1932

Abstract

Nucleosomes and chromatin control eukaryotic genome accessibility and thereby regulate DNA processes, including transcription, replication, and repair. Conformational dynamics within the nucleosome and chromatin structure play a key role in this regulatory function. Structural fluctuations continuously expose internal DNA sequences and nucleosome surfaces, thereby providing transient access for the nuclear machinery. Progress in structural studies of nucleosomes and chromatin has provided detailed insight into local chromatin organization and has set the stage for recent in-depth investigations of the structural dynamics of nucleosomes and chromatin fibers. Here, we discuss the dynamic processes observed in chromatin over different length scales and timescales and review current knowledge about the biophysics of distinct structural transitions.

Loading

Article metrics loading...

/content/journals/10.1146/annurev-biophys-070317-032847
2019-05-06
2024-06-25
Loading full text...

Full text loading...

/deliver/fulltext/biophys/48/1/annurev-biophys-070317-032847.html?itemId=/content/journals/10.1146/annurev-biophys-070317-032847&mimeType=html&fmt=ahah

Literature Cited

  1. 1.
    Allahverdi A, Yang R, Korolev N, Fan Y, Davey CA et al. 2011. The effects of histone H4 tail acetylations on cation-induced chromatin folding and self-association. Nucleic Acids Res 39:1680–91
    [Google Scholar]
  2. 2.
    Anderson JD, Lowary PT, Widom J 2001. Effects of histone acetylation on the equilibrium accessibility of nucleosomal DNA target sites. J. Mol. Biol. 307:977–85
    [Google Scholar]
  3. 3.
    Anderson JD, Thastrom A, Widom J 2002. Spontaneous access of proteins to buried nucleosomal DNA target sites occurs via a mechanism that is distinct from nucleosome translocation. Mol. Cell. Biol. 22:7147–57
    [Google Scholar]
  4. 4.
    Anderson JD, Widom J 2000. Sequence and position-dependence of the equilibrium accessibility of nucleosomal DNA target sites. J. Mol. Biol. 296:979–87
    [Google Scholar]
  5. 5.
    Anderson JD, Widom J 2001. Poly(dA-dT) promoter elements increase the equilibrium accessibility of nucleosomal DNA target sites. Mol. Cell. Biol. 21:3830–39
    [Google Scholar]
  6. 6.
    Andrews AJ, Chen X, Zevin A, Stargell LA, Luger K 2010. The histone chaperone Nap1 promotes nucleosome assembly by eliminating nonnucleosomal histone DNA interactions. Mol. Cell 37:834–42
    [Google Scholar]
  7. 7.
    Andrews AJ, Luger K 2011. Nucleosome structure(s) and stability: variations on a theme. Annu. Rev. Biophys. 40:99–117
    [Google Scholar]
  8. 8.
    Angelov D, Vitolo JM, Mutskov V, Dimitrov S, Hayes JJ 2001. Preferential interaction of the core histone tail domains with linker DNA. PNAS 98:6599–604
    [Google Scholar]
  9. 9.
    Azzaz AM, Vitalini MW, Thomas AS, Price JP, Blacketer MJ et al. 2014. Human heterochromatin protein 1α promotes nucleosome associations that drive chromatin condensation. J. Biol. Chem. 289:6850–61
    [Google Scholar]
  10. 10.
    Bancaud A, Conde e Silva N, Barbi M, Wagner G, Allemand JF et al. 2006. Structural plasticity of single chromatin fibers revealed by torsional manipulation. Nat. Struct. Mol. Biol. 13:444–50
    [Google Scholar]
  11. 11.
    Beard DA, Schlick T 2001. Computational modeling predicts the structure and dynamics of chromatin fiber. Structure 9:105–14
    [Google Scholar]
  12. 12.
    Bednar J, Garcia-Saez I, Boopathi R, Cutter AR, Papai G et al. 2017. Structure and dynamics of a 197 bp nucleosome in complex with linker histone H1. Mol. Cell 66:384–97.e8
    [Google Scholar]
  13. 13.
    Bilokapic S, Strauss M, Halic M 2018. Histone octamer rearranges to adapt to DNA unwrapping. Nat. Struct. Mol. Biol. 25:101–8
    [Google Scholar]
  14. 14.
    Bintu L, Ishibashi T, Dangkulwanich M, Wu YY, Lubkowska L et al. 2012. Nucleosomal elements that control the topography of the barrier to transcription. Cell 151:738–49
    [Google Scholar]
  15. 15.
    Blossey R, Schiessel H 2011. The dynamics of the nucleosome: thermal effects, external forces and ATP. FEBS J 278:3619–32
    [Google Scholar]
  16. 16.
    Bohm V, Hieb AR, Andrews AJ, Gansen A, Rocker A et al. 2011. Nucleosome accessibility governed by the dimer/tetramer interface. Nucleic Acids Res 39:3093–102
    [Google Scholar]
  17. 17.
