Nucleosome positioning and gene regulation: Advances through genomics

Nature Reviews Genetics

Volumn 10, Issue 3, 2009, Pages 161-172

  Jiang, Cizhong ^a   Pugh, B Franklin ^a  

^a PENNSYLVANIA STATE UNIVERSITY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CHROMATIN ASSEMBLY AND DISASSEMBLY; CHROMATIN STRUCTURE; DNA SEQUENCE; GENE CONTROL; GENE SEQUENCE; GENETIC TRANSCRIPTION; GENOME; GENOMICS; NONHUMAN; NUCLEOSOME; PRIORITY JOURNAL; PROMOTER REGION; REVIEW; TRANSCRIPTION REGULATION;

ANIMALS; CHROMATIN ASSEMBLY AND DISASSEMBLY; GENE EXPRESSION REGULATION; GENOMICS; HUMANS; NUCLEOSOMES; SACCHAROMYCES CEREVISIAE;

EID: 60349089645     PISSN: 14710056     EISSN: 14710064     Source Type: Journal    
DOI: 10.1038/nrg2522     Document Type: Review

References (131)

1. Kornberg, R. D. & Klug, A. The nucleosome. Sci. Am. 244, 52-64 (1981).
2. Luger, K., Mader, A. W., Richmond, R. K., Sargent, D. F. & Richmond, T. J. Crystal structure of the nucleosome core particle at 2.8 Å resolution. Nature 389, 251-260 (1997).
3. Kamakaka, R. T. & Biggins, S. Histone variants: deviants? Genes Dev. 19, 295-310 (2005).
4. Sarma, K. & Reinberg, D. Histone variants meet their match. Nature Rev. Mol. Cell. Biol. 6, 139-149 (2005).
5. Lee, C. K., Shibata, Y., Rao, B., Strahl, B. D. & Lieb, J. D. Evidence for nucleosome depletion at active regulatory regions genome-wide. Nature Genet. 36, 900-905 (2004).
6. Sekinger, E. A., Moqtaderi, Z. & Struhl, K. Intrinsic histone-DNA interactions and low nucleosome density are important for preferential accessibility of promoter regions in yeast. Mol. Cell 18, 735-748 (2005). An early study that showed, using in vitro reconstituted nucleosomes at specific loci, that NFRs and nucleosomes positioned nearby might be dictated largely by intrinsic DNA sequence preference rather than by trans-acting factors.
7. Bernstein, B. E., Liu, C. L., Humphrey, E. L., Perlstein, E. O. & Schreiber, S. L. Global nucleosome occupancy in yeast. Genome Biol. 5, R62 (2004).
8. Guillemette, B. et al. Variant histone H2A.Z is globally localized to the promoters of inactive yeast genes and regulates nucleosome positioning. PLoS Biol. 3, e384 (2005).
9. Schwabish, M. A. & Struhl, K. Evidence for eviction and rapid deposition of histones upon transcriptional elongation by RNA polymerase II. Mol. Cell. Biol. 24, 10111-10117 (2004).
10. Zanton, S. J. & Pugh, B. F. Full and partial genomewide assembly and disassembly of the yeast transcription machinery in response to heat shock. Genes Dev. 20, 2250-2265 (2006).
11. Zhang, H., Roberts, D. N. & Cairns, B. R. Genome-wide dynamics of Htz1, a histone H2A variant that poises repressed/basal promoters for activation through histone loss. Cell 123, 219-231 (2005).
12. Kurdistani, S. K., Tavazoie, S. & Grunstein, M. Mapping global histone acetylation patterns to gene expression. Cell 117, 721-733 (2004).
13. Vogelauer, M., Wu, J., Suka, N. & Grunstein, M. Global histone acetylation and deacetylation in yeast. Nature 408, 495-498 (2000).
