The ligand-binding domains of the three RXR-USP nuclear receptor types support distinct tissue and ligand specific hormonal responses in transgenic Drosophila

Developmental Biology

Volumn 330, Issue 1, 2009, Pages 1-11

  Beck, Yannick ^a,b,c   Delaporte, Claude ^a,b,c   Moras, Dino ^a,b,c   Richards, Geoff ^d   Billas, Isabelle M L ^a,b,c  

^a INSTITUT DE GÉNÉTIQUE ET DE BIOLOGIE MOLÉCULAIRE ET CELLULAIRE   (France)

^b INSERM   (France)

^c CNRS   (France)

^d HFSP (Human Frontier Science Program)   (France)

Author keywords

Drosophila; GAL4; Juvenile hormone; Nuclear receptor; Retinoid X receptor; Tribolium; Ultraspiracle

Indexed keywords

CELL NUCLEUS RECEPTOR; ECDYSONE RECEPTOR; JUVENILE HORMONE; RETINOID X RECEPTOR;

ARTICLE; BEETLE; DROSOPHILA MELANOGASTER; FLY; HORMONAL REGULATION; HORMONE RESPONSE; IN VIVO STUDY; LEPIDOPTERA; LIGAND BINDING; NONHUMAN; ORGAN CULTURE; PRIORITY JOURNAL; TISSUE SPECIFICITY; TRANSGENIC ANIMAL; TRIBOLIUM; VERTEBRATE;

ANIMALIA; COLEOPTERA; DROSOPHILA MELANOGASTER; HEXAPODA; TRIBOLIUM (BEETLE); TRIBOLIUM CASTANEUM; VERTEBRATA;

EID: 67349092121     PISSN: 00121606     EISSN: 1095564X     Source Type: Journal    
DOI: 10.1016/j.ydbio.2008.12.042     Document Type: Article

References (53)

