Skip to main content

Advertisement

SpringerLink
Log in

The impact of histone post-translational modifications on developmental gene regulation

  • Review Article
  • Published:
Amino Acids Aims and scope Submit manuscript

Abstract

Eukaryotic genomic DNA is orderly compacted to fit into the nucleus and to inhibit accessibility of specific sequences. DNA is manipulated in many different ways by bound RNA and proteins within the composite material known as chromatin. All of the biological processes that require access to genomic DNA (such as replication, recombination and transcription) therefore are dependent on the precise characteristics of chromatin in eukaryotes. This distinction underlies a fundamental property of eukaryotic versus prokaryotic gene regulation such that chromatin structure must be regulated to precisely repress or relieve repression of particular regions of the genome in an appropriate spatio-temporal manner. As well as playing a key role in structuring genomic DNA, histones are subject to site-specific modifications that can influence the organization of chromatin structure. This review examines the molecular processes regulating site-specific histone acetylation, methylation and phosphorylation with an emphasis on how these processes underpin differentiation-regulated transcription.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3

Similar content being viewed by others

References

  • Adachi S, Rothenberg EV (2005) Cell-type-specific epigenetic marking of the IL2 gene at a distal cis-regulatory region in competent, nontranscribing T-cells. Nucleic Acids Res 33:3200–3210

    Article  PubMed  CAS  Google Scholar 

  • Ahel D, Horejsi Z, Wiechens N, Polo SE, Garcia-Wilson E, Ahel I, Flynn H, Skehel M, West SC, Jackson SP, Owen-Hughes T, Boulton SJ (2009) Poly(ADP-ribose)-dependent regulation of DNA repair by the chromatin remodeling enzyme ALC1. Science 325:1240–1243

    Article  PubMed  CAS  Google Scholar 

  • Allfrey VG, Littau VC, Mirsky AE (1963) On the role of of histones in regulation ribonucleic acid synthesis in the cell nucleus. Proc Natl Acad Sci USA 49:414–421

    Article  PubMed  CAS  Google Scholar 

  • Altaf M, Auger A, Covic M, Cote J (2009) Connection between histone H2A variants and chromatin remodeling complexes. Biochem Cell Biol 87:35–50

    Article  PubMed  CAS  Google Scholar 

  • Ansel KM, Lee DU, Rao A (2003) An epigenetic view of helper T cell differentiation. Nat Immunol 4:616–623

    Article  PubMed  CAS  Google Scholar 

  • Araki Y, Wang Z, Zang C, Wood WH 3rd, Schones D, Cui K, Roh TY, Lhotsky B, Wersto RP, Peng W, Becker KG, Zhao K, Weng NP (2009) Genome-wide analysis of histone methylation reveals chromatin state-based regulation of gene transcription and function of memory CD8+ T cells. Immunity 30:912–925

    Article  PubMed  CAS  Google Scholar 

  • Attia M, Rachez C, De Pauw A, Avner P, Rogner UC (2007) Nap1l2 promotes histone acetylation activity during neuronal differentiation. Mol Cell Biol 27:6093–6102

    Article  PubMed  CAS  Google Scholar 

  • Attwood PV, Piggott MJ, Zu XL, Besant PG (2007) Focus on phosphohistidine. Amino Acids 32:145–156

    Article  PubMed  CAS  Google Scholar 

  • Avni O, Lee D, Macian F, Szabo SJ, Glimcher LH, Rao A (2002) T(H) cell differentiation is accompanied by dynamic changes in histone acetylation of cytokine genes. Nat Immunol 3:643–651

    Article  PubMed  CAS  Google Scholar 

  • Bannister AJ, Kouzarides T (2005) Reversing histone methylation. Nature 436:1103–1106

    Article  PubMed  CAS  Google Scholar 

  • Bannister AJ, Schneider R, Kouzarides T (2002) Histone methylation: dynamic or static? Cell 109:801–806

    Article  PubMed  CAS  Google Scholar 

  • Barski A, Cuddapah S, Cui K, Roh TY, Schones DE, Wang Z, Wei G, Chepelev I, Zhao K (2007) High-resolution profiling of histone methylations in the human genome. Cell 129:823–837

    Article  PubMed  CAS  Google Scholar 

  • Bassett A, Cooper S, Wu C, Travers A (2009) The folding and unfolding of eukaryotic chromatin. Curr Opin Genet Dev 19:159–165

    Article  PubMed  CAS  Google Scholar 

  • Bell O, Schubeler D (2009) Chromatin: sub out the replacement. Curr Biol 19:R545–R547

    Article  PubMed  CAS  Google Scholar 

  • Belova GI, Postnikov YV, Furusawa T, Birger Y, Bustin M (2008) Chromosomal protein HMGN1 enhances the heat shock-induced remodeling of Hsp70 chromatin. J Biol Chem 283:8080–8088

    Article  PubMed  CAS  Google Scholar 

  • Bender MA, Bulger M, Close J, Groudine M (2000) Beta-globin gene switching and DNase I sensitivity of the endogenous beta-globin locus in mice do not require the locus control region. Mol Cell 5:387–393

    Article  PubMed  CAS  Google Scholar 

  • Bernstein BE, Mikkelsen TS, Xie X, Kamal M, Huebert DJ, Cuff J, Fry B, Meissner A, Wernig M, Plath K, Jaenisch R, Wagschal A, Feil R, Schreiber SL, Lander ES (2006) A bivalent chromatin structure marks key developmental genes in embryonic stem cells. Cell 125:315–326

    Article  PubMed  CAS  Google Scholar 

  • Besant PG, Attwood PV (2000) Detection of a mammalian histone H4 kinase that has yeast histidine kinase-like enzymic activity. Int J Biochem Cell Biol 32:243–253

    Article  PubMed  CAS  Google Scholar 

  • Besant PG, Tan E, Attwood PV (2003) Mammalian protein histidine kinases. Int J Biochem Cell Biol 35:297–309

    Article  PubMed  CAS  Google Scholar 

  • Borde V, Robine N, Lin W, Bonfils S, Geli V, Nicolas A (2009) Histone H3 lysine 4 trimethylation marks meiotic recombination initiation sites. EMBO J 28:99–111

    Article  PubMed  CAS  Google Scholar 

  • Bottardi S, Aumont A, Grosveld F, Milot E (2003) Developmental stage-specific epigenetic control of human beta-globin gene expression is potentiated in hematopoietic progenitor cells prior to their transcriptional activation. Blood 102:3989–3997

    Article  PubMed  CAS  Google Scholar 

  • Bottomley MJ (2004) Structures of protein domains that create or recognize histone modifications. EMBO Rep 5:464–469

    Article  PubMed  CAS  Google Scholar 

  • Bradbury EM (1992) Reversible histone modifications and the chromosome cell cycle. Bioessays 14:9–16

    Article  PubMed  CAS  Google Scholar 

  • Bream JH, Hodge DL, Gonsky R, Spolski R, Leonard WJ, Krebs S, Targan S, Morinobu A, O’Shea JJ, Young HA (2004) A distal region in the interferon-gamma gene is a site of epigenetic remodeling and transcriptional regulation by interleukin-2. J Biol Chem 279:41249–41257

    Article  PubMed  CAS  Google Scholar 

  • Brittle AL, Nanba Y, Ito T, Ohkura H (2007) Concerted action of Aurora B, Polo and NHK-1 kinases in centromere-specific histone 2A phosphorylation. Exp Cell Res 313:2780–2785

    Article  PubMed  CAS  Google Scholar 

  • Buard J, Barthes P, Grey C, de Massy B (2009) Distinct histone modifications define initiation and repair of meiotic recombination in the mouse. EMBO J 28:2616–2624

    Article  PubMed  CAS  Google Scholar 

  • Bulger M, Schubeler D, Bender MA, Hamilton J, Farrell CM, Hardison RC, Groudine M (2003) A complex chromatin landscape revealed by patterns of nuclease sensitivity and histone modification within the mouse beta-globin locus. Mol Cell Biol 23:5234–5244

    Article  PubMed  CAS  Google Scholar 

  • Cai S, Han HJ, Kohwi-Shigematsu T (2003) Tissue-specific nuclear architecture and gene expression regulated by SATB1. Nat Genet 34:42–51

    Article  PubMed  CAS  Google Scholar 

  • Campos EI, Reinberg D (2009) Histones: annotating chromatin. Annu Rev Genet 43:559–599

