Modeling the relationship of epigenetic modifications to transcription factor binding

Nucleic Acids Research

Volumn 43, Issue 8, 2015, Pages 3873-3885

  Liu, Liang ^a   Jin, Guangxu ^a   Zhou, Xiaobo ^a  

^a WAKE FOREST SCHOOL OF MEDICINE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

TRANSCRIPTION FACTOR; HISTONE; PROTEIN BINDING;

ARTICLE; BINDING AFFINITY; CHROMATIN STRUCTURE; CONTROLLED STUDY; DNA METHYLATION; DNA SEQUENCE; EPIGENETICS; GENE LOCATION; HUMAN; HUMAN CELL; PRIORITY JOURNAL; TRANSCRIPTION INITIATION SITE; BIOLOGICAL MODEL; BIOLOGY; CELL LINE; GENETIC EPIGENESIS; HUMAN GENOME; METABOLISM;

CELL LINE; COMPUTATIONAL BIOLOGY; EPIGENESIS, GENETIC; GENOME, HUMAN; HISTONES; HUMANS; MODELS, GENETIC; PROTEIN BINDING; TRANSCRIPTION FACTORS; TRANSCRIPTION INITIATION SITE;

EID: 84930221683     PISSN: 03051048     EISSN: 13624962     Source Type: Journal    
DOI: 10.1093/nar/gkv255     Document Type: Article

References (83)

