Histone structure and the organization of the nucleosome

Annual Review of Biophysics and Biomolecular Structure

Volumn 26, Issue , 1997, Pages 83-112

  Ramakrishnan, V ^a  

^a UNIVERSITY OF UTAH SCHOOL OF MEDICINE   (United States)

Author keywords

Chromatin; Chromatosome; H1; H5; Histone fold

Indexed keywords

HISTONE; HISTONE H1; HISTONE H5; TRANSCRIPTION FACTOR;

ACETYLATION; CHROMATIN STRUCTURE; NUCLEOSOME; PRIORITY JOURNAL; PROTEIN DNA BINDING; PROTEIN DNA INTERACTION; PROTEIN DOMAIN; PROTEIN FAMILY; PROTEIN FOLDING; PROTEIN TERTIARY STRUCTURE; REVIEW;

AMINO ACID SEQUENCE; ANIMALS; HISTONES; MODELS, MOLECULAR; MOLECULAR SEQUENCE DATA; NUCLEOSOMES;

EID: 0030956032     PISSN: 10568700     EISSN: None     Source Type: Book Series    
DOI: 10.1146/annurev.biophys.26.1.83     Document Type: Review

References (138)

1. Allan J, Hartman PG, Crane-Robinson C, Aviles FX. 1980. The structure of histone H1 and its location in chromatin. Nature 288:675-79
2. Allan J, Mitchell T, Harborne N, Bohm L, Crane-Robinson C. 1986. Roles of H1 domains in determining higher order chromatin structure and H1 location. J. Mol. Biol. 187:591-601
3. Arents G, Burlingame RW, Wang BC, Love WE, Moudrianakis EN. 1991. The nucleosomal core histone octamer at 3.1 Å resolution: a tripartite protein assembly and a left-handed superhelix. Proc. Natl. Acad. Sci. USA 88:10148-52
4. Arents G, Moudrianakis EN. 1993. Topography of the histone octamer surface: repeating structural motifs utilized in the docking of nucleosomal DNA. Proc. Natl. Acad. Sci. USA 90:10489-93
5. Arents G, Moudrianakis EN. 1995. The histone fold: a ubiquitous architectural motif utilized in DNA compaction and protein dimerization. Proc. Natl. Acad. Sci. USA 92:11170-74
6. Aviles J, Chapman GE, Kneale GG, Crane-Robinson C, Bradbury EM. 1978. The conformation of histone H5. Eur. J. Biochem. 88:363-71
7. Bauer WR, Hayes JJ, White JH, Wolffe AP. 1994. Nucleosome structural changes due to acetylation. J. Mol. Biol. 236:685-90
8. Baxevanis AD, Arents G, Moudrianakis EN, Landsman D. 1995. A variety of DNA-binding and multimeric proteins contain the histone fold motif. Nucleic Acids Res. 23:2685-91
9. Bird A. 1995. Gene number, noise reduction and biological complexity. Trends Genet. 11:94-100
10. Boulikas T, Wiseman JM, Garrard WT. 1980. Points of contact between histone H1 and the histone octamer. Proc. Natl. Acad. Sci. USA 77:127-31
11. Bradbury EM. 1992. Reversible histone modifications and the chromosome cell cycle. BioEssays 14:9-16
12. Braunstein M, Rose AB, Holmes SG, Allis CD, Broach JR. 1993. Transcriptional silencing in yeast is associated with reduced nucleosome acetylation. Genes Dev. 7:592-604
13. Brennan RG. 1993. The winged-helix DNA-binding motif: another helix-turn-helix takeoff. Cell 74:773-76
14. Brownell JE, Zhou J, Ranalli T, Kobayashi R, Edmondson DG, et al. 1996. Tetrahymena histone acetyltransferase A: a homolog to yeast Gcn5p linking histone acetylation to gene activation. Cell 84:843-51
15. Burlingame RW, Love WE, Moudrianakis EN. 1984. Crystals of the octameric histone core of the nucleosome. Science 223:413-14
16. Burlingame RW, Love WE, Wang BC, Hamlin R, Xuong N-H, Moudrianakis EN. 1985. Crystallographic structure of the octameric histone core of the nucleosome at a resolution of 3.3 Å. Science 228:546-53
17. Cerf C, Lippens G, Ramakrishnan V, Muyldermans S, Segers A, et al. 1994. 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 33:11079-86
18. Churchill ME, Travers AA. 1991. Protein motifs that recognize structural features of DNA. Trends Biochem. Sci. 16:92-97
