Structure and organization of chromatin fiber in the nucleus

FEBS Letters

Volumn 589, Issue 20, 2015, Pages 2893-2904

  Li, Guohong ^a   Zhu, Ping ^a  

^a INSTITUTE OF BIOPHYSICS   (China)

Author keywords

30 nm chromatin fiber; Epigenetics; Histone; Nucleosome; Nucleosome repeat length

Indexed keywords

DEOXYRIBONUCLEASE I; DEOXYRIBONUCLEASE II; HISTONE H1; HISTONE H2A; HISTONE H2B; HISTONE H5; CHROMATIN; DNA;

AMINO TERMINAL SEQUENCE; CARBOXY TERMINAL SEQUENCE; CELL NUCLEUS; CELLULAR PARAMETERS; CHROMATIN; CHROMATIN FIBER; CHROMATIN STRUCTURE; COMPUTER MODEL; CONFORMATION; CRYOELECTRON MICROSCOPY; CRYSTAL STRUCTURE; DNA POLYMORPHISM; DNA SEQUENCE; EPIGENETICS; GENETIC REGULATION; HUMAN; IN VITRO STUDY; MOLECULAR DYNAMICS; MOLECULAR INTERACTION; NONHUMAN; NUCLEOSOME; NUCLEOSOME NUCLEOSOME INTERACTION; NUCLEOSOME REPEAT LENGTH; PRIORITY JOURNAL; PROTEIN FUNCTION; REVIEW; SOLENOID MODEL; STRUCTURE ACTIVITY RELATION; STRUCTURE ANALYSIS; ZIG ZAG MODEL; ANIMAL; CHEMICAL STRUCTURE; GENETIC EPIGENESIS; GENETIC POLYMORPHISM; GENETICS; PHYSIOLOGY; ULTRASTRUCTURE;

ANIMALS; CELL NUCLEUS; CHROMATIN; DNA; EPIGENESIS, GENETIC; HUMANS; MODELS, MOLECULAR; NUCLEIC ACID CONFORMATION; POLYMORPHISM, GENETIC;

EID: 84943197820     PISSN: 00145793     EISSN: 18733468     Source Type: Journal    
DOI: 10.1016/j.febslet.2015.04.023     Document Type: Review

References (135)

1. R.D. Kornberg Chromatin structure: a repeating unit of histones and DNA Science 184 1974 868 871
2. K. Luger, A.W. Mader, R.K. Richmond, D.F. Sargent, and T.J. Richmond Crystal structure of the nucleosome core particle at 2.8 angstrom resolution Nature 389 1997 251 260
3. G.H. Li, and D. Reinberg Chromatin higher-order structures and gene regulation Curr. Opin. Genet. Dev. 21 2011 175 186
4. F. Thoma, T. Koller, and A. Klug Involvement of histone-H1 in the organization of the nucleosome and of the salt-dependent superstructures of chromatin J. Cell Biol. 83 1979 403 427
5. J. Widom, and A. Klug Structure of the 300A chromatin filament: X-ray diffraction from oriented samples Cell 43 1985 207 213
6. C.A. Davey, D.F. Sargent, K. Luger, A.W. Maeder, and T.J. Richmond Solvent mediated interactions in the structure of the nucleosome core particle at 1.9 angstrom resolution J. Mol. Biol. 319 2002 1097 1113
7. P.J. Robinson, and D. Rhodes Structure of the '30 nm' chromatin fibre: a key role for the linker histone Curr. Opin. Struct. Biol. 16 2006 336 343
8. A. Hamiche, P. Schultz, V. Ramakrishnan, P. Oudet, and A. Prunell Linker histone-dependent DNA structure in linear mononucleosomes J. Mol. Biol. 257 1996 30 42
9. D. Pruss, B. Bartholomew, J. Persinger, J. Hayes, G. Arents, E.N. Moudrianakis, and A.P. Wolffe An asymmetric model for the nucleosome: a binding site for linker histones inside the DNA gyres Science 274 1996 614 617
10. G.H. Li, R. Margueron, G.B. Hu, D. Stokes, Y.H. Wang, and D. Reinberg Highly compacted chromatin formed in vitro reflects the dynamics of transcription activation in vivo Mol. Cell 38 2010 41 53
11. J.T. Finch, and A. Klug Solenoidal model for superstructure in chromatin Proc. Natl. Acad. Sci. U.S.A. 73 1976 1897 1901
12. J.D. Mcghee, J.M. Nickol, G. Felsenfeld, and D.C. Rau Higher-order structure of chromatin - orientation of nucleosomes within the 30 nm chromatin solenoid is independent of species and spacer length Cell 33 1983 831 841