1. Matys, V., Kel-Margoulis, O.V., Fricke, E., Liebich, I., Land, S., Barre-Dirrie, A., Reuter, I., Chekmenev, D., Krull, M., Hornischer, K. et al. (2006) TRANSFAC and its module TRANSCompel: transcriptional gene regulation in eukaryotes. Nucleic Acids Res., 34, D108-D110.
2. Bryne, J.C., Valen, E., Tang, M.H., Marstrand, T., Winther, O., da Piedade, I., Krogh, A., Lenhard, B. and Sandelin, A. (2008) JASPAR, the open access database of transcription factor-binding profiles: new content and tools in the 2008 update. Nucleic Acids Res., 36, D102-D106.
3. Lupien, M., Eeckhoute, J., Meyer, C.A., Wang, Q., Zhang, Y., Li, W., Carroll, J.S., Liu, X.S. and Brown, M. (2008) FoxA1 translates epigenetic signatures into enhancer-driven lineage-specific transcription. Cell, 132, 958-970.
4. Berger, S.L. (2007) The complex language of chromatin regulation during transcription. Nature, 447, 407-412.
5. Suganuma, T. and Workman, J.L. (2008) Crosstalk among Histone Modifications. Cell, 135, 604-607.
6. Lee, J.S., Smith, E. and Shilatifard, A. (2010) The language of histone crosstalk. Cell, 142, 682-685.
7. You, J.S. and Jones, P.A. (2012) Cancer genetics and epigenetics: two sides of the same coin? Cancer Cell, 22, 9-20.
8. Esteller, M. (2007) Cancer epigenomics: DNA methylomes and histone-modification maps. Nat. Rev. Genet., 8, 286-298.
9. Fraga, M.F. and Esteller, M. (2007) Epigenetics and aging: the targets and the marks. Trends Genet., 23, 413-418.
10. Aran, D., Sabato, S. and Hellman, A. (2013) DNA methylation of distal regulatory sites characterizes dysregulation of cancer genes. Genome Biol., 14, R21.
11. Siegfried, Z., Eden, S., Mendelsohn, M., Feng, X., Tsuberi, B.Z. and Cedar, H. (1999) DNA methylation represses transcription in vivo. Nat. Genet., 22, 203-206.
12. Cheng, C., Alexander, R., Min, R., Leng, J., Yip, K.Y., Rozowsky, J., Yan, K.K., Dong, X., Djebali, S., Ruan, Y. et al. (2012) Understanding transcriptional regulation by integrative analysis of transcription factor binding data. Genome Res., 22, 1658-1667.
13. Ernst, J. and Kellis, M. (2012) ChromHMM: automating chromatin-state discovery and characterization. Nat. Methods, 9, 215-216.
14. Bernstein, B.E., Meissner, A. and Lander, E.S. (2007) The mammalian epigenome. Cell, 128, 669-681.
15. Encode. Project. Consortium. (2012) An integrated encyclopedia of DNA elements in the human genome. Nature, 489, 57-74.
16. Cheng, C. and Gerstein, M. (2012) Modeling the relative relationship of transcription factor binding and histone modifications to gene expression levels in mouse embryonic stem cells. Nucleic Acids Res., 40, 553-568.
17. Dong, X., Greven, M.C., Kundaje, A., Djebali, S., Brown, J.B., Cheng, C., Gingeras, T.R., Gerstein, M., Guigo, R., Birney, E. et al. (2012) Modeling gene expression using chromatin features in various cellular contexts. Genome Biol., 13, R53.
18. Berger, S.L. (2002) Histone modifications in transcriptional regulation. Curr. Opin. Genet. Dev., 12, 142-148.
19. Cedar, H. and Bergman, Y. (2012) Programming of DNA methylation patterns. Annu. Rev. Biochem., 81, 97-117.
20. Kouzarides, T. (2007) Chromatin modifications and their function. Cell, 128, 693-705.
21. Shogren-Knaak, M., Ishii, H., Sun, J.M., Pazin, M.J., Davie, J.R. and Peterson, C.L. (2006) Histone H4-K16 acetylation controls chromatin structure and protein interactions. Science, 311, 844-847.
22. Kornberg, R.D. and Lorch, Y. (1995) Interplay between chromatin structure and transcription. Curr. Opin. Cell Biol., 7, 371-375.
23. Hassan, A.H., Neely, K.E. and Workman, J.L. (2001) Histone acetyltransferase complexes stabilize swi/snf binding to promoter nucleosomes. Cell, 104, 817-827.
24. Li, G. and Reinberg, D. (2011) Chromatin higher-order structures and gene regulation. Curr. Opin. Genet. Dev., 21, 175-186.
25. Hubner, M.R., Eckersley-Maslin, M.A. and Spector, D.L. (2013) Chromatin organization and transcriptional regulation. Curr. Opin. Genet. Dev., 23, 89-95.
26. Zhang, Y. and Reinberg, D. (2001) Transcription regulation by histone methylation: interplay between different covalent modifications of the core histone tails. Genes Dev., 15, 2343-2360.
