昆虫类胰岛素及其功能研究进展

doi:10.16409/j.cnki.2095-039x.2017.05.018

摘要/Abstract

摘要： 胰岛素是一类生物体内在进化上非常保守的具有调控代谢、生长、发育、生殖和寿命等多种功能的肽类激素。在昆虫中，以多基因家族编码的类胰岛素为主，在结构上与脊椎动物胰岛素同源。近年来，有关昆虫类胰岛素及其信号通路等方面已有较多研究，特别是对黑腹果蝇的研究，为人类胰岛素相关疾病诊断与治疗提供了较好的试验模型。本文主要介绍昆虫类胰岛素及其受体、类胰岛素表达与释放、类胰岛素信号通路及其在调控昆虫生殖、寿命、代谢、生长与发育和翅型分化等生理功能的最新研究进展，为促进其在害虫控制或天敌保护利用等方面的应用提供参考。

关键词: 类胰岛素, 类胰岛素受体, 昆虫, 生理功能

Abstract: Insulins are an evolutionary conserved group of peptide hormones in many organisms which regulate metabolism, growth, development, reproduction, and lifespan. In insulin superfamily, insulin-like peptides (ILPs) exit in insects encoded by multigene families and structurally homologous to vertebrate insulin. In recent years, there have been an increase in research on insect ILPs and insulin-like signaling pathways, especially the study of Drosophila homologs provides a good model for diagnosis and therapy of human insulin-related diseases. Recent research advances on insect ILPs and their receptors, expression and release of ILPs and downstream signaling pathways, and roles of ILPs in physiology are reviewed in this paper for providing a basis on the utilization of genes in insulin-like signaling pathways in control of insect pests or conservation of natural enemies.

Key words: insulin-like peptides, insulin-like receptors, insects, physiological functions

中图分类号:

S476

陈晓昂, 姚洪渭, 叶恭银. 昆虫类胰岛素及其功能研究进展[J]. 中国生物防治学报, 2017, 33(5): 699-712.

CHEN Xiaoang, YAO Hongwei, YE Gongyin. Research Advances on Insulin-like Peptides and Their Functions in Insects[J]. journal1, 2017, 33(5): 699-712.

参考文献

[1] Nässel D R, Broeck J V. Insulin/IGF signaling in Drosophila and other insects:factors that regulate production, release and post-release action of the insulinlike peptides[J]. Cellular and Molecular Life Sciences, 2016, 73(2):271-290.
[2] Banting F G, Best C H. The internal secretion of the pancreas[J]. The Journal of Laboratory and Clinical Medicine, 1922, 7(5):251-266.
[3] Cohen P. The twentieth century struggle to decipher insulin signaling[J]. Nature Reviews Molecular Cell Biology, 2006, 7(11):867-873.
[4] Hall K D. A review of the carbohydrate-insulin model of obesity[J]. European Journal of Clinical Nutrition, 2017, 71(3):323-326.
[5] Kenyon C, Chang J, Gensch E, et al. A C. elegans mutant that lives twice as long as wild type[J]. Nature, 1993, 366(6454):461-464.
[6] Clancy D J, Gems D, Harshman L G, et al. Extension of life-span by loss of CHICO, a Drosophila insulin receptor substrate protein[J]. Science, 2001, 292(5514):104-106.
[7] Tatar M, Kopelman A, Epstein D, et al. A mutant Drosophila insulin receptor homolog that extends life-span and impairs neuroendocrine function[J]. Science, 2001, 292(5514):107-110.
[8] Fontana L, Partridge L, Longo V D. Extending healthy life span-from yeast to humans[J]. Science, 2010, 328(5976):321-326.
[9] 顾世红, 陈建国. 胰岛素信号转导、昆虫发育与老化[J]. 昆虫知识, 2009, 46(4):501-508.
[10] 张龙辉, 王国栋. 无脊椎动物胰岛素样蛋白(Insulin-like/related peptides)研究进展-以昆虫为例[J]. 生物技术通报, 2014, (10):33-42.
