Hormone-Responsive Enhancer-Activity Maps Reveal Predictive Motifs, Indirect Repression, and Targeting of Closed Chromatin

Molecular Cell

Volumn 54, Issue 1, 2014, Pages 180-192

  Shlyueva, Daria ^a   Stelzer, Christoph ^a   Gerlach, Daniel ^a   Yáñez Cuna, J Omar ^a   Rath, Martina ^a   Boryń, Łukasz M ^a   Arnold, Cosmas D ^a   Stark, Alexander ^a  

^a RESEARCH INSTITUTE OF MOLECULAR PATHOLOGY   (Austria)

Author keywords

[No Author keywords available]

Indexed keywords

ECDYSONE; CIS ACTING ELEMENT; STEROID HORMONE;

ARTICLE; BINDING SITE; CELL SPECIFICITY; CELL TYPE; CHROMATIN; CHROMATIN STRUCTURE; CONTROLLED STUDY; DROSOPHILA MELANOGASTER; ENHANCER REGION; GENE EXPRESSION; GENE REPRESSION; GENETIC ASSOCIATION; HORMONAL THERAPY; HORMONE RESPONSE; HORMONE RESPONSIVE ELEMENT; IN VIVO STUDY; NONHUMAN; POINT MUTATION; RECEPTOR BINDING; SCREENING; CELLS BY BODY ANATOMY; DROSOPHILA; GENE SEQUENCE; GENE TARGETING; GENOME ANALYSIS; SCREENING TEST; SIGNAL TRANSDUCTION;

ANIMALS; CELL LINE; CHROMATIN ASSEMBLY AND DISASSEMBLY; COMPUTATIONAL BIOLOGY; DATABASES, GENETIC; DROSOPHILA MELANOGASTER; ECDYSONE; ENHANCER ELEMENTS, GENETIC; EPIGENETIC REPRESSION; FEMALE; GENE EXPRESSION REGULATION; HIGH-THROUGHPUT NUCLEOTIDE SEQUENCING; NUCLEOTIDE MOTIFS; OVARY; SIGNAL TRANSDUCTION; SUPPORT VECTOR MACHINES; TRANSCRIPTIONAL ACTIVATION; TRANSFECTION;

EID: 84898025687     PISSN: 10972765     EISSN: 10974164     Source Type: Journal    
DOI: 10.1016/j.molcel.2014.02.026     Document Type: Article

References (60)

