Effects of DNA methylation on nucleosome stability

Nucleic Acids Research

Volumn 41, Issue 5, 2013, Pages 2918-2931

  Collings, Clayton K ^a   Waddell, Peter J ^a   Anderson, John N ^a  

^a PURDUE UNIVERSITY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

DNA; HISTONE;

ARTICLE; CONTROLLED STUDY; CPG ISLAND; DNA METHYLATION; DNA SEQUENCE; EPIGENETICS; EXON; HIGH THROUGHPUT SEQUENCING; HUMAN; IN VITRO STUDY; INTRON; MOUSE; NONHUMAN; NUCLEOSOME; PRIORITY JOURNAL; TRANSCRIPTION INITIATION SITE;

CHROMOSOMES, ARTIFICIAL, BACTERIAL; CPG ISLANDS; DNA METHYLATION; EPIGENESIS, GENETIC; EXONS; HUMANS; INTRONS; ISOCHORES; NUCLEOSOMES; PROTEIN BINDING; TRANSCRIPTION INITIATION SITE;

VERTEBRATA;

EID: 84876389811     PISSN: 03051048     EISSN: 13624962     Source Type: Journal    
DOI: 10.1093/nar/gks893     Document Type: Article

References (74)

1. Jones, P. and Baylin, S. (2007) The epigenomics of cancer. Cell, 128, 683-692.
2. Feil, R. (2009) Epigenetics: ready for the marks. Nature, 461, 359-360.
3. Lee, J. (2011) Gracefully ageing at 50, X-chromosome inactivation becomes a paradigm for RNA and chromatin control. Nat. Rev. Mol. Cell Biol., 12, 815-826.
4. Cedar, H. and Bergman, Y. (2009) Linking DNA methylation and histone modification: patterns and paradigms. Nat. Rev. Genet., 10, 295-304.
5. Bird, A. (2011) The Dinucleotide CG as a Genomic Signalling Module. J. Mol. Biol., 409, 47-53.
6. Deaton, A. and Bird, A. (2011) CpG islands and the regulation of transcription. Gene. Dev., 25, 1010-1022.
7. Cedar, H. and Bergman, Y. (2012) Programming of DNA methylation patterns. Annu. Rev. Biochem., 81, 97-117.
8. Lienert, F., Wirbelauer, C., Som, I., Dean, A., Mohn, F. and Schubeler, D. (2011) Identification of genetic elements that autonomously determine DNA methylation states. Nat. Genet., 43, 1091-1097.
9. Straussman, R., Nejman, D., Roberts, D., Steinfeld, I., Blum, B., Benvenisty, N., Simon, I., Yakhini, Z. and Cedar, H. (2009) Developmental programming of CpG island methylation profiles in the human genome. Nat. Struct. Mol. Biol., 16, 564-571.
10. Hendrich, B. and Bird, A. (1998) Identification and characterization of a family of mammalian methyl-CpG binding proteins. Mol. Cell. Biol., 18, 6538-6547.
11. Guy, J., Cheval, H., Selfridge, J., Bird, A., Schekman, R., Goldstein, L. and Lehmann, R. (2011) The role of MeCP2 in the brain. Ann. Rev. Cell Dev. Biol., 27, 631-652.
12. Choy, J., Wei, S., Lee, J., Tan, S., Chu, S. and Lee, T. (2010) DNA methylation increases nucleosome compaction and rigidity. J. Am. Chem. Soc., 132, 1782-1783.
13. Lee, J. and Lee, T. (2012) Effects of DNA methylation on the structure of nucleosomes. J. Am. Chem. Soc., 134, 173-175.
14. Godde, J., Kass, S., Hirst, M. and Wolffe, A. (1996) Nucleosome assembly on methylated CGG triplet repeats in the Fragile X Mental Retardation gene 1 promoter. J. Biol. Chem., 271, 24325-24328.
15. Wang, Y. (2007) Chromatin structure of repeating CTG/CAG and CGG/CCG sequences in human disease. Front. Biosci., 12, 4731-4741.
16. Davey, C., Pennings, S. and Allan, J. (1997) CpG methylation remodels chromatin structure in vitro. J. Mol. Biol., 267, 276-288.
17. Fernandez, A.G. and Anderson, J.N. (2007) Nucleosome positioning determinants. J. Mol. Biol., 371, 649-668.
18. Fitzgerald, D.J. and Anderson, J.N. (1999) DNA distortion as a factor in nucleosome positioning. J. Mol. Biol., 293, 477-491.
