Facultative Heterochromatin: Is There a Distinctive Molecular Signature?

Molecular Cell

Volumn 28, Issue 1, 2007, Pages 1-13

  Trojer, Patrick ^a   Reinberg, Danny ^a  

^a NEW YORK UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

HISTONE H1;

ACETYLATION; CELL STRUCTURE; DNA METHYLATION; DNA TEMPLATE; EPIGENETICS; EUCHROMATIN; GENE EXPRESSION; GENE SILENCING; HETEROCHROMATIN; IMMUNOPRECIPITATION; PHOSPHORYLATION; PROTEIN PROCESSING; REVIEW;

ANIMALS; EPIGENESIS, GENETIC; EUKARYOTIC CELLS; GENE EXPRESSION REGULATION; GENE SILENCING; GENOME; HETEROCHROMATIN; HISTONES; MODELS, GENETIC; NUCLEIC ACID CONFORMATION;

EUKARYOTA;

EID: 34948839944     PISSN: 10972765     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.molcel.2007.09.011     Document Type: Review

References (120)

1. Agelopoulos M., and Thanos D. Epigenetic determination of a cell-specific gene expression program by ATF-2 and the histone variant macroH2A. EMBO J. 25 (2006) 4843-4853
2. Alami R., Fan Y., Pack S., Sonbuchner T.M., Besse A., Lin Q., Greally J.M., Skoultchi A.I., and Bouhassira E.E. Mammalian linker-histone subtypes differentially affect gene expression in vivo. Proc. Natl. Acad. Sci. USA 100 (2003) 5920-5925
3. Albright S.C., Nelson P.P., and Garrard W.T. Histone molar ratios among different electrophoretic forms of mono- and dinucleosomes. J. Biol. Chem. 254 (1979) 1065-1073
4. Bartolome S., Bermudez A., and Daban J.R. Internal structure of the 30 nm chromatin fiber. J. Cell Sci. 107 (1994) 2983-2992
5. Bates D.L., and Thomas J.O. Histones H1 and H5: one or two molecules per nucleosome?. Nucleic Acids Res. 9 (1981) 5883-5894
6. Bayne E.H., and Allshire R.C. RNA-directed transcriptional gene silencing in mammals. Trends Genet. 21 (2005) 370-373
7. Berger S.L. The complex language of chromatin regulation during transcription. Nature 447 (2007) 407-412
8. Bernstein E., Duncan E.M., Masui O., Gil J., Heard E., and Allis C.D. Mouse polycomb proteins bind differentially to methylated histone H3 and RNA and are enriched in facultative heterochromatin. Mol. Cell. Biol. 26 (2006) 2560-2569
9. Bernstein B.E., Meissner A., and Lander E.S. The mammalian epigenome. Cell 128 (2007) 669-681
10. Bloom W., and Fawcett D.W. A Textbook of Histology. 12th Edition (1994), Chapman and Hall, New York
11. Boveri T. Ergebnisse über die Konstitution der chromatischen Substanz des Zellkerns (1904), G. Fischer, Jena, Germany
12. Boyer L.A., Plath K., Zeitlinger J., Brambrink T., Medeiros L.A., Lee T.I., Levine S.S., Wernig M., Tajonar A., Ray M.K., et al. Polycomb complexes repress developmental regulators in murine embryonic stem cells. Nature 441 (2006) 349-353
13. Bracken A.P., Dietrich N., Pasini D., Hansen K.H., and Helin K. Genome-wide mapping of Polycomb target genes unravels their roles in cell fate transitions. Genes Dev. 20 (2006) 1123-1136
14. Brown S.W. Heterochromatin. Science 151 (1966) 417-425
15. Brown C.J., Ballabio A., Rupert J.L., Lafreniere R.G., Grompe M., Tonlorenzi R., and Willard H.F. A gene from the region of the human X inactivation centre is expressed exclusively from the inactive X chromosome. Nature 349 (1991) 38-44
16. Brown D.T., Izard T., and Misteli T. 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
17. Catez F., Ueda T., and Bustin M. Determinants of histone H1 mobility and chromatin binding in living cells. Nat. Struct. Mol. Biol. 13 (2006) 305-310
18. Changolkar L.N., and Pehrson J.R. Reconstitution of nucleosomes with histone macroH2A1.2. Biochemistry 41 (2002) 179-184
