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Host-dependence of in vitro reassortment dynamics among the Sathuperi and Shamonda Simbuviruses
Orthobunyaviruses are arboviruses (Arthropod Borne Virus) and possess multipartite genomes made up of three negative RNAs corresponding to the small (S), medium (M) and large (L) segments. Reassortment and recombination are evolutionary driving forces of such segmented viruses and lead to the emerge...
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Published in: | Emerging microbes & infections 2019-01, Vol.8 (1), p.381-395 |
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creator | Coupeau, Damien Bayrou, Calixte Baillieux, Pierre Marichal, Axel Lenaerts, Anne-Cécile Caty, Céline Wiggers, Laetitia Kirschvink, Nathalie Desmecht, Daniel Muylkens, Benoît |
description | Orthobunyaviruses are arboviruses (Arthropod Borne Virus) and possess multipartite genomes made up of three negative RNAs corresponding to the small (S), medium (M) and large (L) segments. Reassortment and recombination are evolutionary driving forces of such segmented viruses and lead to the emergence of new strains and species. Retrospective studies based on phylogenetical analysis are able to evaluate these mechanisms at the end of the selection process but fail to address the dynamics of emergence. This issue was addressed using two Orthobunyaviruses infecting ruminants and belonging to the Simbu serogroup: the Sathuperi virus (SATV) and the Shamonda virus (SHAV). Both viruses were associated with abortion, stillbirth and congenital malformations occurring after transplacental transmission and were suspected to spread together in different ruminant and insect populations. This study showed that different viruses related to SHAV and SATV are spreading simultaneously in ruminants and equids of the Sub-Saharan region. Their reassortment and recombination potential was evaluated in mammalian and in insect contexts. A method was set up to determine the genomic background of any clonal progeny viruses isolated after in vitro coinfections assays. All the reassortment combinations were generated in both contexts while no recombinant virus was isolated. Progeny virus populations revealed a high level of reassortment in mammalian cells and a much lower level in insect cells. In vitro selection pressure that mimicked the host switching (insect-mammal) revealed that the best adapted reassortant virus was connected with an advantageous replicative fitness and with the presence of a specific segment. |
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Reassortment and recombination are evolutionary driving forces of such segmented viruses and lead to the emergence of new strains and species. Retrospective studies based on phylogenetical analysis are able to evaluate these mechanisms at the end of the selection process but fail to address the dynamics of emergence. This issue was addressed using two Orthobunyaviruses infecting ruminants and belonging to the Simbu serogroup: the Sathuperi virus (SATV) and the Shamonda virus (SHAV). Both viruses were associated with abortion, stillbirth and congenital malformations occurring after transplacental transmission and were suspected to spread together in different ruminant and insect populations. This study showed that different viruses related to SHAV and SATV are spreading simultaneously in ruminants and equids of the Sub-Saharan region. Their reassortment and recombination potential was evaluated in mammalian and in insect contexts. A method was set up to determine the genomic background of any clonal progeny viruses isolated after in vitro coinfections assays. All the reassortment combinations were generated in both contexts while no recombinant virus was isolated. Progeny virus populations revealed a high level of reassortment in mammalian cells and a much lower level in insect cells. In vitro selection pressure that mimicked the host switching (insect-mammal) revealed that the best adapted reassortant virus was connected with an advantageous replicative fitness and with the presence of a specific segment.