Ecdysteroid receptor and ultraspiracle from Chironomus tentans (Insecta) are phosphoproteins and are regulated differently by molting hormone

Insect Biochemistry and Molecular Biology

Volumn 28, Issue 4, 1998, Pages 265-275

  Rauch, Peter ^a   Grebe, Marco ^a   Elke, Carsten ^b   Spindler, Klaus Dieter ^b   Spindler Barth, Margarethe ^a  

^a HEINRICH HEINE UNIVERSITY   (Germany)

^b UNIVERSITY OF ULM   (Germany)

Author keywords

Chironomus tentans cell line; Ecdysone receptor; Ligand induced changes; Phosphorylation; Ultraspiracle

Indexed keywords

ECDYSONE; ECDYSTEROID; ECDYSTERONE; INSECT PROTEIN; LIGAND; MURISTERONE; PHOSPHATASE; PHOSPHOPROTEIN; PONASTERONE A; RECEPTOR PROTEIN; SERINE; STEROID HORMONE; STEROID RECEPTOR; THREONINE; TRANSCRIPTION FACTOR; ULTRASPIRACLE PROTEIN; UNCLASSIFIED DRUG;

ANIMAL; ANIMAL ANATOMY; ANIMAL CELL; ARTICLE; BINDING AFFINITY; CELL LINE; CHEMISTRY; CHIRONOMIDAE; CONTROLLED STUDY; ELECTROPHORETIC MOBILITY; EPITHELIUM CELL; IN VITRO STUDY; LIGAND BINDING; METABOLISM; MOLTING; NONHUMAN; PHOSPHORYLATION; PHYSIOLOGY; PROTEIN ANALYSIS; PROTEIN PHOSPHORYLATION; PROTEIN PROCESSING;

ANIMAL STRUCTURES; ANIMALS; CELL LINE; CHIRONOMIDAE; ECDYSONE; EPITHELIAL CELLS; LIGANDS; MOLTING; PHOSPHOPROTEINS; PHOSPHORYLATION; PROTEIN PROCESSING, POST-TRANSLATIONAL; RECEPTORS, STEROID;

ANIMALIA; CHIRONOMIDAE; CHIRONOMUS TENTANS; HEXAPODA; INSECTA;

EID: 0032052753     PISSN: 09651748     EISSN: None     Source Type: Journal    
DOI: 10.1016/S0965-1748(98)00026-5     Document Type: Article

References (73)