19. Choo J.H., Kim J.D., Chung J.H., Stubbs L., and Kim J. Allele-specific deposition of macroH2A1 in imprinting control regions. Hum. Mol. Genet. 15 (2006) 717-724
20. Costanzi C., and Pehrson J.R. Histone macroH2A1 is concentrated in the inactive X chromosome of female mammals. Nature 393 (1998) 599-601
21. Craig J.M. Heterochromatin-many flavours, common themes. Bioessays 27 (2005) 17-28
22. Dahiya A., Wong S., Gonzalo S., Gavin M., and Dean D.C. Linking the Rb and polycomb pathways. Mol. Cell 8 (2001) 557-569
23. Davey C.A., Sargent D.F., Luger K., Maeder A.W., and Richmond T.J. Solvent mediated interactions in the structure of the nucleosome core particle at 1.9 Å resolution. J. Mol. Biol. 319 (2002) 1097-1113
24. Delaval K., Govin J., Cerqueira F., Rousseaux S., Khochbin S., and Feil R. Differential histone modifications mark mouse imprinting control regions during spermatogenesis. EMBO J. 26 (2007) 720-729
25. Dimova D.K., and Dyson N.J. The E2F transcriptional network: old acquaintances with new faces. Oncogene 24 (2005) 2810-2826
26. Dorigo B., Schalch T., Bystricky K., and Richmond T.J. Chromatin fiber folding: requirement for the histone H4 N-terminal tail. J. Mol. Biol. 327 (2003) 85-96
27. Doyen C.M., An W., Angelov D., Bondarenko V., Mietton F., Studitsky V.M., Hamiche A., Roeder R.G., Bouvet P., and Dimitrov S. Mechanism of polymerase II transcription repression by the histone variant macroH2A. Mol. Cell. Biol. 26 (2006) 1156-1164
28. Eils R., Dietzel S., Bertin E., Schrock E., Speicher M.R., Ried T., Robert-Nicoud M., Cremer C., and Cremer T. Three-dimensional reconstruction of painted human interphase chromosomes: active and inactive X chromosome territories have similar volumes but differ in shape and surface structure. J. Cell Biol. 135 (1996) 1427-1440
29. ENCODE Project Consortium. Identification and analysis of functional elements in 1% of the human genome by the ENCODE pilot project. Nature 447 (2007) 799-816
30. Fan Y., Sirotkin A., Russell R.G., Ayala J., and Skoultchi A.I. Individual somatic H1 subtypes are dispensable for mouse development even in mice lacking the H1(0) replacement subtype. Mol. Cell. Biol. 21 (2001) 7933-7943
31. Fan Y., Nikitina T., Morin-Kensicki E.M., Zhao J., Magnuson T.R., Woodcock C.L., and Skoultchi A.I. H1 linker histones are essential for mouse development and affect nucleosome spacing in vivo. Mol. Cell. Biol. 23 (2003) 4559-4572
32. Fan Y., Nikitina T., Zhao J., Fleury T.J., Bhattacharyya R., Bouhassira E.E., Stein A., Woodcock C.L., and Skoultchi A.I. Histone H1 depletion in mammals alters global chromatin structure but causes specific changes in gene regulation. Cell 123 (2005) 1199-1212
33. Fang J., Chen T., Chadwick B., Li E., and Zhang Y. Ring1b-mediated H2A ubiquitination associates with inactive X chromosomes and is involved in initiation of X inactivation. J. Biol. Chem. 279 (2004) 52812-52815
34. Feil R., and Berger F. Convergent evolution of genomic imprinting in plants and mammals. Trends Genet. 23 (2007) 192-199
35. Felsenfeld G., and McGhee J.D. Structure of the 30 nm chromatin fiber. Cell 44 (1986) 375-377
36. Flemming W. Beitraege zur Kenntniss der Zelle und ihrer Lebenserscheinungen. Arch. Mikroskop. Anat. 16 (1878) 302-436
37. Flemming W. Zellsubstanz, Kern und Zelltheilung (1882), Verlag von F.C.W. Vogel, Leipzig, Germany
38. Grewal S.I., and Elgin S.C. Transcription and RNA interference in the formation of heterochromatin. Nature 447 (2007) 399-406
39. Grewal S.I., and Jia S. Heterochromatin revisited. Nat. Rev. Genet. 8 (2007) 35-46
