Sensing of latent EBV infection through exosomal transfer of 5'pppRNA
Complex interactions between DNA herpesviruses and host factors determine the establishment of a life-long asymptomatic latent infection. The lymphotropic Epstein-Barr virus (EBV) seems to avoid recognition by innate sensors despite massive transcription of immunostimulatory small RNAs (EBV-EBERs)....
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| Veröffentlicht in: | Proceedings of the National Academy of Sciences - PNAS 2016-02, Vol.113 (5), p.E587-E596 |
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| creator | Baglio, S Rubina van Eijndhoven, Monique A J Koppers-Lalic, Danijela Berenguer, Jordi Lougheed, Sinéad M Gibbs, Susan Léveillé, Nicolas Rinkel, Rico N P M Hopmans, Erik S Swaminathan, Sankar Verkuijlen, Sandra A W M Scheffer, George L van Kuppeveld, Frank J M de Gruijl, Tanja D Bultink, Irene E M Jordanova, Ekaterina S Hackenberg, Michael Piersma, Sander R Knol, Jaco C Voskuyl, Alexandre E Wurdinger, Thomas Jiménez, Connie R Middeldorp, Jaap M Pegtel, D Michiel |
| description | Complex interactions between DNA herpesviruses and host factors determine the establishment of a life-long asymptomatic latent infection. The lymphotropic Epstein-Barr virus (EBV) seems to avoid recognition by innate sensors despite massive transcription of immunostimulatory small RNAs (EBV-EBERs). Here we demonstrate that in latently infected B cells, EBER1 transcripts interact with the lupus antigen (La) ribonucleoprotein, avoiding cytoplasmic RNA sensors. However, in coculture experiments we observed that latent-infected cells trigger antiviral immunity in dendritic cells (DCs) through selective release and transfer of RNA via exosomes. In ex vivo tonsillar cultures, we observed that EBER1-loaded exosomes are preferentially captured and internalized by human plasmacytoid DCs (pDCs) that express the TIM1 phosphatidylserine receptor, a known viral- and exosomal target. Using an EBER-deficient EBV strain, enzymatic removal of 5'ppp, in vitro transcripts, and coculture experiments, we established that 5'pppEBER1 transfer via exosomes drives antiviral immunity in nonpermissive DCs. Lupus erythematosus patients suffer from elevated EBV load and activated antiviral immunity, in particular in skin lesions that are infiltrated with pDCs. We detected high levels of EBER1 RNA in such skin lesions, as well as EBV-microRNAs, but no intact EBV-DNA, linking non-cell-autonomous EBER1 presence with skin inflammation in predisposed individuals. Collectively, our studies indicate that virus-modified exosomes have a physiological role in the host-pathogen stand-off and may promote inflammatory disease. |
| doi_str_mv | 10.1073/pnas.1518130113 |
| format | Article |
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The lymphotropic Epstein-Barr virus (EBV) seems to avoid recognition by innate sensors despite massive transcription of immunostimulatory small RNAs (EBV-EBERs). Here we demonstrate that in latently infected B cells, EBER1 transcripts interact with the lupus antigen (La) ribonucleoprotein, avoiding cytoplasmic RNA sensors. However, in coculture experiments we observed that latent-infected cells trigger antiviral immunity in dendritic cells (DCs) through selective release and transfer of RNA via exosomes. In ex vivo tonsillar cultures, we observed that EBER1-loaded exosomes are preferentially captured and internalized by human plasmacytoid DCs (pDCs) that express the TIM1 phosphatidylserine receptor, a known viral- and exosomal target. Using an EBER-deficient EBV strain, enzymatic removal of 5'ppp, in vitro transcripts, and coculture experiments, we established