1. Affolter M., Pyrowolakis G., Weiss A., Basler K. Signal-induced repression: the exception or the rule in developmental signaling?. Dev. Cell 2008, 15:11-22.
2. Arnold C.D., Gerlach D., Stelzer C., Boryń Ł.M., Rath M., Stark A. Genome-wide quantitative enhancer activity maps identified by STARR-seq. Science 2013, 339:1074-1077.
3. Arnosti D.N., Kulkarni M.M. Transcriptional enhancers: Intelligent enhanceosomes or flexible billboards?. J.Cell. Biochem. 2005, 94:890-898.
4. *. Annu. Rev. Immunol. 2000, 18:309-345.
5. Ballaré C., Castellano G., Gaveglia L., Althammer S., González-Vallinas J., Eyras E., Le Dily F., Zaurin R., Soronellas D., Vicent G.P., Beato M. Nucleosome-driven transcription factor binding and gene regulation. Mol. Cell 2013, 49:67-79.
6. Banerji J., Rusconi S., Schaffner W. Expression of a beta-globin gene is enhanced by remote SV40 DNA sequences. Cell 1981, 27:299-308.
7. Barolo S., Posakony J.W. Three habits of highly effective signaling pathways: principles of transcriptional control by developmental cell signaling. Genes Dev. 2002, 16:1167-1181.
8. Bernardo T.J., Dubrovskaya V.A., Jannat H., Maughan B., Dubrovsky E.B. Hormonal regulation of the E75 gene in Drosophila: identifying functional regulatory elements through computational and biological analysis. J.Mol. Biol. 2009, 387:794-808.
9. Bialecki M., Shilton A., Fichtenberg C., Segraves W.A., Thummel C.S. Loss of the ecdysteroid-inducible E75A orphan nuclear receptor uncouples molting from metamorphosis in Drosophila. Dev. Cell 2002, 3:209-220.
10. Biddie S.C., John S., Sabo P.J., Thurman R.E., Johnson T.A., Schiltz R.L., Miranda T.B., Sung M.-H., Trump S., Lightman S.L., et al. Transcription factor AP1 potentiates chromatin accessibility and glucocorticoid receptor binding. Mol. Cell 2011, 43:145-155.
11. Boyle A.P., Davis S., Shulha H.P., Meltzer P., Margulies E.H., Weng Z., Furey T.S., Crawford G.E. High-resolution mapping and characterization of open chromatin across the genome. Cell 2008, 132:311-322.
12. Brodu V., Mugat B., Roignant J.Y., Lepesant J.A., Antoniewski C. Dual requirement for the EcR/USP nuclear receptor and the dGATAb factor in an ecdysone response in Drosophila melanogaster. Mol. Cell. Biol. 1999, 19:5732-5742.
13. Brodu V., Mugat B., Fichelson P., Lepesant J.A., Antoniewski C. A UAS site substitution approach to the invivo dissection of promoters: interplay between the GATAb activator and the AEF-1 repressor at a Drosophila ecdysone response unit. Development 2001, 128:2593-2602.
14. Buecker C., Wysocka J. Enhancers as information integration hubs in development: lessons from genomics. Trends Genet. 2012, 28:276-284.
15. Cappabianca L., Thomassin H., Pictet R., Grange T. Genomic footprinting using nucleases. Methods Mol. Biol. 1999, 119:427-442.
16. Deroo B.J., Korach K.S. Estrogen receptors and human disease. J.Clin. Invest. 2006, 116:561-570.
17. Dobens L., Rudolph K., Berger E.M. Ecdysterone regulatory elements function as both transcriptional activators and repressors. Mol. Cell. Biol. 1991, 11:1846-1853.
18. Falb D., Maniatis T. Drosophila transcriptional repressor protein that binds specifically to negative control elements in fat body enhancers. Mol. Cell. Biol. 1992, 12:4093-4103.
19. Fletcher J.C., Burtis K.C., Hogness D.S., Thummel C.S. The Drosophila E74 gene is required for metamorphosis and plays a role in thepolytene chromosome puffing response to ecdysone. Development 1995, 121:1455-1465.
20. Flores G.V., Duan H., Yan H., Nagaraj R., Fu W., Zou Y., Noll M., Banerjee U. Combinatorial signaling in the specification of unique cell fates. Cell 2000, 103:75-85.
21. Gauhar Z., Sun L.V., Hua S., Mason C.E., Fuchs F., Li T.-R., Boutros M., White K.P. Genomic mapping of binding regions for the Ecdysone receptor protein complex. Genome Res. 2009, 19:1006-1013.
