A brief review of nucleosome structure

FEBS Letters

Volumn 589, Issue 20, 2015, Pages 2914-2922

  Cutter, Amber R ^a   Hayes, Jeffrey J ^a  

^a UNIVERSITY OF ROCHESTER MEDICAL CENTER   (United States)

Author keywords

Chromatin structure; Histone; Nucleosome structure

Indexed keywords

DNA; HISTONE; HISTONE H1; NUCLEOSOME;

AMINO TERMINAL SEQUENCE; CARBOXY TERMINAL SEQUENCE; CELL FUNCTION; CELL INTERACTION; CELL STRUCTURE; CHROMATIN STRUCTURE; DNA DAMAGE; DNA HISTONE INTERACTION; DNA REPAIR; DNA REPLICATION; DNA SEQUENCE; DNA TRANSCRIPTION; MOLECULAR RECOGNITION; NONHUMAN; NUCLEOSOME; PRIORITY JOURNAL; PROTEIN ASSEMBLY; PROTEIN DOMAIN; PROTEIN FUNCTION; REVIEW; SIGNAL TRANSDUCTION; ANIMAL; CHEMICAL STRUCTURE; CHEMISTRY; CHROMATIN ASSEMBLY AND DISASSEMBLY; CONFORMATION; GENETICS; HUMAN; PHYSIOLOGY; PROTEIN QUATERNARY STRUCTURE; PROTEIN TERTIARY STRUCTURE; ULTRASTRUCTURE;

ANIMALS; CHROMATIN ASSEMBLY AND DISASSEMBLY; DNA; DNA REPAIR; DNA REPLICATION; HISTONES; HUMANS; MODELS, MOLECULAR; NUCLEIC ACID CONFORMATION; NUCLEOSOMES; PROTEIN STRUCTURE, QUATERNARY; PROTEIN STRUCTURE, TERTIARY;

EID: 84944358170     PISSN: 00145793     EISSN: 18733468     Source Type: Journal    
DOI: 10.1016/j.febslet.2015.05.016     Document Type: Review

References (119)

