Two insulin-like peptide family members from the mosquito Aedes aegypti exhibit differential biological and receptor binding activities

Molecular and Cellular Endocrinology

Volumn 328, Issue 1-2, 2010, Pages 47-55

  Wen, Zhimou ^a   Gulia, Monika ^a   Clark, Kevin D ^a   Dhara, Animesh ^b   Crim, Joe W ^b   Strand, Michael R ^a   Brown, Mark R ^a  

^a UNIVERSITY OF GEORGIA   (United States)

^b UNIVERSITY OF GEORGIA   (United States)

Author keywords

Insect; Insulin; Metabolism; Mosquito; Reproduction

Indexed keywords

ECDYSTEROID; G PROTEIN COUPLED RECEPTOR; INSULIN; INSULIN LIKE PROTEIN 3; INSULIN LIKE PROTEIN 4; INSULIN RECEPTOR; PROTEIN KINASE B; SOMATOMEDIN; UNCLASSIFIED DRUG;

AEDES AEGYPTI; ARTICLE; BIOLOGICAL ACTIVITY; BRAIN METABOLISM; CARBOHYDRATE METABOLISM; CONTROLLED STUDY; CROSS LINKING; DOSE RESPONSE; FEMALE; IMMUNOBLOTTING; LIPID STORAGE; NEUROSECRETION; NONHUMAN; NUCLEOTIDE SEQUENCE; OOCYTE; OOCYTE MATURATION; PRIORITY JOURNAL; PROTEIN BINDING; PROTEIN EXPRESSION; PROTEIN FOLDING; PROTEIN PHOSPHORYLATION; PROTEIN SYNTHESIS; RECEPTOR BINDING; RNA INTERFERENCE; SIGNAL TRANSDUCTION;

AEDES; ANIMALS; FEMALE; INSECT PROTEINS; MULTIGENE FAMILY; OVARY; PEPTIDES; PROTEIN BINDING; RECEPTORS, PEPTIDE; RECEPTORS, SOMATOMEDIN; SIGNAL TRANSDUCTION; SOMATOMEDINS; SUBSTRATE SPECIFICITY;

EID: 77956343172     PISSN: 03037207     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.mce.2010.07.003     Document Type: Article

References (52)