14. Bernstein, B. E. et al. Methylation of histone H3 Lys 4 in coding regions of active genes. Proc. Natl Acad. Sci. USA 99, 8695-8700 (2002).
15. Yuan, G. C. et al. Genome-scale identification of nucleosome positions in S. cerevisiae. Science 309, 626-630 (2005). The first high-resolution genome-wide study to reveal a NFR and a canonical arrangement of nucleosomes, including the DNA sequences that contribute to this arrangement.
16. Barski, A. et al. High-resolution profiling of histone methylations in the human genome. Cell 129, 823-837 (2007). One of the most extensive catalogues of the positions of post-translationally modified nucleosomes throughout the human genome. The study used ChIP-Seq and reports on patterns associated with each nucleosome modification.
17. Mavrich, T. N. et al. Nucleosome organization in the Drosophila genome. Nature 453, 358-362 (2008).
18. Lee, W. et al. A high-resolution atlas of nucleosome occupancy in yeast. Nature Genet. 39, 1235-1244 (2007).
19. Albert, I. et al. Translational and rotational settings of H2A.Z nucleosomes across the Saccharomyces cerevisiae genome. Nature 446, 572-576 (2007). This paper provides the first report of the use of ChIP-Seq to develop high-resolution maps of nucleosome positions, which allowed the rotational and translational context of DNA regulatory elements to be determined.
20. Mavrich, T. N. et al. A barrier nucleosome model for statistical positioning of nucleosomes throughout the yeast genome. Genome Res. 18, 1073-1083 (2008). This paper provides evidence that sequence-based nucleosome positioning is largely restricted to promoter regions, and that adjacent positions are dictated largely by packing principles.
21. Mito, Y., Henikoff, J. G. & Henikoff, S. Histone replacement marks the boundaries of cis-regulatory domains. Science 315, 1408-1411 (2007).
22. Schones, D. E. et al. Dynamic regulation of nucleosome positioning in the human genome. Cell 132, 887-898 (2008).
23. Shivaswamy, S. et al. Dynamic remodeling of individual nucleosomes across a eukaryotic genome in response to transcriptional perturbation. PLoS Biol. 6, e65 (2008).
24. Valouev, A. et al. A high-resolution, nucleosome position map of C. elegans reveals a lack of universal sequence-dictated positioning. Genome Res. 18, 1051-1063 (2008).
25. Ito, T., Bulger, M., Pazin, M. J., Kobayashi, R. & Kadonaga, J. T. ACF, an ISWI-containing and ATP-utilizing chromatin assembly and remodeling factor. Cell 90, 145-155 (1997).
26. Varga-Weisz, P. D. et al. Chromatin-remodelling factor CHRAC contains the ATPases ISWI and topoisomerase II. Nature 388, 598-602 (1997).
27. Saha, A., Wittmeyer, J. & Cairns, B. R. Mechanisms for nucleosome movement by ATP-dependent chromatin remodeling complexes. Results Probl. Cell Differ. 41, 127-148 (2006).
28. Gangaraju, V. K. & Bartholomew, B. Mechanisms of ATP-dependent chromatin remodeling. Mutat. Res. 618, 3-17 (2007).
29. Kagalwala, M. N., Glaus, B. J., Dang, W., Zofall, M. & Bartholomew, B. Topography of the ISW2-nucleosome complex: insights into nucleosome spacing and chromatin remodeling. EMBO J. 23, 2092-2104 (2004).
30. Ferreira, H. & Owen-Hughes, T. Lighting up nucleosome spacing. Nature Struct. Mol. Biol. 13, 1047-1049 (2006).
31. Rippe, K. et al. DNA sequence- and conformationdirected positioning of nucleosomes by chromatin-remodeling complexes. Proc. Natl Acad. Sci. USA 104, 15635-15640 (2007).
32. Blank, T. A. & Becker, P. B. Electrostatic mechanism of nucleosome spacing. J. Mol. Biol. 252, 305-313 (1995).
33. Fan, Y. et al. H1 linker histones are essential for mouse development and affect nucleosome spacing in vivo. Mol. Cell. Biol. 23, 4559-4572 (2003).