40. Grimaud C., Bantignies F., Pal-Bhadra M., Ghana P., Bhadra U., and Cavalli G. RNAi components are required for nuclear clustering of Polycomb group response elements. Cell 124 (2006) 957-971
41. Grunstein M. Yeast heterochromatin: regulation of its assembly and inheritance by histones. Cell 93 (1998) 325-328
42. Guenther M.G., Levine S.S., Boyer L.A., Jaenisch R., and Young R.A. A chromatin landmark and transcription initiation at most promoters in human cells. Cell 130 (2007) 77-88
43. Heard E. Delving into the diversity of facultative heterochromatin: the epigenetics of the inactive X chromosome. Curr. Opin. Genet. Dev. 15 (2005) 482-489
44. Heard E., and Disteche C.M. Dosage compensation in mammals: fine-tuning the expression of the X chromosome. Genes Dev. 20 (2006) 1848-1867
45. Heitz E. Das Heterochromatin der Moose, 1. Jahrb. Wiss. Bot. 69 (1928) 762-818
46. Heitz E. Heterochromatin, Chromocentren, Chromomeren (Vorlaufige Mitteilung). Ber. Dtsch. Bot. Ges. 47 (1929) 274-284
47. Hernandez-Munoz I., Lund A.H., van der Stoop P., Boutsma E., Muijrers I., Verhoeven E., Nusinow D.A., Panning B., Marahrens Y., and van Lohuizen M. Stable X chromosome inactivation involves the PRC1 Polycomb complex and requires histone MACROH2A1 and the CULLIN3/SPOP ubiquitin E3 ligase. Proc. Natl. Acad. Sci. USA 102 (2005) 7635-7640
48. Jason L.J., Finn R.M., Lindsey G., and Ausio J. Histone H2A ubiquitination does not preclude histone H1 binding, but it facilitates its association with the nucleosome. J. Biol. Chem. 280 (2005) 4975-4982
49. Jeppesen P., and Turner B.M. The inactive X chromosome in female mammals is distinguished by a lack of histone H4 acetylation, a cytogenetic marker for gene expression. Cell 74 (1993) 281-289
50. Kalantry S., Mills K.C., Yee D., Otte A.P., Panning B., and Magnuson T. The Polycomb group protein Eed protects the inactive X-chromosome from differentiation-induced reactivation. Nat. Cell Biol. 8 (2006) 195-202
51. Kent W.J., Sugnet C.W., Furey T.S., Roskin K.M., Pringle T.H., Zahler A.M., and Haussler D. The human genome browser at UCSC. Genome Res. 12 (2002) 996-1006
52. Kim M.Y., Mauro S., Gevry N., Lis J.T., and Kraus W.L. NAD+-dependent modulation of chromatin structure and transcription by nucleosome binding properties of PARP-1. Cell 119 (2004) 803-814
53. Kim M.Y., Zhang T., and Kraus W.L. Poly(ADP-ribosyl)ation by PARP-1: 'PAR-laying' NAD+ into a nuclear signal. Genes Dev. 19 (2005) 1951-1967
54. Kim J., Daniel J., Espejo A., Lake A., Krishna M., Xia L., Zhang Y., and Bedford M.T. Tudor, MBT and chromo domains gauge the degree of lysine methylation. EMBO Rep. 7 (2006) 397-403 10.1038/sj.embor.7400625 Published online January 13, 2006
55. Klymenko T., Papp B., Fischle W., Kocher T., Schelder M., Fritsch C., Wild B., Wilm M., and Muller J. A Polycomb group protein complex with sequence-specific DNA-binding and selective methyl-lysine-binding activities. Genes Dev. 20 (2006) 1110-1122
56. Koop R., Di Croce L., and Beato M. Histone H1 enhances synergistic activation of the MMTV promoter in chromatin. EMBO J. 22 (2003) 588-599
57. Kornberg R.D. Chromatin structure: a repeating unit of histones and DNA. Science 184 (1974) 868-871
58. Kornberg R.D., and Thomas J.O. Chromatin structure; oligomers of the histones. Science 184 (1974) 865-868
59. Kotake Y., Cao R., Viatour P., Sage J., Zhang Y., and Xiong Y. pRB family proteins are required for H3K27 trimethylation and Polycomb repression complexes binding to and silencing p16INK4alpha tumor suppressor gene. Genes Dev. 21 (2007) 49-54
60. Kustatscher G., Hothorn M., Pugieux C., Scheffzek K., and Ladurner A.G. Splicing regulates NAD metabolite binding to histone macroH2A. Nat. Struct. Mol. Biol. 12 (2005) 624-625
