Chromosome Research

, Volume 14, Issue 1, pp 53–69

The end adjusts the means: Heterochromatin remodelling during terminal cell differentiation

  • Sergei A. Grigoryev
  • Yaroslava A. Bulynko
  • Evgenya Y. Popova
Article

Abstract

All cells that constitute mature tissues in an eukaryotic organism undergo a multistep process of cell differentiation. At the terminal stage of this process, cells either cease to proliferate forever or rest for a very long period of time. During terminal differentiation, most of the genes that are required for cell ‘housekeeping’ functions, such as proto-oncogenes and other cell-cycle and cell proliferation genes, become stably repressed. At the same time, nuclear chromatin undergoes dramatic morphological and structural changes at the higher-order levels of chromatin organization. These changes involve both constitutively inactive chromosomal regions (constitutive heterochromatin) and the formerly active genes that become silenced and structurally modified to form facultative heterochromatin. Here we approach terminal cell differentiation as a unique system that allows us to combine biochemical, ultrastructural and molecular genetic techniques to study the relationship between the hierarchy of chromatin higher-order structures in the nucleus and its function(s) in dynamic packing of genetic material in a form that remains amenable to regulation of gene activity and other DNA-dependent cellular processes.

Key words

cell differentiation chromatin higher-order structure heterochromatin histone nucleosome 

Preview

Unable to display preview. Download preview PDF.

Unable to display preview. Download preview PDF.

