MicroRNA-14 As an Efficient Suppressor to Switch off Ecdysone Production After Ecdysis in Insects

Overview

Journal RNA Biol

Specialty Molecular Biology

Date 2019 Jun 12

PMID 31184522

Citations 11

Authors

Kang He

Huamei Xiao

Yang Sun

Gongming Situ

Yu Xi

Fei Li

Affiliations

Soon will be listed here.

Abstract

The precise increase and decrease of hormone ecdysone are critical for accurate development in insects. Most previous works focus on transcriptional activation of ecdysone production; however, little is known about the mechanism of switching off ecdysone biosynthesis after ecdysis. Here, we showed that the precursor microRNA-14 (pre-miR-14) encodes two mature miRNAs in silkworm; both of these two mature miRNAs regulate various genes in the ecdysone-signalling pathway. targets on nine genes whereas targets on two genes in the same pathway. These two mature miRNAs increased immediately after the ecdysis, efficiently suppressing the 20-hydroxyecdysone (20E) biosynthesis, the upstream regulation, and the downstream response genes. Knocking down either of two mature miRNAs or both of them delays moult development, impairing development synchrony in antagomir-treated groups. In addition, overexpressing but not significantly affected the 20E titer and increased the moulting time variation, suggesting that , though it is less abundant, has more potent effects in development regulation than . In summary, we present evidence that a pre-miRNA encodes two mature miRNAs targeting on the same pathway, which significantly improves miRNA regulation efficiencies to programmatically switch off ecdysone biosynthesis.

Citing Articles

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References

Rewitz K, Rybczynski R, Warren J, Gilbert L . The Halloween genes code for cytochrome P450 enzymes mediating synthesis of the insect moulting hormone. Biochem Soc Trans. 2006; 34(Pt 6):1256-60. DOI: 10.1042/BST0341256. View

Rewitz K, Yamanaka N, Gilbert L, OConnor M . The insect neuropeptide PTTH activates receptor tyrosine kinase torso to initiate metamorphosis. Science. 2009; 326(5958):1403-5. DOI: 10.1126/science.1176450. View

Okamura K, Phillips M, Tyler D, Duan H, Chou Y, Lai E . The regulatory activity of microRNA* species has substantial influence on microRNA and 3' UTR evolution. Nat Struct Mol Biol. 2008; 15(4):354-63. PMC: 2698667. DOI: 10.1038/nsmb.1409. View

Krutzfeldt J, Rajewsky N, Braich R, Rajeev K, Tuschl T, Manoharan M . Silencing of microRNAs in vivo with 'antagomirs'. Nature. 2005; 438(7068):685-9. DOI: 10.1038/nature04303. View

Chen J, Liang Z, Liang Y, Pang R, Zhang W . 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. 2013; 43(9):839-48. DOI: 10.1016/j.ibmb.2013.06.002. View

Lozano J, Montanez R, Belles X . MiR-2 family regulates insect metamorphosis by controlling the juvenile hormone signaling pathway. Proc Natl Acad Sci U S A. 2015; 112(12):3740-5. PMC: 4378413. DOI: 10.1073/pnas.1418522112. View

Cai Y, Yu X, Zhou Q, Yu C, Hu H, Liu J . Novel microRNAs in silkworm (Bombyx mori). Funct Integr Genomics. 2010; 10(3):405-15. DOI: 10.1007/s10142-010-0162-7. View

Liu Z, Ling L, Xu J, Zeng B, Huang Y, Shang P . MicroRNA-14 regulates larval development time in Bombyx mori. Insect Biochem Mol Biol. 2017; 93:57-65. DOI: 10.1016/j.ibmb.2017.12.009. View

Vidigal J, Ventura A . The biological functions of miRNAs: lessons from in vivo studies. Trends Cell Biol. 2014; 25(3):137-47. PMC: 4344861. DOI: 10.1016/j.tcb.2014.11.004. View

10.

Zhang Y, Huang Q, Yin G, Lee S, Jia R, Liu Z . Identification of microRNAs by small RNA deep sequencing for synthetic microRNA mimics to control Spodoptera exigua. Gene. 2014; 557(2):215-21. DOI: 10.1016/j.gene.2014.12.038. View

11.

Ling L, Ge X, Li Z, Zeng B, Xu J, Aslam A . MicroRNA Let-7 regulates molting and metamorphosis in the silkworm, Bombyx mori. Insect Biochem Mol Biol. 2014; 53:13-21. DOI: 10.1016/j.ibmb.2014.06.011. View

12.

Hwang C, Matoso A, Corney D, Flesken-Nikitin A, Korner S, Wang W . Wild-type p53 controls cell motility and invasion by dual regulation of MET expression. Proc Natl Acad Sci U S A. 2011; 108(34):14240-5. PMC: 3161601. DOI: 10.1073/pnas.1017536108. View

13.

Gomez-Orte E, Belles X . MicroRNA-dependent metamorphosis in hemimetabolan insects. Proc Natl Acad Sci U S A. 2009; 106(51):21678-82. PMC: 2799836. DOI: 10.1073/pnas.0907391106. View

14.

Wang Y, Yang M, Jiang F, Zhang J, Kang L . MicroRNA-dependent development revealed by RNA interference-mediated gene silencing of LmDicer1 in the migratory locust. Insect Sci. 2013; 20(1):53-60. DOI: 10.1111/j.1744-7917.2012.01542.x. View

15.

Sempere L, Sokol N, Dubrovsky E, Berger E, Ambros V . Temporal regulation of microRNA expression in Drosophila melanogaster mediated by hormonal signals and broad-Complex gene activity. Dev Biol. 2003; 259(1):9-18. DOI: 10.1016/s0012-1606(03)00208-2. View

16.

Niwa Y, Niwa R . Transcriptional regulation of insect steroid hormone biosynthesis and its role in controlling timing of molting and metamorphosis. Dev Growth Differ. 2015; 58(1):94-105. PMC: 11520982. DOI: 10.1111/dgd.12248. View

17.

Satake S, Kaya M, Sakurai S . Hemolymph ecdysteroid titer and ecdysteroid-dependent developmental events in the last-larval stadium of the silkworm, Bombyx mori: role of low ecdysteroid titer in larval-pupal metamorphosis and a reappraisal of the head critical period. J Insect Physiol. 2003; 44(10):867-881. DOI: 10.1016/s0022-1910(98)00075-4. View

18.

Jiang J, Ge X, Li Z, Wang Y, Song Q, Stanley D . MicroRNA-281 regulates the expression of ecdysone receptor (EcR) isoform B in the silkworm, Bombyx mori. Insect Biochem Mol Biol. 2013; 43(8):692-700. DOI: 10.1016/j.ibmb.2013.05.002. View

19.

Kozomara A, Griffiths-Jones S . miRBase: annotating high confidence microRNAs using deep sequencing data. Nucleic Acids Res. 2013; 42(Database issue):D68-73. PMC: 3965103. DOI: 10.1093/nar/gkt1181. View

20.

Guittard E, Blais C, Maria A, Parvy J, Pasricha S, Lumb C . CYP18A1, a key enzyme of Drosophila steroid hormone inactivation, is essential for metamorphosis. Dev Biol. 2010; 349(1):35-45. DOI: 10.1016/j.ydbio.2010.09.023. View