De novo DNA demethylation and noncoding transcription define active intergenic regulatory elements

Genome Research

Volumn 23, Issue 10, 2013, Pages 1601-1614

  Schlesinger, Felix ^a   Smith, Andrew D ^b   Gingeras, Thomas R ^a   Hannon, Gregory J ^a,c   Hodges, Emily ^a,c  

^a Howard Hughes Medical Institute Cold Spring Harbor Laboratory Cold Spring Harbor   (United States)

^b UNIVERSITY OF SOUTHERN CALIFORNIA   (United States)

^c HOWARD HUGHES MEDICAL INSTITUTE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

BISULFITE; DNA; UNTRANSLATED RNA;

ANIMAL CELL; ARTICLE; B LYMPHOCYTE; CHROMATIN; CONTROLLED STUDY; DEMETHYLATION; DNA METHYLATION; DNA TRANSCRIPTION; FEMALE; GENE ACTIVITY; GENE EXPRESSION; GENOME; HUMAN; HUMAN CELL; NONHUMAN; PLASTICITY; PRIORITY JOURNAL; PROMOTER REGION; REGULATORY DNA SEQUENCE; TATA BOX;

ANIMALS; B-LYMPHOCYTES; CELL DIFFERENTIATION; CELL LINE; CHROMATIN; CPG ISLANDS; DNA METHYLATION; DNA, INTERGENIC; ENHANCER ELEMENTS, GENETIC; EVOLUTION, MOLECULAR; FEMALE; GENE EXPRESSION PROFILING; HEMATOPOIETIC STEM CELLS; HIGH-THROUGHPUT NUCLEOTIDE SEQUENCING; HUMANS; LYMPHOPOIESIS; PAN TROGLODYTES; PHYLOGENY; PROMOTER REGIONS, GENETIC; REGULATORY ELEMENTS, TRANSCRIPTIONAL; RNA, UNTRANSLATED; SEQUENCE ANALYSIS, DNA; TRANSCRIPTION INITIATION, GENETIC;

EID: 84885061881     PISSN: 10889051     EISSN: 15495469     Source Type: Journal    
DOI: 10.1101/gr.157271.113     Document Type: Article

References (41)