References

  1. Adkins NL, Watts M, Georgel PT (2004) To the 30-nm chromatin fiber and beyond. Biochim Biophys Acta 1677: 12–23.PubMedGoogle Scholar
  2. Alcobia I, Dilao R, Parreira L (2000) Spatial associations of centromeres in the nuclei of hematopoietic cells: evidence for cell-type-specific organizational patterns. Blood 95: 1608–1615.PubMedGoogle Scholar
  3. Alcobia I, Quina AS, Neves H, Clode N, Parreira L (2003) The spatial organization of centromeric heterochromatin during normal human lymphopoiesis: evidence for ontogenically determined spatial patterns. Exp Cell Res 290: 358–369.CrossRefPubMedGoogle Scholar
  4. Angelov D, Molla A, Perche PY et al. (2003) The histone variant macroH2A interferes with transcription factor binding and SWI/SNF nucleosome remodeling. Mol Cell 11: 1033–1041.CrossRefPubMedGoogle Scholar
  5. Bachman KE, Rountree MR, Baylin SB (2001) Dnmt3a and Dnmt3b are transcriptional repressors that exhibit unique localization properties to heterochromatin. J Biol Chem 276: 32282–32287.CrossRefPubMedGoogle Scholar
  6. Bannister AJ, Zegerman P, Partridge JF et al (2001) Selective recognition of methylated lysine 9 on histone H3 by the HP1 chromo domain. Nature 410: 120–124.CrossRefPubMedGoogle Scholar
  7. Bapat S, Galande S (2005) Association by guilt: identification of DLX5 as a target for MeCP2 provides a molecular link between genomic imprinting and Rett syndrome. Bioessays 27: 676–680.CrossRefPubMedGoogle Scholar
  8. Bartova E, Kozubek S, Jirsova P et al (2002) Nuclear structure and gene activity in human differentiated cells. J Struct Biol 139: 76–89.CrossRefPubMedGoogle Scholar
  9. Baxter J, Sauer S, Peters A et al (2004) Histone hypomethylation is an indicator of epigenetic plasticity in quiescent lymphocytes. EMBO J 23: 4462–4472.CrossRefPubMedGoogle Scholar
  10. Bednar J, Horowitz RA, Dubochet J, Woodcock CL (1995) Chromatin conformation and salt-induced compaction: three-dimensional structural information from cryoelectron microscopy. J Cell Biol 131: 1365–1376.CrossRefPubMedGoogle Scholar
  11. Bednar J, Horowitz RA, Grigoryev SA et al (1998) Nucleosomes, linker DNA, and linker histone form a unique structural motif that directs the higher-order folding and compaction of chromatin. Proc Natl Acad Sci USA 95: 14173–14178.CrossRefPubMedGoogle Scholar
  12. Bernstein E, Allis CD (2005) RNA meets chromatin. Genes Dev 19: 1635–1655.CrossRefPubMedGoogle Scholar
  13. Brero A, Easwaran HP, Nowak D et al (2005) Methyl CpG-binding proteins induce large-scale chromatin reorganization during terminal differentiation. J Cell Biol 169: 733–743.CrossRefPubMedGoogle Scholar
  14. Brown DT (2003) Histone H1 and the dynamic regulation of chromatin function. Biochem Cell Biol 81: 221–227.CrossRefPubMedGoogle Scholar
  15. Brown KE, Guest SS, Smale ST, Hahm K, Merkenschlager M, Fisher AG (1997) Association of transcriptionally silent genes with Ikaros complexes at centromeric heterochromatin. Cell 91: 845–854.CrossRefPubMedGoogle Scholar
  16. Brown KE, Baxter J, Graf D, Merkenschlager M, Fisher A (1999a) Dynamic repositioning of genes in the nucleus of lymphocytes preparing for cell division. Mol Cell 3: 207–218.CrossRefPubMedGoogle Scholar
  17. Brown KE, Baxter J, Graf D, Merkenschlager M, Fisher AG (1999b) Dynamic repositioning of genes in the nucleus of lymphocytes preparing for cell division. Mol Cell 3: 207–217.CrossRefPubMedGoogle Scholar