1. Andres A.J., Fletcher J.C., Karim F.D., Thummel C.S. Molecular analysis of the initiation of insect metamorphosis: a comparative study of Drosophila ecdysone-regulated transcription. Dev. Biol. 160:1993;388-404.
2. Au-Fliegner M., Helmer E., Casanova J., Raaka B.M., Samuels H.H. The conserved ninth C-terminal heptad in thyroid hormone and retinoic acid receptors mediates diverse responses by affecting heterodimer but not homodimer formation. Mol. Cell. Biol. 13:1993;5725-5737.
3. Bai, W.L. and Weigel, N.L., 1995. Phosphorylation and steroid hormone action. In: Litwack G. (Ed.), Vitamins and Hormones - Advances in Research and Applications 51, Academic Press Inc., San Diego, USA. pp. 289-313.
4. Bairoch A., Bucher P., Hofmann K. The PROSITE database, its status in 1995. Nucl. Acids Res. 24:1995;189-196.
5. Blok L.J., de Ruiter P.E., Brinkmann A.O. Androgen receptor phosphorylation. Endocr. Res. 22:1996;197-219.
6. Bradford M.M. A rapid and sensitive method for quantitation of protein utilising the principle of protein-dye binding. Anal. Biochem. 72:1976;248-254.
7. Chartier F.L., Bossu J.P., Laudet V., Fruchart J.C., Laine B. Cloning ands sequencing of cDNAs encoding the human hepatocyte nuclear factor 4 indicates the presence of two isoforms in human liver. Gene. 147:1994;269-272.
8. Cho W.L., Kapitskaya M.Z., Raikhel A.S. Mosquito ecdysteroid receptor: analysis of cDNA and expression during vitellogenesis. Insect Biochem. Mol. Biol. 25:1995;19-28.
9. Dinan L. Ecdysteroid receptors in a tumorous blood cell line of Drosophila melanogaster. Arch. Insect Biochem. Physiol. 2:1985;295-317.
10. Fisk G.J., Thummel C.S. Isolation, regulation, and DNA-binding properties of three Drosophila nuclear hormone receptor superfamily members. Proc. Natl. Acad. Sci. USA. 92:1995;10604-10608.
11. Forman B.M., Samuels H.H. Minireview: interactions among a subfamily of nuclear hormone receptors: the regulatory zipper hypothesis. Mol. Endocrinol. 4:1990;1293-1302.
12. Forman B.M., Yang C.R., Au M., Casanova J., Ghysdael J., Samuels H.H. A domain containing leucine-zipper-like motifs mediate novel in vivo interactions between the thyroid hormone and retinoic acid receptors. Mol. Endocrinol. 3:1989;1610-1626.
13. Fujiwara H., Jindra M., Newitt R., Palli S.R., Hiruma K., Riddiford L.M. Cloning of an ecdysone receptor homolog from Manduca sexta and the developmental profile of its mRNA in wings. Insect Biochem. Molec. Biol. 25:1995;845-856.
14. Georgakopoulos A., Tsawdaroglou N. Insulin potentiates the transactivation potency of the glucocorticoid receptor. FEBS Lett. 381:1996;177-182.
15. Handler A.M., Maroy P. Ecdysteroid receptors in Drosophila melanogaster adult females. Mol. Cell. Endocrinol. 63:1989;103-109.
16. 1: a functional ecdysone receptor from the sheep blowfly Lucilia cuprina. Insect Biochem. Mol. Biol. 27:1997;479-488.
17. Hatt P.J., Moriniere M., Oberlander H., Porcheron P. Roles for insulin and ecdysteroids in differentation of an insect cell line of epidermal origin. In Vitro Cell Dev. Biol. 30A:1994;717-720.
18. Henrich V.C., Sliter T.J., Lubahn D.B., MacIntyre A., Gilbert L.J. A steroid/thyroid hormone receptor superfamily member in Drosophila melanogaster that shares extensive sequence similarity with a mammalian homologue. Nucl. Acids Res. 18:1990;4143-4148.
19. Henrich V.C., Szekely A.A., Kim S.J., Brown N.E., Antoniewski C., Hayden M.A., Lepesant J.A., Gilbert L.I. Expression and function of the ultraspiracle (usp) gene during development of Drosophila melanogaster. Dev. Biol. 165:1994;38-52.
20. Hoppe I.A., Struhl K. GCN4, a eukaryotic transcriptional activator protein, binds as dimer to target DNA. EMBO J. 6:1987;2781-2784.
21. 3 modulates phosphorylation of serin 205 in the human vitamin D receptor: site-directed mutagenesis of this residue promotes alternative phosphorylation. Biochemistry. 33:1994;4300-4311.
22. Hsieh J.-C., Jurutka P.W., Galligan M.A., Terpening C.M., Haussler C.A., Samuels D.S., Shimuzu Y., Nobuyoshy S., Haussler M.R. Human vitamin D receptor is selectively phosphorylated by protein kinase C on serine 51, a residue crucial to its transactivation function. Proc. Natl. Acad. Sci. USA. 88:1991;9315-9319.
23. Hunter T., Karin M. The regulation of transcription by phosphorylation. Cell. 70:1992;375-387.
24. Imhof M.O., Rusconi S., Lezzi M. Cloning of a Chironomus tentans cDNA encoding a protein (cEcRH) homologous to the Drosophila melanogaster ecdysteroid receptor (dEcR). Insect Biochem. Mol. Biol. 23:1993;115-124.
25. Jiang G.Q., Nepomuceno L., Yang Q., Sladek F.M. Serine/threonin phosphorylation of orphan receptor hepatocyte nuclear factor 4. Arch. Biochem. Biophys. 340(1):1997;1-9.
