RNA interference acts as a natural antiviral response to O'nyong-nyong virus (Alphavirus, Togaviridae) infection of Anopheles gambiae
RNA interference (RNAi) is triggered in eukaryotic organisms by double-stranded RNA (dsRNA), and it destroys any mRNA that has sequence identity with the dsRNA trigger. The RNAi pathway in Anopheles gambiae can be silenced by transfecting cells with dsRNA derived from exon sequence of the A. gambiae...
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| Veröffentlicht in: | Proceedings of the National Academy of Sciences - PNAS 2004-12, Vol.101 (49), p.17240-17245 |
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| container_title | Proceedings of the National Academy of Sciences - PNAS |
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| creator | Keene, K.M Foy, B.D Sanchez-Vargas, I Beaty, B.J Blair, C.D Olson, K.E |
| description | RNA interference (RNAi) is triggered in eukaryotic organisms by double-stranded RNA (dsRNA), and it destroys any mRNA that has sequence identity with the dsRNA trigger. The RNAi pathway in Anopheles gambiae can be silenced by transfecting cells with dsRNA derived from exon sequence of the A. gambiae Argonaute2 (AgAgo2) gene. We hypothesized that RNAi may also act as an antagonist to alphavirus replication in A. gambiae because RNA viruses form dsRNA during replication. Silencing AgAgo2 expression would make A. gambiae mosquitoes more permissive to virus infection. To determine whether RNAi conditions the vector competence of A. gambiae for O'nyong-nyong virus (ONNV), we engineered a genetically modified ONNV that expresses enhanced GFP (eGFP) as a marker. After intrathoracic injection, ONNV-eGFP slowly spread to other A. gambiae tissues over a 9-day incubation period. Mosquitoes were then coinjected with virus and either control beta-galactosidase dsRNA (ds(beta)gal; note that "ds" is used as a prefix to indicate the dsRNA derived from a given gene throughout) or ONNV dsnsP3. Treatment with dsnsP3 inhibited virus spread significantly, as determined by eGFP expression patterns. ONNV-eGFP titers from mosquitoes coinjected with dsnsP3 were significantly lower at 3 and 6 days after injection than in mosquitoes coinjected with ds(beta)gal. Mosquitoes were then coinjected with ONNV-eGFP and dsAgAgo2. Mosquitoes coinjected with virus and AgAgo2 dsRNA displayed widespread eGFP expression and virus titers 16-fold higher than ds(beta)gal controls after 3 or 6 days after injection. These observations provide direct evidence that RNAi is an antagonist of ONNV replication in A. gambiae, and they suggest that the innate immune response conditions vector competence. |
| doi_str_mv | 10.1073/pnas.0406983101 |
| format | Article |
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The RNAi pathway in Anopheles gambiae can be silenced by transfecting cells with dsRNA derived from exon sequence of the A. gambiae Argonaute2 (AgAgo2) gene. We hypothesized that RNAi may also act as an antagonist to alphavirus replication in A. gambiae because RNA viruses form dsRNA during replication. Silencing AgAgo2 expression would make A. gambiae mosquitoes more permissive to virus infection. To determine whether RNAi conditions the vector competence of A. gambiae for O'nyong-nyong virus (ONNV), we engineered a genetically modified ONNV that expresses enhanced GFP (eGFP) as a marker. After intrathoracic injection, ONNV-eGFP slowly spread to other A. gambiae tissues over a 9-day incubation period. Mosquitoes were then coinjected with virus and either control beta-galactosidase dsRNA (ds(beta)gal; note that "ds" is used as a prefix to indicate the dsRNA derived from a given gene throughout) or ONNV