that 5'pppEBER1 transfer via exosomes drives antiviral immunity in nonpermissive DCs. Lupus erythematosus patients suffer from elevated EBV load and activated antiviral immunity, in particular in skin lesions that are infiltrated with pDCs. We detected high levels of EBER1 RNA in such skin lesions, as well as EBV-microRNAs, but no intact EBV-DNA, linking non-cell-autonomous EBER1 presence with skin inflammation in predisposed individuals. Collectively, our studies indicate that virus-modified exosomes have a physiological role in the host-pathogen stand-off and may promote inflammatory disease.</description><identifier>ISSN: 0027-8424</identifier><identifier>EISSN: 1091-6490</identifier><identifier>DOI: 10.1073/pnas.1518130113</identifier><identifier>PMID: 26768848</identifier><language>eng</language><publisher>United States: National Academy of Sciences</publisher><subject>Biological Transport ; Biosensors ; Cellular biology ; Dendritic Cells - virology ; Deoxyribonucleic acid ; DNA ; Epstein-Barr virus ; Epstein-Barr Virus Infections - genetics ; Epstein-Barr Virus Infections - immunology ; Exosomes - metabolism ; Experiments ; Herpes viruses ; Herpesvirus 4, Human - genetics ; Humans ; Proteome ; RNA, Viral - metabolism ; Viral infections</subject><ispartof>Proceedings of the National Academy of Sciences - PNAS, 2016-02, Vol.113 (5), p.E587-E596</ispartof><rights>Copyright National Academy of Sciences Feb 2, 2016</rights><lds50>peer_reviewed</lds50><woscitedreferencessubscribed>false</woscitedreferencessubscribed></display><links><openurl>$$Topenurl_article</openurl><openurlfulltext>$$Topenurlfull_article</openurlfulltext><thumbnail>$$Tsyndetics_thumb_exl</thumbnail><link.rule.ids>314,776,780,27901,27902</link.rule.ids><backlink>$$Uhttps://www.ncbi.nlm.nih.gov/pubmed/26768848$$D View this record in MEDLINE/PubMed$$Hfree_for_read</backlink></links><search><creatorcontrib>Baglio, S Rubina</creatorcontrib><creatorcontrib>van Eijndhoven, Monique A J</creatorcontrib><creatorcontrib>Koppers-Lalic, Danijela</creatorcontrib><creatorcontrib>Berenguer, Jordi</creatorcontrib><creatorcontrib>Lougheed, Sinéad M</creatorcontrib><creatorcontrib>Gibbs, Susan</creatorcontrib><creatorcontrib>Léveillé, Nicolas</creatorcontrib><creatorcontrib>Rinkel, Rico N P M</creatorcontrib><creatorcontrib>Hopmans, Erik S</creatorcontrib><creatorcontrib>Swaminathan, Sankar</creatorcontrib><creatorcontrib>Verkuijlen, Sandra A W M</creatorcontrib><creatorcontrib>Scheffer, George L</creatorcontrib><creatorcontrib>van Kuppeveld, Frank J M</creatorcontrib><creatorcontrib>de Gruijl, Tanja D</creatorcontrib><creatorcontrib>Bultink, Irene E M</creatorcontrib><creatorcontrib>Jordanova, Ekaterina S</creatorcontrib><creatorcontrib>Hackenberg, Michael</creatorcontrib><creatorcontrib>Piersma, Sander R</creatorcontrib><creatorcontrib>Knol, Jaco C</creatorcontrib><creatorcontrib>Voskuyl, Alexandre E</creatorcontrib><creatorcontrib>Wurdinger, Thomas</creatorcontrib><creatorcontrib>Jiménez, Connie R</creatorcontrib><creatorcontrib>Middeldorp, Jaap M</creatorcontrib><creatorcontrib>Pegtel, D Michiel</creatorcontrib><title>Sensing of latent EBV infection through exosomal transfer of 5'pppRNA</title><title>Proceedings of the National Academy of Sciences - PNAS</title><addtitle>Proc Natl Acad Sci U S A</addtitle><description>Complex interactions between DNA herpesviruses and host factors determine the establishment of a life-long asymptomatic latent infection. The lymphotropic Epstein-Barr virus (EBV) seems to avoid recognition by innate sensors despite massive transcription of immunostimulatory small RNAs (EBV-EBERs). Here we demonstrate that in latently infected