Investigating the role of aae-miR-34-5p in the regulation of juvenile hormone biosynthesis genes in the mosquito Aedes aegypti

. 2023 Nov 03 ; 13 (1) : 19023. [epub] 20231103

Jazyk angličtina Země Velká Británie, Anglie Médium electronic

Typ dokumentu časopisecké články, Research Support, N.I.H., Extramural, práce podpořená grantem

Perzistentní odkaz   https://www.medvik.cz/link/pmid37923767

Grantová podpora
R21 AI167849 NIAID NIH HHS - United States

Odkazy

PubMed 37923767
PubMed Central PMC10624809
DOI 10.1038/s41598-023-46154-4
PII: 10.1038/s41598-023-46154-4
Knihovny.cz E-zdroje

Juvenile hormone (JH) controls the development and reproduction of insects. Therefore, a tight regulation of the expression of JH biosynthetic enzymes is critical. microRNAs (miRNAs) play significant roles in the post-transcriptional regulation of gene expression by interacting with complementary sequences in target genes. Previously, we reported that several miRNAs were differentially expressed during three developmental stages of Aedes aegypti mosquitoes with different JH levels (no JH, high JH, and low JH). One of these miRNAs was aae-miR-34-5p. In this study, we identified the presence of potential target sequences of aae-miR-34-5p in the transcripts of some genes encoding JH biosynthetic enzymes. We analysed the developmental expression patterns of aae-miR-34-5p and the predicted target genes involved in JH biogenesis. Increases in miRNA abundance were followed, with a delay, by decreases in transcript levels of target genes. Application of an inhibitor and a mimic of aae-miR-34-5p led respectively to increased and decreased levels of thiolase transcripts, which is one of the early genes of JH biosynthesis. Female adult mosquitoes injected with an aae-miR-34-5p inhibitor exhibited significantly increased transcript levels of three genes encoding JH biosynthetic enzymes, acetoacetyl-CoA thiolase (thiolase), farnesyl diphosphate phosphatase, and farnesal dehydrogenase. Overall, our results suggest a potential role of miRNAs in JH production by directly targeting genes involved in its biosynthesis.

Zobrazit více v PubMed

Noriega FG. Juvenile hormone biosynthesis in insects: What is new, what do we know, and what questions remain? Int. Sch. Res. Notices. 2014;2014:967361. PubMed PMC

Rivera-Perez C, Clifton ME, Noriega FG, Jindra M. Juvenile hormone regulation and action. In: Saleuddin S, Lange AB, Orchard I, editors. Advances in Invertebrate (Neuro) Endocrinology. Apple Academic Press; 2020. pp. 1–76.

Zhu J, Noriega F. The Role of Juvenile Hormone in Mosquito Development and Reproduction. In: Raikhel AS, editor. Advances in Insect Physiology. Elsevier; 2016. pp. 93–113.

Tobe SS, Stay B. Structure and Regulation of the Corpus allatum. In: Berridge MJ, Treherne JE, Wigglesworth VB, editors. Advances in Insect Physiology. Elsevier; 1985. pp. 305–432.

Nouzova M, Edwards MJ, Mayoral JG, Noriega FG. A coordinated expression of biosynthetic enzymes controls the flux of juvenile hormone precursors in the corpora allata of mosquitoes. Insect Biochem. Mol. Biol. 2011;41:660–669. doi: 10.1016/j.ibmb.2011.04.008. PubMed DOI PMC

Bartel DP. MicroRNAs: Target recognition and regulatory functions. Cell. 2009;23:215–233. doi: 10.1016/j.cell.2009.01.002. PubMed DOI PMC

Bartel DP. Metazoan microRNAs. Cell. 2018;173:20–51. doi: 10.1016/j.cell.2018.03.006. PubMed DOI PMC

Asgari S. MicroRNA functions in insects. Insect Biochem. Mol. Biol. 2013;43:388–397. doi: 10.1016/j.ibmb.2012.10.005. PubMed DOI

Hussain M, Asgari S. MicroRNAs as mediators of insect host–pathogen interactions and immunity. J. Insect Physiol. 2014;70:151–158. doi: 10.1016/j.jinsphys.2014.08.003. PubMed DOI

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

Pfaffl MW. A new mathematical model for relative quantification in real-time RT-PCR. Nucl. Acids Res. 2001;29:e45. doi: 10.1093/nar/29.9.e45. PubMed DOI PMC

Bryant B, Macdonad W, Raikhel AS. microRNA miR-275 is indispensable for blood digestion and egg development in the mosquito Aedes aegypti. Proc. Natl. Acad. Sci. USA. 2010;107:22391–22398. doi: 10.1073/pnas.1016230107. PubMed DOI PMC