</description><identifier>ISSN: 2222-1751</identifier><identifier>EISSN: 2222-1751</identifier><identifier>DOI: 10.1080/22221751.2019.1586410</identifier><identifier>PMID: 30896304</identifier><language>eng</language><publisher>United States: Taylor & Francis</publisher><subject><![CDATA[Animals ; arbovirus ; Bunyaviridae Infections - virology ; Cell Line ; Cricetinae ; Insecta ; Life sciences ; Médecine vétérinaire & santé animale ; Orthobunyavirus ; Orthobunyavirus - genetics ; Orthobunyavirus - growth & development ; Orthobunyavirus - isolation & purification ; Orthobunyavirus/genetics/growth & development/isolation & purification ; Reassortant Viruses - genetics ; Reassortant Viruses - growth & development ; Reassortant Viruses - isolation & purification ; Reassortant Viruses/genetics/growth & development/isolation & purification ; reassortment ; recombination ; Recombination, Genetic ; Retrospective Studies ; Sciences du vivant ; Veterinary medicine & animal health ; viral selection ; Viruses]]></subject><ispartof>Emerging microbes & infections, 2019-01, Vol.8 (1), p.381-395</ispartof><rights>2019 The Author(s). Published by Informa UK Limited, trading as Taylor & Francis Group, on behalf of Shanghai Shangyixun Cultural Communication Co., Ltd 2019</rights><rights>2019 The Author(s). Published by Informa UK Limited, trading as Taylor & Francis Group, on behalf of Shanghai Shangyixun Cultural Communication Co., Ltd. This work is licensed under the Creative Commons Attribution License http://creativecommons.org/licenses/by/4.0/ (the “License”). Notwithstanding the ProQuest Terms and Conditions, you may use this content in accordance with the terms of the License.</rights><rights>2019 The Author(s). Published by Informa UK Limited, trading as Taylor & Francis Group, on behalf of Shanghai Shangyixun Cultural Communication Co., Ltd 2019 The Author(s)</rights><lds50>peer_reviewed</lds50><oa>free_for_read</oa><woscitedreferencessubscribed>false</woscitedreferencessubscribed><citedby>FETCH-LOGICAL-c606t-a89869c9fd96096f36b6f9ff7b6c2bec539110fbb9f21c78a0ea88eafbc9b3123</citedby><cites>FETCH-LOGICAL-c606t-a89869c9fd96096f36b6f9ff7b6c2bec539110fbb9f21c78a0ea88eafbc9b3123</cites><orcidid>0000-0002-4636-3996 ; 0000-0001-7058-7757 ; 0000-0001-5616-5099</orcidid></display><links><openurl>$$Topenurl_article</openurl><openurlfulltext>$$Topenurlfull_article</openurlfulltext><thumbnail>$$Tsyndetics_thumb_exl</thumbnail><linktopdf>$$Uhttps://www.ncbi.nlm.nih.gov/pmc/articles/PMC6455117/pdf/$$EPDF$$P50$$Gpubmedcentral$$Hfree_for_read</linktopdf><linktohtml>$$Uhttps://www.proquest.com/docview/2427525424?pq-origsite=primo$$EHTML$$P50$$Gproquest$$Hfree_for_read</linktohtml><link.rule.ids>230,314,727,780,784,885,25753,27502,27924,27925,37012,37013,44590,53791,53793,59143,59144</link.rule.ids><backlink>$$Uhttps://www.ncbi.nlm.nih.gov/pubmed/30896304$$D View this record in MEDLINE/PubMed$$Hfree_for_read</backlink></links><search><creatorcontrib>Coupeau, Damien</creatorcontrib><creatorcontrib>Bayrou, Calixte</creatorcontrib><creatorcontrib>Baillieux, Pierre</creatorcontrib><creatorcontrib>Marichal, Axel</creatorcontrib><creatorcontrib>Lenaerts, Anne-Cécile</creatorcontrib><creatorcontrib>Caty, Céline</creatorcontrib><creatorcontrib>Wiggers, Laetitia</creatorcontrib><creatorcontrib>Kirschvink, Nathalie</creatorcontrib><creatorcontrib>Desmecht, Daniel</creatorcontrib><creatorcontrib>Muylkens, Benoît</creatorcontrib><title>Host-dependence of in vitro reassortment dynamics among the Sathuperi and Shamonda Simbuviruses</title><title>Emerging microbes & infections</title><addtitle>Emerg Microbes Infect</addtitle><description>Orthobunyaviruses are arboviruses (Arthropod Borne Virus) and possess multipartite genomes made up of three negative RNAs corresponding to the small (S), medium (M) and large (L) segments. Reassortment and recombination are evolutionary driving forces of such segmented viruses and lead to the emergence of new strains and species. Retrospective studies based on phylogenetical analysis are able to evaluate these mechanisms at the end of the selection process but fail to address the dynamics of emergence. This