Intra- and inter-nucleosome interactions of the core histone tail domains in higher-order chromatin structure

Chromosoma

Volumn 123, Issue 1-2, 2014, Pages 3-13

  Pepenella, Sharon ^a   Murphy, Kevin J ^a   Hayes, Jeffrey J ^a  

^a UNIVERSITY OF ROCHESTER MEDICAL CENTER   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

DNA; HISTONE H3; HISTONE H4; PROTEIN; TRANS ACTING FACTOR;

AMINO TERMINAL SEQUENCE; CELL INTERACTION; CHROMATIN STRUCTURE; GENE EXPRESSION REGULATION; HISTONE ACETYLATION; NUCLEOSOME; PROTEIN PROCESSING; REVIEW; STRUCTURE ANALYSIS;

EUKARYOTA;

ACETYLATION; ANIMALS; HISTONES; HUMANS; NUCLEOSOMES; PROTEIN STRUCTURE, TERTIARY;

EID: 84897475985     PISSN: 00095915     EISSN: 14320886     Source Type: Journal    
DOI: 10.1007/s00412-013-0435-8     Document Type: Review

References (91)

1. Allahverdi A, Yang R, Korolev N, Fan Y, Davey CA, Liu CF, Nordenskiold L (2011) The effects of histone H4 tail acetylations on cation-induced chromatin folding and self-association. Nucleic Acids Res 39:1680-1691
2. Allan J, Hartman PG, Crane-Robinson C, Aviles FX (1980) The structure of histone H1 and its location in chromatin. Nature 288:675-679 (Pubitemid 11168522)
3. Allan J, Harborne N, Rau DC, Gould H (1982) Participation of the core histone tails in the stabilization of the chromatin solenoid. J Cell Biol 93:285-297
4. Allfrey VG, Faulkner R, Mirsky AE (1964) Acetylation and methylation of histones and their possible role in the regulation of RNA synthesis. Proc Natl Acad Sci U S A 51:786-794
5. Angelov D, Vitolo JM, Mutskov V, Dimitrov S, Hayes JJ (2001) Preferential interaction of the core histone tail domains with linker DNA. Proc Natl Acad Sci U S A 98:6599-6604 (Pubitemid 32538262)
6. Annunziato AT, Hansen JC (2000) Role of histone acetylation in the assembly and modulation of chromatin structures. Gene Expr 9:37-61
7. 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 U S A 90:10489-10493 (Pubitemid 23347067)
8. Arents G, Burlingame RW, Wang BC, Love WE, Moudrianakis EN (1991) 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 88:10148-10152 (Pubitemid 21915792)
9. Armache KJ, Garlick JD, Canzio D, Narlikar GJ, Kingston RE (2011) Structural basis of silencing: Sir3 BAH domain in complex with a nucleosome at 3.0 Å resolution. Science 334:977-982
10. Ausio J, Dong F, van Holde KE (1989) Use of selectively trypsinized nucleosome core particles to analyze the role of the histone "tails" in the stabilization of the nucleosome. J Mol Biol 206:451-463 (Pubitemid 19104985)
11. Bai L, Charvin G, Siggia ED, Cross FR (2010) Nucleosome-depleted regions in cell-cycle-regulated promoters ensure reliable gene expression in every cell cycle. Dev Cell 18:544-555
12. Barbera AJ, Chodaparambil JV, Kelley-Clarke B, Joukov V, Walter JC, Luher K, Kaye KM (2006) The nucleosomal surface as a docking station for Kaposi's sarcoma herpesvirus LANA. Science. 311:856-861 (Pubitemid 43228851)
13. Bates DL, Butler JG, Pearson EC, Thomas JO (1981) Stability of the higher-order structure of chicken erythrocyte chromatin in solution. Eur J Biochem 119:469-476
14. Belmont AS, Bruce K (1994) Visualization of G1 chromosomes: a folded, twisted, supercoiled chromonema model of interphase chromatid structure. J Cell Biol 127:287-302 (Pubitemid 24313721)
15. Bohm L, Crane-Robinson C (1984) Proteases as structural probes for chromatin: the domain structure of histones. Biosci Rep 4:365-386 (Pubitemid 14076152)
16. Camerini-Otero RD, Sollner-Webb B, Felsenfeld G (1976) The organization of histones and DNA in chromatin: evidence for an arginine-rich histone kernel. Cell 8:333-347
17. Carruthers LM, Bednar J, Woodcock CL, Hansen JC (1998) Linker histones stabilize the intrinsic salt-dependent folding of nucleosomal arrays: mechanistic ramifications for higher-order chromatin folding. Biochemistry 37:14776-14787 (Pubitemid 28487585)
18. Caterino TL, Fang H, Hayes JJ (2011) Nucleosome linker DNA contacts and induces specific folding of the intrinsically disordered H1 carboxyl-terminal domain. Mol Cell Biol 31:2341-2348