19. Drew, H. and McCall, M. (1987) Structural-analysis of a reconstituted DNA containing 3 histone octamers and histone-H5. J. Mol. Biol., 197, 485-511.
20. Nightingale, K. and Wolffe, A. (1995) Methylation at CpG sequences does not influence histone-H1 binding to a nucleosome including a Xenopus-Borealis 5-S-ribosomal RNA gene. J. Biol. Chem., 270, 4197-4200.
21. Bloom, K. and Anderson, J. (1978) Fractionation and characterization of chromosomal-proteins by hydroxyapatite dissociation method. J. Biol. Chem., 253, 4446-4450.
22. Anders, S. and Huber, -W. (2010) Differential expression analysis for sequence count data. Genome Biol., 11, R106.
23. Kaplan, N., Moore, I., Fondufe-Mittendorf, Y., Gossett, A., Tillo, D., Field, Y., LeProust, E., Hughes, T., Lieb, J., Widom, J. et al. (2009) The DNA-encoded nucleosome organization of a eukaryotic genome. Nature, 458, 362-368.
24. Valouev, A., Ichikawa, J., Tonthat, T., Stuart, J., Ranade, S., Peckham, H., Zeng, K., Malek, J., Costa, G., McKernan, K. et al. (2008) A high-resolution, nucleosome position map of C. elegans reveals a lack of universal sequence-dictated positioning. Genome Res., 18, 1051-1063.
25. Chodavarapu, R., Feng, S., Bernatavichute, Y., Chen, P., Stroud, H., Yu, Y., Hetzel, J., Kuo, F., Kim, J., Cokus, S. et al. (2010) Relationship between nucleosome positioning and DNA methylation. Nature, 466, 388-392.
26. Li, Y., Zhu, J., Tian, G., Li, N., Li, Q., Ye, M., Zheng, H., Yu, J., Wu, H., Sun, J. et al. (2010) The DNA methylome of human peripheral blood mononuclear cells. PLoS Biol., 8, e1000533.
27. Langmead, B., Trapnell, C., Pop, M. and Salzberg, S.L. (2009) Ultrafast and memory-efficient alignment of short DNA sequences to the human genome. Genome Biol., 10, R25.
28. Cokus, S., Feng, S., Zhang, X., Chen, Z., Merriman, B., Haudenschild, C., Pradhan, S., Nelson, S., Pellegrini, M. and Jacobsen, S. (2008) Shotgun bisulphite sequencing of the Arabidopsis genome reveals DNA methylation patterning. Nature, 452, 215-219.
29. Kent, W., Sugnet, C., Furey, T., Roskin, K., Pringle, T., Zahler, A. and Haussler, D. (2002) The human genome browser at UCSC. Genome Res., 12, 996-1006.
30. Karolchik, D., Hinrichs, A., Furey, T., Roskin, K., Sugnet, C., Haussler, D. and Kent, W. (2004) The UCSC Table Browser data retrieval tool. Nucleic Acids Res., 32, D493-D496.
31. Wierstra, I., Alves, J., Klein, G. and VandeWoude, G. (2008) The c-myc promoter: Still (M)under-baryster(Y)under-bar and (C)under-barhallenge. Adv. Cancer Res., 99, 113-333.
32. Snykers, S., Henkens, T., De Rop, E., Vinken, M., Fraczek, J., De Kock, J., De Prins, E., Geerts, A., Rogiers, V. and Vanhaecke, T. (2009) Role of epigenetics in liver-specific gene transcription, hepatocyte differentiation and stem cell reprogrammation. J. Hepatol., 51, 187-211.
33. Saldana-Meyer, R. and Recillas-Targa, F. (2011) Transcriptional and epigenetic regulation of the p53 tumor suppressor gene. Epigenetics, 6, 1068-1077.
34. 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.
35. Kaplan, N., Moore, I., Fondufe-Mittendorf, Y., Gossett, A., Tillo, D., Field, Y., Hughes, T., Lieb, J., Widom, J. and Segal, E. (2010) Nucleosome sequence preferences influence in vivo nucleosome organization. Nat. Struct. Mol. Biol., 17, 918-920.
36. Zhang, Y., Moqtaderi, Z., Rattner, B., Euskirchen, G., Snyder, M., Kadonaga, J., Liu, X. and Struhl, K. (2010) Evidence against a genomic code for nucleosome positioning. Nat. Struct. Mol. Biol., 17, 920-923.
