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Increased Akt signaling in the fat body of Anopheles stephensi extends lifespan and increases lifetime fecundity through modulation of insulin-like peptides.

ABSTRACT: Insulin-like peptides (ILPs) and the insulin/insulin-like growth factor 1 signaling (IIS) cascade regulate numerous physiological functions, including lifespan, reproduction, immunity, and metabolism, in diverse eukaryotes. We previously demonstrated that in female Anopheles stephensi and Aedes aegypti mosquitoes, activation of the IIS cascade in the fat body led to a significant increase in lifespan. In this work, we elucidated two putative mechanisms in A. stephensi behind the observed lifespan extension and assessed whether this lifespan extension confers an overall fitness advantage to the mosquito. Specifically, we demonstrated that increased Akt signaling in the mosquito fat body following a blood meal significantly suppressed the expression of ILP2 in the head. Moreover, overexpression of active Akt in the fat body altered the expression of a putative insulin binding protein ortholog, Imaginal morphogenesis protein-Late 2 (Imp-L2), in response to transgene expression. Combined, these two factors may act to reduce overall levels of circulating ILP2 or other ILPs in the mosquito, in turn conferring increased survival. We also examined the impact increased fat body IIS had on lifetime fecundity and demonstrated that transgenic female mosquito populations had higher lifetime fecundity relative to non-transgenic sibling controls. These studies provide new insights into the complex hormonal and molecular mechanisms regulating the interplay between IIS, aging, and reproduction in this important vector of human malaria parasites.

SUBMITTER: Hun LV

PROVIDER: S-EPMC6810901 | biostudies-literature | 2019 Oct

REPOSITORIES: biostudies-literature

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Increased Akt signaling in the fat body of Anopheles stephensi extends lifespan and increases lifetime fecundity through modulation of insulin-like peptides.

Hun Lewis V LV Luckhart Shirley S Riehle Michael A MA

Journal of insect physiology 20190822

Insulin-like peptides (ILPs) and the insulin/insulin-like growth factor 1 signaling (IIS) cascade regulate numerous physiological functions, including lifespan, reproduction, immunity, and metabolism, in diverse eukaryotes. We previously demonstrated that in female Anopheles stephensi and Aedes aegypti mosquitoes, activation of the IIS cascade in the fat body led to a significant increase in lifespan. In this work, we elucidated two putative mechanisms in A. stephensi behind the observed lifespa ...[more]

PMID: 31445957

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Project description:BackgroundMosquito-borne diseases threaten human health, but mosquito control faces various challenges, such as resistance to chemical insecticides. Thus, there is an urgent need for more effective and environment-friendly control agents. Capsaicin can downregulate the mTOR signaling pathway of tumor cells. The TOR signaling pathway can mediate the expression of vitellogenin (Vg) to regulate the fecundity of insects. Whether capsaicin has the potential to inhibit fecundity of mosquitoes by regulating TOR pathway and Vg expression is currently unclear.MethodsAnopheles stephensi were fed with blood of mice administered capsaicin by gavage or sugar containing capsaicin followed by a blood feeding with normal mice. Then, the engorged female mosquitoes were tubed individually and underwent oviposition. The eggs and individuals in the subsequent development stages, including larvae, pupae, and emerging adults, were counted and compared between the capsaicin treatment and control groups. Additionally, total RNA and protein were extracted from the engorged mosquitoes at 24 h post blood feeding. Real-time PCR and western blot were performed to detect the transcriptional level and protein expression of the key fecundity-related molecules of mosquitoes. Finally, TOR signaling pathway was inhibited via rapamycin treatment, and changes in fecundity and the key molecule transcription and protein expression levels were examined to verify the role of TOR signaling pathway in the effect of capsaicin on mosquito fecundity.ResultsThe laid and total eggs (laid eggs plus retained eggs) of An. stephensi were significantly reduced by feeding on the blood of capsaicin-treated mice (P < 0.01) or capsaicin-containing sugar (P < 0.01) compared with those in the control group. Moreover, the transcription and protein expression or phosphorylation levels of fecundity-related molecules, such as Akt, TOR, S6K, and Vg, were significantly decreased by capsaicin treatment. However, the effects disappeared between control group and CAP group after the TOR signaling pathway was inhibited by rapamycin.ConclusionsCapsaicin can decrease the fecundity of An. stephensi by inhibiting the TOR signaling pathway. These data can help us to not only understand the effect of capsaicin on the reproductive ability of An. stephensi and its underlying mechanism, but also develop new efficient, safe, and pollution-free mosquito vector control agents.

Dataset Information

Increased Akt signaling in the fat body of Anopheles stephensi extends lifespan and increases lifetime fecundity through modulation of insulin-like peptides.

Publications

Increased Akt signaling in the fat body of Anopheles stephensi extends lifespan and increases lifetime fecundity through modulation of insulin-like peptides.

Similar Datasets

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