Inferring regulatory element landscapes and transcription factor networks from cancer methylomes

Genome Biology

Volumn 16, Issue 1, 2015, Pages

  Yao, Lijing ^a   Shen, Hui ^b   Laird, Peter W ^b   Farnham, Peggy J ^a   Berman, Benjamin P ^a,c  

^a UNIVERSITY OF SOUTHERN CALIFORNIA   (United States)

^b VAN ANDEL RESEARCH INSTITUTE   (United States)

^c CEDARS SINAI MEDICAL CENTER   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

HEPATOCYTE NUCLEAR FACTOR 3ALPHA; HEPATOCYTE NUCLEAR FACTOR 3BETA; PROTEIN P63; TRANSCRIPTION FACTOR; TRANSCRIPTION FACTOR GATA 3; TRANSCRIPTION FACTOR NRF2; TRANSCRIPTION FACTOR RUNX1; TRANSCRIPTION FACTOR SOX17; TRANSCRIPTION FACTOR SOX2; FOXA1 PROTEIN, HUMAN; FOXA2 PROTEIN, HUMAN; GATA3 PROTEIN, HUMAN; NEOPLASM-ASSOCIATED FACTOR; NFE2L2 PROTEIN, HUMAN; RUNX1 PROTEIN, HUMAN; SOX17 PROTEIN, HUMAN; SOX2 PROTEIN, HUMAN; TP63 PROTEIN, HUMAN; TRANSCRIPTION FACTOR SOX; TUMOR PROTEIN; TUMOR SUPPRESSOR PROTEIN;

ARTICLE; BLADDER CARCINOMA; BREAST CANCER; CANCER GENETICS; CLEAR CELL CARCINOMA; COLON ADENOCARCINOMA; COMPUTER PROGRAM; CONTROLLED STUDY; DNA METHYLATION; ENDOMETRIOID CARCINOMA; ENDOMETRIUM CANCER; ENHANCER REGION; GENE EXPRESSION; GENE TARGETING; GLIOBLASTOMA; HEAD AND NECK SQUAMOUS CELL CARCINOMA; KIDNEY CARCINOMA; LEUKEMIA; LUNG ADENOCARCINOMA; REGULATORY SEQUENCE; SQUAMOUS CELL LUNG CARCINOMA; TRANSITIONAL CELL CARCINOMA; GENE EXPRESSION REGULATION; GENE REGULATORY NETWORK; GENETIC DATABASE; GENETICS; HUMAN; MCF-7 CELL LINE; METABOLISM; NEOPLASM; SEQUENCE ANALYSIS; TUMOR CELL LINE;

CELL LINE, TUMOR; CORE BINDING FACTOR ALPHA 2 SUBUNIT; DATABASES, GENETIC; DNA METHYLATION; ENHANCER ELEMENTS, GENETIC; GATA3 TRANSCRIPTION FACTOR; GENE EXPRESSION REGULATION, NEOPLASTIC; GENE REGULATORY NETWORKS; HEPATOCYTE NUCLEAR FACTOR 3-ALPHA; HEPATOCYTE NUCLEAR FACTOR 3-BETA; HUMANS; MCF-7 CELLS; NEOPLASM PROTEINS; NEOPLASMS; NF-E2-RELATED FACTOR 2; SEQUENCE ANALYSIS, RNA; SOXB1 TRANSCRIPTION FACTORS; SOXF TRANSCRIPTION FACTORS; TRANSCRIPTION FACTORS; TUMOR SUPPRESSOR PROTEINS;

EID: 84938923353     PISSN: 14747596     EISSN: 1474760X     Source Type: Journal    
DOI: 10.1186/s13059-015-0668-3     Document Type: Article

References (97)