    Boublik M, Bradbury EM, Crane-Robinson C, Johns EW 1970. An investigation of the conformational changes of histone F2b by high resolution nuclear magnetic resonance. Eur. J. Biochem. 17:151–59
    [Google Scholar]
  18. 18.
    Bowman GD, Poirier MG 2015. Post-translational modifications of histones that influence nucleosome dynamics. Chem. Rev. 115:2274–95
    [Google Scholar]
  19. 19.
    Brehove M, Wang T, North J, Luo Y, Dreher SJ et al. 2015. Histone core phosphorylation regulates DNA accessibility. J. Biol. Chem. 290:22612–21
    [Google Scholar]
  20. 20.
    Brogaard K, Xi L, Wang JP, Widom J 2012. A map of nucleosome positions in yeast at base-pair resolution. Nature 486:496–501
    [Google Scholar]
  21. 21.
    Brower-Toland BD, Smith CL, Yeh RC, Lis JT, Peterson CL, Wang MD 2002. Mechanical disruption of individual nucleosomes reveals a reversible multistage release of DNA. PNAS 99:1960–65
    [Google Scholar]
  22. 22.
    Bryan LC, Weilandt DR, Bachmann AL, Kilic S, Lechner CC et al. 2017. Single-molecule kinetic analysis of HP1-chromatin binding reveals a dynamic network of histone modification and DNA interactions. Nucleic Acids Res 45:10504–17
    [Google Scholar]
  23. 23.
    Canzio D, Chang EY, Shankar S, Kuchenbecker KM, Simon MD et al. 2011. Chromodomain-mediated oligomerization of HP1 suggests a nucleosome-bridging mechanism for heterochromatin assembly. Mol. Cell 41:67–81
    [Google Scholar]
  24. 24.
    Canzio D, Liao M, Naber N, Pate E, Larson A et al. 2013. A conformational switch in HP1 releases auto-inhibition to drive heterochromatin assembly. Nature 496:377–81
    [Google Scholar]
  25. 25.
    Carter GJ, van Holde K 1998. Self-association of linker histone H5 and of its globular domain: evidence for specific self-contacts. Biochemistry 37:12477–88
    [Google Scholar]
  26. 26.
    Caterino TL, Hayes JJ 2011. Structure of the H1 C-terminal domain and function in chromatin condensation. Biochem. Cell Biol. 89:35–44
    [Google Scholar]
  27. 27.
    Chatterjee N, North JA, Dechassa ML, Manohar M, Prasad R et al. 2015. Histone acetylation near the nucleosome dyad axis enhances nucleosome disassembly by RSC and SWI/SNF. Mol. Cell. Biol. 35:4083–92
    [Google Scholar]
  28. 28.
    Chen C, Bundschuh R 2014. Quantitative models for accelerated protein dissociation from nucleosomal DNA. Nucleic Acids Res 42:9753–60
    [Google Scholar]
  29. 29.
    Chen Y, Tokuda JM, Topping T, Meisburger SP, Pabit SA et al. 2017. Asymmetric unwrapping of nucleosomal DNA propagates asymmetric opening and dissociation of the histone core. PNAS 114:334–39
    [Google Scholar]
  30. 30.
    Chereji RV, Morozov AV 2014. Ubiquitous nucleosome crowding in the yeast genome. PNAS 111:5236–41
    [Google Scholar]
  31. 31.
    Cheutin T, McNairn AJ, Jenuwein T, Gilbert DM, Singh PB, Misteli T 2003. Maintenance of stable heterochromatin domains by dynamic HP1 binding. Science 299:721–25
    [Google Scholar]
  32. 32.
    Chien FT, van Noort J 2009. 10 years of tension on chromatin: results from single molecule force spectroscopy. Curr. Pharm. Biotechnol. 10:474–85
    [Google Scholar]
  33. 33.
    Choy JS, Wei S, Lee JY, Tan S, Chu S, Lee TH 2010. DNA methylation increases nucleosome compaction and rigidity. J. Am. Chem. Soc. 132:1782–83
    [Google Scholar]
  34. 34.
    Collepardo-Guevara R, Portella G, Vendruscolo M, Frenkel D, Schlick T, Orozco M 2015. Chromatin unfolding by epigenetic modifications explained by dramatic impairment of internucleosome interactions: a multiscale computational study. J. Am. Chem. Soc. 137:10205–15
    [Google Scholar]
  35. 35.
    Correll SJ, Schubert MH, Grigoryev SA 2012. Short nucleosome repeats impose rotational modulations on chromatin fibre folding. EMBO J 31:2416–26
    [Google Scholar]
  36. 36.
    Cui Y, Bustamante C 2000. Pulling a single chromatin fiber reveals the forces that maintain its higher-order structure. PNAS 97:127–32
    [Google Scholar]
  37. 37.