    Google Scholar 

  • Cao R, Zhang Y (2004) The functions of E(Z)/EZH2-mediated methylation of lysine 27 in histone H3. Curr Opin Genet Dev 14:155–164

    Article  PubMed  CAS  Google Scholar 

  • Cao R, Wang L, Wang H, Xia L, Erdjument-Bromage H, Tempst P, Jones RS, Zhang Y (2002) Role of histone H3 lysine 27 methylation in polycomb-group silencing. Science 298:1039–1043

    Article  PubMed  CAS  Google Scholar 

  • Cao R, Wang H, He J, Erdjument-Bromage H, Tempst P, Zhang Y (2008) Role of hPHF1 in H3K27 methylation and Hox gene silencing. Mol Cell Biol 28:1862–1872

    Article  PubMed  CAS  Google Scholar 

  • Chakrabarti SK, Francis J, Ziesmann SM, Garmey JC, Mirmira RG (2003) Covalent histone modifications underlie the developmental regulation of insulin gene transcription in pancreatic beta cells. J Biol Chem 278:23617–23623

    Article  PubMed  CAS  Google Scholar 

  • Chang S, Collins PL, Aune TM (2008) T-bet dependent removal of Sin3A-histone deacetylase complexes at the Ifng locus drives Th1 differentiation. J Immunol 181:8372–8381

    PubMed  CAS  Google Scholar 

  • Chaturvedi CP, Hosey AM, Palii C, Perez-Iratxeta C, Nakatani Y, Ranish JA, Dilworth FJ, Brand M (2009) Dual role for the methyltransferase G9a in the maintenance of beta-globin gene transcription in adult erythroid cells. Proc Natl Acad Sci USA 106:18303–18308

    Article  PubMed  Google Scholar 

  • Chen HT, Hahn S (2004) Mapping the location of TFIIB within the RNA polymerase II transcription preinitiation complex: a model for the structure of the PIC. Cell 119:169–180

    Article  PubMed  CAS  Google Scholar 

  • Chen CC, Smith DL, Bruegger BB, Halpern RM, Smith RA (1974) Occurrence and distribution of acid-labile histone phosphates in regenerating rat liver. Biochemistry 13:3785–3789

    Article  PubMed  CAS  Google Scholar 

  • Chen CC, Bruegger BB, Kern CW, Lin YC, Halpern RM, Smith RA (1977) Phosphorylation of nuclear proteins in rat regenerating liver. Biochemistry 16:4852–4855

    Article  PubMed  CAS  Google Scholar 

  • Cheung P, Allis CD, Sassone-Corsi P (2000) Signaling to chromatin through histone modifications. Cell 103:263–271

    Article  PubMed  CAS  Google Scholar 

  • Chi AS, Bernstein BE (2009) Developmental biology. Pluripotent chromatin state. Science 323:220–221

    Article  PubMed  CAS  Google Scholar 

  • Clayton AL, Hazzalin CA, Mahadevan LC (2006) Enhanced histone acetylation and transcription: a dynamic perspective. Mol Cell 23:289–296

    Article  PubMed  CAS  Google Scholar 

  • Cloos PA, Christensen J, Agger K, Helin K (2008) Erasing the methyl mark: histone demethylases at the center of cellular differentiation and disease. Genes Dev 22:1115–1140

    Article  PubMed  CAS  Google Scholar 

  • Cook PJ, Ju BG, Telese F, Wang X, Glass CK, Rosenfeld MG (2009) Tyrosine dephosphorylation of H2AX modulates apoptosis and survival decisions. Nature 458:591–596

    Article  PubMed  CAS  Google Scholar 

  • Corpet A, Almouzni G (2009) Making copies of chromatin: the challenge of nucleosomal organization and epigenetic information. Trends Cell Biol 19:29–41

    Article  PubMed  CAS  Google Scholar 

  • Cosgrove MS, Wolberger C (2005) How does the histone code work? Biochem Cell Biol 83:468–476

    Article  PubMed  CAS  Google Scholar 

  • Cosgrove MS, Boeke JD, Wolberger C (2004) Regulated nucleosome mobility and the histone code. Nat Struct Mol Biol 11:1037–1043

    Article  PubMed  CAS  Google Scholar 

  • Craig JM (2005) Heterochromatin—many flavours, common themes. Bioessays 27:17–28

    Article  PubMed  CAS  Google Scholar 

  • Dawson MA, Bannister AJ, Gottgens B, Foster SD, Bartke T, Green AR, Kouzarides T (2009) JAK2 phosphorylates histone H3Y41 and excludes HP1alpha from chromatin. Nature 461:819–822

    Article  PubMed  CAS  Google Scholar 

  • de la Serna IL, Ohkawa Y, Berkes CA, Bergstrom DA, Dacwag CS, Tapscott SJ, Imbalzano AN (2005) MyoD targets chromatin remodeling complexes to the myogenin locus prior to forming a stable DNA-bound complex. Mol Cell Biol 25:3997–4009

    Article  CAS  Google Scholar 

  • Delmas V, Stokes DG, Perry RP (1993) A mammalian DNA-binding protein that contains a chromodomain and an SNF2/SWI2-like helicase domain. Proc Natl Acad Sci USA 90:2414–2418

    Article  PubMed  CAS  Google Scholar 

  • Deng Z, Norseen J, Wiedmer A, Riethman H, Lieberman PM (2009) TERRA RNA binding to TRF2 facilitates heterochromatin formation and ORC recruitment at telomeres. Mol Cell 35:403–413

    Article  PubMed  CAS  Google Scholar 

  • Denu JM (2005) The Sir 2 family of protein deacetylases. Curr Opin Chem Biol 9:431–440

    Article  PubMed  CAS  Google Scholar 

  • Dey A, Chitsaz F, Abbasi A, Misteli T, Ozato K (2003) The double bromodomain protein Brd4 binds to acetylated chromatin during interphase and mitosis. Proc Natl Acad Sci USA 100:8758–8763

    Article  PubMed  CAS  Google Scholar 

  • Dhalluin C, Carlson JE, Zeng L, He C, Aggarwal AK, Zhou MM (1999) Structure and ligand of a histone acetyltransferase bromodomain. Nature 399:491–496

    Article  PubMed  CAS  Google Scholar 

  • Dinger ME, Amaral PP, Mercer TR, Pang KC, Bruce SJ, Gardiner BB, Askarian-Amiri ME, Ru K, Solda G, Simons C, Sunkin SM, Crowe ML, Grimmond SM, Perkins AC, Mattick JS (2008) Long noncoding RNAs in mouse embryonic stem cell pluripotency and differentiation. Genome Res 18:1433–1445

    Article  PubMed  CAS  Google Scholar 

  • Downs JA, Lowndes NF, Jackson SP (2000) A role for Saccharomyces cerevisiae histone H2A in DNA repair. Nature 408:1001–1004

    Article  PubMed  CAS  Google Scholar 

  • Edmunds JW, Mahadevan LC, Clayton AL (2008) Dynamic histone H3 methylation during gene induction: HYPB/Setd2 mediates all H3K36 trimethylation. EMBO J 27:406–420

    Article  PubMed  CAS  Google Scholar 

  • Fields PE, Kim ST, Flavell RA (2002) Cutting edge: changes in histone acetylation at the IL-4 and IFN-gamma loci accompany Th1/Th2 differentiation. J Immunol 169:647–650

    PubMed  CAS  Google Scholar 

  • Fillingham J, Greenblatt JF (2008) A histone code for chromatin assembly. Cell 134:206–208

    Article  PubMed  CAS  Google Scholar 

  • Fish JE, Matouk CC, Rachlis A, Lin S, Tai SC, D’Abreo C, Marsden PA (2005) The expression of endothelial nitric-oxide synthase is controlled by a cell-specific histone code. J Biol Chem 280:24824–24838

    Article  PubMed  CAS  Google Scholar 

  • Flajollet S, Lefebvre B, Rachez C, Lefebvre P (2006) Distinct roles of the steroid receptor coactivator 1 and of MED1 in retinoid-induced transcription and cellular differentiation. J Biol Chem 281:20338–20348

    Article  PubMed  CAS  Google Scholar 

  • Flanagan JF, Mi LZ, Chruszcz M, Cymborowski M, Clines KL, Kim Y, Minor W, Rastinejad F, Khorasanizadeh S (2005) Double chromodomains cooperate to recognize the methylated histone H3 tail. Nature 438:1181–1185