19. Chafin DR, Vitolo JM, Henricksen LA, Bambara RA, Hayes JJ (2000) Human DNA ligase I efficiently seals nicks in nucleosomes. EMBO J 19:5492-5501
20. Chodaparambil JV, Barbera AJ, Lu X, Kaye KM, Hansen JC, Luger K (2007) A charged and contoured surface on the nucleosome regulates chromatin compaction. Nat Struct Mol Biol 14:1105-1107 (Pubitemid 350060342)
21. Clark DJ, Kimura T (1990) Electrostatic mechanism of chromatin folding. J Mol Biol 211:883-896 (Pubitemid 20113668)
22. Daban JR (2011) Electron microscopy and atomic force microscopy studies of chromatin and metaphase chromosome structure. Micron 42:733-750
23. Davey CA, Sargent DF, Luger K, Maeder AW, Richmond TJ (2002) Solvent mediated interactions in the structure of the nucleosome core particle at 1.9 a resolution. J Mol Biol 319:1097-1113 (Pubitemid 34729421)
24. Dion MF, Altschuler SJ, Wu LF, Rando OJ (2005) Genomic characterization reveals a simple histone H4 acetylation code. Proc Natl Acad Sci USA 102:5501-5506 (Pubitemid 40530287)
25. 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 (Pubitemid 36293304)
26. Dorigo B, Schalch T, Kulangara A, Duda S, Schroeder RR, Richmond TJ (2004) Nucleosome arrays reveal the two-start organization of the chromatin fiber. Science 306:1571-1573 (Pubitemid 39564956)
27. Eberharter A, Becker PB (2002) Histone acetylation: a switch between repressive and permissive chromatin. Second in review series on chromatin dynamics. EMBO Rep 3:224-229 (Pubitemid 34269514)
28. Ebralidse KK, Grachev SA, Mirzabekov AD (1988) A highly basic histone H4 domain bound to the sharply bent region of nucleosomal DNA. Nature 331:365-367 (Pubitemid 18042496)
29. Fan JY, Gordon F, Luger K, Hansen JC, Tremethick DJ (2002) The essential histone variant H2A.Z regulates the equilibrium between different chromatin conformational states. Nat Struct Biol 9:172-176 (Pubitemid 34171307)
30. Fan JY, Rangasamy D, Luger K, Tremethick DJ (2004) H2A.Z alters the nucleosome surface to promote HP1alpha-mediated chromatin fiber folding. Mol Cell 16:655-661 (Pubitemid 39531887)
31. Garcia-Ramirez M, Dong F, Ausio J (1992) Role of the histone "tails" in the folding of oligonucleosomes depleted of histone H1. J Biol Chem 267:19587-19595
32. Garcia-Ramirez M, Rocchini C, Ausio J (1995) Modulation of chromatin folding by histone acetylation. J Biol Chem 270:17923-17928
33. Gordon F, Luger K, Hansen JC (2005) The core histone N-terminal tail domains function independently and additively during saltdependent oligomerization of nucleosomal arrays. J Biol Chem 280:33701-33706 (Pubitemid 41443087)
34. Graziano V, Gerchman SE, Ramakrishnan V (1988) Reconstitution of chromatin higher-order structure from histone H5 and depleted chromatin. J Mol Biol 203:997-1007
35. Grigoryev SA, Woodcock CL (2012) Chromatin organization - the 30 nm fiber. Exp Cell Res 318:1448-1455
36. Grunstein M (1997) Histone acetylation in chromatin structure and transcription. Nature 389:349-352
37. Han M, Grunstein M (1988) Nucleosome loss activates yeast downstream promoters in vivo. Cell 55:1137-1145 (Pubitemid 19020066)
38. Hansen JC (2002) Conformational dynamics of the chromatin fiber in solution: determinants, mechanisms, and functions. Annu Rev Biophys Biomol Struct 31:361-392
39. Hansen JC, Ausio J, Stanik VH, van Holde KE (1989) Homogeneous reconstituted oligonucleosomes, evidence for salt-dependent folding in the absence of histone H1. Biochemistry 28:9129-9136 (Pubitemid 19283481)
40. Hong L, Schroth GP, Matthews HR, Yau P, Bradbury EM (1993) 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 268:305-314 (Pubitemid 23021321)
41. Huynh VA, Robinson PJ, Rhodes D (2005) A method for the in vitro reconstitution of a defined "30 nm" chromatin fibre containing stoichiometric amounts of the linker histone. J Mol Biol 345:957-968 (Pubitemid 40092217)
42. James TC, Elgin SC (1986) Identification of a nonhistone chromosomal protein associated with heterochromatin in Drosophila melanogaster and its gene. Mol Cell Biol 6:3862-3872