    Debelouchina GT, Gerecht K, Muir TW 2017. Ubiquitin utilizes an acidic surface patch to alter chromatin structure. Nat. Chem. Biol. 13:105–10
    [Google Scholar]
  38. 38.
    Dekker J, Heard E 2015. Structural and functional diversity of topologically associating domains. FEBS Lett 589:2877–84
    [Google Scholar]
  39. 39.
    Dekker J, Rippe K, Dekker M, Kleckner N 2002. Capturing chromosome conformation. Science 295:1306–11
    [Google Scholar]
  40. 40.
    Dhall A, Wei S, Fierz B, Woodcock CL, Lee TH, Chatterjee C 2014. Sumoylated human histone H4 prevents chromatin compaction by inhibiting long-range internucleosomal interactions. J. Biol. Chem. 289:33827–37
    [Google Scholar]
  41. 41.
    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
    [Google Scholar]
  42. 42.
    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 306:1571–73
    [Google Scholar]
  43. 43.
    Ekundayo B, Richmond TJ, Schalch T 2017. Capturing structural heterogeneity in chromatin fibers. J. Mol. Biol. 429:3031–42
    [Google Scholar]
  44. 44.
    Eslami-Mossallam B, Schiessel H, van Noort J 2016. Nucleosome dynamics: Sequence matters. Adv. Colloid Interface Sci. 232:101–13
    [Google Scholar]
  45. 45.
    Festenstein R, Pagakis SN, Hiragami K, Lyon D, Verreault A et al. 2003. Modulation of heterochromatin protein 1 dynamics in primary mammalian cells. Science 299:719–21
    [Google Scholar]
  46. 46.
    Fierz B 2016. Dynamic chromatin regulation from a single molecule perspective. ACS Chem. Biol. 11:609–20
    [Google Scholar]
  47. 47.
    Fierz B, Chatterjee C, McGinty RK, Bar-Dagan M, Raleigh DP, Muir TW 2011. Histone H2B ubiquitylation disrupts local and higher-order chromatin compaction. Nat. Chem. Biol. 7:113–19
    [Google Scholar]
  48. 48.
    Finch JT, Klug A 1976. Solenoidal model for superstructure in chromatin. PNAS 73:1897–901
    [Google Scholar]
  49. 49.
    Finch JT, Noll M, Kornberg RD 1975. Electron microscopy of defined lengths of chromatin. PNAS 72:3320–22
    [Google Scholar]
  50. 50.
    Forties RA, North JA, Javaid S, Tabbaa OP, Fishel R et al. 2011. A quantitative model of nucleosome dynamics. Nucleic Acids Res 39:8306–13
    [Google Scholar]
  51. 51.
    Fussner E, Ching RW, Bazett-Jones DP 2011. Living without 30 nm chromatin fibers. Trends Biochem. Sci. 36:1–6
    [Google Scholar]
  52. 52.
    Gao M, Nadaud PS, Bernier MW, North JA, Hammel PC et al. 2013. Histone H3 and H4 N-terminal tails in nucleosome arrays at cellular concentrations probed by magic angle spinning NMR spectroscopy. J. Am. Chem. Soc. 135:15278–81
    [Google Scholar]
  53. 53.
    Gatchalian J, Wang X, Ikebe J, Cox KL, Tencer AH et al. 2017. Accessibility of the histone H3 tail in the nucleosome for binding of paired readers. Nat. Commun. 8:1489
    [Google Scholar]
  54. 54.
    Geggier S, Vologodskii A 2010. Sequence dependence of DNA bending rigidity. PNAS 107:15421–26
    [Google Scholar]
  55. 55.
    Graziano V, Gerchman SE, Schneider DK, Ramakrishnan V 1994. Histone H1 is located in the interior of the chromatin 30-nm filament. Nature 368:351–54
    [Google Scholar]
  56. 56.
    Grigoryev SA, Arya G, Correll S, Woodcock CL, Schlick T 2009. Evidence for heteromorphic chromatin fibers from analysis of nucleosome interactions. PNAS 106:13317–22
    [Google Scholar]
  57. 57.
    Grigoryev SA, Bascom G, Buckwalter JM, Schubert MB, Woodcock CL, Schlick T 2016. Hierarchical looping of zigzag nucleosome chains in metaphase chromosomes. PNAS 113:1238–43
    [Google Scholar]
  58. 58.
    Hager GL, McNally JG, Misteli T 2009. Transcription dynamics. Mol. Cell 35:741–53
    [Google Scholar]
  59. 59.
    Hall MA, Shundrovsky A, Bai L, Fulbright RM, Lis JT, Wang MD 2009. High-resolution dynamic mapping of histone-DNA interactions in a nucleosome. Nat. Struct. Mol. Biol. 16:124–29
    [Google Scholar]
  60. 60.
    Hansen JC 2002. Conformational dynamics of the chromatin fiber in solution: determinants, mechanisms, and functions. Annu. Rev. Biophys. Biomol. Struct. 31:361–92
    [Google Scholar]
  61. 61.
