Epigenomic analysis detects aberrant super-enhancer DNA methylation in human cancer

Genome Biology

Volumn 17, Issue 1, 2016, Pages

  Heyn, Holger ^a   Vidal, Enrique ^a   Ferreira, Humberto J ^a   Vizoso, Miguel ^a   Sayols, Sergi ^a   Gomez, Antonio ^a   Moran, Sebastian ^a   Boque Sastre, Raquel ^a   Guil, Sonia ^a   Martinez Cardus, Anna ^a   Lin, Charles Y ^b,c,d   Royo, Romina ^e   Sanchez Mut, Jose V ^a   Martinez, Ramon ^f   Gut, Marta ^g   Torrents, David ^e,h   Orozco, Modesto ^e,i   Gut, Ivo ^g   Young, Richard A ^b,c   Esteller, Manel ^a,h,i  

^a BELLVITGE BIOMEDICAL RESEARCH INSTITUTE IDIBELL   (Spain)

^b WHITEHEAD INSTITUTE FOR BIOMEDICAL RESEARCH   (United States)

^c MASSACHUSETTS INSTITUTE OF TECHNOLOGY   (United States)

^d DANA FARBER CANCER INSTITUTE   (United States)

^e INSTITUTE FOR RESEARCH IN BIOMEDICINE   (Spain)

^f UNIVERSITY OF GÖTTINGEN   (Germany)

^g Centre Nacional d'Analisi Genomica   (Spain)

^h INSTITUCIÓ CATALANA DE RECERCA I ESTUDIS AVANÇATS ICREA   (Spain)

ⁱ UNIVERSITY OF BARCELONA   (Spain)

Author keywords

Cancer; DNA methylation; Epigenomics; Super enhancer

Indexed keywords

CD19 ANTIGEN; FORKHEAD TRANSCRIPTION FACTOR; HISTIDINE; LYSINE; MYC PROTEIN; TRANSCRIPTION FACTOR FOXQ1; UNCLASSIFIED DRUG;

AMINO ACID SUBSTITUTION; ARTICLE; BINDING SITE; BREAST CANCER CELL LINE; COLORECTAL CANCER; CONTROLLED STUDY; COPY NUMBER VARIATION; CPG ISLAND; DNA METHYLATION; DNA SEQUENCE; DOWN REGULATION; ENHANCER REGION; EPIGENETICS; FOXQ1 GENE; GENE; GENE ACTIVATION; GENE EXPRESSION REGULATION; GENE REPRESSION; GENE SILENCING; GENETIC ASSOCIATION; GENETIC VARIABILITY; GLIOBLASTOMA CELL LINE; GPRC5A GENE; HUMAN; HUMAN CELL; HUMAN TISSUE; LUNG ADENOCARCINOMA; NEOPLASM; ONCOGENE MYC; PROTEIN BINDING; RNF43 GENE; SEQUENCE ANALYSIS; SQUAMOUS CELL LUNG CARCINOMA; WHOLE GENOME BISULFITE SEQUENCING; GENETICS; HIGH THROUGHPUT SEQUENCING; HUMAN GENOME; PROMOTER REGION;

CPG ISLANDS; DNA METHYLATION; EPIGENOMICS; GENOME, HUMAN; HIGH-THROUGHPUT NUCLEOTIDE SEQUENCING; HUMANS; NEOPLASMS; PROMOTER REGIONS, GENETIC;

EID: 84956586301     PISSN: 14747596     EISSN: 1474760X     Source Type: Journal    
DOI: 10.1186/s13059-016-0879-2     Document Type: Article

References (56)