13. A. Worcel, S. Strogatz, and D. Riley Structure of chromatin and the linking number of DNA Proc. Natl. Acad. Sci. Biol. 78 1981 1461 1465
14. C.L.F. Woodcock, L.L.Y. Frado, and J.B. Rattner The higher-order structure of chromatin - evidence for a helical ribbon arrangement J. Cell Biol. 99 1984 42 52
15. D.Z. Staynov, S. Dunn, J.P. Baldwin, and C. Cranerobinson Nuclease digestion patterns as a criterion for nucleosome orientation in the higher-order structure of chromatin FEBS Lett. 157 1983 311 315
16. S.P. Williams, B.D. Athey, L.J. Muglia, R.S. Schappe, A.H. Gough, and J.P. Langmore Chromatin fibers are left-handed double helices with diameter and mass per unit length that depend on linker length Biophys. J. 49 1986 233 248
17. H. Zentgraf, and W.W. Franke Differences of supranucleosomal organization in different kinds of chromatin - cell type-specific globular subunits containing different numbers of nucleosomes J. Cell Biol. 99 1984 272 286
18. R.T. Simpson, F. Thoma, and J.M. Brubaker Chromatin reconstituted from tandemly repeated cloned dna fragments and core histones - a model system for study of higher-order structure Cell 42 1985 799 808
19. M. Garciaramirez, F. Dong, and J. Ausio Role of the histone tails in the folding of oligonucleosomes depleted of histone-H1 J. Biol. Chem. 267 1992 19587 19595
20. L.M. Carruthers, J. Bednar, C.L. Woodcock, and J.C. Hansen Linker histones stabilize the intrinsic salt-dependent folding of nucleosomal arrays: mechanistic ramifications for higher-order chromatin folding Biochem.-Us 37 1998 14776 14787
21. P.T. Lowary, and J. Widom New DNA sequence rules for high affinity binding to histone octamer and sequence-directed nucleosome positioning J. Mol. Biol. 276 1998 19 42
22. B. Dorigo, T. Schalch, A. Kulangara, S. Duda, R.R. Schroeder, and T.J. Richmond Nucleosome arrays reveal the two-start organization of the chromatin fiber Science 306 2004 1571 1573
23. P.J. Robinson, L. Fairall, V.A. Huynh, and D. Rhodes EM measurements define the dimensions of the "30-nm" chromatin fiber: evidence for a compact, interdigitated structure Proc. Natl. Acad. Sci. U.S.A. 103 2006 6506 6511
24. T. Schalch, S. Duda, D.F. Sargent, and T.J. Richmond X-ray structure of a tetranucleosome and its implications for the chromatin fibre Nature 436 2005 138 141
25. S.A. Grigoryev, G. Arya, S. Correll, C.L. Woodcock, and T. Schlick Evidence for heteromorphic chromatin fibers from analysis of nucleosome interactions Proc. Natl. Acad. Sci. U.S.A. 106 2009 13317 13322
26. B. Rydberg, W.R. Holley, I.S. Mian, and A. Chatterjee Chromatin conformation in living cells: support for a zig-zag model of the 30 nm chromatin fiber J. Mol. Biol. 284 1998 71 84
27. A. Routh, S. Sandin, and D. Rhodes Nucleosome repeat length and linker histone stoichiometry determine chromatin fiber structure Proc. Natl. Acad. Sci. U.S.A. 105 2008 8872 8877
28. F. Song, P. Chen, D. Sun, M. Wang, L. Dong, D. Liang, R.M. Xu, P. Zhu, and G. Li Cryo-EM study of the chromatin fiber reveals a double helix twisted by tetranucleosomal units Science 344 2014 376 380
29. A. Travers Structural biology. The 30-nm fiber redux Science 344 2014 370 372
30. V. Ramakrishnan, J.T. Finch, V. Graziano, P.L. Lee, and R.M. Sweet Crystal-structure of globular domain of Histone H5 and its implications for nucleosome binding Nature 362 1993 219 223