1. Bernstein BE, Birney E, Dunham I, Green ED, Gunter C, Snyder M. An integrated encyclopedia of DNA elements in the human genome. Nature. 2012;489:57-74.
2. Roadmap Epigenomics Consortium. Integrative analysis of 111 reference human epigenomes. Nature. 2015;19:317-30.
3. Henikoff S. ENCODE and our very busy genome. Nat Genet. 2007;39:817-8.
4. Filion GJ, Van Bemmel JG, Braunschweig U, Talhout W, Kind J, Ward LD, et al. Systematic protein location mapping reveals five principal chromatin types in Drosophila cells. Cell. 2010;143:212-24.
5. Ernst J, Kheradpour P, Mikkelsen TS, Shoresh N, Ward LD, Epstein CB, et al. Mapping and analysis of chromatin state dynamics in nine human cell types. Nature. 2011;473:43-9.
6. Hoffman MM, Buske OJ, Wang J, Weng Z, Bilmes J, Noble WS. Unsupervised pattern discovery in human chromatin structure through genomic segmentation. Nat Methods. 2012;9:473-6.
7. Creyghton MP, Cheng AW, Welstead GG, Kooistra T, Carey BW, Steine EJ, et al. Histone H3K27ac separates active from poised enhancers and predicts developmental state. Proc Natl Acad Sci U S A. 2010;107:21931-6.
8. Rada-Iglesias A, Bajpai R, Swigut T, Brugmann SA, Flynn RA, Wysocka J. A unique chromatin signature uncovers early developmental enhancers in humans. Nature. 2011;470:279-83.
9. Bernstein BE, Stamatoyannopoulos JA, Costello JF, Ren B, Milosavljevic A, Meissner A, et al. The NIH Roadmap Epigenomics Mapping Consortium. Nat Biotechnol. 2010;28:1045-8.
10. Beck S, Bernstein BE, Campbell RM, Costello JF, Dhanak D, Ecker JR, et al. A blueprint for an international cancer epigenome consortium. A report from the AACR Cancer Epigenome Task Force. Cancer Res. 2012;72:6319-24.
11. He B, Chen C, Teng L, Tan K. Global view of enhancer-promoter interactome in human cells. Proc Natl Acad Sci U S A. 2014;111:E2191-9.
12. Sheffield NC, Thurman RE, Song L, Safi A, Stamatoyannopoulos JA, Lenhard B, et al. Patterns of regulatory activity across diverse human cell types predict tissue identity, transcription factor binding, and long-range interactions. Genome Res. 2013;23:777-88.
13. Pastor WA, Stroud H, Nee K, Liu W, Pezic D, Manakov S, et al. MORC1 represses transposable elements in the mouse male germline. Nat Commun. 2014;5:5795.
14. Bergman Y, Cedar H. DNA methylation dynamics in health and disease. Nat Struct Mol Biol. 2013;20:274-81.
15. Thomassin H, Flavin M, Espinás ML, Grange T. Glucocorticoid-induced DNA demethylation and gene memory during development. EMBO J. 2001;20:1974-83.
16. Lister R, Pelizzola M, Dowen RH, Hawkins RD, Hon G, Tonti-Filippini J, et al. Human DNA methylomes at base resolution show widespread epigenomic differences. Nature. 2009;462:315-22.
17. Stadler MB, Murr R, Burger L, Ivanek R, Lienert F, Schöler A, et al. DNA-binding factors shape the mouse methylome at distal regulatory regions. Nature. 2011;480:490-5.
18. Blattler A, Farnham PJ. Cross-talk between site-specific transcription factors and DNA methylation states. J Biol Chem. 2013;288:34287-94.
19. Ooi L, Wood IC. Chromatin crosstalk in development and disease: lessons from REST. Nat Rev Genet. 2007;8:544-54.
20. Gebhard C, Benner C, Ehrich M, Schwarzfischer L, Schilling E, Klug M, et al. General transcription factor binding at CpG islands in normal cells correlates with resistance to de novo DNA methylation in cancer cells. Cancer Res. 2010;70:1398-407.
21. Berman BP, Weisenberger DJ, Aman JF, Hinoue T, Ramjan Z, Liu Y, et al. Regions of focal DNA hypermethylation and long-range hypomethylation in colorectal cancer coincide with nuclear lamina-associated domains. Nat Genet. 2012;44:40-6.
22. Aran D, Sabato S, Hellman A. DNA methylation of distal regulatory sites characterizes dysregulation of cancer genes. Genome Biol. 2013;14:R21.
23. Hovestadt V, Jones DT, Picelli S, Wang W, Kool M, Northcott PA, et al. Decoding the regulatory landscape of medulloblastoma using DNA methylation sequencing. Nature. 2014;510:537-41.
