A view through a chromatin loop: Insights into the ecdysone activation of early genes in Drosophila

Nucleic Acids Research

Volumn 42, Issue 16, 2014, Pages 10409-10424

  Bernardo, Travis J ^a,b   Dubrovskaya, Veronica A ^a   Xie, Xie ^a   Dubrovsky, Edward B ^a  

^a FORDHAM UNIVERSITY   (United States)

^b ALBERT EINSTEIN COLLEGE OF MEDICINE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ECDYSONE; CHROMATIN;

ANIMAL CELL; ARTICLE; BROAD GENE; CHROMATIN STRUCTURE; CONTROLLED STUDY; DROSOPHILA; E74 GENE; EARLY GENE; ECDYSONE RESPONSE ELEMENT; GENE; GENE ACTIVATION; GENE LOCUS; HORMONAL REGULATION; HORMONE RESPONSIVE ELEMENT; METAMORPHOSIS; NONHUMAN; PROMOTER REGION; TRANSCRIPTION REGULATION; ANIMAL; CELL LINE; CHEMISTRY; CHROMATIN; DNA RESPONSIVE ELEMENT; DRUG EFFECTS; GENETICS; GROWTH, DEVELOPMENT AND AGING; METABOLISM; TRANSCRIPTION INITIATION;

ANIMALS; CELL LINE; CHROMATIN; DROSOPHILA; ECDYSONE; GENES, INSECT; METAMORPHOSIS, BIOLOGICAL; PROMOTER REGIONS, GENETIC; RESPONSE ELEMENTS; TRANSCRIPTIONAL ACTIVATION;

EID: 84921326680     PISSN: 03051048     EISSN: 13624962     Source Type: Journal    
DOI: 10.1093/nar/gku754     Document Type: Article

References (48)

