Genome-wide profiling of nucleosome sensitivity and chromatin accessibility in Drosophila melanogaster

Nucleic Acids Research

Volumn 44, Issue 3, 2016, Pages 1036-1051

  Chereji, Řazvan V ^a   Kan, Tsung Wai ^b   Grudniewska, Magda K ^c   Romashchenko, Alexander V ^d   Berezikov, Eugene ^c   Zhimulev, Igor F ^e   Guryev, Victor ^c   Morozov, Alexandre V ^f   Moshkin, Yuri M ^b,d,e  

^a EUNICE KENNEDY SHRIVER NATIONAL INSTITUTE OF CHILD HEALTH AND HUMAN DEVELOPMENT   (United States)

^b ERASMUS MEDICAL CENTER   (Netherlands)

^c UNIVERSITY MEDICAL CENTER GRONINGEN   (Netherlands)

^d INSTITUTE OF CYTOLOGY AND GENETICS   (Russian Federation)

^e INSTITUTE OF MOLECULAR AND CELLULAR BIOLOGY   (Russian Federation)

^f RUTGERS UNIVERSITY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

DINUCLEOTIDE; MICROCOCCAL NUCLEASE; CHROMATIN; NUCLEOSOME;

ANIMAL CELL; ANIMAL TISSUE; ARTICLE; AT RICH SEQUENCE; CELL ENERGY; CHROMATIN; CONTROLLED STUDY; DROSOPHILA MELANOGASTER; EMBRYO; ENHANCER REGION; ENZYME ACTIVITY; GENE ACTIVITY; GENOME; MOLECULAR INTERACTION; MOLECULAR STABILITY; NONHUMAN; NUCLEOSOME; PRIORITY JOURNAL; TEMPERATURE; TRANSCRIPTION INITIATION SITE; ANIMAL; CHROMATIN IMMUNOPRECIPITATION; EMBRYOLOGY; GENE EXPRESSION PROFILING; GENETICS; METABOLISM;

ANIMALS; CHROMATIN; CHROMATIN IMMUNOPRECIPITATION; DROSOPHILA MELANOGASTER; GENE EXPRESSION PROFILING; GENOME; NUCLEOSOMES;

EID: 84965027284     PISSN: 03051048     EISSN: 13624962     Source Type: Journal    
DOI: 10.1093/nar/gkv978     Document Type: Article

References (72)

