1932

Abstract

The synthesis of vitellogenin and its uptake by maturing oocytes during egg maturation are essential for successful female reproduction. These events are regulated by the juvenile hormones and ecdysteroids and by the nutritional signaling pathway regulated by neuropeptides. Juvenile hormones act as gonadotropins, regulating vitellogenesis in most insects, but ecdysteroids control this process in Diptera and some Hymenoptera and Lepidoptera. The complex crosstalk between the juvenile hormones, ecdysteroids, and nutritional signaling pathways differs distinctly depending on the reproductive strategies adopted by various insects. Molecular studies within the past decade have revealed much about the relationships among, and the role of, these pathways with respect to regulation of insect reproduction. Here, we review the role of juvenile hormones, ecdysteroids, and nutritional signaling, along with that of microRNAs, in regulating female insect reproduction at the molecular level.

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2018-01-07
2024-03-28
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Literature Cited

  1. Ables ET, Drummond-Barbosa D. 1.  2010. The steroid hormone ecdysone functions with intrinsic chromatin remodeling factors to control female germline stem cells in Drosophila. Cell Stem Cell 7:581–92 [Google Scholar]
  2. Ables ET, Hwang GH, Finger DS, Hinnant TD, Drummond-Barbosa D. 2.  2016. A genetic mosaic screen reveals ecdysone-responsive genes regulating Drosophila oogenesis. G3 6:2629–42 [Google Scholar]
  3. Abrisqueta M, Suren-Castillo S, Maestro JL. 3.  2014. Insulin receptor–mediated nutritional signalling regulates juvenile hormone biosynthesis and vitellogenin production in the German cockroach. Insect Biochem. Mol. Biol. 49:14–23 [Google Scholar]
  4. Akbari OS, Matzen KD, Marshall JM, Huang H, Ward CM, Hay BA. 4.  2013. A synthetic gene drive system for local, reversible modification and suppression of insect populations. Curr. Biol. 23:671–77 [Google Scholar]
  5. Amdam GV, Omholt SW. 5.  2003. The hive bee to forager transition in honeybee colonies: the double repressor hypothesis. J. Theor. Biol. 223:451–64 [Google Scholar]
  6. Ashburner M. 6.  1990. Puffs, genes, and hormones revisited. Cell 61:1–3 [Google Scholar]
  7. Ashburner M, Chihara C, Meltzer P, Richards G. 7.  1974. Temporal control of puffing activity in polytene chromosomes. Cold Spring Harb. Symp. Quant. Biol. 38:655–62 [Google Scholar]
  8. Ashok M, Turner C, Wilson TG. 8.  1998. Insect juvenile hormone resistance gene homology with the bHLH-PAS family of transcriptional regulators. PNAS 95:2761–66 [Google Scholar]
  9. Aslam AF, Kiya T, Mita K, Iwami M. 9.  2011. Identification of novel bombyxin genes from the genome of the silkmoth Bombyx mori and analysis of their expression. Zool. Sci. 28:609–16 [Google Scholar]
  10. Attardo GM, Hansen IA, Raikhel AS. 10.  2005. Nutritional regulation of vitellogenesis in mosquitoes: implications for anautogeny. Insect Biochem. Mol. Biol. 35:661–75 [Google Scholar]
  11. Attardo GM, Hansen IA, Shiao SH, Raikhel AS. 11.  2006. Identification of two cationic amino acid transporters required for nutritional signaling during mosquito reproduction. J. Exp. Biol. 209:3071–78 [Google Scholar]
  12. Azzam G, Smibert P, Lai EC, Liu JL. 12.  2012. Drosophila Argonaute 1 and its miRNA biogenesis partners are required for oocyte formation and germline cell division. Dev. Biol. 365:384–94 [Google Scholar]
  13. Badisco L, Claeys I, Van Hiel M, Clynen E, Huybrechts J. 13.  et al. 2008. Purification and characterization of an insulin-related peptide in the desert locust, Schistocerca gregaria: immunolocalization, cDNA cloning, transcript profiling and interaction with neuroparsin. J. Mol. Endocrinol. 40:137–50 [Google Scholar]
  14. Badisco L, Van Wielendaele P, Vanden Broeck J. 14.  2013. Eat to reproduce: a key role for the insulin signaling pathway in adult insects. Front. Physiol. 4:202 [Google Scholar]
  15. Belles X. 15.  2004. Vitellogenesis directed by juvenile hormone. Reprod. Biol. Invertebr. 12:157–98 [Google Scholar]
  16. Belles X, Cristino AS, Tanaka ED, Rubio M, Piulachs M-D. 16.  2012. Insect microRNAs: from molecular mechanisms to biological roles. Insect Molecular Biology and Biochemistry L Gilbert 30–56 Amsterdam: Elsevier [Google Scholar]
  17. Bernardi F, Romani P, Tzertzinis G, Gargiulo G, Cavaliere V. 17.  2009. EcR-B1 and Usp nuclear hormone receptors regulate expression of the VM32E eggshell gene during Drosophila oogenesis. Dev. Biol. 328:541–51 [Google Scholar]
  18. Bernstein E, Caudy AA, Hammond SM, Hannon GJ. 18.  2001. Role for a bidentate ribonuclease in the initiation step of RNA interference. Nature 409:363–66 [Google Scholar]
  19. Billas IM, Iwema T, Garnier JM, Mitschler A, Rochel N, Moras D. 19.  2003. Structural adaptability in the ligand-binding pocket of the ecdysone hormone receptor. Nature 426:91–96 [Google Scholar]
  20. Bloch G, Borst DW, Huang Z, Robinson GE, Cnaani J, Hefetz A. 20.  2000. Juvenile hormone titers, juvenile hormone biosynthesis, ovarian development and social environment in Bombus terrestris. J. Insect Physiol. 46:47–57 [Google Scholar]
  21. Broadus J, McCabe JR, Endrizzi B, Thummel CS, Woodard CT. 21.  1999. The Drosophila βFTZ-F1 orphan nuclear receptor provides competence for stage-specific responses to the steroid hormone ecdysone. Mol. Cell 3:143–49 [Google Scholar]
  22. Brown MR, Clark KD, Gulia M, Zhao Z, Garczynski SF. 22.  et al. 2008. An insulin-like peptide regulates egg maturation and metabolism in the mosquito Aedes aegypti. PNAS 105:5716–21 [Google Scholar]