    Article  PubMed  CAS  Google Scholar 

  • Franchina M, Kay PH (2000) Evidence that cytosine residues within 5′-CCTGG-3′ pentanucleotides can be methylated in human DNA independently of the methylating system that modifies 5′-CG-3′ dinucleotides. DNA Cell Biol 19:521–526

    Article  PubMed  CAS  Google Scholar 

  • Francis NJ, Kingston RE, Woodcock CL (2004) Chromatin compaction by a polycomb group protein complex. Science 306:1574–1577

    Article  PubMed  CAS  Google Scholar 

  • Francis J, Chakrabarti SK, Garmey JC, Mirmira RG (2005) Pdx-1 links histone H3-Lys-4 methylation to RNA polymerase II elongation during activation of insulin transcription. J Biol Chem 280:36244–36253

    Article  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 137:110–122

    Article  PubMed  CAS  Google Scholar 

  • Frenster JH, Allfrey VG, Mirsky AE (1963) Repressed and active chromatin isolated from interphase lymphocytes. Proc Natl Acad Sci USA 50:1026–1032

    Article  PubMed  CAS  Google Scholar 

  • Fromm G, de Vries C, Byron R, Fields J, Fiering S, Groudine M, Bender MA, Palis J, Bulger M (2009) Histone hyperacetylation within the beta-globin locus is context-dependent and precedes high-level gene expression. Blood 114:3479–3488

    Article  PubMed  CAS  Google Scholar 

  • Fujitaki JM, Fung G, Oh EY, Smith RA (1981) Characterization of chemical and enzymatic acid-labile phosphorylation of histone H4 using phosphorus-31 nuclear magnetic resonance. Biochemistry 20:3658–3664

    Article  PubMed  CAS  Google Scholar 

  • Gerber M, Shilatifard A (2003) Transcriptional elongation by RNA polymerase II and histone methylation. J Biol Chem 278:26303–26306

    Article  PubMed  CAS  Google Scholar 

  • Giambra V, Volpi S, Emelyanov AV, Pflugh D, Bothwell AL, Norio P, Fan Y, Ju Z, Skoultchi AI, Hardy RR, Frezza D, Birshtein BK (2008) Pax5 and linker histone H1 coordinate DNA methylation and histone modifications in the 3′ regulatory region of the immunoglobulin heavy chain locus. Mol Cell Biol 28:6123–6133

    Article  PubMed  CAS  Google Scholar 

  • Goldberg ML, Atchley WA (1966) The effect of hormones of DNA. Proc Natl Acad Sci USA 55:989–996

    Article  PubMed  CAS  Google Scholar 

  • Goldman JA, Garlick JD, Kingston RE (2010) Chromatin remodeling by imitation switch (ISWI) class ATP-dependent remodelers is stimulated by histone variant H2A.Z. J Biol Chem 285:4645–4651

    Article  PubMed  CAS  Google Scholar 

  • Goren A, Tabib A, Hecht M, Cedar H (2008) DNA replication timing of the human beta-globin domain is controlled by histone modification at the origin. Genes Dev 22:1319–1324

    Article  PubMed  CAS  Google Scholar 

  • Grant PA (2001) A tale of histone modifications. Genome Biol 2:REVIEWS0003

    Google Scholar 

  • Green MR, Yoon H, Boss JM (2006) Epigenetic regulation during B cell differentiation controls CIITA promoter accessibility. J Immunol 177:3865–3873

    PubMed  CAS  Google Scholar 

  • Grewal SI, Jia S (2007) Heterochromatin revisited. Nat Rev Genet 8:35–46

    Article  PubMed  CAS  Google Scholar 

  • Grigoryev SA, Arya G, Correll S, Woodcock CL, Schlick T (2009) Evidence for heteromorphic chromatin fibers from analysis of nucleosome interactions. Proc Natl Acad Sci USA 106:13317–13322

    Article  PubMed  Google Scholar 

  • Grimaud C, Bantignies F, Pal-Bhadra M, Ghana P, Bhadra U, Cavalli G (2006) RNAi components are required for nuclear clustering of polycomb group response elements. Cell 124:957–971

    Article  PubMed  CAS  Google Scholar 

  • Grune T, Brzeski J, Eberharter A, Clapier CR, Corona DF, Becker PB, Muller CW (2003) Crystal structure and functional analysis of a nucleosome recognition module of the remodeling factor ISWI. Mol Cell 12:449–460

    Article  PubMed  Google Scholar 

  • Grunstein M (1997) Histone acetylation in chromatin structure and transcription. Nature 389:349–352

    Article  PubMed  CAS  Google Scholar 

  • Guenther MG, Jenner RG, Chevalier B, Nakamura T, Croce CM, Canaani E, Young RA (2005) Global and Hox-specific roles for the MLL1 methyltransferase. Proc Natl Acad Sci USA 102:8603–8608

    Article  PubMed  CAS  Google Scholar 

  • Guenther MG, Levine SS, Boyer LA, Jaenisch R, Young RA (2007) A chromatin landmark and transcription initiation at most promoters in human cells. Cell 130:77–88

    Article  PubMed  CAS  Google Scholar 

  • Guo C, Hu Q, Yan C, Zhang J (2009) Multivalent binding of the ETO corepressor to E proteins facilitates dual repression controls targeting chromatin and the basal transcription machinery. Mol Cell Biol 29:2644–2657

    Article  PubMed  CAS  Google Scholar 

  • Gurley LR, Walters RA, Barham SS, Deaven LL (1978) Heterochromatin and histone phosphorylation. Exp Cell Res 111:373–383

    Article  PubMed  CAS  Google Scholar 

  • Hahn S (2004) Structure and mechanism of the RNA polymerase II transcription machinery. Nat Struct Mol Biol 11:394–403

    Article  PubMed  CAS  Google Scholar 

  • Hake SB, Allis CD (2006) Histone H3 variants and their potential role in indexing mammalian genomes: the “H3 barcode hypothesis”. Proc Natl Acad Sci USA 103:6428–6435

    Article  PubMed  CAS  Google Scholar 

  • Hamamoto R, Furukawa Y, Morita M, Iimura Y, Silva FP, Li M, Yagyu R, Nakamura Y (2004) SMYD3 encodes a histone methyltransferase involved in the proliferation of cancer cells. Nat Cell Biol 6:731–740

    Article  PubMed  CAS  Google Scholar 

  • Hampsey M, Reinberg D (2003) Tails of intrigue: phosphorylation of RNA polymerase II mediates histone methylation. Cell 113:429–432

    Article  PubMed  CAS  Google Scholar 

  • Han L, Lee DH, Szabo PE (2008) CTCF is the master organizer of domain-wide allele-specific chromatin at the H19/Igf2 imprinted region. Mol Cell Biol 28:1124–1135

    Article  PubMed  CAS  Google Scholar 

  • Hassan AH, Neely KE, Workman JL (2001) Histone acetyltransferase complexes stabilize swi/snf binding to promoter nucleosomes. Cell 104:817–827

    Article  PubMed  CAS  Google Scholar 

  • Hatzis P, Talianidis I (2002) Dynamics of enhancer-promoter communication during differentiation-induced gene activation. Mol Cell 10:1467–1477

    Article  PubMed  CAS  Google Scholar 

  • Hawkins PG, Santoso S, Adams C, Anest V, Morris KV (2009) Promoter targeted small RNAs induce long-term transcriptional gene silencing in human cells. Nucleic Acids Res 37:2984–2995

    Article  PubMed  CAS  Google Scholar 

  • He XJ, Hsu YF, Zhu S, Liu HL, Pontes O, Zhu J, Cui X, Wang CS and Zhu JK (2009) A conserved transcriptional regulator is required for RNA-directed DNA methylation and plant development. Genes Dev 23:17–22

    Google Scholar 

  • Heintzman ND, Stuart RK, Hon G, Fu Y, Ching CW, Hawkins RD, Barrera LO, Van Calcar S, Qu C, Ching KA, Wang W, Weng Z, Green RD, Crawford GE, Ren B (2007) Distinct and predictive chromatin signatures of transcriptional promoters and enhancers in the human genome. Nat Genet 39:311–318

    Article  PubMed  CAS  Google Scholar 

  • Heintzman ND, Hon GC, Hawkins RD, Kheradpour P, Stark A, Harp LF, Ye Z, Lee LK, Stuart RK, Ching CW, Ching KA, Antosiewicz-Bourget JE, Liu H, Zhang X, Green RD, Lobanenkov VV, Stewart R, Thomson JA, Crawford GE, Kellis M, Ren B (2009) Histone modifications at human enhancers reflect global cell-type-specific gene expression. Nature 459:108–112