31. N. Happel, and D. Doenecke Histone H1 and its isoforms: contribution to chromatin structure and function Gene 431 2009 1 12
32. A. Izzo, K. Kamieniarz, and R. Schneider The histone H1 family: specific members, specific functions? Biol. Chem. 389 2008 333 343
33. J. Allan, P.G. Hartman, C. Cranerobinson, and F.X. Aviles The structure of histone-H1 and its location in chromatin Nature 288 1980 675 679
34. L.L.Y. Frado, C.V. Mura, B.D. Stollar, and C.L.F. Woodcock Mapping of histone-H5 sites on nucleosomes using immunoelectron microscopy J. Biol. Chem. 258 1983 1984 1990
35. S.H. Syed, D. Goutte-Gattat, N. Becker, S. Meyer, M.S. Shukla, J.J. Hayes, R. Everaers, D. Angelov, J. Bednar, and S. Dimitrov Single-base resolution mapping of H1-nucleosome interactions and 3D organization of the nucleosome Proc. Natl. Acad. Sci. U.S.A. 107 2010 9620 9625
36. D.T. Brown, T. Izard, and T. Misteli Mapping the interaction surface of linker histone H1(0) with the nucleosome of native chromatin in vivo (vol. 13, p. 250) Nat. Struct. Mol. Biol. 13 2006 465-465
37. J. Bednar, R.A. Horowitz, S.A. Grigoryev, L.M. Carruthers, J.C. Hansen, A.J. Koster, and C.L. Woodcock 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. U.S.A. 95 1998 14173 14178
38. P. Puigdomenech, M. Jose, A. Ruizcarrillo, and C. Cranerobinson Isolation of a 167 basepair chromatosome containing a partially digested histone-H5 FEBS Lett. 154 1983 151 155
39. C. CraneRobinson Where is the globular domain of linker histone located on the nucleosome? Trends Biochem. Sci. 22 1997 75 77
40. M. Vignali, and J.L. Workman Location and function of linker histones Nat. Struct. Biol. 5 1998 1025 1028
41. A. Travers The location of the linker histone on the nucleosome Trends Biochem. Sci. 24 1999 4 7
42. D.Z. Staynov, and C. Cranerobinson Footprinting of linker histones-H5 and histones-H1 on the nucleosome EMBO J. 7 1988 3685 3691
43. L. Fan, and V.A. Roberts Complex of linker histone H5 with the nucleosome and its implications for chromatin packing Proc. Natl. Acad. Sci. U.S.A. 103 2006 8384 8389
44. W.J. An, S.H. Leuba, K. van Holde, and J. Zlatanova Linker histone protects linker DNA on only one side of the core particle and in a sequence-dependent manner Proc. Natl. Acad. Sci. U.S.A. 95 1998 3396 3401
45. J.J. Hayes, and A.P. Wolffe Preferential and asymmetric interaction of linker histones with 5s DNA in the nucleosome Proc. Natl. Acad. Sci. U.S.A. 90 1993 6415 6419
46. J. Wong, Q. Li, B.Z. Levi, Y.B. Shi, and A.P. Wolffe Structural and functional features of a specific nucleosome containing a recognition element for the thyroid hormone receptor EMBO J. 16 1997 7130 7145
47. S.I. Dimitrov, V.R. Russanova, and I.G. Pashev The globular domain of histone H-5 is internally located in the 30-nm chromatin fiber - an immunochemical study EMBO J. 6 1987 2387 2392
48. A.C. Lennard, and J.O. Thomas The arrangement of H-5 molecules in extended and condensed chicken erythrocyte chromatin EMBO J. 4 1985 3455 3462
49. G.J. Carter, and K. van Holde Self-association of linker histone H5 and of its globular domain: evidence for specific self-contacts Biochem.-Us 37 1998 12477 12488
50. B.R. Zhou, H.Q. Feng, H. Kato, L. Dai, Y.D. Yang, Y.Q. Zhou, and Y.W. Bai Structural insights into the histone H1-nucleosome complex Proc. Natl. Acad. Sci. U.S.A. 110 2013 19390 19395
