1. Precise coordination between nutrient transporters ensures fertility in the malaria mosquito Anopheles gambiae.
- Author
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Stryapunina, Iryna, Itoe, Maurice A., Trinh, Queenie, Vidoudez, Charles, Du, Esrah, Mendoza, Lydia, Hulai, Oleksandr, Kauffman, Jamie, Carew, John, Shaw, W. Robert, and Catteruccia, Flaminia
- Subjects
ANOPHELES gambiae ,MOSQUITOES ,OVARIAN follicle ,AEDES aegypti ,ENDOCYTOSIS ,FERTILITY ,EGGS ,FAT - Abstract
Females from many mosquito species feed on blood to acquire nutrients for egg development. The oogenetic cycle has been characterized in the arboviral vector Aedes aegypti, where after a bloodmeal, the lipid transporter lipophorin (Lp) shuttles lipids from the midgut and fat body to the ovaries, and a yolk precursor protein, vitellogenin (Vg), is deposited into the oocyte by receptor-mediated endocytosis. Our understanding of how the roles of these two nutrient transporters are mutually coordinated is however limited in this and other mosquito species. Here, we demonstrate that in the malaria mosquito Anopheles gambiae, Lp and Vg are reciprocally regulated in a timely manner to optimize egg development and ensure fertility. Defective lipid transport via Lp knockdown triggers abortive ovarian follicle development, leading to misregulation of Vg and aberrant yolk granules. Conversely, depletion of Vg causes an upregulation of Lp in the fat body in a manner that appears to be at least partially dependent on target of rapamycin (TOR) signaling, resulting in excess lipid accumulation in the developing follicles. Embryos deposited by Vg-depleted mothers are completely inviable, and are arrested early during development, likely due to severely reduced amino acid levels and protein synthesis. Our findings demonstrate that the mutual regulation of these two nutrient transporters is essential to safeguard fertility by ensuring correct nutrient balance in the developing oocyte, and validate Vg and Lp as two potential candidates for mosquito control. Author summary: Female mosquitoes bite humans to acquire nutrients for egg development. The shuttling of nutrients from the gut (where the blood is digested) to the ovaries (where eggs are produced) relies on several nutrient transporters to move through the mosquito circulation, including Lipophorin (Lp), a fat transporter expressed early and Vitellogenin (Vg), a large protein expressed later that transports amino acids. We know relatively little of how these two nutrient transporters are successfully coordinated in any mosquito species, so we undertook to examine their interplay in the Anopheles malaria mosquito. We found that without Lp expression, Vg is incorrectly distributed within ovarian follicles and egg production is aborted, whereas without Vg, fat transport by Lp is not switched off in a timely manner. This results in excess fat and minimal protein deposition in eggs, rendering females completely infertile. We also find evidence that the mutual regulation of these transporters may be mediated by TOR signaling. As well as providing further insight into the regulation of essential reproductive processes, these results may aid in the development of malaria control strategies that aim to reduce the size of mosquito populations. [ABSTRACT FROM AUTHOR]
- Published
- 2024
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