Differential Inductions of RNA Silencing among Encapsidated Double-Stranded RNA Mycoviruses in the White Root Rot Fungus Rosellinia necatrix

RNA silencing acts as a defense mechanism against virus infection in a wide variety of organisms. Here, we investigated inductions of RNA silencing against encapsidated double-stranded RNA (dsRNA) fungal viruses (mycoviruses), including a partitivirus (RnPV1), a quadrivirus (RnQV1), a victorivirus (...

Ausführliche Beschreibung

Gespeichert in:
Bibliographische Detailangaben
Veröffentlicht in:Journal of virology 2016-06, Vol.90 (12), p.5677-5692
Hauptverfasser: Yaegashi, Hajime, Shimizu, Takeo, Ito, Tsutae, Kanematsu, Satoko
Format: Artikel
Sprache:eng
Schlagworte:
Online-Zugang:Volltext
Tags: Tag hinzufügen
Keine Tags, Fügen Sie den ersten Tag hinzu!
container_end_page 5692
container_issue 12
container_start_page 5677
container_title Journal of virology
container_volume 90
creator Yaegashi, Hajime
Shimizu, Takeo
Ito, Tsutae
Kanematsu, Satoko
description RNA silencing acts as a defense mechanism against virus infection in a wide variety of organisms. Here, we investigated inductions of RNA silencing against encapsidated double-stranded RNA (dsRNA) fungal viruses (mycoviruses), including a partitivirus (RnPV1), a quadrivirus (RnQV1), a victorivirus (RnVV1), a mycoreovirus (RnMyRV3), and a megabirnavirus (RnMBV1) in the phytopathogenic fungus Rosellinia necatrix Expression profiling of RNA silencing-related genes revealed that a dicer-like gene, an Argonaute-like gene, and two RNA-dependent RNA polymerase genes were upregulated by RnMyRV3 or RnMBV1 infection but not by other virus infections or by constitutive expression of dsRNA in R. necatrix Massive analysis of viral small RNAs (vsRNAs) from the five mycoviruses showed that 19- to 22-nucleotide (nt) vsRNAs were predominant; however, their ability to form duplexes with 3' overhangs and the 5' nucleotide preferences of vsRNAs differed among the five mycoviruses. The abundances of 19- to 22-nt vsRNAs from RnPV1, RnQV1, RnVV1, RnMyRV3, and RnMBV1 were 6.8%, 1.2%, 0.3%, 13.0%, and 24.9%, respectively. Importantly, the vsRNA abundances and accumulation levels of viral RNA were not always correlated, and the origins of the vsRNAs were distinguishable among the five mycoviruses. These data corroborated diverse interactions between encapsidated dsRNA mycoviruses and RNA silencing. Moreover, a green fluorescent protein (GFP)-based sensor assay in R. necatrix revealed that RnMBV1 infection induced silencing of the target sensor gene (GFP gene and the partial RnMBV1 sequence), suggesting that vsRNAs from RnMBV1 activated the RNA-induced silencing complex. Overall, this study provides insights into RNA silencing against encapsidated dsRNA mycoviruses. Encapsidated dsRNA fungal viruses (mycoviruses) are believed to replicate inside their virions; therefore, there is a question of whether they induce RNA silencing. Here, we investigated inductions of RNA silencing against encapsidated dsRNA mycoviruses (a partitivirus, a quadrivirus, a victorivirus, a mycoreovirus, and a megabirnavirus) in Rosellinia necatrix We revealed upregulation of RNA silencing-related genes in R. necatrix infected with a mycoreovirus or a megabirnavirus but not with other viruses, which was consistent with the relatively high abundances of vsRNAs from the two mycoviruses. We also showed common and different molecular features and origins of the vsRNAs from the five mycoviruses. Furthermore, we de
doi_str_mv 10.1128/jvi.02951-15
format Article