24. Li G, Ruan X, Auerbach RK, Sandhu KS, Zheng M, Wang P, et al. Extensive promoter-centered chromatin interactions provide a topological basis for transcription regulation. Cell. 2012;148:84-98.
25. Aran D, Hellman A. DNA methylation of transcriptional enhancers and cancer predisposition. Cell. 2013;154:11-3.
26. Wiench M, John S, Baek S, Johnson TA, Sung MH, Escobar T, et al. DNA methylation status predicts cell type-specific enhancer activity. EMBO J. 2011;30:3028-39.
27. Weinstein JN, Collisson EA, Mills GB, Shaw KR, Ozenberger BA, Ellrott K, et al. The Cancer Genome Atlas Pan-Cancer analysis project. Nat Genet. 2013;45:1113-20.
28. The Cancer Genome Atlas. Comprehensive molecular characterization of human colon and rectal cancer. Nature. 2012;487:330-7.
29. GENCODE gene annotations. [ http://www.gencodegenes.org/releases/15.html ]
30. Ernst J, Kellis M. ChromHMM: automating chromatin-state discovery and characterization. Nat Methods. 2012;9:215-6.
31. ENCODE_Project_Consortium. An integrated encyclopedia of DNA elements in the human genome. Nature. 2012;489:57-74.
32. Andersson R, Gebhard C, Miguel-Escalada I, Hoof I, Bornholdt J, Boyd M, et al. An atlas of active enhancers across human cell types and tissues. Nature. 2014;507:455-61.
33. Kwasnieski JC, Fiore C, Chaudhari HG, Cohen BA. High-throughput functional testing of ENCODE segmentation predictions. Genome Res. 2014;24:1595-602.
34. Blow MJ, McCulley DJ, Li Z, Zhang T, Akiyama JA, Holt A, et al. ChIP-Seq identification of weakly conserved heart enhancers. Nat Genet. 2010;42:806-10.
35. Sanyal A, Lajoie BR, Jain G, Dekker J. The long-range interaction landscape of gene promoters. Nature. 2012;489:109-13.
36. Jin F, Li Y, Dixon JR, Selvaraj S, Ye Z, Lee AY, et al. A high-resolution map of the three-dimensional chromatin interactome in human cells. Nature. 2013;503:290-4.
37. Rao SS, Huntley MH, Durand NC, Stamenova EK, Bochkov ID, Robinson JT, et al. A 3D map of the human genome at kilobase resolution reveals principles of chromatin looping. Cell. 2014;159:1665-80.
38. Mathelier A, Zhao X, Zhang AW, Parcy F, Worsley-Hunt R, Arenillas DJ, et al. JASPAR 2014: an extensively expanded and updated open-access database of transcription factor binding profiles. Nucleic Acids Res. 2014;42:D142-7.
39. Wang J, Zhuang J, Iyer S, Lin XY, Greven MC, Kim BH, et al. Factorbook.org: a Wiki-based database for transcription factor-binding data generated by the ENCODE consortium. Nucleic Acids Res. 2013;41:D171-6.
40. Fujiwara T, O'Geen H, Keles S, Blahnik K, Linnemann AK, Kang YA, et al. Discovering hematopoietic mechanisms through genome-wide analysis of GATA factor chromatin occupancy. Mol Cell. 2009;36:667-81.
41. Xu X, Bieda M, Jin VX, Rabinovich A, Oberley MJ, Green R, et al. A comprehensive ChIP-chip analysis of E2F1, E2F4, and E2F6 in normal and tumor cells reveals iterchangeable roles of E2F family members. Genome Res. 2007;17:1550-61.
42. Shakya A, Callister C, Goren A, Yosef N, Garg N, Khoddami V, et al. Pluripotency transcription factor oct4 mediates stepwise nucleosome demethylation and depletion. Mol Cell Biol. 2015;35:1014-25.
43. Lee DS, Shin JY, Tonge PD, Puri MC, Lee S, Park H, et al. An epigenomic roadmap to induced pluripotency reveals DNA methylation as a reprogramming modulator. Nat Commun. 2014;5:5619.
44. Bresnick EH, Lee HY, Fujiwara T, Johnson KD, Keles S. GATA switches as developmental drivers. J Biol Chem. 2010;285:31087-93.
45. Brewer A, Pizzey J. GATA factors in vertebrate heart development and disease. Expert Rev Mol Med. 2006;8:1-20.
46. Chou J, Provot S, Werb Z. GATA3 in development and cancer differentiation: cells GATA have it! J Cell Physiol. 2010;222:42-9.
47. Patient RK, McGhee JD. The GATA family (vertebrates and invertebrates). Curr Opin Genet Dev. 2002;12:416-22.
48. Kouros-Mehr H, Bechis SK, Slorach EM, Littlepage LE, Egeblad M, Ewald AJ, et al. GATA-3 links tumor differentiation and dissemination in a luminal breast cancer model. Cancer Cell. 2008;13:141-52.
