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Mosquito densovirus significantly reduces the vector susceptibility to dengue virus serotype 2 in Aedes albopictus mosquitoes (Diptera: Culicidae)

BACKGROUND: Dengue virus (DENV) is a major public health threat, with Aedes albopictus being the confirmed vector responsible for dengue epidemics in Guangzhou, China. Mosquito densoviruses (MDVs) are pathogenic mosquito-specific viruses, and a novel MDV was previously isolated from Ae. albopictus i...

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Autores principales: Kong, Ling, Xiao, Jie, Yang, Lu, Sui, Yuan, Wang, Duoquan, Chen, Shaoqiang, Liu, Peiwen, Chen, Xiao-Guang, Gu, Jinbao
Formato: Online Artículo Texto
Lenguaje:English
Publicado: BioMed Central 2023
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC10169196/
https://www.ncbi.nlm.nih.gov/pubmed/37161462
http://dx.doi.org/10.1186/s40249-023-01099-8
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author Kong, Ling
Xiao, Jie
Yang, Lu
Sui, Yuan
Wang, Duoquan
Chen, Shaoqiang
Liu, Peiwen
Chen, Xiao-Guang
Gu, Jinbao
author_facet Kong, Ling
Xiao, Jie
Yang, Lu
Sui, Yuan
Wang, Duoquan
Chen, Shaoqiang
Liu, Peiwen
Chen, Xiao-Guang
Gu, Jinbao
author_sort Kong, Ling
collection PubMed
description BACKGROUND: Dengue virus (DENV) is a major public health threat, with Aedes albopictus being the confirmed vector responsible for dengue epidemics in Guangzhou, China. Mosquito densoviruses (MDVs) are pathogenic mosquito-specific viruses, and a novel MDV was previously isolated from Ae. albopictus in Guangzhou. This study aims to determine the prevalence of MDVs in wild Ae. albopictus populations and investigate their potential interactions with DENV and impact on vector susceptibility for DENV. METHODS: The prevalence of MDV in wild mosquitoes in China was investigated using open access sequencing data and PCR detection in Ae. albopictus in Guangzhou. The viral infection rate and titers in MDV-persistent C6/36 cells were evaluated at 12, 24, 48, 72, 96, and 120 h post infection (hpi) by indirect immunofluorescence assay (IFA) and real time quantitative PCR (RT-qPCR). The midgut infection rate (MIR), dissemination rate (DR), and salivary gland infection rate (SGIR) in various tissues of MDV-infected mosquitoes were detected and quantified at 0, 5, 10, and 15 days post infection (dpi) by RT-PCR and RT-qPCR. The chi-square test evaluated dengue virus serotype 2 (DENV-2) and Aedes aegypti densovirus (AaeDV) infection rates and related indices in mosquitoes, while Tukey's LSD and t-tests compared viral titers in C6/36 cells and tissues over time. RESULTS: The results revealed a relatively wide distribution of MDVs in Aedes, Culex, and Anopheles mosquitoes in China and an over 68% positive rate. In vitro, significant reductions in DENV-2 titers in supernatant at 120 hpi, and an apparent decrease in DENV-2-positive cells at 96 and 120 hpi were observed. In vivo, DENV-2 in the ovaries and salivary glands was first detected at 10 dpi in both monoinfected and superinfected Ae. albopictus females, while MDV superinfection with DENV-2 suppressed the salivary gland infection rate at 15 dpi. DENV-2 titer in the ovary and salivary glands of Ae. albopictus was reduced in superinfected mosquitoes at 15 dpi. CONCLUSIONS: MDVs is widespread in natural mosquito populations, and replication of DENV-2 is suppressed in MDV-infected Ae. albopictus, thus reducing vector susceptibility to DENV-2. Our study supports the hypothesis that MDVs may contribute to reducing transmission of DENV and provides an alternative strategy for mosquito-transmitted disease control. GRAPHICAL ABSTRACT: [Image: see text] SUPPLEMENTARY INFORMATION: The online version contains supplementary material available at 10.1186/s40249-023-01099-8.