  23. Brown MR, Sieglaff DH, Rees HH. 23.  2009. Gonadal ecdysteroidogenesis in arthropoda: occurrence and regulation. Annu. Rev. Entomol. 54:105–25 [Google Scholar]
  24. Bryant B, Macdonald W, Raikhel AS. 24.  2010. microRNA miR-275 is indispensable for blood digestion and egg development in the mosquito Aedes aegypti. PNAS 107:22391–98 [Google Scholar]
  25. Bryant B, Raikhel AS. 25.  2011. Programmed autophagy in the fat body of Aedes aegypti is required to maintain egg maturation cycles. PLOS ONE 6:e25502 [Google Scholar]
  26. Buszczak M, Freeman MR, Carlson JR, Bender M, Cooley L, Segraves WA. 26.  1999. Ecdysone response genes govern egg chamber development during mid-oogenesis in Drosophila. Development 126:4581–89 [Google Scholar]
  27. Cardoen D, Wenseleers T, Ernst UR, Danneels EL, Laget D. 27.  et al. 2011. Genome-wide analysis of alternative reproductive phenotypes in honeybee workers. Mol. Ecol. 20:4070–84 [Google Scholar]
  28. Carpenter VK, Drake LL, Aguirre SE, Price DP, Rodriguez SD, Hansen IA. 28.  2012. SLC7 amino acid transporters of the yellow fever mosquito Aedes aegypti and their role in fat body TOR signaling and reproduction. J. Insect Physiol. 58:513–22 [Google Scholar]
  29. Chang YY, Juhasz G, Goraksha-Hicks P, Arsham AM, Mallin DR. 29.  et al. 2009. Nutrient-dependent regulation of autophagy through the target of rapamycin pathway. Biochem. Soc. Trans. 37:232–36 [Google Scholar]
  30. Chang YY, Neufeld TP. 30.  2010. Autophagy takes flight in Drosophila. FEBS Lett 584:1342–49 [Google Scholar]
  31. Charles JP, Iwema T, Epa VC, Takaki K, Rynes J, Jindra M. 31.  2011. Ligand-binding properties of a juvenile hormone receptor, Methoprene-tolerant. PNAS 108:21128–33 [Google Scholar]
  32. Chawla G, Deosthale P, Childress S, Wu YC, Sokol NS. 32.  2016. A let-7-to-miR-125 microRNA switch regulates neuronal integrity and lifespan in Drosophila. PLOS Genet 12:e1006247 [Google Scholar]
  33. Chen J, Liang Z, Liang Y, Pang R, Zhang W. 33.  2013. Conserved microRNAs miR-8-5p and miR-2a-3p modulate chitin biosynthesis in response to 20-hydroxyecdysone signaling in the brown planthopper, Nilaparvata lugens. Insect Biochem. Mol. Biol. 43:839–48 [Google Scholar]
  34. Chen L, Zhu J, Sun G, Raikhel AS. 34.  2004. The early gene Broad is involved in the ecdysteroid hierarchy governing vitellogenesis of the mosquito Aedes aegypti. J. Mol. Endocrinol. 33:743–61 [Google Scholar]
  35. Clifton ME, Noriega FG. 35.  2011. Nutrient limitation results in juvenile hormone-mediated resorption of previtellogenic ovarian follicles in mosquitoes. J. Insect Physiol. 57:1274–81 [Google Scholar]
  36. Clifton ME, Noriega FG. 36.  2012. The fate of follicles after a blood meal is dependent on previtellogenic nutrition and juvenile hormone in Aedes aegypti. J. Insect Physiol. 58:1007–19 [Google Scholar]
  37. Colombani J, Andersen DS, Leopold P. 37.  2012. Secreted peptide Dilp8 coordinates Drosophila tissue growth with developmental timing. Science 336:582–85 [Google Scholar]
  38. Colombani J, Raisin S, Pantalacci S, Radimerski T, Montagne J, Leopold P. 38.  2003. A nutrient sensor mechanism controls Drosophila growth. Cell 114:739–49 [Google Scholar]
  39. Comas D, Piulachs MD, Belles X. 39.  1999. Fast induction of vitellogenin gene expression by juvenile hormone III in the cockroach Blattella germanica (L.) (Dictyoptera, Blattellidae). Insect Biochem. Mol. Biol. 29:821–27 [Google Scholar]
  40. Comas D, Piulachs MD, Belles X. 40.  2001. Induction of vitellogenin gene transcription in vitro by juvenile hormone in Blattella germanica. Mol. Cell. Endocrinol. 183:93–100 [Google Scholar]
  41. Corona M, Velarde RA, Remolina S, Moran-Lauter A, Wang Y. 41.  et al. 2007. Vitellogenin, juvenile hormone, insulin signaling, and queen honey bee longevity. PNAS 104:7128–33 [Google Scholar]
  42. Cristino AS, Tanaka ED, Rubio M, Piulachs MD, Belles X. 42.  2011. Deep sequencing of organ- and stage-specific microRNAs in the evolutionarily basal insect Blattella germanica (L.) (Dictyoptera, Blattellidae). PLOS ONE 6:e19350 [Google Scholar]
  43. Cruz J, Mane-Padros D, Zou Z, Raikhel AS. 43.  2012. Distinct roles of isoforms of the heme-liganded nuclear receptor E75, an insect ortholog of the vertebrate Rev-Erb, in mosquito reproduction. Mol. Cell. Endocrinol. 349:262–71 [Google Scholar]
  44. Cruz J, Martin D, Pascual N, Maestro JL, Piulachs MD, Belles X. 44.  2003. Quantity does matter: juvenile hormone and the onset of vitellogenesis in the German cockroach. Insect Biochem. Mol. Biol. 33:1219–25 [Google Scholar]
  45. Cui Y, Sui Y, Xu J, Zhu F, Palli SR. 45.  2014. Juvenile hormone regulates Aedes aegypti Krüppel homolog 1 through a conserved E box motif. Insect Biochem. Mol. Biol. 52:23–32 [Google Scholar]
  46. Czech B, Hannon GJ. 46.  2011. Small RNA sorting: matchmaking for Argonautes. Nat. Rev. Genet. 12:19–31 [Google Scholar]
  47. Danielsen ET, Moeller ME, Yamanaka N, Ou Q, Laursen JM. 47.  et al. 2016. A Drosophila genome-wide screen identifies regulators of steroid hormone production and developmental timing. Dev. Cell 37:558–70 [Google Scholar]
  48. Dhara A, Eum JH, Robertson A, Gulia-Nuss M, Vogel KJ. 48.  et al. 2013. Ovary ecdysteroidogenic hormone functions independently of the insulin receptor in the yellow fever mosquito. Aedes aegypti. Insect Biochem. Mol. Biol. 43:1100–8 [Google Scholar]
  49. Di Bartolomeo S, Nazio F, Cecconi F. 49.  2010. The role of autophagy during development in higher eukaryotes. Traffic 11:1280–89 [Google Scholar]