49. Kouros-Mehr H, Kim JW, Bechis SK, Werb Z. GATA-3 and the regulation of the mammary luminal cell fate. Curr Opin Cell Biol. 2008;20:164-70.
50. Yan W, Cao QJ, Arenas RB, Bentley B, Shao R. GATA3 inhibits breast cancer metastasis through the reversal of epithelial-mesenchymal transition. J Biol Chem. 2010;285:14042-51.
51. Heintzman ND, Stuart RK, Hon G, Fu Y, Ching CW, Hawkins RD, et al. Distinct predictive chromatin signatures of transcriptional promoters and enhancers in the human genome. Nature Genetics. 2007;39:311-8.
52. Blattler A, Yao L, Witt H, Guo Y, Nicolet CM, Berman BP, et al. Global loss of DNA methylation uncovers intronic enhancers in genes showing expression changes. Genome Biol. 2014;15:469.
53. Maunakea AK, Nagarajan RP, Bilenky M, Ballinger TJ, D'Souza C, Fouse SD, et al. Conserved role of intragenic DNA methylation in regulating alternative promoters. Nature. 2010;466:253-7.
54. Kowalczyk MS, Hughes JR, Garrick D, Lynch MD, Sharpe JA, Sloane-Stanley JA, et al. Intragenic enhancers act as alternative promoters. Mol Cell. 2012;45:447-58.
55. Raviram R, Rocha PP, Bonneau R, Skok JA. Interpreting 4C-Seq data: how far can we go? Epigenomics. 2014;6:455-7.
56. Eeckhoute J, Carroll JS, Geistlinger TR, Torres-Arzayus MI, Brown M. A cell-type-specific transcriptional network required for estrogen regulation of cyclin D1 and cell cycle progression in breast cancer. Genes & Dev. 2015;20:2513-26.
57. Yochum GS, Cleland R, Goodman RH. A genome-wide screen for beta-catenin binding sites identifies a downstream enhancer element that controls c-Myc gene expression. Mol Cell Biol. 2008;28:7368-79.
58. Konsavage Jr WM, Yochum GS. The myc 3' wnt-responsive element suppresses colonic tumorigenesis. Mol Cell Biol. 2014;34:1659-69.
59. Rosenbauer F, Wagner K, Kutok JL, Iwasaki H, Le Beau MM, Okuno Y, et al. Acute myeloid leukemia induced by graded reduction of a lineage-specific transcription factor, PU.1. Nat Genet. 2004;36:624-30.
60. Bass AJ, Lawrence MS, Brace LE, Ramos AH, Drier Y, Cibulskis K, et al. Genomic sequencing of colorectal adenocarcinomas identifies a recurrent VTI1A-TCF7L2 fusion. Nat Genet. 2011;43:964-8.
61. Frietze S, Wang R, Yao L, Tak YG, Ye Z, Gaddis M, et al. Cell type-specific binding patterns reveal that TCF7L2 can be tethered to the genome by association with GATA3. Genome Biol. 2012;13:R52.
62. Sur IK, Hallikas O, Vaharautio A, Yan J, Turunen M, Enge M, et al. Mice lacking a Myc enhancer that includes human SNP rs6983267 are resistant to intestinal tumors. Science. 2012;338:1360-3.
63. Pomerantz MM, Ahmadiyeh N, Jia L, Herman P, Verzi MP, Doddapaneni H, et al. The 8q24 cancer risk variant rs6983267 shows long-range interaction with MYC in colorectal cancer. Nat Genet. 2009;41:882-4.
64. The Cancer Genome Atlas. Comprehensive genomic characterization of squamous cell lung cancers. Nature. 2012;489:519-25.
65. Massion PP, Taflan PM, Jamshedur Rahman SM, Yildiz P, Shyr Y, Edgerton ME, et al. Significance of p63 amplification and overexpression in lung cancer development and prognosis. Cancer Res. 2003;63:7113-21.
66. Watanabe H, Ma Q, Peng S, Adelmant G, Swain D, Song W, et al. SOX2 and p63 colocalize at genetic loci in squamous cell carcinomas. J Clin Invest. 2014;124:1636-45.
67. Kandoth C, McLellan MD, Vandin F, Ye K, Niu B, Lu C, et al. Mutational landscape and significance across 12 major cancer types. Nature. 2013;502:333-9.
68. Worsley Hunt R, Wasserman WW. Non-targeted transcription factors motifs are a systemic component of ChIP-seq datasets. Genome Biol. 2014;15:412.
69. Aguilera C, Nakagawa K, Sancho R, Chakraborty A, Hendrich B, Behrens A. c-Jun N-terminal phosphorylation antagonises recruitment of the Mbd3/NuRD repressor complex. Nature. 2011;469:231-5.
70. Tupler R, Perini G, Green MR. Expressing the human genome. Nature. 2001;409:832-3.