26. Jindra M., Huang J.Y., Malone F., Asahina M., Riddiford L.M. Identification and mRNA developmental profiles of two ultraspiracle isoforms in the epidermis and wings of Manduca sexta. Insect Mol. Biol. 6:1997;41-53.
27. Jurutka P.W., Hsieh J.C., Nakajima S., Haussler C.A., Whitfield G.K., Haussler M.R. Human vitamin D receptor phosphorylation by casein kinase II at Ser-208 potentiates transcriptional activation. Proc. Natl. Acad. Sci. USA. 93:1996;3519-3524.
28. Karim F.D., Thummel C.S. Temporal coordination of regulatory gene expression by the steroid hormone ecdysone. EMBO J. 11:1992;4083-4093.
29. Kapitskaya M., Wang S., Cress D.E., Dhadialla T.S., Raikhel A.S. The mosquito ultraspiracle homologue, a partner of ecdysteroid receptor heterodimer: cloning and characterization of isoforms expressed during vitellogenesis. Mol. Cell. Endocrinol. 121:1996;119-132.
30. Katz D., Reginato M.J., Lazar M.A. Functional regulation of thyroid hormone receptor variant Trα2 by phosphorylation. Mol. Cell Biol. 15:1995;2341-2348.
31. Khoury Christianson A.M., King D.L., Hatzivassiliou E., Casas J.E., Hallenbeck P.L., Nikodem V.M., Mitsialis S.A., Kafatos F.C. DNA binding and heterodimerization of the Drosophila transcription factor chorion factor 1/ultraspiracle. Proc. Natl. Acad. Sci. USA. 89:1992;11503-11507.
32. Kothapalli R., Palli S.R., Ladd T.R., Sohi S.S., Cress D., Dhadialla T.S., Tzertzinis G., Retnakaran A. Cloning and developmental expression of the ecdysone receptor gene from the spruce budworm, Choristoneura fumiferana. Dev. Genet. 17:1995;319-330.
33. Khyse-Andersen J. Electroblotting of multiple gels: a simple apparatus without buffer tank for rapid transfer of proteins from polyacrylamide to nitrocellulose. J. Biochem. Biophys. Meth. 10:1984;203-209.
34. Koelle M.R., Talbot W.S., Segraves W.A., Bender M.T., Cherbas P., Hogness D.S. The Drosophila EcR gene encodes an ecdysone receptor, a new member of the steroid receptor superfamily. Cell. 67:1991;59-77.
35. Kouzarides T., Ziff E. The role of the leucine zipper in the fos-jun interaction. Nature. 336:1988;646-651.
36. Kuiper G.G.J.M., Brinkman A.O. Steroid hormone receptor phosphorylation - is there a physiological role. Mol. Cell. Endocrinol. 100:1994;103-107.
37. Kuppert P., Spindler K.-D. Characterization of nuclear ecdysteroid receptors from crayfish integument. J. Steroid Biochem. 17:1982;205-210.
38. Laemmli U.K. Cleavage of structural proteins during the assembly of the head of bacteriophage T4. Nature. 27:1970;680-685.
39. Lammerding-Köppel, M., Spindler-Barth, M., Lezzi, M. and Spindler, K.-D. (in press) Immunuhistochemical localization of ecdysteroid receptor and ultraspiracle in the epithelial cell line from Chironomus tentans (Insecta, Diptera), Tissue Cell
40. Londershausen M., Kuppert P., Spindler K.-D. Ecdysteroid receptors: a comparison of cytoplasmic and nuclear receptors from crayfish hypodermis. Hoppe Seyler's Z Physiol. Chem. 363:1982;797-802.
41. Martin P., Shearn A. Development of Drosophila imaginal discs in vitro. Effects of ecdysone concentration and insulin. J. Exp. Zool. 211:1980;291-301.
42. Miyajima N., Kadowaki Y., Fukushige S., Shimizu S., Semba K., Yamanashi Y., Matsubara K., Toyoshima K., Yamamoto T. Identification of two novel members of erbA superfamily by molecular cloning: the gene products of the two are highly related to each other. Nucl. Acids Res. 16:1988;11057-11074.
43. Mlodzik M., Hiromi Y., Weber U., Goodman C.S., Rubin G.M. The Drosophila seven-up gene, a member of the steroid receptor gene superfamily controls photoreceptor cell fate. Cell. 60:1990;211-224.
44. Mouillet J.F., Delbecque J.P., Quennedey B., Delachambre J. Cloning of two putative ecdysteroid receptor isoforms from Tenebrio molitor and their developmental expression in the epidermis during metamorphosis. Eur. J. Biochem. 248:1997;856-863.
45. Perlmann T., Umesono K., Rangarajan P.N., Forman B.M., Evans R.M. Two distinct dimerization interfaces differentially modulate target gene specificity of nuclear hormone receptors. Mol. Endocrinol. 10:1996;958-966.
46. Pignoni F., Baldarelli R.M., Steingrimsson E., Diaz R.J., Patapoutin A., Merriam J.R., Lengyel J.A. The Drosophila gene tailless is expressed at the embryonic termini and is a member of the steroid receptor superfamily. Cell. 62:1990;151-163.
47. Rauch, P., Grebe, M. and Spindler-Barth, M., 1998. Characterization of RH 5992 resistant subclones of the epithelial cell line from Chironomus tentans.