fullrecord <record><control><sourceid>proquest_pubme</sourceid><recordid>TN_cdi_pubmedcentral_primary_oai_pubmedcentral_nih_gov_4886788</recordid><sourceformat>XML</sourceformat><sourcesystem>PC</sourcesystem><sourcerecordid>1793567098</sourcerecordid><originalsourceid>FETCH-LOGICAL-c483t-207bd4fe8a8bac023099402404926bf6705c961a70a8bd4dc3a2a4bb57f992933</originalsourceid><addsrcrecordid>eNqFkU1v1DAQhi0Eokvhxhn5yIGUsWMn9gWp6gdd1Bap5etmOY6z6yprb21nRf9Df3S9bangxGXGo3n8al69CL0lsEcIFR-vNm4PqOSkIvwZmhGQouKcsOdoBkBpxWvxawe9SukKgDDWsJdoh7ZQA23JDN0eumGw0frs9Ijnvp9MdsEnHAZ8cb6PL91ovXF-gfUqlHrkjV4n1-tse3wYpm601WWO2vdl3n44uzFh4-KUbMLO47y0-OfSZYsvQsilZHw8-cWUyjPZcXTeaeyt0Tm636_Ri0GPyb557Lvo-_HRt4OT6vTr5_nB_mllmKhzRaHtejZYoUWnDdAapGRAGTBJm25oWuBGNkS3UICe9abWVLOu4-0gJZV1vYs-Peiup25le1PcRz2qdXQrHW9U0E79u_FuqRZho5gQTStEEXj_KBDD9WRTViuXTLGjvQ1TUkSAaIgkXP4fbWXNy8lyq_rhATUxpBTt8HQRAbXNWn35MVf3WSvCC_7ubxdP8J9w6zuusKbw</addsrcrecordid><sourcetype>Open Access Repository</sourcetype><iscdi>true</iscdi><recordtype>article</recordtype><pqid>1793567098</pqid></control><display><type>article</type><title>Differential Inductions of RNA Silencing among Encapsidated Double-Stranded RNA Mycoviruses in the White Root Rot Fungus Rosellinia necatrix</title><source>MEDLINE</source><source>EZB-FREE-00999 freely available EZB journals</source><source>PubMed Central</source><creator>Yaegashi, Hajime ; Shimizu, Takeo ; Ito, Tsutae ; Kanematsu, Satoko</creator><contributor>Simon, A.</contributor><creatorcontrib>Yaegashi, Hajime ; Shimizu, Takeo ; Ito, Tsutae ; Kanematsu, Satoko ; Simon, A.</creatorcontrib><description>RNA silencing acts as a defense mechanism against virus infection in a wide variety of organisms. Here, we investigated inductions of RNA silencing against encapsidated double-stranded RNA (dsRNA) fungal viruses (mycoviruses), including a partitivirus (RnPV1), a quadrivirus (RnQV1), a victorivirus (RnVV1), a mycoreovirus (RnMyRV3), and a megabirnavirus (RnMBV1) in the phytopathogenic fungus Rosellinia necatrix Expression profiling of RNA silencing-related genes revealed that a dicer-like gene, an Argonaute-like gene, and two RNA-dependent RNA polymerase genes were upregulated by RnMyRV3 or RnMBV1 infection but not by other virus infections or by constitutive expression of dsRNA in R. necatrix Massive analysis of viral small RNAs (vsRNAs) from the five mycoviruses showed that 19- to 22-nucleotide (nt) vsRNAs were predominant; however, their ability to form duplexes with 3' overhangs and the 5' nucleotide preferences of vsRNAs differed among the five mycoviruses. The abundances of 19- to 22-nt vsRNAs from RnPV1, RnQV1, RnVV1, RnMyRV3, and RnMBV1 were 6.8%, 1.2%, 0.3%, 13.0%, and 24.9%, respectively. Importantly, the vsRNA abundances and accumulation levels of viral RNA were not always correlated, and the origins of the vsRNAs were distinguishable among the five mycoviruses. These data corroborated diverse interactions between encapsidated dsRNA mycoviruses and RNA silencing. Moreover, a green fluorescent protein (GFP)-based sensor assay in R. necatrix revealed that RnMBV1 infection induced silencing of the target sensor gene (GFP gene and the partial RnMBV1 sequence), suggesting that vsRNAs from RnMBV1 activated the RNA-induced silencing complex. Overall, this study provides insights into RNA silencing against encapsidated dsRNA mycoviruses. Encapsidated dsRNA fungal viruses (mycoviruses) are believed to replicate inside their virions; therefore, there is a question of whether they induce RNA silencing. Here, we investigated inductions of RNA silencing against encapsidated dsRNA mycoviruses (a partitivirus, a quadrivirus, a victorivirus, a mycoreovirus, and a megabirnavirus) in Rosellinia necatrix We revealed upregulation of RNA silencing-related genes in R. necatrix infected