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spelling pubmed-101691962023-05-11 Mosquito densovirus significantly reduces the vector susceptibility to dengue virus serotype 2 in Aedes albopictus mosquitoes (Diptera: Culicidae) Kong, Ling Xiao, Jie Yang, Lu Sui, Yuan Wang, Duoquan Chen, Shaoqiang Liu, Peiwen Chen, Xiao-Guang Gu, Jinbao Infect Dis Poverty Research Article BACKGROUND: Dengue virus (DENV) is a major public health threat, with Aedes albopictus being the confirmed vector responsible for dengue epidemics in Guangzhou, China. Mosquito densoviruses (MDVs) are pathogenic mosquito-specific viruses, and a novel MDV was previously isolated from Ae. albopictus in Guangzhou. This study aims to determine the prevalence of MDVs in wild Ae. albopictus populations and investigate their potential interactions with DENV and impact on vector susceptibility for DENV. METHODS: The prevalence of MDV in wild mosquitoes in China was investigated using open access sequencing data and PCR detection in Ae. albopictus in Guangzhou. The viral infection rate and titers in MDV-persistent C6/36 cells were evaluated at 12, 24, 48, 72, 96, and 120 h post infection (hpi) by indirect immunofluorescence assay (IFA) and real time quantitative PCR (RT-qPCR). The midgut infection rate (MIR), dissemination rate (DR), and salivary gland infection rate (SGIR) in various tissues of MDV-infected mosquitoes were detected and quantified at 0, 5, 10, and 15 days post infection (dpi) by RT-PCR and RT-qPCR. The chi-square test evaluated dengue virus serotype 2 (DENV-2) and Aedes aegypti densovirus (AaeDV) infection rates and related indices in mosquitoes, while Tukey's LSD and t-tests compared viral titers in C6/36 cells and tissues over time. RESULTS: The results revealed a relatively wide distribution of MDVs in Aedes, Culex, and Anopheles mosquitoes in China and an over 68% positive rate. In vitro, significant reductions in DENV-2 titers in supernatant at 120 hpi, and an apparent decrease in DENV-2-positive cells at 96 and 120 hpi were observed. In vivo, DENV-2 in the ovaries and salivary glands was first detected at 10 dpi in both monoinfected and superinfected Ae. albopictus females, while MDV superinfection with DENV-2 suppressed the salivary gland infection rate at 15 dpi. DENV-2 titer in the ovary and salivary glands of Ae. albopictus was reduced in superinfected mosquitoes at 15 dpi. CONCLUSIONS: MDVs is widespread in natural mosquito populations, and replication of DENV-2 is suppressed in MDV-infected Ae. albopictus, thus reducing vector susceptibility to DENV-2. Our study supports the hypothesis that MDVs may contribute to reducing transmission of DENV and provides an alternative strategy for mosquito-transmitted disease control. GRAPHICAL ABSTRACT: [Image: see text] SUPPLEMENTARY INFORMATION: The online version contains supplementary material available at 10.1186/s40249-023-01099-8. BioMed Central 2023-05-09 /pmc/articles/PMC10169196/ /pubmed/37161462 http://dx.doi.org/10.1186/s40249-023-01099-8 Text en © The Author(s) 2023 https://creativecommons.org/licenses/by/4.0/Open AccessThis article is licensed under a Creative Commons Attribution 4.0 International License, which permits use, sharing, adaptation, distribution and reproduction in any medium or format, as long as you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons licence, and indicate if changes were made. The images or other third party material in this article are included in the article's Creative Commons licence, unless indicated otherwise in a credit line to the material. If material is not included in the article's Creative Commons licence and your intended use is not permitted by statutory regulation or exceeds the permitted use, you will need to obtain permission directly from the copyright holder. To view a copy of this licence, visit http://creativecommons.org/licenses/by/4.0/ (https://creativecommons.org/licenses/by/4.0/) . The Creative Commons Public Domain Dedication waiver (http://creativecommons.org/publicdomain/zero/1.0/ (https://creativecommons.org/publicdomain/zero/1.0/) ) applies to the data made available in this article, unless otherwise stated in a credit line to the data.
spellingShingle Research Article
Kong, Ling
Xiao, Jie
Yang, Lu
Sui, Yuan
Wang, Duoquan
Chen, Shaoqiang
Liu, Peiwen
Chen, Xiao-Guang
Gu, Jinbao
Mosquito densovirus significantly reduces the vector susceptibility to dengue virus serotype 2 in Aedes albopictus mosquitoes (Diptera: Culicidae)
title Mosquito densovirus significantly reduces the vector susceptibility to dengue virus serotype 2 in Aedes albopictus mosquitoes (Diptera: Culicidae)
title_full Mosquito densovirus significantly reduces the vector susceptibility to dengue virus serotype 2 in Aedes albopictus mosquitoes (Diptera: Culicidae)
title_fullStr Mosquito densovirus significantly reduces the vector susceptibility to dengue virus serotype 2 in Aedes albopictus mosquitoes (Diptera: Culicidae)
title_full_unstemmed Mosquito densovirus significantly reduces the vector susceptibility to dengue virus serotype 2 in Aedes albopictus mosquitoes (Diptera: Culicidae)
title_short Mosquito densovirus significantly reduces the vector susceptibility to dengue virus serotype 2 in Aedes albopictus mosquitoes (Diptera: Culicidae)
title_sort mosquito densovirus significantly reduces the vector susceptibility to dengue virus serotype 2 in aedes albopictus mosquitoes (diptera: culicidae)
topic Research Article
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC10169196/
https://www.ncbi.nlm.nih.gov/pubmed/37161462
http://dx.doi.org/10.1186/s40249-023-01099-8
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