    Article  PubMed  CAS  Google Scholar 

  • Hisahara S, Chiba S, Matsumoto H, Tanno M, Yagi H, Shimohama S, Sato M, Horio Y (2008) Histone deacetylase SIRT1 modulates neuronal differentiation by its nuclear translocation. Proc Natl Acad Sci USA 105:15599–15604

    Article  PubMed  Google Scholar 

  • Ho Y, Elefant F, Liebhaber SA, Cooke NE (2006) Locus control region transcription plays an active role in long-range gene activation. Mol Cell 23:365–375

    Article  PubMed  CAS  Google Scholar 

  • Horn PJ, Peterson CL (2002) Molecular biology. Chromatin higher order folding–wrapping up transcription. Science 297:1824–1827

    Article  PubMed  CAS  Google Scholar 

  • Hou C, Zhao H, Tanimoto K, Dean A (2008) CTCF-dependent enhancer-blocking by alternative chromatin loop formation. Proc Natl Acad Sci USA 105:20398–20403

    Article  PubMed  Google Scholar 

  • Huang JM, Wei YF, Kim YH, Osterberg L, Matthews HR (1991) Purification of a protein histidine kinase from the yeast Saccharomyces cerevisiae. The first member of this class of protein kinases. J Biol Chem 266:9023–9031

    PubMed  CAS  Google Scholar 

  • Huang Y, Fang J, Bedford MT, Zhang Y, Xu RM (2006) Recognition of histone H3 lysine-4 methylation by the double Tudor domain of JMJD2A. Science 312:748–751

    Article  PubMed  CAS  Google Scholar 

  • Huebner VD, Matthews HR (1985) Phosphorylation of histidine in proteins by a nuclear extract of Physarum polycephalum plasmodia. J Biol Chem 260:16106–16113

    PubMed  CAS  Google Scholar 

  • Hurd PJ, Bannister AJ, Halls K, Dawson MA, Vermeulen M, Olsen JV, Ismail H, Somers J, Mann M, Owen-Hughes T, Gout I, Kouzarides T (2009) Phosphorylation of histone H3 Thr-45 is linked to apoptosis. J Biol Chem 284:16575–16583

    Article  PubMed  CAS  Google Scholar 

  • Ikura T, Ogryzko VV, Grigoriev M, Groisman R, Wang J, Horikoshi M, Scully R, Qin J, Nakatani Y (2000) Involvement of the TIP60 histone acetylase complex in DNA repair and apoptosis. Cell 102:463–473

    Article  PubMed  CAS  Google Scholar 

  • Ishihara K, Oshimura M, Nakao M (2006) CTCF-dependent chromatin insulator is linked to epigenetic remodeling. Mol Cell 23:733–742

    Article  PubMed  CAS  Google Scholar 

  • Jensen ED, Gopalakrishnan R, Westendorf JJ (2009) Bone morphogenic protein 2 activates protein kinase D to regulate histone deacetylase 7 localization and repression of Runx2. J Biol Chem 284:2225–2234

    Article  PubMed  CAS  Google Scholar 

  • Jenuwein T, Allis CD (2001) Translating the histone code. Science 293:1074–1080

    Article  PubMed  CAS  Google Scholar 

  • Kadam S, Emerson BM (2003) Transcriptional specificity of human SWI/SNF BRG1 and BRM chromatin remodeling complexes. Mol Cell 11:377–389

    Article  PubMed  CAS  Google Scholar 

  • Kang JS, Alliston T, Delston R, Derynck R (2005) Repression of Runx2 function by TGF-beta through recruitment of class II histone deacetylases by Smad3. EMBO J 24:2543–2555

    Article  PubMed  CAS  Google Scholar 

  • Kanno T, Kanno Y, Siegel RM, Jang MK, Lenardo MJ, Ozato K (2004) Selective recognition of acetylated histones by bromodomain proteins visualized in living cells. Mol Cell 13:33–43

    Article  PubMed  CAS  Google Scholar 

  • Khorasanizadeh S (2004) The nucleosome: from genomic organization to genomic regulation. Cell 116:259–272

    Article  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 137:259–272

    Article  PubMed  CAS  Google Scholar 

  • Kim A, Dean A (2004) Developmental stage differences in chromatin subdomains of the beta-globin locus. Proc Natl Acad Sci USA 101:7028–7033

    Article  PubMed  CAS  Google Scholar 

  • King IF, Francis NJ, Kingston RE (2002) Native and recombinant polycomb group complexes establish a selective block to template accessibility to repress transcription in vitro. Mol Cell Biol 22:7919–7928

    Article  PubMed  CAS  Google Scholar 

  • Kireeva ML, Hancock B, Cremona GH, Walter W, Studitsky VM, Kashlev M (2005) Nature of the nucleosomal barrier to RNA polymerase II. Mol Cell 18:97–108

    Article  PubMed  CAS  Google Scholar 

  • Kleinjan DA, Lettice LA (2008) Long-range gene control and genetic disease. Adv Genet 61:339–388

    Article  PubMed  CAS  Google Scholar 

  • Kleinjan DA, van Heyningen V (2005) Long-range control of gene expression: emerging mechanisms and disruption in disease. Am J Hum Genet 76:8–32

    Article  PubMed  CAS  Google Scholar 

  • Koike M, Mashino M, Sugasawa J, Koike A (2008a) Histone H2AX phosphorylation independent of ATM after X-irradiation in mouse liver and kidney in situ. J Radiat Res (Tokyo) 49:445–449

    Article  CAS  Google Scholar 

  • Koike M, Sugasawa J, Yasuda M, Koike A (2008b) Tissue-specific DNA-PK-dependent H2AX phosphorylation and gamma-H2AX elimination after X-irradiation in vivo. Biochem Biophys Res Commun 376:52–55

    Article  PubMed  CAS  Google Scholar 

  • Kornberg RD (1974) Chromatin structure: a repeating unit of histones and DNA. Science 184:868–871

    Article  PubMed  CAS  Google Scholar 

  • Kossel A (1910) Lecture for the nobel prize for physiology or medicine 1910: the chemical composition of the cell nucleus. In: Nobel lectures, physiology or medicine 1901–1921. Elsevier, Amsterdam, 1967

  • Koyanagi M, Baguet A, Martens J, Margueron R, Jenuwein T, Bix M (2005) EZH2 and histone 3 trimethyl lysine 27 associated with Il4 and Il13 gene silencing in Th1 cells. J Biol Chem 280:31470–31477

    Article  PubMed  CAS  Google Scholar 

  • Kruithof M, Chien FT, Routh A, Logie C, Rhodes D, van Noort J (2009) Single-molecule force spectroscopy reveals a highly compliant helical folding for the 30-nm chromatin fiber. Nat Struct Mol Biol 16:534–540

    Article  PubMed  CAS  Google Scholar 

  • Ku M, Koche RP, Rheinbay E, Mendenhall EM, Endoh M, Mikkelsen TS, Presser A, Nusbaum C, Xie X, Chi AS, Adli M, Kasif S, Ptaszek LM, Cowan CA, Lander ES, Koseki H, Bernstein BE (2008) Genomewide analysis of PRC1 and PRC2 occupancy identifies two classes of bivalent domains. PLoS Genet 4:e1000242

    Article  PubMed  CAS  Google Scholar 

  • Kuzmichev A, Nishioka K, Erdjument-Bromage H, Tempst P, Reinberg D (2002) Histone methyltransferase activity associated with a human multiprotein complex containing the Enhancer of Zeste protein. Genes Dev 16:2893–2905

    Article  PubMed  CAS  Google Scholar 

  • Kuzmichev A, Margueron R, Vaquero A, Preissner TS, Scher M, Kirmizis A, Ouyang X, Brockdorff N, Abate-Shen C, Farnham P, Reinberg D (2005) Composition and histone substrates of polycomb repressive group complexes change during cellular differentiation. Proc Natl Acad Sci USA 102:1859–1864

    Article  PubMed  CAS  Google Scholar 

  • Lande-Diner L, Zhang J, Cedar H (2009) Shifts in replication timing actively affect histone acetylation during nucleosome reassembly. Mol Cell 34:767–774