with a mycoreovirus or a megabirnavirus but not with other viruses, which was consistent with the relatively high abundances of vsRNAs from the two mycoviruses. We also showed common and different molecular features and origins of the vsRNAs from the five mycoviruses. Furthermore, we demonstrated the activation of RNA-induced silencing complex by mycoviruses in R. necatrix Taken together, our data provide insights into an RNA silencing pathway against encapsidated dsRNA mycoviruses which is differentially induced among encapsidated dsRNA mycoviruses; that is, diverse replication strategies exist among encapsidated dsRNA mycoviruses.</description><identifier>ISSN: 0022-538X</identifier><identifier>EISSN: 1098-5514</identifier><identifier>DOI: 10.1128/jvi.02951-15</identifier><identifier>PMID: 27030271</identifier><language>eng</language><publisher>United States: American Society for Microbiology</publisher><subject>Fungal Viruses - genetics ; Green Fluorescent Proteins - genetics ; Open Reading Frames ; Partitivirus ; Pathogenesis and Immunity ; Reoviridae - genetics ; RNA Interference ; RNA, Double-Stranded - genetics ; RNA, Viral - genetics ; Spotlight ; Totiviridae - genetics ; Virion ; Xylariales - virology</subject><ispartof>Journal of virology, 2016-06, Vol.90 (12), p.5677-5692</ispartof><rights>Copyright © 2016, American Society for Microbiology. All Rights Reserved.</rights><rights>Copyright © 2016, American Society for Microbiology. All Rights Reserved. 2016 American Society for Microbiology</rights><lds50>peer_reviewed</lds50><oa>free_for_read</oa><woscitedreferencessubscribed>false</woscitedreferencessubscribed><citedby>FETCH-LOGICAL-c483t-207bd4fe8a8bac023099402404926bf6705c961a70a8bd4dc3a2a4bb57f992933</citedby><cites>FETCH-LOGICAL-c483t-207bd4fe8a8bac023099402404926bf6705c961a70a8bd4dc3a2a4bb57f992933</cites></display><links><openurl>$$Topenurl_article</openurl><openurlfulltext>$$Topenurlfull_article</openurlfulltext><thumbnail>$$Tsyndetics_thumb_exl</thumbnail><linktopdf>$$Uhttps://www.ncbi.nlm.nih.gov/pmc/articles/PMC4886788/pdf/$$EPDF$$P50$$Gpubmedcentral$$H</linktopdf><linktohtml>$$Uhttps://www.ncbi.nlm.nih.gov/pmc/articles/PMC4886788/$$EHTML$$P50$$Gpubmedcentral$$H</linktohtml><link.rule.ids>230,314,727,780,784,885,27924,27925,53791,53793</link.rule.ids><backlink>$$Uhttps://www.ncbi.nlm.nih.gov/pubmed/27030271$$D View this record in MEDLINE/PubMed$$Hfree_for_read</backlink></links><search><contributor>Simon, A.</contributor><creatorcontrib>Yaegashi, Hajime</creatorcontrib><creatorcontrib>Shimizu, Takeo</creatorcontrib><creatorcontrib>Ito, Tsutae</creatorcontrib><creatorcontrib>Kanematsu, Satoko</creatorcontrib><title>Differential Inductions of RNA Silencing among Encapsidated Double-Stranded RNA Mycoviruses in the White Root Rot Fungus Rosellinia necatrix</title><title>Journal of virology</title><addtitle>J Virol</addtitle><description>RNA silencing acts as a defense mechanism against virus infection in a wide variety of organisms. Here, we investigated inductions of RNA silencing against encapsidated double-stranded RNA (dsRNA) fungal viruses (mycoviruses), including a partitivirus (RnPV1), a quadrivirus (RnQV1), a victorivirus (RnVV1), a mycoreovirus (RnMyRV3), and a megabirnavirus (RnMBV1) in the phytopathogenic fungus Rosellinia necatrix Expression profiling of RNA silencing-related genes revealed that a dicer-like gene, an Argonaute-like gene, and two RNA-dependent RNA polymerase genes were upregulated by RnMyRV3 or RnMBV1 infection but not by other virus infections or by constitutive expression of dsRNA in R. necatrix Massive analysis of viral small RNAs (vsRNAs) from the five mycoviruses