Skip to main content

Advertisement

Log in

Post-transcriptional regulation of insect metamorphosis and oogenesis

  • Review
  • Published:
Cellular and Molecular Life Sciences Aims and scope Submit manuscript

Abstract

Metamorphic transformation from larvae to adults along with the high fecundity is key to insect success. Insect metamorphosis and reproduction are governed by two critical endocrines, juvenile hormone (JH), and 20-hydroxyecdysone (20E). Recent studies have established a crucial role of microRNA (miRNA) in insect metamorphosis and oogenesis. While miRNAs target genes involved in JH and 20E-signaling pathways, these two hormones reciprocally regulate miRNA expression, forming regulatory loops of miRNA with JH and 20E-signaling cascades. Insect metamorphosis and oogenesis rely on the coordination of hormones, cognate genes, and miRNAs for precise regulation. In addition, the alternative splicing of genes in JH and 20E-signaling pathways has distinct functions in insect metamorphosis and oogenesis. We, therefore, focus in this review on recent advances in post-transcriptional regulation, with the emphasis on the regulatory role of miRNA and alternative splicing, in insect metamorphosis and oogenesis. We will highlight important new findings of miRNA interactions with hormonal signaling and alternative splicing of JH receptor heterodimer gene Taiman.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5

Similar content being viewed by others

References

  1. Debecker S, Dinh KV, Stoks R (2017) Strong delayed interactive effects of metal exposure and warming: latitude-dependent synergisms persist across metamorphosis. Environ Sci Technol 51(4):2409–2417. https://doi.org/10.1021/acs.est.6b04989

    Article  CAS  PubMed  Google Scholar 

  2. Heneberg P, Bogusch P, Astapenková A (2019) The effects of contact exposure to azole fungicides on insect metamorphosis. Crop Protect 121:66–72. https://doi.org/10.1016/j.cropro.2019.03.012

    Article  CAS  Google Scholar 

  3. Wesner JS, Kraus JM, Schmidt TS, Walters DM, Clements WH (2014) Metamorphosis enhances the effects of metal exposure on the mayfly, Centroptilum triangulifer. Environ Sci Technol 48(17):10415–10422. https://doi.org/10.1021/es501914y

    Article  CAS  PubMed  Google Scholar 

  4. Jindra M, Belles X, Shinoda T (2015) Molecular basis of juvenile hormone signaling. Curr Opin Insect Sci 11:39–46. https://doi.org/10.1016/j.cois.2015.08.004

    Article  PubMed  Google Scholar 

  5. Jindra M, Palli SR, Riddiford LM (2013) The juvenile hormone signaling pathway in insect development. Annu Rev Entomol 58:181–204. https://doi.org/10.1146/annurev-ento-120811-153700

    Article  CAS  PubMed  Google Scholar 

  6. Riddiford LM (1994) Cellular and molecular actions of juvenile-hormone I. General-considerations and premetamorphic actions. Adv Insect Physiol 24:213–274. https://doi.org/10.1016/S0065-2806(08)60084-3

    Article  CAS  Google Scholar 

  7. Zhou B, Hiruma K, Shinoda T, Riddiford LM (1998) Juvenile hormone prevents ecdysteroid-induced expression of broad complex RNAs in the epidermis of the tobacco hornworm, Manduca sexta. Dev Biol 203(2):233–244. https://doi.org/10.1006/dbio.1998.9059

    Article  CAS  PubMed  Google Scholar 

  8. Zhou X, Riddiford LM (2002) Broad specifies pupal development and mediates the ‘status quo’ action of juvenile hormone on the pupal-adult transformation in Drosophila and Manduca. Development 129(9):2259–2269

    CAS  PubMed  Google Scholar 

  9. Raikhel AS, Brown MR, Belles X (2005) Hormonal control of reproductive processes. In: Gilbert LI (ed) Comprehensive molecular insect science. Elsevier, Amsterdam, pp 433–491. https://doi.org/10.1016/b0-44-451924-6/00040-5

    Chapter  Google Scholar 

  10. Roy S, Saha TT, Zou Z, Raikhel AS (2018) Regulatory pathways controlling female insect reproduction. Annu Rev Entomol 63:489–511. https://doi.org/10.1146/annurev-ento-020117-043258

    Article  CAS  PubMed  Google Scholar 

  11. Belles X (2005) Vitellogenesis directed by juvenile hormone. Reprod Biol Invertebr 12:157–197

    CAS  Google Scholar 

  12. Wyatt GR, Davey KG (1996) Cellular and molecular actions of juvenile hormone. II. Roles of juvenile hormone in adult insects. Adv Insect Physiol 26:1–155. https://doi.org/10.1016/S0065-2806(08)60030-2

    Article  CAS  Google Scholar 

  13. Yao TP, Forman BM, Jiang Z, Cherbas L, Chen JD, McKeown M, Cherbas P, Evans RM (1993) Functional ecdysone receptor is the product of EcR and Ultraspiracle genes. Nature 366(6454):476–479. https://doi.org/10.1038/366476a0

    Article  CAS  PubMed  Google Scholar 

  14. Buszczak M, Segraves WA (2000) Insect metamorphosis: out with the old, in with the new. Curr Biol 10(22):R830–R833. https://doi.org/10.1016/s0960-9822(00)00792-2

    Article  CAS  PubMed  Google Scholar 

  15. Yamanaka N, Rewitz KF, O’Connor MB (2013) Ecdysone control of developmental transitions: lessons from Drosophila research. Annu Rev Entomol 58:497–516. https://doi.org/10.1146/annurev-ento-120811-153608

    Article  CAS  PubMed  Google Scholar 

  16. Schwedes CC, Carney GE (2012) Ecdysone signaling in adult Drosophila melanogaster. J Insect Physiol 58(3):293–302. https://doi.org/10.1016/j.jinsphys.2012.01.013

    Article  CAS  PubMed  Google Scholar 

  17. Swevers L (2019) An update on ecdysone signaling during insect oogenesis. Curr Opin Insect Sci 31:8–13. https://doi.org/10.1016/j.cois.2018.07.003

    Article  PubMed  Google Scholar 

  18. Belles X, Piulachs MD (2015) Ecdysone signalling and ovarian development in insects: from stem cells to ovarian follicle formation. Biochim Biophys Acta 1849(2):181–186. https://doi.org/10.1016/j.bbagrm.2014.05.025

    Article  CAS  PubMed  Google Scholar 

  19. Truman JW, Riddiford LM (2002) Endocrine insights into the evolution of metamorphosis in insects. Annu Rev Entomol 47:467–500. https://doi.org/10.1146/annurev.ento.47.091201.145230

    Article  CAS  PubMed  Google Scholar 

  20. Charles JP, Iwema T, Epa VC, Takaki K, Rynes J, Jindra M (2011) Ligand-binding properties of a juvenile hormone receptor, Methoprene-tolerant. Proc Natl Acad Sci USA 108(52):21128–21133. https://doi.org/10.1073/pnas.1116123109

    Article  PubMed  PubMed Central  Google Scholar 

  21. Li M, Mead EA, Zhu J (2011) Heterodimer of two bHLH-PAS proteins mediates juvenile hormone-induced gene expression. Proc Natl Acad Sci USA 108(2):638–643. https://doi.org/10.1073/pnas.1013914108