    Article  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 437:432–435

    PubMed  CAS  Google Scholar 

  • Lee TI, Jenner RG, Boyer LA, Guenther MG, Levine SS, Kumar RM, Chevalier B, Johnstone SE, Cole MF, Isono K, Koseki H, Fuchikami T, Abe K, Murray HL, Zucker JP, Yuan B, Bell GW, Herbolsheimer E, Hannett NM, Sun K, Odom DT, Otte AP, Volkert TL, Bartel DP, Melton DA, Gifford DK, Jaenisch R, Young RA (2006) Control of developmental regulators by polycomb in human embryonic stem cells. Cell 125:301–313

    Article  PubMed  CAS  Google Scholar 

  • Lefevre P, Lacroix C, Tagoh H, Hoogenkamp M, Melnik S, Ingram R, Bonifer C (2005) Differentiation-dependent alterations in histone methylation and chromatin architecture at the inducible chicken lysozyme gene. J Biol Chem 280:27552–27560

    Article  PubMed  CAS  Google Scholar 

  • Legube G, Trouche D (2003) Regulating histone acetyltransferases and deacetylases. EMBO Rep 4:944–947

    Article  PubMed  CAS  Google Scholar 

  • Levings PP, Zhou Z, Vieira KF, Crusselle-Davis VJ, Bungert J (2006) Recruitment of transcription complexes to the beta-globin locus control region and transcription of hypersensitive site 3 prior to erythroid differentiation of murine embryonic stem cells. FEBS J 273:746–755

    Article  PubMed  CAS  Google Scholar 

  • Liang G, Lin JC, Wei V, Yoo C, Cheng JC, Nguyen CT, Weisenberger DJ, Egger G, Takai D, Gonzales FA, Jones PA (2004) Distinct localization of histone H3 acetylation and H3-K4 methylation to the transcription start sites in the human genome. Proc Natl Acad Sci USA 101:7357–7362

    Article  PubMed  CAS  Google Scholar 

  • Liang MD, Zhang Y, McDevit D, Marecki S, Nikolajczyk BS (2006) The interleukin-1beta gene is transcribed from a poised promoter architecture in monocytes. J Biol Chem 281:9227–9237

    Article  PubMed  CAS  Google Scholar 

  • Lim JH, Cho SJ, Park SK, Kim J, Cho D, Lee WJ, Kang CJ (2006) Stage-specific expression of two neighboring Crlz1 and IgJ genes during B cell development is regulated by their chromatin accessibility and histone acetylation. J Immunol 177:5420–5429

    PubMed  CAS  Google Scholar 

  • Lim DA, Huang YC, Swigut T, Mirick AL, Garcia-Verdugo JM, Wysocka J, Ernst P, Alvarez-Buylla A (2009a) Chromatin remodelling factor Mll1 is essential for neurogenesis from postnatal neural stem cells. Nature 458:529–533

    Article  PubMed  CAS  Google Scholar 

  • Lim PS, Hardy K, Bunting KL, Ma L, Peng K, Chen X, Shannon MF (2009b) Defining the chromatin signature of inducible genes in T cells. Genome Biol 10:R107

    Article  PubMed  CAS  Google Scholar 

  • Lister R, O’Malley RC, Tonti-Filippini J, Gregory BD, Berry CC, Millar AH, Ecker JR (2008) Highly integrated single-base resolution maps of the epigenome in Arabidopsis. Cell 133:523–536

    Article  PubMed  CAS  Google Scholar 

  • Lister R, Pelizzola M, Dowen RH, Hawkins RD, Hon G, Tonti-Filippini J, Nery JR, Lee L, Ye Z, Ngo QM, Edsall L, Antosiewicz-Bourget J, Stewart R, Ruotti V, Millar AH, Thomson JA, Ren B, Ecker JR (2009) Human DNA methylomes at base resolution show widespread epigenomic differences. Nature 462:315–322

    Article  PubMed  CAS  Google Scholar 

  • Litt MD, Simpson M, Gaszner M, Allis CD, Felsenfeld G (2001a) Correlation between histone lysine methylation and developmental changes at the chicken beta-globin locus. Science 293:2453–2455

    Article  PubMed  CAS  Google Scholar 

  • Litt MD, Simpson M, Recillas-Targa F, Prioleau MN, Felsenfeld G (2001b) Transitions in histone acetylation reveal boundaries of three separately regulated neighboring loci. EMBO J 20:2224–2235

    Article  PubMed  CAS  Google Scholar 

  • Littau VC, Allfrey VG, Frenster JH, Mirsky AE (1964) Active and inactive regions of nuclear chromatin as revealed by electron microscope autoradiography. Proc Natl Acad Sci USA 52:93–100

    Article  PubMed  CAS  Google Scholar 

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

    Article  PubMed  CAS  Google Scholar 

  • Loyola A, Tagami H, Bonaldi T, Roche D, Quivy JP, Imhof A, Nakatani Y, Dent SY, Almouzni G (2009) The HP1alpha-CAF1-SetDB1-containing complex provides H3K9me1 for Suv39-mediated K9me3 in pericentric heterochromatin. EMBO Rep 10:769–775

    Article  PubMed  CAS  Google Scholar 

  • Luger K, Mader AW, Richmond RK, Sargent DF, Richmond TJ (1997a) Crystal structure of the nucleosome core particle at 2.8 A resolution. Nature 389:251–260

    Article  PubMed  CAS  Google Scholar 

  • Luger K, Rechsteiner TJ, Flaus AJ, Waye MM, Richmond TJ (1997b) Characterization of nucleosome core particles containing histone proteins made in bacteria. J Mol Biol 272:301–311

    Article  PubMed  CAS  Google Scholar 

  • Lusser A, Urwin DL, Kadonaga JT (2005) Distinct activities of CHD1 and ACF in ATP-dependent chromatin assembly. Nat Struct Mol Biol 12:160–166

    Article  PubMed  CAS  Google Scholar 

  • Mal A, Harter ML (2003) MyoD is functionally linked to the silencing of a muscle-specific regulatory gene prior to skeletal myogenesis. Proc Natl Acad Sci USA 100:1735–1739

    Article  PubMed  CAS  Google Scholar 

  • Margueron R, Trojer P, Reinberg D (2005) The key to development: interpreting the histone code? Curr Opin Genet Dev 15:163–176

    Article  PubMed  CAS  Google Scholar 

  • Margueron R, Justin N, Ohno K, Sharpe ML, Son J, Drury WJ 3rd, Voigt P, Martin SR, Taylor WR, De Marco V, Pirrotta V, Reinberg D, Gamblin SJ (2009) Role of the polycomb protein EED in the propagation of repressive histone marks. Nature 461:762–767

    Article  PubMed  CAS  Google Scholar 

  • Marmorstein R, Roth SY (2001) Histone acetyltransferases: function, structure, and catalysis. Curr Opin Genet Dev 11:155–161

    Article  PubMed  CAS  Google Scholar 

  • Martens JH, Verlaan M, Kalkhoven E, Zantema A (2003) Cascade of distinct histone modifications during collagenase gene activation. Mol Cell Biol 23:1808–1816

    Article  PubMed  CAS  Google Scholar 

  • Maruyama T, Farina A, Dey A, Cheong J, Bermudez VP, Tamura T, Sciortino S, Shuman J, Hurwitz J, Ozato K (2002) A mammalian bromodomain protein, brd4, interacts with replication factor C and inhibits progression to S phase. Mol Cell Biol 22:6509–6520

    Article  PubMed  CAS  Google Scholar 

  • Mattick JS, Amaral PP, Dinger ME, Mercer TR, Mehler MF (2009) RNA regulation of epigenetic processes. Bioessays 31:51–59

    Article  PubMed  CAS  Google Scholar 

  • Mellor J, Dudek P, Clynes D (2008) A glimpse into the epigenetic landscape of gene regulation. Curr Opin Genet Dev 18:116–122

    Article  PubMed  CAS  Google Scholar 

  • Metzger E, Wissmann M, Yin N, Muller JM, Schneider R, Peters AH, Gunther T, Buettner R, Schule R (2005) LSD1 demethylates repressive histone marks to promote androgen-receptor-dependent transcription. Nature 437:436–439

    PubMed  CAS  Google Scholar 

  • Mikkelsen TS, Ku M, Jaffe DB, Issac B, Lieberman E, Giannoukos G, Alvarez P, Brockman W, Kim TK, Koche RP, Lee W, Mendenhall E, O’Donovan A, Presser A, Russ C, Xie X, Meissner A, Wernig M, Jaenisch R, Nusbaum C, Lander ES, Bernstein BE (2007) Genome-wide maps of chromatin state in pluripotent and lineage-committed cells. Nature 448:553–560