    Hansen JC, Turgeon CL 1999. Analytical ultracentrifugation of chromatin. Methods Mol. Biol. 119:127–41
    [Google Scholar]
  62. 62.
    Hilliard PR Jr., Smith RM, Rill RL 1986. Natural abundance carbon-13 nuclear magnetic resonance studies of histone and DNA dynamics in nucleosome cores. J. Biol. Chem. 261:5992–98
    [Google Scholar]
  63. 63.
    Hiragami-Hamada K, Soeroes S, Nikolov M, Wilkins B, Kreuz S et al. 2016. Dynamic and flexible H3K9me3 bridging via HP1β dimerization establishes a plastic state of condensed chromatin. Nat. Commun. 7:11310
    [Google Scholar]
  64. 64.
    Hsieh TH, Weiner A, Lajoie B, Dekker J, Friedman N, Rando OJ 2015. Mapping nucleosome resolution chromosome folding in yeast by Micro-C. Cell 162:108–19
    [Google Scholar]
  65. 65.
    Hsieh TS, Fudenberg G, Goloborodko A, Rando OJ 2016. Micro-C XL: assaying chromosome conformation from the nucleosome to the entire genome. Nat. Methods 13:1009–11
    [Google Scholar]
  66. 66.
    Ikebe J, Sakuraba S, Kono H 2016. H3 histone tail conformation within the nucleosome and the impact of K14 acetylation studied using enhanced sampling simulation. PLOS Comput. Biol. 12:e1004788
    [Google Scholar]
  67. 67.
    Ishida H, Kono H 2017. H4 tails potentially produce the diversity in the orientation of two nucleosomes. Biophys. J. 113:978–90
    [Google Scholar]
  68. 68.
    Joti Y, Hikima T, Nishino Y, Kamada F, Hihara S et al. 2012. Chromosomes without a 30-nm chromatin fiber. Nucleus 3:404–10
    [Google Scholar]
  69. 69.
    Kaczmarczyk A, Allahverdi A, Brouwer TB, Nordenskiold L, Dekker NH, van Noort J 2017. Single-molecule force spectroscopy on histone H4 tail-cross-linked chromatin reveals fiber folding. J. Biol. Chem. 292:17506–13
    [Google Scholar]
  70. 70.
    Kelbauskas L, Woodbury N, Lohr D 2009. DNA sequence-dependent variation in nucleosome structure, stability, and dynamics detected by a FRET-based analysis. Biochem. Cell Biol. 87:323–35
    [Google Scholar]
  71. 71.
    Kilic S, Bachmann AL, Bryan LC, Fierz B 2015. Multivalency governs HP1α association dynamics with the silent chromatin state. Nat. Commun. 6:7313
    [Google Scholar]
  72. 72.
    Kilic S, Boichenko I, Lechner CC, Fierz B 2018. A bi-terminal protein ligation strategy to probe chromatin structure during DNA damage. Chem. Sci. 9:3704–9
    [Google Scholar]
  73. 73.
    Kilic S, Felekyan S, Doroshenko O, Boichenko I, Dimura M et al. 2018. Single-molecule FRET reveals multiscale chromatin dynamics modulated by HP1α. Nat. Commun. 9:235
    [Google Scholar]
  74. 74.
    Kim J, Lee J, Lee TH 2015. Lysine acetylation facilitates spontaneous DNA dynamics in the nucleosome. J. Phys. Chem. B 119:15001–5
    [Google Scholar]
  75. 75.
    Kim S, Brostromer E, Xing D, Jin J, Chong S et al. 2013. Probing allostery through DNA. Science 339:816–19
    [Google Scholar]
  76. 76.
    Kitevski-LeBlanc JL, Yuwen T, Dyer PN, Rudolph J, Luger K, Kay LE 2018. Investigating the dynamics of destabilized nucleosomes using methyl-TROSY NMR. J. Am. Chem. Soc. 140:4774–77
    [Google Scholar]
  77. 77.
    Koopmans WJ, Buning R, Schmidt T, van Noort J 2009. spFRET using alternating excitation and FCS reveals progressive DNA unwrapping in nucleosomes. Biophys. J. 97:195–204
    [Google Scholar]
  78. 78.
    Korolev N, Lyubartsev AP, Nordenskiold L 2018. A systematic analysis of nucleosome core particle and nucleosome-nucleosome stacking structure. Sci. Rep. 8:1543
    [Google Scholar]
  79. 79.
    Koslover EF, Fuller CJ, Straight AF, Spakowitz AJ 2010. Local geometry and elasticity in compact chromatin structure. Biophys. J. 99:3941–50
    [Google Scholar]
  80. 80.
    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. 16:534–40
    [Google Scholar]
  81. 81.
    Kruithof M, van Noort J 2009. Hidden Markov analysis of nucleosome unwrapping under force. Biophys. J. 96:3708–15
    [Google Scholar]
  82. 82.
