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Dynamic nucleosomes

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Abstract

It is now widely recognized that the packaging of genomic DNA together with core histones, linker histones, and other functional proteins into chromatin profoundly influences nuclear processes such as transcription, replication, repair and recombination. How chromatin structure modulates the expression and maintenance of knowledge encoded in eukaryotic genomes, and how these processes take place within the context of a highly complex and compacted genomic chromatin environment remains a major unresolved question in biology. Here we review recent advances in our understanding of how nucleosome and chromatin structure may have to adapt to promote these vital functions.

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References

  • Abbott DW, Ivanova VS, Wang X, Bonner WM, Ausio J (2001) Characterization of the stability and folding of H2A.Z chromatin particles: implications for transcriptional activation. J Biol Chem 276: 41945–41949.

    CAS  PubMed  Google Scholar 

  • Agresti A, Scaffidi P, Riva A, Caiolfa VR, Bianchi ME (2005) GR and HMGB1 interact only within chromatin and influence each other's residence time. Mol Cell 18: 109–121.

    Article  CAS  PubMed  Google Scholar 

  • Ahmad K, Henikoff S (2002) The histone variant H3.3 marks active chromatin by replication-independent nucleosome assembly. Mol Cell 9: 1191–1200.

    Article  CAS  PubMed  Google Scholar 

  • Akey CW, Luger K (2003) Histone chaperones and nucleosome assembly. Curr Opin Struct Biol 13: 6–14.

    Article  CAS  PubMed  Google Scholar 

  • Anderson JD, Widom J (2000) Sequence and position-dependence of the equilibrium accessibility of nucleosomal DNA target sites. J Mol Biol 296: 979–987.

    Article  CAS  PubMed  Google Scholar 

  • Angelov D, Charra M, Seve M, Cote J, Khochbin S, Dimitrov S (2000) Differential remodeling of the HIV-1 nucleosome upon transcription activators and SWI/SNF complex binding. J Mol Biol 302: 315–326.

    Article  CAS  PubMed  Google Scholar 

  • Bao Y, Konesky K, Park YJ et al. (2004) Nucleosomes containing the histone variant H2A.Bbd organize only 118 base pairs of DNA. EMBO J 23: 3314–3324.

    Article  CAS  PubMed  Google Scholar 

  • 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.

    Article  CAS  PubMed  Google Scholar 

  • Bianchi ME, Agresti A (2005) HMG proteins: dynamic players in gene regulation and differentiation. Curr Opin Genet Dev 15: 496–506.

    Article  CAS  PubMed  Google Scholar 

  • Bruno M, Flaus A, Stockdale C, Rencurel C, Ferreira H, Owen-Hughes T (2003) Histone H2A/H2B dimer exchange by ATP-dependent chromatin remodeling activities. Mol Cell 12: 1599–1606.

    Article  CAS  PubMed  Google Scholar 

  • Bruno M, Flaus A, Owen-Hughes T (2004) Site-specific attachment of reporter compounds to recombinant histones. Meth Enzymol 375: 211–228.

    CAS  PubMed  Google Scholar 

  • Bustin M (1999) Regulation of DNA-dependent activities by the functional motifs of the high-mobility-group chromosomal proteins. Mol Cell Biol 19: 5237–5246.

    CAS  PubMed  Google Scholar 

  • 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.

    Article  CAS  PubMed  Google Scholar 

  • Chakravarthy S, Bao Y, Roberts VA, Tremethick DJ, Luger K (2004) Structural characterisation of histone H2A variants. Cold Spring Harb Symp Quant Biol 69: 227–234.

    Google Scholar 

  • Chakravarthy S, Gundimella SK, Caron C et al. (2005) Structural characterization of the histone variant macroH2A. Mol Cell Biol 25: 7616–7624.

    Article  CAS  PubMed  Google Scholar 

  • Chantalat L, Nicholson JM, Lambert SJ (2003) Structure of the histone-core octamer in KCl/phosphate crystals at 2.15 A resolution. Acta Crystallogr D Biol Crystallogr 59: 1395–1407.

    Article  CAS  PubMed  Google Scholar 

  • Chen H, Li B, Workman JL (1994) A histone-binding protein, nucleoplasmin, stimulates transcription factor binding to nucleosomes and factor-induced nucleosome disassembly. EMBO J 13: 380–390.

    CAS  PubMed  Google Scholar 

  • Cirillo LA, Lin FR, Cuesta I, Friedman D, Jarnik M, Zaret KS (2002) Opening of compacted chromatin by early developmental transcription factors HNF3 (FoxA) and GATA-4. Mol Cell 9: 279–289.

    Article  CAS  PubMed  Google Scholar 

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

    Article  CAS  PubMed  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: 1097–1113.