51. F.A. Goytisolo, S.E. Gerchman, X. Yu, C. Rees, V. Graziano, V. Ramakrishnan, and J.O. Thomas Identification of two DNA-binding sites on the globular domain of histone H5 EMBO J. 15 1996 3421 3429
52. Y.B. Zhou, S.E. Gerchman, V. Ramakrishnan, A. Travers, and S. Muyldermans Position and orientation of the globular domain of linker histone H5 on the nucleosome Nature 395 1998 402 405
53. L. Chantalat, J.M. Nicholson, S.J. Lambert, A.J. Reid, M.J. Donovan, C.D. Reynolds, C.M. Wood, and J.P. Baldwin Structure of the histone-core octamer in KCl/phosphate crystals at 2.15 angstrom resolution Acta Crystallogr. D 59 2003 1395 1407
54. B. Dorigo, T. Schalch, K. Bystricky, and T.J. Richmond Chromatin fiber folding: requirement for the histone H4N-terminal tail J. Mol. Biol. 327 2003 85 96
55. A.A. Kalashnikova, M.E. Porter-Goff, U.M. Muthurajan, K. Luger, and J.C. Hansen The role of the nucleosome acidic patch in modulating higher order chromatin structure J. R. Soc. Interface 10 2013
56. D.Z. Staynov DNase I digestion reveals alternating asymmetrical protection of the nucleosome by the higher order chromatin structure Nucleic Acids Res. 28 2000 3092 3099
57. R.K. McGinty, R.C. Henrici, and S. Tan Crystal structure of the PRC1 ubiquitylation module bound to the nucleosome Nature 514 2014 591 596
58. M.P. Scheffer, M. Eltsov, and A.S. Frangakis Evidence for short-range helical order in the 30-nm chromatin fibers of erythrocyte nuclei Proc. Natl. Acad. Sci. U.S.A. 108 2011 16992 16997
59. M.J. Blacketer, S.J. Feely, and M.A. Shogren-Knaak Nucleosome interactions and stability in an ordered nucleosome array model system J. Biol. Chem. 285 2010 34597 34607
60. T.D. Frouws, H.G. Patterton, and B.T. Sewell Histone octamer helical tubes suggest that an internucleosomal four-helix bundle stabilizes the chromatin fiber Biophys. J. 96 2009 3363 3371
61. J. Ausio The shades of gray of the chromatin fiber: recent literature provides new insights into the structure of chromatin BioEssays 37 2015 46 51
62. J.P. Wang, Y. Fondufe-Mittendorf, L.Q. Xi, G.F. Tsai, E. Segal, and J. Widom Preferentially quantized linker DNA lengths in Saccharomyces cerevisiae PLoS Comput. Biol. 4 2008
63. J. Widom A relationship between the helical twist of DNA and the ordered positioning of nucleosomes in all eukaryotic cells Proc. Natl. Acad. Sci. U.S.A. 89 1992 1095 1099
64. M. Depken, and H. Schiessel Nucleosome shape dictates chromatin fiber structure Biophys. J. 96 2009 777 784
65. H. Wong, J.M. Victor, and J. Mozziconacci An all-atom model of the chromatin fiber containing linker histones reveals a versatile structure tuned by the nucleosomal repeat length PLoS ONE 2 2007
66. E.F. Koslover, C. Fuller, A.F. Straight, and A.J. Spakowitz Role of DNA elasticity and nucleosome geometry in hierarchical packaging of chromatin Biophys. J. 98 2010 474a
67. R. Collepardo-Guevara, and T. Schlick Chromatin fiber polymorphism triggered by variations of DNA linker lengths Proc. Natl. Acad. Sci. U.S.A. 111 2014 8061 8066
68. M. Kruithof, F.T. Chien, A. Routh, C. Logie, D. Rhodes, and J. van Noort Single-molecule force spectroscopy reveals a highly compliant helical folding for the 30-nm chromatin fiber Nat. Struct. Mol. Biol. 16 2009 534 540
69. S.J. Correll, M.H. Schubert, and S.A. Grigoryev Short nucleosome repeats impose rotational modulations on chromatin fibre folding EMBO J. 31 2012 2416 2426