    Article  PubMed  CAS  Google Scholar 

  • Milne TA, Hughes CM, Lloyd R, Yang Z, Rozenblatt-Rosen O, Dou Y, Schnepp RW, Krankel C, Livolsi VA, Gibbs D, Hua X, Roeder RG, Meyerson M, Hess JL (2005) Menin and MLL cooperatively regulate expression of cyclin-dependent kinase inhibitors. Proc Natl Acad Sci USA 102:749–754

    Article  PubMed  CAS  Google Scholar 

  • Mizzen C, Kuo MH, Smith E, Brownell J, Zhou J, Ohba R, Wei Y, Monaco L, Sassone-Corsi P, Allis CD (1998) Signaling to chromatin through histone modifications: how clear is the signal? Cold Spring Harb Symp Quant Biol 63:469–481

    Article  PubMed  CAS  Google Scholar 

  • Moazed D (2009) Small RNAs in transcriptional gene silencing and genome defence. Nature 457:413–420

    Article  PubMed  CAS  Google Scholar 

  • Moriniere J, Rousseaux S, Steuerwald U, Soler-Lopez M, Curtet S, Vitte AL, Govin J, Gaucher J, Sadoul K, Hart DJ, Krijgsveld J, Khochbin S, Muller CW, Petosa C (2009) Cooperative binding of two acetylation marks on a histone tail by a single bromodomain. Nature 461:664–668

    Article  PubMed  CAS  Google Scholar 

  • Muller J, Verrijzer P (2009) Biochemical mechanisms of gene regulation by polycomb group protein complexes. Curr Opin Genet Dev 19:150–158

    Article  PubMed  CAS  Google Scholar 

  • Musri MM, Corominola H, Casamitjana R, Gomis R, Parrizas M (2006) Histone H3 lysine 4 dimethylation signals the transcriptional competence of the adiponectin promoter in preadipocytes. J Biol Chem 281:17180–17188

    Article  PubMed  CAS  Google Scholar 

  • Mutskov V, Felsenfeld G (2009) The human insulin gene is part of a large open chromatin domain specific for human islets. Proc Natl Acad Sci USA 106:17419–17424

    Article  PubMed  Google Scholar 

  • Nakade K, Pan J, Yoshiki A, Ugai H, Kimura M, Liu B, Li H, Obata Y, Iwama M, Itohara S, Murata T, Yokoyama KK (2007) JDP2 suppresses adipocyte differentiation by regulating histone acetylation. Cell Death Differ 14:1398–1405

    Article  PubMed  CAS  Google Scholar 

  • Nott A, Watson PM, Robinson JD, Crepaldi L, Riccio A (2008) S-Nitrosylation of histone deacetylase 2 induces chromatin remodelling in neurons. Nature 455:411–415

    Article  PubMed  CAS  Google Scholar 

  • Osborne CS, Chakalova L, Brown KE, Carter D, Horton A, Debrand E, Goyenechea B, Mitchell JA, Lopes S, Reik W, Fraser P (2004) Active genes dynamically colocalize to shared sites of ongoing transcription. Nat Genet 36:1065–1071

    Article  PubMed  CAS  Google Scholar 

  • Oudet P, Gross-Bellard M, Chambon P (1975) Electron microscopic and biochemical evidence that chromatin structure is a repeating unit. Cell 4:281–300

    Article  PubMed  CAS  Google Scholar 

  • Pavan Kumar P, Purbey PK, Sinha CK, Notani D, Limaye A, Jayani RS, Galande S (2006) Phosphorylation of SATB1, a global gene regulator, acts as a molecular switch regulating its transcriptional activity in vivo. Mol Cell 22:231–243

    Article  PubMed  CAS  Google Scholar 

  • Pavri R, Zhu B, Li G, Trojer P, Mandal S, Shilatifard A, Reinberg D (2006) Histone H2B monoubiquitination functions cooperatively with FACT to regulate elongation by RNA polymerase II. Cell 125:703–717

    Article  PubMed  CAS  Google Scholar 

  • Peters AH, Mermoud JE, O’Carroll D, Pagani M, Schweizer D, Brockdorff N, Jenuwein T (2002) Histone H3 lysine 9 methylation is an epigenetic imprint of facultative heterochromatin. Nat Genet 30:77–80

    Article  PubMed  CAS  Google Scholar 

  • Peters AH, Kubicek S, Mechtler K, O’Sullivan RJ, Derijck AA, Perez-Burgos L, Kohlmaier A, Opravil S, Tachibana M, Shinkai Y, Martens JH, Jenuwein T (2003) Partitioning and plasticity of repressive histone methylation states in mammalian chromatin. Mol Cell 12:1577–1589

    Article  PubMed  CAS  Google Scholar 

  • Peterson CL, Laniel MA (2004) Histones and histone modifications. Curr Biol 14:R546–R551

    Article  PubMed  CAS  Google Scholar 

  • Pradhan S, Chin HG, Esteve PO, Jacobsen SE (2009) SET7/9 mediated methylation of non-histone proteins in mammalian cells. Epigenetics 4:383–387

    Article  PubMed  CAS  Google Scholar 

  • Preuss SB, Costa-Nunes P, Tucker S, Pontes O, Lawrence RJ, Mosher R, Kasschau KD, Carrington JC, Baulcombe DC, Viegas W, Pikaard CS (2008) Multimegabase silencing in nucleolar dominance involves siRNA-directed DNA methylation and specific methylcytosine-binding proteins. Mol Cell 32:673–684

    Article  PubMed  CAS  Google Scholar 

  • Ren X, Vincenz C, Kerppola TK (2008) Changes in the distributions and dynamics of polycomb repressive complexes during embryonic stem cell differentiation. Mol Cell Biol 28:2884–2895

    Article  PubMed  CAS  Google Scholar 

  • Rice JC, Briggs SD, Ueberheide B, Barber CM, Shabanowitz J, Hunt DF, Shinkai Y, Allis CD (2003) Histone methyltransferases direct different degrees of methylation to define distinct chromatin domains. Mol Cell 12:1591–1598

    Article  PubMed  CAS  Google Scholar 

  • Richmond TJ, Davey CA (2003) The structure of DNA in the nucleosome core. Nature 423:145–150

    Article  PubMed  CAS  Google Scholar 

  • Rochman M, Postnikov Y, Correll S, Malicet C, Wincovitch S, Karpova TS, McNally JG, Wu X, Bubunenko NA, Grigoryev S, Bustin M (2009) The interaction of NSBP1/HMGN5 with nucleosomes in euchromatin counteracts linker histone-mediated chromatin compaction and modulates transcription. Mol Cell 35:642–656

    Article  PubMed  CAS  Google Scholar 

  • Rogakou EP, Nieves-Neira W, Boon C, Pommier Y, Bonner WM (2000) Initiation of DNA fragmentation during apoptosis induces phosphorylation of H2AX histone at serine 139. J Biol Chem 275:9390–9395

    Article  PubMed  CAS  Google Scholar 

  • Roopra A, Qazi R, Schoenike B, Daley TJ, Morrison JF (2004) Localized domains of G9a-mediated histone methylation are required for silencing of neuronal genes. Mol Cell 14:727–738

    Article  PubMed  CAS  Google Scholar 

  • Rosenfeld MG, Glass CK (2001) Coregulator codes of transcriptional regulation by nuclear receptors. J Biol Chem 276:36865–36868

    Article  PubMed  CAS  Google Scholar 

  • Routh A, Sandin S, Rhodes D (2008) Nucleosome repeat length and linker histone stoichiometry determine chromatin fiber structure. Proc Natl Acad Sci USA 105:8872–8877

    Article  PubMed  Google Scholar 

  • Sampath SC, Marazzi I, Yap KL, Sampath SC, Krutchinsky AN, Mecklenbrauker I, Viale A, Rudensky E, Zhou MM, Chait BT, Tarakhovsky A (2007) Methylation of a histone mimic within the histone methyltransferase G9a regulates protein complex assembly. Mol Cell 27:596–608

    Article  PubMed  CAS  Google Scholar 

  • Sanz LA, Chamberlain S, Sabourin JC, Henckel A, Magnuson T, Hugnot JP, Feil R, Arnaud P (2008) A mono-allelic bivalent chromatin domain controls tissue-specific imprinting at Grb10. EMBO J 27:2523–2532