1. Bai J., Uehara Y., and Montell D.J. Regulation of invasive cell behavior by Taiman, a Drosophila protein related to AIB1, a steroid receptor coactivator amplified in breast cancer. Cell 103 (2000) 1047-1058
2. Baker K.D., Shewchuk L.M., Kozlova T., Makishima M., Hassell A., Wisely B., Caravella J.A., Lambert M.H., Reinking J.L., Krause H., et al. The Drosophila orphan nuclear receptor DHR38 mediates an atypical ecdysteroid signaling pathway. Cell 113 (2003) 731-742
3. Beckstead R., Ortiz J.A., Sanchez C., Prokopenko S.N., Chambon P., Losson R., and Bellen H.J. Bonus, a Drosophila homolog of TIF1 proteins, interacts with nuclear receptors and inhibits betaFTZ-F1-dependent transcription. Mol. Cell 7 (2001) 753-765
4. Berger E.M., Goudie K., Klieger L., Berger M., and DeCato R. The juvenile hormone analogue, methoprene, inhibits ecdysterone induction of small heat shock protein gene expression. Dev. Biol. 151 (1992) 410-418
5. Billas I.M.L., Moulinier L., Rochel N., and Moras D. Crystal structure of the ligand binding domain of the ultraspiracle protein USP, the ortholog of RXRs in insects. J. Biol. Chem. 276 (2001) 7465-7474
6. Bonneton F., Zelus D., Iwema T., Robinson-Rechavi M., and Laudet V. Rapid divergence of the ecdysone receptor in Diptera and Lepidoptera suggests coevolution between EcR and USP-RXR. Mol. Biol. Evol. 20 (2003) 541-553
7. Bonneton F., Brunet F.G., Kathirithamby J., and Laudet V. The rapid divergence of the ecdysone receptor is a synapomorphy for Mecopterida that clarifies the Strepsiptera problem. Insect Mol. Biol. 15 (2006) 351-362
8. Bonneton F., Chaumot A., and Laudet V. Annotation of Tribolium nuclear receptors reveals an increase in evolutionary rate of a network controlling the ecdysone cascade. Insect Biochem. Mol. Biol. 38 (2008) 416-429
9. Bourguet W., Ruff M., Chambon P., Gronemeyer H., and Moras D. Crystal structure of the ligand-binding domain of the human nuclear receptor RXR-alpha. Nature 375 (1995) 377-382
10. Bouton D., Escriva H., de Mendonca R.L., Glineur C., Bertin B., Noel C., Robinson-Rechavi M., de Groot A., Cornette J., Laudet V., et al. A conserved retinoid X receptor (RXR) from the mollusk Biomphalaria glabrata transactivates transcription in the presence of retinoids. J. Mol. Endocrinol. 34 (2005) 567-582
11. Carmichael J.A., Lawrence M.C., Graham L.D., Pilling P.A., Epa V.C., Noyce L., Lovrecz G., Winkler D.A., Pawlak-Skrzecz A., Eaton R.E., et al. The X-ray structure of a hemipteran ecdysone receptor ligand-binding domain: comparison with a lepidopteran ecdysone receptor ligand-binding domain and implications for insecticide design. J. Biol. Chem. 280 (2005) 22258-22269
12. Christianson A.M.K., King D.L., Hatzivassiliou E., Casas J., Hallenbeck P.L., Nikodem V.M., Mitsialis S.A., and Kafatos F.C. DNA binding and heterodimerization of the Drosophila transcription factor chorion factor 1 / ultraspiracle. Proc. Natl. Acad. Sci. U. S. A. 89 (1992) 11503-11507
13. Clayton G.M., Peak-Chew S.Y., Evans R.M., and Schwabe J.W.R. The structure of the ultraspiracle ligand-binding domain reveals a nuclear receptor locked in an inactive conformation. Proc. Natl. Acad. Sci. U. S. A. 98 (2001) 1549-1554
14. de Urquiza A.M., Liu S., Sjoeberg M., Zetterstroem R.H., Griffiths W., Sjoevall J., and Perlmann T. Docosahexaenoic acid, a ligand for the retinoid X receptor in mouse brain. Science 290 (2000) 2140-2144
15. Dhadialla T.S., Carlson G.R., and Le D.P. New insecticides with ecdysteroidal and juvenile hormone activity. Annu. Rev. Entomol. 43 (1998) 545-569
16. Dressel U., Thormeyer D., Altincicek B., Paululat A., Eggert M., Schneider S., Tenbaum S.P., Renkawitz R., and Baniahmad A. Alien, a highly conserved protein with characteristics of a corepressor for members of the nuclear hormone receptor superfamily. Mol. Cell. Biol. 19 (1999) 3383-3394