27. Medvedeva, Y.A., Khamis, A.M., Kulakovskiy, I.V., Ba-Alawi, W., Bhuyan, M.S., Kawaji, H., Lassmann, T., Harbers, M., Forrest, A.R., Bajic, V.B. et al. (2014) Effects of cytosine methylation on transcription factor binding sites. BMC Genomics, 15, 119.
28. Feng, W., Dong, Z., He, B. and Wang, K. (2012) Analysis method of epigenetic DNA methylation to dynamically investigate the functional activity of transcription factors in gene expression. BMC Genomics, 13, 532.
29. Deaton, A.M. and Bird, A. (2011) CpG islands and the regulation of transcription. Genes Dev., 25, 1010-1022.
30. Watt, F. and Molloy, P.L. (1988) Cytosine methylation prevents binding to DNA of a HeLa cell transcription factor required for optimal expression of the adenovirus major late promoter. Genes Dev., 2, 1136-1143.
31. Arvey, A., Agius, P., Noble, W.S. and Leslie, C. (2012) Sequence and chromatin determinants of cell-type-specific transcription factor binding. Genome Res., 22, 1723-1734.
32. Barrera, L.O., Li, Z., Smith, A.D., Arden, K.C., Cavenee, W.K., Zhang, M.Q., Green, R.D. and Ren, B. (2008) Genome-wide mapping and analysis of active promoters in mouse embryonic stem cells and adult organs. Genome Res., 18, 46-59.
33. Heintzman, N.D., Stuart, R.K., Hon, G., Fu, Y., Ching, C.W., Hawkins, R.D., Barrera, L.O., Van Calcar, S., Qu, C., Ching, K.A. et al. (2007) Distinct and predictive chromatin signatures of transcriptional promoters and enhancers in the human genome. Nat. Genet., 39, 311-318.
34. Heintzman, N.D., Hon, G.C., Hawkins, R.D., Kheradpour, P., Stark, A., Harp, L.F., Ye, Z., Lee, L.K., Stuart, R.K., Ching, C.W. et al. (2009) Histone modifications at human enhancers reflect global cell-type-specific gene expression. Nature, 459, 108-112.
35. Chen, C., Zhang, S. and Zhang, X.S. (2013) Discovery of cell-type specific regulatory elements in the human genome using differential chromatin modification analysis. Nucleic Acids Res., 41, 9230-9242.
36. Wiench, M., John, S., Baek, S., Johnson, T.A., Sung, M.H., Escobar, T., Simmons, C.A., Pearce, K.H., Biddie, S.C., Sabo, P.J. et al. (2011) DNA methylation status predicts cell type-specific enhancer activity. EMBO J., 30, 3028-3039.
37. Nie, Y., Liu, H. and Sun, X. (2013) The patterns of histone modifications in the vicinity of transcription factor binding sites in human lymphoblastoid cell lines. PLoS One, 8, e60002.
38. Koch, C.M., Andrews, R.M., Flicek, P., Dillon, S.C., Karaoz, U., Clelland, G.K., Wilcox, S., Beare, D.M., Fowler, J.C., Couttet, P. et al. (2007) The landscape of histone modifications across 1% of the human genome in five human cell lines. Genome Res., 17, 691-707.
39. Lin, J.M., Collins, P.J., Trinklein, N.D., Fu, Y., Xi, H., Myers, R.M. and Weng, Z. (2007) Transcription factor binding and modified histones in human bidirectional promoters. Genome Res., 17, 818-827.
40. Rye, M., Saetrom, P., Handstad, T. and Drablos, F. (2011) Clustered ChIP-Seq-defined transcription factor binding sites and histone modifications map distinct classes of regulatory elements. BMC Biol., 9, 80.
41. Benveniste, D., Sonntag, H.J., Sanguinetti, G. and Sproul, D. (2014) Transcription factor binding predicts histone modifications in human cell lines. Proc. Natl. Acad. Sci. U.S.A., 111, 13367-13372.
42. Hu, S., Wan, J., Su, Y., Song, Q., Zeng, Y., Nguyen, H.N., Shin, J., Cox, E., Rho, H.S., Woodard, C. et al. (2013) DNA methylation presents distinct binding sites for human transcription factors. Elife, 2, e00726.
43. Luu, P.L., Scholer, H.R. and Arauzo-Bravo, M.J. (2013) Disclosing the crosstalk among DNA methylation, transcription factors, and histone marks in human pluripotent cells through discovery of DNA methylation motifs. Genome Res., 23, 2013-2029.
44. Wang, J., Zhuang, J., Iyer, S., Lin, X., Whitfield, T.W., Greven, M.C., Pierce, B.G., Dong, X., Kundaje, A., Cheng, Y. et al. (2012) Sequence features and chromatin structure around the genomic regions bound by 119 human transcription factors. Genome Res., 22, 1798-1812.