71. Razin SV, Borunova VV, Maksimenko OG, Kantidze OL. Cys2His2 zinc finger protein family: classification, functions, and major members. Biochemistry (Mosc). 2012;77:217-26.
72. Vaquerizas JM, Kummerfeld SK, Teichmann SA, Luscombe NM. A census of human transcription factors: function, expression and evolution. Nat Reviews Genetics. 2009;10:252-63.
73. Reynisdottir I, Arason A, Einarsdottir BO, Gunnarsson H, Staaf J, Vallon-Christersson J, et al. High expression of ZNF703 independent of amplification indicates worse prognosis in patients with luminal B breast cancer. Cancer Med. 2013;2:437-46.
74. Kang X, Chen W, Kim RH, Kang MK, Park NH. Regulation of the hTERT promoter activity by MSH2, the hnRNPs K and D, and GRHL2 in human oral squamous cell carcinoma cells. Oncogene. 2009;28:565-74.
75. Schaub MA, Boyle AP, Kundaje A, Batzoglou S, Snyder M. Linking disease associations with regulatory information in the human genome. Genome Res. 2012;22:1748-59.
76. Maurano MT, Humbert R, Rynes E, Thurman RE, Haugen E, Wang H, et al. Systematic localization of common disease-associated variation in regulatory DNA. Science. 2012;337:1190-5.
77. Akhtar-Zaidi B, Cowper-Sal-lari R, Corradin O, Saiakhova A, Bartels CF, Balasubramanian D, et al. Epigenomic enhancer profiling defines a signature of colon cancer. Science. 2012;336:736-9.
78. Hardison RC. Genome-wide epigenetic data facilitate understanding of disease susceptibility association studies. J Biol Chem. 2012;287:30932-40.
79. Yao L, Tak YG, Berman BP, Farnham PJ. Functional annotation of colon cancer risk SNPs. Nat Commun. 2014;5:5114.
80. Fredriksson NJ, Ny L, Nilsson JA, Larsson E. Systematic analysis of noncoding somatic mutations and gene expression alterations across 14 tumor types. Nat Genet. 2014;46:1258-63.
81. Huang FW, Hodis E, Xu MJ, Kryukov GV, Chin L, Garraway LA. Highly recurrent TERT promoter mutations in human melanoma. Science. 2013;339:957-9.
82. Weinhold N, Jacobsen A, Schultz N, Sander C, Lee W. Genome-wide analysis of noncoding regulatory mutations in cancer. Nat Genet. 2014;46:1160-5.
83. Hansen KD, Timp W, Bravo HC, Sabunciyan S, Langmead B, McDonald OG, et al. Increased methylation variation in epigenetic domains across cancer types. Nat Genet. 2011;43:768-75.
84. BioConductor. [ http://www.bioconductor.org/ ]
85. ELMER source code. [ https://github.com/lijingya/ELMER.git ]
86. ELMER usage vignette. [ https://github.com/lijingya/ELMER/blob/master/vignettes/vignettes.pdf ]
87. ELMER user manual. [ https://github.com/lijingya/ELMER/blob/master/inst/doc/ELMER_manual.pdf ]
88. TCGA data access. [ https://tcga-data.nci.nih.gov/tcgafiles/ftp_auth/distro_ftpusers/anonymous/tumor/ ]
89. TCGA pan-can analysis (Synapse).[ https://www.synapse.org/ ]
90. Lawrence M, Huber W, Pages H, Aboyoun P, Carlson M, Gentleman R, et al. Software for computing and annotating genomic ranges. PLoS Comput Biol. 2013;9:e1003118.
91. Epigenomics Roadmap data access. [ https://sites.google.com/site/epigenomeroadmapawg/project-updates/finalsignaltracksandalignmentfiles ]
92. FANTOM enhancer annotations. [ http://enhancer.binf.ku.dk/presets/ ]
93. Alexa A, Rahnenfuhrer J. topGO: Enrichment analysis for Gene Ontology. R package version 2180. 2010. [ http://www.bioconductor.org/packages/release/bioc/html/topGO.html ]
94. Grant CE, Bailey TL, Noble WS. FIMO: scanning for occurrences of a given motif. Bioinformatics. 2011;27:1017-8.
95. Wang J, Zhuang J, Iyer S, Lin X, Whitfield TW, Greven MC, et al. Sequence features and chromatin structure around the genomic regions bound by 119 human transcription factors. Genome Res. 2012;22:1798-812.
96. Shannon P. MotifDb: An annotated collection of Protein-DNA binding sequence motifs. Bioconductor. 2014, R package version 1.8.0. [ http://www.bioconductor.org/packages/release/bioc/html/MotifDb.html ]
97. Ravasi T, Suzuki H, Cannistraci CV, Katayama S, Bajic VB, Tan K, et al. An atlas of combinatorial transcriptional regulation in mouse and man. Cell. 2010;140:744-52.