70. M. Manohar, A.M. Mooney, J.A. North, R.J. Nakkula, J.W. Picking, A. Edon, R. Fishel, M.G. Poirier, and J.J. Ottesen Acetylation of histone H3 at the nucleosome dyad alters DNA-histone binding J. Biol. Chem. 284 2009 23312 23321
71. H. Tachiwana, W. Kagawa, T. Shiga, A. Osakabe, Y. Miya, K. Saito, Y. Hayashi-Takanaka, T. Oda, M. Sato, S.Y. Park, H. Kimura, and H. Kurumizaka Crystal structure of the human centromeric nucleosome containing CENP-A Nature 476 2011 232 235
72. C.M. Doyen, F. Montel, T. Gautier, H. Menoni, C. Claudet, M. Delacour-Larose, D. Angelov, A. Hamiche, J. Bednar, C. Faivre-Moskalenko, P. Bouvet, and S. Dimitrov Dissection of the unusual structural and functional properties of the variant H2A.Bbd nucleosome EMBO J. 25 2006 4234 4244
73. S.R. Kassabov, B. Zhang, J. Persinger, and B. Bartholomew SWI/SNF unwraps, slides, and rewraps the nucleosome Mol. Cell 11 2003 391 403
74. Y. Dalal, H. Wang, S. Lindsay, and S. Henikoff Tetrameric structure of centromeric nucleosomes in interphase Drosophila cells PLoS Biol. 5 2007 1798 1809
75. V.L. Makarov, S.I. Dimitrov, I.R. Tsaneva, and I.G. Pashev The role of histone-H1 and non-structured domains of core histones in maintaining the orientation of nucleosomes within the chromatin fiber Biochem. Biophys. Res. Co. 122 1984 1021 1027
76. L.L. Wallrath, and S.C.R. Elgin Position effect variegation in drosophila is associated with an altered chromatin structure Gene Dev. 9 1995 1263 1277
77. A.T. Annunziato, and J.C. Hansen Role of histone acetylation in the assembly and modulation of chromatin structures Gene Expr. 9 2000 37 61
78. V.G. Allfrey, R. Faulkner, and A.E. Mirsky Acetylation + methylation of histones + their possible role in regulation of RNA synthesis Proc. Natl. Acad. Sci. U.S.A. 51 1964 786 794
79. M. Roberge, T.E. Oneill, and E.M. Bradbury Inhibition of 5s RNA-transcription invitro by nucleosome cores with low or high-levels of histone acetylation FEBS Lett. 288 1991 215 218
80. L. Hong, G.P. Schroth, H.R. Matthews, P. Yau, and E.M. Bradbury Studies of the DNA-binding properties of histone H4 amino terminus - thermal-denaturation studies reveal that acetylation markedly reduces the binding constant of the H4 tail to DNA J. Biol. Chem. 268 1993 305 314
81. M. Garcia-Ramirez, C. Rocchini, and J. Ausio Modulation of chromatin folding by histone acetylation J. Biol. Chem. 270 1995 17923 17928
82. C. Tse, T. Sera, A.P. Wolffe, and J.C. Hansen Disruption of higher-order folding by core histone acetylation dramatically enhances transcription of nucleosomal arrays by RNA polymerase III Mol. Cell. Biol. 18 1998 4629 4638
83. A. Allahverdi, R.L. Yang, N. Korolev, Y.P. Fan, C.A. Davey, C.F. Liu, and L. Nordenskiold The effects of histone H4 tail acetylations on cation-induced chromatin folding and self-association Nucleic Acids Res. 39 2011 1680 1691
84. P.J. Robinson, W. An, A. Routh, F. Martino, L. Chapman, R.G. Roeder, and D. Rhodes 30 nm chromatin fibre decompaction requires both H4-K16 acetylation and linker histone eviction J. Mol. Biol. 381 2008 816 825
85. M. Shogren-Knaak, H. Ishii, J.M. Sun, M.J. Pazin, J.R. Davie, and C.L. Peterson Histone H4-K16 acetylation controls chromatin structure and protein interactions Science 311 2006 844 847
86. X.Y. Wang, C. He, S.C. Moore, and J. Ausio Effects of histone acetylation on the solubility and folding of the chromatin fiber J. Biol. Chem. 276 2001 12764 12768