17. Dubrovskaya V.A., Berger E.M., and Dubrovsky E.B. Juvenile hormone regulation of the E75 nuclear receptor is conserved in Diptera and Lepidoptera. Gene 340 (2004) 171-177
18. Dubrovsky E.B. Hormonal cross talk in insect development. Trends Endocrinol. Metab. 16 (2005) 6-11
19. Dubrovsky E.B., Dubrovskaya V.A., Bilderback A.L., and Berger E.M. The isolation of two juvenile hormone-inducible genes in Drosophila melanogaster. Dev. Biol. 224 (2000) 486-495
20. Dubrovsky E.B., Dubrovskaya V.A., and Berger E.M. Juvenile hormone signaling during oogenesis in Drosophila melanogaster. Insect Biochem. Mol. Biol. 32 (2002) 1555-1565
21. Egea P.F., Mitschler A., Rochel N., Ruff M., Chambon P., and Moras D. Crystal structure of the human RXRalpha ligand-binding domain bound to its natural ligand 9-cis retinoic acid. EMBO J. 19 (2000) 2592-2601
22. Egea P.F., Mitschler A., and Moras D. Molecular recognition of agonist ligands by RXRs. Mol. Endocrinol. 16 (2002) 987
23. Fang F., Xu Y., Jones D., and Jones G. Interactions of ultraspiracle with ecdysone receptor in the transduction of ecdysone- and juvenile hormone-signaling. FEBS J. 272 (2005) 1577-1589
24. Gates J., Lam G., Ortiz J.A., Losson R., and Thummel C.S. rigor mortis encodes a novel nuclear receptor interacting protein required for ecdysone signaling during Drosophila larval development. Development 131 (2004) 25-36
25. Harmon M.A., Boehm M., Heyman R.A., and Mangelsdorf D.J. Activation of mammalian retinoid X receptors by the insect growth regulator methoprene. Proc. Natl. Acad. Sci. U. S. A. 92 (1995) 6157-6160
26. Heyman R.A., Mangelsdorf D.J., Dyck J.A., Stein R.B., Eichele G., Evans R.M., and Thaller C. 9-cis retinoic acid is a high affinity ligand for the retinoid X receptor. Cell 68 (1992) 397-406
27. Huet F., Ruiz C., and Richards G. Sequential gene activation by ecdysone in Drosophila melanogaster: the hierarchical equivalence of early and early late genes. Development 121 (1995) 1195-1204
28. Iwema T., Billas I.M.L., Beck Y., Bonneton F., Nierengarten H., Chaumot A., Richards G., Laudet V., and Moras D. Structural and functional characterization of a novel type of ligand-independent RXR-USP receptor. EMBO J. 26 (2007) 3770-3782
29. Jones G., and Sharp P.A. Ultraspiracle: an invertebrate nuclear receptor for juvenile hormones. Proc. Natl. Acad. Sci. U. S. A. 94 (1997) 13499-13503
30. Jones G., Jones D., Teal P., Sapa A., and Wozniak M. The retinoid-X receptor ortholog, ultraspiracle, binds with nanomolar affinity to an endogenous morphogenetic ligand. FEBS J. 273 (2006) 4983-4996
31. King-Jones K., and Thummel C.S. Nuclear receptors-a perspective from Drosophila. Nat Rev. Genet. 6 (2005) 311-323
32. Kitareewan S., Burka L.T., Tomer K.B., Parker C.E., Deterding L.J., Stevens R.D., Forman B.M., Mais D.E., Heyman R.A., McMorris T., et al. Phytol metabolites are circulating dietary factors that activate the nuclear receptor RXR. Mol. Biol. Cell 7 (1996) 1153-1166
33. Koelle M.R., Talbot W.S., Segraves W.A., Bender M., Cherbas P., and Hogness D.S. The Drosophila EcR gene encodes an ecdysone receptor, a new member of the steroid receptor superfamily. Cell 67 (1991) 59-77
34. Kozlova T., and Thummel C.S. Spatial patterns of ecdysteroid receptor activation during the onset of Drosophila metamorphosis. Development 129 (2002) 1739-1750
35. Kozlova T., and Thummel C.S. Methods to characterize Drosophila nuclear receptor activation and function in vivo. Methods Enzymol. 364 (2003) 475-490
36. Lee T., Marticke S., Sung C., Robinow S., and Luo L. Cell-autonomous requirement of the USP/EcR-B ecdysone receptor for mushroom body neuronal remodeling in Drosophila. Neuron 28 (2000) 807-818