34. Fan, Y. et al. Histone H1 depletion in mammals alters global chromatin structure but causes specific changes in gene regulation. Cell 123, 1199-1212 (2005).
35. Malik, H. S. & Henikoff, S. Phylogenomics of the nucleosome. Nature Struct. Biol. 10, 882-891 (2003).
36. Cosgrove, M. S. & Wolberger, C. How does the histone code work? Biochem. Cell Biol. 83, 468-476 (2005).
37. Kouzarides, T. Chromatin modifications and their function. Cell 128, 693-705 (2007).
38. Li, B., Carey, M. & Workman, J. L. The role of chromatin during transcription. Cell 128, 707-719 (2007).
39. Lieb, J. D. & Clarke, N. D. Control of transcription through intragenic patterns of nucleosome composition. Cell 123, 1187-1190 (2005).
40. Kiyama, R. & Trifonov, E. N. What positions nucleosomes? A model. FEBS Lett. 523, 7-11 (2002).
41. Kornberg, R. D. Chromatin structure: a repeating unit of histones and DNA. Science 184, 868-871 (1974).
42. Ioshikhes, I. P., Albert, I., Zanton, S. J. & Pugh, B. F. Nucleosome positions predicted through comparative genomics. Nature Genet. 38, 1210-1215 (2006).
43. Rando, O. J. & Ahmad, K. Rules and regulation in the primary structure of chromatin. Curr. Opin. Cell Biol. 19, 250-256 (2007).
44. Gupta, S. et al. Predicting human nucleosome occupancy from primary sequence. PLoS Comput. Biol. 4, e1000134 (2008).
45. Satchwell, S. C., Drew, H. R. & Travers, A. A. Sequence periodicities in chicken nucleosome core DNA. J. Mol. Biol. 191, 659-675 (1986).
46. Segal, E. et al. A genomic code for nucleosome positioning. Nature 442, 772-778 (2006). Together with Reference 42, this study provides evidence that at least some genomic sequences favour nucleosome assembly, which can be used to approximately predict nucleosome positions.
47. Wang, J. P. & Widom, J. Improved alignment of nucleosome DNA sequences using a mixture model. Nucleic Acids Res. 33, 6743-6755 (2005).
48. Miele, V., Vaillant, C., d'Aubenton-Carafa, Y., Thermes, C. & Grange, T. DNA physical properties determine nucleosome occupancy from yeast to fly. Nucleic Acids Res. 36, 3746-3756 (2008).
49. Peckham, H. E. et al. Nucleosome positioning signals in genomic DNA. Genome Res. 17, 1170-1177 (2007).
50. Trifonov, E. N. Sequence-dependent deformational anisotropy of chromatin DNA. Nucleic Acids Res. 8, 4041-4053 (1980).
51. Widom, J. Role of DNA sequence in nucleosome stability and dynamics. Q. Rev. Biophys. 34, 269-324 (2001).
52. Wang, J. P. et al. Preferentially quantized linker DNA lengths in Saccharomyces cerevisiae. PLoS Comput. Biol. 4, e1000175 (2008).
53. Field, Y. et al. Distinct modes of regulation by chromatin encoded through nucleosome positioning signals. PLoS Comput. Biol. 4, e1000216 (2008).
54. Yuan, G. C. & Liu, J. S. Genomic sequence is highly predictive of local nucleosome depletion. PLoS Comput. Biol. 4, e13 (2008).
55. Whitehouse, I., Rando, O. J., Delrow, J. & Tsukiyama, T. Chromatin remodelling at promoters suppresses antisense transcription. Nature 450, 1031-1035 (2007).
56. Whitehouse, I. & Tsukiyama, T. Antagonistic forces that position nucleosomes in vivo. Nature Struct. Mol. Biol. 13, 633-640 (2006).
