Juvenile hormone regulation of Drosophila Epac-A guanine nucleotide exchange factor

Molecular and Cellular Endocrinology

Volumn 305, Issue 1-2, 2009, Pages 30-37

  Wang, Jun ^a   Lindholm, Joliene R ^a   Willis, David K ^a   Orth, Anthony ^b   Goodman, Walter G ^a  

^a UNIVERSITY OF WISCONSIN MADISON   (United States)

^b GENOMICS INSTITUTE OF THE NOVARTIS RESEARCH FOUNDATION   (United States)

Author keywords

20 Hydroxyecdysone; Bisepoxy JH III; Epac; GEF; JH; Methoprene; Methyl farnesoate; Quantitative real time RT PCR

Indexed keywords

CYCLIC AMP; ECDYSTERONE; EXCHANGE PROTEIN DIRECTLY ACTIVATED BY CYCLIC AMP; GUANINE NUCLEOTIDE EXCHANGE FACTOR; JUVENILE HORMONE; METHOPRENE; UNCLASSIFIED DRUG;

ANIMAL CELL; ARTICLE; BIOLOGICAL ACTIVITY; CELL LINE; CELL STRAIN HEK293; DIET; DOSE RESPONSE; DROSOPHILA; HORMONE ACTION; HUMAN; HUMAN CELL; NONHUMAN; NUCLEOTIDE SEQUENCE; PRIORITY JOURNAL; PROTEIN EXPRESSION; TIME;

ANIMALS; CELL LINE; CELLS, CULTURED; DOSE-RESPONSE RELATIONSHIP, DRUG; DROSOPHILA; DROSOPHILA PROTEINS; ECDYSTERONE; GENE EXPRESSION; GUANINE NUCLEOTIDE EXCHANGE FACTORS; HUMANS; JUVENILE HORMONES; LARVA; METHOPRENE; RAP1 GTP-BINDING PROTEINS; SESQUITERPENES;

EID: 67349264416     PISSN: 03037207     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.mce.2009.02.002     Document Type: Article

References (73)