  18. Catez F, Yang H, Tracey KJ, Reeves R, Misteli T, Bustin M (2004) Network of dynamic interactions between histone H1 and high-mobility-group proteins in chromatin. Mol Cell Biol 24: 4321–4328.CrossRefPubMedGoogle Scholar
  19. Chadwick BP, Willard HF (2004) Multiple spatially distinct types of facultative heterochromatin on the human inactive X chromosome. Proc Natl Acad Sci USA 101: 17450–17455.CrossRefPubMedGoogle Scholar
  20. Chakravarthy S, Gundimella SK, Caron C et al (2005) Structural characterization of the histone variant macroH2A. Mol Cell Biol 25: 7616–7624.CrossRefPubMedGoogle Scholar
  21. Chen D, Dundr M, Wang C et al (2005) Condensed mitotic chromatin is accessible to transcription factors and chromatin structural proteins. J Cell Biol 168: 41–54.PubMedGoogle Scholar
  22. Cheutin T, AJ McNairn, Jenuwein T, Gilbert DM, Singh PB, Misteli T (2003) Maintenance of stable heterochromatin domains by dynamic HP1 binding. Science 299: 721–725.CrossRefPubMedGoogle Scholar
  23. Costanzi C, Pehrson JR (1998) Histone macroH2A1 is concentrated in the inactive X chromosome of female mammals. Nature 393: 599–601.PubMedGoogle Scholar
  24. Dorigo B, Schalch T, Bystricky K, Richmond TJ (2003) Chromatin fiber folding: requirement for the histone H4 N-terminal tail. JMol Biol 327: 85–96.CrossRefPubMedGoogle Scholar
  25. Dorigo B, Schalch T, Kulangara A, Duda S, Schroeder RR, Richmond TJ (2004) Nucleosome arrays reveal the two-start organization of the chromatin fiber. Science 306: 1571–1573.CrossRefPubMedGoogle Scholar
  26. Echeverri K, Tanaka EM (2002) Mechanisms of muscle dedifferentiation during regeneration. Semin Cell Dev Biol 13: 353–360.CrossRefPubMedGoogle Scholar
  27. Eissenberg JC, Elgin SC (2000) The HP1 protein family: getting a grip on chromatin. Curr Opin Genet Dev 10: 204–210.CrossRefPubMedGoogle Scholar
  28. Fan JY, Gordon F, Luger K, Hansen JC, Tremethick DJ (2002) The essential histone variant H2AZ regulates the equilibrium between different chromatin conformational states. Nat Struct Biol 9: 172–176.CrossRefPubMedGoogle Scholar
  29. Fan Y, Nikitina T, Morin-Kensicki EM et al (2003) H1 linker histones are essential for mouse development and affect nucleosome spacing in in vivo. Mol Cell Biol 23: 4559–4572.PubMedGoogle Scholar
  30. Fan JY, Rangasamy D, Luger K, Tremethick DJ (2004) H2A.Z alters the nucleosome surface to promote HP1alpha-mediated chromatin fiber folding. Mol Cell 16: 655–661.CrossRefPubMedGoogle Scholar
  31. Festenstein R, Pagakis SN, Hiragami K et al (2003) Modulation of heterochromatin protein 1 dynamics in primary mammalian cells. Science 299: 719–721.CrossRefPubMedGoogle Scholar
  32. Fischle W, Tseng BS, Dormann HL et al (2005) Regulation of HP1-chromatin binding by histone H3 methylation and phosphorylation. Nature, Epub 12 Oct 2005.Google Scholar
  33. Francastel C, Schubeler D, Martin DI, Groudine M (2000) Nuclear compartmentalization and gene activity. Nat Rev Mol Cell Biol 1: 137–143.CrossRefPubMedGoogle Scholar
  34. Francastel C, Magis W, Groudine M (2001) Nuclear relocation of a transactivator subunit precedes target gene activation. Proc Natl Acad Sci USA 98: 12120–12125.CrossRefPubMedGoogle Scholar
  35. Garcia-Ramirez M, Rocchini C, Ausio J (1995). Modulation of chromatin folding by histone acetylation. J Biol Chem 270: 17923–17928.PubMedGoogle Scholar