[11] Garofalo R S. Genetic analysis of insulin signaling in Drosophila[J]. Trends in Endocrinology and Metabolism, 2002, 13(4):156-162.
[12] Goberdhan D C, Wilson C. The functions of insulin signaling:Size isn't everything, even in Drosophila[J]. Differentiation, 2003, 71(7):375-397.
[13] Wu Q, Brown M R. Signaling and function of insulin-like peptides in insects[J]. Annual Review of Entomology, 2006, 51:1-24.
[14] Teleman A A. Molecular mechanisms of metabolic regulation by insulin in Drosophila[J]. Biochemical Journal, 2010, 425(1):13-26.
[15] Partridge L, Alic N, Bjedov I, et al. Ageing in Drosophila:the role of the insulin/Igf and TOR signalling network[J]. Experimental Gerontology, 2011,46(5):376-381.
[16] Antonova Y, Arik A J, Moore W, et al. Insulin-like peptides:Structure, signaling and function[M]//Gilbert L I ed. Insect Endocrinology. London:Elsevier Academic Press, 2012, 63-92.
[17] Erion R, Sehgal A. Regulation of insect behavior via the insulin-signaling pathway[J]. Frontiers in Physiology, 2013, 4:353.
[18] Green D A 2nd, Extavour C G. Insulin signalling underlies both plasticity and divergence of a reproductive trait in Drosophila[J]. Proceedings of the Royal Society B:Biological Sciences, 2014, 281(1779):20132673.
[19] Nässel D R, Liu Y, Luo J. Insulin/IGF signaling and its regulation in Drosophila[J]. General and Comparative Endocrinology, 2015, 221:255-266.
[20] Altintas O, Park S, Lee S J. The role of insulin/IGF-1 signaling in the longevity of model invertebrates, C. elegans and D. melanogaster[J]. BMB Reports, 2016, 49(2):81-92.
[21] Nagasawa H, Kataoka H, Isogai A, et al. Amino acid sequence of a prothoracicotropic hormone of the silkworm Bombyx mori[J]. Proceedings of the National Academy of Sciences of the United States of America, 1986, 83(16):5840-5843.
[22] Nagasawa H, Kataoka H, Hori Y, et al. Isolation and some characterization of the prothoracicotropic hormone from Bombyx mori[J]. General and Comparative Endocrinology, 1984, 53(1):143-152.
[23] Adachi T, Takiya S, Suzuki Y, et al. cDNA structure and expression of bombyxin, an insulin-like brain secretory peptide of the silkmoth Bombyx mori[J]. Journal of Biological Chemistry, 1989, 264(13):7681-7685.
[24] Kawakami A, Iwami M, Nagasawa H, et al. Structure and organization of four clustered genes that encode bombyxin, an insulin-related brain secretory peptide of the silkmoth Bombyx mori[J]. Proceedings of the National Academy of Sciences of the United States of America, 1989, 86(18):6843-6847.
[25] Aslam AF, Kiya T, Mita K, et al. Identification of novel bombyxin genes from the genome of the silkmoth Bombyx mori and analysis of their expression[J]. Zoological Science, 2011, 28(8):609-616.
[26] Iwami M, Tanaka A, Hano N, et al. Bombyxin gene expression in tissues other than brain detected by reverse transcription-polymerase chain reaction (RT-PCR) and in situ hybridization. Experientia, 1996, 52(9):882-887.
[27] Grönke S, Clarke D F, Broughton S, et al. Molecular evolution and functional characterization of Drosophila insulin-like peptides[J]. Plos Genetics, 2010, 6(2):e1000857.
[28] Garelli A, Gontijo A M, Miguela V, et al. Imaginal discs secrete insulin-like peptide 8 to mediate plasticity of growth and maturation[J]. Science, 2012, 336(6081):579-582.
[29] Krieger M J, Jahan N, Riehle M A, et al. Molecular characterization of insulin-like peptide genes and their expression in the African malaria mosquito, Anopheles gambiae[J]. Insect Molecular Biology, 2004, 13(3):305-315.