1. Dubrovsky, E.B. (2005) Hormonal cross talk in insect development. Trends Endocrinol. Metab., 16, 6-11.
2. Ou, Q. and King-Jones, K. (2013). What goes up must come down: transcription factors have their say in making ecdysone pulses. Curr. Top. Dev. Biol. 103, 35-71.
3. Cherbas, P. and Cherbas, L. (1996) Molecular aspects of ecdysteroid hormone action. In: Gilbert, LI, Tata, JR and Atkinson, BG (eds.) Metamorphosis: Postembryonic Programming of Gene Expression in Amphibian and Insect Cells. Academic Press, San Diego, CA, USA, pp. 175-221.
4. Bernardo, T.J., Dubrovskaya, V.A., Jannat, H., Maughan, B. and Dubrovsky, E.B. (2009) Hormonal regulation of the E75 gene in Drosophila: identifying functional regulatory elements through computational and biological analysis. J. Mol. Biol., 387, 794-808.
5. Huet, F., Ruiz, C. and Richards, G. (1993) Puffs and PCR: the in vivo dynamics of early gene expression during ecdysone responses in Drosophila. Development, 118, 613-627.
6. Li, T.-R. and White, K.P. (2003) Tissue-specific gene expression and ecdysone-regulated genomic networks in Drosophila. Dev. Cell, 5, 59-72.
7. Burtis, K.C., Thummel, C.S., Jones, C.W., Karim, F.D. and Hogness, D.S. (1990) The Drosophila 74EF early puff contains E74, a complex ecdysone-inducible gene that encodes two ets-related proteins. Cell, 61, 85-99.
8. Segraves, W.A. and Hogness, D.S. (1990) The E75 ecdysone-inducible gene responsible for the 75B early puff in Drosophila encodes two new members of the steroid receptor superfamily. Genes Dev., 4, 204-219.
9. DiBello, P.R., Withers, D.A., Bayer, C.A., Fristrom, J.W. and Guild, G.M. (1991) The Drosophila Broad-Complex encodes a family of related proteins containing zinc fingers. Genetics, 129, 385-397.
10. Ashburner, M., Chihara, C., Meltzer, P. and Richards, G. (1974) Temporal control of puffing activity in polytene chromosomes. Cold Spring Harb. Sym. Quant. Biol., 38, 655-662.
11. Karim, F.D. and Thummel, C.S. (1992) Temporal coordination of regulatory gene expression by the steroid hormone ecdysone. EMBO J., 11, 4083-4093.
12. Dubrovsky, E.B., Dubrovskaya, V.A. and Berger, E.M. (2004) Hormonal regulation and functional role of Drosophila E75A orphan nuclear receptor in the juvenile hormone signaling pathway. Dev. Biol., 268, 258-270.
13. Smallwood, A. and Ren, B. (2013) Genome organization and long-range regulation of gene expression by enhancers. Curr. Opin. Cell Biol., 25, 387-394.
14. Bolton, E.C., So, A.Y., Chaivorapol, C., Haqq, C.M., Li, H. and Yamamoto, K.R. (2007) Cell-and gene-specific regulation of primary target genes by the androgen receptor. Genes Dev., 21, 2005-2017.
15. Fullwood, M.J., Liu, M.H., Pan, Y.F., Liu, J., Han, X., Mohamed, Y.B., Orlov, Y.L., Velkov, S., Ho, A., Mei, P.H. et al. (2009) An oestrogen receptorβ-bound human chromatin interactome. Nature, 462, 58-64.
16. Dubrovsky, E.B., Dubrovskaya, V.A., Bernardo, T., Otte, V., DiFilippo, R. and Bryan, H. (2011) The Drosophila FTZ-F1 nuclear receptor mediates juvenile hormone activation of E75A gene expression through an intracellular pathway. J. Biol. Chem., 286, 33689-33700.
17. Yavatkar, A.S., Lin, Y., Ross, J., Fann, Y., Brody, T. and Odenwald, W.F. (2008) Rapid detection and curation of conserved DNA via enhanced-BLAT and EvoPrinterHD analysis. BMC Genomics, 9, 106.
18. Mrázek, J. and Xie, S. (2006) Pattern locator: a new tool for finding local sequence patterns in genomic DNA sequences. Bioinformatics, 22, 3099-3100.
19. Court, F., Baniol, M., Hagege, H., Petit, J.S., Lelay-Taha, M.-N., Carbonell, F., Weber, M., Cathala, G. and Forne, T. (2011) Long-range chromatin interactions at the mouse Igf2/H19 locus reveal a novel paternally expressed long non-coding RNA. Nucleic Acids Res., 39, 5893-5906.
20. Dekker, J. (2006) The three "C" s of chromosome conformation capture: controls, controls, controls. Nat. Methods, 3, 17-21.
21. Hagège, H., Klous, P., Braem, C., Splinter, E., Dekker, J., Cathala, G., de Laat, W. and Forné, T. (2007) Quantitative analysis of chromosome conformation capture assays (3C-qPCR). Nat. Protoc., 2, 1722-1733.
22. Schmittgen, T.D. and Livak, K.J. (2008) Analyzing real-time PCR data by the comparative C(T) method. Nat. Protoc., 3, 1101-1108.
23. Heinz, S., Benner, C., Spann, N., Bertolino, E., Lin, Y.C., Laslo, P., Cheng, J.X., Murre, C., Singh, H. and Glass, C.K. (2010) Simple combinations of lineage-determining transcription factors prime cis-regulatory elements required for macrophage and B cell identities. Mol. Cell, 38, 576-589.
24. Gauhar, Z., Sun, L.V., Hua, S., Mason, C.E., Fuchs, F., Li, T.-R., Boutros, M. and White, K.P. (2009) Genomic mapping of binding regions for the Ecdysone receptor protein complex. Genome Res., 19, 1006-1013.
25. Quinlan, A.R. and Hall, I.M. (2010) BEDTools: a flexible suite of utilities for comparing genomic features. Bioinformatics, 26, 841-842.