87. J.Y. Fan, D. Rangasamy, K. Luger, and D.J. Tremethick H2A.Z alters the nucleosome surface to promote HP1alpha-mediated chromatin fiber folding Mol. Cell 16 2004 655 661
88. J.Y. Fan, F. Gordon, K. Luger, J.C. Hansen, and D.J. Tremethick The essential histone variant H2A.Z regulates the equilibrium between different chromatin conformational states Nat. Struct. Biol. 9 2002 172 176
89. P. Chen, J.C. Zhao, Y. Wang, M. Wang, H.Z. Long, D. Liang, L. Huang, Z.Q. Wen, W. Li, X. Li, H.L. Feng, H.Y. Zhao, P. Zhu, M. Li, Q.F. Wang, and G.H. Li H3.3 actively marks enhancers and primes gene transcription via opening higher-ordered chromatin Gene Dev. 27 2013 2109 2124
90. J. Zhou, J.Y. Fan, D. Rangasamy, and D.J. Tremethick The nucleosome surface regulates chromatin compaction and couples it with transcriptional repression Nat. Struct. Mol. Biol. 14 2007 1070 1076
91. C. Vogler, C. Huber, T. Waldmann, R. Ettig, L. Braun, A. Izzo, S. Daujat, I. Chassignet, A.J. Lopez-Contreras, O. Fernandez-Capetillo, M. Dundr, K. Rippe, G. Langst, and R. Schneider Histone H2A C-terminus regulates chromatin dynamics, remodeling, and histone H1 binding PLoS Genet. 6 2010
92. S.I. Usachenko, S.G. Bavykin, I.M. Gavin, and E.M. Bradbury Rearrangement of the histone H2a C-terminal domain in the nucleosome Proc. Natl. Acad. Sci. U.S.A. 91 1994 6845 6849
93. M.A. Christophorou, G. Castelo-Branco, R.P. Halley-Stott, C.S. Oliveira, R. Loos, A. Radzisheuskaya, K.A. Mowen, P. Bertone, J.C.R. Silva, M. Zernicka-Goetz, M.L. Nielsen, J.B. Gurdon, and T. Kouzarides Citrullination regulates pluripotency and histone H1 binding to chromatin Nature 507 2014 104 108
94. A. Roque, I. Ponte, and P. Suau Role of charge neutralization in the folding of the carboxy-terminal domain of histone H1 J. Phys. Chem. B 113 2009 12061 12066
95. A. Roque, I. Ponte, J.L. Arrondo, and P. Suau Phosphorylation of the carboxy-terminal domain of histone H1: effects on secondary structure and DNA condensation Nucleic Acids Res. 36 2008 4719 4726
96. S.P. Hergeth, M. Dundr, P. Tropberger, B.M. Zee, B.A. Garcia, S. Daujat, and R. Schneider Isoform-specific phosphorylation of human linker histone H1.4 in mitosis by the kinase Aurora B J. Cell Sci. 124 2011 1623 1628
97. H. Kato, H. van Ingen, B.R. Zhou, H.Q. Feng, M. Bustin, L.E. Kay, and Y.W. Bai Architecture of the high mobility group nucleosomal protein 2-nucleosome complex as revealed by methyl-based NMR Proc. Natl. Acad. Sci. U.S.A. 108 2011 12283 12288
98. A.J. Barbera, J.V. Chodaparambil, B. Kelley-Clarke, V. Joukov, J.C. Walter, K. Luger, and K.M. Kaye The nucleosomal surface as a docking station for Kaposi's sarcoma herpesvirus LANA Science 311 2006 856 861
99. J.V. Chodaparambil, A.J. Barbera, X. Lu, K.M. Kaye, J.C. Hansen, and K. Luger A charged and contoured surface on the nucleosome regulates chromatin compaction Nat. Struct. Mol. Biol. 14 2007 1105 1107
100. K.J. Armache, J.D. Garlick, D. Canzio, G.J. Narlikar, and R.E. Kingston Structural basis of silencing: Sir3 BAH domain in complex with a nucleosome at 3.0 angstrom resolution Science 334 2011 977 982
101. R.D. Makde, J.R. England, H.P. Yennawar, and S. Tan Structure of RCC1 chromatin factor bound to the nucleosome core particle Nature 467 2010 U562 U581
102. D.X. Yang, Q.L. Fang, M.Z. Wang, R. Ren, H. Wang, M. He, Y.W. Sun, N. Yang, and R.M. Xu N alpha-acetylated Sir3 stabilizes the conformation of a nucleosome-binding loop in the BAH domain Nat. Struct. Mol. Biol. 20 2013 1116 1118