  50. Engelmann F. 50.  1983. Vitellogenesis controlled by juvenile hormone. Endocrinology of Insects, Vol. 1 R Downer, H Laufer259–70 New York: Liss [Google Scholar]
  51. Fletcher JC, Burtis KC, Hogness DS, Thummel CS. 51.  1995. The Drosophila E74 gene is required for metamorphosis and plays a role in the polytene chromosome puffing response to ecdysone. Development 121:1455–65 [Google Scholar]
  52. Fletcher JC, Thummel CS. 52.  1995. The Drosophila E74 gene is required for the proper stage- and tissue-specific transcription of ecdysone-regulated genes at the onset of metamorphosis. Development 121:1411–21 [Google Scholar]
  53. Forstemann K, Horwich MD, Wee L, Tomari Y, Zamore PD. 53.  2007. Drosophila microRNAs are sorted into functionally distinct Argonaute complexes after production by Dicer-1. Cell 130:287–97 [Google Scholar]
  54. Forstemann K, Tomari Y, Du T, Vagin VV, Denli AM. 54.  et al. 2005. Normal microRNA maturation and germ-line stem cell maintenance requires Loquacious, a double-stranded RNA-binding domain protein. PLOS Biol 3:e236 [Google Scholar]
  55. Fricke C, Green D, Smith D, Dalmay T, Chapman T. 55.  2014. MicroRNAs influence reproductive responses by females to male sex peptide in Drosophila melanogaster. Genetics 198:1603–19 [Google Scholar]
  56. Fronstin RB, Hatle JD. 56.  2008. A cumulative feeding threshold required for vitellogenesis can be obviated with juvenile hormone treatment in lubber grasshoppers. J. Exp. Biol. 211:79–85 [Google Scholar]
  57. Fu X, Li T, Chen J, Dong Y, Qiu J. 57.  et al. 2015. Functional screen for microRNAs of Nilaparvata lugens reveals that targeting of glutamine synthase by miR-4868b regulates fecundity. J. Insect Physiol. 83:22–29 [Google Scholar]
  58. Gancz D, Gilboa L. 58.  2013. Insulin and Target of rapamycin signaling orchestrate the development of ovarian niche–stem cell units in Drosophila. Development 140:4145–54 [Google Scholar]
  59. Garaulet DL, Castellanos MC, Bejarano F, Sanfilippo P, Tyler DM. 59.  et al. 2014. Homeotic function of Drosophila Bithorax-complex miRNAs mediates fertility by restricting multiple Hox genes and TALE cofactors in the CNS. Dev. Cell 29:635–48 [Google Scholar]
  60. Gaziova I, Bonnette PC, Henrich VC, Jindra M. 60.  2004. Cell-autonomous roles of the ecdysoneless gene in Drosophila development and oogenesis. Development 131:2715–25 [Google Scholar]
  61. Ge W, Deng Q, Guo T, Hong X, Kugler JM. 61.  et al. 2015. Regulation of pattern formation and gene amplification during Drosophila oogenesis by the miR-318 microRNA. Genetics 200:255–65 [Google Scholar]
  62. Geminard C, Rulifson EJ, Leopold P. 62.  2009. Remote control of insulin secretion by fat cells in Drosophila. Cell Metab 10:199–207 [Google Scholar]
  63. Giray T, Giovanetti M, West-Eberhard MJ. 63.  2005. Juvenile hormone, reproduction, and worker behavior in the neotropical social wasp Polistes canadensis. PNAS 102:3330–35 [Google Scholar]
  64. Glinka A, Wyatt G. 64.  1996. Juvenile hormone activation of gene transcription in locust fat body. Insect Biochem. Mol. Biol. 26:13–18 [Google Scholar]
  65. Groenewoud MJ, Zwartkruis FJ. 65.  2013. Rheb and Rags come together at the lysosome to activate mTORC1. Biochem. Soc. Trans. 41:951–55 [Google Scholar]
  66. Gu SH, Yeh WL, Young SC, Lin PL, Li S. 66.  2012. TOR signaling is involved in PTTH-stimulated ecdysteroidogenesis by prothoracic glands in the silkworm, Bombyx mori. Insect Biochem. Mol. Biol. 42:296–303 [Google Scholar]
  67. Gujar H, Palli SR. 67.  2016. Juvenile hormone regulation of female reproduction in the common bed bug, Cimex lectularius. Sci. Rep. 6:35546 [Google Scholar]
  68. Gulia-Nuss M, Robertson AE, Brown MR, Strand MR. 68.  2011. Insulin-like peptides and the target of rapamycin pathway coordinately regulate blood digestion and egg maturation in the mosquito Aedes aegypti. PLOS ONE 6:e20401 [Google Scholar]
  69. Guo W, Wu Z, Song J, Jiang F, Wang Z. 69.  et al. 2014. Juvenile hormone-receptor complex acts on Mcm4 and Mcm7 to promote polyploidy and vitellogenesis in the migratory locust. PLOS Genet 10:e1004702 [Google Scholar]
  70. Gwadz RW, Spielman A. 70.  1973. Corpus allatum control of ovarian development in Aedes aegypti. J. Insect Physiol. 19:1441–48 [Google Scholar]
  71. Hackney JF, Pucci C, Naes E, Dobens L. 71.  2007. Ras signaling modulates activity of the ecdysone receptor EcR during cell migration in the Drosophila ovary. Dev. Dyn. 236:1213–26 [Google Scholar]
  72. Hagedorn H. 72.  1985. The role of ecdysteroids in reproduction. Comprehensive Insect Physiology, Biochemistry and Pharmacology G Kerkut, L Gilbert 205–26 New York: Pergamon [Google Scholar]
  73. Hagedorn H. 73.  2005. Mosquito endocrinology. Biology of Disease Vectors W Marquardt 317–27 London: Elsevier [Google Scholar]
  74. Hansen IA, Attardo GM, Park JH, Peng Q, Raikhel AS. 74.  2004. Target of rapamycin-mediated amino acid signaling in mosquito anautogeny. PNAS 101:10626–31 [Google Scholar]
  75. Hansen IA, Attardo GM, Roy SG, Raikhel AS. 75.  2005. Target of rapamycin-dependent activation of S6 kinase is a central step in the transduction of nutritional signals during egg development in a mosquito. J. Biol. Chem. 280:20565–72 [Google Scholar]
  76. Hansen IA, Boudko DY, Shiao SH, Voronov DA, Meleshkevitch EA. 76.  et al. 2011. AaCAT1 of the yellow fever mosquito, Aedes aegypti: a novel histidine-specific amino acid transporter from the SLC7 family. J. Biol. Chem. 286:10803–13 [Google Scholar]
  77. Hartfelder K, Bitondi MM, Santana WC, Simoes ZL. 77.  2002. Ecdysteroid titer and reproduction in queens and workers of the honey bee and of a stingless bee: loss of ecdysteroid function at increasing levels of sociality?. Insect Biochem. Mol. Biol. 32:211–16 [Google Scholar]