Liu S, Lucas K, Roy S, Ha J, Raikhel A. Mosquito-specific microRNA-1174 targets serine hydroxymethyltransferase to control key functions in the gut. Proc. Natl. Acad. Sci. USA. 2014;111:14460–14465. doi: 10.1073/pnas.1416278111. PubMed DOI PMC

Lucas K, et al. MicroRNA-8 targets the Wingless signaling pathway in the female mosquito fat body to regulate reproductive processes. Proc. Natl. Acad. Sci. USA. 2015;112:1440–1445. doi: 10.1073/pnas.1424408112. PubMed DOI PMC

Zhang Y, et al. microRNA-309 targets the Homeobox gene SIX4 and controls ovarian development in the mosquito Aedes aegypti. Proc. Natl. Acad. Sci. USA. 2016;113:E4828–E4836. PubMed PMC

Ono H. Ecdysone differentially regulates metamorphic timing relative to 20-hydroxyecdysone by antagonizing juvenile hormone in Drosophila melanogaster. Dev. Biol. 2014;391:32–42. doi: 10.1016/j.ydbio.2014.04.004. PubMed DOI

Xiong X-P, et al. miR-34 modulates innate immunity and ecdysone signaling in Drosophila. PLoS Pathog. 2016;12:e1006034. doi: 10.1371/journal.ppat.1006034. PubMed DOI PMC

Jin X, et al. 20-Hydroxyecdysone-responsive microRNAs of insects. RNA Biol. 2020;17:1454–1471. doi: 10.1080/15476286.2020.1775395. PubMed DOI PMC

Ye X, et al. miR-34 modulates wing polyphenism in planthopper. PLoS Genet. 2019;15:e1008235. doi: 10.1371/journal.pgen.1008235. PubMed DOI PMC

Rivera-Perez C, Nouzova M, Lamboglia I, Noriega FG. Metabolic analysis reveals changes in the mevalonate and juvenile hormone synthesis pathways linked to the mosquito reproductive physiology. Insect Biochem. Mol. Biol. 2014;51:1–9. doi: 10.1016/j.ibmb.2014.05.001. PubMed DOI PMC

Wang C, et al. microRNA-34 family: From mechanism to potential applications. Int. J. Biochem. Cell Biol. 2022;144:106168. doi: 10.1016/j.biocel.2022.106168. PubMed DOI

Rivera-Perez C, et al. Aldehyde dehydrogenase 3 converts farnesal into farnesoic acid in the corpora allata of mosquitoes. Insect Biochem. Mol. Biol. 2013;43:675–682. doi: 10.1016/j.ibmb.2013.04.002. PubMed DOI PMC

Fan F, et al. MicroRNA-34a promotes cardiomyocyte apoptosis post myocardial infarction through down-regulating aldehyde dehydrogenase 2. Curr. Pharm. Des. 2013;19:4865–4873. doi: 10.2174/13816128113199990325. PubMed DOI

Gomez-Orte E, Belles X. MicroRNA-dependent metamorphosis in hemimetabolan insects. Proc. Natl. Acad. Sci. USA. 2009;106:21678–21682. doi: 10.1073/pnas.0907391106. PubMed DOI PMC

Lozano J, Montanez R, Belles X. MiR-2 family regulates insect metamorphosis by controlling the juvenile hormone signaling pathway. Proc. Natl. Acad. Sci. USA. 2015;112:3740–3745. doi: 10.1073/pnas.1418522112. PubMed DOI PMC

Song J, et al. The microRNAs let-7 and miR-278 regulate insect metamorphosis and oogenesis by targeting the juvenile hormone early-response gene Krüppel-homolog 1. Development. 2018;145:dev170670. doi: 10.1242/dev.170670. PubMed DOI

Qu Z, et al. MicroRNAs regulate the sesquiterpenoid hormonal pathway in Drosophila and other arthropods. Proc. Biol. Sci. 2017;284:20171827. PubMed PMC

Fu X, Liu P, Dimopoulos G, Zhu J. Dynamic miRNA-mRNA interactions coordinate gene expression in adult Anopheles gambiae. PLoS Genet. 2020;16:e1008765. doi: 10.1371/journal.pgen.1008765. PubMed DOI PMC

Ou Q, et al. The insect prothoracic gland as a model for steroid hormone biosynthesis and regulation. Cell Rep. 2016;16:247–262. doi: 10.1016/j.celrep.2016.05.053. PubMed DOI PMC

Martínez-Rincón RO, Rivera-Pérez C, Diambra L, Noriega FG. Modeling the flux of metabolites in the juvenile hormone biosynthesis pathway using generalized additive models and ordinary differential equations. PLoS One. 2017;12:e0171516. doi: 10.1371/journal.pone.0171516. PubMed DOI PMC

Najít záznam

Citační ukazatele

Nahrávání dat ...

Možnosti archivace

Nahrávání dat ...