37. Stein, A., Takasuka, T. and Collings, C. (2010) Are nucleosome positions in vivo primarily determined by histone-DNA sequence preferences? Nucleic Acids Res., 38, 709-719.
38. Chung, H., Dunkel, I., Heise, F., Linke, C., Krobitsch, S., Ehrenhofer-Murray, A., Sperling, S. and Vingron, M. (2010) The effect of micrococcal nuclease digestion on nucleosome positioning data. PLoS ONE, 5, e15754.
39. Satchwell, S.C., Drew, H.R. and Travers, A.A. (1986) Sequence periodicities in chicken nucleosome core DNA. J. Mol. Biol., 191, 659-675.
40. Trifonov, E.N. and Sussman, J.L. (1980) The pitch of chromatin DNA is reflected in its nucleotide-sequence. Proc. Natl Acad. Sci. USA-Biol. Sci., 77, 3816-3820.
41. Collings, C., Fernandez, A., Pitschka, C., Hawkins, T. and Anderson, J. (2010) Oligonucleotide sequence motifs as nucleosome positioning signals. PLoS ONE, 5, e10933.
42. Kim, S., Hollstein, M., Pfeifer, G. and Besaratinia, A. (2010) Unveiling the methylation status of CpG dinucleotides in the substituted segment of the human p53 knock-In (Hupki) mouse genome. Mol. Carcinogen., 49, 999-1006.
43. Tornaletti, S. and Pfeifer, G. (1995) Complete and tissue-independent methylation of CpG sites in the p53 gene - implications for mutations in human cancers. Oncogene, 10, 1493-1499.
44. Cole, H., Howard, B. and Clark, D. (2011) Activation-induced disruption of nucleosome position clusters on the coding regions of Gcn4-dependent genes extends into neighbouring genes. Nucleic Acids Res., 39, 9521-9535.
45. Tillo, D. and Hughes, T.R. (2009) G plus C content dominates intrinsic nucleosome occupancy. BMC Bioinformatics, 10, 13.
46. Li, Z., Schug, J., Tuteja, G., White, P. and Kaestner, K. (2011) The nucleosome map of the mammalian liver. Nat. Struct. Mol. Biol., 18, 742-746.
47. Ramirez-Carrozzi, V., Braas, D., Bhatt, D., Cheng, C., Hong, C., Doty, K., Black, J., Hoffmann, A., Carey, M. and Smale, S. (2009) A unifying model for the selective regulation of inducible transcription by CpG islands and nucleosome remodeling. Cell, 138, 114-128.
48. Varriale, A. and Bernardi, G. (2010) Distribution of DNA methylation, CpGs, and CpG islands in human isochores. Genomics, 95, 25-28.
49. Tillo, D., Kaplan, N., Moore, I., Fondufe-Mittendorf, Y., Gossett, A., Field, Y., Lieb, J., Widom, J., Segal, E. and Hughes, T. (2010) High nucleosome occupancy is encoded at human regulatory sequences. PLoS ONE, 5, e9129.
50. Widlund, H.R., Cao, H., Simonsson, S., Magnusson, E., Simonsson, T., Nielsen, P.E., Kahn, J.D., Crothers, D.M. and Kubista, M. (1997) Identification and characterization of genomic nucleosome-positioning sequences. J. Mol. Biol., 267, 807-817.
51. Lowary, P.T. and 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.
52. Cui, F. and Zhurkin, V. (2010) Structure-based analysis of DNA sequence patterns guiding nucleosome positioning in vitro. J. Biomol. Struct. Dyn., 27, 821-841.
53. Locke, G., Tolkunov, D., Moqtaderi, Z., Struhl, K. and Morozov, A. (2010) High-throughput sequencing reveals a simple model of nucleosome energetics. Proc. Natl Acad. Sci. USA, 107, 20998-21003.
54. Allan, J., Fraser, R., Owen-Hughes, T. and Keszenman-Pereyra, D. (2012) Micrococcal nuclease does not substantially bias nucleosome mapping. J. Mol. Biol., 417, 152-164.
55. Brogaard, K., Xi, L., Wang, J. and Widom, J. (2012) A map of nucleosome positions in yeast at base-pair resolution. Nature, 486, 496-501.