1. Luger, K., Mader, A.W., Richmond, R.K., Sargent, D.F. and Richmond, T.J. (1997) Crystal structure of the nucleosome core particle at 2.8 A resolution. Nature, 389, 251-260.
2. Lee, W., Tillo, D., Bray, N., Morse, R.H., Davis, R.W., Hughes, T.R. and Nislow, C. (2007) A high-resolution atlas of nucleosome occupancy in yeast. Nat. Genet., 39, 1235-1244.
3. van Holde, K.E. (1988) Chromatin. Springer-Verlag, NY.
4. Schalch, T., Duda, S., Sargent, D.F. and Richmond, T.J. (2005) X-ray structure of a tetranucleosome and its implications for the chromatin fibre. Nature, 436, 138-141.
5. Dorigo, B., Schalch, T., Kulangara, A., Duda, S., Schroeder, R.R. and Richmond, T.J. (2004) Nucleosome arrays reveal the two-start organization of the chromatin fiber. Science, 306, 1571-1573.
6. Li, G. and Reinberg, D. (2011) Chromatin higher-order structures and gene regulation. Curr. Opin. Genet. Dev., 21, 175-186.
7. Song, F., Chen, P., Sun, D., Wang, M., Dong, L., Liang, D., Xu, R.M., Zhu, P. and Li, G. (2014) Cryo-EM study of the chromatin fiber reveals a double helix twisted by tetranucleosomal units. Science, 344, 376-380.
8. Teves, S.S., Weber, C.M. and Henikoff, S. (2014) Transcribing through the nucleosome. Trends Biochem. Sci., 39, 577-586.
9. Studitsky, V.M., Walter, W., Kireeva, M., Kashlev, M. and Felsenfeld, G. (2004) Chromatin remodeling by RNA polymerases. Trends Biochem. Sci., 29, 127-135.
10. Becker, P.B. and Workman, J.L. (2013) Nucleosome remodeling and epigenetics. Cold Spring Harb. Perspect. Biol., 5, doi:10.1101/cshperspect.a017905.
11. Peterson, C.L. and Almouzni, G. (2013) Nucleosome dynamics as modular systems that integrate DNA damage and repair. Cold Spring Harb. Perspect. Biol., 5, doi:10.1101/cshperspect.a012658.
12. Cairns, B.R. (2009) The logic of chromatin architecture and remodelling at promoters. Nature, 461, 193-198.
13. Bassett, A., Cooper, S., Wu, C. and Travers, A. (2009) The folding and unfolding of eukaryotic chromatin. Curr. Opin. Genet. Dev., 19, 159-165.
14. Hughes, A.L. and Rando, O.J. (2014) Mechanisms underlying nucleosome positioning in vivo. Annu. Rev. Biophys., 43, 41-63.
15. Moshkin, Y.M., Chalkley, G.E., Kan, T.W., Reddy, B.A., Ozgur, Z., van Ijcken, W.F., Dekkers, D.H., Demmers, J.A., Travers, A.A. and Verrijzer, C.P. (2012) Remodelers organize cellular chromatin by counteracting intrinsic histone-DNA sequence preferences in a class-specific manner. Mol. Cell. Biol., 32, 675-688.
16. Struhl, K. and Segal, E. (2013) Determinants of nucleosome positioning. Nat. Struct. Mol. Biol., 20, 267-273.
17. Zhang, Z., Wippo, C.J., Wal, M., Ward, E., Korber, P. and Pugh, B.F. (2011) A packing mechanism for nucleosome organization reconstituted across a eukaryotic genome. Science, 332, 977-980.
18. Gkikopoulos, T., Schofield, P., Singh, V., Pinskaya, M., Mellor, J., Smolle, M., Workman, J.L., Barton, G.J. and Owen-Hughes, T. (2011) A role for Snf2-related nucleosome-spacing enzymes in genome-wide nucleosome organization. Science, 333, 1758-1760.
19. Valouev, A., Johnson, S.M., Boyd, S.D., Smith, C.L., Fire, A.Z. and Sidow, A. (2011) Determinants of nucleosome organization in primary human cells. Nature, 474, 516-520.
20. Teif, V.B., Vainshtein, Y., Caudron-Herger, M., Mallm, J.P., Marth, C., Hofer, T. and Rippe, K. (2012) Genome-wide nucleosome positioning during embryonic stem cell development. Nat. Struct. Mol. Biol., 19, 1185-1192.