    Article  CAS  PubMed  Google Scholar 

  • Dorigo B, Schalch T, Bystricky K, Richmond TJ (2003) Chromatin fiber folding: requirement for the histone H4 N-terminal tail. J Mol Biol 327: 85–96.

    Article  CAS  PubMed  Google Scholar 

  • 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.

    Article  CAS  PubMed  Google Scholar 

  • Fan HY, Narlikar GJ, Kingston RE (2004a) Noncovalent modification of chromatin: different remodeled products with different ATPase domains. Cold Spring Harb Symp Quant Biol 69: 183–192.

    CAS  PubMed  Google Scholar 

  • Fan JY, Rangasamy D, Luger K, Tremethick DJ (2004b) H2A.Z alters the nucleosome surface to promote HP1alpha-mediated chromatin fiber folding. Mol Cell 16: 655–661.

    Article  CAS  PubMed  Google Scholar 

  • Flaus A, Owen-Hughes T (2003) Dynamic properties of nucleosomes during thermal and ATP-driven mobilization. Mol Cell Biol 23: 7767–7779.

    Article  CAS  PubMed  Google Scholar 

  • Flaus A, Rencurel C, Ferreira H, Wiechens N, Owen-Hughes T (2004) Sin mutations alter inherent nucleosome mobility. EMBO J 23: 343–353.

    Article  CAS  PubMed  Google Scholar 

  • Freitas MA, Sklenar AR, Parthun MR (2004) Application of mass spectrometry to the identification and quantification of histone post-translational modifications. J Cell Biochem 92: 691–700.

    Article  CAS  PubMed  Google Scholar 

  • Gautier T, Abbott DW, Molla A, Verdel A, Ausio J, Dimitrov S (2004) Histone variant H2ABbd confers lower stability to the nucleosome. EMBO Rep 5: 715–720.

    Article  CAS  PubMed  Google Scholar 

  • Georgel PT, Hansen JC (2001) Linker histone function in chromatin: dual mechanisms of action. Biochem Cell Biol 79: 313–316.

    Article  CAS  PubMed  Google Scholar 

  • Glotov BO, Rudin AV, Severin ES (1982) Conditions for sliding of nucleosomes along DNA: SV 40 minichromosomes. Biochim Biophys Acta 696: 275–284.

    CAS  PubMed  Google Scholar 

  • Gordon F, Luger K, Hansen JC (2005) The core histone N-terminal tail domains function independently and additively during salt-dependent oligomerization of nucleosomal arrays. J Biol Chem 280: 33701–33706.

    CAS  PubMed  Google Scholar 

  • Gottesfeld JM, Melander C, Suto RK, Raviol H, Luger K, Dervan PB (2001) Sequence-specific recognition of DNA in the nucleosome by pyrrole–imidazole polyamides. J Mol Biol 309: 625–639.

    Article  Google Scholar 

  • Hansen JC (2002) Conformational dynamics of the chromatin fiber in solution: Determinants, mechanisms, and functions. Annu Rev Biophys Biomol Struct 31: 361–392.

    Article  CAS  PubMed  Google Scholar 

  • Hill DA, Imbalzano AN (2000) Human SWI/SNF nucleosome remodeling activity is partially inhibited by linker histone H1. Biochemistry 39: 11649–11656.

    CAS  PubMed  Google Scholar 

  • Hill DA, Peterson CL, Imbalzano AN (2005) Effects of HMGN1 on chromatin structure and SWI/SNF-mediated chromatin remodeling. J Biol Chem 280: 41777–41783.

    Google Scholar 

  • Ito T, Ikehara T, Nakagawa T, Kraus WL, Muramatsu M (2000) p300-mediated acetylation facilitates the transfer of histone H2A–H2B dimers from nucleosomes to a histone chaperone. Genes Dev 14: 1899–1907.

    CAS  PubMed  Google Scholar 

  • Jackson V (1990) In vivo studies on the dynamics of histone–DNA interaction: evidence for nucleosome dissolution during replication and transcription and a low level of dissolution independent of both. Biochemistry 29: 719–731.

    Article  CAS  PubMed  Google Scholar 

  • Jacobs SA, Khorasanizadeh S (2002) Structure of HP1 chromodomain bound to a lysine 9-methylated histone H3 tail. Science 295: 2080–2083.

    Article  CAS  PubMed  Google Scholar 

  • Khochbin S (2001) Histone H1 diversity: bridging regulatory signals to linker histone function. Gene 271: 1–12.

    Article  CAS  PubMed  Google Scholar 

  • Kimura H, Cook PR (2001) Kinetics of core histones in living human cells: little exchange of H3 and H4 and some rapid exchange of H2B. J Cell Biol 153: 1341–1353.

    Article  CAS  PubMed  Google Scholar 

  • Lee DY, Hayes JJ, Pruss D, Wolffe AP (1993) A positive role for histone acetylation in transcription factor access to nucleosomal DNA. Cell 72: 73–84.

