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Neuropeptide Bursicon Influences Reproductive Physiology in Tribolium Castaneum

Bursicon is a neuropeptide belonging to the cystine knot family and is composed of burs and partner of burs (pburs) subunits. It can form heterodimers or homodimers to execute different biological functions. Bursicon heterodimers regulate cuticle sclerotization and wing maturation, whereas bursicon...

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Autores principales: Li, Jingjing, Zhu, Zidan, Bi, Jingxiu, Feng, Qili, Beerntsen, Brenda T., Song, Qisheng
Formato: Online Artículo Texto
Lenguaje:English
Publicado: Frontiers Media S.A. 2021
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC8567023/
https://www.ncbi.nlm.nih.gov/pubmed/34744761
http://dx.doi.org/10.3389/fphys.2021.717437
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author Li, Jingjing
Zhu, Zidan
Bi, Jingxiu
Feng, Qili
Beerntsen, Brenda T.
Song, Qisheng
author_facet Li, Jingjing
Zhu, Zidan
Bi, Jingxiu
Feng, Qili
Beerntsen, Brenda T.
Song, Qisheng
author_sort Li, Jingjing
collection PubMed
description Bursicon is a neuropeptide belonging to the cystine knot family and is composed of burs and partner of burs (pburs) subunits. It can form heterodimers or homodimers to execute different biological functions. Bursicon heterodimers regulate cuticle sclerotization and wing maturation, whereas bursicon homodimers mediate innate immunity and midgut stem cell proliferation. A recent study has shown that bursicon potentially induces the expression of vitellogenin (Vg) in the black tiger shrimp Penaeus monodon; however, the underlying mechanism remains unknown. In this study, we investigated the role of bursicon in the reproductive physiology of the red flour beetle, Tribolium castaneum. The knockdown of burs, pburs, or its receptor T. castaneum rickets (Tcrk) in 2-day pupae significantly downregulated the expression levels of Vg1, Vg2, and Vg receptor (VgR) genes in females 3- and 5-day post-adult emergence, leading to abnormal oocytes with limited Vg content. The silencing of burs repressed the number of eggs laid and completely inhibited egg hatch, whereas the silencing of pburs dramatically decreased the number of eggs laid, hatch rate, and offspring larval size, and this RNA interference (RNAi) effects persisted to the next generation. Furthermore, the knockdown of burs or pburs downregulated the expression of the insulin/insulin-like signaling/target of rapamycin (TOR) signaling genes encoding insulin receptor (InR), protein kinase B (Akt), TOR, and ribosomal protein S6 kinase (S6K). Most importantly, the injection of recombinant pburs (r-pburs) protein was able to upregulate the expression of Vg, VgR, InR, Akt, TOR, S6K, JH synthesis (JHAMT), Methoprene-tolerant (Met), and Taiman (Tai) in normal females and rescue the expression of Vg and VgR in pburs RNAi females but failed to rescue Vg and VgR in Tcrk knockdown females. We infer that bursicon homodimers influence Vg expression via the receptor Tcrk, possibly by mediating the expression of the juvenile hormone (JH) and IIS/TOR pathway genes, thereby regulating reproduction in T. castaneum.
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spelling pubmed-85670232021-11-05 Neuropeptide Bursicon Influences Reproductive Physiology in Tribolium Castaneum Li, Jingjing Zhu, Zidan Bi, Jingxiu Feng, Qili Beerntsen, Brenda T. Song, Qisheng Front Physiol Physiology Bursicon is a neuropeptide belonging to the cystine knot family and is composed of burs and partner of burs (pburs) subunits. It can form heterodimers or homodimers to execute different biological functions. Bursicon heterodimers regulate cuticle sclerotization and wing maturation, whereas bursicon homodimers mediate innate immunity and midgut stem cell proliferation. A recent study has shown that bursicon potentially induces the expression of vitellogenin (Vg) in the black tiger shrimp Penaeus monodon; however, the underlying mechanism remains unknown. In this study, we investigated the role of bursicon in the reproductive physiology of the red flour beetle, Tribolium castaneum. The knockdown of burs, pburs, or its receptor T. castaneum rickets (Tcrk) in 2-day pupae significantly downregulated the expression levels of Vg1, Vg2, and Vg receptor (VgR) genes in females 3- and 5-day post-adult emergence, leading to abnormal oocytes with limited Vg content. The silencing of burs repressed the number of eggs laid and completely inhibited egg hatch, whereas the silencing of pburs dramatically decreased the number of eggs laid, hatch rate, and offspring larval size, and this RNA interference (RNAi) effects persisted to the next generation. Furthermore, the knockdown of burs or pburs downregulated the expression of the insulin/insulin-like signaling/target of rapamycin (TOR) signaling genes encoding insulin receptor (InR), protein kinase B (Akt), TOR, and ribosomal protein S6 kinase (S6K). Most importantly, the injection of recombinant pburs (r-pburs) protein was able to upregulate the expression of Vg, VgR, InR, Akt, TOR, S6K, JH synthesis (JHAMT), Methoprene-tolerant (Met), and Taiman (Tai) in normal females and rescue the expression of Vg and VgR in pburs RNAi females but failed to rescue Vg and VgR in Tcrk knockdown females. We infer that bursicon homodimers influence Vg expression via the receptor Tcrk, possibly by mediating the expression of the juvenile hormone (JH) and IIS/TOR pathway genes, thereby regulating reproduction in T. castaneum. Frontiers Media S.A. 2021-10-21 /pmc/articles/PMC8567023/ /pubmed/34744761 http://dx.doi.org/10.3389/fphys.2021.717437 Text en Copyright © 2021 Li, Zhu, Bi, Feng, Beerntsen and Song. https://creativecommons.org/licenses/by/4.0/This is an open-access article distributed under the terms of the Creative Commons Attribution License (CC BY). The use, distribution or reproduction in other forums is permitted, provided the original author(s) and the copyright owner(s) are credited and that the original publication in this journal is cited, in accordance with accepted academic practice. No use, distribution or reproduction is permitted which does not comply with these terms.
spellingShingle Physiology
Li, Jingjing
Zhu, Zidan
Bi, Jingxiu
Feng, Qili
Beerntsen, Brenda T.
Song, Qisheng
Neuropeptide Bursicon Influences Reproductive Physiology in Tribolium Castaneum
title Neuropeptide Bursicon Influences Reproductive Physiology in Tribolium Castaneum
title_full Neuropeptide Bursicon Influences Reproductive Physiology in Tribolium Castaneum
title_fullStr Neuropeptide Bursicon Influences Reproductive Physiology in Tribolium Castaneum
title_full_unstemmed Neuropeptide Bursicon Influences Reproductive Physiology in Tribolium Castaneum
title_short Neuropeptide Bursicon Influences Reproductive Physiology in Tribolium Castaneum
title_sort neuropeptide bursicon influences reproductive physiology in tribolium castaneum
topic Physiology
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC8567023/
https://www.ncbi.nlm.nih.gov/pubmed/34744761
http://dx.doi.org/10.3389/fphys.2021.717437
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