  36. Georgel PT, Horowitz-Scherer RA, Adkins N, Woodcock CL, Wade PA, Hansen JC (2003) Chromatin compaction by human MeCP2: assembly of novel secondary chromatin structures in the absence ofDNA methylation. J Biol Chem 278: 32181–32188.CrossRefPubMedGoogle Scholar
  37. Ghirlando R, Litt MD, Prioleau MN, F Recillas-Targa, Felsenfeld G (2004) Physical properties of a genomic condensed chromatin fragment. J Mol Biol 336: 597–605.CrossRefPubMedGoogle Scholar
  38. Gilbert N, Allan J (2001) Distinctive higher-order chromatin structure at mammalian centromeres. Proc Natl Acad Sci USA 98: 11949–11954.CrossRefPubMedGoogle Scholar
  39. Gilbert N, Boyle S, Sutherland H, J de Las Heras, Allan J, Jenuwein T, Bickmore WA (2003) Formation of facultative heterochromatin in the absence of HP1. EMBO J 22: 5540–5550.CrossRefPubMedGoogle Scholar
  40. Gilbert N, Boyle S, Fiegler H, Woodfine K, Carter NP, Bickmore WA (2004) Chromatin architecture of the human genome: gene-rich domains are enriched in open chromatin fibers. Cell 118: 555–566.CrossRefPubMedGoogle Scholar
  41. Grigoryev SA (2001) Higher-order folding of heterochromatin: protein bridges span the nucleosome arrays. Biochem Cell Biol 79: 227–241.CrossRefPubMedGoogle Scholar
  42. Grigoryev SA (2004) Keeping fingers crossed: heterochromatin spreading through interdigitation of nucleosome arrays. FEBS Lett 564: 4–8.CrossRefPubMedGoogle Scholar
  43. Grigoryev SA, Woodcock CL (1998) Chromatin structure in granulocytes. A link between tight compaction and accumulation of a heterochromatin-associated protein (MENT). J Biol Chem 273: 3082–3089.CrossRefPubMedGoogle Scholar
  44. Grigoryev SA, Bednar J, Woodcock CL (1999) MENT, a heterochromatin protein that mediates higher order chromatin folding, isa new serpin family member. J Biol Chem 274: 5626–5636.CrossRefPubMedGoogle Scholar
  45. Grigoryev SA, Nikitina T, Pehrson JR, Singh PB, Woodcock CL (2004) Dynamic relocation of epigenetic chromatin markers reveals an active role of constitutive heterochromatin in the transition from proliferation to quiescence. J Cell Sci 117: 6153–6162.CrossRefPubMedGoogle Scholar
  46. Guenatri M, Bailly D, Maison C, Almouzni G (2004) Mouse centric and pericentric satellite repeats form distinct functional heterochromatin. J Cell Biol 166: 493–505.CrossRefPubMedGoogle Scholar
  47. Haaf T, Schmid M (2000) Experimental condensation inhibition in constitutive and facultative heterochromatin of mammalian chromosomes. Cytogenet Cell Genet 91: 113–123.CrossRefPubMedGoogle Scholar
  48. Hamiche A, Schultz P, Ramakrishnan V, Oudet P, Prunell A (1996) Linker histone-dependent DNA structure in linear mononucleosomes. J Mol Biol 257: 30–42.CrossRefPubMedGoogle Scholar
  49. Hansen, JC (2002) Conformational dynamics of the chromatin fiber in solution: determinants, mechanisms, and functions. Annu Rev Biophys Biomol Struct 31: 361–392.CrossRefPubMedGoogle Scholar
  50. Harp JM, Hanson BL, Timm DE, Bunick GJ (2000) Asymmetries in the nucleosome core particle at 2.5 A resolution. Acta Crystallogr D Biol Crystallogr 56: 1513–1534.CrossRefPubMedGoogle Scholar
  51. Heitz, E (1928) Das Heterochromatin der Moose. I Jb Wisensch Bot 69: 762–818.Google Scholar
  52. Hennig, W (1999) Heterochromatin. Chromosoma 108: 1–9.CrossRefPubMedGoogle Scholar
  53. Hirota T, Lipp JJ, Toh BH, Peters JM (2005) Histone H3 serine 10 phosphorylation by Aurora B causes HP1 dissociation from heterochromatin. Nature, Epub 12 Oct 2005.Google Scholar
