Transcriptional enhancers: Functional insights and role in human disease

Current Opinion in Genetics and Development

Volumn 33, Issue , 2015, Pages 71-76

  Miguel Escalada, Irene ^a,b,c   Pasquali, Lorenzo ^c,d,e   Ferrer, Jorge ^a,b,c  

^a IMPERIAL COLLEGE LONDON   (United Kingdom)

^b ALBA SYNCHROTRON LIGHT SOURCE   (Spain)

^c INSTITUTO DE SALUD CARLOS III   (Spain)

^d HOSPITAL UNIVERSITARI GERMANS TRIAS I PUJOL   (Spain)

^e JOSEP CARRERAS LEUKAEMIA RESEARCH INSTITUTE IJC   (Spain)

Author keywords

[No Author keywords available]

Indexed keywords

DNA;

CHROMOSOME; ENHANCER REGION; EPIGENETICS; GENE CONTROL; GENE FUNCTION; GENE SEQUENCE; GENETIC TRANSCRIPTION; GENOMICS; HUMAN; NONHUMAN; PRIORITY JOURNAL; PROMOTER REGION; REVIEW; GENE EXPRESSION REGULATION; GENETIC DISORDER; GENETIC EPIGENESIS; GENETICS; PATHOLOGY;

ENHANCER ELEMENTS, GENETIC; EPIGENESIS, GENETIC; GENE EXPRESSION REGULATION; GENETIC DISEASES, INBORN; HUMANS; TRANSCRIPTION, GENETIC;

EID: 84945187780     PISSN: 0959437X     EISSN: 18790380     Source Type: Journal    
DOI: 10.1016/j.gde.2015.08.009     Document Type: Review

References (52)