1. Akhtar-Zaidi B, Cowper-Sal Lari R, Corradin O, Saiakhova A, Bartels CF, Balasubramanian D, Myeroff L, Lutterbaugh J, Jarrar A, Kalady MF, et al. 2012. Epigenomic enhancer profiling defines a signature of colon cancer. Science 336: 736-739.
2. Arnosti DN, Kulkarni MM. 2005. Transcriptional enhancers: Intelligent enhanceosomes or flexible billboards? J Cell Biochem 94: 890-898.
3. Bock C, Beerman I, LienWH, Smith ZD, Gu H, Boyle P, Gnirke A, Fuchs E, Rossi DJ, Meissner A. 2012. DNA methylation dynamics during in vivo differentiation of blood and skin stem cells. Mol Cell 47: 633-647.
4. Bulger M, Groudine M. 2011. Functional and mechanistic diversity of distal transcription enhancers. Cell 144: 327-339.
5. Creyghton MP, Cheng AW, Welstead GG, Kooistra T, Carey BW, Steine EJ, Hanna J, Lodato MA, Frampton GM, Sharp P, et al. 2010. Histone h3k27ac separates active from poised enhancers and predicts developmental state. Proc Natl Acad Sci 107: 21931-21936.
6. Djebali S, Davis CA, Merkel A, Dobin A, Lassmann T, Mortazavi A, Tanzer A, Lagarde J, Lin W, Schlesinger F, et al. 2012. Landscape of transcription in human cells. Nature 489: 101-108.
7. The ENCODE Project Consortium. 2007. Identification and analysis of functional elements in 1% of the human genome by the ENCODE pilot project. Nature 447: 799-816.
8. The ENCODE Project Consortium. 2011. A user's guide to the encyclopedia of DNA elements (ENCODE). PLoS Biol 9: e1001046.
9. The ENCODE Project Consortium. 2012. An integrated encyclopedia of DNA elements in the human genome. Nature 489: 57-74.
10. Ernst J, Kheradpour P, Mikkelsen TS, Shoresh N, Ward LD, Epstein CB, Zhang X, Wang L, Issner R, Coyne M, et al. 2011. Mapping and analysis of chromatin state dynamics in nine human cell types. Nature 473: 43-49.
11. Gardiner-Garden M, Frommer M. 1987. Cpg islands in vertebrate genomes. J Mol Biol 196: 261-282.
12. Ginno PA, Lott PL, Christensen HC, Korf I, Chedin F. 2012. R-loop formation is a distinctive characteristic of unmethylated human CpG island promoters. Mol Cell 45: 814-825.
13. Heintzman ND, Stuart RK, Hon G, Fu Y, ChingCW, Hawkins RD, Barrera LO, Van Calcar S, Qu C, Ching KA, et al. 2007. Distinct and predictive chromatin signatures of transcriptional promoters and enhancers in the human genome. Nat Genet 39: 311-318.
14. Hodges E, Molaro A, Dos Santos CO, Thekkat P, Song Q, Uren PJ, Park J, Butler J, Rafii S, McCombie WR, et al. 2011. Directional DNA methylation changes and complex intermediate states accompany lineage specificity in the adult hematopoietic compartment. Mol Cell 44: 17-28.
15. Kharchenko PV, Alekseyenko AA, Schwartz YB, Minoda A, Riddle NC, Ernst J, Sabo PJ, Larschan E, Gorchakov AA, Gu T, et al. 2011. Comprehensive analysis of the chromatin landscape in Drosophila melanogaster. Nature 471: 480-485.
16. Kim T, Hemberg M, Gray JM, Costa AM, Bear DM, Wu J, Harmin DA, Laptewicz M, Barbara-Haley K, Kuersten S, et al. 2010. Widespread transcription at neuronal activity-regulated enhancers. Nature 465: 182.
17. Lenhard B, Sandelin A, Carninci P. 2012. Metazoan promoters: Emerging characteristics and insights into transcriptional regulation. Nat Rev Genet 13: 233-245.
18. Lindblad-Toh K, Garber M, Zuk O, LinMF, Parker BJ, Washietl S, Kheradpour P, Ernst J, Jordan G, Mauceli E, et al. 2011. A high-resolution map of human evolutionary constraint using 29 mammals. Nature 478: 476-482.
19. Ling J, Ainol L, Zhang L, Yu X, Pi W, Tuan D. 2004. HS2 enhancer function is blocked by a transcriptional terminator inserted between the enhancer and the promoter. J Biol Chem 279: 51704-51713.
20. Lister R, Pelizzola M, Dowen RH, Hawkins RD, Hon G, Tonti-Filippini J, Nery JR, Lee L, Ye Z, Ngo QM, et al. 2009. Human DNA methylomes at base resolution show widespread epigenomic differences. Nature 462: 315-322.
21. Long HK, Sims D, Heger A, Blackledge NP, Kutter C, Wright ML, Grutzner F, Odom DT, Patient R, Ponting CP, et al. 2013. Epigenetic conservation at gene regulatory elements revealed by non-methylated DNA profiling in seven vertebrates. eLife 2: e00348.