    Kujirai T, Ehara H, Fujino Y, Shirouzu M, Sekine SI, Kurumizaka H 2018. Structural basis of the nucleosome transition during RNA polymerase II passage. Science 362:595–98
    [Google Scholar]
  83. 83.
    Lee J, Lee TH 2017. Single-molecule investigations on histone H2A-H2B dynamics in the nucleosome. Biochemistry 56:977–85
    [Google Scholar]
  84. 84.
    Lee JY, Lee J, Yue H, Lee TH 2015. Dynamics of nucleosome assembly and effects of DNA methylation. J. Biol. Chem. 290:4291–303
    [Google Scholar]
  85. 85.
    Lee JY, Wei S, Lee TH 2011. Effects of histone acetylation by Piccolo NuA4 on the structure of a nucleosome and the interactions between two nucleosomes. J. Biol. Chem. 286:11099–109
    [Google Scholar]
  86. 86.
    Leforestier A, Fudaley S, Livolant F 1999. Spermidine-induced aggregation of nucleosome core particles: evidence for multiple liquid crystalline phases. J. Mol. Biol. 290:481–94
    [Google Scholar]
  87. 87.
    Li G, Levitus M, Bustamante C, Widom J 2005. Rapid spontaneous accessibility of nucleosomal DNA. Nat. Struct. Mol. Biol. 12:46–53
    [Google Scholar]
  88. 88.
    Li G, Reinberg D 2011. Chromatin higher-order structures and gene regulation. Curr. Opin. Genet. Dev. 21:175–86
    [Google Scholar]
  89. 89.
    Li G, Widom J 2004. Nucleosomes facilitate their own invasion. Nat. Struct. Mol. Biol. 11:763–69
    [Google Scholar]
  90. 90.
    Li W, Chen P, Yu J, Dong L, Liang D et al. 2016. FACT remodels the tetranucleosomal unit of chromatin fibers for gene transcription. Mol. Cell 64:120–33
    [Google Scholar]
  91. 91.
    Lilley DM, Howarth OW, Clark VM, Pardon JF, Richards BM 1976. The existence of random coil N-terminal peptides—‘tails’—in native histone complexes. FEBS Lett 62:7–10
    [Google Scholar]
  92. 92.
    Luger K, Dechassa ML, Tremethick DJ 2012. New insights into nucleosome and chromatin structure: an ordered state or a disordered affair. ? Nat. Rev. Mol. Cell Biol. 13:436–47
    [Google Scholar]
  93. 93.
    Luger K, Hansen JC 2005. Nucleosome and chromatin fiber dynamics. Curr. Opin. Struct. Biol. 15:188–96
    [Google Scholar]
  94. 94.
    Luger K, Mäder AW, Richmond RK, Sargent DF, Richmond TJ 1997. Crystal structure of the nucleosome core particle at 2.8 Å resolution. Nature 389:251–60
    [Google Scholar]
  95. 95.
    Luger K, Rechsteiner TJ, Flaus AJ, Waye MM, Richmond TJ 1997. Characterization of nucleosome core particles containing histone proteins made in bacteria. J. Mol. Biol. 272:301–11
    [Google Scholar]
  96. 96.
    Luo Y, North JA, Rose SD, Poirier MG 2014. Nucleosomes accelerate transcription factor dissociation. Nucleic Acids Res 42:3017–27
    [Google Scholar]
  97. 97.
    Mack AH, Schlingman DJ, Ilagan RP, Regan L, Mochrie SG 2012. Kinetics and thermodynamics of phenotype: unwinding and rewinding the nucleosome. J. Mol. Biol. 423:687–701
    [Google Scholar]
  98. 98.
    Mattiroli F, Bhattacharyya S, Dyer PN, White AE, Sandman K et al. 2017. Structure of histone-based chromatin in Archaea. Science 357:609–12
    [Google Scholar]
  99. 99.
    McGinty RK, Tan S 2015. Nucleosome structure and function. Chem. Rev. 115:2255–73
    [Google Scholar]
  100. 100.
    Mihardja S, Spakowitz AJ, Zhang Y, Bustamante C 2006. Effect of force on mononucleosomal dynamics. PNAS 103:15871–76
    [Google Scholar]
  101. 101.
    Miyagi A, Ando T, Lyubchenko YL 2011. Dynamics of nucleosomes assessed with time-lapse high-speed atomic force microscopy. Biochemistry 50:7901–8
    [Google Scholar]
  102. 102.
    Morrison EA, Bowerman S, Sylvers KL, Wereszczynski J, Musselman CA 2018. The conformation of the histone H3 tail inhibits association of the BPTF PHD finger with the nucleosome. eLife 7:e31481
    [Google Scholar]
  103. 103.
    Moyle-Heyrman G, Tims HS, Widom J 2011. Structural constraints in collaborative competition of transcription factors against the nucleosome. J. Mol. Biol. 412:634–46
    [Google Scholar]
  104. 104.