    Article  CAS  PubMed  Google Scholar 

  22. Jindra M, Uhlirova M, Charles JP, Smykal V, Hill RJ (2015) Genetic evidence for function of the bHLH-PAS protein Gce/Met As a Juvenile hormone receptor. PLoS Genet 11(7):e1005394. https://doi.org/10.1371/journal.pgen.1005394

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  23. Cui Y, Sui Y, Xu J, Zhu F, Palli SR (2014) Juvenile hormone regulates Aedes aegypti Krüppel homolog 1 through a conserved E box motif. Insect Biochem Mol Biol 52:23–32. https://doi.org/10.1016/j.ibmb.2014.05.009

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  24. Guo W, Wu Z, Song J, Jiang F, Wang Z, Deng S, Walker VK, Zhou S (2014) Juvenile hormone-receptor complex acts on mcm4 and mcm7 to promote polyploidy and vitellogenesis in the migratory locust. PLoS Genet 10(10):e1004702. https://doi.org/10.1371/journal.pgen.1004702

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  25. Li K, Jia QQ, Li S (2019) Juvenile hormone signaling—a mini review. Insect Sci 26(4):600–606. https://doi.org/10.1111/1744-7917.12614

    Article  CAS  PubMed  Google Scholar 

  26. Wu Z, Guo W, Xie Y, Zhou S (2016) Juvenile hormone activates the transcription of cell-division-cycle 6 (Cdc6) for polyploidy-dependent insect vitellogenesis and oogenesis. J Biol Chem 291(10):5418–5427. https://doi.org/10.1074/jbc.M115.698936

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  27. Wu Z, Guo W, Yang L, He Q, Zhou S (2018) Juvenile hormone promotes locust fat body cell polyploidization and vitellogenesis by activating the transcription of Cdk6 and E2f1. Insect Biochem Mol Biol 102:1–10. https://doi.org/10.1016/j.ibmb.2018.09.002

    Article  CAS  PubMed  Google Scholar 

  28. Kayukawa T, Minakuchi C, Namiki T, Togawa T, Yoshiyama M, Kamimura M, Mita K, Imanishi S, Kiuchi M, Ishikawa Y, Shinoda T (2012) Transcriptional regulation of juvenile hormone-mediated induction of Kruppel homolog 1, a repressor of insect metamorphosis. Proc Natl Acad Sci USA 109(29):11729–11734. https://doi.org/10.1073/pnas.1204951109

    Article  PubMed  PubMed Central  Google Scholar 

  29. Lozano J, Belles X (2011) Conserved repressive function of Kruppel homolog 1 on insect metamorphosis in hemimetabolous and holometabolous species. Sci Rep 1:163. https://doi.org/10.1038/srep00163

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  30. Konopova B, Smykal V, Jindra M (2011) Common and distinct roles of juvenile hormone signaling genes in metamorphosis of holometabolous and hemimetabolous insects. PLoS One 6(12):e28728. https://doi.org/10.1371/journal.pone.0028728

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  31. Kayukawa T, Nagamine K, Ito Y, Nishita Y, Ishikawa Y, Shinoda T (2016) Kruppel homolog 1 inhibits insect metamorphosis via direct tanscriptional repression of Broad-complex, a pupal specifier gene. J Biol Chem 291(4):1751–1762. https://doi.org/10.1074/jbc.M115.686121

    Article  CAS  PubMed  Google Scholar 

  32. Urena E, Chafino S, Manjon C, Franch-Marro X, Martin D (2016) The occurrence of the holometabolous pupal stage requires the interaction between E93, Kruppel-homolog 1 and Broad-complex. PLoS Genet 12(5):e1006020. https://doi.org/10.1371/journal.pgen.1006020

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  33. Belles X, Santos CG (2014) The MEKRE93 (Methoprene tolerant-Kruppel homolog 1-E93) pathway in the regulation of insect metamorphosis, and the homology of the pupal stage. Insect Biochem Mol Biol 52:60–68. https://doi.org/10.1016/j.ibmb.2014.06.009

    Article  CAS  PubMed  Google Scholar 

  34. Gujar H, Palli SR (2016) Kruppel homolog 1 and E93 mediate Juvenile hormone regulation of metamorphosis in the common bed bug, Cimex lectularius. Sci Rep 6:26092. https://doi.org/10.1038/srep26092

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  35. Kayukawa T, Jouraku A, Ito Y, Shinoda T (2017) Molecular mechanism underlying juvenile hormone-mediated repression of precocious larval-adult metamorphosis. Proc Natl Acad Sci USA 114(5):1057–1062. https://doi.org/10.1073/pnas.1615423114

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  36. Zhang T, Song W, Li Z, Qian W, Wei L, Yang Y, Wang W, Zhou X, Meng M, Peng J, Xia Q, Perrimon N, Cheng D (2018) Kruppel homolog 1 represses insect ecdysone biosynthesis by directly inhibiting the transcription of steroidogenic enzymes. Proc Natl Acad Sci USA 115(15):3960–3965. https://doi.org/10.1073/pnas.1800435115

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  37. Liu S, Li K, Gao Y, Liu X, Chen W, Ge W, Feng Q, Palli SR, Li S (2018) Antagonistic actions of juvenile hormone and 20-hydroxyecdysone within the ring gland determine developmental transitions in Drosophila. Proc Natl Acad Sci USA 115(1):139–144. https://doi.org/10.1073/pnas.1716897115

    Article  CAS  PubMed  Google Scholar 

  38. Santos CG, Humann FC, Hartfelder K (2019) Juvenile hormone signaling in insect oogenesis. Curr Opin Insect Sci 31:43–48. https://doi.org/10.1016/j.cois.2018.07.010

    Article  PubMed  Google Scholar 

  39. Ojani R, Fu X, Ahmed T, Liu P, Zhu J (2018) Kruppel homologue 1 acts as a repressor and an activator in the transcriptional response to juvenile hormone in adult mosquitoes. Insect Mol Biol 27(2):268–278. https://doi.org/10.1111/imb.12370

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  40. Zhang WN, Ma L, Liu C, Chen L, Xiao HJ, Liang GM (2018) Dissecting the role of Kruppel homolog 1 in the metamorphosis and female reproduction of the cotton bollworm, Helicoverpa armigera. Insect Mol Biol. https://doi.org/10.1111/imb.12389

    Article  PubMed  PubMed Central  Google Scholar 

  41. Yue Y, Yang RL, Wang WP, Zhou QH, Chen EH, Yuan GR, Wang JJ, Dou W (2018) Involvement of Met and Kr-h1 in JH-Mediated Reproduction of Female Bactrocera dorsalis (Hendel). Front Physiol 9:482. https://doi.org/10.3389/fphys.2018.00482

    Article  PubMed  PubMed Central  Google Scholar 

  42. Tang Y, He H, Qu X, Cai Y, Ding W, Qiu L, Li Y (2019) RNA interference-mediated knockdown of the transcription factor Kruppel homolog 1 suppresses vitellogenesis in Chilo suppressalis. Insect Mol Biol. https://doi.org/10.1111/imb.12617