issue was addressed using two Orthobunyaviruses infecting ruminants and belonging to the Simbu serogroup: the Sathuperi virus (SATV) and the Shamonda virus (SHAV). Both viruses were associated with abortion, stillbirth and congenital malformations occurring after transplacental transmission and were suspected to spread together in different ruminant and insect populations. This study showed that different viruses related to SHAV and SATV are spreading simultaneously in ruminants and equids of the Sub-Saharan region. Their reassortment and recombination potential was evaluated in mammalian and in insect contexts. A method was set up to determine the genomic background of any clonal progeny viruses isolated after in vitro coinfections assays. All the reassortment combinations were generated in both contexts while no recombinant virus was isolated. Progeny virus populations revealed a high level of reassortment in mammalian cells and a much lower level in insect cells. In vitro selection pressure that mimicked the host switching (insect-mammal) revealed that the best adapted reassortant virus was connected with an advantageous replicative fitness and with the presence of a specific segment.</description><subject>Animals</subject><subject>arbovirus</subject><subject>Bunyaviridae Infections - virology</subject><subject>Cell Line</subject><subject>Cricetinae</subject><subject>Insecta</subject><subject>Life sciences</subject><subject>Médecine vétérinaire & santé animale</subject><subject>Orthobunyavirus</subject><subject>Orthobunyavirus - genetics</subject><subject>Orthobunyavirus - growth & development</subject><subject>Orthobunyavirus - isolation & purification</subject><subject>Orthobunyavirus/genetics/growth & development/isolation & purification</subject><subject>Reassortant Viruses - genetics</subject><subject>Reassortant Viruses - growth & development</subject><subject>Reassortant Viruses - isolation & purification</subject><subject>Reassortant Viruses/genetics/growth & development/isolation & purification</subject><subject>reassortment</subject><subject>recombination</subject><subject>Recombination, Genetic</subject><subject>Retrospective Studies</subject><subject>Sciences du vivant</subject><subject>Veterinary medicine & animal health</subject><subject>viral selection</subject><subject>Viruses</subject><issn>2222-1751</issn><issn>2222-1751</issn><fulltext>true</fulltext><rsrctype>article</rsrctype><creationdate>2019</creationdate><recordtype>article</recordtype><sourceid>0YH</sourceid><sourceid>PIMPY</sourceid><sourceid>DOA</sourceid><recordid>eNp9UktvEzEQXiEQrUJ_AsgSFy4JtnftXV8QqAJaqRKHwNnyY5y42rWDvRuUf483SauWA754NN9jPNZXVW8JXhHc4Y-0HNIysqKYiBVhHW8IflFdzv3lDLx8Ul9UVznf43JaXHjN6-qixp3gNW4uK3kT87i0sINgIRhA0SEf0N6PKaIEKueYxgHCiOwhqMGbjNQQwwaNW0BrNW6nHSSPVLBovZ0Rq9DaD3ra-zRlyG-qV071Ga7O96L69e3rz-ub5d2P77fXX-6WhmM-LlUnOi6McFZwLLirueZOONdqbqgGw2pBCHZaC0eJaTuFQXUdKKeN0DWh9aK6PfnaqO7lLvlBpYOMystjI6aNVGn0pgcJrG2JpYyaRjQ1I9qaWogGs1orY4vdovp08tpNegBryvZJ9c9MnyPBb-Um7iVvGCOkLQb1yaD3sIEyXHu5p0fhsZ768hojNUhKeScpE6JriurDeWyKvyfIoxx8NtD3KkCcsqREMMppQ7tCff8P9T5OKZQPlgVvGWUNnQ3ZiWVSzDmBe1yBYDnnSD7kSM45kuccFd27p_s_qh5SUwifTwQfXEyD-hNTb-WoDn1MLqlgfJb1_2f8BYeP18o</recordid><startdate>20190101</startdate><enddate>20190101</enddate><creator>Coupeau, Damien</creator><creator>Bayrou, Calixte</creator><creator>Baillieux, Pierre</creator><creator>Marichal, Axel</creator><creator>Lenaerts, Anne-Cécile</creator><creator>Caty, Céline</creator><creator>Wiggers, Laetitia</creator><creator>Kirschvink, Nathalie</creator><creator>Desmecht, Daniel</creator><creator>Muylkens, Benoît</creator><general>Taylor & Francis</general><general>Taylor & Francis Ltd</general><general>Taylor and Francis</general><general>Taylor & Francis Group</general><scope>0YH</scope><scope>CGR</scope><scope>CUY</scope><scope>CVF</scope><scope>ECM</scope><scope>EIF</scope><scope>NPM</scope><scope>AAYXX</scope><scope>CITATION</scope><scope>3V.</scope><scope>7X7</scope><scope>7XB</scope><scope>88E</scope><scope>8FI</scope><scope>8FJ</scope><scope>8FK</scope><scope>ABUWG</scope><scope>AFKRA</scope><scope>AZQEC</scope><scope>BENPR</scope><scope>CCPQU</scope><scope>DWQXO</scope><scope>FYUFA</scope><scope>GHDGH</scope><scope>K9.