    Narlikar GJ, Sundaramoorthy R, Owen-Hughes T 2013. Mechanisms and functions of ATP-dependent chromatin-remodeling enzymes. Cell 154:490–503
    [Google Scholar]
  105. 105.
    Neumann H, Hancock SM, Buning R, Routh A, Chapman L et al. 2009. A method for genetically installing site-specific acetylation in recombinant histones defines the effects of H3 K56 acetylation. Mol. Cell 36:153–63
    [Google Scholar]
  106. 106.
    Ngo TT, Ha T 2015. Nucleosomes undergo slow spontaneous gaping. Nucleic Acids Res 43:3964–71
    [Google Scholar]
  107. 107.
    Ngo TT, Zhang Q, Zhou R, Yodh JG, Ha T 2015. Asymmetric unwrapping of nucleosomes under tension directed by DNA local flexibility. Cell 160:1135–44
    [Google Scholar]
  108. 108.
    Nikitina T, Norouzi D, Grigoryev SA, Zhurkin VB 2017. DNA topology in chromatin is defined by nucleosome spacing. Sci. Adv. 3:e1700957
    [Google Scholar]
  109. 109.
    Nishino Y, Eltsov M, Joti Y, Ito K, Takata H et al. 2012. Human mitotic chromosomes consist predominantly of irregularly folded nucleosome fibres without a 30-nm chromatin structure. EMBO J 31:1644–53
    [Google Scholar]
  110. 110.
    North JA, Shimko JC, Javaid S, Mooney AM, Shoffner MA et al. 2012. Regulation of the nucleosome unwrapping rate controls DNA accessibility. Nucleic Acids Res 40:10215–27
    [Google Scholar]
  111. 111.
    Ou HD, Phan S, Deerinck TJ, Thor A, Ellisman MH, O'Shea CC 2017. ChromEMT: visualizing 3D chromatin structure and compaction in interphase and mitotic cells. Science 357:eaag0025
    [Google Scholar]
  112. 112.
    Poirier MG, Bussiek M, Langowski J, Widom J 2008. Spontaneous access to DNA target sites in folded chromatin fibers. J. Mol. Biol. 379:772–86
    [Google Scholar]
  113. 113.
    Poirier MG, Oh E, Tims HS, Widom J 2009. Dynamics and function of compact nucleosome arrays. Nat. Struct. Mol. Biol. 16:938–44
    [Google Scholar]
  114. 114.
    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. 298:211–23
    [Google Scholar]
  115. 115.
    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. 254:130–49
    [Google Scholar]
  116. 116.
    Potoyan DA, Papoian GA 2012. Regulation of the H4 tail binding and folding landscapes via Lys-16 acetylation. PNAS 109:17857–62
    [Google Scholar]
  117. 117.
    Ranjith P, Yan J, Marko JF 2007. Nucleosome hopping and sliding kinetics determined from dynamics of single chromatin fibers in Xenopus egg extracts. PNAS 104:13649–54
    [Google Scholar]
  118. 118.
    Ricci MA, Manzo C, Garcia-Parajo MF, Lakadamyali M, Cosma MP 2015. Chromatin fibers are formed by heterogeneous groups of nucleosomes in vivo. Cell 160:1145–58
    [Google Scholar]
  119. 119.
    Richmond TJ, Davey CA 2003. The structure of DNA in the nucleosome core. Nature 423:145–50
    [Google Scholar]
  120. 120.
    Risca VI, Denny SK, Straight AF, Greenleaf WJ 2017. Variable chromatin structure revealed by in situ spatially correlated DNA cleavage mapping. Nature 541:237–41
    [Google Scholar]
  121. 121.
    Robinson PJ, An W, Routh A, Martino F, Chapman L et al. 2008. 30 nm chromatin fibre decompaction requires both H4-K16 acetylation and linker histone eviction. J. Mol. Biol. 381:816–25
    [Google Scholar]
  122. 122.
    Robinson PJ, Fairall L, Huynh VA, Rhodes D 2006. EM measurements define the dimensions of the “30-nm” chromatin fiber: evidence for a compact, interdigitated structure. PNAS 103:6506–11
    [Google Scholar]
  123. 123.
    Rothbart SB, Strahl BD 2014. Interpreting the language of histone and DNA modifications. Biochim. Biophys. Acta 1839:627–43
    [Google Scholar]
  124. 124.
    Routh A, Sandin S, Rhodes D 2008. Nucleosome repeat length and linker histone stoichiometry determine chromatin fiber structure. PNAS 105:8872–77
    [Google Scholar]
  125. 125.
    Schalch T, Duda S, Sargent DF, Richmond TJ 2005. X-ray structure of a tetranucleosome and its implications for the chromatin fibre. Nature 436:138–41
    [Google Scholar]
  126. 126.