22. Gonsalves S.E., Neal S.J., Kehoe A.S., Westwood J.T. Genome-wide examination of the transcriptional response to ecdysteroids 20-hydroxyecdysone and ponasterone A in Drosophila melanogaster. BMC Genomics 2011, 12:475.
23. Hah N., Danko C.G., Core L., Waterfall J.J., Siepel A., Lis J.T., Kraus W.L. A rapid, extensive, and transient transcriptional response to estrogen signaling in breast cancer cells. Cell 2011, 145:622-634.
24. Hah N., Murakami S., Nagari A., Danko C.G., Kraus W.L. Enhancer transcripts mark active estrogen receptor binding sites. Genome Res. 2013, 23:1210-1223.
25. Halfon M.S., Carmena A., Gisselbrecht S., Sackerson C.M., Jiménez F., Baylies M.K., Michelson A.M. Ras pathway specificity is determined by the integration of multiple signal-activated and tissue-restricted transcription factors. Cell 2000, 103:63-74.
26. Halfon M.S., Grad Y., Church G.M., Michelson A.M. Computation-based discovery of related transcriptional regulatory modules and motifs using an experimentally validated combinatorial model. Genome Res. 2002, 12:1019-1028.
27. Hammachi F., Morrison G.M., Sharov A.A., Livigni A., Narayan S., Papapetrou E.P., O'Malley J., Kaji K., Ko M.S.H., Ptashne M., Brickman J.M. Transcriptional activation by Oct4 is sufficient for themaintenance and induction of pluripotency. Cell Rep. 2012, 1:99-109.
28. Heinz S., Benner C., Spann N., Bertolino E., Lin Y.C., Laslo P., Cheng J.X., Murre C., Singh H., Glass C.K. Simple combinations of lineage-determining transcription factors prime cis-regulatory elements required formacrophage and B cell identities. Mol. Cell 2010, 38:576-589.
29. Hodin J., Riddiford L.M. The ecdysone receptor and ultraspiracleregulate the timing and progression of ovarian morphogenesis during Drosophila metamorphosis. Dev. Genes Evol. 1998, 208:304-317.
30. Hurtado A., Holmes K.A., Ross-Innes C.S., Schmidt D., Carroll J.S. FOXA1 is a key determinant of estrogen receptor function and endocrine response. Nat. Genet. 2011, 43:27-33.
31. John S., Sabo P.J., Thurman R.E., Sung M.-H., Biddie S.C., Johnson T.A., Hager G.L., Stamatoyannopoulos J.A. Chromatin accessibility pre-determines glucocorticoid receptor binding patterns. Nat. Genet. 2011, 43:264-268.
32. Junion G., Spivakov M., Girardot C., Braun M., Gustafson E.H., Birney E., Furlong E.E.M. A transcription factor collective defines cardiac cellfate and reflects lineage history. Cell 2012, 148:473-486.
33. Kent W.J., Sugnet C.W., Furey T.S., Roskin K.M., Pringle T.H., Zahler A.M., Haussler D. The human genome browser at UCSC. Genome Res. 2002, 12:996-1006.
34. Kim T.-K., Hemberg M., Gray J.M., Costa A.M., Bear D.M., Wu J., Harmin D.A., Laptewicz M., Barbara-Haley K., Kuersten S., et al. Widespread transcription at neuronal activity-regulated enhancers. Nature 2010, 465:182-187.
35. King-Jones K., Thummel C.S. Nuclear receptors-a perspective from Drosophila. Nat. Rev. Genet. 2005, 6:311-323.
36. Kvon E.Z., Stampfel G., Yáñez-Cuna J.O., Dickson B.J., Stark A. HOT regions function as patterned developmental enhancers and have a distinct cis-regulatory signature. Genes Dev. 2012, 26:908-913.
37. Lam M.T.Y., Cho H., Lesch H.P., Gosselin D., Heinz S., Tanaka-Oishi Y., Benner C., Kaikkonen M.U., Kim A.S., Kosaka M., et al. Rev-Erbs repress macrophage gene expression by inhibiting enhancer-directed transcription. Nature 2013, 498:511-515.
38. Laval M., Pourrain F., Deutsch J., Lepesant J.A. Invivo functional characterization of an ecdysone response enhancer in the proximal upstream region of the Fbp1 gene of D. melanogaster. Mech. Dev. 1993, 44:123-138.
39. Lee T.I., Johnstone S.E., Young R.A. Chromatin immunoprecipitation and microarray-based analysis of protein location. Nat. Protoc. 2006, 1:729-748.
40. Levine M. Transcriptional enhancers in animal development and evolution. Curr. Biol. 2010, 20:R754-R763.