1. 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 A resolution Nature 389 1997 251 260
2. C.L. White, R.K. Suto, and K. Luger Structure of the yeast nucleosome core particle reveals fundamental changes in internucleosome interactions EMBO J. 20 2001 5207 5218
3. T.J. Richmond, J.T. Finch, B. Rushton, D. Rhodes, and A. Klug Structure of the nucleosome core particle at 7 A resolution Nature 311 1984 532 537
4. K.E. van Holde Chromatin 1989 Springer Verlag New York
5. G. Arents, R.W. Burlingame, B.C. Wang, W.E. Love, and E.N. Moudrianakis The nucleosomal core histone octamer at 3.1 A resolution: a tripartite protein assembly and a left-handed superhelix Proc. Natl. Acad. Sci. U.S.A. 88 1991 10148 10152
6. G. Arents, and E.N. Moudrianakis Topography of the histone octamer surface: repeating structural motifs utilized in the docking of nucleosomal DNA Proc. Natl. Acad. Sci. U.S.A. 90 1993 10489 10493
7. V. Karantza, E. Freire, and E.N. Moudrianakis Thermodynamic studies of the core histones: pH and ionic strength effects on the stability of the (H3-H4)/(H3-H4)2 system Biochemistry 35 1996 2037 2046
8. D.D. Banks, and L.M. Gloss Folding mechanism of the (H3-H4)2 histone tetramer of the core nucleosome Protein Sci. 13 2004 1304 1316
9. L.M. Gloss, and B.J. Placek The effect of salts on the stability of the H2A-H2B histone dimer Biochemistry 41 2002 14951 14959
10. A.D. Baxevanis, G. Arents, E.N. Moudrianakis, and D. Landsman A variety of DNA-binding and multimeric proteins contain the histone fold motif Nucleic Acids Res. 23 1995 2685 2691
11. T. Nikitina, D. Wang, M. Gomberg, S.A. Grigoryev, and V.B. Zhurkin Combined micrococcal nuclease and exonuclease III digestion reveals precise positions of the nucleosome core/linker junctions: implications for high-resolution nucleosome mapping J. Mol. Biol. 425 2013 1946 1960
12. T.J. Richmond, and C.A. Davey The structure of DNA in the nucleosome core Nature 423 2003 145 150
13. M.Y. Tolstorukov, A.V. Colasanti, D.M. McCandlish, W.K. Olson, and V.B. Zhurkin A novel roll-and-slide mechanism of DNA folding in chromatin: implications for nucleosome positioning J. Mol. Biol. 371 2007 725 738
14. J.J. Hayes, J. Bashkin, T.D. Tullius, and A.P. Wolffe The histone core exerts a dominant constraint on the structure of DNA in a nucleosome Biochemistry 30 1991 8434 8440
15. Y. Bao, C.L. White, and K. Luger Nucleosome core particles containing a poly(dA.dT) sequence element exhibit a locally distorted DNA structure J. Mol. Biol. 361 2006 617 624
16. K. Struhl, and E. Segal Determinants of nucleosome positioning Nat. Struct. Mol. Biol. 20 2013 267 273
17. J.J. Hayes, D.J. Clark, and A.P. Wolffe Histone contributions to the structure of DNA in the nucleosome Proc. Natl. Acad. Sci. U.S.A. 88 1991 6829 6833
18. J.J. Hayes, T.D. Tullius, and A.P. Wolffe The structure of DNA in a nucleosome Proc. Natl. Acad. Sci. U.S.A. 87 1990 7405 7409
19. A.A. Travers, and A. Klug The bending of DNA in nucleosomes and its wider implications Philos. Trans. R. Soc. Lond. B Biol. Sci. 317 1987 537 561
20. 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 a resolution J. Mol. Biol. 319 2002 1097 1113
21. R.S. Edayathumangalam, P. Weyermann, P.B. Dervan, J.M. Gottesfeld, and K. Luger Nucleosomes in solution exist as a mixture of twist-defect states J. Mol. Biol. 345 2005 103 114
22. J.D. McGhee, and G. Felsenfeld The number of charge-charge interactions stabilizing the ends of nucleosome DNA Nucleic Acids Res. 8 1980 2751 2769
23. D. Wang, N.B. Ulyanov, and V.B. Zhurkin Sequence-dependent Kink-and-Slide deformations of nucleosomal DNA facilitated by histone arginines bound in the minor groove J. Biomol. Struct. Dyn. 27 2010 843 859
24. H. Neumann, and et al. A method for genetically installing site-specific acetylation in recombinant histones defines the effects of H3 K56 acetylation Mol. Cell 36 2009 153 163