37. Lengqvist J., Mata de Urquiza A., Bergman A.C., Willson T.M., Sjovall J., Perlmann T., and Griffiths W.J. Polyunsaturated fatty acids including docosahexaenoic and arachidonic acid bind to the retinoid X receptor {alpha} ligand-binding domain. Mol. Cell Proteomics 3 (2004) 692-703
38. Levin A.A., Sturzenbecker L.J., Kazmer S., Bosakowski T., Huselton C., Allenby G., Speck J., Kratzeisen C., Rosenberger M., Lovey A., et al. 9-cis retinoic acid stereoisomer binds and activates the nuclear receptor RXR alpha. Nature 355 (1992) 359-361
39. Mangelsdorf D.J., Ong E.S., Dyck J.A., and Evans R.M. Nuclear receptor that identifies a novel retinoic acid response pathway. Nature 345 (1990) 224-229
40. Oro A.E., McKeown M., and Evans R.M. Relationship between the product of the Drosophila ultraspiracle locus and the vertebrate retinoid X receptor. Nature 347 (1990) 298-301
41. Palanker L., Necakov A.S., Sampson H.M., Ni R., Hu C., Thummel C.S., and Krause H.M. Dynamic regulation of Drosophila nuclear receptor activity in vivo. Development 133 (2006) 3549-3562
42. Petryk A., Warren J.T., Marques G., Jarcho M.P., Gilbert L.I., Kahler J., Parvy J.P., Li Y., Dauphin-Villemant C., and O'Connor M.B. Shade is the Drosophila P450 enzyme that mediates the hydroxylation of ecdysone to the steroid insect molting hormone 20-hydroxyecdysone. Proc. Natl. Acad. Sci. 100 (2003) 13773-13778
43. Saez E., Nelson M.C., Eshelman B., Banayo E., Koder A., Cho G.J., and Evans R.M. Identification of ligands and coligands for the ecdysone-regulated gene switch. Proc. Natl. Acad. Sci. U. S. A. 97 (2000) 14512-14517
44. Schubiger M., Wade A.A., Carney G.E., Truman J.W., and Bender M. Drosophila EcR-B ecdysone receptor isoforms are required for larval molting and for neuron remodeling during metamorphosis. Development 125 (1998) 2053-2062
45. Sutherland J.D., Kozlova T., Tzertzinis G., and Kafatos F.C. Drosophila hormone receptor 38: a second partner for Drosophila USP suggests an unexpected role for nuclear receptors of the nerve growth factor-induced B-type. Proc. Natl. Acad. Sci. U. S. A. 92 (1995) 7966-7970
46. Szanto A., Narkar V., Shen Q., Uray I.P., Davies P.J., and Nagy L. Retinoid X receptors: X-ploring their (patho)physiological functions. Cell Death. Differ. 11 Suppl. 2 (2004) S126-S143
47. Talbot W.S., Swyryd E.A., and Hogness D.S. Drosophila tissues with different metamorphic responses to ecdysone express different ecdysone receptor isoforms. Cell 73 (1993) 1323-1337
48. Thomas H.E., Stunnenberg H.G., and Stewart A.F. Heterodimerization of the Drosophila ecdysone receptor with retinoid X receptor and ultraspiracle. Nature 362 (1993) 471-475
49. Truman J.W., Talbot W.S., Fahrbach S.E., and Hogness D.S. Ecdysone receptor expression in the CNS correlates with stage-specific responses to ecdysteroids during Drosophila and Manduca development. Development 120 (1994) 219-234
50. Tsai C.-C., Kao H.-Y., Yao T.-P., McKeown M., and Evans R.M. SMRTER, a Drosophila nuclear receptor coregulator, reveals that EcR-mediated repression is critical for development. Mol. Cell 4 (1999) 175-186
51. Yao T.-P., Segraves W.A., Oro A.E., McKeown M., and Evans R.M. Drosophila ultraspiracle modulates ecdysone receptor function via heterodimer formation. Cell 71 (1992) 63-72
52. Yao T.-P., Forman B.M., Jiang Z., Cherbas L., Chen J.-D., McKeown M., Cherbas P., and Evans R.M. Functional ecdysone receptor is the product of EcR and ultraspiracle genes. Nature 366 (1993) 476-479
53. Zhou B., Hiruma K., Shinoda T., and Riddiford L.M. Juvenile hormone prevents ecdysteroid-induced expression of Broad complex RNAs in the epidermis of the tobacco hornworm, Manduca sexta. Dev. Biol. 203 (1998) 233-244