Multiple Wolbachia strains provide comparative levels of protection against dengue virus infection in Aedes aegypti

The insect bacterium Wolbachia pipientis is being introgressed into Aedes aegypti populations as an intervention against the transmission of medically important arboviruses. Here we compare Ae. aegypti mosquitoes infected with wMelCS or wAlbB to the widely used wMel Wolbachia strain on an Australian...

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Veröffentlicht in:PLoS pathogens 2020-04, Vol.16 (4), p.e1008433-e1008433
Hauptverfasser: Flores, Heather A, Taneja de Bruyne, Jyotika, O'Donnell, Tanya B, Tuyet Nhu, Vu, Thi Giang, Nguyen, Thi Xuan Trang, Huynh, Thi Thuy Van, Huynh, Thi Long, Vo, Thi Dui, Le, Le Anh Huy, Huynh, Thi Le Duyen, Huynh, Thi Van Thuy, Nguyen, Thanh Phong, Nguyen, Van Vinh Chau, Nguyen, Thi Hue Kien, Duong, Thuy Vi, Tran, Wills, Bridget, O'Neill, Scott L, Simmons, Cameron P, Carrington, Lauren B
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container_issue 4
container_start_page e1008433
container_title PLoS pathogens
container_volume 16
creator Flores, Heather A
Taneja de Bruyne, Jyotika
O'Donnell, Tanya B
Tuyet Nhu, Vu
Thi Giang, Nguyen
Thi Xuan Trang, Huynh
Thi Thuy Van, Huynh
Thi Long, Vo
Thi Dui, Le
Le Anh Huy, Huynh
Thi Le Duyen, Huynh
Thi Van Thuy, Nguyen
Thanh Phong, Nguyen
Van Vinh Chau, Nguyen
Thi Hue Kien, Duong
Thuy Vi, Tran
Wills, Bridget
O'Neill, Scott L
Simmons, Cameron P
Carrington, Lauren B
description The insect bacterium Wolbachia pipientis is being introgressed into Aedes aegypti populations as an intervention against the transmission of medically important arboviruses. Here we compare Ae. aegypti mosquitoes infected with wMelCS or wAlbB to the widely used wMel Wolbachia strain on an Australian nuclear genetic background for their susceptibility to infection by dengue virus (DENV) genotypes spanning all four serotypes. All Wolbachia-infected mosquitoes were more resistant to intrathoracic DENV challenge than their wildtype counterparts. Blocking of DENV replication was greatest by wMelCS. Conversely, wAlbB-infected mosquitoes were more susceptible to whole body infection than wMel and wMelCS. We extended these findings via mosquito oral feeding experiments, using viremic blood from 36 acute, hospitalised dengue cases in Vietnam, additionally including wMel and wildtype mosquitoes on a Vietnamese nuclear genetic background. As above, wAlbB was less effective at blocking DENV replication in the abdomen compared to wMel and wMelCS. The transmission potential of all Wolbachia-infected mosquito lines (measured by the presence/absence of infectious DENV in mosquito saliva) after 14 days, was significantly reduced compared to their wildtype counterparts, and lowest for wMelCS and wAlbB. These data support the use of wAlbB and wMelCS strains for introgression field trials and the biocontrol of DENV transmission. Furthermore, despite observing significant differences in transmission potential between wildtype mosquitoes from Australia and Vietnam, no difference was observed between wMel-infected mosquitoes from each background suggesting that Wolbachia may override any underlying variation in DENV transmission potential.