  78. Hatakeyama M, Kageyama Y, Kinoshita T, Oishi K. 78.  1995. Completion of development in Athalia rosae (Hymenoptera) eggs matured with heterospecific Athalia infumata yolk protein. J. Insect Physiol. 41:351–55 [Google Scholar]
  79. He J, Chen Q, Wei Y, Jiang F, Yang M. 79.  et al. 2016. MicroRNA-276 promotes egg-hatching synchrony by up-regulating brm in locusts. PNAS 113:584–89 [Google Scholar]
  80. He Q, Wen D, Jia Q, Cui C, Wang J. 80.  et al. 2014. Heat shock protein 83 (Hsp83) facilitates Methoprene-tolerant (Met) nuclear import to modulate juvenile hormone signaling. J. Biol. Chem. 289:27874–85 [Google Scholar]
  81. He Q, Zhang Y, Zhang X, Xu D, Dong W. 81.  et al. 2017. Nucleoporin Nup358 facilitates nuclear import of Methoprene-tolerant (Met) in an importin β- and Hsp83-dependent manner. Insect Biochem. Mol. Biol. 81:10–18 [Google Scholar]
  82. Hill RJ, Billas IM, Bonneton F, Graham LD, Lawrence MC. 82.  2013. Ecdysone receptors: from the Ashburner model to structural biology. Annu. Rev. Entomol. 58:251–71 [Google Scholar]
  83. Hou Y, Wang XL, Saha TT, Roy S, Zhao B. 83.  et al. 2015. Temporal coordination of carbohydrate metabolism during mosquito reproduction. PLOS Genet 11:e1005309 [Google Scholar]
  84. Howell JJ, Manning BD. 84.  2011. mTOR couples cellular nutrient sensing to organismal metabolic homeostasis. Trends Endocrinol. Metab. 22:94–102 [Google Scholar]
  85. Hyun S. 85.  2013. Body size regulation and insulin-like growth factor signaling. Cell. Mol. Life Sci. 70:2351–65 [Google Scholar]
  86. Iovino N, Pane A, Gaul U. 86.  2009. miR-184 has multiple roles in Drosophila female germline development. Dev. Cell 17:123–33 [Google Scholar]
  87. Jain S, Rana V, Tridibes A, Sunil S, Bhatnagar RK. 87.  2015. Dynamic expression of miRNAs across immature and adult stages of the malaria mosquito Anopheles stephensi. Parasites Vectors 8:179 [Google Scholar]
  88. Jindra M, Belles X, Shinoda T. 88.  2015. Molecular basis of juvenile hormone signaling. Curr. Opin. Insect Sci. 11:39–46 [Google Scholar]
  89. Jindra M, Uhlirova M, Charles JP, Smykal V, Hill RJ. 89.  2015. Genetic evidence for function of the bHLH-PAS protein Gce/Met as a juvenile hormone receptor. PLOS Genet 11:e1005394 [Google Scholar]
  90. Kapitskaya M, Wang S, Cress DE, Dhadialla TS, Raikhel AS. 90.  1996. The mosquito ultraspiracle homologue, a partner of ecdysteroid receptor heterodimer: cloning and characterization of isoforms expressed during vitellogenesis. Mol. Cell. Endocrinol. 121:119–32 [Google Scholar]
  91. Karim FD, Guild GM, Thummel CS. 91.  1993. The Drosophila Broad-Complex plays a key role in controlling ecdysone-regulated gene expression at the onset of metamorphosis. Development 118:977–88 [Google Scholar]
  92. Kayukawa T, Minakuchi C, Namiki T, Togawa T, Yoshiyama M. 92.  et al. 2012. Transcriptional regulation of juvenile hormone–mediated induction of Krüppel homolog 1, a repressor of insect metamorphosis. PNAS 109:11729–34 [Google Scholar]
  93. Kim J, Guan KL. 93.  2011. Amino acid signaling in TOR activation. Annu Rev. Biochem. 80:1001–32 [Google Scholar]
  94. King-Jones K, Thummel CS. 94.  2005. Nuclear receptors—a perspective from Drosophila. Nat. Rev. Genet. 6:311–23 [Google Scholar]
  95. Knapp E, Sun J. 95.  2017. Steroid signaling in mature follicles is important for Drosophila ovulation. PNAS 114:699–704 [Google Scholar]
  96. Koelle MR, Talbot WS, Segraves WA, Bender MT, Cherbas P, Hogness DS. 96.  1991. The Drosophila EcR gene encodes an ecdysone receptor, a new member of the steroid receptor superfamily. Cell 67:59–77 [Google Scholar]
  97. Kokoza VA, Martin D, Mienaltowski MJ, Ahmed A, Morton CM, Raikhel AS. 97.  2001. Transcriptional regulation of the mosquito vitellogenin gene via a blood meal–triggered cascade. Gene 274:47–65 [Google Scholar]
  98. Konig A, Shcherbata HR. 98.  2015. Soma influences GSC progeny differentiation via the cell adhesion–mediated steroid-let-7-Wingless signaling cascade that regulates chromatin dynamics. Biol. Open 4:285–300 [Google Scholar]
  99. Konig A, Yatsenko AS, Weiss M, Shcherbata HR. 99.  2011. Ecdysteroids affect Drosophila ovarian stem cell niche formation and early germline differentiation. EMBO J 30:1549–62 [Google Scholar]
  100. Koyama T, Mendes CC, Mirth CK. 100.  2013. Mechanisms regulating nutrition-dependent developmental plasticity through organ-specific effects in insects. Front. Physiol. 4:263 [Google Scholar]
  101. Kugler JM, Chen YW, Weng R, Cohen SM. 101.  2013. Maternal loss of miRNAs leads to increased variance in primordial germ cell numbers in Drosophila melanogaster. G3 3:1573–76 [Google Scholar]
  102. LaFever L, Drummond-Barbosa D. 102.  2005. Direct control of germline stem cell division and cyst growth by neural insulin in Drosophila. Science 309:1071–73 [Google Scholar]
  103. Lasko P. 103.  2011. Posttranscriptional regulation in Drosophila oocytes and early embryos. Wiley Interdiscip. Rev. RNA 2:408–16 [Google Scholar]
  104. Li B, Predel R, Neupert S, Hauser F, Tanaka Y. 104.  et al. 2008. Genomics, transcriptomics, and peptidomics of neuropeptides and protein hormones in the red flour beetle Tribolium castaneum. Genome Res 18:113–22 [Google Scholar]
  105. Li M, Liu P, Wiley JD, Ojani R, Bevan DR. 105.  et al. 2014. A steroid receptor coactivator acts as the DNA-binding partner of the Methoprene-tolerant protein in regulating juvenile hormone response genes. Mol. Cell. Endocrinol. 394:47–58 [Google Scholar]