    Article  PubMed  Google Scholar 

  43. Song J, Wu Z, Wang Z, Deng S, Zhou S (2014) Kruppel-homolog 1 mediates juvenile hormone action to promote vitellogenesis and oocyte maturation in the migratory locust. Insect Biochem Mol Biol 52:94–101. https://doi.org/10.1016/j.ibmb.2014.07.001

    Article  CAS  PubMed  Google Scholar 

  44. Wang Z, Yang L, Song J, Kang L, Zhou S (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. https://doi.org/10.1016/j.ibmb.2017.01.009

    Article  CAS  PubMed  Google Scholar 

  45. Shin SW, Zou Z, Saha TT, Raikhel AS (2012) bHLH-PAS heterodimer of methoprene-tolerant and Cycle mediates circadian expression of juvenile hormone-induced mosquito genes. Proc Natl Acad Sci USA 109(41):16576–16581. https://doi.org/10.1073/pnas.1214209109

    Article  PubMed  PubMed Central  Google Scholar 

  46. Lucas KJ, Zhao B, Liu S, Raikhel AS (2015) Regulation of physiological processes by microRNAs in insects. Curr Opin Insect Sci 11:1–7. https://doi.org/10.1016/j.cois.2015.06.004

    Article  PubMed  PubMed Central  Google Scholar 

  47. Belles X (2017) MicroRNAs and the evolution of insect metamorphosis. Annu Rev Entomol 62:111–125. https://doi.org/10.1146/annurev-ento-031616-034925

    Article  CAS  PubMed  Google Scholar 

  48. Liu P, Fu X, Zhu J (2018) Juvenile hormone-regulated alternative splicing of the taiman gene primes the ecdysteroid response in adult mosquitoes. Proc Natl Acad Sci USA 115(33):E7738–E7747. https://doi.org/10.1073/pnas.1808146115

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  49. Lozano J, Kayukawa T, Shinoda T, Belles X (2014) A role for Taiman in insect metamorphosis. PLoS Genet 10(10):e1004769. https://doi.org/10.1371/journal.pgen.1004769

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  50. Wu Y, Cheng T, Liu C, Liu D, Zhang Q, Long R, Zhao P, Xia Q (2016) Systematic identification and characterization of long non-coding RNAs in the Silkworm. Bombyx mori. PLoS One 11(1):e0147147. https://doi.org/10.1371/journal.pone.0147147

    Article  PubMed  Google Scholar 

  51. Xiao H, Yuan Z, Guo D, Hou B, Yin C, Zhang W, Li F (2015) Genome-wide identification of long noncoding RNA genes and their potential association with fecundity and virulence in rice brown planthopper, Nilaparvata lugens. BMC Genom 16:749. https://doi.org/10.1186/s12864-015-1953-y

    Article  CAS  Google Scholar 

  52. Zhu B, Xu M, Shi H, Gao X, Liang P (2017) Genome-wide identification of lncRNAs associated with chlorantraniliprole resistance in diamondback moth Plutella xylostella (L.). BMC Genomics 18(1):380. https://doi.org/10.1186/s12864-017-3748-9

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  53. Ashwal-Fluss R, Meyer M, Pamudurti NR, Ivanov A, Bartok O, Hanan M, Evantal N, Memczak S, Rajewsky N, Kadener S (2014) circRNA biogenesis competes with pre-mRNA splicing. Mol Cell 56(1):55–66. https://doi.org/10.1016/j.molcel.2014.08.019

    Article  CAS  PubMed  Google Scholar 

  54. Gan H, Feng T, Wu Y, Liu C, Xia Q, Cheng T (2017) Identification of circular RNA in the Bombyx mori silk gland. Insect Biochem Mol Biol 89:97–106. https://doi.org/10.1016/j.ibmb.2017.09.003

    Article  CAS  PubMed  Google Scholar 

  55. Tholken C, Thamm M, Erbacher C, Lechner M (2019) Sequence and structural properties of circular RNAs in the brain of nurse and forager honeybees (Apis mellifera). BMC Genomics 20(1):88. https://doi.org/10.1186/s12864-018-5402-6

    Article  PubMed  PubMed Central  Google Scholar 

  56. Li K, Tian Y, Yuan Y, Fan X, Yang M, He Z, Yang D (2019) Insights into the functions of LncRNAs in Drosophila. Int J Mol Sci. https://doi.org/10.3390/ijms20184646

    Article  PubMed  PubMed Central  Google Scholar 

  57. Reinhart BJ, Slack FJ, Basson M, Pasquinelli AE, Bettinger JC, Rougvie AE, Horvitz HR, Ruvkun G (2000) The 21-nucleotide let-7 RNA regulates developmental timing in Caenorhabditis elegans. Nature 403(6772):901–906. https://doi.org/10.1038/35002607

    Article  CAS  PubMed  Google Scholar 

  58. Vella MC, Choi EY, Lin SY, Reinert K, Slack FJ (2004) The C. elegans microRNA let-7 binds to imperfect let-7 complementary sites from the lin-41 3′UTR. Genes Dev 18(2):132–137. https://doi.org/10.1101/gad.1165404

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  59. Chi SW, Zang JB, Mele A, Darnell RB (2009) Argonaute HITS-CLIP decodes microRNA-mRNA interaction maps. Nature 460(7254):479–486. https://doi.org/10.1038/nature08170

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  60. Hafner M, Landthaler M, Burger L, Khorshid M, Hausser J, Berninger P, Rothballer A, Ascano M Jr, Jungkamp AC, Munschauer M, Ulrich A, Wardle GS, Dewell S, Zavolan M, Tuschl T (2010) Transcriptome-wide identification of RNA-binding protein and microRNA target sites by PAR-CLIP. Cell 141(1):129–141. https://doi.org/10.1016/j.cell.2010.03.009

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  61. Tay Y, Zhang J, Thomson AM, Lim B, Rigoutsos I (2008) MicroRNAs to Nanog, Oct4 and Sox2 coding regions modulate embryonic stem cell differentiation. Nature 455(7216):1124–1128. https://doi.org/10.1038/nature07299

    Article  CAS  PubMed  Google Scholar 

  62. Zhou X, Duan X, Qian J, Li F (2009) Abundant conserved microRNA target sites in the 5′-untranslated region and coding sequence. Genetica 137(2):159–164. https://doi.org/10.1007/s10709-009-9378-7

    Article  CAS  PubMed  Google Scholar 

  63. Yang M, Wei Y, Jiang F, Wang Y, Guo X, He J, Kang L (2014) MicroRNA-133 inhibits behavioral aggregation by controlling dopamine synthesis in locusts. PLoS Genet 10(2):e1004206. https://doi.org/10.1371/journal.pgen.1004206

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  64. He J, Chen Q, Wei Y, Jiang F, Yang M, Hao S, Guo X, Chen D, Kang L (2016) MicroRNA-276 promotes egg-hatching synchrony by up-regulating brm in locusts. Proc Natl Acad Sci USA 113(3):584–589. https://doi.org/10.1073/pnas.1521098113