21. Kaplan, N., Moore, I.K., Fondufe-Mittendorf, Y., Gossett, A.J., Tillo, D., Field, Y., LeProust, E.M., Hughes, T.R., Lieb, J.D., Widom, J. et al. (2009) The DNA-encoded nucleosome organization of a eukaryotic genome. Nature, 458, 362-366.
22. Locke, G., Tolkunov, D., Moqtaderi, Z., Struhl, K. and Morozov, A.V. (2010) High- Throughput sequencing reveals a simple model of nucleosome energetics. Proc. Natl. Acad. Sci. U.S.A., 107, 20998-21003.
23. Ioshikhes, I.P., Albert, I., Zanton, S.J. and Pugh, B.F. (2006) Nucleosome positions predicted through comparative genomics. Nat. Genet., 38, 1210-1215.
24. Mavrich, T.N., Ioshikhes, I.P., Venters, B.J., Jiang, C., Tomsho, L.P., Qi, J., Schuster, S.C., Albert, I. and Pugh, B.F. (2008) A barrier nucleosome model for statistical positioning of nucleosomes throughout the yeast genome. Genome Res., 18, 1073-1083.
25. Albert, I., Mavrich, T.N., Tomsho, L.P., Qi, J., Zanton, S.J., Schuster, S.C. and Pugh, B.F. (2007) Translational and rotational settings of H2A.Z nucleosomes across the Saccharomyces cerevisiae genome. Nature, 446, 572-576.
26. Segal, E., Fondufe-Mittendorf, Y., Chen, L., Thastrom, A., Field, Y., Moore, I.K., Wang, J.P. and Widom, J. (2006) A genomic code for nucleosome positioning. Nature, 442, 772-778.
27. Gracey, L.E., Chen, Z.Y., Maniar, J.M., Valouev, A., Sidow, A., Kay, M.A. and Fire, A.Z. (2010) An in vitro-identified high- Affinity nucleosome-positioning signal is capable of transiently positioning a nucleosome in vivo. Epigenetics Chromatin, 3, doi:10.1186/1756-8935-3-13.
28. Zhang, Y., Moqtaderi, Z., Rattner, B.P., Euskirchen, G., Snyder, M., Kadonaga, J.T., Liu, X.S. and Struhl, K. (2009) Intrinsic histone-DNA interactions are not the major determinant of nucleosome positions in vivo. Nat. Struct. Mol. Biol., 16, 847-852.
29. Erdel, F., Krug, J., Langst, G. and Rippe, K. (2011) Targeting chromatin remodelers: Signals and search mechanisms. Biochim. Biophys. Acta, 1809, 497-508.
30. Mueller-Planitz, F., Klinker, H. and Becker, P.B. (2013) Nucleosome sliding mechanisms: New twists in a looped history. Nat. Struct. Mol. Biol., 20, 1026-1032.
31. Ganguli, D., Chereji, R.V., Iben, J.R., Cole, H.A. and Clark, D.J. (2014) RSC-dependent constructive and destructive interference between opposing arrays of phased nucleosomes in yeast. Genome Res., 24, 1637-1649.
32. Chereji, R.V., Tolkunov, D., Locke, G. and Morozov, A.V. (2011) Statistical mechanics of nucleosome ordering by chromatin-structure-induced two-body interactions. Phys. Rev. E Stat. Nonlin. Soft Matter Phys., 83, doi:10.1103/PhysRevE.83.050903.
33. Chereji, R.V. and Morozov, A.V. (2011) Statistical Mechanics of Nucleosomes Constrained by Higher-Order Chromatin Structure. J. Stat. Phys., 144, 379-404.
34. Rube, H.T. and Song, J.S. (2014) Quantifying the role of steric constraints in nucleosome positioning. Nucleic Acids Res., 42, 2147-2158.
35. Cole, H.A., Howard, B.H. and Clark, D.J. (2012) Genome-wide mapping of nucleosomes in yeast using paired-end sequencing. Methods Enzymol., 513, 145-168.
36. Zentner, G.E. and Henikoff, S. (2014) High-resolution digital profiling of the epigenome. Nat. Rev. Genet., 15, 814-827.
37. Moyle-Heyrman, G., Zaichuk, T., Xi, L., Zhang, Q., Uhlenbeck, O.C., Holmgren, R., Widom, J. and Wang, J.P. (2013) Chemical map of Schizosaccharomyces pombe reveals species-specific features in nucleosome positioning. Proc. Natl. Acad. Sci. U.S.A., 110, 20158-20163.