19. Churchill MEA, Suzuki M. 1989. 'SPKK' motifs prefer to bind to DNA at A/T rich sites. EMBO J. 8:4189-95
20. Clark DJ, Felsenfeld G. 1992. A nucleosome core is transferred out of the path of a transcribing polymerase. Cell 71:11-22
21. Clark DJ, Hill CS, Martin SR, Thomas JO. 1988. α-Helix in the carboxy-terminal domains of histones H1 and H5. EMBO J. 7:69-75
22. Clark KL, Halay DE, Lai E, Burley SK. 1993. Co-crystal structure of the HNF-3/fork head DNA-recognition motif resembles histone H5. Nature 364:412-20
23. Clore GM, Gronenborn AM, Nilges M, Sukumaran DK, Zarbock J. 1987. The polypeptide fold of the globular domain of H5 in solution. EMBO J. 6:1833-42
24. Cote J, Quin J, Workman JL, Peterson CL. 1994. Stimulation of GAL4 derivative binding to nucleosomal DNA by the yeast SWI/SNF complex. Science 265:53-60
25. Crane-Robinson C, Ptitsyn OB. 1989. Binding of the globular domain of linker histones H5/H1 to the nucleosome: a hypothesis. Protein Eng. 2:577-82
26. Croston GE, Kerrigan LA, Lira LM, Marshak DR, Kadonaga JT. 1991. Sequence-specific antirepression of histone H1-mediated inhibition of basal RNA polymerase II transcription. Science 251:643-49
27. Dong F, Hansen JC, van Holde KE. 1990. DNA and protein determinants of nucleosome positioning on sea urchin 5S rRNA gene sequences in vitro. Proc. Natl. Acad. Sci. USA 87:5724-28
28. 2 tetramer. Proc. Natl. Acad. Sci. USA 88:10596-600
29. Draves PH, Lowary PT, Widom J. 1992. Co-operative binding of the globular domain of histone H5 to DNA. J. Mol. Biol. 225:1105-21
30. Drew HR, Travers AA. 1985. DNA bending and its relation to nucleosome positioning. J. Mol. Biol. 186:773-90
31. Eickbush TH, Moudrianakis EN. 1978. The histone core complex: an octamer assembled by two sets of protein-protein interactions. Biochemistry 17:4955-64
32. Faus A, Luger K, Tan S, Richmond TJ. 1996. Mapping nucleosome position at single base-pair resolution by using site-directed hydroxyl radicals. Proc. Natl. Acad. Sci. USA 93:1370-75
33. Finch JT, Klug A. 1976. Solenoidal model for superstructure in chromatin. Proc. Natl. Acad. Sci. USA 73:1897-901
34. Frado LL, Mura CV, Stollar BD, Woodcock CL. 1983. Mapping of histone H5 sites on nucleosomes using immunoelectron microscopy. J. Biol. Chem. 258:11984-90
35. Fragoso G, John S, Roberts MS, Hager GL. 1995. Nucleosome positioning on the MMTV LTR results from the frequency-biased occupancy of multiple frames. Genes Dev. 9:1933-47
36. Goytisolo FA, Gerchman SE, Yu X, Rees C, Graziano V, et al. 1996. Identification of two DNA-binding sites on the globular domain of histone H5. EMBO J. 15:3421-29
37. Grayling RA, Becktel WJ, Reeve JN. 1995. Structure and stability of histone HMf from the hyperthermophilic archaeon Methanothermus fervidus. Biochemistry 34:8441-48
38. Grunstein M. 1990. Histone function in transcription. Annu. Rev. Cell Biol. 6:643-78
39. Grunstein M. 1990. Nucleosomes: regulators of transcription. Trends Genet. 6:395-400
40. 2 tetramer of the nucleosome under positive torsional stress. Proc. Natl. Acad. Sci. USA 93:7588-93
41. Hamiche A, Schultz P, Ramakrishnan V, Oudet P, Prunell A. 1996. Linker histone-dependent DNA structure in linear mononucleosomes. J. Mol. Biol. 257:30-42
42. Harp JM, Uberbacher E, Roberson A, Palmer EL, Gewiess A, Bunick GJ. 1995. X-ray diffraction analysis of crystals containing twofold symmetric nucleosome core particles. Acta Crystallogr. D52:283-88
43. Hartman PG, Chapman GE, Moss T, Bradbury EM. 1977. Studies on the role and mode of operation of the very-lysine rich histone H1 in eukaryote chromatin. Eur. J. Biochem. 77:45-51