41. Li X.-Y., MacArthur S., Bourgon R., Nix D., Pollard D.A., Iyer V.N., Hechmer A., Simirenko L., Stapleton M., Luengo Hendriks C.L., et al. Transcription factors bind thousands of active and inactive regions in the Drosophila blastoderm. PLoS Biol. 2008, 6:e27.
42. Mullen A.C., Orlando D.A., Newman J.J., Lovén J., Kumar R.M., Bilodeau S., Reddy J., Guenther M.G., DeKoter R.P., Young R.A. Master transcription factors determine cell-type-specific responses to TGF-β signaling. Cell 2011, 147:565-576.
43. Ogawa S., Lozach J., Benner C., Pascual G., Tangirala R.K., Westin S., Hoffmann A., Subramaniam S., David M., Rosenfeld M.G., Glass C.K. Molecular determinants of crosstalk between nuclear receptors and toll-like receptors. Cell 2005, 122:707-721.
44. Ong C.-T., Corces V.G. Enhancer function: new insights into the regulation of tissue-specific gene expression. Nat. Rev. Genet. 2011, 12:283-293.
45. Poorey K., Viswanathan R., Carver M.N., Karpova T.S., Cirimotich S.M., McNally J.G., Bekiranov S., Auble D.T. Measuring chromatin interaction dynamics on the second time scale at single-copy genes. Science 2013, 342:369-372.
46. Rämet M., Manfruelli P., Pearson A., Mathey-Prevot B., Ezekowitz R.A.B. Functional genomic analysis of phagocytosis and identification of a Drosophila receptor for E. coli. Nature 2002, 416:644-648.
47. Rehorn K.P., Thelen H., Michelson A.M., Reuter R. A molecular aspect of hematopoiesis and endoderm development common to vertebrates and Drosophila. Development 1996, 122:4023-4031.
48. Riddihough G., Pelham H.R. An ecdysone response element in the Drosophila hsp27 promoter. EMBO J. 1987, 6:3729-3734.
49. Saito K., Inagaki S., Mituyama T., Kawamura Y., Ono Y., Sakota E., Kotani H., Asai K., Siomi H., Siomi M.C. A regulatory circuit for piwi by the large Maf gene traffic jam in Drosophila. Nature 2009, 461:1296-1299.
50. Segraves W.A., Hogness D.S. The E75 ecdysone-inducible gene responsible for the 75B early puff in Drosophila encodes two new members of the steroid receptor superfamily. Genes Dev. 1990, 4:204-219.
51. Sempere L.F., Sokol N.S., Dubrovsky E.B., Berger E.M., Ambros V. Temporal regulation of microRNA expression in Drosophila melanogaster mediated by hormonal signals and broad-Complex gene activity. Dev. Biol. 2003, 259:9-18.
52. Spitz F., Furlong E.E.M. Transcription factors: from enhancer binding to developmental control. Nat. Rev. Genet. 2012, 13:613-626.
53. Stark A., Lin M.F., Kheradpour P., Pedersen J.S., Parts L., Carlson J.W., Crosby M.A., Rasmussen M.D., Roy S., Deoras A.N., et al. Discovery of functional elements in 12 Drosophila genomes using evolutionary signatures. Nature 2007, 450:219-232. Harvard FlyBase curators, Berkeley Drosophila Genome ProjectBerkeley Drosophila Genome Project.
54. Tata J.R. Signalling through nuclear receptors. Nat. Rev. Mol. Cell Biol. 2002, 3:702-710.
55. Teytelman L., Thurtle D.M., Rine J., van Oudenaarden A. Highly expressed loci are vulnerable to misleading ChIP localization of multiple unrelated proteins. Proc. Natl. Acad. Sci. USA 2013, 110:18602-18607.
56. Tsai C.C., Kao H.Y., Yao T.P., McKeown M., Evans R.M. SMRTER, a Drosophila nuclear receptor coregulator, reveals that EcR-mediated repression is critical for development. Mol. Cell 1999, 4:175-186.
57. Yáñez-Cuna J.O., Dinh H.Q., Kvon E.Z., Shlyueva D., Stark A. Uncovering cis-regulatory sequence requirements for context-specific transcription factor binding. Genome Res. 2012, 22:2018-2030.
58. Yáñez-Cuna J.O., Kvon E.Z., Stark A. Deciphering the transcriptional cis-regulatory code. Trends Genet. 2013, 29:11-22.
59. Zaret K.S., Yamamoto K.R. Reversible and persistent changes inchromatin structure accompany activation of a glucocorticoid-dependent enhancer element. Cell 1984, 38:29-38.
60. Zhong S., Joung J.-G., Zheng Y., Chen Y.-R., Liu B., Shao Y., Xiang J.Z., Fei Z., Giovannoni J.J. High-throughput illumina strand-specificRNA sequencing library preparation. Cold Spring Harb. Protoc. 2011, 2011:940-949.