57. Radwan, A., Younis, A., Luykx, P. & Khuri, S. Prediction and analysis of nucleosome exclusion regions in the human genome. BMC Genomics 9, 186 (2008).
58. Iyer, V. & Struhl, K. Poly(dA:dT), a ubiquitous promoter element that stimulates transcription via its intrinsic DNA structure. EMBO J. 14, 2570-2579 (1995).
59. Anderson, J. D. & Widom, J. Poly(dA-dT) promoter elements increase the equilibrium accessibility of nucleosomal DNA target sites. Mol. Cell. Biol. 21, 3830-3839 (2001).
60. Nelson, H. C., Finch, J. T., Luisi, B. F. & Klug, A. The structure of an oligo(dA).oligo(dT) tract and its biological implications. Nature 330, 221-226 (1987).
61. Struhl, K. Naturally occurring poly(dA-dT) sequences are upstream promoter elements for constitutive transcription in yeast. Proc. Natl Acad. Sci. USA 82, 8419-8423 (1985).
62. Raisner, R. M. et al. Histone variant H2A.Z marks the 5? ends of both active and inactive genes in euchromatin. Cell 123, 233-248 (2005).
63. Mito, Y., Henikoff, J. G. & Henikoff, S. Genome-scale profiling of histone H3.3 replacement patterns. Nature Genet. 37, 1090-1097 (2005).
64. Arigo, J. T., Eyler, D. E., Carroll, K. L. & Corden, J. L. Termination of cryptic unstable transcripts is directed by yeast RNA-binding proteins Nrd1 and Nab3. Mol. Cell 23, 841-851 (2006).
65. Thiebaut, M., Kisseleva-Romanova, E., Rouge-maille, M., Boulay, J. & Libri, D. Transcription termination and nuclear degradation of cryptic unstable transcripts: a role for the Nrd1-Nab3 pathway in genome surveillance. Mol. Cell 23, 853-864 (2006).
66. Thompson, D. M. & Parker, R. Cytoplasmic decay of intergenic transcripts in Saccharomyces cerevisiae. Mol. Cell. Biol. 27, 92-101 (2007).
67. Petesch, S. J. & Lis, J. T. Rapid, transcription-independent loss of nucleosomes over a large chromatin domain at Hsp70 loci. Cell 134, 74-84 (2008).
68. Venters, B. J. & Pugh, B. F. A canonical promoter organization of the transcription machinery and its regulators in the Saccharomyces genome. Genome Res. 5 Jan 2009 (doi:10.1101/gr.084970.108).
69. Juven-Gershon, T., Hsu, J. Y., Theisen, J. W. & Kadonaga, J. T. The RNA polymerase II core promoter - the gateway to transcription. Curr. Opin. Cell Biol. 20, 253-259 (2008).
70. Smale, S. T. & Kadonaga, J. T. The RNA polymerase II core promoter. Annu. Rev. Biochem. 72, 449-479 (2003).
71. Thomas, M. C. & Chiang, C. M. The general transcription machinery and general cofactors. Crit. Rev. Biochem. Mol. Biol. 41, 105-178 (2006).
72. David, L. et al. A high-resolution map of transcription in the yeast genome. Proc. Natl Acad. Sci. USA 103, 5320-5325 (2006).
73. Zhang, Z. & Dietrich, F. S. Mapping of transcription start sites in Saccharomyces cerevisiae using 5′ SAGE. Nucleic Acids Res. 33, 2838-2851 (2005).
74. Kuehner, J. N. & Brow, D. A. Quantitative analysis of in vivo initiator selection by yeast RNA polymerase II supports a scanning model. J. Biol. Chem. 281, 14119-14128 (2006).
75. Hassan, A. H. et al. Function and selectivity of bromodomains in anchoring chromatin-modifying complexes to promoter nucleosomes. Cell 111, 369-379 (2002).