[30] Riehle M A, Fan Y, Cao C, et al. Molecular characterization of insulin-like peptides in the yellow fever mosquito, Aedes aegypti:Expression, cellular localization, and phylogeny[J]. Peptides, 2006, 27(11):2547-2560.
[31] Lagueux M, Lwoff L, Meister M, et al. cDNAs from neurosecretory cells of brains of Locusta migratoria (Insecta, Orthoptera) encoding a novel member of the superfamily of insulins[J]. European Journal of Biochemistry, 1990, 187(1):249-254.
[32] Badisco L, Claeys I, Van Hiel M, et al. Purification and characterization of an insulin-related peptide in the desert locust, Schistocerca gregaria:immunolocalization, cDNA cloning, transcript profiling and interaction with neuroparsin[J]. Journal of Molecular Endocrinology, 2008, 40(3):137-150.
[33] Brogiolo W, Stocker H, Ikeya T, et al. An evolutionarily conserved function of the Drosophila insulin receptor and insulin-like peptides in growth control[J]. Current Biology, 2001, 11(4):213-221.
[34] Okamoto N, Yamanaka N, Satake H, et al. An ecdysteroid-inducible insulin-like growth factor-like peptide regulates adult development of the silkmoth Bombyx mori[J]. The FEBS Journal, 2009, 276(5):1221-1232.
[35] Ward C W, Lawrence M C. Landmarks in insulin research[J]. Frontiers in Endocrinology, 2011, 2(2):76.
[36] Ruan Y, Chen C, Cao Y, et al. The Drosophila insulin receptor contains a novel carboxyl-terminal extension likely to play an important role in signal transduction[J]. Journal of Biological Chemistry, 1995, 270(9):4236-4243.
[37] Xu K K, Yang W J, Tian Y, et al. Insulin signaling pathway in the oriental fruit fly:The role of insulin receptor substrate in ovarian development[J]. General and Comparative Endocrinology, 2015, 216:125-133.
[38] Graf R, Neuenschwander S, Brown M R, et al. Insulin-mediated secretion of ecdysteroids from mosquito ovaries and molecular cloning of the insulin receptor homologue from ovaries of bloodfed Aedes aegypti[J]. Insect Molecular Biology, 1997, 6(2):151-163.
[39] Fullbright G, Lacy E R, Büllesbach E E. The prothoracicotropic hormone Bombyxin has specific receptors on insect ovarian cells[J]. European Journal of Biochemistry, 1997, 245(3):774-780.
[40] Abrisqueta M, Süren-Castillo S, Maestro J L. Insulin receptor-mediated nutritional signalling regulates juvenile hormone biosynthesis and vitellogenin production in the German cockroach[J]. Insect Biochemistry and Molecular Biology, 2014, 49(6):14-23.
[41] Lavine L C, Hahn L L, Warren I A, et al. Cloning and characterization of an mrna encoding an insulin receptor from the horned scarab beetle Onthophagus nigriventris (Coleoptera:Scarabaeidae)[J]. Archives of Insect Biochemistry and Physiology, 2013, 82(1):43-57.
[42] de Azevedo S V, Hartfelder K. The insulin signaling pathway in honey bee (Apis mellifera) caste development-differential expression of insulin-like peptides and insulin receptors in queen and worker larvae[J]. Journal of Insect Physiology, 2008, 54(6):1064-1071.
[43] Lu H L, Pietrantonio P V. Insect insulin receptors:insights from sequence and caste expression analyses of two cloned hymenopteran insulin receptor cDNAs from the fire ant[J]. Insect Molecular Biology, 2011, 20(5):637-649.
[44] Xu H J, Xue J, Lu B, et al. Two insulin receptors determine alternative wing morphs in planthoppers[J]. Nature, 2015, 519(7544):464-467.