44. Hayes JJ. 1996. Site-specific mapping of the linker histone binding site on the nucleosome core. Biochemistry. 35:11931-37
45. Hayes JJ, Bashkin J, Tullius TD, Wolffe AP. 1991. The histone core exerts a dominant constraint on the structure of DNA in a nucleosome. Biochemistry 30:8434-40
46. Hayes JJ, Clark DJ, Wolffe AP. 1991. Histone contributions to the structure of DNA in the nucleosome. Proc. Natl. Acad. Sci. USA 88:6829-33
47. Hayes JJ, Pruss D, Wolffe AP. 1994. Contacts of the globular domain of histone H5 and core histones with DNA in a chromatosome. Proc. Natl. Acad. Sci. USA 91:7817-21
48. Hayes JJ, Tullius TD, Wolffe AP. 1990. The structure of DNA in a nucleosome. Proc. Natl. Acad. Sci. USA 87:7405-9
49. Hayes JJ, Wolffe AP. 1992. Histones H2a/H2b inhibit the interactions of transcription factor IIIA with the Xenopus borealis somatic 5S RNA gene in a nucleosome. Proc. Natl. Acad. Sci. USA 89:1229-33
50. Hayes JJ, Wolffe AP. 1993. Preferential and asymmetric interaction of linker histones with 5S DNA in the nucleosome. Proc. Natl. Acad. Sci. USA 90:6415-19
51. Hecht A, Laroche T, Strahl-Bolsinger S, Gasser SM, Grunstein M. 1995. Histone H3 and H4 N-termini interact with SIR3 and SIR4 proteins: a molecular model for the formation of heterochromatin in yeast. Cell 80:583-92
52. Hoffmann A, Chiang CM, Oelgeschlager T, Xie X, Burley SK, et al. 1996. A histone octamer-like structure within TFIID. Nature 380:356-59
53. Imai BS, Yau P, Baldwin JP, Ibel K, May RP, Bradbury EM. 1986. Hyperacetylation of core histones does not cause unfolding of nucleosomes. Neutron scatter data accords with disc shape of the nucleosome. J. Biol. Chem. 261:8784-92
54. Imbalzano AN, Kwon H, Green MR, Kingston RE. 1994. Facilitated binding of TATA-binding protein to nucleosomal DNA. Nature 370:481-85
55. Johnson LM, Fisher-Adams G, Grunstein M. 1992. Identification of a non-basic domain in the histone H4 N-terminus required for repression of the yeast silent mating loci. EMBO J. 11:2201-9
56. Karantza V, Baxevanis AD, Freire E, Moudrianakis EN. 1995. Thermodynamic studies of the core histones: ionic strength and pH dependence of H2A-H2B dimer stability. Biochemistry 34:5988-96
57. Khochbin S, Wolffe AP. 1994. Developmentally regulated expression of linker-histone variants in vertebrates. Eur. J. Biochem. 225:501-10
58. Kingston RE, Bunker CA, Imbalzano AN. 1996. Repression and activation by multiprotein complexes that alter chromatin structure. Genes Dev. 10:905-20
59. Kleff S, Andrulis ED, Anderson CW, Sternglanz R. 1995. Identification of a gene encoding a yeast histone H4 acetyltransferase. J. Biol. Chem. 270:24674-77
60. Klug A, Finch JT, Richmond TJ. 1985. Scientific correspondence. Science 229:1109-10
61. Klug A, Rhodes D, Smith J, Finch JT, Thomas JO. 1980. A low resolution structure for the histone core of the nucleosome. Nature 287:509-16
62. Kornberg RD, Lorch Y. 1995. Interplay between chromatin structure and transcription. Curr. Opin. Cell Biol. 7:371-75
63. Krude T, Elgin SCR. 1996. Chromatin: Pushing nucleosomes around. Curr. Biol. 6:511-15
64. Krylov D, Leuba S, van Holde K, Zlatanova J. 1993. Histones H1 and H5 interact preferentially with crossovers of double-helical DNA. Proc. Natl. Acad. Sci. USA 90:5052-56
65. Kwon H, Imbalzano AN, Khavarl PA, Kingston RE, Green MR. 1994. Nucleosome disruption and enhancement of activator binding by a human SW1/SNF complex. Nature 370:477-81
66. 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