  54. Hoffmann K, Dreger CK, Olins AL et al (2002) Mutations in the gene encoding the lamin B receptor produce an altered nuclear morphology in granulocytes (Pelger-Huet anomaly). Nat Genet 31: 410–414.PubMedGoogle Scholar
  55. Horike S, Cai S, Miyano M, Cheng JF, T Kohwi-Shigematsu (2005) Loss of silent-chromatin looping and impaired imprinting of DLX5 in Rett syndrome. Nat Genet 37: 31–40.PubMedGoogle Scholar
  56. Horowitz RA, Agard DA, Sedat JW, Woodcock CL (1994) The three-dimensional architecture of chromatin in situ: electron tomography reveals fibers composed of a continuously variable zig-zag nucleosomal ribbon. J Cell Biol 125: 1–10.CrossRefPubMedGoogle Scholar
  57. Huynh VA, Robinson PJ, Rhodes D (2005) A method for the in vitro reconstitution of a defined “30 nm” chromatin fibre containing stoichiometric amounts of the linker histone. J Mol Biol 345: 957–968.CrossRefPubMedGoogle Scholar
  58. Irving JA, Shushanov SS, Pike RN et al (2002). Inhibitory activity of a heterochromatin-associated serpin (MENT) against papain-like cysteine proteinases affects chromatin structure and blocks cell proliferation. J Biol Chem 277: 13192–13201.CrossRefPubMedGoogle Scholar
  59. Istomina NE, Shushanov SS, Springhetti EM et al (2003) Insulation of the chicken b-globin chromosomal domain from a chromatin-condensing protein, MENT Mol Cell Biol 23: 6455–6468.CrossRefPubMedGoogle Scholar
  60. Jacobs SA, Khorasanizadeh S (2002) Structure of HP1 chromodomain bound to a lysine 9-methylated histone H3 tail. Science 295: 2080–2083.CrossRefPubMedGoogle Scholar
  61. Jenuwein T, Allis CD (2001) Translating the histone code. Science 293: 1074–1080.CrossRefPubMedGoogle Scholar
  62. Kamakaka RT, Biggins S (2005) Histone variants: deviants? Genes Dev 19: 295–310.CrossRefPubMedGoogle Scholar
  63. Keohane AM, Lavender JS, LP O'Neill, Turner BM (1998) Histone acetylation and X inactivation. Dev Genet 22: 65–73.CrossRefPubMedGoogle Scholar
  64. Kireeva N, Lakonishok M, Kireev I, Hirano T, Belmont AS (2004) Visualization of early chromosome condensation: a hierarchical folding, axial glue model of chromosome structure. J Cell Biol 166: 775–785.CrossRefPubMedGoogle Scholar
  65. Klose R, Bird A (2003) Molecular biology. MeCP2 repression goes nonglobal. Science 302: 793–795.CrossRefPubMedGoogle Scholar
  66. Krauss SW, Lo AJ, Short SA, Koury MJ, Mohandas N, Chasis JA (2005) Nuclear substructure reorganization during late-stage erythropoiesis is selective and does not involve caspase cleavage of major nuclear substructural proteins. Blood 106: 2200–2205.CrossRefPubMedGoogle Scholar
  67. Kulessa H, Frampton J, Graf T (1995) GATA-1 reprograms avian myelomonocytic cell lines into eosinophils, thromboblasts, erythroblasts. Genes Dev 9: 1250–1262.PubMedGoogle Scholar
  68. Kustatscher G, Hothorn M, Pugieux C, Scheffzek K, Ladurner AG (2005) Splicing regulates NAD metabolite binding to histone macroH2A. Nat Struct Mol Biol 12: 624–625.CrossRefPubMedGoogle Scholar
  69. Lachner M, O'Carroll D, Rea S, Mechtler K, Jenuwein T (2001) Methylation of histone H3 lysine 9 creates a binding site for HP1 proteins. Nature 410: 116–120.CrossRefPubMedGoogle Scholar
  70. Ladurner, AG (2003) Inactivating chromosomes: a macro domain that minimizes transcription. Mol Cell 12: 1–3.CrossRefPubMedGoogle Scholar
  71. Leitch, AR (2000) Higher levels of organization in the interphase nucleus of cycling and differentiated cells. Microbiol Mol Biol Rev 64: 138–152.PubMedGoogle Scholar