1. Ament S.A., Corona M., Pollock H.S., Robinson G.E. Insulin signaling is involved in the regulation of worker division of labor in honey bee colonies. Proc. Natl. Acad. Sci. U.S.A. 2008, 105:4226-4231.
2. Arik A.J., Rasgon J.L., Quicke K.M., Riehle M.A. Manipulating insulin signaling to enhance mosquito reproduction. BMC Physiol. 2009, 9(15):1-11.
3. Arquier N., Geminard C., Bourouis M., Jarretou G., Honegger B., Paix A., Leopold P. Drosophila ALS regulates growth and metabolism through functional interaction with insulin-like peptides. Cell Metab. 2008, 7:333-338.
4. Belfiore A., Frasca F., Pandini G., Sciacca L., Vigneri R. Insulin receptor isoforms and insulin receptor/insulin-like growth factor receptor hybrids in physiology and disease. Endocr. Rev. 2009, 30:586-623.
5. Belgacem Y.H., Martin J.R. Disruption of insulin pathways alters trehalose level and abolishes sexual dimorphism in locomotor activity in Drosophila. J. Neurobiol. 2006, 66:19-32.
6. Bohni R., Riesgo-Escovar J., Oldham S., Brogiolo W., Stocker H., Andruss B.F., Beckingham K., Hafen E. Autonomous control of cell and organ size by CHICO, a Drosophila homolog of vertebrate IRS1-4. Cell 1999, 97:865-875.
7. Brogiolo W., Stocker H., Ikeya T., Rintelen F., Fernandez R., Hafen E. An evolutionarily conserved function of the Drosophila insulin receptor and insulin-like peptides in growth control. Curr. Biol. 2001, 11:213-221.
8. Broughton S.J., Piper M.D.W., Ikeya T., Bass T.M., Jacobson J., Driege Y., Martinez P., Hafen E., Withers D.J., Leevers S.J., Partridge L. Longer lifespan, altered metabolism, and stress resistance in Drosophila from ablation of cells making insulin-like ligands. Proc. Natl. Acad. Sci. U.S.A. 2005, 102:3105-3110.
9. Brown M.R., Graf R., Swiderek K.M., Fendley D., Stracker T.H., Champagne D.E., Lea A.O. Identification of a steroidogenic neurohormone in female mosquitoes. J. Biol. Chem. 1998, 273:3967-3971.
10. Brown M.R., Clark K.D., Gulia M., Zhao Z., Garczynski S.F., Crim J.W., Suderman R.J., Strand M.R. An insulin-like peptide regulates egg maturation and metabolism in the mosquito Aedes aegypti. Proc. Natl. Acad. Sci. U.S.A. 2008, 105:5716-5721.
11. Crim J.W., Garczynski S.F., Brown M.R. Approaches to radioiodination of insect peptides. Peptides 2002, 23:2045-2051.
12. Delcourt N., Bockaert J., Marin P. GPCR-jacking: from a new in RTK signaling to a new concept in GPCR activation. Trends Pharmacol. Sci. 2007, 28:603-607.
13. Fernandez R., Tabarini D., Azpiazu N., Frasch M., Schlessinger J. The Drosophila insulin receptor homolog: a gene essential for embryonic development encodes two receptor isoforms with different signaling potential. EMBO J. 1995, 14:3373-3384.
14. Géminard C., Rulifson E.J., Léopold P. Remote control of insulin secretion by fat cells in Drosophila. Cell Metabol. 2009, 10:199-207.
15. Gershman B., Puig O., Hang L., Peitzsch R.M., Tatar M., Garofalo R.S. High-resolution dynamics of the transcriptional response to nutrition in Drosophila: a key role for dFOXO. Physiol. Genomics 2007, 29:24-34.
16. Graf R., Neuenschwander S., Brown M.R., Ackermann U. Insulin-mediated secretion of ecdysteroids from mosquito ovaries and molecular cloning of the insulin receptor homologue from ovaries of bloodfed Aedes aegypti. Insect Mol. Biol. 1997, 6:151-163.
17. Grönke S., Clark D.-F., Broughton S., Andrews T.D., Partridge L. Molecular evolution and functional characterization of Drosophila insulin-like peptides. PLOS Genet. 2010, 6:e1000857.
18. Gu S.H., Lin J.L., Lin P.L., Chen C.H. Insulin stimulates ecdysteroidogenesis by prothoracic glands in the silkworm, Bombyx mori. Insect Biochem. Mol. Biol. 2009, 39:171-179.
19. Halls M.L., van der Westhuizen E.T., Bathgate R.A.D., Summers R.J. Relaxin family peptide receptors: former orphans reunite with their parent ligands to activate multiple signaling pathways. Br. J. Pharmacol. 2007, 150:677-691.
20. Honegger B., Galic M., Köhler K., Wittwer F., Brogiolo W., Hafen E., Stocker H. Imp-L2, a putative homolog of vertebrate IGF-binding protein 7, counteracts insulin signaling in Drosophila and is essential for starvation resistance. J. Biol. 2008, 7:10.
21. Hsu S.Y., Nakabayashi K., Nishi S., Kumagai J., Kudo M., Sherwood O.D., Hsueh A.J. Activation of orphan receptors by the hormone relaxin. Science 2002, 295:671-674.
22. Ikeya T., Galic M., Belawat P., Nairz K., Hafen E. Nutrient-dependent expression of insulin-like peptides from neuroendocrine cells in the CNS contributes to growth regulation in Drosophila. Curr. Biol. 2002, 12:1293-1300.
23. Kang M.A., Mott T.M., Tapley E.C., Lewis E.E., Luckhart S. Insulin regulates aging and oxidative stress in Anopheles stephensi. J. Exp. Biol. 2008, 211:741-748.
24. Kim S.E., Cho J.Y., Kim K.S., Lee S.J., Lee K.H., Choi K.Y. Drosophila PI3 kinase and Akt involved in insulin-stimulated proliferation and ERK pathway activation in Schneider cells. Cell Signaling 2004, 16:1309-1317.