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  65. Vasudevan S, Tong Y, Steitz JA (2007) Switching from repression to activation: microRNAs can up-regulate translation. Science 318(5858):1931–1934. https://doi.org/10.1126/science.1149460

    Article  CAS  PubMed  Google Scholar 

  66. Azzam G, Smibert P, Lai EC, Liu JL (2012) Drosophila Argonaute 1 and its miRNA biogenesis partners are required for oocyte formation and germline cell division. Dev Biol 365(2):384–394. https://doi.org/10.1016/j.ydbio.2012.03.005

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  67. Tanaka ED, Piulachs MD (2012) Dicer-1 is a key enzyme in the regulation of oogenesis in panoistic ovaries. Biol Cell 104(8):452–461. https://doi.org/10.1111/boc.201100044

    Article  CAS  PubMed  Google Scholar 

  68. Nakahara K, Kim K, Sciulli C, Dowd SR, Minden JS, Carthew RW (2005) Targets of microRNA regulation in the Drosophila oocyte proteome. Proc Natl Acad Sci USA 102(34):12023–12028. https://doi.org/10.1073/pnas.0500053102

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  69. Wu W, Xiong W, Li C, Zhai M, Li Y, Ma F, Li B (2017) MicroRNA-dependent regulation of metamorphosis and identification of microRNAs in the red flour beetle, Tribolium castaneum. Genomics 109(5–6):362–373. https://doi.org/10.1016/j.ygeno.2017.06.001

    Article  CAS  PubMed  Google Scholar 

  70. Rahimpour H, Moharramipour S, Asgari S, Mehrabadi M (2019) The microRNA pathway core genes are differentially expressed during the development of Helicoverpa armigera and contribute in the insect’s development. Insect Biochem Mol Biol 110:121–127. https://doi.org/10.1016/j.ibmb.2019.05.005

    Article  CAS  PubMed  Google Scholar 

  71. Gomez-Orte E, Belles X (2009) MicroRNA-dependent metamorphosis in hemimetabolan insects. Proc Natl Acad Sci USA 106(51):21678–21682. https://doi.org/10.1073/pnas.0907391106

    Article  PubMed  PubMed Central  Google Scholar 

  72. Song J, Guo W, Jiang F, Kang L, Zhou S (2013) Argonaute 1 is indispensable for juvenile hormone mediated oogenesis in the migratory locust, Locusta migratoria. Insect Biochem Mol Biol 43(9):879–887. https://doi.org/10.1016/j.ibmb.2013.06.004

    Article  CAS  PubMed  Google Scholar 

  73. Wang YL, Yang ML, Jiang F, Zhang JZ, Kang L (2013) MicroRNA-dependent development revealed by RNA interference-mediated gene silencing of LmDicer1 in the migratory locust. Insect Sci 20(1):53–60. https://doi.org/10.1111/j.1744-7917.2012.01542.x

    Article  CAS  PubMed  Google Scholar 

  74. Zhu L, Liao SE, Fukunaga R (2019) Drosophila Regnase-1 RNase is required for mRNA and miRNA profile remodelling during larva-to-adult metamorphosis. RNA Biol 16(10):1386–1400. https://doi.org/10.1080/15476286.2019.1630799

    Article  PubMed  PubMed Central  Google Scholar 

  75. Shcherbata HR (2019) miRNA functions in stem cells and their niches: lessons from the Drosophila ovary. Curr Opin Insect Sci 31:29–36. https://doi.org/10.1016/j.cois.2018.07.006

    Article  PubMed  Google Scholar 

  76. Chawla G, Sokol NS (2011) MicroRNAs in Drosophila development. Int Rev Cell Mol Biol 286:1–65. https://doi.org/10.1016/b978-0-12-385859-7.00001-x

    Article  CAS  PubMed  Google Scholar 

  77. Roush S, Slack FJ (2008) The let-7 family of microRNAs. Trends Cell Biol 18(10):505–516. https://doi.org/10.1016/j.tcb.2008.07.007

    Article  CAS  PubMed  Google Scholar 

  78. Sokol NS, Xu P, Jan YN, Ambros V (2008) Drosophila let-7 microRNA is required for remodeling of the neuromusculature during metamorphosis. Genes Dev 22(12):1591–1596. https://doi.org/10.1101/gad.1671708

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  79. Tennessen JM, Thummel CS (2008) Developmental timing: let-7 function conserved through evolution. Curr Biol 18(16):R707–R708. https://doi.org/10.1016/j.cub.2008.07.013

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  80. Caygill EE, Johnston LA (2008) Temporal regulation of metamorphic processes in Drosophila by the let-7 and miR-125 heterochronic microRNAs. Curr Biol 18(13):943–950. https://doi.org/10.1016/j.cub.2008.06.020

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  81. Wu YC, Chen CH, Mercer A, Sokol NS (2012) Let-7-complex microRNAs regulate the temporal identity of Drosophila mushroom body neurons via chinmo. Dev Cell 23(1):202–209. https://doi.org/10.1016/j.devcel.2012.05.013

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  82. Jiang S (2019) A regulator of metabolic reprogramming: microRNA let-7. Transl Oncol 12(7):1005–1013. https://doi.org/10.1016/j.tranon.2019.04.013

    Article  PubMed  PubMed Central  Google Scholar 

  83. Kucherenko MM, Barth J, Fiala A, Shcherbata HR (2012) Steroid-induced microRNA let-7 acts as a spatio-temporal code for neuronal cell fate in the developing Drosophila brain. EMBO J 31(24):4511–4523. https://doi.org/10.1038/emboj.2012.298

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  84. Ling L, Ge X, Li Z, Zeng B, Xu J, Aslam AF, Song Q, Shang P, Huang Y, Tan A (2014) MicroRNA Let-7 regulates molting and metamorphosis in the silkworm, Bombyx mori. Insect Biochem Mol Biol 53:13–21. https://doi.org/10.1016/j.ibmb.2014.06.011

    Article  CAS  PubMed  Google Scholar 

  85. Peng W, Zheng WW, Tariq K, Yu SN, Zhang HY (2019) MicroRNA Let-7 targets the ecdysone signaling pathway E75 gene to control larval-pupal development in Bactrocera dorsalis. Insect Sci 26(2):229–239. https://doi.org/10.1111/1744-7917.12542

    Article  CAS  PubMed  Google Scholar 

  86. Rubio M, de Horna A, Belles X (2012) MicroRNAs in metamorphic and non-metamorphic transitions in hemimetabolan insect metamorphosis. BMC Genomics 13:386. https://doi.org/10.1186/1471-2164-13-386

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  87. Rubio M, Belles X (2013) Subtle roles of microRNAs let-7, miR-100 and miR-125 on wing morphogenesis in hemimetabolan metamorphosis. J Insect Physiol 59(11):1089–1094. https://doi.org/10.1016/j.jinsphys.2013.09.003

    Article  CAS  PubMed  Google Scholar 

  88. Song J, Li W, Zhao H, Gao L, Fan Y, Zhou S (2018) The microRNAs let-7 and miR-278 regulate insect metamorphosis and oogenesis by targeting the juvenile hormone early-response gene Kruppel-homolog 1. Development. https://doi.org/10.1242/dev.170670