  106. Li M, Mead EA, Zhu J. 106.  2011. Heterodimer of two bHLH-PAS proteins mediates juvenile hormone–induced gene expression. PNAS 108:638–43 [Google Scholar]
  107. Liao XH, Majithia A, Huang X, Kimmel AR. 107.  2008. Growth control via TOR kinase signaling, an intracellular sensor of amino acid and energy availability, with crosstalk potential to proline metabolism. Amino Acids 35:761–70 [Google Scholar]
  108. Liu P, Peng HJ, Zhu J. 108.  2015. Juvenile hormone–activated phospholipase C pathway enhances transcriptional activation by the Methoprene-tolerant protein. PNAS 112:E1871–79 [Google Scholar]
  109. Liu S, Lucas KJ, Roy S, Ha J, Raikhel AS. 109.  2014. Mosquito-specific microRNA-1174 targets serine hydroxymethyltransferase to control key functions in the gut. PNAS 111:14460–65 [Google Scholar]
  110. Loewith R, Hall MN. 110.  2011. Target of rapamycin (TOR) in nutrient signaling and growth control. Genetics 189:1177–201 [Google Scholar]
  111. Lozano J, Kayukawa T, Shinoda T, Belles X. 111.  2014. A role for Taiman in insect metamorphosis. PLOS Genet 10:e1004769 [Google Scholar]
  112. Lu K, Chen X, Liu WT, Zhang XY, Chen MX, Zhou Q. 112.  2016. Nutritional signaling regulates vitellogenin synthesis and egg development through juvenile hormone in Nilaparvata lugens (Stål). Int. J. Mol. Sci. 17:269 [Google Scholar]
  113. Lu K, Chen X, Liu WT, Zhou Q. 113.  2016. TOR pathway-mediated juvenile hormone synthesis regulates nutrient-dependent female reproduction in Nilaparvata lugens (Stål). Int. J. Mol. Sci. 17:438 [Google Scholar]
  114. Lucas KJ, Myles KM, Raikhel AS. 114.  2013. Small RNAs: a new frontier in mosquito biology. Trends Parasitol 29:295–303 [Google Scholar]
  115. Lucas KJ, Raikhel AS. 115.  2013. Insect microRNAs: biogenesis, expression profiling and biological functions. Insect Biochem. Mol. Biol. 43:24–38 [Google Scholar]
  116. Lucas KJ, Roy S, Ha J, Gervaise AL, Kokoza VA, Raikhel AS. 116.  2015. MicroRNA-8 targets the Wingless signaling pathway in the female mosquito fat body to regulate reproductive processes. PNAS 112:1440–45 [Google Scholar]
  117. Lucas KJ, Zhao B, Liu S, Raikhel AS. 117.  2015. Regulation of physiological processes by microRNAs in insects. Curr. Opin. Insect Sci. 11:1–7 [Google Scholar]
  118. Lucas KJ, Zhao B, Roy S, Gervaise AL, Raikhel AS. 118.  2015. Mosquito-specific microRNA-1890 targets the juvenile hormone–regulated serine protease JHA15 in the female mosquito gut. RNA Biol 12:1383–90 [Google Scholar]
  119. Luhur A, Chawla G, Sokol NS. 119.  2013. MicroRNAs as components of systemic signaling pathways in Drosophila melanogaster. Curr. Top. Dev. Biol. 105:97–123 [Google Scholar]
  120. Luo M, Li D, Wang Z, Guo W, Kang L, Zhou S. 120.  2017. Juvenile hormone differentially regulates two Grp78 genes encoding protein chaperones required for insect fat body cell homeostasis and vitellogenesis. J. Biol. Chem. 292:8823–34 [Google Scholar]
  121. Maestro JL, Cobo J, Belles X. 121.  2009. Target of rapamycin (TOR) mediates the transduction of nutritional signals into juvenile hormone production. J. Biol. Chem. 284:5506–13 [Google Scholar]
  122. Mane-Padros D, Cruz J, Cheng A, Raikhel AS. 122.  2012. A critical role of the nuclear receptor HR3 in regulation of gonadotrophic cycles of the mosquito Aedes aegypti. PLOS ONE 7:e45019 [Google Scholar]
  123. Marchal E, Hult EF, Huang J, Pang Z, Stay B, Tobe SS. 123.  2014. Methoprene-tolerant (Met) knockdown in the adult female cockroach, Diploptera punctata, completely inhibits ovarian development. PLOS ONE 9:e106737 [Google Scholar]
  124. Mead EA, Tu Z. 124.  2008. Cloning, characterization, and expression of microRNAs from the Asian malaria mosquito, Anopheles stephensi. BMC Genom. 9:244 [Google Scholar]
  125. Mello TR, Aleixo AC, Pinheiro DG, Nunes FM, Bitondi MM. 125.  et al. 2014. Developmental regulation of ecdysone receptor (EcR) and EcR-controlled gene expression during pharate–adult development of honeybees (Apis mellifera). Front. Genet. 5:445 [Google Scholar]
  126. Miura K, Oda M, Makita S, Chinzei Y. 126.  2005. Characterization of the Drosophila Methoprene-tolerant gene product: juvenile hormone binding and ligand-dependent gene regulation. FEBS J 272:1169–78 [Google Scholar]
  127. Nakahara K, Kim K, Sciulli C, Dowd SR, Minden JS, Carthew RW. 127.  2005. Targets of microRNA regulation in the Drosophila oocyte proteome. PNAS 102:12023–28 [Google Scholar]
  128. Nassel DR, Liu Y, Luo J. 128.  2015. Insulin/IGF signaling and its regulation in Drosophila. Gen. Comp. Endocrinol. 221:255–66 [Google Scholar]
  129. Ojani R, Liu P, Fu X, Zhu J. 129.  2016. Protein kinase C modulates transcriptional activation by the juvenile hormone receptor Methoprene-tolerant. Insect Biochem. Mol. Biol. 70:44–52 [Google Scholar]
  130. Park JH, Attardo GM, Hansen IA, Raikhel AS. 130.  2006. GATA factor translation is the final downstream step in the amino acid/target-of-rapamycin-mediated vitellogenin gene expression in the anautogenous mosquito Aedes aegypti. J. Biol. Chem. 281:11167–76 [Google Scholar]
  131. Parthasarathy R, Palli SR. 131.  2011. Molecular analysis of nutritional and hormonal regulation of female reproduction in the red flour beetle, Tribolium castaneum. Insect Biochem. Mol. Biol. 41:294–305 [Google Scholar]
  132. Parthasarathy R, Sheng Z, Sun Z, Palli SR. 132.  2010. Ecdysteroid regulation of ovarian growth and oocyte maturation in the red flour beetle, Tribolium castaneum. Insect Biochem. Mol. Biol. 40:429–39 [Google Scholar]
  133. Parthasarathy R, Sun Z, Bai H, Palli SR. 133.  2010. Juvenile hormone regulation of vitellogenin synthesis in the red flour beetle, Tribolium castaneum. Insect Biochem. Mol. Biol. 40:405–14 [Google Scholar]