67. Lu Q, Wallrath LL, Elgin SC. 1995. The role of a positioned nucleosome at the Drosophila melanogaster hsp26 promoter. EMBO J. 14:4738-46
68. Lutter LC, Judis L, Paretti RF. 1992. Effects of histone acetylation on chromatin topology in vivo. Mol. Cell. Biol. 12:5004-14
69. Marmorstein R, Carey M, Ptashne M, Harrison SC. 1992. DNA recognition by GAL4: structure of aprotein-DNA complex. Nature 356:408-14
70. McGhee JD, Felsenfeld G. 1983. Another potential artifact in the study of nucleosome phasing by chromatin digestion with micrococcal nuclease. Cell 32:1205-15
71. McPherson CE, Shim E-Y, Friedman DS, Zaret KS. 1993. An active tissue-specific enhancer and bound transcription factors existing in a precisely positioned nucleosomal array. Cell 75:387-98
72. Meersseman G, Pennings S, Bradbury EM. 1992. Mobile nucleosomes - a general behavior. EMBO J. 11:2951-59
73. Meersseman G, Pennings S, Bradbury EM. 1991. Chromatosome positioning on assembled long chromatin. Linker histones affect nucleosome placement on 5 S rDNA. J. Mol. Biol. 220:89-100
74. Mirzabekov A, Pruss DV, Ebralidse KK. 1989. Chromatin superstructure-dependent crosslinking with DNA of the histone H5 residues Thr1, His25 and His62. J. Mol. Biol. 211:479-91
75. Mirzabekov AD, Pruss DV, Ebralidse KK. 1990. Chromatin superstructure-dependent crosslinking with DNA of the histone H5 residues Thr1, His25 and His62. J. Mol. Biol. 211:479-91
76. Moudrianakis EN, Arents G. 1993. Structure of the histone octamer core of the nucleosome and its potential interactions with DNA. Cold Spring Harbor Symp. Quant. Biol. 58:273-79
77. Moudrianakis EN, Love WE, Wang BC, Xuong NG, Burlingame RW. 1985. Scientific correspondence. Science 229:1110-12
78. Musgrave DR, Sandman KM, Reeve JN. 1991. DNA binding by the archaeal histone HMf results in positive supercoiling. Proc. Natl. Acad. Sci. USA 88:10397-401
79. Muyldermans S, Travers AA. 1994. DNA sequence organisation in chromatosomes J. Mol. Biol. 235:855-70
80. Ner SS, Travers AA. 1994. HMG-D, the Drosophila melanogaster homologue of HMG 1 protein, is associated with early embryonic chromatin in the absence of histone H1. EMBO J. 13:1817-22
81. Noll M, Kornberg RD. 1977. Action of micrococcal nuclease on chromatin and the location of histone H1. J. Mol. Biol. 109:393-404
82. Norton VG, Imai BS, Yau P, Bradbury EM. 1989. Histone acetylation reduces nucleosome core particle linking number change. Cell 57:449-57
83. Norton VG, Marvin KW, Yau P, Bradbury EM. 1990. Nucleosome linking number change controlled by acetylation of histones H3 and H4. J. Biol. Chem. 265:19848-52
84. O'Neill T, Meersseman G, Pennings S, Bradbury EM. 1995. Deposition of histone H1 onto reconstituted nucleosome arrays inhibits both initiation and elongation of transcripts by T7 RNA polymerase. Nucleic Acids Res. 23:1075-82
85. Pennings S, Meersseman S, Bradbury EM. 1991. Mobility of positioned nucleosomes on 5S rDNA. J. Mol. Biol. 220:101-10
86. Pennings S, Meersseman G, Bradbury EM. 1994. Linker histones H1 and H5 prevent the mobility of positioned nucleosomes. Proc. Natl. Acad. Sci. USA 91:10275-79
87. Poccia D. 1987. Regulation of chromatin condensation and decondensation in sea urchin pronuclei. In Regulation of Chromatin Condensation and Decondensation in Sea Urchin Pronuclei, ed. RA Schlegel, MS Halleck, PN Rao, pp. 149-77. New York: Academic
88. 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
89. Pruss D, Reeves R, Bushman FD, Wolffe AP. 1994. The influence of DNA and nucleosome structure on integration events directed by HIV integrase. J. Biol. Chem. 269:25031-41