showed that 19- to 22-nucleotide (nt) vsRNAs were predominant; however, their ability to form duplexes with 3' overhangs and the 5' nucleotide preferences of vsRNAs differed among the five mycoviruses. The abundances of 19- to 22-nt vsRNAs from RnPV1, RnQV1, RnVV1, RnMyRV3, and RnMBV1 were 6.8%, 1.2%, 0.3%, 13.0%, and 24.9%, respectively. Importantly, the vsRNA abundances and accumulation levels of viral RNA were not always correlated, and the origins of the vsRNAs were distinguishable among the five mycoviruses. These data corroborated diverse interactions between encapsidated dsRNA mycoviruses and RNA silencing. Moreover, a green fluorescent protein (GFP)-based sensor assay in R. necatrix revealed that RnMBV1 infection induced silencing of the target sensor gene (GFP gene and the partial RnMBV1 sequence), suggesting that vsRNAs from RnMBV1 activated the RNA-induced silencing complex. Overall, this study provides insights into RNA silencing against encapsidated dsRNA mycoviruses. Encapsidated dsRNA fungal viruses (mycoviruses) are believed to replicate inside their virions; therefore, there is a question of whether they induce RNA silencing. Here, we investigated inductions of RNA silencing against encapsidated dsRNA mycoviruses (a partitivirus, a quadrivirus, a victorivirus, a mycoreovirus, and a megabirnavirus) in Rosellinia necatrix We revealed upregulation of RNA silencing-related genes in R. necatrix infected with a mycoreovirus or a megabirnavirus but not with other viruses, which was consistent with the relatively high abundances of vsRNAs from the two mycoviruses. We also showed common and different molecular features and origins of the vsRNAs from the five mycoviruses. Furthermore, we demonstrated the activation of RNA-induced silencing complex by mycoviruses in R. necatrix Taken together, our data provide insights into an RNA silencing pathway against encapsidated dsRNA mycoviruses which is differentially induced among encapsidated dsRNA mycoviruses; that is, diverse replication strategies exist among encapsidated dsRNA mycoviruses.</description><subject>Fungal Viruses - genetics</subject><subject>Green Fluorescent Proteins - genetics</subject><subject>Open Reading Frames</subject><subject>Partitivirus</subject><subject>Pathogenesis and Immunity</subject><subject>Reoviridae - genetics</subject><subject>RNA Interference</subject><subject>RNA, Double-Stranded - genetics</subject><subject>RNA, Viral - genetics</subject><subject>Spotlight</subject><subject>Totiviridae - genetics</subject><subject>Virion</subject><subject>Xylariales - virology</subject><issn>0022-538X</issn><issn>1098-5514</issn><fulltext>true</fulltext><rsrctype>article</rsrctype><creationdate>2016</creationdate><recordtype>article</recordtype><sourceid>EIF</sourceid><recordid>eNqFkU1v1DAQhi0Eokvhxhn5yIGUsWMn9gWp6gdd1Bap5etmOY6z6yprb21nRf9Df3S9bangxGXGo3n8al69CL0lsEcIFR-vNm4PqOSkIvwZmhGQouKcsOdoBkBpxWvxawe9SukKgDDWsJdoh7ZQA23JDN0eumGw0frs9Ijnvp9MdsEnHAZ8cb6PL91ovXF-gfUqlHrkjV4n1-tse3wYpm601WWO2vdl3n44uzFh4-KUbMLO47y0-OfSZYsvQsilZHw8-cWUyjPZcXTeaeyt0Tm636_Ri0GPyb557Lvo-_HRt4OT6vTr5_nB_mllmKhzRaHtejZYoUWnDdAapGRAGTBJm25oWuBGNkS3UICe9abWVLOu4-0gJZV1vYs-Peiup25le1PcRz2qdXQrHW9U0E79u_FuqRZho5gQTStEEXj_KBDD9WRTViuXTLGjvQ1TUkSAaIgkXP4fbWXNy8lyq_rhATUxpBTt8HQRAbXNWn35MVf3WSvCC_7ubxdP8J9w6zuusKbw</recordid><startdate>20160615</startdate><enddate>20160615</enddate><creator>Yaegashi, Hajime</creator><creator>Shimizu, Takeo</creator><creator>Ito, Tsutae</creator><creator>Kanematsu, Satoko</creator><general>American Society for Microbiology</general><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>7X8</scope><scope>7TM</scope><scope>7U9</scope><scope>H94</scope><scope>M7N</scope><scope>5PM</scope></search><sort><creationdate>20160615</creationdate><title>Differential