  134. Paulo DF, Azeredo-Espin AM, Canesin LE, Vicentini R, Junqueira AC. 134.  2017. Identification and characterization of microRNAs in the screwworm flies Cochliomyia hominivorax and Cochliomyia macellaria (Diptera: Calliphoridae). Insect Mol. Biol. 26:46–57 [Google Scholar]
  135. Penick CA, Liebig J, Brent CS. 135.  2011. Reproduction, dominance, and caste: endocrine profiles of queens and workers of the ant Harpegnathos saltator. J. Comp. Physiol. A 197:1063–71 [Google Scholar]
  136. Perez-Hedo M, Rivera-Perez C, Noriega FG. 136.  2013. The insulin/TOR signal transduction pathway is involved in the nutritional regulation of juvenile hormone synthesis in Aedes aegypti. Insect Biochem. Mol. Biol. 43:495–500 [Google Scholar]
  137. Pierceall WE, Li C, Biran A, Miura K, Raikhel AS, Segraves WA. 137.  1999. E75 expression in mosquito ovary and fat body suggests reiterative use of ecdysone-regulated hierarchies in development and reproduction. Mol. Cell. Endocrinol. 150:73–89 [Google Scholar]
  138. Puthiyakunnon S, Yao Y, Li Y, Gu J, Peng H, Chen X. 138.  2013. Functional characterization of three microRNAs of the Asian tiger mosquito, Aedes albopictus. Parasites Vectors 6:230 [Google Scholar]
  139. Raikhel A. 139.  2005. Vitellogenesis of disease vectors, from physiology to genes. Biology of Disease Vectors W Marquardt 329–46 London: Elsevier [Google Scholar]
  140. Raikhel A, Brown M, Belles X. 140.  2005. Hormonal control of reproductive processes. Comprehensive Insect Physiology, Biochemistry, Pharmacology and Molecular Biology 3 L Gilbert, S Gill, K Iatrou 433–91 Amsterdam: Elsevier [Google Scholar]
  141. Ramaswamy SB, Shu S, Park YI, Zeng F. 141.  1997. Dynamics of juvenile hormone-‐mediated gonadotropism in the Lepidoptera. Arch. Insect Biochem. Physiol. 35:539–58 [Google Scholar]
  142. Reinking J, Lam MM, Pardee K, Sampson HM, Liu S. 142.  et al. 2005. The Drosophila nuclear receptor E75 contains heme and is gas responsive. Cell 122:195–207 [Google Scholar]
  143. Richard DS, Rybczynski R, Wilson TG, Wang Y, Wayne ML. 143.  et al. 2005. 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. Insect Physiol. 51:455–64 [Google Scholar]
  144. Riddiford LM. 144.  2012. How does juvenile hormone control insect metamorphosis and reproduction?. Gen. Comp. Endocrinol. 179:477–84 [Google Scholar]
  145. Riehle MA, Fan Y, Cao C, Brown MR. 145.  2006. Molecular characterization of insulin-like peptides in the yellow fever mosquito, Aedes aegypti: expression, cellular localization, and phylogeny. Peptides 27:2547–60 [Google Scholar]
  146. Robinson GE, Strambi C, Strambi A, Feldlaufer MF. 146.  1991. Comparison of juvenile hormone and ecdysteroid haemolymph titres in adult worker and queen honey bees (Apis mellifera). J. Insect Physiol. 37:929–35 [Google Scholar]
  147. Robinson GE, Vargo EL. 147.  1997. Juvenile hormone in adult eusocial Hymenoptera: gonadotropin and behavioral pacemaker. Arch. Insect Biochem. Physiol. 35:559–83 [Google Scholar]
  148. Romani P, Bernardi F, Hackney J, Dobens L, Gargiulo G, Cavaliere V. 148.  2009. Cell survival and polarity of Drosophila follicle cells require the activity of ecdysone receptor B1 isoform. Genetics 181:165–75 [Google Scholar]
  149. Roy S, Saha TT, Johnson L, Zhao B, Ha J. 149.  et al. 2015. Regulation of gene expression patterns in mosquito reproduction. PLOS Genet 11:e1005450 [Google Scholar]
  150. Roy S, Smykal V, Johnson L, Saha TT, Zou Z, Raikhel AS. 150.  2016. Regulation of reproductive processes in female mosquitoes. Adv. Insect Physiol. 51:115–44 [Google Scholar]
  151. Roy SG, Raikhel AS. 151.  2011. The small GTPase Rheb is a key component linking amino acid signaling and TOR in the nutritional pathway that controls mosquito egg development. Insect Biochem. Mol. Biol. 41:62–69 [Google Scholar]
  152. Roy SG, Raikhel AS. 152.  2012. Nutritional and hormonal regulation of the TOR effector 4E-binding protein (4E-BP) in the mosquito Aedes aegypti. FASEB J 26:1334–42 [Google Scholar]
  153. Saha TT, Shin SW, Dou W, Roy S, Zhao B. 153.  et al. 2016. Hairy and Groucho mediate the action of juvenile hormone receptor Methoprene-tolerant in gene repression. PNAS 113:E735–43 [Google Scholar]
  154. Sancak Y, Peterson TR, Shaul YD, Lindquist RA, Thoreen CC. 154.  et al. 2008. The Rag GTPases bind raptor and mediate amino acid signaling to mTORC1. Science 320:1496–501 [Google Scholar]
  155. Segraves WA, Hogness DS. 155.  1990. The E75 ecdysone-inducible gene responsible for the 75B early puff in Drosophila encodes two new members of the steroid receptor superfamily. Genes Dev 4:204–19 [Google Scholar]
  156. Sehnal F, Svacha P, Zrzavy J. 156.  1996. Evolution of insect metamorphosis. Metamorphosis: Postembryonic Reprogramming of Gene Expression in Amphibian and Insect Cells L Gilbert, J Tata, B Atkinson 3–58 San Diego: Academic [Google Scholar]
  157. Sheng Z, Xu J, Bai H, Zhu F, Palli SR. 157.  2011. Juvenile hormone regulates vitellogenin gene expression through insulin-like peptide signaling pathway in the red flour beetle, Tribolium castaneum. J. Biol. Chem. 286:41924–36 [Google Scholar]
  158. Shiao SH, Hansen IA, Zhu J, Sieglaff DH, Raikhel AS. 158.  2008. Juvenile hormone connects larval nutrition with target of rapamycin signaling in the mosquito Aedes aegypti. J. Insect Physiol. 54:231–39 [Google Scholar]
  159. Shin SW, Zou Z, Saha TT, Raikhel AS. 159.  2012. bHLH-PAS heterodimer of Methoprene-tolerant and Cycle mediates circadian expression of juvenile hormone–induced mosquito genes. PNAS 109:16576–81 [Google Scholar]