48. Rochette-Egly C., Ouladabdelghani M., Staub A., Pfister V., Scheuer I., Chambon P., Gaub M.P. Phosphorylation of the retinoic acid receptor α Boy protein kinase A. Mol. Endocrinol. 9:1995;860-871.
49. Sassone-Corsi P., Ransone L.J., Lamph W.W., Verma I.M. Direct interaction between fos and jun nuclear oncoproteins: role of the "leucine zipper" domain. Nature. 336:1988;692-695.
50. Scatchard G. The attractions of proteins for small molecules and ions. Ann. NY Acad. Sci. 51:1949;660-672.
51. Spindler, K.-D., Dinan, L. and Londershausen, M., 1984. On the mode of action of ecdysteroids in crustaceans. In: Hoffmann J., Porchet M. (Eds.). Biosynthesis, Metabolism and Mode of Action of Invertebrate Hormones. Springer-Verlag, Berlin. pp. 255-264.
52. Spindler-Barth M., Spindler K.-D. Ecdysteroid resistant subclones of the epithelial cell line from Chironomus tentans. I. Selection and characterization of the resistant clones. In Vitro Cell. Dev. Biol. Animal. 36:1998;116-122.
53. Stevens B., Alvarez C.M., Bohman R., O'Connor J.D. An ecdysteroid-induced alteration in the cell cycle of cultured Drosophila cells. Cell. 22:1980;675-682.
54. Sutherland J.D., Kozlova T., Tzertzinis G., Kafatos F.C. Drosophila hormone receptor 38: a second partner for the Drosophila USP suggests an unexpected role for nuclear receptors of the nerve growth factor-induced protein B type. Proc. Natl. Acad. Sci. USA. 92:1995;7966-7970.
55. Swevers L., Drevet J.R., Lunke M.D., Iatrou K. The silkworm homolog of the Drosophila ecdysone receptor (B1 isoform): cloning and analysis of expression during follicular cell differentiation. Insect Biochem. Mol. Biol. 25:1995;857-866.
56. Talbot W.S., Swyryd E.A., Hogness D.S. Drosophila tissues with different metamorphic responses to ecdysone express different ecdysone receptor isoforms. Cell. 73:1993;1323-1337.
57. Thummel C.S. From embryogenesis to metamorphosis: the regulation and function of Drosophila nuclear receptor superfamily members. Cell. 83:1995;871-877.
58. Turberg A., Spindler K.-D. Properties of nuclear and cytosolic ecdysteroid receptors from an epithelial cell line from Chironomus tentans. J. Insect Physiol. 38:1992;81-91.
59. Turgeon J.L., Waring D.W. Functional cross-talk between receptors for peptide and steroid hormones. Trends Endocrinol. Metab. 3:1992;360-365.
60. Tzertzinis G., Maleck A., Kafatos F.C. BMCF1, a Bombyx mori RXR-type receptor related to the Drosophila ultraspiracle. J. Mol. Biol. 258:1994;479-486.
61. Vögtli, M. et al. (in preparation).
62. Wang L.-H., Tsai S.Y., Cook R.G., Beattie W.G., Tsai M.-J., O'Malley B.W. COUP transcription factor is a member of the steroid receptor superfamily. Nature. 340:1989;163-166.
63. Wegmann I.S., Quack S., Spindler K.-D., Dorsch-Häsler K., Vögtl M., Lezzi M. Immunological studies on the developmental and chromosomal distribution of ecdysteroid receptor protein in Chironomus tentans. Arch. Insect Biochem. Physiol. 30:1995;95-114.
64. Weigel N.L. Steroid hormone receptors and their phosphorylation. Biochem. J. 319:1996;657-667.
65. Wyss C. Chironomus tentans epithelial cell lines sensitive to ecdysteroids, juvenile hormones, insulin and heat shock. Exp. Cell Res. 139:1982;309-319.
66. Yao T.P., Forman B.M., Jiang Z., Cherbas L., Chen J.D., McKeown M., Cherbas P., Evans R.M. Functional ecdysone receptor is the product of EcR and ultraspiracle genes. Nature. 366:1993;476-479.
67. Yu R.T., McKeown M., Evans R.M., Umesono K. Relationship between Drosophila gap gene tailless and a vertebrate receptor Tlx. Nature. 370:1994;375-379.
68. Yund M.A. Specific binding of 20-hydroxyecdysone to nuclei of imaginal discs of Drosophila melonogaster. Mol. Cell. Endocrinol. 14:1979;19-35.
69. Zelhof A.C., Yao T.P., Chen J.D., Evans R.M., McKeown M. Seven-up inhibits ultraspiracle-based signaling pathways in vitro and in vivo. Mol. Cell Biol. 15:1995;6736-6745.
70. Zelhof A.C., Yao T.P., Evans R.M., Mckeown M. Identification and characterization of a Drosophila nuclear receptor with the ability to inhibit the ecdysone response. Proc. Natl. Acad. Sci. USA. 92:1995;10477-10481.
71. Zhang X.-K., Salbert G., Lee M.-O., Pfahl M. Mutations that alter ligand-induced switches of dimerization activities in the retinoid X receptor. Mol. Cell. Biol. 14:1994;4311-4323.
72. Zhong W., Sladek F.M., Darnell J.E. The expression pattern of a Drosophila homolog to the mouse transcription factor HNF-4 suggests a determinative role in gut formation. EMBO J. 12:1993;537-544.
73. Zhuo S., Clemens J.C., Hakes D.J., Barford D., Dixon J.E. Expression, purification, crystallization, and biochemical characterization of a recombinant protein phosphatase. J. Biol. Chem. 268:1993;17754-17761.