  72. Lowary PT, Widom J (1998) New DNA sequence rules for high affinity binding to histone octamer and sequence-directed nucleosome positioning. J Mol Biol 276: 19–42.CrossRefPubMedGoogle Scholar
  73. Lu ZH, Xu H, Leno GH (1999) DNA replication in quiescent cell nuclei: regulation by the nuclear envelope and chromatin structure. Mol Biol Cell 10: 4091–4106.PubMedGoogle Scholar
  74. Luger K, Hansen JC (2005) Nucleosome and chromatin fiber dynamics. Curr Opin Struct Biol 15: 188–196.CrossRefPubMedGoogle Scholar
  75. Lukasova E, Koristek Z, Falk M (2005). Methylation of histones in myeloid leukemias as a potential marker of granulocyte abnormalities. J Leukoc Biol 77: 100–111.PubMedGoogle Scholar
  76. Lund AH, van Lohuizen M (2004) Epigenetics and cancer. Genes Dev 18: 2315–2335.CrossRefPubMedGoogle Scholar
  77. Maison C, Almouzni G (2004) HP1 and the dynamics of heterochromatin maintenance. Nat Rev Mol Cell Biol 5: 296–304.CrossRefPubMedGoogle Scholar
  78. McBryant SJ, Adams VH, Hansen JC (2006) Chromatin architectural proteins. Chromosome Res 14: 39–51. Google Scholar
  79. Meehan RR, Kao CF, Pennings S (2003) HP1 binding to native chromatin in vitro is determined by the hinge region and not by the chromodomain. EMBO J 22: 3164–3174.CrossRefPubMedGoogle Scholar
  80. Meneghini MD, Wu M, Madhani HD (2003) Conserved histone variant H2A.Z protects euchromatin from the ectopic spread of silent heterochromatin. Cell 112: 725–736.CrossRefPubMedGoogle Scholar
  81. Misteli, T (2001) Protein dynamics: implications for nuclear architecture and gene expression. Science 291: 843–847.CrossRefPubMedGoogle Scholar
  82. Nan X, Ng H, Johnson C (1998) Transcriptional repression by the methyl-CpG-binding protein MeCp2 involves a histone deacetylase complex. Nature 393: 386–389.PubMedGoogle Scholar
  83. Patterton HG, Landel CC, Landsman D, Peterson, CL, Simpson, RT (1998) The biochemical and phenotypic characterization of Hho1p, the putative linker histone H1 of Saccharomyces cerevisiae. J Biol Chem 273: 7268–7276.CrossRefPubMedGoogle Scholar
  84. Pehrson JR, Fuji RN (1998) Evolutionary conservation of histone macroH2A subtypes and domains. Nucleic Acids Res. 26: 2837–2842.CrossRefPubMedGoogle Scholar
  85. Plath K, Mlynarczyk-Evans S, Nusinow DA, Panning B (2002) Xist RNA and the mechanism of X chromosome inactivation. Annu Rev Genet 36: 233–278.CrossRefPubMedGoogle Scholar
  86. Raisner RM, Hartley PD, Meneghini MD et al (2005) Histone variant H2A.Z marks the 5′ ends of both active and inactive genes in euchromatin. Cell 123: 233–248.CrossRefPubMedGoogle Scholar
  87. Rangasamy D, Berven L, Ridgway P, Tremethick DJ (2003) Pericentric heterochromatin becomes enriched with H2A.Z during early mammalian development. EMBO J 22: 1599–1607.CrossRefPubMedGoogle Scholar
  88. Rangasamy D, Greaves I, Tremethick DJ (2004) RNA interference demonstrates a novel role for H2AZ in chromosome segregation. Nat Struct Mol Biol 11: 650–655.CrossRefPubMedGoogle Scholar
  89. Richards EJ, Elgin SC (2002) Epigenetic codes for heterochromatin formation and silencing: rounding up the usual suspects. Cell 108: 489–500.CrossRefPubMedGoogle Scholar
  90. Richmond TJ, Davey CA (2003) The structure of DNA in the nucleosome core. Nature 423: 145–150.CrossRefPubMedGoogle Scholar
  91. Schalch T, Duda S, Sargent DF, Richmond TJ (2005) X-ray structure of a tetranucleosome and its implications for the chromatin fibre. Nature 436: 138–141.CrossRefPubMedGoogle Scholar