[45] Guo S S, Zhang M, Liu T X. Insulin-related peptide 5 is involved in regulating embryo development and biochemical composition in pea aphid with wing polyphenism[J]. Frontiers in Physiology, 2016, 7:31.
[46] Ding B Y, Shang F, Zhang Q, et al. Silencing of two insulin receptor genes disrupts nymph-adult transition of alate brown citrus aphid[J]. International Journal of Molecular Sciences, 2017, 18(2):357.
[47] Sang M, Li C, Wu W, et al. Identification and evolution of two insulin receptor genes involved in Tribolium castaneum development and reproduction[J]. Gene, 2016, 585(2):196-204.
[48] Van Hiel M B, Vandersmissen H P, Proost P, et al. Cloning, constitutive activity and expression profiling of two receptors related to relaxin receptors in Drosophila melanogaster[J]. Peptides, 2014, 68:83.
[49] Colombani J, Andersen D S, Boulan L, et al. Drosophila Lgr3 couples organ growth with maturation and ensures developmental stability[J]. Current Biology, 2015, 25(20):2723-2729.
[50] Rajan A, Perrimon N. Drosophila cytokine unpaired 2 regulates physiological homeostasis by remotely controlling insulin secretion[J]. Cell, 2012, 151(1):123-137.
[51] Kwak S J, Hong S H, Bajracharya R, et al. Drosophila adiponectin receptor in insulin producing cells regulates glucose and lipid metabolism by controlling insulin secretion[J]. PLoS ONE, 2013, 8(7):e68641.
[52] Kapan N, Lushchak O V, Luo J, et al. Identified peptidergic neurons in the Drosophila brain regulate insulinproducing cells, stress responses and metabolism by coexpressed short neuropeptide F and corazonin[J]. Cellular and Molecular Life Sciences, 2012, 69(23):4051-4066.
[53] Hentze J L, Carlsson M A, Kondo S, et al. The neuropeptide allatostatin A regulates metabolism and feeding decisions in Drosophila[J]. Scientific Reports, 2015, 5:11680.
[54] Alfa R W, Park S, Skelly K R, et al. Suppression of insulin production and secretion by a decretin hormone[J]. Cell Metabolism, 2015, 21(2):323-333.
[55] Luo J, Becnel J, Nichols C D, et al. Insulin-producing cells in the brain of adult Drosophila are regulated by the serotonin 5-HT(1A) receptor[J]. Cellular and Molecular Life Sciences, 2012, 69(3):471-484.
[56] Luo J, Lushchak O V, Goergen P, et al. Drosophila insulin-producing cells are differentially modulated by serotonin and octopamine receptors and affect social behavior[J]. PLoS ONE, 2014, 9(6):e99732.
[57] Siviter R J, Coast G M, Winther A M, et al. Expression and functional characterization of a Drosophila neuropeptide precursor with homology to mammalian preprotachykinin A[J]. Journal of Biological Chemistry, 2000, 275(30):23273-23280.
[58] Böhni R, Riesgo-Escovar J, Oldham S, et al. Autonomous control of cell and organ size by CHICO, a Drosophila homolog of vertebrate IRS1-4[J]. Cell, 1999, 97(7):865-875.
[59] Verdu J, Buratovich M A, Wilder E L, et al. Cell-autonomous regulation of cell and organ growth in Drosophila by Akt/PKB[J]. Nature Cell Biology, 1999, 1(8):500-506.
[60] Weinkove D, Neufeld T P, Twardzik T, et al. Regulation of imaginal disc cell size, cell number and organ size by Drosophila class I(A) phosphoinositide 3-kinase and its adaptor[J]. Current Biology, 1999, 9(18):1019-1029.
[61] Jünger M A, Rintelen F, Stocker H, et al. The Drosophila forkhead transcription factor FOXO mediates the reduction in cell number associated with reduced insulin signaling[J]. Journal of Biology, 2003, 2(3):20.
[62] Blenis J. Signal transduction via the MAP kinases:Proceed at your own RSK[J]. Proceedings of the National Academy of Sciences of the United States of America, 1993, 90(13):5889-5892.