61. Lee J.T. Sex chromosome inactivation: the importance of pairing. Curr. Biol. 15 (2005) R249-R252
62. Lee H., Habas R., and Abate-Shen C. MSX1 cooperates with histone H1b for inhibition of transcription and myogenesis. Science 304 (2004) 1675-1678
63. Lee T.I., Jenner R.G., Boyer L.A., Guenther M.G., Levine S.S., Kumar R.M., Chevalier B., Johnstone S.E., Cole M.F., Isono K., et al. Control of developmental regulators by Polycomb in human embryonic stem cells. Cell 125 (2006) 301-313
64. Lei E.P., and Corces V.G. A long-distance relationship between RNAi and Polycomb. Cell 124 (2006) 886-888
65. Lever M.A., Th'ng J.P., Sun X., and Hendzel M.J. Rapid exchange of histone H1.1 on chromatin in living human cells. Nature 408 (2000) 873-876
66. Lewis E.B. A gene complex controlling segmentation in Drosophila. Nature 276 (1978) 565-570
67. Li B., Carey M., and Workman J.L. The role of chromatin during transcription. Cell 128 (2007) 707-719
68. Mainguy G., Koster J., Woltering J., Jansen H., and Durston A. Extensive polycistronism and antisense transcription in the Mammalian Hox clusters. PLoS ONE 2 (2007) e356 10.1371/journal.pone.0000356
69. Maison C., and Almouzni G. HP1 and the dynamics of heterochromatin maintenance. Nat. Rev. Mol. Cell Biol. 5 (2004) 296-304
70. Martens J.H., O'Sullivan R.J., Braunschweig U., Opravil S., Radolf M., Steinlein P., and Jenuwein T. The profile of repeat-associated histone lysine methylation states in the mouse epigenome. EMBO J. 24 (2005) 800-812
71. Masui O., and Heard E. RNA and protein actors in X-chromosome inactivation. Cold Spring Harb. Symp. Quant. Biol. 71 (2006) 419-428
72. McClintock B. The origin and behavior of mutable loci in maize. Proc. Natl. Acad. Sci. USA 36 (1950) 344-355
73. McGarvey K.M., Greene E., Fahrner J.A., Jenuwein T., and Baylin S.B. DNA methylation and complete transcriptional silencing of cancer genes persist after depletion of EZH2. Cancer Res. 67 (2007) 5097-5102
74. McManus K.J., and Hendzel M.J. Using quantitative imaging microscopy to define the target substrate specificities of histone post-translational-modifying enzymes. Methods 36 (2005) 351-361
75. Mikkelsen T.S., Ku M., Jaffe D.B., Issac B., Lieberman E., Giannoukos G., Alvarez P., Brockman W., Kim T.K., Koche R.P., et al. Genome-wide maps of chromatin state in pluripotent and lineage-committed cells. Nature 448 (2007) 553-560
76. Millar C.B., and Grunstein M. Genome-wide patterns of histone modifications in yeast. Nat. Rev. Mol. Cell Biol. 7 (2006) 657-666
77. Misteli T., Gunjan A., Hock R., Bustin M., and Brown D.T. Dynamic binding of histone H1 to chromatin in living cells. Nature 408 (2000) 877-881
78. Mohd-Sarip A., van der Knaap J.A., Wyman C., Kanaar R., Schedl P., and Verrijzer C.P. Architecture of a polycomb nucleoprotein complex. Mol. Cell 24 (2006) 91-100
79. Muller H. The frequency of translocations produced by X-rays in Drosophila. Genetics 16 (1930) 277-285
80. Mutskov V.J., Farrell C.M., Wade P.A., Wolffe A.P., and Felsenfeld G. The barrier function of an insulator couples high histone acetylation levels with specific protection of promoter DNA from methylation. Genes Dev. 16 (2002) 1540-1554
81. Nielsen S.J., Schneider R., Bauer U.M., Bannister A.J., Morrison A., O'Carroll D., Firestein R., Cleary M., Jenuwein T., Herrera R.E., and Kouzarides T. Rb targets histone H3 methylation and HP1 to promoters. Nature 412 (2001) 561-565