43. Kalashnikova AA, Porter-Goff ME, Muthurajan UM, Luger K, Hansen JC (2013) The role of the nucleosome acidic patch in modulating higher order chromatin structure. J R Soc Interface 10:20121022
44. Kan PY, Hayes JJ (2007) Detection of interactions between nucleosome arrays mediated by specific core histone tail domains. Methods 41: 278-285
45. Kan PY, Lu X, Hansen JC, Hayes JJ (2007) The H3 tail domain participates in multiple interactions during folding and self-association of nucleosome arrays. Mol Cell Biol 27:2084-2091 (Pubitemid 46418466)
46. Kan PY, Caterino TL, Hayes JJ (2009) The H4 tail domain participates in intra- and internucleosome interactions with protein and DNA during folding and oligomerization of nucleosome arrays. Mol Cell Biol 29:538-546
47. Kato H, van Ingen H, Zhou BR, Feng H, Bustin M, Kay LE, Bai Y (2011) Architecture of the high mobility group nucleosomal protein 2-nucleosome complex as revealed by methyl-based NMR. Proc Natl Acad Sci U S A 108:12283-12288
48. Lee KM, Hayes JJ (1997) The N-terminal tail of histone H2A binds to two distinct sites within the nucleosome core. Proc Natl Acad Sci U S A 94:8959-8964
49. Lee KM, Hayes JJ (1998) Linker DNA and H1-dependent reorganization of histone-DNA interactions within the nucleosome. Biochemistry 37:8622-8628
50. 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 (Pubitemid 23029694)
51. Lowary PT, Widom J (1998) New DNA sequence rules for high affinity binding to histone octamer and sequence-directed nucleosome positioning. J Mol Biol 276:19-42 (Pubitemid 28085408)
52. Luger K, Hansen JC (2005) Nucleosome and chromatin fiber dynamics. Curr Opin Struct Biol 15:188-196
53. Luger K, Mader AW, Richmond RK, Sargent DF, Richmond TJ (1997) Crystal structure of the nucleosome core particle at 2.8 A resolution. Nature 389:251-260 (Pubitemid 27406632)
54. 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 13:436-447
55. Makde RD, England JR, Yennawar HP, Tan S (2010) Structure of RCC1 chromatin factor bound to the nucleosome core particle. Nature 467:562-566
56. Mirzabekov AD, Bavykin SG, Karpov VL, Preobrazhenskaya OV, Ebralidze KK, Tuneev VM, Melnikova AF, Goguadze EG, Chenchick AA, Beabealashvili RS (1983) Structure of nucleosomes, chromatin, and RNA polymerase-promoter complex as revealed by DNA-protein cross-linking. Cold Spring Harb Symp Quant Biol 47: 503-510 (Pubitemid 13071232)
57. Nishino Y, Eltsov M, Joti Y, Ito K, Takata H, Takahashi Y, Hihara S, Frangakis AS, Imamoto N, Ishikawa T, Maeshima K (2012) Human mitotic chromosomes consist predominantly of irregularly folded nucleosome fibres without a 30-nm chromatin structure. EMBO J 31:1644-1653
58. Olins AL, Olins DE (1974) Spheroid chromatin units (v bodies). Science 183:330-332
59. 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 298:211-233
60. 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 362:219-224
61. Ridsdale JA, Hendzel MJ, Delcuve GP, Davie JR (1990) Histone acetylation alters the capacity of the H1 histones to condense transcriptionally active/competent chromatin. J Biol Chem 265:5150-5156
62. Roberge M, O'Neill TE, Bradbury EM (1991) Inhibition of 5S RNA transcription in vitro by nucleosome cores with low or high levels of histone acetylation. FEBS Lett 288:215-218
63. Robinson PJ, An W, Routh A, Martino F, Chapman L, Roeder RG, Rhodes D (2008) 30 nm chromatin fibre decompaction requires both H4-K16 acetylation and linker histone eviction. J Mol Biol 381:816-825
64. Schwarz PM, Felthauser A, Fletcher TM, Hansen JC (1996) Reversible oligonucleosome self-association: dependence on divalent cations and core histone tail domains. Biochemistry 35:4009-4015 (Pubitemid 26113457)
65. Shahbazian MD, Grunstein M (2007) Functions of site-specific histone acetylation and deacetylation. Annu Rev Biochem 76:75-100
66. 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 311:844-847 (Pubitemid 43228847)
67. Simpson RT (1978) Structure of chromatin containing extensively acetylated H3 and H4. Cell 13:691-699