doi_str_mv 10.1371/journal.ppat.1008433
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The transmission potential of all Wolbachia-infected mosquito lines (measured by the presence/absence of infectious DENV in mosquito saliva) after 14 days, was significantly reduced compared to their wildtype counterparts, and lowest for wMelCS and wAlbB. These data support the use of wAlbB and wMelCS strains for introgression field trials and the biocontrol of DENV transmission. 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Furthermore, despite observing significant differences in transmission potential between wildtype mosquitoes from Australia and Vietnam, no difference was observed between wMel-infected mosquitoes from each background suggesting that Wolbachia may override any underlying variation in DENV transmission potential.</description><subject>Aedes aegypti</subject><subject>Aquatic insects</subject><subject>Australia</subject><subject>Biological control</subject><subject>Biological pest control</subject><subject>Biology and Life Sciences</subject><subject>Comparative analysis</subject><subject>Culicidae</subject><subject>Dengue</subject><subject>Dengue fever</subject><subject>Dengue virus</subject><subject>Disease susceptibility</subject><subject>Disease transmission</subject><subject>Diseases</subject><subject>Genetic aspects</subject><subject>Genotypes</subject><subject>Health aspects</subject><subject>Infection</subject><subject>Infections</subject><subject>Insects</subject><subject>Medicine and Health Sciences</subject><subject>Mosquitoes</subject><subject>Replication</subject><subject>Research and Analysis Methods</subject><subject>Saliva</subject><subject>Serotypes</subject><subject>Strains (organisms)</subject><subject>Tropical diseases</subject><subject>Vector-borne diseases</subject><subject>Vietnam</subject><subject>Virus diseases</subject><subject>Viruses</subject><subject>Wolbachia</subject><issn>1553-7374</issn><issn>1553-7366</issn><issn>1553-7374</issn><fulltext>true</fulltext><rsrctype>article</rsrctype><creationdate>2020</creationdate><recordtype>article</recordtype><sourceid>BENPR</sourceid><sourceid>DOA</sourceid><recordid>eNqVkk1v1DAQhiMEoqXwDxBY4gKHXfyVdXJBWlV8rFRA4kMcLceepF5549R2VvTf47Bp1UW9IB9seZ55x_N6iuI5wUvCBHm79WPolVsOg0pLgnHFGXtQnJKyZAvBBH9453xSPIlxizEnjKweFyeM0opWK3paxM-jS3ZwgH551yh9aRWKKSjbRzQEv7cGkPa7QQWV7B6Qgz24iHw7RRPoZH2PVDfxCRnouxHQ3oYxItu3c9j2aA0GIlLQXQ_JPi0etcpFeDbvZ8XPD-9_nH9aXHz9uDlfXyy0oCIthGmNMWWFa4Kp4QIbZUSrTC0Ar5pGU04I40oxDQ01xCjSgAAAQwFzrEt2Vrw86A7ORzn7FSXlmAmx4ngiNgfCeLWVQ7A7Fa6lV1b-vfChkyokqx3IrK0FI5jkrjipdYUbzjQ1lHBFlWZZ691cbWx2YDT02UZ3JHoc6e2l7PxeCiLqmtVZ4PUsEPzVCDHJnY0anFM9-DG_m1W1wNUBffUPen93M9Wp3ED-D5_r6klUrleUlrguy4la3kPlZWBnte-htfn-KOHNUUJmEvxOnRpjlJvv3_6D_XLM8gOrg48xQHvrHcFyGvmbJuU08nIe-Zz24q7vt0k3M87-ALiW_5s</recordid><startdate>20200413</startdate><enddate>20200413</enddate><creator>Flores, Heather A</creator><creator>Taneja de Bruyne, Jyotika</creator><creator>O'Donnell, Tanya B</creator><creator>Tuyet Nhu, Vu</creator><creator>Thi Giang, Nguyen</creator><creator>Thi Xuan Trang, Huynh</creator><creator>Thi Thuy Van, Huynh</creator><creator>Thi Long, Vo</creator><creator>Thi Dui, Le</creator><creator>Le Anh Huy, Huynh</creator><creator>Thi Le Duyen, Huynh</creator><creator>Thi Van Thuy, Nguyen</creator><creator>Thanh Phong, Nguyen</creator><creator>Van Vinh Chau, Nguyen</creator><creator>Thi Hue Kien, Duong</creator><creator>Thuy Vi, Tran</creator><creator>Wills, Bridget</creator><creator>O'Neill, Scott L</creator><creator>Simmons, Cameron P</creator><creator>Carrington, Lauren B</creator><general>Public Library of Science</general><general>Public Library of Science (PLoS)</general><scope>NPM</scope><scope>AAYXX</scope><scope>CITATION</scope><scope>ISN</scope><scope>ISR</scope><scope>3V.