82. Nusinow D.A., Hernandez-Munoz I., Fazzio T.G., Shah G.M., Kraus W.L., and Panning B. Poly(ADP-ribose) polymerase 1 is inhibited by a histone H2A variant, macroH2A, and contributes to silencing of the inactive X chromosome. J. Biol. Chem. 282 (2007) 12851-12859
83. Ogawa H., Ishiguro K., Gaubatz S., Livingston D.M., and Nakatani Y. A complex with chromatin modifiers that occupies E2F- and Myc-responsive genes in G0 cells. Science 296 (2002) 1132-1136
84. Olins A.L., and Olins D.E. Spheroid chromatin units (v bodies). Science 183 (1974) 330-332
85. Ouararhni K., Hadj-Slimane R., Ait-Si-Ali S., Robin P., Mietton F., Harel-Bellan A., Dimitrov S., and Hamiche A. The histone variant mH2A1.1 interferes with transcription by down-regulating PARP-1 enzymatic activity. Genes Dev. 20 (2006) 3324-3336
86. Oudet P., Gross-Bellard M., and Chambon P. Electron microscopic and biochemical evidence that chromatin structure is a repeating unit. Cell 4 (1975) 281-300
87. Ozsolak F., Song J.S., Liu X.S., and Fisher D.E. High-throughput mapping of the chromatin structure of human promoters. Nat. Biotechnol. 25 (2007) 244-248
88. Papp B., and Muller J. Histone trimethylation and the maintenance of transcriptional ON and OFF states by trxG and PcG proteins. Genes Dev. 20 (2006) 2041-2054
89. Parseghian M.H., and Hamkalo B.A. A compendium of the histone H1 family of somatic subtypes: an elusive cast of characters and their characteristics. Biochem. Cell Biol. 79 (2001) 289-304
90. Petruk S., Sedkov Y., Riley K.M., Hodgson J., Schweisguth F., Hirose S., Jaynes J.B., Brock H.W., and Mazo A. Transcription of bxd noncoding RNAs promoted by trithorax represses Ubx in cis by transcriptional interference. Cell 127 (2006) 1209-1221
91. Pien S., and Grossniklaus U. Polycomb group and trithorax group proteins in Arabidopsis. Biochim. Biophys. Acta 1769 (2007) 375-382
92. Pirrotta V. Polycombing the genome: PcG, trxG, and chromatin silencing. Cell 93 (1998) 333-336
93. Ptashne M. On the use of the word 'epigenetic'. Curr. Biol. 17 (2007) R233-R236
94. Ringrose L., and Paro R. Polycomb/trithorax response elements and epigenetic memory of cell identity. Development 134 (2007) 223-232
95. Rinn J.L., Kertesz M., Wang J.K., Squazzo S.L., Xu X., Brugmann S.A., Goodnough L.H., Helms J.A., Farnham P.J., Segal E., and Chang H.Y. Functional demarcation of active and silent chromatin domains in human HOX loci by noncoding RNAs. Cell 129 (2007) 1311-1323
96. Sakamoto Y., Watanabe S., Ichimura T., Kawasuji M., Koseki H., Baba H., and Nakao M. Overlapping roles of the methylated DNA-binding protein MBD1 and polycomb group proteins in transcriptional repression of HOXA genes and heterochromatin foci formation. J. Biol. Chem. 282 (2007) 16391-16400
97. Schlesinger Y., Straussman R., Keshet I., Farkash S., Hecht M., Zimmerman J., Eden E., Yakhini Z., Ben-Shushan E., Reubinoff B.E., et al. Polycomb-mediated methylation on Lys27 of histone H3 pre-marks genes for de novo methylation in cancer. Nat. Genet. 39 (2007) 232-236
98. Schoeftner S., Sengupta A.K., Kubicek S., Mechtler K., Spahn L., Koseki H., Jenuwein T., and Wutz A. Recruitment of PRC1 function at the initiation of X inactivation independent of PRC2 and silencing. EMBO J. 25 (2006) 3110-3122
99. Schuettengruber B., Chourrout D., Vervoort M., Leblanc B., and Cavalli G. Genome regulation by polycomb and trithorax proteins. Cell 128 (2007) 735-745
100. Schwartz Y.B., and Pirrotta V. Polycomb silencing mechanisms and the management of genomic programmes. Nat. Rev. Genet. 8 (2007) 9-22
101. Schwartz Y.B., Kahn T.G., Nix D.A., Li X.Y., Bourgon R., Biggin M., and Pirrotta V. Genome-wide analysis of Polycomb targets in Drosophila melanogaster. Nat. Genet. 38 (2006) 700-705