    Article  PubMed  CAS  Google Scholar 

  • Sarma K, Margueron R, Ivanov A, Pirrotta V, Reinberg D (2008) Ezh2 requires PHF1 to efficiently catalyze H3 lysine 27 trimethylation in vivo. Mol Cell Biol 28:2718–2731

    Article  PubMed  CAS  Google Scholar 

  • Saunders A, Werner J, Andrulis ED, Nakayama T, Hirose S, Reinberg D, Lis JT (2003) Tracking FACT and the RNA polymerase II elongation complex through chromatin in vivo. Science 301:1094–1096

    Article  PubMed  CAS  Google Scholar 

  • Schneider R, Bannister AJ, Myers FA, Thorne AW, Crane-Robinson C, Kouzarides T (2004) Histone H3 lysine 4 methylation patterns in higher eukaryotic genes. Nat Cell Biol 6:73–77

    Article  PubMed  CAS  Google Scholar 

  • Schuettengruber B, Cavalli G (2009) Recruitment of polycomb group complexes and their role in the dynamic regulation of cell fate choice. Development 136:3531–3542

    Article  PubMed  CAS  Google Scholar 

  • Shen X, Liu Y, Hsu YJ, Fujiwara Y, Kim J, Mao X, Yuan GC, Orkin SH (2008) EZH1 mediates methylation on histone H3 lysine 27 and complements EZH2 in maintaining stem cell identity and executing pluripotency. Mol Cell 32:491–502

    Article  PubMed  CAS  Google Scholar 

  • Shi Y, Whetstine JR (2007) Dynamic regulation of histone lysine methylation by demethylases. Mol Cell 25:1–14

    Article  PubMed  CAS  Google Scholar 

  • Shi Y, Lan F, Matson C, Mulligan P, Whetstine JR, Cole PA, Casero RA, Shi Y (2004) Histone demethylation mediated by the nuclear amine oxidase homolog LSD1. Cell 119:941–953

    Article  PubMed  CAS  Google Scholar 

  • Shi YJ, Matson C, Lan F, Iwase S, Baba T, Shi Y (2005) Regulation of LSD1 histone demethylase activity by its associated factors. Mol Cell 19:857–864

    Article  PubMed  CAS  Google Scholar 

  • Shi M, Lin TH, Appell KC, Berg LJ (2008) Janus-kinase-3-dependent signals induce chromatin remodeling at the Ifng locus during T helper 1 cell differentiation. Immunity 28:763–773

    Article  PubMed  CAS  Google Scholar 

  • Simon JA, Kingston RE (2009) Mechanisms of polycomb gene silencing: knowns and unknowns. Nat Rev Mol Cell Biol 10:697–708

    PubMed  CAS  Google Scholar 

  • Simon JA, Lange CA (2008) Roles of the EZH2 histone methyltransferase in cancer epigenetics. Mutat Res 647:21–29

    PubMed  CAS  Google Scholar 

  • Sims RJ 3rd, Reinberg D (2008) Is there a code embedded in proteins that is based on post-translational modifications? Nat Rev Mol Cell Biol 9:815–820

    Article  PubMed  CAS  Google Scholar 

  • Sims RJ 3rd, Chen CF, Santos-Rosa H, Kouzarides T, Patel SS, Reinberg D (2005) 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

    Article  PubMed  CAS  Google Scholar 

  • Smith DL, Chen CC, Bruegger BB, Holtz SL, Halpern RM, Smith RA (1974) Characterization of protein kinases forming acid-labile histone phosphates in Walker-256 carcinosarcoma cell nuclei. Biochemistry 13:3780–3785

    Article  PubMed  CAS  Google Scholar 

  • Smtih DL, Bruegger BB, Halpern RM, Smith RA (1973) New histone kinases in nuclei of rat tissues. Nature 246:103–104

    Article  PubMed  CAS  Google Scholar 

  • Snykers S, Henkens T, De Rop E, Vinken M, Fraczek J, De Kock J, De Prins E, Geerts A, Rogiers V, Vanhaecke T (2009) Role of epigenetics in liver-specific gene transcription, hepatocyte differentiation and stem cell reprogrammation. J Hepatol 51:187–211

    Article  PubMed  CAS  Google Scholar 

  • Solier S, Pommier Y (2009) The apoptotic ring: a novel entity with phosphorylated histones H2AX and H2B and activated DNA damage response kinases. Cell Cycle 8:1853–1859

    PubMed  CAS  Google Scholar 

  • Soutoglou E, Talianidis I (2002) Coordination of PIC assembly and chromatin remodeling during differentiation-induced gene activation. Science 295:1901–1904

    Article  PubMed  CAS  Google Scholar 

  • Spies N, Nielsen CB, Padgett RA, Burge CB (2009) Biased chromatin signatures around polyadenylation sites and exons. Mol Cell 36:245–254

    Article  PubMed  CAS  Google Scholar 

  • Sterner DE, Berger SL (2000) Acetylation of histones and transcription-related factors. Microbiol Mol Biol Rev 64:435–459

    Article  PubMed  CAS  Google Scholar 

  • Strahl BD, Allis CD (2000) The language of covalent histone modifications. Nature 403:41–45

    Article  PubMed  CAS  Google Scholar 

  • Stucki M, Jackson SP (2004) Tudor domains track down DNA breaks. Nat Cell Biol 6:1150–1152

    Article  PubMed  CAS  Google Scholar 

  • Suganuma T, Workman JL (2008) Crosstalk among histone modifications. Cell 135:604–607

    Article  PubMed  CAS  Google Scholar 

  • Tachibana M, Sugimoto K, Nozaki M, Ueda J, Ohta T, Ohki M, Fukuda M, Takeda N, Niida H, Kato H, Shinkai Y (2002) G9a histone methyltransferase plays a dominant role in euchromatic histone H3 lysine 9 methylation and is essential for early embryogenesis. Genes Dev 16:1779–1791

    Article  PubMed  CAS  Google Scholar 

  • Tachibana M, Ueda J, Fukuda M, Takeda N, Ohta T, Iwanari H, Sakihama T, Kodama T, Hamakubo T, Shinkai Y (2005) Histone methyltransferases G9a and GLP form heteromeric complexes and are both crucial for methylation of euchromatin at H3-K9. Genes Dev 19:815–826

    Article  PubMed  CAS  Google Scholar 

  • Tan E, Besant PG, Zu XL, Turck CW, Bogoyevitch MA, Lim SG, Attwood PV, Yeoh GC (2004) Histone H4 histidine kinase displays the expression pattern of a liver oncodevelopmental marker. Carcinogenesis 25:2083–2088

    Article  PubMed  CAS  Google Scholar 

  • Taverna SD, Li H, Ruthenburg AJ, Allis CD, Patel DJ (2007) How chromatin-binding modules interpret histone modifications: lessons from professional pocket pickers. Nat Struct Mol Biol 14:1025–1040

    Article  PubMed  CAS  Google Scholar 

  • Thomas LR, Miyashita H, Cobb RM, Pierce S, Tachibana M, Hobeika E, Reth M, Shinkai Y, Oltz EM (2008) Functional analysis of histone methyltransferase g9a in B and T lymphocytes. J Immunol 181:485–493

    PubMed  CAS  Google Scholar 

  • Tremethick DJ (2007) Higher-order structures of chromatin: the elusive 30 nm fiber. Cell 128:651–654

    Article  PubMed  CAS  Google Scholar 

  • Tse C, Sera T, Wolffe AP, Hansen JC (1998) 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

    PubMed  CAS  Google Scholar 

  • Turner BM (2005) Reading signals on the nucleosome with a new nomenclature for modified histones. Nat Struct Mol Biol 12:110–112

    Article  PubMed  CAS  Google Scholar 

  • Vakoc CR, Mandat SA, Olenchock BA, Blobel GA (2005) Histone H3 lysine 9 methylation and HP1gamma are associated with transcription elongation through mammalian chromatin. Mol Cell 19:381–391

    Article  PubMed  CAS  Google Scholar 

  • Vakoc CR, Sachdeva MM, Wang H, Blobel GA (2006) Profile of histone lysine methylation across transcribed mammalian chromatin. Mol Cell Biol 26:9185–9195

    Article  PubMed  CAS  Google Scholar 

  • Valls E, Sanchez-Molina S, Martinez-Balbas MA (2005) Role of histone modifications in marking and activating genes through mitosis. J Biol Chem 280:42592–42600