90. Ramakrishnan V. 1994. Histone structure. Curr. Opinion. Struct. Biol. 4:44-50
91. Ramakrishnan V. 1995. The histone fold: evolutionary questions. Proc. Natl. Acad. Sci. USA 92:11328-30
92. Ramakrishnan V, Finch JT, Graziano V, Lee PL, Sweet RM. 1993. Crystal structure of globular domain of histone H5 and its implications for nucleosome binding. Nature 362:219-23
93. Rhodes D. 1985. Structural analysis of a triple complex between the histone octamer, a Xenopus gene for 5S RNA and transcription factor IIIA. EMBO J. 4:3473-82
94. Richmond TJ, Finch JT, Rushton B, Rhodes D, Klug A. 1984. Structure of the nucleosome core particle at 7 Å resolution. Nature 311:532-37
95. Richmond TJ, Rechsteiner T, Luger K. 1993. Studies of nucleosome structure. Cold Spring Harbor Symp. Quant. Biol. 58:265-72
96. Richmond TJ, Searles MA, Simpson RT. 1988. Crystals of a nucleosome core particle containing defined sequence DNA. J. Mol. Biol. 199:161-70
97. Roth SY, Allis CD. 1992. Chromatin condensation: Does histone H1 dephosphorylation play a role? Trends Biochem. Sci. 17:93-98
98. Satchwell SC, Drew HR, Travers AA. 1986. Sequence periodicities in chicken nucleosome core DNA. J. Mol. Biol. 191:659-75
99. Schild C, Claret FX, Wahli W, Wolffe AP. 1993. A nucleosome-dependent static loop potentiates estrogen-regulated transcription from the Xenopus vitellogenin B1 promoter in vitro. EMBO J. 12:423-33
100. Schlissel MS, Brown DD. 1984. The transcriptional regulation of Xenopus 5S RNA genes in chromatin: the roles of active stable transcription complexes and histone H1. Cell 37:903-13
101. Schultz SC, Shields GC, Steitz TA. 1991. Crystal structure of a CAP-DNA complex: the DNA is bent by 90°. Science 253:1001-7
102. Shick VV, Belyavsky AV, Bavykin SG, Mirzabekov AD. 1980. Primary organization of the nucleosome core particles. Sequential arrangement of histones along DNA. J. Mol. Biol. 139:491-517
103. Shrader TE, Crothers DM. 1989. Artificial nucleosome positioning sequences. Proc. Natl. Acad. Sci. USA 86:7418-22
104. Simpson RT. 1978. Structure of the chromatosome, a chromatin particle containing 160 base pairs of DNA and all the histones. Biochemistry 17:5524-31
105. Simpson RT. 1991. Nucleosome positioning: occurrence, mechanisms, and functional consequences. Prog. Nucleic Acid Res. Mol. Biol. 40:143-84
106. Simpson RT, Stafford DW. 1983. Structural features of a phased nucleosome core particle. Proc. Natl. Acad. Sci. USA 80:51-55
107. Starich MR, Sandman K, Reeve JN, Summers MF. 1996. NMR structure of HMfB from the hyperthermophile, Methanothermus fervidus, confirms that this archaeal protein is a histone. J. Mol. Biol. 255:187-203
108. Staynov DZ, Crane-Robinson C. 1988. Footprinting of linker histones H5 and H1 on the nucleosome. EMBO J. 7:3685-91
109. Studitsky VM, Clark DJ, Felsenfeld G. 1994. A histone octamer can step around a transcribing polymerase without leaving the template. Cell 76:371-82
110. Studitsky VM, Clark DJ, Felsenfeld G. 1995. Overcoming a nucleosomal barrier to transcription. Cell 83:19-27
111. Suzuki M. 1989. SPKK, a new nucleic acid-binding unit of protein found in histone. EMBO J. 8:797-804
112. Suzuki M, Gerstein M, Johnson T. 1993. An NMR study on the DNA-binding SPKK motif and a model for its interaction with DNA. Protein Eng. 6:565-74
113. Taunton J, Hassig CA, Schreiber SL. 1996. A mammalian histone deacetylase related to the yeast transcriptional regulator Rpd3p. Science 272:408-11
114. 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