    Scheffer MP, Eltsov M, Frangakis AS 2011. Evidence for short-range helical order in the 30-nm chromatin fibers of erythrocyte nuclei. PNAS 108:16992–97
    [Google Scholar]
  127. 127.
    Schiessel H, Gelbart WM, Bruinsma R 2001. DNA folding: structural and mechanical properties of the two-angle model for chromatin. Biophys. J. 80:1940–56
    [Google Scholar]
  128. 128.
    Shi X, Prasanna C, Nagashima T, Yamazaki T, Pervushin K, Nordenskiold L 2018. Structure and dynamics in the nucleosome revealed by solid-state NMR. Angew. Chem. Int. Ed. Engl. 57:9734–38
    [Google Scholar]
  129. 129.
    Shimko JC, North JA, Bruns AN, Poirier MG, Ottesen JJ 2011. Preparation of fully synthetic histone H3 reveals that acetyl-lysine 56 facilitates protein binding within nucleosomes. J. Mol. Biol. 408:187–204
    [Google Scholar]
  130. 130.
    Shogren-Knaak M, Ishii H, Sun JM, Pazin MJ, Davie JR, Peterson CL 2006. Histone H4-K16 acetylation controls chromatin structure and protein interactions. Science 311:844–47
    [Google Scholar]
  131. 131.
    Simon M, North JA, Shimko JC, Forties RA, Ferdinand MB et al. 2011. Histone fold modifications control nucleosome unwrapping and disassembly. PNAS 108:12711–16
    [Google Scholar]
  132. 132.
    Sinha KK, Gross JD, Narlikar GJ 2017. Distortion of histone octamer core promotes nucleosome mobilization by a chromatin remodeler. Science 355:eaaa3761
    [Google Scholar]
  133. 133.
    Song F, Chen P, Sun D, Wang M, Dong L et al. 2014. Cryo-EM study of the chromatin fiber reveals a double helix twisted by tetranucleosomal units. Science 344:376–80
    [Google Scholar]
  134. 134.
    Stehr R, Schopflin R, Ettig R, Kepper N, Rippe K, Wedemann G 2010. Exploring the conformational space of chromatin fibers and their stability by numerical dynamic phase diagrams. Biophys. J. 98:1028–37
    [Google Scholar]
  135. 135.
    Stockdale C, Bruno M, Ferreira H, Garcia-Wilson E, Wiechens N et al. 2006. Nucleosome dynamics. Biochem. Soc. Symp.73109–19
    [Google Scholar]
  136. 136.
    Stützer A, Liokatis S, Kiesel A, Schwarzer D, Sprangers R et al. 2016. Modulations of DNA contacts by linker histones and post-translational modifications determine the mobility and modifiability of nucleosomal H3 tails. Mol. Cell 61:247–59
    [Google Scholar]
  137. 137.
    Syed SH, Goutte-Gattat D, Becker N, Meyer S, Shukla MS et al. 2010. Single-base resolution mapping of H1-nucleosome interactions and 3D organization of the nucleosome. PNAS 107:9620–25
    [Google Scholar]
  138. 138.
    Tessarz P, Kouzarides T 2014. Histone core modifications regulating nucleosome structure and dynamics. Nat. Rev. Mol. Cell Biol. 15:703–8
    [Google Scholar]
  139. 139.
    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. 83:403–27
    [Google Scholar]
  140. 140.
    Thomas JO, Khabaza AJ 1980. Cross-linking of histone H1 in chromatin. Eur. J. Biochem. 112:501–11
    [Google Scholar]
  141. 141.
    Tims HS, Gurunathan K, Levitus M, Widom J 2011. Dynamics of nucleosome invasion by DNA binding proteins. J. Mol. Biol. 411:430–48
    [Google Scholar]
  142. 142.
    Torigoe SE, Urwin DL, Ishii H, Smith DE, Kadonaga JT 2011. Identification of a rapidly formed nonnucleosomal histone-DNA intermediate that is converted into chromatin by ACF. Mol. Cell 43:638–48
    [Google Scholar]
  143. 143.
    Valouev A, Johnson SM, Boyd SD, Smith CL, Fire AZ, Sidow A 2011. Determinants of nucleosome organization in primary human cells. Nature 474:516–20
    [Google Scholar]
  144. 144.
    Wang JP, Fondufe-Mittendorf Y, Xi L, Tsai GF, Segal E, Widom J 2008. Preferentially quantized linker DNA lengths in Saccharomyces cerevisiae. PLOS Comput. . Biol 4:e1000175
    [Google Scholar]
  145. 145.
    Wang X, Hayes JJ 2006. Physical methods used to study core histone tail structures and interactions in solution. Biochem. Cell Biol. 84:578–88
    [Google Scholar]
  146. 146.
    Wang X, Moore SC, Laszckzak M, Ausio J 2000. Acetylation increases the alpha-helical content of the histone tails of the nucleosome. J. Biol. Chem. 275:35013–20
    [Google Scholar]
  147. 147.