</scope><scope>7QL</scope><scope>7U9</scope><scope>7X7</scope><scope>7XB</scope><scope>88E</scope><scope>8FE</scope><scope>8FH</scope><scope>8FI</scope><scope>8FJ</scope><scope>8FK</scope><scope>ABUWG</scope><scope>AEUYN</scope><scope>AFKRA</scope><scope>AZQEC</scope><scope>BBNVY</scope><scope>BENPR</scope><scope>BHPHI</scope><scope>C1K</scope><scope>CCPQU</scope><scope>DWQXO</scope><scope>FYUFA</scope><scope>GHDGH</scope><scope>GNUQQ</scope><scope>H94</scope><scope>HCIFZ</scope><scope>K9.</scope><scope>LK8</scope><scope>M0S</scope><scope>M1P</scope><scope>M7P</scope><scope>PHGZM</scope><scope>PHGZT</scope><scope>PIMPY</scope><scope>PJZUB</scope><scope>PKEHL</scope><scope>PPXIY</scope><scope>PQEST</scope><scope>PQGLB</scope><scope>PQQKQ</scope><scope>PQUKI</scope><scope>7X8</scope><scope>5PM</scope><scope>DOA</scope><orcidid>https://orcid.org/0000-0001-9273-7912</orcidid><orcidid>https://orcid.org/0000-0001-7298-5724</orcidid><orcidid>https://orcid.org/0000-0001-9086-8804</orcidid><orcidid>https://orcid.org/0000-0001-5003-7547</orcidid><orcidid>https://orcid.org/0000-0003-4668-1019</orcidid><orcidid>https://orcid.org/0000-0002-4131-3615</orcidid></search><sort><creationdate>20200413</creationdate><title>Multiple Wolbachia strains provide comparative levels of protection against dengue virus infection in Aedes aegypti</title><author>Flores, Heather A ; Taneja de Bruyne, Jyotika ; O'Donnell, Tanya B ; Tuyet Nhu, Vu ; Thi Giang, Nguyen ; Thi Xuan Trang, Huynh ; Thi Thuy Van, Huynh ; Thi Long, Vo ; Thi Dui, Le ; Le Anh Huy, Huynh ; Thi Le Duyen, Huynh ; Thi Van Thuy, Nguyen ; Thanh Phong, Nguyen ; Van Vinh Chau, Nguyen ; Thi Hue Kien, Duong ; Thuy Vi, Tran ; Wills, Bridget ; O'Neill, Scott L ; Simmons, Cameron P ; Carrington, Lauren B</author></sort><facets><frbrtype>5</frbrtype><frbrgroupid>cdi_FETCH-LOGICAL-c727t-7dfddd5809102d470dad7fad97e06bbc241134aa3ceb2d1da1be7eeed2e040c53</frbrgroupid><rsrctype>articles</rsrctype><prefilter>articles</prefilter><language>eng</language><creationdate>2020</creationdate><topic>Aedes aegypti</topic><topic>Aquatic insects</topic><topic>Australia</topic><topic>Biological control</topic><topic>Biological pest control</topic><topic>Biology and Life Sciences</topic><topic>Comparative analysis</topic><topic>Culicidae</topic><topic>Dengue</topic><topic>Dengue fever</topic><topic>Dengue virus</topic><topic>Disease susceptibility</topic><topic>Disease transmission</topic><topic>Diseases</topic><topic>Genetic aspects</topic><topic>Genotypes</topic><topic>Health aspects</topic><topic>Infection</topic><topic>Infections</topic><topic>Insects</topic><topic>Medicine and Health Sciences</topic><topic>Mosquitoes</topic><topic>Replication</topic><topic>Research and Analysis Methods</topic><topic>Saliva</topic><topic>Serotypes</topic><topic>Strains (organisms)</topic><topic>Tropical diseases</topic><topic>Vector-borne diseases</topic><topic>Vietnam</topic><topic>Virus diseases</topic><topic>Viruses</topic><topic>Wolbachia</topic><toplevel>peer_reviewed</toplevel><toplevel>online_resources</toplevel><creatorcontrib>Flores, Heather A</creatorcontrib><creatorcontrib>Taneja de Bruyne, Jyotika</creatorcontrib><creatorcontrib>O'Donnell, Tanya B</creatorcontrib><creatorcontrib>Tuyet Nhu, Vu</creatorcontrib><creatorcontrib>Thi Giang, Nguyen</creatorcontrib><creatorcontrib>Thi Xuan Trang, Huynh</creatorcontrib><creatorcontrib>Thi Thuy Van, Huynh</creatorcontrib><creatorcontrib>Thi Long, Vo</creatorcontrib><creatorcontrib>Thi Dui, Le</creatorcontrib><creatorcontrib>Le Anh Huy, Huynh</creatorcontrib><creatorcontrib>Thi Le Duyen, Huynh</creatorcontrib><creatorcontrib>Thi Van Thuy, Nguyen</creatorcontrib><creatorcontrib>Thanh Phong, Nguyen</creatorcontrib><creatorcontrib>Van Vinh Chau, Nguyen</creatorcontrib><creatorcontrib>Thi Hue Kien, Duong</creatorcontrib><creatorcontrib>Thuy