25. L. Bohm, and C. Crane-Robinson Proteases as structural probes for chromatin: the domain structure of histones Biosci. Rep. 4 1984 365 386
26. I.O. Walker Differential dissociation of histone tails from core chromatin Biochemistry 23 1984 5622 5628
27. R.M. Smith, and R.L. Rill Mobile histone tails in nucleosomes. Assignments of mobile segments and investigations of their role in chromatin folding J. Biol. Chem. 264 1989 10574 10581
28. J.C. Hansen, X. Lu, E.D. Ross, and R.W. Woody Intrinsic protein disorder, amino acid composition, and histone terminal domains J. Biol. Chem. 281 2006 1853 1856
29. X. Wang, and J.J. Hayes Site-specific binding affinities within the H2B tail domain indicate specific effects of lysine acetylation J. Biol. Chem. 282 2007 32867 32876
30. J. Ausio, F. Dong, and K.E. van Holde Use of selectively trypsinized nucleosome core particles to analyze the role of the histone "tails" in the stabilization of the nucleosome J. Mol. Biol. 206 1989 451 463
31. D.Y. Lee, J.J. Hayes, D. Pruss, and A.P. Wolffe A positive role for histone acetylation in transcription factor access to nucleosomal DNA Cell 72 1993 73 84
32. K.J. Polach, P.T. Lowary, and J. Widom Effects of core histone tail domains on the equilibrium constants for dynamic DNA site accessibility in nucleosomes J. Mol. Biol. 298 2000 211 233
33. M. Vettese-Dadey, P. Walter, H. Chen, L.J. Juan, and J.L. Workman Role of the histone amino termini in facilitated binding of a transcription factor, GAL4-AH, to nucleosome cores Mol. Cell. Biol. 14 1994 970 981
34. P.P. Walter, T.A. Owen-Hughes, J. Cote, and J.L. Workman Stimulation of transcription factor binding and histone displacement by nucleosome assembly protein 1 and nucleoplasmin requires disruption of the histone octamer Mol. Cell. Biol. 15 1995 6178 6187
35. Z. Yang, C. Zheng, C. Thiriet, and J.J. Hayes The core histone N-terminal tail domains negatively regulate binding of transcription factor IIIA to a nucleosome containing a 5S RNA gene via a novel mechanism Mol. Cell. Biol. 25 2005 241 249
36. K.M. Lee, and J.J. Hayes The N-terminal tail of histone H2A binds to two distinct sites within the nucleosome core Proc. Natl. Acad. Sci. U.S.A. 94 1997 8959 8964
37. K.M. Lee, and J.J. Hayes Linker DNA and H1-dependent reorganization of histone-DNA interactions within the nucleosome Biochemistry 37 1998 8622 8628
38. X. Wang, S.C. Moore, M. Laszckzak, and J. Ausio Acetylation increases the alpha-helical content of the histone tails of the nucleosome J. Biol. Chem. 275 2000 35013 35020
39. J. Allan, N. Harborne, D.C. Rau, and H. Gould Participation of the core histone tails in the stabilization of the chromatin solenoid J. Cell Biol. 93 1982 285 297
40. P.M. Schwarz, and J.C. Hansen Formation and stability of higher order chromatin structures. Contributions of the histone octamer J. Biol. Chem. 269 1994 16284 16289
41. M. Garcia-Ramirez, C. Rocchini, and J. Ausio Modulation of chromatin folding by histone acetylation J. Biol. Chem. 270 1995 17923 17928
42. C. Zheng, and J.J. Hayes Structures and interactions of the core histone tail domains Biopolymers 68 2003 539 546
43. B. Dorigo, T. Schalch, K. Bystricky, and T.J. Richmond Chromatin fiber folding: requirement for the histone H4 N-terminal tail J. Mol. Biol. 327 2003 85 96
44. 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
45. B.J. Wilkins, and et al. A cascade of histone modifications induces chromatin condensation in mitosis Science 343 2014 77 80
46. C. Zheng, X. Lu, J.C. Hansen, and J.J. Hayes Salt-dependent intra- and internucleosomal interactions of the H3 tail domain in a model oligonucleosomal array J. Biol. Chem. 280 2005 33552 33557