    Wedemann G, Langowski J 2002. Computer simulation of the 30-nanometer chromatin fiber. Biophys. J. 82:2847–59
    [Google Scholar]
  148. 148.
    Wei S, Falk SJ, Black BE, Lee TH 2015. A novel hybrid single molecule approach reveals spontaneous DNA motion in the nucleosome. Nucleic Acids Res 43:e111
    [Google Scholar]
  149. 149.
    Widlund HR, Vitolo JM, Thiriet C, Hayes JJ 2000. DNA sequence-dependent contributions of core histone tails to nucleosome stability: differential effects of acetylation and proteolytic tail removal. Biochemistry 39:3835–41
    [Google Scholar]
  150. 150.
    Widom J 1992. A relationship between the helical twist of DNA and the ordered positioning of nucleosomes in all eukaryotic cells. PNAS 89:1095–99
    [Google Scholar]
  151. 151.
    Widom J 2001. Role of DNA sequence in nucleosome stability and dynamics. Q. Rev. Biophys. 34:269–324
    [Google Scholar]
  152. 152.
    Wilkins B, Rall N, Ostwal Y, Kruitwagen T, Hiragami-Hamada K et al. 2014. A cascade of histone modifications induces chromatin condensation in mitosis. Science 343:77–80
    [Google Scholar]
  153. 153.
    Wolffe AP 1994. Gene regulation. Insulating chromatin. Curr. Biol. 4:85–87
    [Google Scholar]
  154. 154.
    Wolffe AP, Almouzni G, Ura K, Pruss D, Hayes JJ 1993. Transcription factor access to DNA in the nucleosome. Cold Spring Harb. Symp. Quant. Biol. 58:225–35
    [Google Scholar]
  155. 155.
    Wong H, Victor JM, Mozziconacci J 2007. An all-atom model of the chromatin fiber containing linker histones reveals a versatile structure tuned by the nucleosomal repeat length. PLOS ONE 2:e877
    [Google Scholar]
  156. 156.
    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
    [Google Scholar]
  157. 157.
    Woodcock CL, Grigoryev SA, Horowitz RA, Whitaker N 1993. A chromatin folding model that incorporates linker variability generates fibers resembling the native structures. PNAS 90:9021–25
    [Google Scholar]
  158. 158.
    Woodcock CL, Skoultchi AI, Fan Y 2006. Role of linker histone in chromatin structure and function: H1 stoichiometry and nucleosome repeat length. Chromosome Res 14:17–25
    [Google Scholar]
  159. 159.
    Worcel A, Strogatz S, Riley D 1981. Structure of chromatin and the linking number of DNA. PNAS 78:1461–65
    [Google Scholar]
  160. 160.
    Xue Y, Ward JM, Yuwen T, Podkorytov IS, Skrynnikov NR 2012. Microsecond time-scale conformational exchange in proteins: using long molecular dynamics trajectory to simulate NMR relaxation dispersion data. J. Am. Chem. Soc. 134:2555–62
    [Google Scholar]
  161. 161.
    Yang D, Arya G 2011. Structure and binding of the H4 histone tail and the effects of lysine 16 acetylation. Phys. Chem. Chem. Phys. 13:2911–21
    [Google Scholar]
  162. 162.
    Zhou BR, Feng H, Ghirlando R, Kato H, Gruschus J, Bai Y 2012. Histone H4 K16Q mutation, an acetylation mimic, causes structural disorder of its N-terminal basic patch in the nucleosome. J. Mol. Biol. 421:30–37
    [Google Scholar]
  163. 163.
    Zhou BR, Feng H, Kato H, Dai L, Yang Y et al. 2013. Structural insights into the histone H1-nucleosome complex. PNAS 110:19390–95
    [Google Scholar]
  164. 164.
    Zhou BR, Jiang J, Feng H, Ghirlando R, Xiao TS, Bai Y 2015. Structural mechanisms of nucleosome recognition by linker histones. Mol. Cell 59:628–38
    [Google Scholar]
  165. 165.
    Zhou CY, Johnson SL, Gamarra NI, Narlikar GJ 2016. Mechanisms of ATP-dependent chromatin remodeling motors. Annu. Rev. Biophys. 45:153–81
    [Google Scholar]
  166. 166.
    Zhou J, Fan JY, Rangasamy D, Tremethick DJ 2007. The nucleosome surface regulates chromatin compaction and couples it with transcriptional repression. Nat. Struct. Mol. Biol. 14:1070–76
    [Google Scholar]
/content/journals/10.1146/annurev-biophys-070317-032847
Loading
/content/journals/10.1146/annurev-biophys-070317-032847
Loading

Data & Media loading...

  • Article Type: Review Article
This is a required field
Please enter a valid email address
Approval was a Success
Invalid data
An Error Occurred
Approval was partially successful, following selected items could not be processed due to error