1. Hon GC, Rajagopal N, Shen Y, McCleary DF, Yue F, Dang MD, et al. Epigenetic memory at embryonic enhancers identified in DNA methylation maps from adult mouse tissues. Nat Genet. 2013;45:1198-206.
2. Fraga MF, Ballestar E, Paz MF, Ropero S, Setien F, Ballestar ML, et al. Epigenetic differences arise during the lifetime of monozygotic twins. Proc Natl Acad Sci U S A. 2005;102:10604-9.
3. Rideout 3rd WM, Eggan K, Jaenisch R. Nuclear cloning and epigenetic reprogramming of the genome. Science. 2001;293:1093-8.
4. Baylin SB, Jones PA. A decade of exploring the cancer epigenome - biological and translational implications. Nat Rev Cancer. 2011;11:726-34.
5. 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. 2011;44:40-6.
6. Hansen KD. Increased methylation variation in epigenetic domains across cancer types. Nat Genet. 2011;43:768-75.
7. Heyn H, Li N, Ferreira HJ, Moran S, Pisano DG, Gomez A, et al. Distinct DNA methylomes of newborns and centenarians. Proc Natl Acad Sci U S A. 2012;109:10522-7.
8. Whyte WA, Orlando DA, Hnisz D, Abraham BJ, Lin CY, Kagey MH, et al. Master transcription factors and mediator establish super-enhancers at key cell identity genes. Cell. 2013;153:307-19.
9. Stamatoyannopoulos JA, Clegg CH, Li Q. Sheltering of gamma-globin expression from position effects requires both an upstream locus control region and a regulatory element 3' to the A gamma-globin gene. Mol Cell Biol. 1997;17:240-7.
10. Talbot D, Collis P, Antoniou M, Vidal M, Grosveld F, Greaves DR. A dominant control region from the human beta-globin locus conferring integration site-independent gene expression. Nature. 1989;338:352-5.
11. Hnisz D, Abraham BJ, Lee TI, Lau A, Saint-André V, Sigova AA, et al. Super-enhancers in the control of cell identity and disease. Cell. 2013;155:934-947.
12. Chapuy B, McKeown MR, Lin CY, Monti S, Roemer MGM, Qi J, et al. Discovery and characterization of super-enhancer-associated dependencies in diffuse large B cell lymphoma. Cancer Cell. 2013;24:777-90.
13. Lovén J, Hoke HA, Lin CY, Lau A, Orlando DA, Vakoc CR, et al. Selective inhibition of tumor oncogenes by disruption of super-enhancers. Cell. 2013;153:320-34.
14. Mansour MR, Abraham BJ, Anders L, Berezovskaya A, Gutierrez A, Durbin AD, et al. An oncogenic super-enhancer formed through somatic mutation of a noncoding intergenic element. Science. 2014;346:1373-1377.
15. Chipumuro E, Marco E, Christensen CL, Kwiatkowski N, Zhang T, Hatheway CM, et al. CDK7 inhibition suppresses super-enhancer-linked oncogenic transcription in MYCN-driven cancer. Cell. 2014;159:1126-39.
16. Network CGA. Comprehensive molecular portraits of human breast tumours. Nature. 2012;490:61-70.
17. Network CGA. Comprehensive molecular characterization of human colon and rectal cancer. Nature. 2012;487:330-7.
18. Cancer Genome Atlas Research Network. Comprehensive molecular profiling of lung adenocarcinoma. Nature. 2014;511:543-50.
19. Consortium TEP. An integrated encyclopedia of DNA elements in the human genome. Nature. 2012;489:57-74.
20. 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.
21. Feldmann A, Ivanek R, Murr R, Gaidatzis D, Burger L, Schübeler D. Transcription factor occupancy can mediate active turnover of DNA methylation at regulatory regions. PLoS Genet. 2013;9:e1003994.
22. Molaro A, Hodges E, Fang F, Song Q, McCombie WR, Hannon GJ, et al. Sperm methylation profiles reveal features of epigenetic inheritance and evolution in primates. Cell. 2011;146:1029-41.
23. Hodges E, Molaro A, Dos Santos CO, Thekkat P, Song Q, Uren PJ, et al. Directional DNA methylation changes and complex intermediate states accompany lineage specificity in the adult hematopoietic compartment. Mol Cell. 2011;44:17-28.
24. Schlesinger F, Smith AD, Gingeras TR, Hannon GJ, Hodges E. De novo DNA demethylation and non-coding transcription define active intergenic regulatory elements. Genome Res. 2013;23:1601-1614.
25. Wiench M, John S, Baek S, Johnson TA, Sung M-H, Escobar T, et al. DNA methylation status predicts cell type-specific enhancer activity. EMBO J. 2011;30:3028-39.
26. Aran D, Sabato S, Hellman A. DNA methylation of distal regulatory sites characterizes dysregulation of cancer genes. Genome Biol. 2013;14:R21.
27. Taberlay PC, Statham AL, Kelly TK, Clark SJ, Jones PA. Reconfiguration of nucleosome-depleted regions at distal regulatory elements accompanies DNA methylation of enhancers and insulators in cancer. Genome Res. 2014;24:1421-32.
28. 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.
29. 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.