1. Banerji J., Rusconi S., Schaffner W. Expression of a beta-globin gene is enhanced by remote SV40 DNA sequences. Cell 1981, 27:299-308.
2. Gaulton K.J., Nammo T., Pasquali L., Simon J.M., Giresi P.G., Fogarty M.P., Panhuis T.M., Mieczkowski P., Secchi A., Bosco D., et al. A map of open chromatin in human pancreatic islets. Nat Genet 2010, 42:255-259.
3. Song L., Zhang Z., Grasfeder L.L., Boyle A.P., Giresi P.G., Lee B.K., Sheffield N.C., Graf S., Huss M., Keefe D., et al. Open chromatin defined by DNaseI and FAIRE identifies regulatory elements that shape cell-type identity. Genome Res 2011, 21:1757-1767.
4. Buenrostro J.D., Giresi P.G., Zaba L.C., Chang H.Y., Greenleaf W.J. Transposition of native chromatin for fast and sensitive epigenomic profiling of open chromatin, DNA-binding proteins and nucleosome position. Nat Methods 2013, 10:1213-1218.
5. Rada-Iglesias A., Bajpai R., Swigut T., Brugmann S.A., Flynn R.A., Wysocka J. A unique chromatin signature uncovers early developmental enhancers in humans. Nature 2011, 470:279-283.
6. Visel A., Blow M.J., Li Z., Zhang T., Akiyama J.A., Holt A., Plajzer-Frick I., Shoukry M., Wright C., Chen F., et al. ChIP-seq accurately predicts tissue-specific activity of enhancers. Nature 2009, 457:854-858.
7. Kagey M.H., Newman J.J., Bilodeau S., Zhan Y., Orlando D.A., van Berkum N.L., Ebmeier C.C., Goossens J., Rahl P.B., Levine S.S., et al. Mediator and cohesin connect gene expression and chromatin architecture. Nature 2010, 467:430-435.
8. Andersson R., Gebhard C., Miguel-Escalada I., Hoof I., Bornholdt J., Boyd M., Chen Y., Zhao X., Schmidl C., Suzuki T., et al. An atlas of active enhancers across human cell types and tissues. Nature 2014, 507:455-461.
9. Roadmap Epigenomics C., Kundaje A., Meuleman W., Ernst J., Bilenky M., Yen A., Heravi-Moussavi A., Kheradpour P., Zhang Z., Wang J., et al. Integrative analysis of 111 reference human epigenomes. Nature 2015, 518:317-330.
10. Consortium E.P. An integrated encyclopedia of DNA elements in the human genome. Nature 2012, 489:57-74.
11. Pasquali L., Gaulton K.J., Rodriguez-Segui S.A., Mularoni L., Miguel-Escalada I., Akerman I., Tena J.J., Moran I., Gomez-Marin C., van de Bunt M., et al. Pancreatic islet enhancer clusters enriched in type 2 diabetes risk-associated variants. Nat Genet 2014, 46:136-143.
12. Akalin A., Fredman D., Arner E., Dong X., Bryne J.C., Suzuki H., Daub C.O., Hayashizaki Y., Lenhard B. Transcriptional features of genomic regulatory blocks. Genome Biol 2009, 10:R38.
13. Whyte W.A., Orlando D.A., Hnisz D., Abraham B.J., Lin C.Y., Kagey M.H., Rahl P.B., Lee T.I., Young R.A. Master transcription factors and mediator establish super-enhancers at key cell identity genes. Cell 2013, 153:307-319.
14. Parker S.C., Stitzel M.L., Taylor D.L., Orozco J.M., Erdos M.R., Akiyama J.A., van Bueren K.L., Chines P.S., Narisu N., Program N.C.S., et al. Chromatin stretch enhancer states drive cell-specific gene regulation and harbor human disease risk variants. Proc Natl Acad Sci U S A 2013, 110:17921-17926.
15. Shen Y., Yue F., McCleary D.F., Ye Z., Edsall L., Kuan S., Wagner U., Dixon J., Lee L., Lobanenkov V.V., et al. A map of the cis-regulatory sequences in the mouse genome. Nature 2012, 488:116-120.
16. Hnisz D., Abraham B.J., Lee T.I., Lau A., Saint-Andre V., Sigova A.A., Hoke H.A., Young R.A. Super-enhancers in the control of cell identity and disease. Cell 2013, 155:934-947.
17. Pott S., Lieb J.D. What are super-enhancers?. Nat Genet 2015, 47:8-12.
18. Loven J., Hoke H.A., Lin C.Y., Lau A., Orlando D.A., Vakoc C.R., Bradner J.E., Lee T.I., Young R.A. Selective inhibition of tumor oncogenes by disruption of super-enhancers. Cell 2013, 153:320-334.
19. Marinic M., Aktas T., Ruf S., Spitz F. An integrated holo-enhancer unit defines tissue and gene specificity of the Fgf8 regulatory landscape. Dev Cell 2013, 24:530-542.