68. Simpson RT, Thoma F, Brubaker JM (1985) Chromatin reconstituted from tandemly repeated cloned DNA fragments and core histones: a model system for study of higher order structure. Cell 42:799-808 (Pubitemid 16083721)
69. Sinha D, Shogren-Knaak MA (2010) Role of direct interactions between the histone H4 tail and the H2A core in long range nucleosome contacts. J Biol Chem 285:16572-16581
70. Smith RM, Rill RL (1989)Mobile histone tails in nucleosomes. Assignments of mobile segments and investigations of their role in chromatin folding. J Biol Chem 264:10574-10581 (Pubitemid 19161625)
71. Strahl BD, Allis CD (2000) The language of covalent histone modifications. Nature 403:41-45 (Pubitemid 30038513)
72. Syed SH, Goutte-Gattat D, Becker N, Meyer S, Shukla MS, Hayes JJ, Everaers R, Angelov D, Bednar J, Dimitrov S (2010) Single-base resolution mapping of H1-nucleosome interactions and 3D organization of the nucleosome. Proc Natl Acad Sci U S A 107:9620-9625
73. Thoma F, Koller T, Klug A (1979) Involvement of histone H1 in the organization of the nucleosome and of the salt-dependent super-structures of chromatin. J Cell Biol 83:403-427 (Pubitemid 10205723)
74. Tremethick DJ (2007) Higher-order structures of chromatin: the elusive 30 nm fiber. Cell 128:651-654
75. Tse C, Hansen JC (1997) Hybrid trypsinized nucleosomal arrays: identification of multiple functional roles of the H2A/H2B and H3/H4 Ntermini in chromatin fiber compaction. Biochemistry 36:11381-11388 (Pubitemid 27408620)
76. Tse C, Sera T, Wolffe AP, Hansen JC (1998) Disruption of higher-order folding by core histone acetylation dramatically enhances transcription of nucleosomal arrays by RNA polymerase III. Mol Cell Biol 18:4629-4638 (Pubitemid 28343048)
77. Usachenko SI, Bavykin SG, Gavin IM, Bradbury EM (1994) Rearrangement of the histone H2A C-terminal domain in the nucleosome. Proc Natl Acad Sci U S A 91:6845-6849 (Pubitemid 24226758)
78. van Holde KE (1989) Chromatin. Springer, New York
79. Vettese-Dadey M, Walter P, Chen H, Juan LJ, Workman JL (1994) Role of the histone amino termini in facilitated binding of a transcription factor, GAL4-AH, to nucleosome cores. Mol Cell Biol 14:970-981 (Pubitemid 24036547)
80. Vitolo JM, Yang Z, Basavappa R, Hayes JJ (2004) Structural features of transcription factor IIIA bound to a nucleosome in solution. Mol Cell Biol 24:697-707 (Pubitemid 38057921)
81. Walker IO (1984) Differential dissociation of histone tails from core chromatin. Biochemistry 23:5622-5628
82. Wang X, Hayes JJ (2007) Site-specific binding affinities within the H2B tail domain indicate specific effects of lysine acetylation. J Biol Chem 282:32867-32876 (Pubitemid 350159266)
83. Wang X, Hayes JJ (2008) Acetylation mimics within individual core histone tail domains indicate distinct roles in regulating the stability of higher-order chromatin structure. Mol Cell Biol 28:227- 236
84. Whitlock JP Jr, Stein A (1978) Folding of DNA by histones which lack their NH2-terminal regions. J Biol Chem 253:3857-3861
85. Widom J (1986) Physicochemical studies of the folding of the 100 A nucleosome filament into the 300 A filament. Cation dependence. J Mol Biol 190:411-424
86. Widom J, Finch JT, Thomas JO (1985) Higher-order structure of long repeat chromatin. EMBO J 4:3189-3194
87. Williams SP, Langmore JP (1991) Small angle x-ray scattering of chromatin. Radius and mass per unit length depend on linker length. Biophys J 59:606-618
88. Wolffe AP, Hayes JJ (1999) Chromatin disruption and modification. Nucleic Acids Res 27:711-720 (Pubitemid 29209356)
89. Woodcock CL, Dimitrov S (2001) Higher-order structure of chromatin and chromosomes. Curr Opin Genet Dev 11:130-135 (Pubitemid 32209195)
90. Zheng C, Lu X, Hansen JC, Hayes JJ (2005) Salt-dependent intra- and internucleosomal interactions of the H3 tail domain in a model oligonucleosomal array. J Biol Chem 280:33552-33557 (Pubitemid 41397155)
91. 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 14:1070-1076 (Pubitemid 350060339)