed  CAS  Google Scholar 

  • Workman JL, Kingston RE (1998) Alteration of nucleosome structure as a mechanism of transcriptional regulation. Annu Rev Biochem 67:545

    PubMed  CAS  Google Scholar 

  • Wu PY, Ruhlmann C, Winston F, Schultz P (2004) Molecular architecture of the S. cerevisiae SAGA complex. Mol Cell 15:199

    PubMed  CAS  Google Scholar 

  • Xu C, Cui G, Botuyan MV, Mer G (2008) Structural basis for the recognition of methylated histone H3K36 by the Eaf3 subunit of histone deacetylase complex Rpd3S. Structure 16:1740

    PubMed  CAS  Google Scholar 

  • Xu C et al (2010) Binding of different histone marks differentially regulates the activity and specificity of polycomb repressive complex 2 (PRC2). Proc Natl Acad Sci USA 107:19266–19271

    PubMed  CAS  Google Scholar 

  • Yang N et al (2012) Distinct mode of methylated lysine-4 of histone H3 recognition by tandem tudor-like domains of Spindlin1. Proc Natl Acad Sci USA 109:17954

    PubMed  CAS  Google Scholar 

  • Yuan W et al (2012) Dense chromatin activates polycomb repressive complex 2 to regulate H3 lysine 27 methylation. Science 337:971

    PubMed  CAS  Google Scholar 

  • Yun M, Wu J, Workman JL, Li B (2011) Readers of histone modifications. Cell Res 21:564

    PubMed  CAS  Google Scholar 

  • Zhou JC, Blackledge NP, Farcas AM, Klose RJ (2012) Recognition of CpG island chromatin by KDM2A requires direct and specific interaction with linker DNA. Mol Cell Biol 32:479

    PubMed  CAS  Google Scholar 

  • Zunder RM, Antczak AJ, Berger JM, Rine J (2012) Two surfaces on the histone chaperone Rtt106 mediate histone binding, replication, and silencing. Proc Natl Acad Sci USA 109:E144

    PubMed  CAS  Google Scholar 

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Acknowledgments

We are grateful to Drs. F. Asturias, E. Nogales, C. Peterson, and P. Schultz for their contributions in Fig. 9.2. BL is a W.A. “Tex” Moncrief, Jr. Scholar in Medical Research, and supported by grants from the National Institutes of Health (R01GM090077), the Welch Foundation (I-1713), and the March of Dimes Foundation.

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  1. Department of Molecular Biology, University of Texas Southwest Medical Center, 5323 Harry Hines Blvd., Dallas, TX, 75390, USA

    Chun Ruan & Bing Li

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  1. Chun Ruan
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  2. Bing Li
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Correspondence to Bing Li .

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Editors and Affiliations

  1. Stowers Institute for Medical Research, Kansas City, Missouri, USA

    Jerry L. Workman

  2. Stowers Institute for Medical Research, Kansas City, Missouri, USA

    Susan M. Abmayr

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Ruan, C., Li, B. (2014). Reading Histone Modifications. In: Workman, J., Abmayr, S. (eds) Fundamentals of Chromatin. Springer, New York, NY. https://doi.org/10.1007/978-1-4614-8624-4_9

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