  160. Shpigler H, Amsalem E, Huang ZY, Cohen M, Siegel AJ. 160.  et al. 2014. Gonadotropic and physiological functions of juvenile hormone in Bumblebee (Bombus terrestris) workers. PLOS ONE 9:e100650 [Google Scholar]
  161. Sieber MH, Spradling AC. 161.  2015. Steroid signaling establishes a female metabolic state and regulates SREBP to control oocyte lipid accumulation. Curr. Biol. 25:993–1004 [Google Scholar]
  162. Sim C, Denlinger DL. 162.  2008. Insulin signaling and FOXO regulate the overwintering diapause of the mosquito Culex pipiens. PNAS 105:6777–81 [Google Scholar]
  163. Smykal V, Bajgar A, Provaznik J, Fexova S, Buricova M. 163.  et al. 2014. Juvenile hormone signaling during reproduction and development of the linden bug, Pyrrhocoris apterus. Insect Biochem. Mol. Biol. 45:69–76 [Google Scholar]
  164. Smykal V, Raikhel AS. 164.  2015. Nutritional control of insect reproduction. Curr. Opin. Insect Sci. 11:31–38 [Google Scholar]
  165. Sokol NS, Xu P, Jan YN, Ambros V. 165.  2008. Drosophila let-7 microRNA is required for remodeling of the neuromusculature during metamorphosis. Genes Dev 22:1591–96 [Google Scholar]
  166. Song J, Guo W, Jiang F, Kang L, Zhou S. 166.  2013. Argonaute 1 is indispensable for juvenile hormone mediated oogenesis in the migratory locust, Locusta migratoria. Insect Biochem. Mol. Biol. 43:879–87 [Google Scholar]
  167. Song J, Wu Z, Wang Z, Deng S, Zhou S. 167.  2014. Krüppel-homolog 1 mediates juvenile hormone action to promote vitellogenesis and oocyte maturation in the migratory locust. Insect Biochem. Mol. Biol. 52:94–101 [Google Scholar]
  168. Soni K, Choudhary A, Patowary A, Singh AR, Bhatia S. 168.  et al. 2013. miR-34 is maternally inherited in Drosophila melanogaster and Danio rerio. Nucleic Acids Res 41:4470–80 [Google Scholar]
  169. Sorge D, Nauen R, Range S, Hoffmann KH. 169.  2000. Regulation of vitellogenesis in the fall armyworm, Spodopterafrugiperda (Lepidoptera: Noctuidae). J. Insect Physiol. 46:969–76 [Google Scholar]
  170. Sun G, Zhu J, Chen L, Raikhel AS. 170.  2005. Synergistic action of E74B and ecdysteroid receptor in activating a 20-hydroxyecdysone effector gene. PNAS 102:15506–11 [Google Scholar]
  171. Sun G, Zhu J, Li C, Tu Z, Raikhel AS. 171.  2002. Two isoforms of the early E74 gene, an Ets transcription factor homologue, are implicated in the ecdysteroid hierarchy governing vitellogenesis of the mosquito, Aedes aegypti. Mol. Cell. Endocrinol. 190:147–57 [Google Scholar]
  172. Sun G, Zhu J, Raikhel AS. 172.  2004. The early gene E74B isoform is a transcriptional activator of the ecdysteroid regulatory hierarchy in mosquito vitellogenesis. Mol. Cell. Endocrinol. 218:95–105 [Google Scholar]
  173. Swevers L, Iatrou K. 173.  2009. Ecdysteroids and ecdysteroid signaling pathways during insect oogenesis. Ecdysone: Structures and Functions G. Smagghe 127–64 Dordrecht, Neth.: Springer [Google Scholar]
  174. Swevers L, Raikhel A, Sappington T, Shirk P, Iatrou K. 174.  2005. Vitellogenesis and post-vitellogenic maturation of the insect ovarian follicle. Comprehensive Insect Physiology, Biochemistry, Pharmacology and Molecular Biology 3 L Gilbert, S Gill, K Iatrou 87–155 Amsterdam: Elsevier [Google Scholar]
  175. Talbot WS, Swyryd EA, Hogness DS. 175.  1993. Drosophila tissues with different metamorphic responses to ecdysone express different ecdysone receptor isoforms. Cell 73:1323–37 [Google Scholar]
  176. Tanaka ED, Piulachs MD. 176.  2012. Dicer-1 is a key enzyme in the regulation of oogenesis in panoistic ovaries. Biol. Cell 104:452–61 [Google Scholar]
  177. Tatar M, Kopelman A, Epstein D, Tu MP, Yin CM, Garofalo RS. 177.  2001. A mutant Drosophila insulin receptor homolog that extends life-span and impairs neuroendocrine function. Science 292:107–10 [Google Scholar]
  178. Terashima J, Bownes M. 178.  2004. Translating available food into the number of eggs laid by Drosophila melanogaster. Genetics 167:1711–19 [Google Scholar]
  179. Terashima J, Bownes M. 179.  2006. E75A and E75B have opposite effects on the apoptosis/development choice of the Drosophila egg chamber. Cell Death Differ 13:454–64 [Google Scholar]
  180. Thomas HE, Stunnenberg HG, Stewart AF. 180.  1993. Heterodimerization of the Drosophila ecdysone receptor with retinoid X receptor and ultraspiracle. Nature 362:471–75 [Google Scholar]
  181. Tu MP, Yin CM, Tatar M. 181.  2002. Impaired ovarian ecdysone synthesis of Drosophila melanogaster insulin receptor mutants. Aging Cell 1:158–60 [Google Scholar]
  182. Tu MP, Yin CM, Tatar M. 182.  2005. Mutations in insulin signaling pathway alter juvenile hormone synthesis in Drosophila melanogaster. Gen. Comp. Endocrinol. 142:347–56 [Google Scholar]
  183. Van Wielendaele P, Badisco L, Vanden Broeck J. 183.  2013. Neuropeptidergic regulation of reproduction in insects. Gen. Comp. Endocrinol. 188:23–34 [Google Scholar]
  184. Vilmos P, Bujna A, Szuperak M, Havelda Z, Varallyay E. 184.  et al. 2013. Viability, longevity, and egg production of Drosophila melanogaster are regulated by the miR-282 microRNA. Genetics 195:469–80 [Google Scholar]
  185. Vogel KJ, Brown MR, Strand MR. 185.  2015. Ovary ecdysteroidogenic hormone requires a receptor tyrosine kinase to activate egg formation in the mosquito Aedes aegypti. PNAS 112:5057–62 [Google Scholar]
  186. Wang JL, Saha TT, Zhang Y, Zhang C, Raikhel AS. 186.  2017. Juvenile hormone and its receptor Methoprene-tolerant promote ribosomal biogenesis and vitellogenesis in the Aedes aegypti mosquito. J. Biol. Chem. 292:10306–15 [Google Scholar]