  92. Schmutzler C, Kohrle J (2000) Retinoic acid redifferentiation therapy for thyroid cancer. Thyroid 10: 393–406.PubMedGoogle Scholar
  93. Schotta G, Lachner M, Sarma K et al (2004) A silencing pathway to induce H3-K9 and H4-K20 trimethylation at constitutive heterochromatin. Genes Dev 18: 1251–1262.CrossRefPubMedGoogle Scholar
  94. Schubeler D, Francastel C, Cimbora DM, Reik A, Martin DI, Groudine M (2000) Nuclear localization and histone acetylation: a pathway for chromatin opening and transcriptional activation of the human beta-globin locus. Genes Dev 14: 940–950.PubMedGoogle Scholar
  95. Schwarz PM, Felthauser A, Fletcher TM, Hansen JC (1996) Reversible oligonucleosome self-association: dependence on divalent cations and core histone tail domains. Biochemistry 35: 4009–4015.CrossRefPubMedGoogle Scholar
  96. Setterfield G, Hall R, Bladon T, Little J, Kaplan JG (1983) Changes in structure and composition of lymphocyte nuclei during mitogenic stimulation. J Ultrastruct Res 82: 264–282.CrossRefPubMedGoogle Scholar
  97. Singh PB, Georgatos SD (2002) HP1: facts, open questions, and speculation. J Struct Biol 140: 10–16.CrossRefPubMedGoogle Scholar
  98. Springhetti EM, Istomina NE, Whisstock JC, Nikitina TV, woodcock CL, Grigoryev SA (2003) Role of the M-loop and reactive center loop domains in the folding and bridging of nucleosome arrays by MENT. J Biol Chem 278: 43384–43393.CrossRefPubMedGoogle Scholar
  99. Stein GS, Montecino M, van Wijnen AJ, Stein JL, Lian JB (2000) Nuclear structure-gene expression interrelationships: implications for aberrant gene expression in cancer. Cancer Res 60: 2067–2076.PubMedGoogle Scholar
  100. Stewart MD, Li J, Wong J (2005) Relationship between histone H3 lysine 9 methylation, transcription repression, and heterochromatin protein 1 recruitment. Mol Cell Biol 25: 2525–2538.PubMedGoogle Scholar
  101. Stocum DL (2002) Vertebrate regeneration. Semin Cell Dev Biol 13: 325–326.CrossRefPubMedGoogle Scholar
  102. Su RC, Brown KE, Saaber S, Fisher AG, Merkenschlager M, Smale ST (2004) Dynamic assembly of silent chromatin during thymocyte maturation. Nat Genet 36: 502–506.CrossRefPubMedGoogle Scholar
  103. Sugimura T, Ushijima T (2000) Genetic and epigenetic alterations in carcinogenesis. Mutat Res 462: 235–246.PubMedGoogle Scholar
  104. Sullivan BA, Karpen GH (2004) Centromeric chromatin exhibits a histone modification pattern that is distinct from both euchromatin and heterochromatin. Nat Struct Mol Biol 11: 1076–1083.CrossRefPubMedGoogle Scholar
  105. Sun FL, Cuaycong MH, Elgin SC (2001) Long-range nucleosome ordering is associated with gene silencing in Drosophila melanogaster pericentric heterochromatin. Mol Cell Biol 21: 2867–2879.CrossRefPubMedGoogle Scholar
  106. Sung MT, Freedlender EF (1978). Sites of in vivo phosphorylation of histone H5. Biochemistry 17: 1884–1890.CrossRefPubMedGoogle Scholar
  107. Suto RK, Clarkson MJ, Tremethick DJ, Luger K (2000) Crystal structure of a nucleosome core particle containing the variant histone H2AZ. Nat Struct Biol 7: 1121–1124.PubMedGoogle Scholar
  108. Swaminathan J, Baxter EM, Corces VG (2005) The role of histone H2Av variant replacement and histone H4 acetylation in the establishment of Drosophila heterochromatin. Genes Dev 19: 65–76.CrossRefPubMedGoogle Scholar
  109. Terranova R, Sauer S, Merkenschlager M, Fisher AG (2005) The reorganisation of constitutive heterochromatin in differentiating muscle requires HDAC activity. Exp Cell Res 20: 20.Google Scholar