    Article  PubMed  PubMed Central  Google Scholar 

  89. Marco A, Hooks K, Griffiths-Jones S (2012) Evolution and function of the extended miR-2 microRNA family. RNA Biol 9(3):242–248. https://doi.org/10.4161/rna.19160

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  90. Ling L, Ge X, Li Z, Zeng B, Xu J, Chen X, Shang P, James AA, Huang Y, Tan A (2015) MiR-2 family targets awd and fng to regulate wing morphogenesis in Bombyx mori. RNA Biol 12(7):742–748. https://doi.org/10.1080/15476286.2015.1048957

    Article  PubMed  PubMed Central  Google Scholar 

  91. Lozano J, Montanez R, Belles X (2015) MiR-2 family regulates insect metamorphosis by controlling the juvenile hormone signaling pathway. Proc Natl Acad Sci USA 112(12):3740–3745. https://doi.org/10.1073/pnas.1418522112

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  92. Hyun S, Lee JH, Jin H, Nam J, Namkoong B, Lee G, Chung J, Kim VN (2009) Conserved MicroRNA miR-8/miR-200 and its target USH/FOG2 control growth by regulating PI3 K. Cell 139(6):1096–1108. https://doi.org/10.1016/j.cell.2009.11.020

    Article  CAS  PubMed  Google Scholar 

  93. Jin H, Kim VN, Hyun S (2012) Conserved microRNA miR-8 controls body size in response to steroid signaling in Drosophila. Genes Dev 26(13):1427–1432. https://doi.org/10.1101/gad.192872.112

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  94. Kennell JA, Cadigan KM, Shakhmantsir I, Waldron EJ (2012) The microRNA miR-8 is a positive regulator of pigmentation and eclosion in Drosophila. Dev Dyn 241(1):161–168. https://doi.org/10.1002/dvdy.23705

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  95. Liu Z, Ling L, Xu J, Zeng B, Huang Y, Shang P, Tan A (2018) MicroRNA-14 regulates larval development time in Bombyx mori. Insect Biochem Mol Biol 93:57–65. https://doi.org/10.1016/j.ibmb.2017.12.009

    Article  CAS  PubMed  Google Scholar 

  96. He K, Xiao H, Sun Y, Situ G, Xi Y, Li F (2019) microRNA-14 as an efficient suppressor to switch off ecdysone production after ecdysis in insects. RNA Biol 16(9):1313–1325. https://doi.org/10.1080/15476286.2019.1629768

    Article  PubMed  PubMed Central  Google Scholar 

  97. He K, Xiao H, Sun Y, Ding S, Situ G, Li F (2019) Transgenic microRNA-14 rice shows high resistance to rice stem borer. Plant Biotechnol J 17(2):461–471. https://doi.org/10.1111/pbi.12990

    Article  CAS  PubMed  Google Scholar 

  98. Chen J, Liang Z, Liang Y, Pang R, Zhang W (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(9):839–848. https://doi.org/10.1016/j.ibmb.2013.06.002

    Article  CAS  PubMed  Google Scholar 

  99. Yang M, Wang Y, Jiang F, Song T, Wang H, Liu Q, Zhang J, Zhang J, Kang L (2016) miR-71 and miR-263 jointly regulate target genes Chitin synthase and Chitinase to control locust molting. PLoS Genet 12(8):e1006257. https://doi.org/10.1371/journal.pgen.1006257

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  100. Puthiyakunnon S, Yao Y, Li Y, Gu J, Peng H, Chen X (2013) Functional characterization of three MicroRNAs of the Asian tiger mosquito, Aedes albopictus. Parasites Vectors 6(1):230. https://doi.org/10.1186/1756-3305-6-230

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  101. Zhang X, Zheng Y, Jagadeeswaran G, Ren R, Sunkar R, Jiang H (2012) Identification and developmental profiling of conserved and novel microRNAs in Manduca sexta. Insect Biochem Mol Biol 42(6):381–395. https://doi.org/10.1016/j.ibmb.2012.01.006

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  102. Chen J, Li TC, Pang R, Yue XZ, Hu J, Zhang WQ (2018) Genome-wide screening and functional analysis reveal that the specific microRNA nlu-miR-173 regulates molting by targeting Ftz-F1 in Nilaparvata lugens. Front Physiol 9:1854. https://doi.org/10.3389/fphys.2018.01854

    Article  PubMed  PubMed Central  Google Scholar 

  103. Chen J, Li T, Pang R (2019) miR-2703 regulates the chitin biosynthesis pathway by targeting chitin synthase 1a in Nilaparvata lugens. Insect Mol Biol. https://doi.org/10.1111/imb.12606

    Article  PubMed  Google Scholar 

  104. Zhang YL, Huang QX, Yin GH, Lee S, Jia RZ, Liu ZX, Yu NT, Pennerman KK, Chen X, Guo AP (2015) Identification of microRNAs by small RNA deep sequencing for synthetic microRNA mimics to control Spodoptera exigua. Gene 557(2):215–221. https://doi.org/10.1016/j.gene.2014.12.038

    Article  CAS  PubMed  Google Scholar 

  105. Wang ZZ, Ye XQ, Shi M, Li F, Wang ZH, Zhou YN, Gu QJ, Wu XT, Yin CL, Guo DH, Hu RM, Hu NN, Chen T, Zheng BY, Zou JN, Zhan LQ, Wei SJ, Wang YP, Huang JH, Fang XD, Strand MR, Chen XX (2018) Parasitic insect-derived miRNAs modulate host development. Nat Commun 9(1):2205. https://doi.org/10.1038/s41467-018-04504-1

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  106. Chawla G, Sokol NS (2012) Hormonal activation of let-7-C microRNAs via EcR is required for adult Drosophila melanogaster morphology and function. Development 139(10):1788–1797. https://doi.org/10.1242/dev.077743

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  107. Varghese J, Cohen SM (2007) microRNA miR-14 acts to modulate a positive autoregulatory loop controlling steroid hormone signaling in Drosophila. Genes Dev 21(18):2277–2282. https://doi.org/10.1101/gad.439807

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  108. Verma P, Cohen SM (2015) miR-965 controls cell proliferation and migration during tissue morphogenesis in the Drosophila abdomen. eLife. https://doi.org/10.7554/elife.07389

    Article  PubMed  PubMed Central  Google Scholar 

  109. Jiang J, Ge X, Li Z, Wang Y, Song Q, Stanley DW, Tan A, Huang Y (2013) MicroRNA-281 regulates the expression of ecdysone receptor (EcR) isoform B in the silkworm, Bombyx mori. Insect Biochem Mol Biol 43(8):692–700. https://doi.org/10.1016/j.ibmb.2013.05.002

    Article  CAS  PubMed  Google Scholar 

  110. Lim DH, Lee S, Han JY, Choi MS, Hong JS, Seong Y, Kwon YS, Lee YS (2018) Ecdysone-responsive microRNA-252-5p controls the cell cycle by targeting Abi in Drosophila. FASEB J 32(8):4519–4533. https://doi.org/10.1096/fj.201701185RR