[63] Shaul Y D, Seger R. The MEK/ERK cascade:From signaling specificity to diverse functions[J]. Biochimica Et Biophysica Acta, 2007, 1773(8):1213-1226.
[64] Chakraborty C, Doss C G, Bandyopadhyay S, et al. Mapping the structural topology of IRS family cascades through computational biology[J]. Cell Biochemistry and Biophysics, 2013, 67(3):1319-1331.
[65] Gingras A C, Raught B, Sonenberg N. Regulation of translation initiation by FRAP/mTOR[J]. Genes and Development, 2001, 15(7):807-826.
[66] Burgering B M, Kops G J. Cell cycle and death control:Long live Forkheads[J]. Trends in Biochemical Sciences, 2002, 27(7):352-360.
[67] Cantley L C. The phosphoinositide 3-kinase pathway[J]. Science, 2002, 296(5573):1655-1657.
[68] Kannan K, Fridell Y W. Functional implications of Drosophila insulin-like peptides in metabolism, aging, and dietary restriction[J]. Frontiers in Physiology, 2013, 4(4):288.
[69] Ikeya T, Galic M, Belawat P, et al. Nutrient-dependent expression of insulin-like peptides from neuroendocrine cells in the CNS contributes to growth regulation in Drosophila[J]. Current Biology, 2002, 12(15):1293-1300.
[70] Broughton S J, Piper M D, Ikeya T, et al. Longer lifespan, altered metabolism, and stress resistance in Drosophila from ablation of cells making insulin-like ligands[J]. Proceedings of the National Academy of Sciences of the United States of America, 2005, 102(8):3105-3110.
[71] Richard D S, Rybczynski R, Wilson T G, et al. Insulin signaling is necessary for vitellogenesis in Drosophila melanogaster independent of the roles of juvenile hormone and ecdysteroids:female sterility of the chico1 insulin signaling mutation is autonomous to the ovary[J]. Journal of Insect Physiology, 2005, 51(4):455-464.
[72] Sheng Z, Xu J, Bai H, et al. Juvenile hormone regulates vitellogenin gene expression through insulin-like peptide signaling pathway in the red flour beetle, Tribolium castaneum[J]. Journal of Biological Chemistry, 2011, 286(49):41924-41936.
[73] Riehle M A, Brown M R. Insulin stimulates ecdysteroid production through a conserved signaling cascade in the mosquito Aedes aegypti[J]. Insect Biochemistry and Molecular Biology, 1999, 29(10):855-860.
[74] Brown M R, Clark K D, Gulia M, et al. An insulin-like peptide regulates egg maturation and metabolism in the mosquito Aedes aegypti[J]. Proceedings of the National Academy of Sciences of the United States of America, 2008, 105(15):5716-5721.
[75] Parthasarathy R, Palli S R. Molecular analysis of nutritional and hormonal regulation of female reproduction in the red flour beetle, Tribolium castaneum[J]. Insect Biochemistry and Molecular Biology, 2011, 41(5):294-305.
[76] Fu K Y, Zhu T T, Guo W C, et al. Knockdown of a putative insulin-like peptide gene LdILP2 in Leptinotarsa decemlineata by RNA interference impairs pupation and adult emergence[J]. Gene, 2016, 581(2):170-177.
[77] Zhang T T, Zhang G C, Zeng F F, et al. Insulin-like peptides regulate vitellogenesis and oviposition in the green lacewing, Chrysopa septempunctata[J]. Bulletin of Entomological Research, 2017, 107(2):148-154.
[78] Tu M P, Epstein D, Tatar M. The demography of slow aging in male and female Drosophila mutant for the insulin-receptor substrate homologue chico[J]. Aging Cell, 2002, 1(1):75-80.
[79] Nielsen M D, Luo X, Biteau B, et al. 14-3-3ε antagonizes FoxO to control growth, apoptosis and longevity in Drosophila[J]. Aging Cell, 2008, 7(5):688-699.