22. Lusk RW, Eisen MB. 2010. Evolutionary mirages: Selection on binding site composition creates the illusion of conserved grammars in Drosophila enhancers. PLoS Genet 6: e1000829.
23. MacArthur S, Brookfield JF. 2004. Expected rates and modes of evolution of enhancer sequences. Mol Biol Evol 21: 1064-1073.
24. McLean CY, Bristor D, Hiller M, Clarke SL, Schaar BT, Lowe CB, Wenger AM, Bejerano G. 2010. GREAT improves functional interpretation of cisregulatory regions. Nat Biotechnol 28: 495-501.
25. Melo CA, Drost J, Wijchers PJ, van deWerken H, deWit E, Oude Vrielink JA, Elkon R, Melo SA, Leveille N, Kalluri R, et al. 2013. eRNAs are required for p53-dependent enhancer activity and gene transcription. Mol Cell 49: 524-535.
26. Molaro A, Hodges E, Fang F, Song Q, McCombie WR, Hannon GJ, Smith AD. 2011. Sperm methylation profiles reveal features of epigenetic inheritance and evolution in primates. Cell 146: 1029-1041.
27. Prabhakar S, Visel A, Akiyama JA, Shoukry M, Lewis KD, Holt A, Plajzer-Frick I, Morrison H, Fitzpatrick DR, Afzal V, et al. 2008. Humanspecific gain of function in a developmental enhancer. Science 321: 1346-1350.
28. Rada-Iglesias A, Bajpai R, Swigut T, Brugmann SA, Flynn RA, Wysocka J. 2011. A unique chromatin signature uncovers early developmental enhancers in humans. Nature 470: 279-283.
29. Schmidt D, Wilson MD, Ballester B, Schwalie PC, Brown GD, Marshall A, Kutter C, Watt S, Martinez-Jimenez CP, Mackay S, et al. 2010. Fivevertebrate ChIP-seq reveals the evolutionary dynamics of transcription factor binding. Science 328: 1036-1040.
30. Serandour AA, Avner S, Oger F, Bizot M, Percevault F, Lucchetti-Miganeh C, Palierne G, Gheeraert C, Barloy-Hubler F, Peron CL, et al. 2012. Dynamic hydroxymethylation of deoxyribonucleic acid marks differentiationassociated enhancers. Nucleic Acids Res 40: 8255-8265.
31. Shen Y, Yue F, McCleary DF, Ye Z, Edsall L, Kuan S, Wagner U, Dixon J, Lee L, Lobanenkov VV, et al. 2012. A map of the cis-regulatory sequences in the mouse genome. Nature 488: 116-120.
32. Smith AD, Chung WY, Hodges E, Kendall J, Hannon G, Hicks J, Xuan Z, Zhang MQ. 2009. Updates to the RMAP short-read mapping software. Bioinformatics 25: 2841-2842.
33. Sonnenburg S, Zien A, Ratsch G. 2006. Arts: Accurate recognition of transcription starts in human. Bioinformatics 22: e472-e480.
34. Stadler MB, Murr R, Burger L, Ivanek R, Lienert F, Scholer A, van Nimwegen E, Wirbelauer C, Oakeley EJ, Gaidatzis D, et al. 2011. DNA-binding factors shape the mouse methylome at distal regulatory regions. Nature 480: 490-495.
35. Taberlay PC, Kelly TK, Liu CC, You JS, De Carvalho DD, Miranda TB, Zhou XJ, Liang G, Jones PA. 2011. Polycomb-repressed genes have permissive enhancers that initiate reprogramming. Cell 147: 1283-1294.
36. Thurman RE, Rynes E, Humbert R, Vierstra J, Maurano MT, Haugen E, Sheffield NC, Stergachis AB, Wang H, Vernot B, et al. 2012. The accessible chromatin landscape of the human genome. Nature 489: 75-82.
37. Toperoff G, Aran D, Kark JD, Rosenberg M, Dubnikov T, Nissan B, Wainstein J, Friedlander Y, Levy-Lahad E, Glaser B, et al. 2012. Genome-wide survey reveals predisposing diabetes type 2-related DNA methylation variations in human peripheral blood. Hum Mol Genet 21: 371-383.
38. Wang D, Garcia-Bassets I, Benner C, Li W, Su X, Zhou Y, Qiu J, Liu W, Kaikkonen MU, Ohgi KA, et al. 2011. Reprogramming transcription by distinct classes of enhancers functionally defined by eRNA. Nature 474: 390-394.
39. Wiench M, John S, Baek S, Johnson TA, Sung M, Escobar T, Simmons CA, Pearce KH, Biddie SC, Sabo PJ, et al. 2011. DNA methylation status predicts cell type-specific enhancer activity. EMBO J 30: 3028.
40. Wilson MD, Odom DT. 2009. Evolution of transcriptional control in mammals. Curr Opin Genet Dev 19: 579-585.
41. Yip KY, Cheng C, Bhardwaj N, Brown JB, 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.