dsnsP3. Treatment with dsnsP3 inhibited virus spread significantly, as determined by eGFP expression patterns. ONNV-eGFP titers from mosquitoes coinjected with dsnsP3 were significantly lower at 3 and 6 days after injection than in mosquitoes coinjected with ds(beta)gal. Mosquitoes were then coinjected with ONNV-eGFP and dsAgAgo2. Mosquitoes coinjected with virus and AgAgo2 dsRNA displayed widespread eGFP expression and virus titers 16-fold higher than ds(beta)gal controls after 3 or 6 days after injection. These observations provide direct evidence that RNAi is an antagonist of ONNV replication in A. gambiae, and they suggest that the innate immune response conditions vector competence.</description><identifier>ISSN: 0027-8424</identifier><identifier>EISSN: 1091-6490</identifier><identifier>DOI: 10.1073/pnas.0406983101</identifier><identifier>PMID: 15583140</identifier><language>eng</language><publisher>United States: National Academy of Sciences</publisher><subject>Alphavirus ; Alphavirus - immunology ; Alphavirus Infections - immunology ; Alphaviruses ; Animals ; Anopheles - immunology ; Anopheles - virology ; Anopheles gambiae ; Arboviruses ; Biological Sciences ; Cell lines ; Culicidae ; disease resistance ; disease vectors ; Double stranded RNA ; Gene expression ; Immunity, Innate ; infection ; Infections ; Injections ; Insect Vectors ; Messenger RNA ; Microbiology ; Mosquitoes ; Mosquitos ; O'nyong-nyong virus ; RNA ; RNA interference ; RNA Interference - immunology ; RNA, Double-Stranded - immunology ; RNA, Double-Stranded - pharmacology ; Small interfering RNA ; Togaviridae ; vector competence ; Virus Replication - drug effects ; Viruses</subject><ispartof>Proceedings of the National Academy of Sciences - PNAS, 2004-12, Vol.101 (49), p.17240-17245</ispartof><rights>Copyright 1993/2004 The National Academy of Sciences of the United States of America</rights><rights>Copyright National Academy of Sciences Dec 7, 2004</rights><rights>Copyright © 2004, The National Academy of Sciences 2004</rights><lds50>peer_reviewed</lds50><oa>free_for_read</oa><woscitedreferencessubscribed>false</woscitedreferencessubscribed><citedby>FETCH-LOGICAL-c552t-ba89663292ca685a5226e1ca9b14de5792bcd83968f09dfe75bc2ca318790fda3</citedby><cites>FETCH-LOGICAL-c552t-ba89663292ca685a5226e1ca9b14de5792bcd83968f09dfe75bc2ca318790fda3</cites></display><links><openurl>$$Topenurl_article</openurl><openurlfulltext>$$Topenurlfull_article</openurlfulltext><thumbnail>$$Uhttp://www.pnas.org/content/101/49.cover.gif</thumbnail><linktopdf>$$Uhttps://www.jstor.org/stable/pdf/3373990$$EPDF$$P50$$Gjstor$$H</linktopdf><linktohtml>$$Uhttps://www.jstor.org/stable/3373990$$EHTML$$P50$$Gjstor$$H</linktohtml><link.rule.ids>230,314,723,776,780,799,881,27901,27902,53766,53768,57992,58225</link.rule.ids><backlink>$$Uhttps://www.ncbi.nlm.nih.gov/pubmed/15583140$$D View this record in MEDLINE/PubMed$$Hfree_for_read</backlink></links><search><creatorcontrib>Keene, K.M</creatorcontrib><creatorcontrib>Foy, B.D</creatorcontrib><creatorcontrib>Sanchez-Vargas, I</creatorcontrib><creatorcontrib>Beaty, B.J</creatorcontrib><creatorcontrib>Blair, C.D</creatorcontrib><creatorcontrib>Olson, K.E</creatorcontrib><title>RNA interference acts as a natural antiviral response to O'nyong-nyong virus (Alphavirus, Togaviridae) infection of Anopheles gambiae</title><title>Proceedings of the National Academy of Sciences - PNAS</title><addtitle>Proc Natl Acad Sci U S A</addtitle><description>RNA interference (RNAi) is triggered in eukaryotic organisms by double-stranded RNA (dsRNA), and it destroys any mRNA that has sequence identity with the dsRNA trigger. The RNAi pathway in Anopheles gambiae can be silenced by