Inductions of RNA Silencing among Encapsidated Double-Stranded RNA Mycoviruses in the White Root Rot Fungus Rosellinia necatrix</title><author>Yaegashi, Hajime ; Shimizu, Takeo ; Ito, Tsutae ; Kanematsu, Satoko</author></sort><facets><frbrtype>5</frbrtype><frbrgroupid>cdi_FETCH-LOGICAL-c483t-207bd4fe8a8bac023099402404926bf6705c961a70a8bd4dc3a2a4bb57f992933</frbrgroupid><rsrctype>articles</rsrctype><prefilter>articles</prefilter><language>eng</language><creationdate>2016</creationdate><topic>Fungal Viruses - genetics</topic><topic>Green Fluorescent Proteins - genetics</topic><topic>Open Reading Frames</topic><topic>Partitivirus</topic><topic>Pathogenesis and Immunity</topic><topic>Reoviridae - genetics</topic><topic>RNA Interference</topic><topic>RNA, Double-Stranded - genetics</topic><topic>RNA, Viral - genetics</topic><topic>Spotlight</topic><topic>Totiviridae - genetics</topic><topic>Virion</topic><topic>Xylariales - virology</topic><toplevel>peer_reviewed</toplevel><toplevel>online_resources</toplevel><creatorcontrib>Yaegashi, Hajime</creatorcontrib><creatorcontrib>Shimizu, Takeo</creatorcontrib><creatorcontrib>Ito, Tsutae</creatorcontrib><creatorcontrib>Kanematsu, Satoko</creatorcontrib><collection>Medline</collection><collection>MEDLINE</collection><collection>MEDLINE (Ovid)</collection><collection>MEDLINE</collection><collection>MEDLINE</collection><collection>PubMed</collection><collection>CrossRef</collection><collection>MEDLINE - Academic</collection><collection>Nucleic Acids Abstracts</collection><collection>Virology and AIDS Abstracts</collection><collection>AIDS and Cancer Research Abstracts</collection><collection>Algology Mycology and Protozoology Abstracts (Microbiology C)</collection><collection>PubMed Central (Full Participant titles)</collection><jtitle>Journal of virology</jtitle></facets><delivery><delcategory>Remote Search Resource</delcategory><fulltext>fulltext</fulltext></delivery><addata><au>Yaegashi, Hajime</au><au>Shimizu, Takeo</au><au>Ito, Tsutae</au><au>Kanematsu, Satoko</au><au>Simon, A.</au><format>journal</format><genre>article</genre><ristype>JOUR</ristype><atitle>Differential Inductions of RNA Silencing among Encapsidated Double-Stranded RNA Mycoviruses in the White Root Rot Fungus Rosellinia necatrix</atitle><jtitle>Journal of virology</jtitle><addtitle>J Virol</addtitle><date>2016-06-15</date><risdate>2016</risdate><volume>90</volume><issue>12</issue><spage>5677</spage><epage>5692</epage><pages>5677-5692</pages><issn>0022-538X</issn><eissn>1098-5514</eissn><abstract>RNA silencing acts as a defense mechanism against virus infection in a wide variety of organisms. Here, we investigated inductions of RNA silencing against encapsidated double-stranded RNA (dsRNA) fungal viruses (mycoviruses), including a partitivirus (RnPV1), a quadrivirus (RnQV1), a victorivirus (RnVV1), a mycoreovirus (RnMyRV3), and a megabirnavirus (RnMBV1) in the phytopathogenic fungus Rosellinia necatrix Expression profiling of RNA silencing-related genes revealed that a dicer-like gene, an Argonaute-like gene, and two RNA-dependent RNA polymerase genes were upregulated by RnMyRV3 or RnMBV1 infection but not by other virus infections or by constitutive expression of dsRNA in R. necatrix Massive analysis of viral small RNAs (vsRNAs) from the five mycoviruses showed that 19- to 22-nucleotide (nt) vsRNAs were predominant; however, their ability to form duplexes with 3' overhangs and the 5' nucleotide preferences of vsRNAs differed among the five mycoviruses. The abundances of 19- to 22-nt vsRNAs from