Precise coordination between nutrient transporters ensures fertility in the malaria mosquito Anopheles gambiae.
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...
| Main Authors: | , , , , , , , , , , |
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| Format: | Article |
| Language: | English |
| Published: |
Public Library of Science (PLoS)
2024-01-01
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| Series: | PLoS Genetics |
| Online Access: | https://doi.org/10.1371/journal.pgen.1011145 |
| _version_ | 1797304784182575104 |
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| author | Iryna Stryapunina Maurice A Itoe Queenie Trinh Charles Vidoudez Esrah Du Lydia Mendoza Oleksandr Hulai Jamie Kauffman John Carew W Robert Shaw Flaminia Catteruccia |
| author_facet | Iryna Stryapunina Maurice A Itoe Queenie Trinh Charles Vidoudez Esrah Du Lydia Mendoza Oleksandr Hulai Jamie Kauffman John Carew W Robert Shaw Flaminia Catteruccia |
| author_sort | Iryna Stryapunina |
| collection | DOAJ |
| description | 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. |
| first_indexed | 2024-03-08T00:15:29Z |
| format | Article |
| id | doaj.art-c785ddf127f44b3687977b934f76adcb |
| institution | Directory Open Access Journal |
| issn | 1553-7390 1553-7404 |
| language | English |
| last_indexed | 2024-03-08T00:15:29Z |
| publishDate | 2024-01-01 |
| publisher | Public Library of Science (PLoS) |
| record_format | Article |
| series | PLoS Genetics |
| spelling | doaj.art-c785ddf127f44b3687977b934f76adcb2024-02-17T05:32:23ZengPublic Library of Science (PLoS)PLoS Genetics1553-73901553-74042024-01-01201e101114510.1371/journal.pgen.1011145Precise coordination between nutrient transporters ensures fertility in the malaria mosquito Anopheles gambiae.Iryna StryapuninaMaurice A ItoeQueenie TrinhCharles VidoudezEsrah DuLydia MendozaOleksandr HulaiJamie KauffmanJohn CarewW Robert ShawFlaminia CatterucciaFemales 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.https://doi.org/10.1371/journal.pgen.1011145 |
| spellingShingle | Iryna Stryapunina Maurice A Itoe Queenie Trinh Charles Vidoudez Esrah Du Lydia Mendoza Oleksandr Hulai Jamie Kauffman John Carew W Robert Shaw Flaminia Catteruccia Precise coordination between nutrient transporters ensures fertility in the malaria mosquito Anopheles gambiae. PLoS Genetics |
| title | Precise coordination between nutrient transporters ensures fertility in the malaria mosquito Anopheles gambiae. |
| title_full | Precise coordination between nutrient transporters ensures fertility in the malaria mosquito Anopheles gambiae. |
| title_fullStr | Precise coordination between nutrient transporters ensures fertility in the malaria mosquito Anopheles gambiae. |
| title_full_unstemmed | Precise coordination between nutrient transporters ensures fertility in the malaria mosquito Anopheles gambiae. |
| title_short | Precise coordination between nutrient transporters ensures fertility in the malaria mosquito Anopheles gambiae. |
| title_sort | precise coordination between nutrient transporters ensures fertility in the malaria mosquito anopheles gambiae |
| url | https://doi.org/10.1371/journal.pgen.1011145 |
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