B cells, EBER1 transcripts interact with the lupus antigen (La) ribonucleoprotein, avoiding cytoplasmic RNA sensors. However, in coculture experiments we observed that latent-infected cells trigger antiviral immunity in dendritic cells (DCs) through selective release and transfer of RNA via exosomes. In ex vivo tonsillar cultures, we observed that EBER1-loaded exosomes are preferentially captured and internalized by human plasmacytoid DCs (pDCs) that express the TIM1 phosphatidylserine receptor, a known viral- and exosomal target. Using an EBER-deficient EBV strain, enzymatic removal of 5'ppp, in vitro transcripts, and coculture experiments, we established that 5'pppEBER1 transfer via exosomes drives antiviral immunity in nonpermissive DCs. Lupus erythematosus patients suffer from elevated EBV load and activated antiviral immunity, in particular in skin lesions that are infiltrated with pDCs. We detected high levels of EBER1 RNA in such skin lesions, as well as EBV-microRNAs, but no intact EBV-DNA, linking non-cell-autonomous EBER1 presence with skin inflammation in predisposed individuals. Collectively, our studies indicate that virus-modified exosomes have a physiological role in the host-pathogen stand-off and may promote inflammatory disease.</description><subject>Biological Transport</subject><subject>Biosensors</subject><subject>Cellular biology</subject><subject>Dendritic Cells - virology</subject><subject>Deoxyribonucleic acid</subject><subject>DNA</subject><subject>Epstein-Barr virus</subject><subject>Epstein-Barr Virus Infections - genetics</subject><subject>Epstein-Barr Virus Infections - immunology</subject><subject>Exosomes - metabolism</subject><subject>Experiments</subject><subject>Herpes viruses</subject><subject>Herpesvirus 4, Human - genetics</subject><subject>Humans</subject><subject>Proteome</subject><subject>RNA, Viral - metabolism</subject><subject>Viral infections</subject><issn>0027-8424</issn><issn>1091-6490</issn><fulltext>true</fulltext><rsrctype>article</rsrctype><creationdate>2016</creationdate><recordtype>article</recordtype><sourceid>EIF</sourceid><recordid>eNqN0DtPwzAUBWALgWgpzGwoEgMsKb5-e2yr8pAqkHitkZM4barEDnEiwb8nFWVhYrrLd450D0LngKeAJb1pnAlT4KCAYgB6gMaANcSCaXyIxhgTGStG2AidhLDFGGuu8DEaESGFUkyN0fLFulC6deSLqDKddV20nL9HpSts1pXeRd2m9f16E9lPH3xtqqhrjQuFbXcJftU0zfPj7BQdFaYK9mx_J-jtdvm6uI9XT3cPi9kqbkDJLs4JVRhSQjKeMcoKIwRRIFOVGy2pBGVzbrnWWlAiqWLGZimkhlGb5anMFZ2g65_epvUfvQ1dUpchs1VlnPV9SEAOMaIp5_-gYlhBMryjl3_o1vetGx7ZKS6w4FQM6mKv-rS2edK0ZW3ar-R3S_oNG7Zz0A</recordid><startdate>20160202</startdate><enddate>20160202</enddate><creator>Baglio, S Rubina</creator><creator>van Eijndhoven, Monique A J</creator><creator>Koppers-Lalic, Danijela</creator><creator>Berenguer, Jordi</creator><creator>Lougheed, Sinéad M</creator><creator>Gibbs, Susan</creator><creator>Léveillé, Nicolas</creator><creator>Rinkel, Rico N P M</creator><creator>Hopmans, Erik S</creator><creator>Swaminathan, Sankar</creator><creator>Verkuijlen, Sandra A W M</creator><creator>Scheffer, George L</creator><creator>van Kuppeveld, Frank J M</creator><creator>de Gruijl, Tanja D</creator><creator>Bultink, Irene E M</creator><creator>Jordanova, Ekaterina S</creator><creator>Hackenberg, Michael</creator><creator>Piersma, Sander R</creator><creator>Knol, Jaco C</creator><creator>Voskuyl, Alexandre E</creator><creator>Wurdinger, Thomas</creator><creator>Jiménez, Connie R</creator><creator>Middeldorp, Jaap M</creator><creator>Pegtel, D Michiel</creator><general>National Academy of Sciences</general><scope>CGR</scope><scope>CUY</scope><scope>CVF</scope><scope>ECM</scope><scope>EIF</scope><scope>NPM</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>7X8</scope></search><sort><creationdate>20160202</creationdate><title>Sensing