    Article  CAS  PubMed  Google Scholar 

  111. Garbuzov A, Tatar M (2010) Hormonal regulation of Drosophila microRNA let-7 and miR-125 that target innate immunity. Fly 4(4):306–311. https://doi.org/10.4161/fly.4.4.13008

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  112. Qu Z, Bendena WG, Nong W, Siggens KW, Noriega FG, Kai ZP, Zang YY, Koon AC, Chan HYE, Chan TF, Chu KH, Lam HM, Akam M, Tobe SS, Lam Hui JH (2017) MicroRNAs regulate the sesquiterpenoid hormonal pathway in Drosophila and other arthropods. Proc Biol Sci. https://doi.org/10.1098/rspb.2017.1827

    Article  PubMed  PubMed Central  Google Scholar 

  113. Boulan L, Martin D, Milan M (2013) bantam miRNA promotes systemic growth by connecting insulin signaling and ecdysone production. Curr Biol 23(6):473–478. https://doi.org/10.1016/j.cub.2013.01.072

    Article  CAS  PubMed  Google Scholar 

  114. He K, Sun Y, Xiao H, Ge C, Li F, Han Z (2017) Multiple miRNAs jointly regulate the biosynthesis of ecdysteroid in the holometabolous insects, Chilo suppressalis. RNA 23(12):1817–1833. https://doi.org/10.1261/rna.061408.117

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  115. Qu Z, Bendena WG, Tobe SS, Hui JHL (2018) Juvenile hormone and sesquiterpenoids in arthropods: biosynthesis, signaling, and role of MicroRNA. J Steroid Biochem Mol Biol 184:69–76. https://doi.org/10.1016/j.jsbmb.2018.01.013

    Article  CAS  PubMed  Google Scholar 

  116. Nouzova M, Etebari K, Noriega FG, Asgari S (2018) A comparative analysis of corpora allata-corpora cardiaca microRNA repertoires revealed significant changes during mosquito metamorphosis. Insect Biochem Mol Biol 96:10–18. https://doi.org/10.1016/j.ibmb.2018.03.007

    Article  CAS  PubMed  Google Scholar 

  117. Raikhel AS, Dhadialla TS (1992) Accumulation of yolk proteins in insect oocytes. Annu Rev Entomol 37:217–251. https://doi.org/10.1146/annurev.en.37.010192.001245

    Article  CAS  PubMed  Google Scholar 

  118. Asgari S (2013) MicroRNA functions in insects. Insect Biochem Mol Biol 43(4):388–397. https://doi.org/10.1016/j.ibmb.2012.10.005

    Article  CAS  PubMed  Google Scholar 

  119. Baumer D, Strohlein NM, Schoppmeier M (2012) Opposing effects of Notch-signaling in maintaining the proliferative state of follicle cells in the telotrophic ovary of the beetle Tribolium. Front Zool 9(1):15. https://doi.org/10.1186/1742-9994-9-15

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  120. Irles P, Elshaer N, Piulachs MD (2016) The Notch pathway regulates both the proliferation and differentiation of follicular cells in the panoistic ovary of Blattella germanica. Open Biol 6(1):150197. https://doi.org/10.1098/rsob.150197

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  121. Xu J, Gridley T (2012) Notch signaling during Oogenesis in Drosophila melanogaster. Genet Res Int 2012:648207. https://doi.org/10.1155/2012/648207

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  122. Song J, Li W, Zhao H, Zhou S (2019) Clustered miR-2, miR-13a, miR-13b and miR-71 coordinately target Notch gene to regulate oogenesis of the migratory locust Locusta migratoria. Insect Biochem Mol Biol 106:39–46. https://doi.org/10.1016/j.ibmb.2018.11.004

    Article  CAS  PubMed  Google Scholar 

  123. Yang L, Chen D, Duan R, Xia L, Wang J, Qurashi A, Jin P, Chen D (2007) Argonaute 1 regulates the fate of germline stem cells in Drosophila. Development 134(23):4265–4272. https://doi.org/10.1242/dev.009159

    Article  CAS  PubMed  Google Scholar 

  124. Jin Z, Xie T (2007) Dcr-1 maintains Drosophila ovarian stem cells. Curr Biol 17(6):539–544. https://doi.org/10.1016/j.cub.2007.01.050

    Article  CAS  PubMed  Google Scholar 

  125. Wang C, Feng T, Wan Q, Kong Y, Yuan L (2014) miR-124 controls Drosophila behavior and is required for neural development. Int J Dev Neurosci 38:105–112. https://doi.org/10.1016/j.ijdevneu.2014.08.006

    Article  CAS  PubMed  Google Scholar 

  126. Garaulet DL, Castellanos MC, Bejarano F, Sanfilippo P, Tyler DM, Allan DW, Sanchez-Herrero E, Lai EC (2014) Homeotic function of Drosophila Bithorax-complex miRNAs mediates fertility by restricting multiple Hox genes and TALE cofactors in the CNS. Dev Cell 29(6):635–648. https://doi.org/10.1016/j.devcel.2014.04.023

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  127. Yatsenko AS, Shcherbata HR (2018) Stereotypical architecture of the stem cell niche is spatiotemporally established by miR-125-dependent coordination of Notch and steroid signaling. Development. https://doi.org/10.1242/dev.159178

    Article  PubMed  PubMed Central  Google Scholar 

  128. Huang YC, Smith L, Poulton J, Deng WM (2013) The microRNA miR-7 regulates Tramtrack69 in a developmental switch in Drosophila follicle cells. Development 140(4):897–905. https://doi.org/10.1242/dev.080192

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  129. Ge W, Deng Q, Guo T, Hong X, Kugler JM, Yang X, Cohen SM (2015) Regulation of pattern formation and gene amplification during Drosophila oogenesis by the miR-318 microRNA. Genetics 200(1):255–265. https://doi.org/10.1534/genetics.115.174748

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  130. Bryant B, Macdonald W, Raikhel AS (2010) microRNA miR-275 is indispensable for blood digestion and egg development in the mosquito Aedes aegypti. Proc Natl Acad Sci USA 107(52):22391–22398. https://doi.org/10.1073/pnas.1016230107

    Article  PubMed  PubMed Central  Google Scholar 

  131. Ling L, Kokoza VA, Zhang C, Aksoy E, Raikhel AS (2017) MicroRNA-277 targets insulin-like peptides 7 and 8 to control lipid metabolism and reproduction in Aedes aegypti mosquitoes. Proc Natl Acad Sci USA 114(38):E8017–E8024. https://doi.org/10.1073/pnas.1710970114

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  132. Liu S, Lucas KJ, Roy S, Ha J, Raikhel AS (2014) Mosquito-specific microRNA-1174 targets serine hydroxymethyltransferase to control key functions in the gut. Proc Natl Acad Sci USA 111(40):14460–14465. https://doi.org/10.1073/pnas.1416278111

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  133. Lucas KJ, Zhao B, Roy S, Gervaise AL, Raikhel AS (2015) Mosquito-specific microRNA-1890 targets the juvenile hormone-regulated serine protease JHA15 in the female mosquito gut. RNA Biol 12(12):1383–1390. https://doi.org/10.1080/15476286.2015.1101525

