Impact of JH Signaling on Reproductive Physiology of the Classical Insect Model,

Overview

Journal Int J Mol Sci

Publisher MDPI

Specialties Biochemistry
Chemistry
Molecular Biology

Date 2022 Nov 26

PMID 36430311

Authors

Jimena Leyria

Ian Orchard

Angela B Lange

Affiliations

Soon will be listed here.

Abstract

In adult females of several insect species, juvenile hormones (JHs) act as gonadotrophic hormones, regulating egg production. JH binds to its nuclear receptor, Methoprene tolerant (Met), triggering its dimerization with the protein Taiman (Tai). The resulting active complex induces transcription of JH response genes, such as Krüppel homolog 1 (Kr-h1). In this study we report for the first time the participation of the isoform JH III skipped bisepoxide (JHSB) and its signaling pathway in the reproductive fitness of the classical insect model . The topical application of synthetic JHSB increases transcript and protein expression of yolk protein precursors (YPPs), mainly by the fat body but also by the ovaries, the second source of YPPs. These results are also confirmed by ex vivo assays. In contrast, when the JH signaling cascade is impaired via RNA interference by downregulating and mRNA, egg production is inhibited. Although transcript expression is highly dependent on JHSB signaling, it is not involved in egg production but rather in successful hatching. This research contributes missing pieces of JH action in the insect model in which JH was first postulated almost 100 years ago.

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References

Gijbels M, Lenaerts C, Broeck J, Marchal E . Juvenile Hormone receptor Met is essential for ovarian maturation in the Desert Locust, Schistocerca gregaria. Sci Rep. 2019; 9(1):10797. PMC: 6658565. DOI: 10.1038/s41598-019-47253-x. View

Leyria J, Orchard I, Lange A . What happens after a blood meal? A transcriptome analysis of the main tissues involved in egg production in Rhodnius prolixus, an insect vector of Chagas disease. PLoS Negl Trop Dis. 2020; 14(10):e0008516. PMC: 7591069. DOI: 10.1371/journal.pntd.0008516. View

Villalobos-Sambucaro M, Nouzova M, Ramirez C, Alzugaray M, Fernandez-Lima F, Ronderos J . The juvenile hormone described in Rhodnius prolixus by Wigglesworth is juvenile hormone III skipped bisepoxide. Sci Rep. 2020; 10(1):3091. PMC: 7033181. DOI: 10.1038/s41598-020-59495-1. View

Liu P, Fu X, Zhu J . Juvenile hormone-regulated alternative splicing of the gene primes the ecdysteroid response in adult mosquitoes. Proc Natl Acad Sci U S A. 2018; 115(33):E7738-E7747. PMC: 6099845. DOI: 10.1073/pnas.1808146115. View

Ramos F, Leyria J, Nouzova M, Fruttero L, Noriega F, Canavoso L . Juvenile hormone mediates lipid storage in the oocytes of Dipetalogaster maxima. Insect Biochem Mol Biol. 2020; 133:103499. DOI: 10.1016/j.ibmb.2020.103499. View

Melo A, Valle D, Machado E, Salerno A, Paiva-Silva G, Cunha E Silva N . Synthesis of vitellogenin by the follicle cells of Rhodnius prolixus. Insect Biochem Mol Biol. 2000; 30(7):549-57. DOI: 10.1016/s0965-1748(00)00023-0. View

Minakuchi C, Zhou X, Riddiford L . Krüppel homolog 1 (Kr-h1) mediates juvenile hormone action during metamorphosis of Drosophila melanogaster. Mech Dev. 2007; 125(1-2):91-105. PMC: 2276646. DOI: 10.1016/j.mod.2007.10.002. View

Bai J, Uehara Y, Montell D . Regulation of invasive cell behavior by taiman, a Drosophila protein related to AIB1, a steroid receptor coactivator amplified in breast cancer. Cell. 2001; 103(7):1047-58. DOI: 10.1016/s0092-8674(00)00208-7. View

Li M, Mead E, Zhu J . Heterodimer of two bHLH-PAS proteins mediates juvenile hormone-induced gene expression. Proc Natl Acad Sci U S A. 2010; 108(2):638-43. PMC: 3021087. DOI: 10.1073/pnas.1013914108. View

10.

Gujar H, Palli S . Juvenile hormone regulation of female reproduction in the common bed bug, Cimex lectularius. Sci Rep. 2016; 6:35546. PMC: 5071884. DOI: 10.1038/srep35546. View

11.

Jones D, Taylor W, Thornton J . The rapid generation of mutation data matrices from protein sequences. Comput Appl Biosci. 1992; 8(3):275-82. DOI: 10.1093/bioinformatics/8.3.275. View

12.

Lin X, Yao Y, Wang B . Methoprene-tolerant (Met) and Krüpple-homologue 1 (Kr-h1) are required for ovariole development and egg maturation in the brown plant hopper. Sci Rep. 2015; 5:18064. PMC: 4677288. DOI: 10.1038/srep18064. View

13.

Kumar S, Stecher G, Li M, Knyaz C, Tamura K . MEGA X: Molecular Evolutionary Genetics Analysis across Computing Platforms. Mol Biol Evol. 2018; 35(6):1547-1549. PMC: 5967553. DOI: 10.1093/molbev/msy096. View

14.

Zhu J, Chen L, Sun G, Raikhel A . The competence factor beta Ftz-F1 potentiates ecdysone receptor activity via recruiting a p160/SRC coactivator. Mol Cell Biol. 2006; 26(24):9402-12. PMC: 1698532. DOI: 10.1128/MCB.01318-06. View

15.

Lange A, Leyria J, Orchard I . The hormonal and neural control of egg production in the historically important model insect, Rhodnius prolixus: A review, with new insights in this post-genomic era. Gen Comp Endocrinol. 2022; 321-322:114030. DOI: 10.1016/j.ygcen.2022.114030. View

16.

Parthasarathy R, Sun Z, Bai H, Palli S . Juvenile hormone regulation of vitellogenin synthesis in the red flour beetle, Tribolium castaneum. Insect Biochem Mol Biol. 2010; 40(5):405-14. PMC: 2875371. DOI: 10.1016/j.ibmb.2010.03.006. View

17.

Davey K . The modes of action of juvenile hormones: some questions we ought to ask. Insect Biochem Mol Biol. 2000; 30(8-9):663-9. DOI: 10.1016/s0965-1748(00)00037-0. View

18.

Hejnikova M, Paroulek M, Hodkova M . Decrease in Methoprene tolerant and Taiman expression reduces juvenile hormone effects and enhances the levels of juvenile hormone circulating in males of the linden bug Pyrrhocoris apterus. J Insect Physiol. 2016; 93-94:72-80. DOI: 10.1016/j.jinsphys.2016.08.009. View

19.

Fruttero L, Leyria J, Canavoso L . Lipids in Insect Oocytes: From the Storage Pathways to Their Multiple Functions. Results Probl Cell Differ. 2017; 63:403-434. DOI: 10.1007/978-3-319-60855-6_18. View

20.

Leyria J, Orchard I, Lange A . The involvement of insulin/ToR signaling pathway in reproductive performance of Rhodnius prolixus. Insect Biochem Mol Biol. 2021; 130:103526. DOI: 10.1016/j.ibmb.2021.103526. View