  110. Thiru A, Nietlispach D, Mott HR et al (2004) Structural basis of HP1/PXVXL motif peptide interactions and HP1 localisation to heterochromatin. EMBO J 23: 489–499.CrossRefPubMedGoogle Scholar
  111. Thoma F, Koller T, Klug A (1979) Involvement of histone H1 in the organization of the nucleosome and of the salt-dependent superstructures of chromatin. J Cell Biol 83: 403–427.CrossRefPubMedGoogle Scholar
  112. Trinh LA, Ferrini R, Cobb BS et al (2001) Down-regulation of TDT transcription in CD4(+)CD8(+) thymocytes by Ikaros proteins in direct competition with an Ets activator. Genes Dev 15: 1817–1832.CrossRefPubMedGoogle Scholar
  113. Tse C, Hansen JC (1997) Hybrid trypsinized nucleosomal arrays: identification of multiple functional roles of the H2A/H2B and H3/H4 N-termini in chromatin fiber compaction. Biochemistry 36: 11381–11388.CrossRefPubMedGoogle Scholar
  114. 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.PubMedGoogle Scholar
  115. Tumbar T, Sudlow G, Belmont AS (1999) Large-scale chromatin unfolding and remodeling induced by VP16 acidic activation domain. J Cell Biol 145: 1341–1354.CrossRefPubMedGoogle Scholar
  116. 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.CrossRefPubMedGoogle Scholar
  117. Verschure PJ, van der Kraan I, de Leeuw W et al (2005) In vivo HP1 targeting causes large-scale chromatin condensation and enhanced histone lysine methylation. Mol Cell Biol 25: 4552–4564.CrossRefPubMedGoogle Scholar
  118. Villeponteau B, Brawley J, Martinson HG (1992) Nucleosome spacing is compressed in active chromatin domains of chick erythroid cells. Biochemistry 31: 1554–1563.CrossRefPubMedGoogle Scholar
  119. Wangh LJ, DeGrace D, Sanchez JA (1995) Efficient reactivation of Xenopus erythrocyte nuclei in Xenopus egg extracts. J Cell Sci 108: 2187–2196.PubMedGoogle Scholar
  120. Widom, J (1986) Physicochemical studies of the folding of the 100 Å nucleosome filament into the 300 Å filament. Cation dependence. J Mol Biol 190: 411–424.CrossRefPubMedGoogle Scholar
  121. Woodcock CL, Dimitrov S (2001) Higher order structure of chromatin and chromosomes. Curr Opin Genet Dev 11: 130–135.CrossRefPubMedGoogle Scholar
  122. Woodcock CL, Horowitz RA (1995) Chromatin organization reviewed. Trends Cell Biol 5: 272–277.CrossRefPubMedGoogle Scholar
  123. Woodcock CL, Frado LL, Rattner JB (1984) The higher-order structure of chromatin: evidence for a helical ribbon arrangement. J Cell Biol 99: 42–52.CrossRefPubMedGoogle Scholar
  124. Ye Q, Callebaut I, Pezhman A, Courvalin JC, Worman HJ (1997) Domain-specific interactions of human HP1-type chromodomain proteins and inner nuclear membrane protein LBR J Biol Chem 272: 14983–14989.PubMedGoogle Scholar
  125. Zlatanova J, Leuba SH (2003) Chromatin fibers, one-at-a-time. JMol Biol 331: 1–19.CrossRefPubMedGoogle Scholar
  126. Zlatanova J, Leuba SH, Yang G, Bustamante C, van Holde K (1994) Linker DNA accessibility in chromatin fibers of different conformations: a reevaluation. Proc Natl Acad Sci USA 91: 5277–5280.PubMedGoogle Scholar

Copyright information

© Springer 2006

Authors and Affiliations

  • Sergei A. Grigoryev
    • 1
  • Yaroslava A. Bulynko
    • 1
  • Evgenya Y. Popova
    • 1
  1. 1.Department of Biochemistry and Molecular Biology, H171Penn State University College of Medicine, Milton S Hershey Medical CenterHersheyUSA

Personalised recommendations