38. Brogaard, K., Xi, L., Wang, J.P. and Widom, J. (2012) A map of nucleosome positions in yeast at base-pair resolution. Nature, 486, 496-501.
39. Chereji, R.V. and Morozov, A.V. (2014) Ubiquitous nucleosome crowding in the yeast genome. Proc. Natl. Acad. Sci. U.S.A., 111, 5236-5241.
40. Henikoff, S., Ramachandran, S., Krassovsky, K., Bryson, T.D., Codomo, C.A., Brogaard, K., Widom, J., Wang, J.P. and Henikoff, J.G. (2014) The budding yeast Centromere DNA Element II wraps a stable Cse4 hemisome in either orientation in vivo. Elife, 3, e01861.
41. Flaus, A., Luger, K., Tan, S. and Richmond, T.J. (1996) Mapping nucleosome position at single base-pair resolution by using site-directed hydroxyl radicals. Proc. Natl. Acad. Sci. U.S.A., 93, 1370-1375.
42. Bryant, G.O., Prabhu, V., Floer, M., Wang, X., Spagna, D., Schreiber, D. and Ptashne, M. (2008) Activator control of nucleosome occupancy in activation and repression of transcription. PLoS Biol., 6, 2928-2939.
43. Xi, Y., Yao, J., Chen, R., Li, W. and He, X. (2011) Nucleosome fragility reveals novel functional states of chromatin and poises genes for activation. Genome Res., 21, 718-724.
44. Knight, B., Kubik, S., Ghosh, B., Bruzzone, M.J., Geertz, M., Martin, V., Denervaud, N., Jacquet, P., Ozkan, B., Rougemont, J. et al. (2014) Two distinct promoter architectures centered on dynamic nucleosomes control ribosomal protein gene transcription. Genes Dev., 28, 1695-1709.
45. Teif, V.B., Beshnova, D.A., Vainshtein, Y., Marth, C., Mallm, J.P., Hofer, T. and Rippe, K. (2014) Nucleosome repositioning links DNA (de)methylation and differential CTCF binding during stem cell development. Genome Res., 24, 1285-1295.
46. Weiner, A., Hughes, A., Yassour, M., Rando, O.J. and Friedman, N. (2010) High-resolution nucleosome mapping reveals transcription-dependent promoter packaging. Genome Res., 20, 90-100.
47. Beshnova, D.A., Cherstvy, A.G., Vainshtein, Y. and Teif, V.B. (2014) Regulation of the nucleosome repeat length in vivo by the DNA sequence, protein concentrations and long-range interactions. PLoS Comput. Biol., 10, e1003698.
48. Mobius, W., Osberg, B., Tsankov, A.M., Rando, O.J. and Gerland, U. (2013) Toward a unified physical model of nucleosome patterns flanking transcription start sites. Proc. Natl. Acad. Sci. U.S.A., 110, 5719-5724.
49. Chevereau, G., Palmeira, L., Thermes, C., Arneodo, A. and Vaillant, C. (2009) Thermodynamics of intragenic nucleosome ordering. Phys. Rev. Lett., 103, doi:10.1103/PhysRevLett.103.188103.
50. Milani, P., Chevereau, G., Vaillant, C., Audit, B., Haftek-Terreau, Z., Marilley, M., Bouvet, P., Argoul, F. and Arneodo, A. (2009) Nucleosome positioning by genomic excluding-energy barriers. Proc. Natl. Acad. Sci. U.S.A., 106, 22257-22262.
51. Kulic, I.M. and Schiessel, H. (2003) Nucleosome repositioning via loop formation. Biophys. J., 84, 3197-3211.
52. Woodcock, C.L., Grigoryev, S.A., Horowitz, R.A. and Whitaker, N. (1993) A chromatin folding model that incorporates linker variability generates fibers resembling the native structures. Proc. Natl. Acad. Sci. U.S.A., 90, 9021-9025.
53. Tillo, D. and Hughes, T.R. (2009) G+C content dominates intrinsic nucleosome occupancy. BMC Bioinformatics, 10, doi:10.1186/1471-2105-10-442.