103. N.J. Francis, R.E. Kingston, and C.L. Woodcock Chromatin compaction by a polycomb group protein complex Science 306 2004 1574 1577
104. R. Margueron, G.H. Li, K. Sarma, A. Blais, J. Zavadil, C.L. Woodcock, B.D. Dyniacht, and D. Reinberg Ezh1 and Ezh2 maintain repressive chromatin through different mechanisms Mol. Cell 32 2008 503 518
105. S.A. Grigoryev, J. Bednar, and C.L. Woodcock MENT, a heterochromatin protein that mediates higher order chromatin folding, is a new serpin family member J. Biol. Chem. 274 1999 5626 5636
106. P.T. Georgel, R.A. Horowitz-Scherer, N. Adkins, C.L. Woodcock, P.A. Wade, and J.C. Hansen Chromatin compaction by human MeCP2 - assembly of novel secondary chromatin structures in the absence of DNA methylation J. Biol. Chem. 278 2003 32181 32188
107. P. Trojer, G. Li, R.J. Sims, A. Vaquero, N. Kalakonda, P. Boccuni, D. Lee, H. Erdjument-Bromage, P. Tempst, S.D. Nimer, Y.H. Wang, and D. Reinberg L3MBTL1, a histone-methylation-dependent chromatin lock Cell 129 2007 915 928
108. A.M. Azzaz, M.W. Vitalini, A.S. Thomas, J.P. Price, M.J. Blacketer, D.E. Cryderman, L.N. Zirbel, C.L. Woodcock, A.H. Elcock, L.L. Wallrath, and M.A. Shogren-Knaak Human heterochromatin protein 1 alpha promotes nucleosome associations that drive chromatin condensation J. Biol. Chem. 289 2014 6850 6861
109. D. Canzio, E.Y. Chang, S. Shankar, K.M. Kuchenbecker, M.D. Simon, H.D. Madhani, G.J. Narlikar, and B. Al-Sady Chromodomain-mediated oligomerization of HP1 suggests a nucleosome-bridging mechanism for heterochromatin assembly Mol. Cell 41 2011 67 81
110. B. Yu, M. Cassani, M. Wang, M. Liu, J. Ma, G. Li, Z. Zhang, and Y. Huang Structural insights into Rhino-mediated germline piRNA cluster formation Cell Res. 25 2015 525 528
111. W. Liu, B. Tanasa, O.V. Tyurina, T.Y. Zhou, R. Gassmann, W.T. Liu, K.A. Ohgi, C. Benner, I. Garcia-Bassets, A.K. Aggarwal, A. Desai, P.C. Dorrestein, C.K. Glass, and M.G. Rosenfeld PHF8 mediates histone H4 lysine 20 demethylation events involved in cell cycle progression Nature 466 2010 508 512
112. M. Eltsov, K.M. MacLellan, K. Maeshima, A.S. Frangakis, and J. Dubochet Analysis of cryo-electron microscopy images does not support the existence of 30-nm chromatin fibers in mitotic chromosomes in situ Proc. Natl. Acad. Sci. U.S.A. 105 2008 19732 19737
113. E. Fussner, R.W. Ching, and D.P. Bazett-Jones Living without 30 nm chromatin fibers Trends Biochem. Sci. 36 2011 1 6
114. C.L. Woodcock Chromatin fibers observed in-situ in frozen-hydrated sections - native fiber diameter is not correlated with nucleosome repeat length J. Cell Biol. 125 1994 11 19
115. R.A. Horowitz, D.A. Agard, J.W. Sedat, and C.L. Woodcock The 3-dimensional architecture of chromatin in-situ - electron tomography reveals fibers composed of a continuously variable zigzag nucleosomal ribbon J. Cell Biol. 125 1994 1 10
116. R.A. Horowitz, A.J. Koster, J. Walz, and C.L. Woodcock Automated electron microscope tomography of frozen-hydrated chromatin: the irregular three-dimensional zigzag architecture persists in compact, isolated fibers J. Struct. Biol. 120 1997 353 362
117. M.P. Scheffer, M. Eltsov, J. Bednar, and A.S. Frangakis Nucleosomes stacked with aligned dyad axes are found in native compact chromatin in vitro J. Struct. Biol. 178 2012 207 214