20. Montavon T., Soshnikova N., Mascrez B., Joye E., Thevenet L., Splinter E., de Laat W., Spitz F., Duboule D. A regulatory archipelago controls Hox genes transcription in digits. Cell 2011, 147:1132-1145.
21. Tolhuis B., Palstra R.J., Splinter E., Grosveld F., de Laat W. Looping and interaction between hypersensitive sites in the active beta-globin locus. Mol Cell 2002, 10:1453-1465.
22. Tena J.J., Alonso M.E., de la Calle-Mustienes E., Splinter E., de Laat W., Manzanares M., Gomez-Skarmeta J.L. An evolutionarily conserved three-dimensional structure in the vertebrate Irx clusters facilitates enhancer sharing and coregulation. Nat Commun 2011, 2:310.
23. Liu Z., Legant W.R., Chen B.C., Li L., Grimm J.B., Lavis L.D., Betzig E. Tjian R3D imaging of Sox2 enhancer clusters in embryonic stem cells. Elife 2014, 3:e04236.
24. Dixon J.R., Selvaraj S., Yue F., Kim A., Li Y., Shen Y., Hu M., Liu J.S., Ren B. Topological domains in mammalian genomes identified by analysis of chromatin interactions. Nature 2012, 485:376-380.
25. Symmons O., Uslu V.V., Tsujimura T., Ruf S., Nassari S., Schwarzer W., Ettwiller L., Spitz F. Functional and topological characteristics of mammalian regulatory domains. Genome Res 2014, 24:390-400.
26. Le Dily F., Bau D., Pohl A., Vicent G.P., Serra F., Soronellas D., Castellano G., Wright R.H., Ballare C., Filion G., et al. Distinct structural transitions of chromatin topological domains correlate with coordinated hormone-induced gene regulation. Genes Dev 2014, 28:2151-2162.
27. Nora E.P., Lajoie B.R., Schulz E.G., Giorgetti L., Okamoto I., Servant N., Piolot T., van Berkum N.L., Meisig J., Sedat J., et al. Spatial partitioning of the regulatory landscape of the X-inactivation centre. Nature 2012, 485:381-385.
28. Phillips-Cremins J.E., Sauria M.E., Sanyal A., Gerasimova T.I., Lajoie B.R., Bell J.S., Ong C.T., Hookway T.A., Guo C., Sun Y., et al. Architectural protein subclasses shape 3D organization of genomes during lineage commitment. Cell 2013, 153:1281-1295.
29. Rao S.S., Huntley M.H., Durand N.C., Stamenova E.K., Bochkov I.D., Robinson J.T., Sanborn A.L., Machol I., Omer A.D., Lander E.S., et al. A 3D map of the human genome at kilobase resolution reveals principles of chromatin looping. Cell 2014, 159:1665-1680.
30. Dixon J.R., Jung I., Selvaraj S., Shen Y., Antosiewicz-Bourget J.E., Lee A.Y., Ye Z., Kim A., Rajagopal N., Xie W., et al. Chromatin architecture reorganization during stem cell differentiation. Nature 2015, 518:331-336.
31. Deng W., Lee J., Wang H., Miller J., Reik A., Gregory P.D., Dean A., Blobel G.A. Controlling long-range genomic interactions at a native locus by targeted tethering of a looping factor. Cell 2012, 149:1233-1244.
32. Li G., Ruan X., Auerbach R.K., Sandhu K.S., Zheng M., Wang P., Poh H.M., Goh Y., Lim J., Zhang J., et al. Extensive promoter-centered chromatin interactions provide a topological basis for transcription regulation. Cell 2012, 148:84-98.
33. Jin F., Li Y., Dixon J.R., Selvaraj S., Ye Z., Lee A.Y., Yen C.A., Schmitt A.D., Espinoza C.A., Ren B. A high-resolution map of the three-dimensional chromatin interactome in human cells. Nature 2013, 503:290-294.
34. Williamson I., Berlivet S., Eskeland R., Boyle S., Illingworth R.S., Paquette D., Dostie J., Bickmore W.A. Spatial genome organizationcontrasting views from chromosome conformation capture and fluorescence in situ hybridization. Genes Dev 2014, 28:2778-2791.
35. Lettice L.A., Heaney S.J., Purdie L.A., Li L., de Beer P., Oostra B.A., Goode D., Elgar G., Hill R.E., de Graaff E. A long-range Shh enhancer regulates expression in the developing limb and fin and is associated with preaxial polydactyly. Hum Mol Genet 2003, 12:1725-1735.