1. Abdel-Aal Y.A.I., and Hammock B.D. 3-Octylthio-1,1,1-trifluoro-2-propanone, a high affinity and slow binding inhibitor of juvenile hormone esterase from Trichoplusia ni (hübner). Insect Biochem. 15 (1985) 111-122
2. Asha H., de Ruiter N., Wang M., and Hariharan I. The Rap1 GTPase functions as a regulator of morphogenesis in vivo. EMBO J. 18 (1999) 605-615
3. Belles X. Vitellogenesis directed by juvenile hormone. In: Raikhel A., and Sappington T.W. (Eds). Reproductive Biology of Invertebrates (2004), Science Publishers, Enfield, NH 157-198
4. Bhaskara S., Chandrasekharan M., and Ganguly R. Caffeine induction of Cyp6a2 and Cyp6a8 genes of Drosophila melanogaster is modulated by cAMP and D-JUN protein levels. Gene 415 (2008) 49-59
5. Bhaskara S., Dean E., Lam V., and Ganguly R. Induction of two cytochrome P450 genes, Cyp6a2 and Cyp6a8, of Drosophila melanogaster by caffeine in adult flies and in cell culture. Gene 377 (2006) 56-64
6. Bos J. Linking Rap to cell adhesion. Curr. Opin. Cell Biol. 17 (2005) 123-128
7. Bos J. Epac proteins: multi-purpose cAMP targets. Trends Biochem. Sci. 31 (2006) 680-686
8. Chang E., Coudron T., Bruce M., Sage B., O'connor J., and Law J. Juvenile hormone-binding protein from the cytosol of Drosophila Kc cells. Proc. Natl. Acad. Sci. U.S.A. 77 (1980) 4657-4661
9. Cusson M., Miller D., and Goodman W. Characterization of antibody 444 using chromatographically purified enantiomers of juvenile hormones I, II, and III: implications for radioimmunoassays. Anal. Biochem. 249 (1997) 83-87
10. Cusson M., and Palli S. Can juvenile hormone research help rejuvenate integrated pest management?. Can. Entomol. 132 (2000) 263-280
11. Cusson M., Yagi K.J.A., Ding Q.A., Duve H.A., Thorpe A.A., McNeil J.N.A., and Tobe S.S. Biosynthesis and release of juvenile hormone and its precursors in insects and crustaceans: the search for a unifying arthropod endocrinology. Insect Biochem. 21 (1991) 1-6
12. Davey K. The modes of action of juvenile hormones: some questions we ought to ask. Insect Biochem. Mol. Biol. 30 (2000) 663-669
13. de Rooij J., Zwartkruis F., Verheijen M., Cool R., Nijman S., Wittinghofer A., and Bos J. Epac is a Rap1 guanine-nucleotide-exchange factor directly activated by cyclic AMP. Nature 396 (1998) 474-477
14. Delany A. Measuring transcription of metalloproteinase genes. Nuclear run-off assay vs. analysis of hnRNA. Methods Mol. Biol. 151 (2001) 321-333
15. Dubrovsky E., Dubrovskaya V., and Berger E. Hormonal regulation and functional role of Drosophila E75A orphan nuclear receptor in the juvenile hormone signaling pathway. Dev. Biol. 268 (2004) 258-270
16. Echalier G. Drosophila Cells in Culture (1997), Academic Press, San Diego, CA
17. Elferink C., and Reiners J.J. Quantitative RT-PCR on CYP1A1 heterogeneous nuclear RNA: a surrogate for the in vitro transcription run-on assay. Biotechniques 20 (1996) 470-477
18. Flatt T., Tu M., and Tatar M. Hormonal pleiotropy and the juvenile hormone regulation of Drosophila development and life history. Bioessays 27 (2005) 999-1010
19. Fukuhara S., Sakurai A., Sano H., Yamagishi A., Somekawa S., Takakura N., Saito Y., Kangawa K., and Mochizuki N. Cyclic AMP potentiates vascular endothelial cadherin-mediated cell-cell contact to enhance endothelial barrier function through an Epac-Rap1 signaling pathway. Mol. Cell. Biol. 25 (2005) 136-146
20. Gerits N., Kostenko S., Shiryaev A., Johannessen M., and Moens U. Relations between the mitogen-activated protein kinase and the cAMP-dependent protein kinase pathways: comradeship and hostility. Cell. Signal. 20 (2008) 1592-1607
21. Giese C., Spindler K., and Emmerich H. The solubility of insect juvenile hormone in aqueous solutions and its adsorption by glassware and plastics. Z. Naturforsch. 32 (1977) 158-160
22. Goodman W., Schooley D., and Gilbert L. Specificity of the juvenile hormone binding prote. The geometrical isomers of juvenile hormone I. Proc. Natl. Acad. Sci. U.S.A. 75 (1978) 185-189
23. Goodman W.G., and Adams B. Semipreparative synthesis and purification of juvenile hormone acids by high-performance liquid chromatography. J. Chromatogr. 294 (1984) 447-451
24. Goodman W.G., and Granger N.A. The juvenile hormones. In: Gilbert L.I., Iatrou K., and Gill S.S. (Eds). Comprehensive Molecular Insect Science (2005), Elsevier, Amsterdam 319-408
25. Henrick C., Staal G., and Siddall J. Alkyl 3,7,11-trimethyl-2,4-dodecadienoates, a new class of potent insect growth regulators with juvenile hormone activity. J. Agric. Food Chem. 21 (1973) 354-359