[80] Hwangbo D S, Gershman B, Tu M P, et al. Drosophila dFOXO controls lifespan and regulates insulin signalling in brain and fat body[J]. Nature, 2004, 429(6991):562-566.
[81] Giannakou M E, Goss M, Junger M A, et al. Long-lived Drosophila with overexpressed dFOXO in adult fat body[J]. Science, 2004, 305(5682):361.
[82] Wessells R J, Fitzgerald E, Cypser J R, et al. Insulin regulation of heart function in aging fruit flies[J]. Nature Genetics, 2004, 36(36):1275-1281.
[83] Demontis F, Perrimon N. FOXO/4E-BP signaling in Drosophila muscles regulates organism-wide proteostasis during aging[J]. Cell, 2010, 143(5):813-825.
[84] Schiesari L, Andreatta G, Kyriacou C P, et al. The Insulin-like proteins dILPs-2/5 determine diapause inducibility in Drosophila[J]. PLoS ONE, 2016, 11(9):e0163680.
[85] Herman W S, Tatar M. Juvenile hormone regulation of longevity in the migratory monarch butterfly[J]. Proceedings of the Royal Society B:Biological Sciences, 2001, 268(1485):2509-2514.
[86] Arpagaus M. Vertebrate insulin induces diapause termination in Pieris brassicae pupae[J]. Development Genes and Evolution, 1987, 196(8):527-530.
[87] Tatar M, Bartke A, Antebi A. The endocrine regulation of aging by insulin-like signals[J]. Science, 2003, 299(5611):1346-1351.
[88] Satake S, Masumura M, Ishizaki H, et al. Bombyxin, an insulin-related peptide of insects, reduces the major storage carbohydrates in the silkworm Bombyx mori[J]. Comparative Biochemistry and Physiology, Part B Biochemistry and Molecular Biology, 1997, 118(2):349-357.
[89] Satake S, Nagata K, Kataoka H, et al. Bombyxin secretion in the adult silkmoth Bombyx mori:Sex-specificity and its correlation with metabolism[J]. Journal of Insect Physiology, 1999, 45(10):939-945.
[90] Rulifson E J, Kim S K, Nusse R. Ablation of insulin-producing neurons in flies:growth and diabetic phenotypes[J]. Science, 2002, 296(5570):1118-1120.
[91] Ceddia R B, Bikopoulos G J, Hilliker A J, et al. Insulin stimulates glucose metabolism via the pentose phosphate pathway in Drosophila Kc cells[J]. FEBS Letters, 2003, 555(2):307-310.
[92] Defferrari M S, Orchard I, Lange A B. Identification of the first insulin-like peptide in the disease vector Rhodnius prolixus:Involvement in metabolic homeostasis of lipids and carbohydrates[J]. Insect Biochemistry and Molecular Biology, 2016, 70:148-159.
[93] Sim C, Denlinger D L. A shut-down in expression of an insulin-like peptide, ILP-1, halts ovarian maturation during the overwintering diapause of the mosquito Culex pipiens[J]. Insect Molecular Biology, 2009, 18(3):325-332.
[94] Chen C, Jack J, Garofalo R S. The Drosophila insulin receptor is required for normal growth[J]. Endocrinology, 1996, 137(3):846-856.
[95] Wang Y, Azevedo S V, Hartfelder K, et al. Insulin-like peptides (AmILP1 and AmILP2) differentially affect female caste development in the honey bee (Apis mellifera L.)[J]. Journal of Experimental Biology, 2013, 216(23):4347-4357.
[96] Scanga S E, Ruel L, Binari RC, et al. The conserved PI3'K/PTEN/Akt signaling pathway regulates both cell size and survival in Drosophila[J]. Oncogene, 2000, 19(35):3971-3977.
[97] Oldham S, Montagne J, Radimerski T, et al. Genetic and biochemical characterization of dTOR, the Drosophila homolog of the target of rapamycin[J]. Genes and Development, 2000, 14(21):2689-2694.
