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The salivary protein Saglin facilitates efficient midgut colonization of Anopheles mosquitoes by malaria parasites

Malaria is caused by the unicellular parasite Plasmodium which is transmitted to humans through the bite of infected female Anopheles mosquitoes. To initiate sexual reproduction and to infect the midgut of the mosquito, Plasmodium gametocytes are able to recognize the intestinal environment after be...

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Autores principales: Klug, Dennis, Gautier, Amandine, Calvo, Eric, Marois, Eric, Blandin, Stéphanie A.
Formato: Online Artículo Texto
Lenguaje:English
Publicado: Public Library of Science 2023
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC10013899/
https://www.ncbi.nlm.nih.gov/pubmed/36862755
http://dx.doi.org/10.1371/journal.ppat.1010538
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author Klug, Dennis
Gautier, Amandine
Calvo, Eric
Marois, Eric
Blandin, Stéphanie A.
author_facet Klug, Dennis
Gautier, Amandine
Calvo, Eric
Marois, Eric
Blandin, Stéphanie A.
author_sort Klug, Dennis
collection PubMed
description Malaria is caused by the unicellular parasite Plasmodium which is transmitted to humans through the bite of infected female Anopheles mosquitoes. To initiate sexual reproduction and to infect the midgut of the mosquito, Plasmodium gametocytes are able to recognize the intestinal environment after being ingested during blood feeding. A shift in temperature, pH change and the presence of the insect-specific compound xanthurenic acid have been shown to be important stimuli perceived by gametocytes to become activated and proceed to sexual reproduction. Here we report that the salivary protein Saglin, previously proposed to be a receptor for the recognition of salivary glands by sporozoites, facilitates Plasmodium colonization of the mosquito midgut, but does not contribute to salivary gland invasion. In mosquito mutants lacking Saglin, Plasmodium infection of Anopheles females is reduced, resulting in impaired transmission of sporozoites at low infection densities. Interestingly, Saglin can be detected in high amounts in the midgut of mosquitoes after blood ingestion, possibly indicating a previously unknown host-pathogen interaction between Saglin and midgut stages of Plasmodium. Furthermore, we were able to show that saglin deletion has no fitness cost in laboratory conditions, suggesting this gene would be an interesting target for gene drive approaches.
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spelling pubmed-100138992023-03-15 The salivary protein Saglin facilitates efficient midgut colonization of Anopheles mosquitoes by malaria parasites Klug, Dennis Gautier, Amandine Calvo, Eric Marois, Eric Blandin, Stéphanie A. PLoS Pathog Research Article Malaria is caused by the unicellular parasite Plasmodium which is transmitted to humans through the bite of infected female Anopheles mosquitoes. To initiate sexual reproduction and to infect the midgut of the mosquito, Plasmodium gametocytes are able to recognize the intestinal environment after being ingested during blood feeding. A shift in temperature, pH change and the presence of the insect-specific compound xanthurenic acid have been shown to be important stimuli perceived by gametocytes to become activated and proceed to sexual reproduction. Here we report that the salivary protein Saglin, previously proposed to be a receptor for the recognition of salivary glands by sporozoites, facilitates Plasmodium colonization of the mosquito midgut, but does not contribute to salivary gland invasion. In mosquito mutants lacking Saglin, Plasmodium infection of Anopheles females is reduced, resulting in impaired transmission of sporozoites at low infection densities. Interestingly, Saglin can be detected in high amounts in the midgut of mosquitoes after blood ingestion, possibly indicating a previously unknown host-pathogen interaction between Saglin and midgut stages of Plasmodium. Furthermore, we were able to show that saglin deletion has no fitness cost in laboratory conditions, suggesting this gene would be an interesting target for gene drive approaches. Public Library of Science 2023-03-02 /pmc/articles/PMC10013899/ /pubmed/36862755 http://dx.doi.org/10.1371/journal.ppat.1010538 Text en https://creativecommons.org/publicdomain/zero/1.0/This is an open access article, free of all copyright, and may be freely reproduced, distributed, transmitted, modified, built upon, or otherwise used by anyone for any lawful purpose. The work is made available under the Creative Commons CC0 (https://creativecommons.org/publicdomain/zero/1.0/) public domain dedication.
spellingShingle Research Article
Klug, Dennis
Gautier, Amandine
Calvo, Eric
Marois, Eric
Blandin, Stéphanie A.
The salivary protein Saglin facilitates efficient midgut colonization of Anopheles mosquitoes by malaria parasites
title The salivary protein Saglin facilitates efficient midgut colonization of Anopheles mosquitoes by malaria parasites
title_full The salivary protein Saglin facilitates efficient midgut colonization of Anopheles mosquitoes by malaria parasites
title_fullStr The salivary protein Saglin facilitates efficient midgut colonization of Anopheles mosquitoes by malaria parasites
title_full_unstemmed The salivary protein Saglin facilitates efficient midgut colonization of Anopheles mosquitoes by malaria parasites
title_short The salivary protein Saglin facilitates efficient midgut colonization of Anopheles mosquitoes by malaria parasites
title_sort salivary protein saglin facilitates efficient midgut colonization of anopheles mosquitoes by malaria parasites
topic Research Article
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC10013899/
https://www.ncbi.nlm.nih.gov/pubmed/36862755
http://dx.doi.org/10.1371/journal.ppat.1010538
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