26. Hou, C., Li, L., Qin, Z.S. and Corces, V.G. (2012) Gene density, transcription, and insulators contribute to the partition of the drosophila genome into physical domains. Mol. Cell, 48, 471-484.
27. Celniker, S.E., Dillon, L.A.L., Gerstein, M.B., Gunsalus, K.C., Henikoff, S., Karpen, G.H., Kellis, M., Lai, E.C., Lieb, J.D., MacAlpine, D.M. et al. (2009) Unlocking the secrets of the genome. Nature, 459, 927-930.
28. Tsai, S.Y., Tsai, M.J. and O'Malley, B.W. (1989) Cooperative binding of steroid hormone receptors contributes to transcriptional synergism at target enhancer elements. Cell, 57, 443-448.
29. Liu, H.C. and Towle, H.C. (1994) Functional synergism between multiple thyroid hormone response elements regulates hepatic expression of the rat S14 gene. Mol. Endocrinol., 8, 1021-1037.
30. Reid, K.J., Hendy, S.C., Saito, J., Sorensen, P. and Nelson, C.C. (2001) Two classes of androgen receptor elements mediate cooperativity through allosteric interactions. J. Biol. Chem., 276, 2943-2952.
31. Klinge, C.M. (2001) Estrogen receptor interaction with estrogen response elements. Nucleic Acids Res., 29, 2905-2919.
32. Zhang, Y., Zolfaghari, R. and Ross, A.C. (2010) Multiple retinoic acid response elements cooperate to enhance the inducibility of CYP26A1 gene expression in liver. Gene, 464, 32-43.
33. Heneghan, A.F., Connaghan-Jones, K.D., Miura, M.T. and Bain, D.L. (2007) Coactivator assembly at the promoter: efficient recruitment of SRC2 is coupled to cooperative DNA binding by the progesterone receptor. Biochemistry, 46, 11023-11032.
34. Connaghan-Jones, K.D., Heneghan, A.F., Miura, M.T. and Bain, D.L. (2008) Thermodynamic dissection of progesterone receptor interactions at the mouse mammary tumor virus promoter: monomer binding and strong cooperativity dominate the assembly reaction. J. Mol. Biol., 377, 1144-1160.
35. Splinter, E. and de Laat, W. (2011) The complex transcription regulatory landscape of our genome: control in three dimensions. EMBO J., 30, 4345-4355.
36. Montavon, T., Soshnikova, N., Mascrez, B., Joye, E., Thevenet, L., Splinter, E., de Laat, W., Spitz, F. and Duboule, D. (2011) A regulatory archipelago controls Hox genes transcription in digits. Cell, 147, 1132-1145.
37. Bonéy-Montoya, J., Ziegler, Y.S., Curtis, C.D., Montoya, J.A. and Nardulli, A.M. (2010) Long-range transcriptional control of progesterone receptor gene expression. Mol. Endocrinol., 24, 346-358.
38. Kabotyanski, E.B., Rijnkels, M., Freeman-Zadrowski, C., Buser, A.C., Edwards, D.P. and Rosen, J.M. (2009) Lactogenic hormonal induction of long distance interactions between beta-casein gene regulatory elements. J. Biol. Chem., 284, 22815-22824.
39. Hakim, O., Sung, M.-H., Voss, T.C., Splinter, E., John, S., Sabo, P.J., Thurman, R.E., Stamatoyannopoulos, J.A., de Laat, W. and Hager, G.L. (2011) Diverse gene reprogramming events occur in the same spatial clusters of distal regulatory elements. Genome Res., 21, 697-706.
40. Jin, F., Li, Y., Dixon, J.R., Selvaraj, S., Ye, Z., Lee, A.Y., Yen, C.-A., Schmitt, A.D., Espinoza, C.A. and Ren, B. (2013) A high-resolution map of the three-dimensional chromatin interactome in human cells. Nature, 503, 290-294.
41. Osmanbeyoglu, H.U., Lu, K.N., Oesterreich, S., Day, R.S., Benos, P.V., Coronnello, C. and Lu, X. (2013) Estrogen represses gene expression through reconfiguring chromatin structures. Nucleic Acids Res., 41, 8061-8071.
42. Tsai, C.C., Kao, H.Y., Yao, T.P., McKeown, M. and Evans, R.M. (1999) SMRTER, a Drosophila nuclear receptor coregulator, reveals that EcR-mediated repression is critical for development. Mol. Cell, 4, 175-186.
43. Ong, C.-T. and Corces, V.G. (2011) Enhancer function: new insights into the regulation of tissue-specific gene expression. Nat. Rev. Genet., 12, 283-293.
44. Hou, C., Dale, R. and Dean, A. (2010) Cell type specificity of chromatin organization mediated by CTCF and cohesin. Proc. Natl. Acad. Sci. USA, 107, 3651-3656.
45. Junier, I., Dale, R.K., Hou, C., Kepes, F. and Dean, A. (2012) CTCF-mediated transcriptional regulation through cell type-specific chromosome organization in the β-globin locus. Nucleic Acids Res., 40, 7718-7727.
46. Phillips-Cremins, J.E., Sauria, M.E.G., Sanyal, A., Gerasimova, T.I., Lajoie, B.R., Bell, J.S.K., Ong, C.-T., Hookway, T.A., Guo, C., Sun, Y. et al. (2013) Architectural protein subclasses shape 3D organization of genomes during lineage commitment. Cell, 153, 1281-1295.
47. Lehmann, M. and Korge, G. (1996) The fork head product directly specifies the tissue-specific hormone responsiveness of the Drosophila Sgs-4 gene. EMBO J. 15, 4825-4834.
48. Brodu, V., Mugat, B., Roignant, J.Y., Lepesant, J.A. and Antoniewski, C. (1999) Dual requirement for the EcR/USP nuclear receptor and the dGATAb factor in an ecdysone response in Drosophila melanogaster. Mol. Cell. Biol., 19, 5732-5742.