76. Jacobson, R. H., Ladurner, A. G., King, D. S. & Tjian, R. Structure and function of a human TAF(II)250 double bromodomain module. Science 288, 1422-1425 (2000).
77. Matangkasombut, O., Buratowski, R. M., Swilling, N. W. & Buratowski, S. Bromodomain factor 1 corresponds to a missing piece of yeast TFIID. Genes Dev. 14, 951-962 (2000).
78. Vermeulen, M. et al. Selective anchoring of TFIID to nucleosomes by trimethylation of histone H3 lysine 4. Cell 131, 58-69 (2007).
79. Pugh, B. F. & Tjian, R. Mechanism of transcriptional activation by Sp1: evidence for coactivators. Cell 61, 1187-1197 (1990).
80. Sermwittayawong, D. & Tan, S. SAGA binds TBP via its Spt8 subunit in competition with DNA: implications for TBP recruitment. EMBO J. 25, 3791-3800 (2006).
81. Nikolov, D. B. et al. Crystal structure of a TFIIB-TBP-TATA- element ternary complex. Nature 377, 119-128 (1995).
82. Hausner, W., Wettach, J., Hethke, C. & Thomm, M. Two transcription factors related with the eucaryal transcription factors TATA-binding protein and transcription factor IIB direct promoter recognition by an archaeal RNA polymerase. J. Biol. Chem. 271, 30144-30148 (1996).
83. Bushnell, D. A., Westover, K. D., Davis, R. E. & Kornberg, R. D. Structural basis of transcription: an RNA polymerase II-TFIIB cocrystal at 4.5 Angstroms. Science 303, 983-988 (2004).
84. Pardee, T. S., Bangur, C. S. & Ponticelli, A. S. The N-terminal region of yeast TFIIB contains two adjacent functional domains involved in stable RNA polymerase II binding and transcription start site selection. J. Biol. Chem. 273, 17859-17864 (1998).
85. Ghazy, M. A., Brodie, S. A., Ammerman, M. L., Ziegler, L. M. & Ponticelli, A. S. Amino acid substitutions in yeast TFIIF confer upstream shifts in transcription initiation and altered interaction with RNA polymerase II. Mol. Cell. Biol. 24, 10975-10985 (2004).
86. Li, Y., Flanagan, P. M., Tschochner, H. & Kornberg, R. D. RNA polymerase II initiation factor interactions and transcription start site selection. Science 263, 805-807 (1994).
87. Geiduschek, E. P. & Kassavetis, G. A. The RNA polymerase III transcription apparatus. J. Mol. Biol. 310, 1-26 (2001).
88. Giardina, C. & Lis, J. T. DNA melting on yeast RNA polymerase II promoters. Science 261, 759-762 (1993).
89. Muse, G. W. et al. RNA polymerase is poised for activation across the genome. Nature Genet. 39, 1507-1511 (2007).
90. Zeitlinger, J. et al. RNA polymerase stalling at developmental control genes in the Drosophila melanogaster embryo. Nature Genet. 39, 1512-1516 (2007).
91. Guenther, M. G., Levine, S. S., Boyer, L. A., Jaenisch, R. & Young, R. A. A chromatin landmark and transcription initiation at most promoters in human cells. Cell 130, 77-88 (2007). This study showed that most genes in human embryonic stem cells seem to have a stalled RNA polymerase II at their 5′ ends (although such sites might actually have low occupancy levels).
92. Polach, K. J. & Widom, J. Mechanism of protein access to specific DNA sequences in chromatin: a dynamic equilibrium model for gene regulation. J. Mol. Biol. 254, 130-149 (1995).
93. Polach, K. J. & Widom, J. A model for the cooperative binding of eukaryotic regulatory proteins to nucleosomal target sites. J. Mol. Biol. 258, 800-812 (1996).