[98] Potter C J, Huang H, Xu T. Drosophila Tsc1 functions with Tsc2 to antagonize insulin signaling in regulating cell growth, cell proliferation, and organ size[J]. Cell, 2001, 105(3):357-368.
[99] Puig O, Marr M T, Ruhf M L, et al. Control of cell number by Drosophila FOXO:downstream and feedback regulation of the insulin receptor pathway[J]. Genes and Development, 2003, 17(16):2006-2020.
[100] Montagne J, Stewart M J, Stocker H, et al. Drosophila S6 kinase:a regulator of cell size[J]. Science, 1999, 285(5436):2126-2129.
[101] Lin X, Yu N, Smagghe G. Insulin receptor regulates food intake through sulfakinin signaling in the red flour beetle, Tribolium castaneum[J]. Peptides, 2016, 80:89-95.
[102] Patel A, Fondrk M K, Kaftanoglu O, et al. The making of a queen:TOR pathway is a key player in diphenic caste development[J]. PLoS ONE, 2007, 2(6):e509.
[103] Wolschin F, Mutti N S, Amdam G V. Insulin receptor substrate influences female caste development in honeybees[J]. Biology Letters, 2011, 7(1):112-115.
[104] Wheeler D E, Buck N A, Evans J D. Expression of insulin/insulin-like signalling and TOR pathway genes in honey bee caste determination[J]. Insect Molecular Biology, 2014, 23(1):113-121.
[105] Wheeler D E, Buck N, Evans J D. Expression of insulin pathway genes during the period of caste determination in the honey bee, Apis mellifera[J]. Insect Molecular Biology, 2006, 15(5):597-602.
[106] Mutti N S, Dolezal A G, Wolschin F, et al. IRS and TOR nutrient-signaling pathways act via juvenile hormone to influence honey bee caste fate[J].Journal of Experimental Biology, 2011, 214(23):3977-3984.
[107] Fernandezalmonacid R, Rosen O M. Structure and ligand specificity of the Drosophila melanogaster insulin receptor[J]. Molecular and cellular biology, 1987, 7(8):2718-2727.
[108] Sim C, Denlinger D L. Insulin signaling and FOXO regulate the overwintering diapause of the mosquito Culex pipiens[J]. Proceedings of the National Academy of Sciences of the United States of America, 2008, 105(105):6777-6781.
[109] Kimura-Kawakami M, Iwami M, Kawakami A, et al. Structure and expression of bombyxin-related peptide genes of the moth Samia cynthia ricini[J]. General and Comparative Endocrinology, 1992, 86(2):257-268.
[110] Iwami M, Furuya I, Kataoka H. Bombyxin-related peptides:cDNA structure and expression in the brain of the hornworm Agrius convoluvuli[J]. Insect Biochemistry and Molecular Biology, 1996, 26(1):25-32.
[111] Van de Velde S, Badisco L, Claeys I, et al. Insulin-like peptides in Spodoptera littoralis (Lepidoptera):Detection, localization and identification[J]. General and Comparative Endocrinology, 2007, 153(1-3):72-79.
[112] Koyama T, Syropyatova M O, Riddiford L M. Insulin/IGF signaling regulates the change in commitment in imaginal discs and primordia by overriding the effect of juvenile hormone[J]. Developmental biology, 2008, 324(2):258-265.
[113] Li B, Predel R, Neupert S, et al. Genomics, transcriptomics, and peptidomics of neuropeptides and protein hormones in the red flour beetle Tribolium castaneum[J]. Genome Research, 2008, 18(1):113-122.
[114] Huybrechts J, Bonhomme J, Minoli S, et al. Neuropeptide and neurohormone precursors in the pea aphid, Acyrthosiphon pisum[J]. Insect Molecular Biology, 2010, 19(S2):87-95.
[115] Das R, Dobens L L. Conservation of gene and tissue networks regulating insulin signalling in flies and vertebrates[J]. Biochemical Society Transactions, 2015, 43(5):1057-1062.