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Family level variation in Wolbachia-mediated dengue virus blocking in Aedes aegypti

BACKGROUND: The mosquito vector Aedes aegypti is responsible for transmitting a range of arboviruses including dengue (DENV) and Zika (ZIKV). The global reach of these viruses is increasing due to an expansion of the mosquito’s geographic range and increasing urbanization and human travel. Vector co...

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Autores principales: Terradas, Gerard, Allen, Scott L., Chenoweth, Stephen F., McGraw, Elizabeth A.
Formato: Online Artículo Texto
Lenguaje:English
Publicado: BioMed Central 2017
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC5746003/
https://www.ncbi.nlm.nih.gov/pubmed/29282144
http://dx.doi.org/10.1186/s13071-017-2589-3
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author Terradas, Gerard
Allen, Scott L.
Chenoweth, Stephen F.
McGraw, Elizabeth A.
author_facet Terradas, Gerard
Allen, Scott L.
Chenoweth, Stephen F.
McGraw, Elizabeth A.
author_sort Terradas, Gerard
collection PubMed
description BACKGROUND: The mosquito vector Aedes aegypti is responsible for transmitting a range of arboviruses including dengue (DENV) and Zika (ZIKV). The global reach of these viruses is increasing due to an expansion of the mosquito’s geographic range and increasing urbanization and human travel. Vector control remains the primary means for limiting these diseases. Wolbachia pipientis is an endosymbiotic bacterium of insects that has the ability to block the replication of pathogens, including flaviviruses such as DENV or ZIKV, inside the body of the vector. A strain of Wolbachia called wMel is currently being released into wild mosquito populations to test its potential to limit virus transmission to humans. The mechanism that underpins the virus blocking effect, however, remains elusive. METHODS: We used a modified full-sib breeding design in conjunction with vector competence assays in wildtype and wMel-infected Aedes aegypti collected from the field. All individuals were injected with DENV-2 intrathoracically at 5–6 days of age. Tissues were dissected 7 days post-infection to allow quantification of DENV and Wolbachia loads. RESULTS: We show the first evidence of family level variation in Wolbachia-mediated blocking in mosquitoes. This variation may stem from either genetic contributions from the mosquito and Wolbachia genomes or environmental influences on Wolbachia. In these families, we also tested for correlations between strength of blocking and expression level for several insect immunity genes with possible roles in blocking, identifying two genes of interest (AGO2 and SCP-2). CONCLUSIONS: In this study we show variation in Wolbachia-mediated DENV blocking in Aedes aegypti that may arise from genetic contributions and environmental influences on the mosquito-Wolbachia association. This suggests that Wolbachia-mediated blocking may have the ability to evolve through time or be expressed differentially across environments. The long-term efficacy of Wolbachia in the field will be dependent on the stability of blocking. Understanding the mechanism of blocking will be necessary for successful development of strategies that counter the emergence of evolved resistance or variation in its expression under diverse field conditions. ELECTRONIC SUPPLEMENTARY MATERIAL: The online version of this article (10.1186/s13071-017-2589-3) contains supplementary material, which is available to authorized users.
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spelling pubmed-57460032018-01-03 Family level variation in Wolbachia-mediated dengue virus blocking in Aedes aegypti Terradas, Gerard Allen, Scott L. Chenoweth, Stephen F. McGraw, Elizabeth A. Parasit Vectors Research BACKGROUND: The mosquito vector Aedes aegypti is responsible for transmitting a range of arboviruses including dengue (DENV) and Zika (ZIKV). The global reach of these viruses is increasing due to an expansion of the mosquito’s geographic range and increasing urbanization and human travel. Vector control remains the primary means for limiting these diseases. Wolbachia pipientis is an endosymbiotic bacterium of insects that has the ability to block the replication of pathogens, including flaviviruses such as DENV or ZIKV, inside the body of the vector. A strain of Wolbachia called wMel is currently being released into wild mosquito populations to test its potential to limit virus transmission to humans. The mechanism that underpins the virus blocking effect, however, remains elusive. METHODS: We used a modified full-sib breeding design in conjunction with vector competence assays in wildtype and wMel-infected Aedes aegypti collected from the field. All individuals were injected with DENV-2 intrathoracically at 5–6 days of age. Tissues were dissected 7 days post-infection to allow quantification of DENV and Wolbachia loads. RESULTS: We show the first evidence of family level variation in Wolbachia-mediated blocking in mosquitoes. This variation may stem from either genetic contributions from the mosquito and Wolbachia genomes or environmental influences on Wolbachia. In these families, we also tested for correlations between strength of blocking and expression level for several insect immunity genes with possible roles in blocking, identifying two genes of interest (AGO2 and SCP-2). CONCLUSIONS: In this study we show variation in Wolbachia-mediated DENV blocking in Aedes aegypti that may arise from genetic contributions and environmental influences on the mosquito-Wolbachia association. This suggests that Wolbachia-mediated blocking may have the ability to evolve through time or be expressed differentially across environments. The long-term efficacy of Wolbachia in the field will be dependent on the stability of blocking. Understanding the mechanism of blocking will be necessary for successful development of strategies that counter the emergence of evolved resistance or variation in its expression under diverse field conditions. ELECTRONIC SUPPLEMENTARY MATERIAL: The online version of this article (10.1186/s13071-017-2589-3) contains supplementary material, which is available to authorized users. BioMed Central 2017-12-28 /pmc/articles/PMC5746003/ /pubmed/29282144 http://dx.doi.org/10.1186/s13071-017-2589-3 Text en © The Author(s). 2017 Open AccessThis article is distributed under the terms of the Creative Commons Attribution 4.0 International License (http://creativecommons.org/licenses/by/4.0/), which permits unrestricted use, distribution, and reproduction in any medium, provided you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons license, and indicate if changes were made. The Creative Commons Public Domain Dedication waiver (http://creativecommons.org/publicdomain/zero/1.0/) applies to the data made available in this article, unless otherwise stated.
spellingShingle Research
Terradas, Gerard
Allen, Scott L.
Chenoweth, Stephen F.
McGraw, Elizabeth A.
Family level variation in Wolbachia-mediated dengue virus blocking in Aedes aegypti
title Family level variation in Wolbachia-mediated dengue virus blocking in Aedes aegypti
title_full Family level variation in Wolbachia-mediated dengue virus blocking in Aedes aegypti
title_fullStr Family level variation in Wolbachia-mediated dengue virus blocking in Aedes aegypti
title_full_unstemmed Family level variation in Wolbachia-mediated dengue virus blocking in Aedes aegypti
title_short Family level variation in Wolbachia-mediated dengue virus blocking in Aedes aegypti
title_sort family level variation in wolbachia-mediated dengue virus blocking in aedes aegypti
topic Research
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC5746003/
https://www.ncbi.nlm.nih.gov/pubmed/29282144
http://dx.doi.org/10.1186/s13071-017-2589-3
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