RnPV1, RnQV1, RnVV1, RnMyRV3, and RnMBV1 were 6.8%, 1.2%, 0.3%, 13.0%, and 24.9%, respectively. Importantly, the vsRNA abundances and accumulation levels of viral RNA were not always correlated, and the origins of the vsRNAs were distinguishable among the five mycoviruses. These data corroborated diverse interactions between encapsidated dsRNA mycoviruses and RNA silencing. Moreover, a green fluorescent protein (GFP)-based sensor assay in R. necatrix revealed that RnMBV1 infection induced silencing of the target sensor gene (GFP gene and the partial RnMBV1 sequence), suggesting that vsRNAs from RnMBV1 activated the RNA-induced silencing complex. Overall, this study provides insights into RNA silencing against encapsidated dsRNA mycoviruses. Encapsidated dsRNA fungal viruses (mycoviruses) are believed to replicate inside their virions; therefore, there is a question of whether they induce RNA silencing. Here, we investigated inductions of RNA silencing against encapsidated dsRNA mycoviruses (a partitivirus, a quadrivirus, a victorivirus, a mycoreovirus, and a megabirnavirus) in Rosellinia necatrix We revealed upregulation of RNA silencing-related genes in R. necatrix infected with a mycoreovirus or a megabirnavirus but not with other viruses, which was consistent with the relatively high abundances of vsRNAs from the two mycoviruses. We also showed common and different molecular features and origins of the vsRNAs from the five mycoviruses. Furthermore, we demonstrated the activation of RNA-induced silencing complex by mycoviruses in R. necatrix Taken together, our data provide insights into an RNA silencing pathway against encapsidated dsRNA mycoviruses which is differentially induced among encapsidated dsRNA mycoviruses; that is, diverse replication strategies exist among encapsidated dsRNA mycoviruses.</abstract><cop>United States</cop><pub>American Society for Microbiology</pub><pmid>27030271</pmid><doi>10.1128/jvi.02951-15</doi><tpages>16</tpages><oa>free_for_read</oa></addata></record>
fulltext fulltext
identifier ISSN: 0022-538X
ispartof Journal of virology, 2016-06, Vol.90 (12), p.5677-5692
issn 0022-538X
1098-5514
language eng
recordid cdi_pubmedcentral_primary_oai_pubmedcentral_nih_gov_4886788
source MEDLINE; EZB-FREE-00999 freely available EZB journals; PubMed Central
subjects Fungal Viruses - genetics
Green Fluorescent Proteins - genetics
Open Reading Frames
Partitivirus
Pathogenesis and Immunity
Reoviridae - genetics
RNA Interference
RNA, Double-Stranded - genetics
RNA, Viral - genetics
Spotlight
Totiviridae - genetics
Virion
Xylariales - virology
title Differential Inductions of RNA Silencing among Encapsidated Double-Stranded RNA Mycoviruses in the White Root Rot Fungus Rosellinia necatrix
url https://sfx.bib-bvb.de/sfx_tum?ctx_ver=Z39.88-2004&ctx_enc=info:ofi/enc:UTF-8&ctx_tim=2024-12-24T16%3A59%3A34IST&url_ver=Z39.88-2004&url_ctx_fmt=infofi/fmt:kev:mtx:ctx&rfr_id=info:sid/primo.exlibrisgroup.com:primo3-Article-proquest_pubme&rft_val_fmt=info:ofi/fmt:kev:mtx:journal&rft.genre=article&rft.atitle=Differential%20Inductions%20of%20RNA%20Silencing%20among%20Encapsidated%20Double-Stranded%20RNA%20Mycoviruses%20in%20the%20White%20Root%20Rot%20Fungus%20Rosellinia%20necatrix&rft.jtitle=Journal%20of%20virology&rft.au=Yaegashi,%20Hajime&rft.date=2016-06-15&rft.volume=90&rft.issue=12&rft.spage=5677&rft.epage=5692&rft.pages=5677-5692&rft.issn=0022-538X&rft.eissn=1098-5514&rft_id=info:doi/10.1128/jvi.02951-15&rft_dat=%3Cproquest_pubme%3E1793567098%3C/proquest_pubme%3E%3Curl%3E%3C/url%3E&disable_directlink=true&sfx.directlink=off&sfx.report_link=0&rft_id=info:oai/&rft_pqid=1793567098&rft_id=info:pmid/27030271&rfr_iscdi=true