</scope><scope>M0S</scope><scope>M1P</scope><scope>PIMPY</scope><scope>PQEST</scope><scope>PQQKQ</scope><scope>PQUKI</scope><scope>7X8</scope><scope>Q33</scope><scope>5PM</scope><scope>DOA</scope><orcidid>https://orcid.org/0000-0002-4636-3996</orcidid><orcidid>https://orcid.org/0000-0001-7058-7757</orcidid><orcidid>https://orcid.org/0000-0001-5616-5099</orcidid></search><sort><creationdate>20190101</creationdate><title>Host-dependence of in vitro reassortment dynamics among the Sathuperi and Shamonda Simbuviruses</title><author>Coupeau, Damien ; Bayrou, Calixte ; Baillieux, Pierre ; Marichal, Axel ; Lenaerts, Anne-Cécile ; Caty, Céline ; Wiggers, Laetitia ; Kirschvink, Nathalie ; Desmecht, Daniel ; Muylkens, Benoît</author></sort><facets><frbrtype>5</frbrtype><frbrgroupid>cdi_FETCH-LOGICAL-c606t-a89869c9fd96096f36b6f9ff7b6c2bec539110fbb9f21c78a0ea88eafbc9b3123</frbrgroupid><rsrctype>articles</rsrctype><prefilter>articles</prefilter><language>eng</language><creationdate>2019</creationdate><topic>Animals</topic><topic>arbovirus</topic><topic>Bunyaviridae Infections - virology</topic><topic>Cell Line</topic><topic>Cricetinae</topic><topic>Insecta</topic><topic>Life sciences</topic><topic>Médecine vétérinaire & santé animale</topic><topic>Orthobunyavirus</topic><topic>Orthobunyavirus - genetics</topic><topic>Orthobunyavirus - growth & development</topic><topic>Orthobunyavirus - isolation & purification</topic><topic>Orthobunyavirus/genetics/growth & development/isolation & purification</topic><topic>Reassortant Viruses - genetics</topic><topic>Reassortant Viruses - growth & development</topic><topic>Reassortant Viruses - isolation & purification</topic><topic>Reassortant Viruses/genetics/growth & development/isolation & purification</topic><topic>reassortment</topic><topic>recombination</topic><topic>Recombination, Genetic</topic><topic>Retrospective Studies</topic><topic>Sciences du vivant</topic><topic>Veterinary medicine & animal health</topic><topic>viral selection</topic><topic>Viruses</topic><toplevel>peer_reviewed</toplevel><toplevel>online_resources</toplevel><creatorcontrib>Coupeau, Damien</creatorcontrib><creatorcontrib>Bayrou, Calixte</creatorcontrib><creatorcontrib>Baillieux, Pierre</creatorcontrib><creatorcontrib>Marichal, Axel</creatorcontrib><creatorcontrib>Lenaerts, Anne-Cécile</creatorcontrib><creatorcontrib>Caty, Céline</creatorcontrib><creatorcontrib>Wiggers, Laetitia</creatorcontrib><creatorcontrib>Kirschvink, Nathalie</creatorcontrib><creatorcontrib>Desmecht, Daniel</creatorcontrib><creatorcontrib>Muylkens, Benoît</creatorcontrib><collection>Taylor & Francis Open Access</collection><collection>Medline</collection><collection>MEDLINE</collection><collection>MEDLINE (Ovid)</collection><collection>MEDLINE</collection><collection>MEDLINE</collection><collection>PubMed</collection><collection>CrossRef</collection><collection>ProQuest Central (Corporate)</collection><collection>Health & Medical Collection</collection><collection>ProQuest Central (purchase pre-March 2016)</collection><collection>Medical Database (Alumni Edition)</collection><collection>Hospital Premium Collection</collection><collection>Hospital Premium Collection (Alumni Edition)</collection><collection>ProQuest Central (Alumni) (purchase pre-March 2016)</collection><collection>ProQuest Central (Alumni)</collection><collection>ProQuest Central</collection><collection>ProQuest Central Essentials</collection><collection>ProQuest Central</collection><collection>ProQuest One Community College</collection><collection>ProQuest Central</collection><collection>Health Research Premium Collection</collection><collection>Health Research Premium Collection (Alumni)</collection><collection>ProQuest Health & Medical Complete (Alumni)</collection><collection>Health & Medical Collection (Alumni Edition)</collection><collection>Medical Database</collection><collection>Publicly Available Content Database</collection><collection>ProQuest One Academic Eastern Edition (DO NOT USE)</collection><collection>ProQuest One Academic</collection><collection>ProQuest