94. Anderson, J. D. & Widom, J. Sequence and position-dependence of the equilibrium accessibility of nucleosomal DNA target sites. J. Mol. Biol. 296, 979-987 (2000).
95. Adams, C. C. & Workman, J. L. Binding of disparate transcriptional activators to nucleosomal DNA is inherently cooperative. Mol. Cell. Biol. 15, 1405-1421 (1995).
96. Smith, C. L. & Peterson, C. L. ATP-dependent chromatin remodeling. Curr. Top. Dev. Biol. 65, 115-148 (2005).
97. Eisen, J. A., Sweder, K. S. & Hanawalt, P. C. Evolution of the SNF2 family of proteins: subfamilies with distinct sequences and functions. Nucleic Acids Res. 23, 2715-2723 (1995).
98. Cairns, B. R. Chromatin remodeling complexes: strength in diversity, precision through specialization. Curr. Opin. Genet. Dev. 15, 185-190 (2005).
99. Gutierrez, J. L., Chandy, M., Carrozza, M. J. & Workman, J. L. Activation domains drive nucleosome eviction by SWI/SNF. EMBO J. 26, 730-740 (2007).
100. Kobor, M. S. et al. A protein complex containing the conserved Swi2/Snf2-related ATPase Swr1p deposits histone variant H2A.Z into euchromatin. PLoS Biol. 2, e131 (2004).
101. Mizuguchi, G. et al. ATP-driven exchange of histone H2AZ variant catalyzed by SWR1 chromatin remodeling complex. Science 303, 343-348 (2004).
102. Krogan, N. J. et al. A Snf2 family ATPase complex required for recruitment of the histone H2A variant Htz1. Mol. Cell 12, 1565-1576 (2003).
103. Konev, A. Y. et al. CHD1 motor protein is required for deposition of histone variant H3.3 into chromatin in vivo. Science 317, 1087-1090 (2007).
104. Martinez-Campa, C. et al. Precise nucleosome positioning and the TATA box dictate requirements for the histone H4 tail and the bromodomain factor Bdf1. Mol. Cell 15, 69-81 (2004).
105. Lomvardas, S. & Thanos, D. Nucleosome sliding via TBP DNA binding in vivo. Cell 106, 685-696 (2001).
106. Kwon, H., Imbalzano, A. N., Khavari, P. A., Kingston, R. E. & Green, M. R. Nucleosome disruption and enhancement of activator binding by a human SW1/SNF complex. Nature 370, 477-481 (1994).
107. Cote, J., Peterson, C. L. & Workman, J. L. Perturbation of nucleosome core structure by the SWI/SNF complex persists after its detachment, enhancing subsequent transcription factor binding. Proc. Natl Acad. Sci. USA 95, 4947-4952 (1998).
108. Burns, L. G. & Peterson, C. L. The yeast SWI-SNF complex facilitates binding of a transcriptional activator to nucleosomal sites in vivo. Mol. Cell. Biol. 17, 4811-4819 (1997).
109. Suganuma, T. et al. ATAC is a double histone acetyltransferase complex that stimulates nucleosome sliding. Nature Struct. Mol. Biol. 15, 364-372 (2008).
110. Hassan, A. H., Neely, K. E. & Workman, J. L. Histone acetyltransferase complexes stabilize SWI/SNF binding to promoter nucleosomes. Cell 104, 817-827 (2001).
111. Dion, M. F., Altschuler, S. J., Wu, L. F. & Rando, O. J. Genomic characterization reveals a simple histone H4 acetylation code. Proc. Natl Acad. Sci. USA 102, 5501-5506 (2005).
112. Wang, X. & Hayes, J. J. 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 (2008).
113. Liu, C. L. et al. Single nucleosome mapping of histone modifications in S. cerevisiae. PLoS Biol. 3, e328 (2005). This study showed that acetylation of histones at specific residues does not elicit a specific transcriptional response, indicating that acetylation might have cumulative effects rather than being encoded.