    Article  CAS  PubMed  Google Scholar 

  • Lee H, Habas R, Abate-Shen C (2004) MSX1 cooperates with histone H1b for inhibition of transcription and myogenesis. Science 304: 1675–1678.

    CAS  PubMed  Google Scholar 

  • Lever MA, Th'ng JP, Sun X, Hendzel MJ (2000) Rapid exchange of histone H1.1 on chromatin in living human cells. Nature 408: 873–876.

    CAS  PubMed  Google Scholar 

  • Li B, Adams CC, Workman JL (1994) Nucleosome binding by the constitutive transcription factor Sp1. J Biol Chem 269: 7756–7763.

    CAS  PubMed  Google Scholar 

  • Li G, Widom J (2004) Nucleosomes facilitate their own invasion. Nat Struct Mol Biol 11: 763–769.

    CAS  PubMed  Google Scholar 

  • Luger K, Hansen JC (2005) Nucleosome and chromatin fiber dynamics. Curr Opin Struct Biol 15: 188–196.

    Article  CAS  PubMed  Google Scholar 

  • Luger K, Richmond TJ (1998a) DNA binding within the nucleosome core. Curr Opin Struck Biol 8: 33–40.

    CAS  Google Scholar 

  • Luger K, Richmond TJ (1998b) The histone tails of the nucleosome. Curr Opin Genet Dev 8: 140–146.

    Article  CAS  PubMed  Google Scholar 

  • Luger K, Maeder AW, Richmond RK, Sargent DF, Richmond TJ (1997) Crystal structure of the nucleosome core particle at 2.8 Å resolution. Nature 389: 251–259.

    CAS  PubMed  Google Scholar 

  • McBryant SJ, Adams VH, Hansen JC (2006) Chromatin architectural proteins. Chromosome Res 14: 39–51.

    Google Scholar 

  • McPherson CE, Shim EY, Friedman DS, Zaret KS (1993) An active tissue-specific enhancer and bound transcription factors existing in a precisely positioned nucleosomal array. Cell 75: 387–398.

    Article  CAS  PubMed  Google Scholar 

  • Millar CB, Kurdistani SK, Grunstein M (2004) Acetylation of yeast histone H4 lysine 16: a switch for protein interactions in heterochromatin and euchromatin. Cold Spring Harb Symp Quant Biol 69: 193–200.

    CAS  PubMed  Google Scholar 

  • Misteli T, Gunjan A, Hock R, Bustin M, Brown DT (2000) Dynamic binding of histone H1 to chromatin in living cells. Nature 408: 877–881.

    Article  CAS  PubMed  Google Scholar 

  • Mizuguchi G, Shen X, Landry J, Wu WH, Sen S, Wu C (2004) ATP-driven exchange of histone H2AZ variant catalyzed by SWR1 chromatin remodeling complex. Science 303: 343–348.

    Article  CAS  PubMed  Google Scholar 

  • Muthurajan UM, Park YJ, Edayathumangalam RS et al. (2003) Structure and dynamics of nucleosomal DNA. Biopolymers 68: 547–556.

    Article  CAS  PubMed  Google Scholar 

  • Muthurajan UM, Bao Y, Forsberg LJ et al. (2004) Crystal structures of histone Sin mutant nucleosomes reveal altered protein-DNA interactions. Embo J 23: 260–271.

    Article  CAS  PubMed  Google Scholar 

  • Mutskov V, Gerber D, Angelov D, Ausio J, Workman J, Dimitrov S (1998) Persistent interactions of core histone tails with nucleosomal DNA following acetylation and transcription factor binding. Mol Cell Biol 18: 6293–6304.

    CAS  PubMed  Google Scholar 

  • Nagaich AK, Walker DA, Wolford R, Hager GL (2004) Rapid periodic binding and displacement of the glucocorticoid receptor during chromatin remodeling. Mol Cell 14: 163–174.

    Article  CAS  PubMed  Google Scholar 

  • Park YJ, Dyer PN, Tremethick DJ, Luger K (2004) A new fluorescence resonance energy transfer approach demonstrates that the histone variant H2AZ stabilizes the histone octamer within the nucleosome. J Biol Chem 279: 24274–24282.

    CAS  PubMed  Google Scholar 

  • Park YJ, Chodaparambil JV, Bao Y, McBryant SJ, Luger K (2005) Nucleosome assembly protein 1 exchanges histone H2A–H2B dimers and assists nucleosome sliding. J Biol Chem 280: 1817–1825.

    CAS  PubMed  Google Scholar 

  • Pennings S, Meersseman G, Bradbury EM (1991) Mobility of positioned nucleosomes on 5 S rDNA. J Mol Biol 220: 101–110.