One Academic UKI Edition</collection><collection>MEDLINE - Academic</collection><collection>Université de Liège - Open Repository and Bibliography (ORBI)</collection><collection>PubMed Central (Full Participant titles)</collection><collection>DOAJ Directory of Open Access Journals</collection><jtitle>Emerging microbes & infections</jtitle></facets><delivery><delcategory>Remote Search Resource</delcategory><fulltext>fulltext</fulltext></delivery><addata><au>Coupeau, Damien</au><au>Bayrou, Calixte</au><au>Baillieux, Pierre</au><au>Marichal, Axel</au><au>Lenaerts, Anne-Cécile</au><au>Caty, Céline</au><au>Wiggers, Laetitia</au><au>Kirschvink, Nathalie</au><au>Desmecht, Daniel</au><au>Muylkens, Benoît</au><format>journal</format><genre>article</genre><ristype>JOUR</ristype><atitle>Host-dependence of in vitro reassortment dynamics among the Sathuperi and Shamonda Simbuviruses</atitle><jtitle>Emerging microbes & infections</jtitle><addtitle>Emerg Microbes Infect</addtitle><date>2019-01-01</date><risdate>2019</risdate><volume>8</volume><issue>1</issue><spage>381</spage><epage>395</epage><pages>381-395</pages><issn>2222-1751</issn><eissn>2222-1751</eissn><abstract>Orthobunyaviruses are arboviruses (Arthropod Borne Virus) and possess multipartite genomes made up of three negative RNAs corresponding to the small (S), medium (M) and large (L) segments. Reassortment and recombination are evolutionary driving forces of such segmented viruses and lead to the emergence of new strains and species. Retrospective studies based on phylogenetical analysis are able to evaluate these mechanisms at the end of the selection process but fail to address the dynamics of emergence. This issue was addressed using two Orthobunyaviruses infecting ruminants and belonging to the Simbu serogroup: the Sathuperi virus (SATV) and the Shamonda virus (SHAV). Both viruses were associated with abortion, stillbirth and congenital malformations occurring after transplacental transmission and were suspected to spread together in different ruminant and insect populations. This study showed that different viruses related to SHAV and SATV are spreading simultaneously in ruminants and equids of the Sub-Saharan region. Their reassortment and recombination potential was evaluated in mammalian and in insect contexts. A method was set up to determine the genomic background of any clonal progeny viruses isolated after in vitro coinfections assays. All the reassortment combinations were generated in both contexts while no recombinant virus was isolated. Progeny virus populations revealed a high level of reassortment in mammalian cells and a much lower level in insect cells. In vitro selection pressure that mimicked the host switching (insect-mammal) revealed that the best adapted reassortant virus was connected with an advantageous replicative fitness and with the presence of a specific segment.</abstract><cop>United States</cop><pub>Taylor & Francis</pub><pmid>30896304</pmid><doi>10.1080/22221751.2019.1586410</doi><tpages>15</tpages><orcidid>https://orcid.org/0000-0002-4636-3996</orcidid><orcidid>https://orcid.org/0000-0001-7058-7757</orcidid><orcidid>https://orcid.org/0000-0001-5616-5099</orcidid><oa>free_for_read</oa></addata></record> |
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subjects | Animals arbovirus Bunyaviridae Infections - virology Cell Line Cricetinae Insecta Life sciences Médecine vétérinaire & santé animale Orthobunyavirus Orthobunyavirus - genetics Orthobunyavirus - growth & development Orthobunyavirus - isolation & purification Orthobunyavirus/genetics/growth & development/isolation & purification Reassortant Viruses - genetics Reassortant Viruses - growth & development Reassortant Viruses - isolation & purification Reassortant Viruses/genetics/growth & development/isolation & purification reassortment recombination Recombination, Genetic Retrospective Studies Sciences du vivant Veterinary medicine & animal health viral selection Viruses |
title | Host-dependence of in vitro reassortment dynamics among the Sathuperi and Shamonda Simbuviruses |
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