114. Pokholok, D. K. et al. Genome-wide map of nucleosome acetylation and methylation in yeast. Cell 122, 517-527 (2005).
115. Shahbazian, M. D. & Grunstein, M. Functions of site-specific histone acetylation and deacetylation. Annu. Rev. Biochem. 76, 75-100 (2007).
116. Santisteban, M. S., Kalashnikova, T. & Smith, M. M. Histone H2A.Z regulates transcription and is partially redundant with nucleosome remodeling complexes. Cell 103, 411-422 (2000).
117. Hogan, G. J., Lee, C. K. & Lieb, J. D. Cell cycle-specified fluctuation of nucleosome occupancy at gene promoters. PLoS Genet. 2, e158 (2006).
118. Boeger, H., Griesenbeck, J., Strattan, J. S. & Kornberg, R. D. Removal of promoter nucleosomes by disassembly rather than sliding in vivo. Mol. Cell 14, 667-673 (2004).
119. Korber, P., Luckenbach, T., Blaschke, D. & Horz, W. Evidence for histone eviction in trans upon induction of the yeast PHO5 promoter. Mol. Cell. Biol. 24, 10965-10974 (2004).
120. Reinke, H. & Horz, W. Histones are first hyperacetylated and then lose contact with the activated PHO5 promoter. Mol. Cell 11, 1599-1607 (2003).
121. Adkins, M. W., Howar, S. R. & Tyler, J. K. Chromatin disassembly mediated by the histone chaperone Asf1 is essential for transcriptional activation of the yeast PHO5 and PHO8 genes. Mol. Cell 14, 657-666 (2004).
122. Moreira, J. M. & Holmberg, S. Transcriptional repression of the yeast CHA1 gene requires the chromatin-remodeling complex RSC. EMBO J. 18, 2836-2844 (1999).
123. Zhao, J., Herrera-Diaz, J. & Gross, D. S. Domain-wide displacement of histones by activated heat shock factor occurs independently of Swi/Snf and is not correlated with RNA polymerase II density. Mol. Cell. Biol. 25, 8985-8999 (2005).
124. Zhang, H. & Reese, J. C. Exposing the core promoter is sufficient to activate transcription and alter coactivator requirement at RNR3. Proc. Natl Acad. Sci. USA 104, 8833-8838 (2007).
125. Almer, A., Rudolph, H., Hinnen, A. & Horz, W. Removal of positioned nucleosomes from the yeast PHO5 promoter upon PHO5 induction releases additional upstream activating DNA elements. EMBO J. 5, 2689-2696 (1986).
126. Cartwright, I. L. & Elgin, S. C. Nucleosomal instability and induction of new upstream protein-DNA associations accompany activation of four small heat shock protein genes in Drosophila melanogaster. Mol. Cell. Biol. 6, 779-791 (1986).
127. Armstrong, J. A. & Emerson, B. M. NF-E2 disrupts chromatin structure at human βlocus control region hypersensitive site 2 in vitro. Mol. Cell. Biol. 16, 5634-5644 (1996).
128. Bu, P., Evrard, Y. A., Lozano, G. & Dent, S. Y. Loss of Gcn5 acetyltransferase activity leads to neural tube closure defects and exencephaly in mouse embryos. Mol. Cell. Biol. 27, 3405-3416 (2007).
129. Shilatifard, A. Chromatin modifications by methylation and ubiquitination: implications in the regulation of gene expression. Annu. Rev. Biochem. 75, 243-269 (2006).
130. Whittle, C. M. et al. The genomic distribution and function of histone variant HTZ-1 during C. elegans embryogenesis. PLoS Genet. 4, e1000187 (2008).
131. Davey, C. A., Sargent, D. F., Luger, K., Maeder, A. W. & Richmond, T. J. Solvent mediated interactions in the structure of the nucleosome core particle at 1.9 Å resolution. J. Mol. Biol. 319, 1097-1113 (2002).