26. Hochbaum D., Hong K., Barila G., Ribeiro-Neto F., and Altschuler D. Epac, in synergy with cAMP-dependent protein kinase (PKA), is required for cAMP-mediated mitogenesis. J. Biol. Chem. 283 (2008) 4464-4468
27. Jahn C., Charkowski A., and Willis D. Evaluation of isolation methods and RNA integrity for bacterial RNA quantitation. J. Microbiol. Methods 75 (2008) 318-324
28. Jones D., and Jones G. Farnesoid secretions of dipteran ring glands: what we do know and what we can know. Insect Biochem. Mol. Biol. 37 (2007) 771-798
29. Jones G. Molecular mechanisms of action of juvenile hormone. Annu. Rev. Entomol. 40 (1995) 147-169
30. Jones G., and Sharp P. Ultraspiracle: an invertebrate nuclear receptor for juvenile hormones. Proc. Natl. Acad. Sci. U.S.A. 94 (1997) 13499-13503
31. 2+-controlled activation of Ras and extracellular signal-regulated kinases by Gs-coupled receptors. J. Biol. Chem. 279 (2004) 46497-46508
32. Kethidi D., Li Y., and Palli S. Protein kinase C mediated phosphorylation blocks juvenile hormone action. Mol. Cell. Endocrinol. 247 (2006) 127-134
33. Klages G., Emmerich H., and Peter M.G. High-affinity binding sites for juvenile hormone I in the larval integument of Drosophila hydei. Nature 286 (1980) 282-285
34. Knox A., and Brown N. Rap1 GTPase regulation of adherens junction positioning and cell adhesion. Science 295 (2002) 1285-1288
35. Kooistra M., Corada M., Dejana E., and Bos J. Epac1 regulates integrity of endothelial cell junctions through VE-cadherin. FEBS Lett. 579 (2005) 4966-4972
36. Kramer K., Dunn P., Peterson R., and Law J. Interaction of juvenile hormone with binding proteins in insect hemolymph. In: LI G. (Ed). The Juvenile Hormones (1976), Plenum Press, New York 327-341
37. Li Y., Zhang Z., Robinson G., and Palli S. Identification and characterization of a juvenile hormone response element and its binding proteins. J. Biol. Chem. 282 (2007) 37605-37617
38. Lipson K., and Baserga R. Transcriptional activity of the human thymidine kinase gene determined by a method using the polymerase chain reaction and an intron-specific probe. Proc. Natl. Acad. Sci. U.S.A. 86 (1989) 9774-9777
39. Lyle K., Raaijmakers J., Bruinsma W., Bos J., and de Rooij J. cAMP-induced Epac-Rap activation inhibits epithelial cell migration by modulating focal adhesion and leading edge dynamics. Cell. Signal. 20 (2008) 1104-1116
40. López De Jesús M., Stope M., Oude Weernink P., Mahlke Y., Börgermann C., Ananaba V., Rimmbach C., Rosskopf D., Michel M., Jakobs K., and Schmidt M. Cyclic AMP-dependent and Epac-mediated activation of R-Ras by G protein-coupled receptors leads to phospholipase D stimulation. J. Biol. Chem. 281 (2006) 21837-21847
41. Nijhout H. Insect Hormones (1994), Princeton University Press, Princeton, NJ
42. Palli S., Osir E., Eng W., Boehm M., Edwards M., Kulcsar P., Ujvary I., Hiruma K., Prestwich G., and Riddiford L. Juvenile hormone receptors in insect larval epidermis: identification by photoaffinity labeling. Proc. Natl. Acad. Sci. U.S.A. 87 (1990) 796-800
43. Pfaffl M., Tichopad A., Prgomet C., and Neuvians T. Determination of stable housekeeping genes, differentially regulated target genes and sample integrity: BestKeeper-excel-based tool using pair-wise correlations. Biotechnol. Lett. 26 (2004) 509-515
44. Pszczolkowski M., Peterson A., Srinivasan A., and Ramaswamy S. Pharmacological analysis of ovarial patency in Heliothis virescens. J. Insect Physiol. 51 (2005) 445-453
45. Rangarajan S., Enserink J., Kuiperij H., de Rooij J., Price L., Schwede F., and Bos J. Cyclic AMP induces integrin-mediated cell adhesion through Epac and Rap1 upon stimulation of the beta 2-adrenergic receptor. J. Cell Biol. 160 (2003) 487-493
46. Rasmussen R. Quantification on the LightCycler instrument. In: Meurer S., Wittwer C., and Nakagawara K. (Eds). Rapid Cycle Real-Time PCR: Methods and Applications. (2001), Springer-Verlag, Berlin 21-34
47. Richard D., Applebaum S., Sliter T., Baker F., Schooley D., Reuter C., Henrich V., and Gilbert L. Juvenile hormone bisepoxide biosynthesis in vitro by the ring gland of Drosophila melanogaster: a putative juvenile hormone in the higher Diptera. Proc. Natl. Acad. Sci. U.S.A. 86 (1989) 1421-1425
48. Riddiford L. Juvenile hormone: the status of its "status quo" action. Arch. Insect Biochem. Physiol. 32 (1996) 271-286
49. Riddiford L. Juvenile hormone action: a 2007 perspective. J. Insect Physiol. 54 (2008) 895-901