56. Jiang, C.Z. and Pugh, B.F. (2009) Nucleosome positioning and gene regulation: advances through genomics. Nat. Rev. Genet., 10, 161-172.
57. Radman-Livaja, M. and Rando, O.J. (2010) Nucleosome positioning: how is it established, and why does it matter? Dev. Biol., 339, 258-266.
58. Tsankov, A., Thompson, D., Socha, A., Regev, A. and Rando, O. (2010) The role of nucleosome positioning in the evolution of gene regulation. PLoS Biol., 8, e1000414.
59. Valouev, A., Johnson, S., Boyd, S., Smith, C., Fire, A. and Sidow, A. (2011) Determinants of nucleosome organization in primary human cells. Nature, 474, 516-520.
60. Wu, C. and Travers, A. (2005) Relative affinities of DNA sequences for the histone octamer depend strongly upon both the temperature and octamer concentration. Biochemistry, 44, 14329-14334.
61. Razin, A. and Cedar, H. (1977) Distribution of 5-methylcytosine in chromatin. Proc. Natl Acad. Sci. USA, 74, 2725-2728.
62. Chandler, S., Guschin, D., Landsberger, N. and Wolffe, A. (1999) The methyl-CpG binding transcriptional repressor MeCP2 stably associates with nucleosomal DNA. Biochemistry, 38, 7008-7018.
63. Scarsdale, J., Webb, H., Ginder, G. and Williams, D. (2011) Solution structure and dynamic analysis of chicken MBD2 methyl binding domain bound to a target-methylated DNA sequence. Nucleic Acids Res., 39, 6741-6752.
64. ElHassan, M.A. and Calladine, C.R. (1997) Conformational characteristics of DNA: empirical classifications and a hypothesis for the conformational behaviour of dinucleotide steps. Phil. Trans. Roy. Soc. A Math. Phys. Eng. Sci., 355, 43-100.
65. Ong, M.S., Richmond, T.J. and Davey, C.A. (2007) DNA stretching and extreme kinking in the nucleosome core. J. Mol. Biol., 368, 1067-1074.
66. Lefebvre, A., Mauffret, O., Elantri, S., Monnot, M., Lescot, E. and Fermandjian, S. (1995) Sequence-dependent effects of CpG cytosine methylation - a joint H-1-NMR and P-31-NMR study. Eur. J. Biochem., 229, 445-454.
67. MayerJung, C., Moras, D. and Timsit, Y. (1997) Effect of cytosine methylation on DNA-DNA recognition at CpG steps. J. Mol. Biol., 270, 328-335.
68. Marcourt, L., Cordier, C., Couesnon, T. and Dodin, G. (1999) Impact of CS-cytosine methylation on the solution structure of d(GAAAACGTTTTC)(2) - An NMR and molecular modelling investigation. Eur. J. Biochem., 265, 1032-1042.
69. Oesterreich, F., Bieberstein, N. and Neugebauer, K. (2011) Pause locally, splice globally. Trends Cell Biol., 21, 328-335.
70. Rando, O. and Chang, H. (2009) Genome-wide views of chromatin structure. Ann. Rev. Biochem., 78, 245-271.
71. Zhang, Z., Wippo, C., Wal, M., Ward, E., Korber, P. and Pugh, B. (2011) A packing mechanism for nucleosome organization reconstituted across a eukaryotic genome. Science, 332, 977-980.
72. Brinkman, A.B., Gu, H., Bartels, S.J., Zhang, Y., Matarese, F., Simmer, F., Marks, H., Bock, C., Gnirke, A., Meissner, A. et al. (2012) Sequential ChIP-bisulfite sequencing enables direct genome-scale investigation of chromatin and DNA methylation cross-talk. Genome Res., 22, 1128-1138.
73. Kass, S.U., Landsberger, N. and Wolffe, A.P. (1997) DNA methylation directs a time-dependent repression of transcription initiation. Curr. Biol., 7, 157-165.
74. Keshet, I., Liemanhurwitz, J. and Cedar, H. (1986) DNA methylation affects the formation of active chromatin. Cell, 44, 535-543.