of latent EBV infection through exosomal transfer of 5'pppRNA</title><author>Baglio, S Rubina ; van Eijndhoven, Monique A J ; Koppers-Lalic, Danijela ; Berenguer, Jordi ; Lougheed, Sinéad M ; Gibbs, Susan ; Léveillé, Nicolas ; Rinkel, Rico N P M ; Hopmans, Erik S ; Swaminathan, Sankar ; Verkuijlen, Sandra A W M ; Scheffer, George L ; van Kuppeveld, Frank J M ; de Gruijl, Tanja D ; Bultink, Irene E M ; Jordanova, Ekaterina S ; Hackenberg, Michael ; Piersma, Sander R ; Knol, Jaco C ; Voskuyl, Alexandre E ; Wurdinger, Thomas ; Jiménez, Connie R ; Middeldorp, Jaap M ; Pegtel, D Michiel</author></sort><facets><frbrtype>5</frbrtype><frbrgroupid>cdi_FETCH-LOGICAL-p187t-d23801b22c5c434fa662817b8da973718ed5e59996327384aecb1ba43ecdb7d83</frbrgroupid><rsrctype>articles</rsrctype><prefilter>articles</prefilter><language>eng</language><creationdate>2016</creationdate><topic>Biological Transport</topic><topic>Biosensors</topic><topic>Cellular biology</topic><topic>Dendritic Cells - 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PNAS</jtitle><addtitle>Proc Natl Acad Sci U S A</addtitle><date>2016-02-02</date><risdate>2016</risdate><volume>113</volume><issue>5</issue><spage>E587</spage><epage>E596</epage><pages>E587-E596</pages><issn>0027-8424</issn><eissn>1091-6490</eissn><abstract>Complex interactions between DNA herpesviruses and host factors determine the establishment of a life-long asymptomatic latent infection. The lymphotropic Epstein-Barr virus (EBV) seems to avoid recognition by innate sensors despite massive transcription of immunostimulatory small RNAs (EBV-EBERs). Here we demonstrate that in latently infected B cells, EBER1 transcripts interact with the lupus antigen (La) ribonucleoprotein, avoiding cytoplasmic RNA sensors. However, in coculture experiments we observed that latent-infected cells trigger antiviral immunity in dendritic cells (DCs) through selective release and transfer of RNA via exosomes. In ex vivo tonsillar cultures, we observed that EBER1-loaded exosomes are preferentially captured and internalized by human plasmacytoid DCs (pDCs) that express the TIM1 phosphatidylserine receptor, a known viral- and exosomal target. Using an EBER-deficient EBV strain, enzymatic removal of 5'ppp, in vitro transcripts, and coculture experiments, we established that 5'pppEBER1 transfer via exosomes drives antiviral immunity in nonpermissive DCs. Lupus erythematosus patients suffer from elevated EBV load and activated antiviral immunity, in particular in skin lesions that are infiltrated with pDCs. We detected high levels of EBER1 RNA in such skin lesions, as well as EBV-microRNAs, but no intact EBV-DNA, linking non-cell-autonomous EBER1 presence with skin inflammation in predisposed individuals. Collectively, our studies indicate that virus-modified exosomes have a physiological role in the host-pathogen stand-off and may promote inflammatory disease.</abstract><cop>United States</cop><pub>National Academy of Sciences</pub><pmid>26768848</pmid><doi>10.1073/pnas.1518130113</doi></addata></record> |
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| subjects | Biological Transport Biosensors Cellular biology Dendritic Cells - virology Deoxyribonucleic acid DNA Epstein-Barr virus Epstein-Barr Virus Infections - genetics Epstein-Barr Virus Infections - immunology Exosomes - metabolism Experiments Herpes viruses Herpesvirus 4, Human - genetics Humans Proteome RNA, Viral - metabolism Viral infections |
| title | Sensing of latent EBV infection through exosomal transfer of 5'pppRNA |
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