47. J.C. Hansen Conformational dynamics of the chromatin fiber in solution: determinants, mechanisms, and functions Annu. Rev. Biophys. Biomol. Struct. 31 2002 361 392
48. P.Y. Kan, T.L. Caterino, and J.J. Hayes The H4 tail domain participates in intra- and internucleosome interactions with protein and DNA during folding and oligomerization of nucleosome arrays Mol. Cell. Biol. 29 2009 538 546
49. S. Pepenella, K.J. Murphy, and J.J. Hayes A distinct switch in interactions of the histone H4 tail domain upon salt-dependent folding of nucleosome arrays J. Biol. Chem. 289 2014 27342 27351
50. T. Jenuwein, and C.D. Allis Translating the histone code Science 293 2001 1074 1080
51. K. Luger, and J.C. Hansen Nucleosome and chromatin fiber dynamics Curr. Opin. Struct. Biol. 15 2005 188 196
52. 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
53. D. Sinha, and M.A. Shogren-Knaak Role of direct interactions between the histone H4 Tail and the H2A core in long range nucleosome contacts J. Biol. Chem. 285 2010 16572 16581
54. A. Allahverdi, R. Yang, N. Korolev, Y. 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
55. T.M. Fletcher, and J.C. Hansen Core histone tail domains mediate oligonucleosome folding and nucleosomal DNA organization through distinct molecular mechanisms J. Biol. Chem. 270 1995 25359 25362
56. 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
57. K.J. Polach, and J. Widom Mechanism of protein access to specific DNA sequences in chromatin: a dynamic equilibrium model for gene regulation J. Mol. Biol. 254 1995 130 149
58. J.D. Anderson, and J. Widom Sequence and position-dependence of the equilibrium accessibility of nucleosomal DNA target sites J. Mol. Biol. 296 2000 979 987
59. T.T. Ngo, Q. Zhang, R. Zhou, J.G. Yodh, and T. Ha Asymmetric unwrapping of nucleosomes under tension directed by DNA local flexibility Cell 160 2015 1135 1144
60. M.G. Poirier, M. Bussiek, J. Langowski, and J. Widom Spontaneous access to DNA target sites in folded chromatin fibers J. Mol. Biol. 379 2008 772 786
61. A. Hamiche, V. Carot, M. Alilat, F. De Lucia, M.F. O'Donohue, B. Revet, and A. Prunell Interaction of the histone (H3-H4)2 tetramer of the nucleosome with positively supercoiled DNA minicircles: Potential flipping of the protein from a left- to a right-handed superhelical form Proc. Natl. Acad. Sci. U.S.A. 93 1996 7588 7593
62. A. Sivolob, F. De Lucia, M. Alilat, and A. Prunell Nucleosome dynamics. VI. Histone tail regulation of tetrasome chiral transition. A relaxation study of tetrasomes on DNA minicircles J. Mol. Biol. 295 2000 55 69
63. S. Peterson, and V. Jackson Acetylation of H4 suppresses the repressive effects of the N-termini of histones H3/H4 and facilitates the formation of positively coiled DNA Biochemistry 47 2008 7053 7065
64. R.H. White, M. Keberlein, and V. Jackson A mutational mimic analysis of histone H3 post-translational modifications: specific sites influence the conformational state of H3/H4, causing either positive or negative supercoiling of DNA Biochemistry 51 2012 8173 8188
65. V. Levchenko, B. Jackson, and V. Jackson Histone release during transcription: displacement of the two H2A-H2B dimers in the nucleosome is dependent on different levels of transcription-induced positive stress Biochemistry 44 2005 5357 5372
66. A. Bancaud, and et al. Nucleosome chiral transition under positive torsional stress in single chromatin fibers Mol. Cell 27 2007 135 147
67. M.Y. Sheinin, M. Li, M. Soltani, K. Luger, and M.D. Wang Torque modulates nucleosome stability and facilitates H2A/H2B dimer loss Nat. Commun. 4 2013 2579
68. V. Bohm, A.R. Hieb, A.J. Andrews, A. Gansen, A. Rocker, K. Toth, K. Luger, and J. Langowski Nucleosome accessibility governed by the dimer/tetramer interface Nucleic Acids Res. 39 2011 3093 3102
69. T.T. Ngo, and T. Ha Nucleosomes undergo slow spontaneous gaping Nucleic Acids Res. 2015 Advance Access published March 30, 2015 online