45. Bernstein, B.E., Kamal, M., Lindblad-Toh, K., Bekiranov, S., Bailey, D.K., Huebert, D.J., McMahon, S., Karlsson, E.K., Kulbokas, E.J. 3rd, Gingeras, T.R. et al. (2005) Genomic maps and comparative analysis of histone modifications in human and mouse. Cell, 120, 169-181.
46. Lee, T.I. and Young, R.A. (2000) Transcription of eukaryotic protein-coding genes. Annu. Rev. Genet., 34, 77-137.
47. Kadonaga, J.T. (2004) Regulation of RNA polymerase II transcription by sequence-specific DNA binding factors. Cell, 116, 247-257.
48. Andersson, R., Gebhard, C., Miguel-Escalada, I., Hoof, I., Bornholdt, J., Boyd, M., Chen, Y., Zhao, X., Schmidl, C., Suzuki, T. et al. (2014) An atlas of active enhancers across human cell types and tissues. Nature, 507, 455-461.
49. Karlic, R., Chung, H.R., Lasserre, J., Vlahovicek, K. and Vingron, M. (2010) Histone modification levels are predictive for gene expression. Proc. Natl. Acad. Sci. U.S.A., 107, 2926-2931.
50. Ha, M., Ng, D.W., Li, W.H. and Chen, Z.J. (2011) Coordinated histone modifications are associated with gene expression variation within and between species. Genome Res., 21, 590-598.
51. Weih, F., Nitsch, D., Reik, A., Schutz, G. and Becker, P.B. (1991) Analysis of Cpg methylation and genomic footprinting at the tyrosine aminotransferase gene - DNA methylation alone Is not sufficient to prevent protein-binding in vivo. EMBO J., 10, 2559-2567.
52. Maurano, M.T., Wang, H., Shafer, A., John, S. and Stamatoyannopoulos, J.A. (2013) DNA methylation alone does not cause most cell-type selective transcription factor binding. Epigenet. Chromatin, 6, P103.
53. Wang, H., Maurano, M.T., Qu, H., Varley, K.E., Gertz, J., Pauli, F., Lee, K., Canfield, T., Weaver, M., Sandstrom, R. et al. (2012) Widespread plasticity in CTCF occupancy linked to DNA methylation. Genome Res., 22, 1680-1688.
54. Gheldof, N., Smith, E.M., Tabuchi, T.M., Koch, C.M., Dunham, I., Stamatoyannopoulos, J.A. and Dekker, J. (2010) Cell-type-specific long-range looping interactions identify distant regulatory elements of the CFTR gene. Nucleic Acids Res., 38, 4325-4336.
55. 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. (2006) Suz12 binds to silenced regions of the genome in a cell-type-specific manner. Genome Res., 16, 890-900.
56. Gotea, V., Visel, A., Westlund, J.M., Nobrega, M.A., Pennacchio, L.A. and Ovcharenko, I. (2010) Homotypic clusters of transcription factor binding sites are a key component of human promoters and enhancers. Genome Res., 20, 565-577.
57. Murakami, K., Kojima, T. and Sakaki, Y. (2004) Assessment of clusters of transcription factor binding sites in relationship to human promoter, CpG islands and gene expression. BMC Genomics, 5, 16.
58. He, X., Duque, T.S. and Sinha, S. (2012) Evolutionary origins of transcription factor binding site clusters. Mol. Biol. Evol., 29, 1059-1070.
59. Hemberg, M., Gray, J.M., Cloonan, N., Kuersten, S., Grimmond, S., Greenberg, M.E. and Kreiman, G. (2012) Integrated genome analysis suggests that most conserved non-coding sequences are regulatory factor binding sites. Nucleic Acids Res., 40, 7858-7869.
60. Yip, K.Y., Cheng, C., Bhardwaj, N., Brown, J.B., Leng, J., Kundaje, A., Rozowsky, J., Birney, E., Bickel, P., Snyder, M. et al. (2012) Classification of human genomic regions based on experimentally determined binding sites of more than 100 transcription-related factors. Genome Biol., 13, R48.
61. Woolfe, A., Goodson, M., Goode, D.K., Snell, P., McEwen, G.K., Vavouri, T., Smith, S.F., North, P., Callaway, H., Kelly, K. et al. (2005) Highly conserved non-coding sequences are associated with vertebrate development. PLoS Biol., 3, e7.
62. Alam, T., Medvedeva, Y.A., Jia, H., Brown, J.B., Lipovich, L. and Bajic, V.B. (2014) Promoter analysis reveals globally differential regulation of human long non-coding RNA and protein-coding genes. PLoS One, 9, e109443.
63. Derrien, T., Johnson, R., Bussotti, G., Tanzer, A., Djebali, S., Tilgner, H., Guernec, G., Martin, D., Merkel, A., Knowles, D.G. et al. (2012) The GENCODE v7 catalog of human long noncoding RNAs: analysis of their gene structure, evolution, and expression. Genome Res., 22, 1775-1789.
