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Selection for insecticide resistance can promote Plasmodium falciparum infection in Anopheles

Insecticide resistance is under strong selective pressure in Anopheles mosquitoes due to widespread usage of insecticides in vector control strategies. Resistance mechanisms likely cause changes that profoundly affect mosquito physiology, yet it remains poorly understood how selective pressures impo...

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Autores principales: Adams, Kelsey L., Selland, Emily K., Willett, Bailey C., Carew, John W., Vidoudez, Charles, Singh, Naresh, Catteruccia, Flaminia
Formato: Online Artículo Texto
Lenguaje:English
Publicado: Public Library of Science 2023
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC10313043/
https://www.ncbi.nlm.nih.gov/pubmed/37339122
http://dx.doi.org/10.1371/journal.ppat.1011448
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author Adams, Kelsey L.
Selland, Emily K.
Willett, Bailey C.
Carew, John W.
Vidoudez, Charles
Singh, Naresh
Catteruccia, Flaminia
author_facet Adams, Kelsey L.
Selland, Emily K.
Willett, Bailey C.
Carew, John W.
Vidoudez, Charles
Singh, Naresh
Catteruccia, Flaminia
author_sort Adams, Kelsey L.
collection PubMed
description Insecticide resistance is under strong selective pressure in Anopheles mosquitoes due to widespread usage of insecticides in vector control strategies. Resistance mechanisms likely cause changes that profoundly affect mosquito physiology, yet it remains poorly understood how selective pressures imposed by insecticides may alter the ability of the mosquito to host and transmit a Plasmodium infection. From pyrethroid-resistant field-derived Anopheles gambiae s.l. mosquitoes, we established resistant (RES) and susceptible (SUS) colonies by either selection for, or loss of insecticide resistance. We show increased oocyst intensity and growth rate as well as increased sporozoite prevalence and intensity in RES compared to SUS females infected with Plasmodium falciparum. The increase in infection intensity in RES females was not associated with the presence of the kdrL1014F mutation and was not impacted by inhibition of Cytochrome P450s. The lipid transporter lipophorin (Lp), which was upregulated in RES compared to SUS, was at least partly implicated in the increased intensity of P. falciparum but not directly involved in the insecticide resistance phenotype. Interestingly, we observed that although P. falciparum infections were not affected when RES females were exposed to permethrin, these females had decreased lipid abundance in the fat body following exposure, pointing to a possible role for lipid mobilization in response to damage caused by insecticide challenge. The finding that selection for insecticide resistance can increase P. falciparum infection intensities and growth rate reinforces the need to assess the overall impact on malaria transmission dynamics caused by selective pressures mosquitoes experience during repeated insecticide challenge.
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spelling pubmed-103130432023-07-01 Selection for insecticide resistance can promote Plasmodium falciparum infection in Anopheles Adams, Kelsey L. Selland, Emily K. Willett, Bailey C. Carew, John W. Vidoudez, Charles Singh, Naresh Catteruccia, Flaminia PLoS Pathog Research Article Insecticide resistance is under strong selective pressure in Anopheles mosquitoes due to widespread usage of insecticides in vector control strategies. Resistance mechanisms likely cause changes that profoundly affect mosquito physiology, yet it remains poorly understood how selective pressures imposed by insecticides may alter the ability of the mosquito to host and transmit a Plasmodium infection. From pyrethroid-resistant field-derived Anopheles gambiae s.l. mosquitoes, we established resistant (RES) and susceptible (SUS) colonies by either selection for, or loss of insecticide resistance. We show increased oocyst intensity and growth rate as well as increased sporozoite prevalence and intensity in RES compared to SUS females infected with Plasmodium falciparum. The increase in infection intensity in RES females was not associated with the presence of the kdrL1014F mutation and was not impacted by inhibition of Cytochrome P450s. The lipid transporter lipophorin (Lp), which was upregulated in RES compared to SUS, was at least partly implicated in the increased intensity of P. falciparum but not directly involved in the insecticide resistance phenotype. Interestingly, we observed that although P. falciparum infections were not affected when RES females were exposed to permethrin, these females had decreased lipid abundance in the fat body following exposure, pointing to a possible role for lipid mobilization in response to damage caused by insecticide challenge. The finding that selection for insecticide resistance can increase P. falciparum infection intensities and growth rate reinforces the need to assess the overall impact on malaria transmission dynamics caused by selective pressures mosquitoes experience during repeated insecticide challenge. Public Library of Science 2023-06-20 /pmc/articles/PMC10313043/ /pubmed/37339122 http://dx.doi.org/10.1371/journal.ppat.1011448 Text en © 2023 Adams et al https://creativecommons.org/licenses/by/4.0/This is an open access article distributed under the terms of the Creative Commons Attribution License (https://creativecommons.org/licenses/by/4.0/) , which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited.
spellingShingle Research Article
Adams, Kelsey L.
Selland, Emily K.
Willett, Bailey C.
Carew, John W.
Vidoudez, Charles
Singh, Naresh
Catteruccia, Flaminia
Selection for insecticide resistance can promote Plasmodium falciparum infection in Anopheles
title Selection for insecticide resistance can promote Plasmodium falciparum infection in Anopheles
title_full Selection for insecticide resistance can promote Plasmodium falciparum infection in Anopheles
title_fullStr Selection for insecticide resistance can promote Plasmodium falciparum infection in Anopheles
title_full_unstemmed Selection for insecticide resistance can promote Plasmodium falciparum infection in Anopheles
title_short Selection for insecticide resistance can promote Plasmodium falciparum infection in Anopheles
title_sort selection for insecticide resistance can promote plasmodium falciparum infection in anopheles
topic Research Article
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC10313043/
https://www.ncbi.nlm.nih.gov/pubmed/37339122
http://dx.doi.org/10.1371/journal.ppat.1011448
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