70. 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
71. J. Allan, T. Mitchell, N. Harborne, L. Bohm, and C. Crane-Robinson Roles of H1 domains in determining higher order chromatin structure and H1 location J. Mol. Biol. 187 1986 591 601
72. T.A. Blank, and P.B. Becker Electrostatic mechanism of nucleosome spacing J. Mol. Biol. 252 1995 305 313
73. Y. Fan, T. Nikitina, E.M. Morin-Kensicki, J. Zhao, T.R. Magnuson, C.L. Woodcock, and A.I. Skoultchi H1 linker histones are essential for mouse development and affect nucleosome spacing in vivo Mol. Cell. Biol. 23 2003 4559 4572
74. X. Shen, and M.A. Gorovsky Linker histone H1 regulates specific gene expression but not global transcription in vivo Cell 86 1996 475 483
75. Y. Fan, and et al. Histone H1 depletion in mammals alters global chromatin structure but causes specific changes in gene regulation Cell 123 2005 1199 1212
76. X. Lu, and et al. Drosophila H1 regulates the genetic activity of heterochromatin by recruitment of Su(var)3-9 Science 340 2013 78 81
77. S.Y. Roth, and C.D. Allis Chromatin condensation: does histone H1 dephosphorylation play a role? Trends Biochem. Sci. 17 1992 93 98
78. C. Thiriet, and J.J. Hayes Linker histone phosphorylation regulates global timing of replication origin firing J. Biol. Chem. 284 2009 2823 2829
79. N. Raghuram, and et al. Pin1 promotes histone H1 dephosphorylation and stabilizes its binding to chromatin J. Cell Biol. 203 2013 57 71
80. T. Misteli, A. Gunjan, R. Hock, M. Bustin, and D.T. Brown Dynamic binding of histone H1 to chromatin in living cells Nature 408 2000 877 881
81. J. Allan, P.G. Hartman, C. Crane-Robinson, and F.X. Aviles The structure of histone H1 and its location in chromatin Nature 288 1980 675 679
82. D. Landsman Histone H1 in Saccharomyces cerevisiae: a double mystery solved? Trends Biochem. Sci. 21 1996 287 288
83. T. Hayashi, H. Hayashi, and K. Iwai Tetrahymena histone H1. Isolation and amino acid sequence lacking the central hydrophobic domain conserved in other H1 histones J. Biochem. 102 1987 369 376
84. M. Wu, C.D. Allis, R. Richman, R.G. Cook, and M.A. Gorovsky An intervening sequence in an unusual histone H1 gene of Tetrahymena thermophila Proc. Natl. Acad. Sci. U.S.A. 83 1986 8674 8678
85. N. Happel, and D. Doenecke Histone H1 and its isoforms: contribution to chromatin structure and function Gene 431 2009 1 12
86. J.P. Whitlock Jr., and R.T. Simpson Removal of histone H1 exposes a fifty base pair DNA segment between nucleosomes Biochemistry 15 1976 3307 3314
87. R.T. Simpson Structure of the chromosome, a chromatin particle containing 160 base pairs of DNA and all the histones Biochemistry 17 1978 5524 5531
88. 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
89. D.L. Bates, and J.O. Thomas Histones H1 and H5: one or two molecules per nucleosome? Nucleic Acids Res. 2 1981 5883 5894
90. C. Cerf, G. Lippens, S. Muyldermans, A. Segers, V. Ramakrishnan, S.J. Wodak, K. Hallenga, and L. Wyns Homo- and heteronuclear two-dimensional NMR studies of the globular domain of histone H1: sequential assignment and secondary structure Biochemistry 32 1993 11345 11351
91. 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 219 224
92. C. Cerf, G. Lippens, V. Ramakrishnan, S. Muyldermans, A. Segers, L. Wyns, S.J. Wodak, and K. Hallenga Homo- and heteronuclear two-dimensional NMR studies of the globular domain of histone H1: full assignment, tertiary structure, and comparison with the globular domain of histone H5 Biochemistry 33 1994 11079 11086
93. L. Bohm, and T.C. Mitchell Sequence conservation in the N-terminal domain of histone H1 FEBS Lett. 193 1985 1 4
94. P. Vyas, and D.T. Brown N- and C-terminal domains determine differential nucleosomal binding geometry and affinity of linker histone isotypes H1(0) and H1c J. Biol. Chem. 287 2012 11778 11787