    Article  PubMed  CAS  Google Scholar 

  • van Attikum H, Gasser SM (2009) Crosstalk between histone modifications during the DNA damage response. Trends Cell Biol 19:207–217

    Article  PubMed  CAS  Google Scholar 

  • van Ingen H, van Schaik FM, Wienk H, Ballering J, Rehmann H, Dechesne AC, Kruijzer JA, Liskamp RM, Timmers HT, Boelens R (2008) Structural insight into the recognition of the H3K4me3 mark by the TFIID subunit TAF3. Structure 16:1245–1256

    Article  PubMed  CAS  Google Scholar 

  • Wada T, Kikuchi J, Nishimura N, Shimizu R, Kitamura T, Furukawa Y (2009) Expression levels of histone deacetylases determine the cell fate of hematopoietic progenitors. J Biol Chem 284:30673–30683

    Article  PubMed  CAS  Google Scholar 

  • Wang H, An W, Cao R, Xia L, Erdjument-Bromage H, Chatton B, Tempst P, Roeder RG, Zhang Y (2003) mAM facilitates conversion by ESET of dimethyl to trimethyl lysine 9 of histone H3 to cause transcriptional repression. Mol Cell 12:475–487

    Article  PubMed  CAS  Google Scholar 

  • Wang AH, Gregoire S, Zika E, Xiao L, Li CS, Li H, Wright KL, Ting JP, Yang XJ (2005) Identification of the ankyrin repeat proteins ANKRA and RFXANK as novel partners of class IIa histone deacetylases. J Biol Chem 280:29117–29127

    Article  PubMed  CAS  Google Scholar 

  • Wang Z, Zang C, Rosenfeld JA, Schones DE, Barski A, Cuddapah S, Cui K, Roh TY, Peng W, Zhang MQ, Zhao K (2008) Combinatorial patterns of histone acetylations and methylations in the human genome. Nat Genet 40:897–903

    Article  PubMed  CAS  Google Scholar 

  • Wang J, Hevi S, Kurash JK, Lei H, Gay F, Bajko J, Su H, Sun W, Chang H, Xu G, Gaudet F, Li E, Chen T (2009a) The lysine demethylase LSD1 (KDM1) is required for maintenance of global DNA methylation. Nat Genet 41:125–129

    Article  PubMed  CAS  Google Scholar 

  • Wang L, Wuerffel R, Feldman S, Khamlichi AA, Kenter AL (2009b) S region sequence, RNA polymerase II, and histone modifications create chromatin accessibility during class switch recombination. J Exp Med 206:1817–1830

    Article  PubMed  CAS  Google Scholar 

  • Wang Z, Zang C, Cui K, Schones DE, Barski A, Peng W, Zhao K (2009c) Genome-wide mapping of HATs and HDACs reveals distinct functions in active and inactive genes. Cell 138:1019–1031

    Article  PubMed  CAS  Google Scholar 

  • Weake VM, Workman JL (2008) Histone ubiquitination: triggering gene activity. Mol Cell 29:653–663

    Article  PubMed  CAS  Google Scholar 

  • Wei YF, Matthews HR (1990) A filter-based protein kinase assay selective for alkali-stable protein phosphorylation and suitable for acid-labile protein phosphorylation. Anal Biochem 190:188–192

    Article  PubMed  CAS  Google Scholar 

  • Wei YF, Morgan JE, Matthews HR (1989) Studies of histidine phosphorylation by a nuclear protein histidine kinase show that histidine-75 in histone H4 is masked in nucleosome core particles and in chromatin. Arch Biochem Biophys 268:546–550

    Article  PubMed  CAS  Google Scholar 

  • Wei G, Wei L, Zhu J, Zang C, Hu-Li J, Yao Z, Cui K, Kanno Y, Roh TY, Watford WT, Schones DE, Peng W, Sun HW, Paul WE, O’Shea JJ, Zhao K (2009) Global mapping of H3K4me3 and H3K27me3 reveals specificity and plasticity in lineage fate determination of differentiating CD4+ T cells. Immunity 30:155–167

    Article  PubMed  CAS  Google Scholar 

  • Whetstine JR, Nottke A, Lan F, Huarte M, Smolikov S, Chen Z, Spooner E, Li E, Zhang G, Colaiacovo M, Shi Y (2006) Reversal of histone lysine trimethylation by the JMJD2 family of histone demethylases. Cell 125:467–481

    Article  PubMed  CAS  Google Scholar 

  • Winston F, Allis CD (1999) The bromodomain: a chromatin-targeting module? Nat Struct Biol 6:601–604

    Article  PubMed  CAS  Google Scholar 

  • Wittmann BM, Fujinaga K, Deng H, Ogba N, Montano MM (2005) The breast cell growth inhibitor, estrogen down regulated gene 1, modulates a novel functional interaction between estrogen receptor alpha and transcriptional elongation factor cyclin T1. Oncogene 24:5576–5588

    Article  PubMed  CAS  Google Scholar 

  • Wood C, Snijders A, Williamson J, Reynolds C, Baldwin J, Dickman M (2009) Post-translational modifications of the linker histone variants and their association with cell mechanisms. FEBS J 276:3685–3697

    Article  PubMed  CAS  Google Scholar 

  • Woychik NA, Hampsey M (2002) The RNA polymerase II machinery: structure illuminates function. Cell 108:453–463

    Article  PubMed  CAS  Google Scholar 

  • Wysocka J, Swigut T, Milne TA, Dou Y, Zhang X, Burlingame AL, Roeder RG, Brivanlou AH, Allis CD (2005) WDR5 associates with histone H3 methylated at K4 and is essential for H3 K4 methylation and vertebrate development. Cell 121:859–872

    Article  PubMed  CAS  Google Scholar 

  • Xiao A, Li H, Shechter D, Ahn SH, Fabrizio LA, Erdjument-Bromage H, Ishibe-Murakami S, Wang B, Tempst P, Hofmann K, Patel DJ, Elledge SJ, Allis CD (2009) WSTF regulates the H2A.X DNA damage response via a novel tyrosine kinase activity. Nature 457:57–62

    Article  PubMed  CAS  Google Scholar 

  • Yang XJ, Seto E (2008) The Rpd3/Hda1 family of lysine deacetylases: from bacteria and yeast to mice and men. Nat Rev Mol Cell Biol 9:206–218

    Article  PubMed  CAS  Google Scholar 

  • Yang X, Karuturi RK, Sun F, Aau M, Yu K, Shao R, Miller LD, Tan PB, Yu Q (2009) CDKN1C (p57) is a direct target of EZH2 and suppressed by multiple epigenetic mechanisms in breast cancer cells. PLoS One 4:e5011

    Article  PubMed  CAS  Google Scholar 

  • Yoo EJ, Chung JJ, Choe SS, Kim KH, Kim JB (2006) Down-regulation of histone deacetylases stimulates adipocyte differentiation. J Biol Chem 281:6608–6615

    Article  PubMed  CAS  Google Scholar 

  • Zhang Q, Wang Y (2008) High mobility group proteins and their post-translational modifications. Biochim Biophys Acta 1784:1159–1166

    PubMed  CAS  Google Scholar 

  • Zhao H, Kim A, Song SH, Dean A (2006) Enhancer blocking by chicken beta-globin 5′-HS4: role of enhancer strength and insulator nucleosome depletion. J Biol Chem 281:30573–30580

    Article  PubMed  CAS  Google Scholar 

  • Zilberman D, Coleman-Derr D, Ballinger T, Henikoff S (2008) Histone H2A.Z and DNA methylation are mutually antagonistic chromatin marks. Nature 456:125–129

    Article  PubMed  CAS  Google Scholar 

Download references

Acknowledgments

D.U. would like acknowledge the support of the National Health and Medical Research Council, Australia.

Author information

Authors and Affiliations

  1. Biochemistry and Molecular Biology, School of Biomedical, Biomolecular and Chemical Sciences, University of Western Australia, 35 Stirling Highway, Crawley, WA, 6009, Australia

    Mark N. Cruickshank, Paul Besant & Daniela Ulgiati

Authors
  1. Mark N. Cruickshank
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Paul Besant
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Daniela Ulgiati
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Daniela Ulgiati.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Cruickshank, M.N., Besant, P. & Ulgiati, D. The impact of histone post-translational modifications on developmental gene regulation. Amino Acids 39, 1087–1105 (2010). https://doi.org/10.1007/s00726-010-0530-6

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00726-010-0530-6

Keywords

Search

Navigation