    Article  CAS  PubMed  Google Scholar 

  • Peterson CL, Tamkun JW (1995) The SWI–SNF complex: a chromatin remodeling machine? Trends Biochem Sci 20: 143–146.

    Article  CAS  PubMed  Google Scholar 

  • Polach KJ, Widom J (1995) Mechanism of protein access to specific DNA sequences in chromatin: a dynamic equilibrium model for gene regulation. J Mol Biol 254: 130–149.

    Article  CAS  PubMed  Google Scholar 

  • Polach KJ, Lowary PT, Widom J (2000) Effects of core histone tail domains on the equilibrium constants for dynamic DNA site accessibility in nucleosomes. J Mol Biol 298: 211–223.

    Article  CAS  PubMed  Google Scholar 

  • Ragab A, Travers A (2003) HMG-D and histone H1 alter the local accessibility of nucleosomal DNA. Nucleic Acids Res 31: 7083–7089.

    Article  CAS  PubMed  Google Scholar 

  • Santisteban MS, Kalashnikova T, Smith MM (2000) Histone H2A.Z regulates transcription and is partially redundant with nucleosome remodeling complexes. Cell 103: 411–422.

    Article  CAS  PubMed  Google Scholar 

  • 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.

    Article  CAS  PubMed  Google Scholar 

  • Shi Y, Lan F, Matson C et al. (2004) Histone demethylation mediated by the nuclear amine oxidase homolog LSD1. Cell 119: 941–953.

    Article  CAS  PubMed  Google Scholar 

  • Smith CL, Peterson CL (2005) ATP-dependent chromatin remodeling. Curr Top Dev Biol 65: 115–148.

    CAS  PubMed  Google Scholar 

  • Spangenberg C, Eisfeld, K Stunkel W et al. (1998) The mouse mammary tumour virus promoter positioned on a tetramer of histones H3 and H4 binds nuclear factor 1 and OTF1. J Mol Biol 275: 725–739.

    Google Scholar 

  • Sullivan S, Sink DW, Trout KL et al. (2002) The histone database. Nucleic Acids Res 30: 341–342.

    Article  CAS  PubMed  Google Scholar 

  • Suto RK, Clarkson MJ, Tremethick DJ, Luger K (2000) Crystal structure of a nucleosome core particle containing the variant histone H2A.Z Nat Struct Biol 7: 1121–1124.

    CAS  PubMed  Google Scholar 

  • Thomas JO (1999) Histone H1: location and role. Curr Opin Cell Biol 11: 312–317.

    Article  CAS  PubMed  Google Scholar 

  • Toth K, Brun N, Langowski J (2001) Trajectory of nucleosomal linker DNA studied by fluorescence resonance energy transfer. Biochemistry 40: 6921–6928.

    Article  CAS  PubMed  Google Scholar 

  • Travers A (1999) The location of the linker histone on the nucleosome. Trends Biochem Sci 24: 4–7.

    Article  CAS  PubMed  Google Scholar 

  • Tsukiyama T, Becker PB, Wu C (1994) ATP-dependent nucleosome disruption at a heat-shock promoter mediated by binding of GAGA transcription factor. Nature 367: 525–532.

    Article  CAS  PubMed  Google Scholar 

  • Tsunaka Y, Kajimura N, Tate S, Morikawa K (2005) Alteration of the nucleosomal DNA path in the crystal structure of a human nucleosome core particle. Nucl Acids Res 33: 3424–3434.

    Article  CAS  PubMed  Google Scholar 

  • Vitolo JM, Thiriet C, Hayes JJ (2000) The H3–H4 N-terminal tail domains are the primary mediators of transcription factor IIIA access to 5S DNA within a nucleosome. Mol Cell Biol 20: 2167–2175.

    Article  CAS  PubMed  Google Scholar 

  • White CL, Luger K (2004) Defined structural changes occur in a nucleosome upon Amt1 transcription factor binding. J Mol Biol 342: 1391–1402.

    Article  CAS  PubMed  Google Scholar 

  • White CL, Suto RK, Luger K (2001) Structure of the yeast nucleosome core particle reveals fundamental changes in internucleosome interactions. EMBO J 20: 5207–5218.

    Article  CAS  PubMed  Google Scholar 

  • Wysocka J, Milne TA, Allis CD (2005) Taking LSD 1 to a new high. Cell 122: 654–658.

    Article  CAS  PubMed  Google Scholar 

  • Zhang H, Roberts DN, Cairns BR (2005) Genome-wide dynamics of Htz1, a histone H2A variant that poises repressed/basal promoters for activation through histone loss. Cell 123: 219–231.

    Article  CAS  PubMed  Google Scholar 

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Correspondence to Karolin Luger.

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Luger, K. Dynamic nucleosomes. Chromosome Res 14, 5–16 (2006). https://doi.org/10.1007/s10577-005-1026-1

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