    Article  PubMed  PubMed Central  Google Scholar 

  134. Lucas KJ, Roy S, Ha J, Gervaise AL, Kokoza VA, Raikhel AS (2015) MicroRNA-8 targets the Wingless signaling pathway in the female mosquito fat body to regulate reproductive processes. Proc Natl Acad Sci USA 112(5):1440–1445. https://doi.org/10.1073/pnas.1424408112

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  135. Bian G, Raikhel AS, Zhu J (2008) Characterization of a juvenile hormone-regulated chymotrypsin-like serine protease gene in Aedes aegypti mosquito. Insect Biochem Mol Biol 38(2):190–200. https://doi.org/10.1016/j.ibmb.2007.10.008

    Article  CAS  PubMed  Google Scholar 

  136. Fu X, Dimopoulos G, Zhu J (2017) Association of microRNAs with Argonaute proteins in the malaria mosquito Anopheles gambiae after blood ingestion. Sci Rep 7(1):6493. https://doi.org/10.1038/s41598-017-07013-1

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  137. Zhang Y, Zhao B, Roy S, Saha TT, Kokoza VA, Li M, Raikhel AS (2016) microRNA-309 targets the Homeobox gene SIX4 and controls ovarian development in the mosquito Aedes aegypti. Proc Natl Acad Sci USA 113(33):E4828–E4836. https://doi.org/10.1073/pnas.1609792113

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  138. Zhang X, Aksoy E, Girke T, Raikhel AS, Karginov FV (2017) Transcriptome-wide microRNA and target dynamics in the fat body during the gonadotrophic cycle of Aedes aegypti. Proc Natl Acad Sci USA 114(10):E1895–E1903. https://doi.org/10.1073/pnas.1701474114

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  139. Jayachandran B, Hussain M, Asgari S (2013) An insect trypsin-like serine protease as a target of microRNA: utilization of microRNA mimics and inhibitors by oral feeding. Insect Biochem Mol Biol 43(4):398–406. https://doi.org/10.1016/j.ibmb.2012.10.004

    Article  CAS  PubMed  Google Scholar 

  140. Zhang X, Lu K, Zhou Q (2013) Dicer1 is crucial for the oocyte maturation of telotrophic ovary in Nilaparvata lugens (STAL) (Hemiptera: Geometroidea). Arch Insect Biochem Physiol 84(4):194–208. https://doi.org/10.1002/arch.21136

    Article  CAS  PubMed  Google Scholar 

  141. Fu X, Li T, Chen J, Dong Y, Qiu J, Kang K, Zhang W (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. https://doi.org/10.1016/j.jinsphys.2015.11.003

    Article  CAS  PubMed  Google Scholar 

  142. Blencowe BJ (2006) Alternative splicing: new insights from global analyses. Cell 126(1):37–47. https://doi.org/10.1016/j.cell.2006.06.023

    Article  CAS  PubMed  Google Scholar 

  143. Wang Z, Burge CB (2008) Splicing regulation: from a parts list of regulatory elements to an integrated splicing code. RNA 14(5):802–813. https://doi.org/10.1261/rna.876308

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  144. Talbot WS, Swyryd EA, Hogness DS (1993) Drosophila tissues with different metamorphic responses to ecdysone express different ecdysone receptor isoforms. Cell 73(7):1323–1337. https://doi.org/10.1016/0092-8674(93)90359-x

    Article  CAS  PubMed  Google Scholar 

  145. Wang SF, Li C, Zhu J, Miura K, Miksicek RJ, Raikhel AS (2000) Differential expression and regulation by 20-hydroxyecdysone of mosquito ultraspiracle isoforms. Dev Biol 218(1):99–113. https://doi.org/10.1006/dbio.1999.9575

    Article  CAS  PubMed  Google Scholar 

  146. Huang LX, Gong YJ, Gu J, Zeng BJ, Huang LH, Feng QL (2015) Expression, subcellular localization and protein-protein interaction of four isoforms of EcR/USP in the common cutworm. Insect Sci 22(1):95–105. https://doi.org/10.1111/1744-7917.12101

    Article  CAS  PubMed  Google Scholar 

  147. Xu QY, Deng P, Zhang Q, Li A, Fu KY, Guo WC, Li GQ (2019) Ecdysone receptor isoforms play distinct roles in larval-pupal-adult transition in Leptinotarsa decemlineata. Insect Sci. https://doi.org/10.1111/1744-7917.12662

    Article  PubMed  PubMed Central  Google Scholar 

  148. Tan A, Palli SR (2008) Edysone receptor isoforms play distinct roles in controlling molting and metamorphosis in the red flour beetle, Tribolium castaneum. Mol Cell Endocrinol 291(1):42–49. https://doi.org/10.1016/j.mce.2008.05.006

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  149. Watanabe T, Takeuchi H, Kubo T (2010) Structural diversity and evolution of the N-terminal isoform-specific region of ecdysone receptor-A and-B1 isoforms in insects. BMC Evol Biol 10:17. https://doi.org/10.1186/1471-2148-10-40

    Article  CAS  Google Scholar 

  150. Tan YA, Xiao LB, Zhao J, Xiao YF, Sun Y, Bai LX (2015) Ecdysone receptor isoform-B mediates soluble trehalase expression to regulate growth and development in the mirid bug, Apolygus lucorum (Meyer-Dur). Insect Mol Biol 24(6):611–623. https://doi.org/10.1111/imb.12185

    Article  CAS  PubMed  Google Scholar 

  151. Chen CH, Pan J, Di YQ, Liu W, Hou L, Wang JX, Zhao XF (2017) Protein kinase C delta phosphorylates ecdysone receptor B1 to promote gene expression and apoptosis under 20-hydroxyecdysone regulation. Proc Natl Acad Sci USA 114(34):E7121–E7130. https://doi.org/10.1073/pnas.1704999114

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  152. Lenaerts C, Van Wielendaele P, Peeters P, Vanden Broeck J, Marchal E (2016) Ecdysteroid signalling components in metamorphosis and development of the desert locust, Schistocerca gregaria. Insect Biochem Mol Biol 75:10–23. https://doi.org/10.1016/j.ibmb.2016.05.003

    Article  CAS  PubMed  Google Scholar 

  153. Tan A, Palli SR (2008) Ecdysone [corrected] receptor isoforms play distinct roles in controlling molting and metamorphosis in the red flour beetle, Tribolium castaneum. Mol Cell Endocrinol 291(1–2):42–49. https://doi.org/10.1016/j.mce.2008.05.006

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  154. Hult EF, Huang J, Marchal E, Lam J, Tobe SS (2015) RXR/USP and EcR are critical for the regulation of reproduction and the control of JH biosynthesis in Diploptera punctata. J Insect Physiol 80:48–60. https://doi.org/10.1016/j.jinsphys.2015.04.006

    Article  CAS  PubMed  Google Scholar 

  155. Maestro O, Cruz J, Pascual N, Martin D, Belles X (2005) Differential expression of two RXR/ultraspiracle isoforms during the life cycle of the hemimetabolous insect Blattella germanica (Dictyoptera, Blattellidae). Mol Cell Endocrinol 238(1–2):27–37. https://doi.org/10.1016/j.mce.2005.04.004