95. T.L. Caterino, and J.J. Hayes Structure of the H1 C-terminal domain and function in chromatin condensation Biochem. Cell Biol. 89 2011 35 44
96. J.A. Subirana Analysis of the charge distribution in the C-terminal region of histone H1 as related to its interaction with DNA Biopolymers 29 1990 1351 1357
97. D.J. Clark, and T. Kimura Electrostatic mechanism of chromatin folding J. Mol. Biol. 211 1990 883 896
98. 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 Biochemistry 37 1998 14776 14787
99. M.J. Hendzel, M.A. Lever, E. Crawford, and J.P. Th'ng The C-terminal domain is the primary determinant of histone H1 binding to chromatin in vivo J. Biol. Chem. 279 2004 20028 20034
100. E.M. Bradbury, and et al. Studies on the role and mode of operation of the very-lysine-rich histone H1 (F1) in eukaryote chromatin. The conformation of histone H1 Eur. J. Biochem. 52 1975 605 613
101. X. Lu, B. Hamkalo, M.H. Parseghian, and J.C. Hansen Chromatin condensing functions of the linker histone C-terminal domain are mediated by specific amino acid composition and intrinsic protein disorder Biochemistry 48 2009 164 172
102. X. Lu, and J.C. Hansen Identification of specific functional subdomains within the linker histone H10 C-terminal domain J. Biol. Chem. 279 2004 8701 8707
103. A.A. Kalashnikova, and et al. Linker histone H1.0 interacts with an extensive network of proteins found in the nucleolus Nucleic Acids Res. 41 2013 4026 4035
104. H.J. Szerlong, J.A. Herman, C.M. Krause, J.G. DeLuca, A. Skoultchi, Q.A. Winger, J.E. Prenni, and J.C. Hansen Proteomic characterization of the nucleolar linker histone H1 interaction network J. Mol. Biol. 2015
105. D.J. Clark, C.S. Hill, S.R. Martin, and J.O. Thomas Alpha-helix in the carboxy-terminal domains of histones H1 and H5 EMBO J. 7 1988 69 75
106. A. Roque, I. Iloro, I. Ponte, J.L. Arrondo, and P. Suau DNA-induced secondary structure of the carboxyl-terminal domain of histone H1 J. Biol. Chem. 280 2005 32141 32147
107. R. Vila, I. Ponte, M. Collado, J.L. Arrondo, and P. Suau Induction of secondary structure in a COOH-terminal peptide of histone H1 by interaction with the DNA: an infrared spectroscopy study J. Biol. Chem. 276 2001 30898 30903
108. T.L. Caterino, H. Fang, and J.J. Hayes Nucleosome linker DNA contacts and induces specific folding of the intrinsically disordered h1 carboxyl-terminal domain Mol. Cell. Biol. 31 2011 2341 2348
109. H. Fang, D.J. Clark, and J.J. Hayes DNA and nucleosomes direct distinct folding of a linker histone H1 C-terminal domain Nucleic Acids Res. 40 2011 1475 1484
110. D.Z. Staynov, and C. Crane-Robinson Footprinting of linker histones H5 and H1 on the nucleosome EMBO J. 7 1988 3685 3691
111. C. Crane-Robinson Where is the globular domain of linker histone located on the nucleosome? Trends Biochem. Sci. 22 1997 75 77
112. 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 Nat. Struct. Mol. Biol. 13 2006 250 255
113. 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
114. J.J. Hayes Site-directed cleavage of DNA by a linker histone-Fe(II) EDTA conjugate: localization of a globular domain binding site within a nucleosome Biochemistry 35 1996 11931 11937
115. 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
116. 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
117. S.H. Syed, and et al. 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
118. B.R. Zhou, H. Feng, H. Kato, L. Dai, Y. Yang, Y. Zhou, and Y. Bai Structural insights into the histone H1-nucleosome complex Proc. Natl. Acad. Sci. U.S.A. 110 2013 19390 19395
119. E.M. George, T. Izard, S.D. Anderson, and D.T. Brown Nucleosome interaction surface of linker histone H1c is distinct from that of H1(0) J. Biol. Chem. 285 2010 20891 20896