54. Chung, H.R., Dunkel, I., Heise, F., Linke, C., Krobitsch, S., Ehrenhofer-Murray, A.E., Sperling, S.R. and Vingron, M. (2010) The effect of micrococcal nuclease digestion on nucleosome positioning data. Plos One, 5, e15754.
55. Deal, R.B., Henikoff, J.G. and Henikoff, S. (2010) Genome-wide kinetics of nucleosome turnover determined by metabolic labeling of histones. Science, 328, 1161-1164.
56. Teves, S.S. and Henikoff, S. (2014) Transcription-generated torsional stress destabilizes nucleosomes. Nat. Struct. Mol. Biol., 21, 88-94.
57. Core, L.J., Waterfall, J.J., Gilchrist, D.A., Fargo, D.C., Kwak, H., Adelman, K. and Lis, J.T. (2012) Defining the status of RNA polymerase at promoters. Cell Reports, 2, 1025-1035.
58. Kornberg, R.D. and Stryer, L. (1988) Statistical distributions of nucleosomes: Nonrandom locations by a stochastic mechanism. Nucleic Acids Res., 16, 6677-6690.
59. Percus, J.K. (1976) Equilibrium State of a Classical Fluid of Hard Rods in an External Field. J. Stat. Phys., 15, 505-511.
60. Chereji, R.V. and Morozov, A.V. (2015) Functional roles of nucleosome stability and dynamics. Brief Funct. Genomics, 14, 50-60.
61. Kulic, I.M. and Schiessel, H. (2003) Chromatin dynamics: Nucleosomes go mobile through twist defects. Phys. Rev. Lett., 91, 148103.
62. Schiessel, H. (2003) The physics of chromatin. J. Phys.-Condensed Matter, 15, R699-R774.
63. Adams, C.C. and Workman, J.L. (1995) Binding of disparate transcriptional activators to nucleosomal DNA is inherently cooperative. Mol. Cell. Biol., 15, 1405-1421.
64. Anderson, J.D., Thastrom, A. and Widom, J. (2002) Spontaneous access of proteins to buried nucleosomal DNA target sites occurs via a mechanism that is distinct from nucleosome translocation. Mol. Cell. Biol., 22, 7147-7157.
65. Felsenfeld, G. and Groudine, M. (2003) Controlling the double helix. Nature, 421, 448-453.
66. Deniz, O., Flores, O., Battistini, F., Perez, A., Soler-Lopez, M. and Orozco, M. (2011) Physical properties of naked DNA influence nucleosome positioning and correlate with transcription start and termination sites in yeast. BMC Genomics, 12, doi:10.1186/1471-2164-12-489.
67. Audit, B., Zaghloul, L., Vaillant, C., Chevereau, G., d'Aubenton-Carafa, Y., Thermes, C. and Arneodo, A. (2009) Open chromatin encoded in DNA sequence is the signature of 'master' replication origins in human cells. Nucleic Acids Res., 37, 6064-6075.
68. Tolkunov, D., Zawadzki, K.A., Singer, C., Elfving, N., Morozov, A.V. and Broach, J.R. (2011) Chromatin remodelers clear nucleosomes from intrinsically unfavorable sites to establish nucleosome-depleted regions at promoters. Mol. Biol. Cell, 22, 2106-2118.
69. Jiang, C. and Pugh, B.F. (2009) Nucleosome positioning and gene regulation: Advances through genomics. Nat. Rev. Genet., 10, 161-172.
70. Flores, O., Deniz, O., Soler-Lopez, M. and Orozco, M. (2014) Fuzziness and noise in nucleosomal architecture. Nucleic Acids Res., 42, 4934-4946.
71. Gerstein, M.B., Rozowsky, J., Yan, K.K., Wang, D., Cheng, C., Brown, J.B., Davis, C.A., Hillier, L., Sisu, C., Li, J.J. et al. (2014) Comparative analysis of the transcriptome across distant species. Nature, 512, 445-448.
72. Kvon, E.Z., Kazmar, T., Stampfel, G., Yanez-Cuna, J.O., Pagani, M., Schernhuber, K., Dickson, B.J. and Stark, A. (2014) Genome-scale functional characterization of Drosophila developmental enhancers in vivo. Nature, 512, 91-95.