Capsaicin decreases fecundity in the Asian malaria vector Anopheles stephensi by inhibiting the target of rapamycin signaling pathway

Abstract

Background Mosquito-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. Methods Anopheles 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. Results The 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. Conclusions Capsaicin 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. Graphical Abstract

Automated analysis of feeding behaviors of females of the mosquito Aedes aegypti using a modified flyPAD system

“…While Anopheles stephensi mosquitoes accepted a 10% sugar solution with 50 µmol L −1 capsaicin for two days, after blood feeding on mice the treated females showed a reduction in the number of eggs laid. The reduction in fertility was caused by capsaicin inhibition of the TOR signaling pathway 67 . Ae.…”

Nutrient Composition of Ovary, Hepatopancreas and Muscle Tissues in Relation to Ovarian Development Stage of Female Swimming Crab, Portunus trituberculatus

“…Moreover, BCAAs are widely believed to activate the mTOR cell signaling pathway, thereby initiating protein synthesis in skeletal muscle and the intestine [51,52]. The mTOR pathway regulates growth, molting, and cell differentiation in crustaceans [53,54], and more importantly, it regulates the expression of vitellogenin to control oocyte maturation, ovarian development, and fecundity in invertebrates [8]. Therefore, exogenous BCAAs are necessary during the maturation process of this species.…”

“…It is well-known that the gonadal development process of crustacea is influenced by critical nutrients. The nutrition intake of broodstocks determines the nutritive value of the ovary, hepatopancreas, and muscle of P. trituberculatus, which affects commercial quality [7] and the ovarian maturation process [8,9]. Some key nutrients, such as amino acids and fatty acids, have been proven to play important roles in regulating the reproductive performance of animals [10][11][12][13].…”

Long-Chain Molecules with Agro-Bioactivities and Their Applications

“…Unlike conventional ryanodine receptor insecticides, Tyclopyrazoflor exhibits a distinctive structure characterized by a unique amide group (Figure 19). Capsaicin ( 36) is a natural alkaloid obtained from the mature fruit of the capsicum [113]. Studies have shown that capsaicin has a stimulating effect in various species, can function as a repellent, and can also influence the egg-laying decisions of various insects [113][114][115].…”