64. Barozzi, I., Simonatto, M., Bonifacio, S., Yang, L., Rohs, R., Ghisletti, S. and Natoli, G. (2014) Coregulation of transcription factor binding and nucleosome occupancy through DNA features of mammalian enhancers. Mol. Cell, 54, 844-857.
65. Zhou, H.L., Luo, G., Wise, J.A. and Lou, H. (2014) Regulation of alternative splicing by local histone modifications: potential roles for RNA-guided mechanisms. Nucleic Acids Res., 42, 701-713.
66. Vaissière, T., Sawan, C. and Herceg, Z. (2008) Epigenetic interplay between histone modifications and DNA methylation in gene silencing. Mutat. Res./Rev. Mutat. in Mutat. Res., 659, 40-48.
67. Palacios, D., Summerbell, D., Rigby, P.W. and Boyes, J. (2010) Interplay between DNA methylation and transcription factor availability: implications for developmental activation of the mouse Myogenin gene. Mol. Cell Biol., 30, 3805-3815.
68. Whitfield, T.W., Wang, J., Collins, P.J., Partridge, E.C., Aldred, S.F., Trinklein, N.D., Myers, R.M. and Weng, Z. (2012) Functional analysis of transcription factor binding sites in human promoters. Genome Biol., 13, R50.
69. Babu, M.M., Luscombe, N.M., Aravind, L., Gerstein, M. and Teichmann, S.A. (2004) Structure and evolution of transcriptional regulatory networks. Curr. Opin. Struct. Biol., 14, 283-291.
70. Teytelman, L., Thurtle, D.M., Rine, J. and van Oudenaarden, A. (2013) Highly expressed loci are vulnerable to misleading ChIP localization of multiple unrelated proteins. Proc. Natl. Acad. Sci. U.S.A., 110, 18602-18607.
71. Park, D., Lee, Y., Bhupindersingh, G. and Iyer, V.R. (2013) Widespread misinterpretable ChIP-seq bias in yeast. PLoS One, 8, e83506.
72. Arnone, M.I. and Davidson, E.H. (1997) The hardwiring of development: organization and function of genomic regulatory systems. Development, 124, 1851-1864.
73. Adhya, S. (1989) Multipartite genetic control elements: communication by DNA loop. Annu. Rev. Genet., 23, 227-250.
74. Kreiman, G. (2004) Identification of sparsely distributed clusters of cis-regulatory elements in sets of co-expressed genes. Nucleic Acids Res., 32, 2889-2900.
75. Yan, J., Enge, M., Whitington, T., Dave, K., Liu, J., Sur, I., Schmierer, B., Jolma, A., Kivioja, T., Taipale, M. et al. (2013) Transcription factor binding in human cells occurs in dense clusters formed around cohesin anchor sites. Cell, 154, 801-813.
76. Seila, A.C., Calabrese, J.M., Levine, S.S., Yeo, G.W., Rahl, P.B., Flynn, R.A., Young, R.A. and Sharp, P.A. (2008) Divergent transcription from active promoters. Science, 322, 1849-1851.
77. Guenther, M.G., Levine, S.S., Boyer, L.A., Jaenisch, R. and Young, R.A. (2007) A chromatin landmark and transcription initiation at most promoters in human cells. Cell, 130, 77-88.
78. Pennacchio, L.A., Bickmore, W., Dean, A., Nobrega, M.A. and Bejerano, G. (2013) Enhancers: five essential questions. Nat. Rev. Genet., 14, 288-295.
79. Blackwood, E.M. and Kadonaga, J.T. (1998) Going the distance: a current view of enhancer action. Science, 281, 60-63.
80. Thomas, S., Li, X.Y., Sabo, P.J., Sandstrom, R., Thurman, R.E., Canfield, T.K., Giste, E., Fisher, W., Hammonds, A., Celniker, S.E. et al. (2011) Dynamic reprogramming of chromatin accessibility during Drosophila embryo development. Genome Biol., 12, R43.
81. Boyle, A.P., Song, L., Lee, B.K., London, D., Keefe, D., Birney, E., Iyer, V.R., Crawford, G.E. and Furey, T.S. (2011) High-resolution genome-wide in vivo footprinting of diverse transcription factors in human cells. Genome Res., 21, 456-464.
82. Wang, Y., Li, X. and Hu, H. (2014) H3K4me2 reliably defines transcription factor binding regions in different cells. Genomics, 103, 222-228.
83. Motallebipour, M., Ameur, A., Reddy Bysani, M.S., Patra, K., Wallerman, O., Mangion, J., Barker, M.A., McKernan, K.J., Komorowski, J. and Wadelius, C. (2009) Differential binding and co-binding pattern of FOXA1 and FOXA3 and their relation to H3K4me3 in HepG2 cells revealed by ChIP-seq. Genome Biol., 10, R129.