transfecting cells with dsRNA derived from exon sequence of the A. gambiae Argonaute2 (AgAgo2) gene. We hypothesized that RNAi may also act as an antagonist to alphavirus replication in A. gambiae because RNA viruses form dsRNA during replication. Silencing AgAgo2 expression would make A. gambiae mosquitoes more permissive to virus infection. To determine whether RNAi conditions the vector competence of A. gambiae for O'nyong-nyong virus (ONNV), we engineered a genetically modified ONNV that expresses enhanced GFP (eGFP) as a marker. After intrathoracic injection, ONNV-eGFP slowly spread to other A. gambiae tissues over a 9-day incubation period. Mosquitoes were then coinjected with virus and either control beta-galactosidase dsRNA (ds(beta)gal; note that "ds" is used as a prefix to indicate the dsRNA derived from a given gene throughout) or ONNV dsnsP3. Treatment with dsnsP3 inhibited virus spread significantly, as determined by eGFP expression patterns. ONNV-eGFP titers from mosquitoes coinjected with dsnsP3 were significantly lower at 3 and 6 days after injection than in mosquitoes coinjected with ds(beta)gal. Mosquitoes were then coinjected with ONNV-eGFP and dsAgAgo2. Mosquitoes coinjected with virus and AgAgo2 dsRNA displayed widespread eGFP expression and virus titers 16-fold higher than ds(beta)gal controls after 3 or 6 days after injection. These observations provide direct evidence that RNAi is an antagonist of ONNV replication in A. gambiae, and they suggest that the innate immune response conditions vector competence.</description><subject>Alphavirus</subject><subject>Alphavirus - immunology</subject><subject>Alphavirus Infections - immunology</subject><subject>Alphaviruses</subject><subject>Animals</subject><subject>Anopheles - immunology</subject><subject>Anopheles - virology</subject><subject>Anopheles gambiae</subject><subject>Arboviruses</subject><subject>Biological Sciences</subject><subject>Cell lines</subject><subject>Culicidae</subject><subject>disease resistance</subject><subject>disease vectors</subject><subject>Double stranded RNA</subject><subject>Gene expression</subject><subject>Immunity, Innate</subject><subject>infection</subject><subject>Infections</subject><subject>Injections</subject><subject>Insect Vectors</subject><subject>Messenger RNA</subject><subject>Microbiology</subject><subject>Mosquitoes</subject><subject>Mosquitos</subject><subject>O'nyong-nyong virus</subject><subject>RNA</subject><subject>RNA interference</subject><subject>RNA Interference - immunology</subject><subject>RNA, Double-Stranded - immunology</subject><subject>RNA, Double-Stranded - pharmacology</subject><subject>Small interfering RNA</subject><subject>Togaviridae</subject><subject>vector competence</subject><subject>Virus Replication - drug effects</subject><subject>Viruses</subject><issn>0027-8424</issn><issn>1091-6490</issn><fulltext>true</fulltext><rsrctype>article</rsrctype><creationdate>2004</creationdate><recordtype>article</recordtype><sourceid>EIF</sourceid><recordid>eNqFkk1v1DAQhiMEokvhzAWBxQGoRFp_xIl94LCq-JIqKkF7tpxkkvUqawfbqegP4H_j7K66wKWSZY80zzuesd8se07wKcEVOxutDqe4wKUUjGDyIFsQLEleFhI_zBYY0yoXBS2OsichrDHGkgv8ODsinCe-wIvs9_dvS2RsBN-BB9sA0k0MSKeFrI6T1wPSNpobM0cewuhsABQdunxrb53t8-2OUn4K6N1yGFd6G79HV66fQ9NqOElXdNBE4yxyHVpaN65ggIB6vamNhqfZo04PAZ7tz-Ps-tPHq_Mv-cXl56_ny4u84ZzGvNZCliWjkja6FFxzSksgjZY1KVrglaR10womS9Fh2XZQ8bpJKCOikrhrNTvOPuzqjlO9gbYBG9NYavRmo_2tctqofzPWrFTvbhRnnAmW9G_2eu9-ThCi2pjQwDBoC24KqqxISTmR94KkEpgSQRL4-j9w7SZv0yMoigkrhCQzdLaDGu9C8NDddUywmn2gZh-ogw-S4uXfgx74_ccnAO2BWXkoR1QhU3d0i5zcg6huGoYIv2JiX-zYdYjO38GMVUzKudSrXbrTTunem6Cuf8zzJUeK9KMF-wPa99vW</recordid><startdate>20041207</startdate><enddate>20041207</enddate><creator>Keene, K.M</creator><creator>Foy, B.D</creator><creator>Sanchez-Vargas, I</creator><creator>Beaty, B.J</creator><creator>Blair, C.D</creator><creator>Olson, K.E</creator><general>National