30. Hon GC, Hawkins RD, Caballero OL, Lo C, Lister R, Pelizzola M, et al. Global DNA hypomethylation coupled to repressive chromatin domain formation and gene silencing in breast cancer. Genome Res. 2012;22:246-58.
31. Rubio-Perez C, Tamborero D, Schroeder MP, Antolín AA, Deu-Pons J, Perez-Llamas C, et al. In silico prescription of anticancer drugs to cohorts of 28 tumor types reveals targeting opportunities. Cancer Cell. 2015;27:382-96.
32. Hon GC, Song C-X, Du T, Jin F, Selvaraj S, Lee AY, et al. 5mC Oxidation by Tet2 modulates enhancer activity and timing of transcriptome reprogramming during differentiation. Mol Cell. 2014;56:286-297.
33. Stewart SK, Morris TJ, Guilhamon P, Bulstrode H, Bachman M, Balasubramanian S, et al. oxBS-450 K: A method for analysing hydroxymethylation using 450 K BeadChips. Methods. 2015;72:9-15.
34. Jones PA. Functions of DNA methylation: islands, start sites, gene bodies and beyond. Nat Rev Genet. 2012;13:484-92.
35. Byers LA, Diao L, Wang J, Saintigny P, Girard L, Peyton M, et al. An epithelial-mesenchymal transition gene signature predicts resistance to EGFR and PI3K inhibitors and identifies Axl as a therapeutic target for overcoming EGFR inhibitor resistance. Clin Cancer Res Off J Am Assoc Cancer Res. 2013;19:279-90.
36. Fernandez AF, Assenov Y, Martin-Subero JI, Balint B, Siebert R, Taniguchi H, et al. A DNA methylation fingerprint of 1628 human samples. Genome Res. 2012;22:407-419.
37. Hanahan D, Weinberg RA. Hallmarks of cancer: the next generation. Cell. 2011;144:646-74.
38. Wang K, Yuen ST, Xu J, Lee SP, Yan HHN, Shi ST, et al. Whole-genome sequencing and comprehensive molecular profiling identify new driver mutations in gastric cancer. Nat Genet. 2014;46:573-82.
39. Bieller A, Pasche B, Frank S, Gläser B, Kunz J, Witt K, et al. Isolation and characterization of the human forkhead gene FOXQ1. DNA Cell Biol. 2001;20:555-61.
40. Cheng Y, Lotan R. Molecular cloning and characterization of a novel retinoic acid-inducible gene that encodes a putative G protein-coupled receptor. J Biol Chem. 1998;273:35008-15.
41. Jeong M, Sun D, Luo M, Huang Y, Challen GA, Rodriguez B, et al. Large conserved domains of low DNA methylation maintained by Dnmt3a. Nat Genet. 2014;46:17-23.
42. Hovestadt V, Jones DTW, 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.
43. Anastas JN, Moon RT. WNT signalling pathways as therapeutic targets in cancer. Nat Rev Cancer. 2012;13:11-26.
44. Wu Z-Q, Brabletz T, Fearon E, Willis AL, Hu CY, Li X-Y, et al. Canonical Wnt suppressor, Axin2, promotes colon carcinoma oncogenic activity. Proc Natl Acad Sci U S A. 2012;109:11312-7.
45. Krueger F, Andrews SR. Bismark: a flexible aligner and methylation caller for Bisulfite-Seq applications. Bioinforma Oxf Engl. 2011;27:1571-2.
46. Li H, Handsaker B, Wysoker A, Fennell T, Ruan J, Homer N, et al. The sequence alignment/map format and SAMtools. Bioinforma Oxf Engl. 2009;25:2078-9.
47. Quinlan AR, Hall IM. BEDTools: a flexible suite of utilities for comparing genomic features. Bioinforma Oxf Engl. 2010;26:841-2.
48. Li H. Tabix: fast retrieval of sequence features from generic TAB-delimited files. Bioinforma Oxf Engl. 2011;27:718-9.
49. R Development Core Team. R: a language and environment for statistical computing. Vienna: R Foundation for Statistical Computing; 2009.
50. Hansen KD, Langmead B, Irizarry RA. BSmooth: from whole genome bisulfite sequencing reads to differentially methylated regions. Genome Biol. 2012;13:R83.
51. Haider S, Ballester B, Smedley D, Zhang J, Rice P, Kasprzyk A. BioMart Central Portal--unified access to biological data. Nucleic Acids Res. 2009;37(Web Server issue):W23-7.
52. Harrow J, Frankish A, Gonzalez JM, Tapanari E, Diekhans M, Kokocinski F, et al. GENCODE: the reference human genome annotation for The ENCODE Project. Genome Res. 2012;22:1760-74.
53. Trapnell C, Pachter L, Salzberg SL. TopHat: discovering splice junctions with RNA-Seq. Bioinforma Oxf Engl. 2009;25:1105-11.
54. Aryee MJ, Jaffe AE, Corrada-Bravo H, Ladd-Acosta C, Feinberg AP, Hansen KD, et al. Minfi: A flexible and comprehensive Bioconductor package for the analysis of Infinium DNA Methylation microarrays. Bioinforma Oxf Engl. 2014;30:1363-1369.
55. Morris TJ, Butcher LM, Feber A, Teschendorff AE, Chakravarthy AR, Wojdacz TK, et al. ChAMP: 450 k Chip Analysis Methylation Pipeline. Bioinforma Oxf Engl. 2014;30:428-30.
56. Leek JT, Storey JD. Capturing heterogeneity in gene expression studies by surrogate variable analysis. PLoS Genet. 2007;3:e161.