50. Riddiford L., and Ashburner M. Effects of juvenile hormone mimics on larval development and metamorphosis of Drosophila melanogaster. Gen. Comp. Endocrinol. 82 (1991) 172-183
51. Rotenberg D., Thompson T., German T., and Willis D. Methods for effective real-time RT-PCR analysis of virus-induced gene silencing. J. Virol. Methods 138 (2006) 49-59
52. Sands W., and Palmer T. Regulating gene transcription in response to cyclic AMP elevation. Cell. Signal. 20 (2008) 460-466
53. Sassone-Corsi P. Transcription factors responsive to cAMP. Annu. Rev. Cell Dev. Biol. 11 (1995) 355-377
54. Schmidt M., Evellin S., Weernink P., von Dorp F., Rehmann H., Lomasney J., and Jakobs K. A new phospholipase-C-calcium signalling pathway mediated by cyclic AMP and a Rap GTPase. Nat. Cell Biol. 3 (2001) 1020-1024
55. Schooley D., Bergot B., Dunham L., and Siddall J. Enviromental degradation of the insect growth regulator methoprene (isopropyl (2E, 4E)-11-methoxy-3,7,11-trimethyl-2,4-dodecadienoate). II. Metabolism by aquatic microorganisms. J. Agric. Food Chem. 23 (1975) 293-298
56. Sevala V., and Davey K. Action of juvenile hormone on the follicle cells of Rhodnius prolixus-evidence for a novel regulatory mechanism involving protein kinase C. Experentia 45 (1989) 355-356
57. Shemshedini L., Lanoue M., and Wilson T. Evidence for a juvenile hormone receptor involved in protein synthesis in Drosophila melanogaster. J. Biol. Chem. 265 (1990) 1913-1918
58. Siaussat D., Bozzolan F., Queguiner I., Porcheron P., and Debernard S. Effects of juvenile hormone on 20-hydroxyecdysone-inducible EcR, HR3, E75 gene expression in imaginal wing cells of Plodia interpunctella lepidoptera. Eur. J. Biochem. 271 (2004) 3017-3027
59. Slama K., Romanuk M., and Sorm F. Insect Hormones and Bioanalogues (1974), Springer-Verlag, New York
60. Somekawa S., Fukuhara S., Nakaoka Y., Fujita H., Saito Y., and Mochizuki N. Enhanced functional gap junction neoformation by protein kinase A-dependent and Epac-dependent signals downstream of cAMP in cardiac myocytes. Circ. Res. 97 (2005) 655-662
61. Truman J., and Riddiford L. The morphostatic actions of juvenile hormone. Insect Biochem. Mol. Biol. 37 (2007) 761-770
62. Venkatesh K., Abdel-Aal Y., Armstrong F., and Roe R. Characterization of affinity-purified juvenile hormone esterase from the plasma of the tobacco hornworm Manduca sexta. J. Biol. Chem. 265 (1990) 21727-21732
63. Wang Z., Dillon T., Pokala V., Mishra S., Labudda K., Hunter B., and Stork P. Rap1-mediated activation of extracellular signal-regulated kinases by cyclic AMP is dependent on the mode of Rap1 activation. Mol. Cell. Biol. 26 (2006) 2130-2145
64. Westphal U. Steroid-protein interactions II. Monogr. Endocrinol. 27 (1986) 1-603
65. Wheeler D., and Nijhout H. A perspective for understanding the modes of juvenile hormone action as a lipid signaling system. Bioessays 25 (2003) 994-1001
66. Willis, D., Wang, J., Lindholm, J., Orth, A., Goodman, W., in press. Microarray analysis of juvenile hormone response in Drosophila melanogaster S2 cells. J. Insect Sci.
67. Wilson T., DeMoor S., and Lei J. Juvenile hormone involvement in Drosophila melanogaster male reproduction as suggested by the methoprene-tolerant(27) mutant phenotype. Insect Biochem. Mol. Biol. 33 (2003) 1167-1175
68. Wilson T., and Fabian J. A Drosophila melanogaster mutant resistant to a chemical analog of juvenile hormone. Dev. Biol. 118 (1986) 190-201
69. Wisniewski J., and Kochman M. Juvenile hormone binding protein from silk gland of Galleria mellonella. FEBS Lett. 171 (1984) 127-130
70. Wisniewski J., Wawrzenczyk C., Prestwich G., and Kochman M. Juvenile hormone binding proteins from the epidermis of Galleria mellonella. Insect Biochem. 18 (1988) 29-36
71. Wittchen E., Worthylake R., Kelly P., Casey P., Quilliam L., and Burridge K. Rap1 GTPase inhibits leukocyte transmigration by promoting endothelial barrier function. J. Biol. Chem. 280 (2005) 11675-11682
72. Yamamoto K., Chadarevian A., and Pellegrini M. Juvenile hormone action mediated in male accessory glands of Drosophila by calcium and kinase C. Science 239 (1988) 916-919
73. Zhang X., Odom D., Koo S., Conkright M., Canettieri G., Best J., Chen H., Jenner R., Herbolsheimer E., Jacobsen E., Kadam S., Ecker J., Emerson B., Hogenesch J., Unterman T., Young R., and Montminy M. Genome-wide analysis of cAMP response element binding protein occupancy, phosphorylation, and target gene activation in human tissues. Proc. Natl. Acad. Sci. U.S.A. 102 (2005) 4459-4464