Academy of Sciences</general><general>National Acad Sciences</general><scope>FBQ</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>7QG</scope><scope>7QL</scope><scope>7QP</scope><scope>7QR</scope><scope>7SN</scope><scope>7SS</scope><scope>7T5</scope><scope>7TK</scope><scope>7TM</scope><scope>7TO</scope><scope>7U9</scope><scope>8FD</scope><scope>C1K</scope><scope>FR3</scope><scope>H94</scope><scope>M7N</scope><scope>P64</scope><scope>RC3</scope><scope>F1W</scope><scope>H95</scope><scope>L.G</scope><scope>7X8</scope><scope>5PM</scope></search><sort><creationdate>20041207</creationdate><title>RNA interference acts as a natural antiviral response to O'nyong-nyong virus (Alphavirus, Togaviridae) infection of Anopheles gambiae</title><author>Keene, K.M ; 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The RNAi pathway in Anopheles gambiae can be silenced by transfecting cells with dsRNA derived from exon sequence of the A. gambiae Argonaute2 (AgAgo2) gene. We hypothesized that RNAi may also act as an antagonist to alphavirus replication in A. gambiae because RNA viruses form dsRNA during replication. Silencing AgAgo2 expression would make A. gambiae mosquitoes more permissive to virus infection. To determine whether RNAi conditions the vector competence of A. gambiae for O'nyong-nyong virus (ONNV), we engineered a genetically modified ONNV that expresses enhanced GFP (eGFP) as a marker. After intrathoracic injection, ONNV-eGFP slowly spread to other A. gambiae tissues over a 9-day incubation period. Mosquitoes were then coinjected with virus and either control beta-galactosidase dsRNA (ds(beta)gal; note that "ds" is used as a prefix to indicate the dsRNA derived from a given gene throughout) or ONNV dsnsP3. Treatment with dsnsP3 inhibited virus spread significantly, as determined by eGFP expression patterns. ONNV-eGFP titers from mosquitoes coinjected with dsnsP3 were significantly lower at 3 and 6 days after injection than in mosquitoes coinjected with ds(beta)gal. Mosquitoes were then coinjected with ONNV-eGFP and dsAgAgo2. Mosquitoes coinjected with virus and AgAgo2 dsRNA displayed widespread eGFP expression and virus titers 16-fold higher than ds(beta)gal controls after 3 or 6 days after injection. These observations provide direct evidence that RNAi is an antagonist of ONNV replication in A. gambiae, and they suggest that the innate immune response conditions vector competence.</abstract><cop>United States</cop><pub>National Academy of Sciences</pub><pmid>15583140</pmid><doi>10.1073/pnas.0406983101</doi><tpages>6</tpages><oa>free_for_read</oa></addata></record> |
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| subjects | Alphavirus Alphavirus - immunology Alphavirus Infections - immunology Alphaviruses Animals Anopheles - immunology Anopheles - virology Anopheles gambiae Arboviruses Biological Sciences Cell lines Culicidae disease resistance disease vectors Double stranded RNA Gene expression Immunity, Innate infection Infections Injections Insect Vectors Messenger RNA Microbiology Mosquitoes Mosquitos O'nyong-nyong virus RNA RNA interference RNA Interference - immunology RNA, Double-Stranded - immunology RNA, Double-Stranded - pharmacology Small interfering RNA Togaviridae vector competence Virus Replication - drug effects Viruses |
| title | RNA interference acts as a natural antiviral response to O'nyong-nyong virus (Alphavirus, Togaviridae) infection of Anopheles gambiae |
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