25. Lea A.O. The medial neurosecretory cells and egg maturation in mosquitoes. J. Insect Physiol. 1967, 13:419-429.
26. Loy T.V., Vandersmissen H.P., Van Hiel M.B., Poels J., Verlinden H., Badisco L., Vassart G., Vanden Broeck J.V. Comparative genomics of leucine-rich repeats containing G protein-coupled receptors and their ligands. Gen. Comp. Endocrinol. 2008, 155:14-21.
27. Luan B., Zhao J., Wu H., Duan B., Shu G., Wang X., Li D., Jia W., Kang J., Pei G. Deficiency of a beta-arrestin-2 signal complex contributes to insulin resistance. Nature 2009, 457:1146-1149.
28. Luckhart S., Riehle M.A. The insulin signaling cascade from nematodes to mammals: insights into innate immunity of Anopheles mosquitoes to malaria parasite infection. Dev. Comp. Immunol. 2007, 31:647-656.
29. Matsumoto S., Brown M.R., Suzuki A., Lea A.O. Isolation and characterization of ovarian ecdysteroidogenic hormones from the mosquito, Aedes aegypti. Insect Biochem. 1989, 19:651-656.
30. Okamoto N., Yamanaka N., Satake H., Saegusa H., Kataoka H., Mizoguchi A. An ecdysteroid-inducible insulin-like growth factor-like peptide regulates adult development of the silkmoth Bombyx mori. FEBS J. 2009, 276:1221-1232.
31. Orme M.H., Alrubaie S., Bradley G.L., Walker C.D., Leevers S.J. Input from RAS is required for maximal PI3K signaling in Drosophila. Nat. Cell Biol. 2006, 8:1298-1302.
32. Petruzzelli L., Herrera R., Garcia R., Rosen O.M. The insulin receptor of Drosophila melanogaster. Cancer Cells 3: Growth Factors and Transformation 1985, 115-121. Cold Spring Harbor Laboratory, Cold Spring Harbor, NY. J. Feramisco, B. Ozanne, C. Stiles (Eds.).
33. Rewitz K.F., Yamanaka N., Gilbert L.I., O'Connor M.B. The insect neuropeptide PTTH activates receptor tyrosine kinase Torso to initiate metamorphosis. Science 2009, 326:1403-1405.
34. Riehle M.A., Brown M.R. Insulin stimulates ecdysteroid production through a conserved signaling cascade in the mosquito Aedes aegypti. Insect Biochem. Mol. Biol. 1999, 29:855-860.
35. Riehle M.A., Brown M.R. Insulin receptor expression during development and a reproductive cycle in the ovary of the mosquito Aedes aegypti. Cell Tissue Res. 2002, 308:409-420.
36. Riehle M.A., Brown M.R. Molecular analysis of the serine/threonine kinase Akt and its expression in the mosquito, Aedes aegypti. Insect Mol. Biol. 2003, 12:225-232.
37. Riehle M.A., Fan Y., Cao C., Brown M.R. Molecular characterization and developmental expression of insulin-like peptides in the yellow fever mosquito, Aedes aegypti. Peptides 2006, 27:2535-3028.
38. Roy S.G., Hansen I.A., Raikhel A.S. Effect of insulin and 20-hydroxyecdysone in the fat body of the yellow fever mosquito, Aedes aegypti. Insect Biochem. Mol. Biol. 2007, 37:1317-1326.
39. Rulifson E.J., Kim S.K., Nusse R. Ablation of insulin-producing neurons in flies: growth and diabetic phenotypes. Science 2002, 296:1118-1120.
40. Saperstein R., Vicario P.P., Strout H.V., Brady E., Slater E.E., Greenlee W.J., Ondeyka D.L., Patchett A.A., Hangauer D.G. Design of a selective insulin receptor tyrosine kinase inhibitor and its effect on glucose uptake and metabolism in intact cells. Biochemistry 1989, 28:5694-5701.
41. Sieglaff D.H., Duncan K.A., Brown M.R. Expression of genes encoding proteins involved in ecdysteroidogenesis in the female mosquito, Aedes aegypti. Insect Biochem. Mol. Biol. 2005, 35:369-514.
42. Sim C., Denlinger D.L. Insulin signaling and FOXO regulate the overwintering diapause of the mosquito Culex pipiens. Proc. Natl. Acad. Sci. U.S.A. 2008, 105:6777-6781.
43. Taguchi A., White M.F. Insulin-like signaling, nutrient homeostasis, and life span. Annu. Rev. Physiol. 2008, 70:191-212.
44. Taniguchi C.M., Emanuelli B., Kahn C.R. Critical nodes in signalling pathways: insights into insulin action. Nat.: Mol. Cell Biol. 2006, 7:85-96.
45. Teleman A.A. Molecular mechanisms of metabolic regulation by insulin in Drosophila. Biochem. J. 2010, 425:13-26.
46. Toivonen J.M., Partridge L. Endocrine regulation of aging and reproduction in Drosophila. Mol. Cell. Endocrinol. 2009, 299:39-50.
47. Veenstra J.A. Peptidergic paracrine and endocrine cells in the midgut of the fruit fly maggot. Cell Tissue Res. 2009, 336:309-323.
48. Werz C., Köhler K., Hafen E., Stocker H. The Drosophila SH2B family adaptor Lnk acts in parallel to chico in the insulin signaling pathway. PLoS Genet. 2009, 5:e1000596.
49. Wu Q., Brown M.R. Signaling and function of insulin-like peptides in insects. Ann. Rev. Entomol. 2006, 51:1-24.
50. Yamaguchi T., Fernandez R., Roth R.A. Comparison of the signaling abilities of the Drosophila and human insulin receptors in mammalian cells. Biochemistry 1995, 34:4962-4968.
51. Yang C.H., Belawat P., Hafen E., Jan L.Y., Jan Y.N. Drosophila egg-laying site selection as a system to study simple decision-making processes. Science 2008, 319:1679-1683.
52. Zhang H., Lui J., Li C.R., Kohanski R.A., Pick L. Deletion of Drosophila insulin-like peptides causes growth defects and metabolic abnormalities. Proc. Natl. Acad. Sci. U.S.A. 2009, 106:19617-19622.