118. J.P. Langmore, and J.R. Paulson Low-angle X-ray-diffraction studies of chromatin structure invivo and in isolated-nuclei and metaphase chromosomes J. Cell Biol. 96 1983 1120 1131
119. C. Kizilyaprak, D. Spehner, D. Devys, and P. Schultz In vivo chromatin organization of mouse rod photoreceptors correlates with histone modifications PLoS ONE 5 2010
120. J. Bordas, L. Perez-Grau, M.H. Koch, M.C. Vega, and C. Nave The superstructure of chromatin and its condensation mechanism. I. Synchrotron radiation X-ray scattering results Eur. Biophys. J. 13 1986 157 173
121. M.F. Smith, B.D. Athey, S.P. Williams, and J.P. Langmore Radial density distribution of chromatin: evidence that chromatin fibers have solid centers J. Cell Biol. 110 1990 245 254
122. V. Graziano, S.E. Gerchman, D.K. Schneider, and V. Ramakrishnan Histone H1 is located in the interior of the chromatin 30-nm filament Nature 368 1994 351 354
123. R.J. Arceci, and P.R. Gross Sea urchin sperm chromatin structure as probed by pancreatic DNase I: evidence for a noval cutting periodicity Dev. Biol. 80 1980 210 224
124. A.T. Khachatrian, V.A. Pospelov, S.B. Svetlikova, and V.I. Vorob'ev Nucleodisome - a new repeat unit of chromatin revealed in nuclei of pigeon erythrocytes by DNase I digestion FEBS Lett. 128 1981 90 92
125. L.A. Burgoyne, and J.D. Skinner Chromatin superstructure: the next level of structure above the nucleosome has an alternating character. A two-nucleosome based series is generated by probes armed with DNAase-I acting on isolated nuclei Biochem. Biophys. Res. Commun. 99 1981 893 899
126. K. Maeshima, R. Imai, S. Tamura, and T. Nozaki Chromatin as dynamic 10-nm fibers Chromosoma 123 2014 225 237
127. E. Fussner, U. Djuric, M. Strauss, A. Hotta, C. Perez-Iratxeta, F. Lanner, F.J. Dilworth, J. Ellis, and D.P. Bazett-Jones Constitutive heterochromatin reorganization during somatic cell reprogramming EMBO J. 30 2011 1778 1789
128. Y. Nishino, M. Eltsov, Y. Joti, K. Ito, H. Takata, Y. Takahashi, S. Hihara, A.S. Frangakis, N. Imamoto, T. Ishikawa, and K. Maeshima Human mitotic chromosomes consist predominantly of irregularly folded nucleosome fibres without a 30-nm chromatin structure EMBO J. 31 2012 1644 1653
129. K. Maeshima, R. Imai, T. Hikima, and Y. Joti Chromatin structure revealed by X-ray scattering analysis and computational modeling Methods 70 2014 154 161
130. L. Gan, M.S. Ladinsky, and G.J. Jensen Chromatin in a marine picoeukaryote is a disordered assemblage of nucleosomes Chromosoma 122 2013 377 386
131. D.P. Bazett-Jones, R. Li, E. Fussner, R. Nisman, and H. Dehghani Elucidating chromatin and nuclear domain architecture with electron spectroscopic imaging Chromosome Res. 16 2008 397 412
132. E. Fussner, M. Strauss, U. Djuric, R. Li, K. Ahmed, M. Hart, J. Ellis, and D.P. Bazett-Jones Open and closed domains in the mouse genome are configured as 10-nm chromatin fibres EMBO Rep. 13 2012 992 996
133. X.C. Bai, G. McMullan, and S.H. Scheres How cryo-EM is revolutionizing structural biology Trends Biochem. Sci. 40 2015 49 57
134. Y. Cui, and C. Bustamante Pulling a single chromatin fiber reveals the forces that maintain its higher-order structure Proc. Natl. Acad. Sci. U.S.A. 97 2000 127 132
135. E.A. Smith, G. McDermott, M. Do, K. Leung, B. Panning, M.A. Le Gros, and C.A. Larabell Quantitatively imaging chromosomes by correlated cryo-fluorescence and soft X-ray tomographies Biophys. J. 107 2014 1988 1996