  187. Wang SF, Li C, Sun G, Zhu J, Raikhel AS. 187.  2002. Differential expression and regulation by 20-hydroxyecdysone of mosquito ecdysteroid receptor isoforms A and B. Mol. Cell. Endocrinol. 196:29–42 [Google Scholar]
  188. Wang X, Hou Y, Saha TT, Pei G, Raikhel AS, Zou Z. 188.  2017. Hormone and receptor interplay in the regulation of mosquito lipid metabolism. PNAS 114:E2709–18 [Google Scholar]
  189. Wang Z, Yang L, Song J, Kang L, Zhou S. 189.  2017. An isoform of Taiman that contains a PRD-repeat motif is indispensable for transducing the vitellogenic juvenile hormone signal in Locusta migratoria. Insect Biochem. Mol. Biol. 82:31–40 [Google Scholar]
  190. Wasielewski O, Wojciechowicz T, Giejdasz K, Krishnan N. 190.  2011. Influence of methoprene and temperature on diapause termination in adult females of the over-wintering solitary bee, Osmia rufa L. J. Insect Physiol. 57:1682–88 [Google Scholar]
  191. Wegener J, Huang ZY, Lorenz MW, Lorenz JI, Bienefeld K. 191.  2013. New insights into the roles of juvenile hormone and ecdysteroids in honey bee reproduction. J. Insect Physiol. 59:655–61 [Google Scholar]
  192. Wen Z, Gulia M, Clark KD, Dhara A, Crim JW. 192.  et al. 2010. Two insulin-like peptide family members from the mosquito Aedes aegypti exhibit differential biological and receptor binding activities. Mol. Cell. Endocrinol. 328:47–55 [Google Scholar]
  193. Weng R, Chin JS, Yew JY, Bushati N, Cohen SM. 193.  2013. miR-124 controls male reproductive success in Drosophila. eLife 2:e00640 [Google Scholar]
  194. Weng SC, Shiao SH. 194.  2015. Frizzled 2 is a key component in the regulation of TOR signaling–mediated egg production in the mosquito Aedes aegypti. Insect Biochem. Mol. Biol. 61:17–24 [Google Scholar]
  195. West-Eberhard MJ. 195.  1996. Wasp societies as microcosms for the study of development and evolution. Natural History and Evolution of Paper-Wasps S Turillazzi, MJ West-Eberhard 290–371 Oxford, UK: Oxford Univ. Press [Google Scholar]
  196. Wigglesworth VB. 196.  1936. The function of the corpus allatum in the growth and reproduction of Rhodnius prolixus (Hemiptera). Q. J. Microsc. Sci. 79:91–121 [Google Scholar]
  197. Wilson TG, Fabian J. 197.  1986. A Drosophila melanogaster mutant resistant to a chemical analog of juvenile hormone. Dev. Biol. 118:190–201 [Google Scholar]
  198. Wu Q, Brown MR. 198.  2006. Signaling and function of insulin-like peptides in insects. Annu. Rev. Entomol. 51:1–24 [Google Scholar]
  199. Wu Z, Guo W, Xie Y, Zhou S. 199.  2016. Juvenile hormone activates the transcription of cell-division-cycle 6 (Cdc6) for polyploidy-dependent insect vitellogenesis and oogenesis. J. Biol. Chem. 291:5418–27 [Google Scholar]
  200. Wullschleger S, Loewith R, Hall MN. 200.  2006. TOR signaling in growth and metabolism. Cell 124:471–84 [Google Scholar]
  201. Wyatt GR, Davey KG. 201.  1996. Cellular and molecular actions of juvenile hormone. II. Roles of juvenile hormone in adult insects. Adv. Insect Physiol. 26:1–155 [Google Scholar]
  202. Xu HJ, Xue J, Lu B, Zhang XC, Zhuo JC. 202.  et al. 2015. Two insulin receptors determine alternative wing morphs in planthoppers. Nature 519:464–67 [Google Scholar]
  203. Yang H, Gong R, Xu Y. 203.  2013. Control of cell growth: Rag GTPases in activation of TORC1. Cell. Mol. Life Sci. 70:2873–85 [Google Scholar]
  204. Yao TP, Forman BM, Jiang Z, Cherbas L, Chen JD. 204.  et al. 1993. Functional ecdysone receptor is the product of EcR and Ultraspiracle genes. Nature 366:476–79 [Google Scholar]
  205. Yao TP, Segraves WA, Oro AE, McKeown M, Evans RM. 205.  1992. Drosophila ultraspiracle modulates ecdysone receptor function via heterodimer formation. Cell 71:63–72 [Google Scholar]
  206. Zhai H, Fesler A, Ju J. 206.  2013. MicroRNA: a third dimension in autophagy. Cell Cycle 12:246–50 [Google Scholar]
  207. Zhang X, Aksoy E, Girke T, Raikhel AS, Karginov FV. 207.  2017. Transcriptome-wide microRNA and target dynamics in the fat body during the gonadotrophic cycle of Aedes aegypti. PNAS 114:E1895–903 [Google Scholar]
  208. Zhang Y, Zhao B, Roy S, Saha TT, Kokoza VA. 208.  et al. 2016. microRNA-309 targets the homeobox gene SIX4 and controls ovarian development in the mosquito Aedes aegypti. PNAS 113:E4828–36 [Google Scholar]
  209. Zhang Z, Xu J, Sheng Z, Sui Y, Palli SR. 209.  2011. Steroid receptor co-activator is required for juvenile hormone signal transduction through a bHLH-PAS transcription factor, Methoprene tolerant. J. Biol. Chem. 286:8437–47 [Google Scholar]
  210. Zhao B, Hou Y, Wang J, Kokoza VA, Saha TT. 210.  et al. 2016. Determination of juvenile hormone titers by means of LC-MS/MS/MS and a juvenile hormone–responsive Gal4/UAS system in Aedes aegypti mosquitoes. Insect Biochem. Mol. Biol. 77:69–77 [Google Scholar]
  211. Zhu J, Busche JM, Zhang X. 211.  2010. Identification of juvenile hormone target genes in the adult female mosquitoes. Insect Biochem. Mol. Biol. 40:23–29 [Google Scholar]
  212. Zhu J, Chen L, Raikhel AS. 212.  2007. Distinct roles of Broad isoforms in regulation of the 20-hydroxyecdysone effector gene, Vitellogenin, in the mosquito Aedes aegypti. Mol. Cell. Endocrinol 267:97–105 [Google Scholar]
  213. Zhu J, Chen L, Sun G, Raikhel AS. 213.  2006. The competence factor βFtz-F1 potentiates ecdysone receptor activity via recruiting a p160/SRC coactivator. Mol. Cell Biol. 26:9402–12 [Google Scholar]
  214. Zou Z, Saha TT, Roy S, Shin SW, Backman TW. 214.  et al. 2013. Juvenile hormone and its receptor, Methoprene-tolerant, control the dynamics of mosquito gene expression. PNAS 110:E2173–81 [Google Scholar]
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