36. Benko S., Fantes J.A., Amiel J., Kleinjan D.J., Thomas S., Ramsay J., Jamshidi N., Essafi A., Heaney S., Gordon C.T., et al. Highly conserved non-coding elements on either side of SOX9 associated with Pierre Robin sequence. Nat Genet 2009, 41:359-364.
37. Smemo S., Campos L.C., Moskowitz I.P., Krieger J.E., Pereira A.C., Nobrega M.A., et al. Regulatory variation in a TBX5 enhancer leads to isolated congenital heart disease. Hum Mol Genet 2012, 21:3255-3263.
38. Weedon M.N., Cebola I., Patch A.M., Flanagan S.E., De Franco E., Caswell R., Rodriguez-Segui S.A., Shaw-Smith C., Cho C.H., Lango Allen H., et al. Recessive mutations in a distal PTF1A enhancer cause isolated pancreatic agenesis. Nat Genet 2014, 46:61-64.
39. Pashos E., Park J.T., Leach S., Fisher S. Distinct enhancers of ptf1a mediate specification and expansion of ventral pancreas in zebrafish. Dev Biol 2013, 381:471-481.
40. Zhou H.Y., Katsman Y., Dhaliwal N.K., Davidson S., Macpherson N.N., Sakthidevi M., Collura F., Mitchell J.A. A Sox2 distal enhancer cluster regulates embryonic stem cell differentiation potential. Genes Dev 2014, 28:2699-2711.
41. Gronau I., Arbiza L., Mohammed J., Siepel A. Inference of natural selection from interspersed genomic elements based on polymorphism and divergence. Mol Biol Evol 2013, 30:1159-1171.
42. Gulko B., Hubisz M.J., Gronau I., Siepel A: A method for calculating probabilities of fitness consequences for point mutations across the human genome. Nat Genet 2015, 47:276-283.
43. Khurana E., Fu Y., Colonna V., Mu X.J., Kang H.M., Lappalainen T., Sboner A., Lochovsky L., Chen J., Harmanci A., et al. Integrative annotation of variants from 1092 humans: application to cancer genomics. Science 2013, 342:1235587.
44. Maurano M.T., Humbert R., Rynes E., Thurman R.E., Haugen E., Wang H., Reynolds A.P., Sandstrom R., Qu H., Brody J., et al. Systematic localization of common disease-associated variation in regulatory DNA. Science 2012, 337:1190-1195.
45. Farh K.K., Marson A., Zhu J., Kleinewietfeld M., Housley W.J., Beik S., Shoresh N., Whitton H., Ryan R.J., Shishkin A.A., et al. Genetic and epigenetic fine mapping of causal autoimmune disease variants. Nature 2015, 518:337-343.
46. Ongen H., Andersen C.L., Bramsen J.B., Oster B., Rasmussen M.H., Ferreira P.G., Sandoval J., Vidal E., Whiffin N., Planchon A., et al. Putative cis-regulatory drivers in colorectal cancer. Nature 2014, 512:87-90.
47. Gjoneska E., Pfenning A.R., Mathys H., Quon G., Kundaje A., Tsai L.H., Kellis M. Conserved epigenomic signals in mice and humans reveal immune basis of Alzheimer's disease. Nature 2015, 518:365-369.
48. Cowper-Sallari R., Zhang X., Wright J.B., Bailey S.D., Cole M.D., Eeckhoute J., Moore J.H., Lupien M. Breast cancer risk-associated SNPs modulate the affinity of chromatin for FOXA1 and alter gene expression. Nat Genet 2012, 44:1191-1198.
49. Corradin O., Saiakhova A., Akhtar-Zaidi B., Myeroff L., Willis J., Cowper-Sal lari R., Lupien M., Markowitz S., Scacheri P.C. Combinatorial effects of multiple enhancer variants in linkage disequilibrium dictate levels of gene expression to confer susceptibility to common traits. Genome Res 2014, 24:1-13.
50. Smemo S., Tena J.J., Kim K.H., Gamazon E.R., Sakabe N.J., Gomez-Marin C., Aneas I., Credidio F.L., Sobreira D.R., Wasserman N.F., et al. Obesity-associated variants within FTO form long-range functional connections with IRX3. Nature 2014, 507:371-375.
51. Fischer J., Koch L., Emmerling C., Vierkotten J., Peters T., Bruning J.C., Ruther U. Inactivation of the Fto gene protects from obesity. Nature 2009, 458:894-898.
52. Frayling T.M., Timpson N.J., Weedon M.N., Zeggini E., Freathy R.M., Lindgren C.M., Perry J.R., Elliott K.S., Lango H., Rayner N.W., et al. A common variant in the FTO gene is associated with body mass index and predisposes to childhood and adult obesity. Science 2007, 316:889-894.