115. Thoma F, Losa R, Koller T. 1983. Involvement of the domains of histones H1 and H5 in the structural organization of soluble chromatin. J. Mol. Biol. 167:619-40
116. Thomas JO. 1984. The higher order structure of chromatin and histone H1. J. Cell. Sci. Suppl. 1:1-20
117. Thomas JO, Rees C, Finch JT. 1992. Cooperative binding of the globular domains of histones H1 and H5 to DNA. Nucleic Acids Res. 20:187-94
118. Thomas JO, Wilson CM. 1986. Selective radiolabelling and identification of a strong nucleosome binding site on the globular domain of histone H5. EMBO J. 5:3531-37
119. Truss M, Bartsch J, Schelbert A, Hache RJ, Beato M. 1995. Hormone induces binding of receptors and transcription factors to a rearranged nucleosome on the MMTV promoter in vivo. EMBO J. 14:1737-51
120. Tsukiyama T, Becker PB, Wu C. 1994. ATP-dependent nucleosome disruption at a heat-shock promoter mediated by binding of GAGA transcription factor. Nature 367:525-32
121. Tsukiyama T, Daniel C, Tamkun J, Wu C. 1995. ISWI, a member of the SWI2/SNF2 ATPase family, encodes the 140 kDa subunit of the nucleosome remodeling factor. Cell 83:1021-26
122. Tsukiyama T, Wu C. 1995. Purification and properties of an ATP-dependent nucleosome remodeling factor. Cell 83:1011-20
123. Tullius TD, Dombroski BA, Churchill MEA, Kam L. 1987. Hydroxyl radical footprinting: a high resolution method for mapping protein-DNA contacts. Methods Enzymol. 155:537-59
124. Uberbacher EC, Harp JM, Bunick GJ. 1988. DNA sequence patterns in precisely positioned nucleosomes. J. Biomol. Struct. Dyn. 6:105-20
125. Ura K, Hayes JJ, Wolffe AP. 1995. A positive role for nucleosome mobility in the transcriptional activity of chromatin templates: restriction by linker histones. EMBO J. 14:3752-65
126. Usachenko SI, Gavin IM, Bavykin SG. 1996. Alterations in nucleosome core structure in linker histone-depleted chromatin. J. Biol. Chem. 271:3831-36
127. van Holde KE. 1989. Chromatin. New York: Springer-Verlag
128. Varga-Weisz P, van Holde K, Zlatanova J. 1993. Preferential binding of histone H1 to four-way helical junction DNA. J. Biol. Chem. 268:20699-700
129. Varga-Weisz P, Zlatanova J, Leuba SH, Schroth GP, van Holde K. 1994. Binding of histones H1 and H5 and their globular domains to four-way junction DNA. Proc. Natl. Acad. Sci. USA 91:3525-29
130. Venter U, Svaren J, Schmitz J, Schmid A, Horz W. 1994. A nucleosome precludes binding of the transcription factor Pho4 in vivo to a critical target site in the PHO5 promoter. EMBO J. 13:4848-55
131. Vogel T, Singer MF. 1975. Interaction of f1 histone with superhelical DNA. Proc. Natl. Acad. Sci. USA 72:2597-600
132. Wang BC, Rose J, Arents G, Moudrianakis EN. 1994. The octameric histone core of the nucleosome. Structural issues resolved. J. Mol. Biol. 236:179-88
133. Weintraub H. 1984. Histone H1 dependent chromatin superstructures and the suppression of gene activity. Cell 38:17-27
134. Whitlock JP Jr, Simpson RT. 1976. Removal of histone H1 exposes a fifty base pair DNA segment between nucleosomes. Biochemistry 15:3307-14
135. Wolffe AP. 1994. Transcription: in tune with the histones. Cell 77:13-16
136. Wolffe AP, Brown DD. 1988. Developmental regulation of two 5S ribosomal RNA genes. Science 241:1626-32
137. Xie X, Kokubo T, Cohen SL, Mirza UA, Hoffmann A, et al. 1996. Structural similarity between TAFs and the heterotetrameric core of the histone octamer. Nalure 380:316-22
138. Zlatanova J, van Holde K. 1996. The linker histone and chromatin structure: new twists. Prog. Nucleic Acid Res. Mol. Biol. 52:217-59