    Article  CAS  PubMed  Google Scholar 

  156. Jindra M, Huang JY, Malone F, Asahina M, Riddiford LM (1997) Identification and mRNA developmental profiles of two ultraspiracle isoforms in the epidermis and wings of Manduca sexta. Insect Mol Biol 6(1):41–53

    Article  CAS  PubMed  Google Scholar 

  157. Kapitskaya M, Wang S, Cress DE, Dhadialla TS, Raikhel AS (1996) The mosquito ultraspiracle homologue, a partner of ecdysteroid receptor heterodimer: cloning and characterization of isoforms expressed during vitellogenesis. Mol Cell Endocrinol 121(2):119–132. https://doi.org/10.1016/0303-7207(96)03847-6

    Article  CAS  PubMed  Google Scholar 

  158. Lan Q, Hiruma K, Hu X, Jindra M, Riddiford LM (1999) Activation of a delayed-early gene encoding MHR3 by the ecdysone receptor heterodimer EcR-B1-USP-1 but not by EcR-B1-USP-2. Mol Cell Biol 19(7):4897–4906

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  159. Parthasarathy R, Palli SR (2007) Stage- and cell-specific expression of ecdysone receptors and ecdysone-induced transcription factors during midgut remodeling in the yellow fever mosquito, Aedes aegypti. J Insect Physiol 53(3):216–229. https://doi.org/10.1016/j.jinsphys.2006.09.009

    Article  CAS  PubMed  Google Scholar 

  160. Cheng D, Meng M, Peng J, Qian W, Kang L, Xia Q (2014) Genome-wide comparison of genes involved in the biosynthesis, metabolism, and signaling of juvenile hormone between silkworm and other insects. Genet Mol Biol 37(2):444–459

    Article  PubMed  PubMed Central  Google Scholar 

  161. Kayukawa T, Shinoda T (2015) Functional characterization of two paralogous JH receptors, methoprene-tolerant 1 and 2, in the silkworm, Bombyx mori (Lepidoptera: Bombycidae). Appl Entomol Zool. https://doi.org/10.1007/s13355-015-0345-8

    Article  Google Scholar 

  162. Jouraku A, Yamamoto K, Kuwazaki S, Urio M, Suetsugu Y, Narukawa J, Miyamoto K, Kurita K, Kanamori H, Katayose Y, Matsumoto T, Noda H (2013) KONAGAbase: a genomic and transcriptomic database for the diamondback moth, Plutella xylostella. BMC Genomics 14:464. https://doi.org/10.1186/1471-2164-14-464

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  163. Baumann A, Fujiwara Y, Wilson TG (2010) Evolutionary divergence of the paralogs Methoprene tolerant (Met) and germ cell expressed (gce) within the genus Drosophila. J Insect Physiol 56(10):1445–1455

    Article  CAS  PubMed  Google Scholar 

  164. Abdou MA, He Q, Wen D, Zyaan O, Wang J, Xu J, Baumann AA, Joseph J, Wilson TG, Li S, Wang J (2011) Drosophila Met and Gce are partially redundant in transducing juvenile hormone action. Insect Biochem Mol Biol 41(12):938–945. https://doi.org/10.1016/j.ibmb.2011.09.003

    Article  CAS  PubMed  Google Scholar 

  165. Dasgupta S, O’Malley BW (2014) Transcriptional coregulators: emerging roles of SRC family of coactivators in disease pathology. J Mol Endocrinol 53(2):R47–R59. https://doi.org/10.1530/JME-14-0080

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  166. Xu J, Wu RC, O’Malley BW (2009) Normal and cancer-related functions of the p160 steroid receptor co-activator (SRC) family. Nat Rev Cancer 9(9):615–630. https://doi.org/10.1038/nrc2695

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  167. York B, O’Malley BW (2010) Steroid receptor coactivator (SRC) family: masters of systems biology. J Biol Chem 285(50):38743–38750. https://doi.org/10.1074/jbc.R110.193367

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  168. Liu H, Li HM, Yue Y, Song ZH, Wang JJ, Dou W (2017) The alternative splicing of BdTai and its involvement in the development of Bactrocera dorsalis (Hendel). J Insect Physiol 101:132–141. https://doi.org/10.1016/j.jinsphys.2017.07.012

    Article  CAS  PubMed  Google Scholar 

  169. Li Y, Zheng F, Xiao X, Xie F, Tao D, Huang C, Liu D, Wang M, Wang L, Zeng F, Jiang G (2017) CircHIPK3 sponges miR-558 to suppress heparanase expression in bladder cancer cells. EMBO Rep 18(9):1646–1659. https://doi.org/10.15252/embr.201643581

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  170. Cao Y, Wang C (2000) The COOH-terminal transactivation domain plays a key role in regulating the in vitro and in vivo function of Pax3 homeodomain. J Biol Chem 275(13):9854–9862. https://doi.org/10.1074/jbc.275.13.9854

    Article  CAS  PubMed  Google Scholar 

  171. Sonnenfeld MJ, Delvecchio C, Sun X (2005) Analysis of the transcriptional activation domain of the Drosophila tango bHLH-PAS transcription factor. Dev Genes Evol 215(5):221–229. https://doi.org/10.1007/s00427-004-0462-9

    Article  CAS  PubMed  Google Scholar 

  172. Bai J, Uehara Y, Montell DJ (2000) Regulation of invasive cell behavior by taiman, a Drosophila protein related to AIB1, a steroid receptor coactivator amplified in breast cancer. Cell 103(7):1047–1058. https://doi.org/10.1016/s0092-8674(00)00208-7

    Article  CAS  PubMed  Google Scholar 

  173. Zhu J, Chen L, Sun G, Raikhel AS (2006) The competence factor beta Ftz-F1 potentiates ecdysone receptor activity via recruiting a p160/SRC coactivator. Mol Cell Biol 26(24):9402–9412. https://doi.org/10.1128/MCB.01318-06

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  174. Hashimoto Y, Akiyama Y, Yuasa Y (2013) Multiple-to-multiple relationships between microRNAs and target genes in gastric cancer. PLoS One 8(5):e62589. https://doi.org/10.1371/journal.pone.0062589

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  175. Gilbert LI, Rybczynski R, Warren JT (2002) Control and biochemical nature of the ecdysteroidogenic pathway. Annu Rev Entomol 47:883–916. https://doi.org/10.1146/annurev.ento.47.091201.145302

    Article  CAS  PubMed  Google Scholar 

  176. Spindler KD, Honl C, Tremmel C, Braun S, Ruff H, Spindler-Barth M (2009) Ecdysteroid hormone action. Cell Mol Life Sci 66(24):3837–3850. https://doi.org/10.1007/s00018-009-0112-5

    Article  CAS  PubMed  Google Scholar 

Download references

Acknowledgements

This work was supported by the National Natural Science Foundation of China (NSFC) Grants 31630070 and 31702063.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Shutang Zhou.

Additional information

Publisher's Note

Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Song, J., Zhou, S. Post-transcriptional regulation of insect metamorphosis and oogenesis. Cell. Mol. Life Sci. 77, 1893–1909 (2020). https://doi.org/10.1007/s00018-019-03361-5

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00018-019-03361-5

Keywords

Navigation