102. Sessa L., Breiling A., Lavorgna G., Silvestri L., Casari G., and Orlando V. Noncoding RNA synthesis and loss of Polycomb group repression accompanies the colinear activation of the human HOXA cluster. RNA 13 (2007) 223-239
103. Sirotkin A.M., Edelmann W., Cheng G., Klein-Szanto A., Kucherlapati R., and Skoultchi A.I. Mice develop normally without the H1(0) linker histone. Proc. Natl. Acad. Sci. USA 92 (1995) 6434-6438
104. Smith C.D., Shu S., Mungall C.J., and Karpen G.H. The Release 5.1 annotation of Drosophila melanogaster heterochromatin. Science 316 (2007) 1586-1591
105. Sparmann A., and van Lohuizen M. Polycomb silencers control cell fate, development and cancer. Nat. Rev. Cancer 6 (2006) 846-856
106. Squazzo S.L., O'Geen H., Komashko V.M., Krig S.R., Jin V.X., Jang S.W., Margueron R., Reinberg D., Green R., and Farnham P.J. Suz12 binds to silenced regions of the genome in a cell-type-specific manner. Genome Res. 16 (2006) 890-900
107. Talasz H., Sapojnikova N., Helliger W., Lindner H., and Puschendorf B. In vitro binding of H1 histone subtypes to nucleosomal organized mouse mammary tumor virus long terminal repeat promotor. J. Biol. Chem. 273 (1998) 32236-32243
108. Talbert P.B., and Henikoff S. Spreading of silent chromatin: inaction at a distance. Nat. Rev. Genet. 7 (2006) 793-803
109. Tanay A., O'Donnell A.H., Damelin M., and Bestor T.H. Hyperconserved CpG domains underlie Polycomb-binding sites. Proc. Natl. Acad. Sci. USA 104 (2007) 5521-5526
110. Tolhuis B., de Wit E., Muijrers I., Teunissen H., Talhout W., van Steensel B., and van Lohuizen M. Genome-wide profiling of PRC1 and PRC2 Polycomb chromatin binding in Drosophila melanogaster. Nat. Genet. 38 (2006) 694-699
111. Trojer P., Li G., Sims III R.J., Vaquero A., Kalakonda N., Boccuni P., Lee D., Erdjument-Bromage H., Tempst P., Nimer S.D., et al. L3MBTL1, a histone-methylation-dependent chromatin lock. Cell 129 (2007) 915-928
112. Turner B.M. Defining an epigenetic code. Nat. Cell Biol. 9 (2007) 2-6
113. Vaquero A., Scher M., Lee D., Erdjument-Bromage H., Tempst P., and Reinberg D. Human SirT1 interacts with histone H1 and promotes formation of facultative heterochromatin. Mol. Cell 16 (2004) 93-105
114. Vire E., Brenner C., Deplus R., Blanchon L., Fraga M., Didelot C., Morey L., Van Eynde A., Bernard D., Vanderwinden J.M., et al. The Polycomb group protein EZH2 directly controls DNA methylation. Nature 439 (2005) 871-874
115. Wang H., Wang L., Erdjument-Bromage H., Vidal M., Tempst P., Jones R.S., and Zhang Y. Role of histone H2A ubiquitination in Polycomb silencing. Nature 431 (2004) 873-878
116. Widschwendter M., Fiegl H., Egle D., Mueller-Holzner E., Spizzo G., Marth C., Weisenberger D.J., Campan M., Young J., Jacobs I., and Laird P.W. Epigenetic stem cell signature in cancer. Nat. Genet. 39 (2007) 157-158
117. Wollfe A. Chromatin, Structure and Function (1998), Academia Press, Trowbridge, UK
118. Woodcock C.L., Skoultchi A.I., and Fan Y. Role of linker histone in chromatin structure and function: H1 stoichiometry and nucleosome repeat length. Chromosome Res. 14 (2006) 17-25
119. Yellajoshyula D., and Brown D.T. Global modulation of chromatin dynamics mediated by dephosphorylation of linker histone H1 is necessary for erythroid differentiation. Proc. Natl. Acad. Sci. USA 103 (2006) 18568-18573
120. Yuan G.C., Liu Y.J., Dion M.F., Slack M.D., Wu L.F., Altschuler S.J., and Rando O.J. Genome-scale identification of nucleosome positions in S. cerevisiae. Science 309 (2005) 626-630