Vi, Tran</creatorcontrib><creatorcontrib>Wills, Bridget</creatorcontrib><creatorcontrib>O'Neill, Scott L</creatorcontrib><creatorcontrib>Simmons, Cameron P</creatorcontrib><creatorcontrib>Carrington, Lauren B</creatorcontrib><collection>PubMed</collection><collection>CrossRef</collection><collection>Gale In Context: Canada</collection><collection>Gale In Context: Science</collection><collection>ProQuest Central (Corporate)</collection><collection>Bacteriology Abstracts (Microbiology B)</collection><collection>Virology and AIDS Abstracts</collection><collection>Health &amp; 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Here we compare Ae. aegypti mosquitoes infected with wMelCS or wAlbB to the widely used wMel Wolbachia strain on an Australian nuclear genetic background for their susceptibility to infection by dengue virus (DENV) genotypes spanning all four serotypes. All Wolbachia-infected mosquitoes were more resistant to intrathoracic DENV challenge than their wildtype counterparts. Blocking of DENV replication was greatest by wMelCS. Conversely, wAlbB-infected mosquitoes were more susceptible to whole body infection than wMel and wMelCS. We extended these findings via mosquito oral feeding experiments, using viremic blood from 36 acute, hospitalised dengue cases in Vietnam, additionally including wMel and wildtype mosquitoes on a Vietnamese nuclear genetic background. As above, wAlbB was less effective at blocking DENV replication in the abdomen compared to wMel and wMelCS. The transmission potential of all Wolbachia-infected mosquito lines (measured by the presence/absence of infectious DENV in mosquito saliva) after 14 days, was significantly reduced compared to their wildtype counterparts, and lowest for wMelCS and wAlbB. These data support the use of wAlbB and wMelCS strains for introgression field trials and the biocontrol of DENV transmission. Furthermore, despite observing significant differences in transmission potential between wildtype mosquitoes from Australia and Vietnam, no difference was observed between wMel-infected mosquitoes from each background suggesting that Wolbachia may override any underlying variation in DENV transmission potential.</abstract><cop>United States</cop><pub>Public Library of Science</pub><pmid>32282862</pmid><doi>10.1371/journal.ppat.1008433</doi><orcidid>https://orcid.org/0000-0001-9273-7912</orcidid><orcidid>https://orcid.org/0000-0001-7298-5724</orcidid><orcidid>https://orcid.org/0000-0001-9086-8804</orcidid><orcidid>https://orcid.org/0000-0001-5003-7547</orcidid><orcidid>https://orcid.org/0000-0003-4668-1019</orcidid><orcidid>https://orcid.org/0000-0002-4131-3615</orcidid><oa>free_for_read</oa></addata></record>
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identifier ISSN: 1553-7374
ispartof PLoS pathogens, 2020-04, Vol.16 (4), p.e1008433-e1008433
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1553-7374
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source Public Library of Science (PLoS) Journals Open Access; DOAJ Directory of Open Access Journals; Elektronische Zeitschriftenbibliothek - Frei zugängliche E-Journals; PubMed Central; PubMed Central Open Access
subjects Aedes aegypti
Aquatic insects
Australia
Biological control
Biological pest control
Biology and Life Sciences
Comparative analysis
Culicidae
Dengue
Dengue fever
Dengue virus
Disease susceptibility
Disease transmission
Diseases
Genetic aspects
Genotypes
Health aspects
Infection
Infections
Insects
Medicine and Health Sciences
Mosquitoes
Replication
Research and Analysis Methods
Saliva
Serotypes
Strains (organisms)
Tropical diseases
Vector-borne diseases
Vietnam
Virus diseases
Viruses
Wolbachia
title Multiple Wolbachia strains provide comparative levels of protection against dengue virus infection in Aedes aegypti
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