Abstract
Exposure of adult mosquitoes to pyriproxyfen (PPF), an analog of insect juvenile hormone (JH), has shown promise to effectively sterilize female mosquitoes. However, the underlying mechanisms of the PPF-induced decrease in mosquito fecundity are largely unknown. We performed a comprehensive study to dissect the mode of PPF action in Aedes aegypti mosquitoes. Exposure to PPF prompted the overgrowth of primary follicles in sugar-fed Ae. aegypti females but blocked the development of primary follicles at Christopher’s Stage III after blood feeding. Secondary follicles were precociously activated in PPF-treated mosquitoes. Moreover, PPF substantially altered the expression of many genes that are essential for mosquito physiology and oocyte development in the fat body and ovary. In particular, many metabolic genes were differentially expressed in response to PPF treatment, thereby affecting the mobilization and utilization of energy reserves. Furthermore, PPF treatment on the previtellogenic female adults considerably modified mosquito responses to JH and 20-hydroxyecdysone (20E), two major hormones that govern mosquito reproduction. Krüppel homolog 1, a JH-inducible transcriptional regulator, showed consistently elevated expression after PPF exposure. Conversely, PPF upregulated the expression of several key players of the 20E regulatory cascades, including HR3 and E75A, in the previtellogenic stage. After blood-feeding, the expression of these 20E response genes was significantly weaker in PPF-treated mosquitoes than the solvent-treated control groups. RNAi-mediated knockdown of the Methoprene-tolerant (Met) protein, the JH receptor, partially rescued the impaired follicular development after PPF exposure and substantially increased the hatching of the eggs produced by PPF-treated female mosquitoes. Thus, the results suggested that PPF relied on Met to exert its sterilizing effects on female mosquitoes. In summary, this study finds that PPF exposure disturbs normal hormonal responses and metabolism in Ae. aegypti, shedding light on the molecular targets and the downstream signaling pathways activated by PPF.
Highlights
The yellow fever mosquito, Aedes aegypti, is a major vector of several globally important human arboviral diseases including zika, dengue, chikungunya, and yellow fever [1]
Aedes aegypti mosquitoes are responsible for the transmission of dengue, yellow fever, chikungunya, and Zika fever
We demonstrated the involvement of the juvenile hormone (JH) receptor Met in pyriproxyfen-induced female sterilization
Summary
The yellow fever mosquito, Aedes aegypti, is a major vector of several globally important human arboviral diseases including zika, dengue, chikungunya, and yellow fever [1]. There is still a lack of effective vaccines and specific antiviral therapies for most of these mosquito-borne diseases. Pyrethroids are the most common insecticides used to reduce mosquito populations [2]. They comprise ~40% of all insecticides used annually and are the only insecticide recommended by the World Health Organization for the treatment of bed nets [3]. Insecticide resistance is evolving readily in mosquito populations and is jeopardizing the effectiveness of several commonly used insecticides including pyrethroids [4,5,6,7]. New mosquito insecticides with different modes of action are urgently needed
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