Skin Injury Activates a Rapid TRPV1-Dependent Antiviral Protein Response
The skin serves as the interface between the body and the environment and plays a fundamental role in innate antimicrobial host immunity. Antiviral proteins (AVPs) are part of the innate host defense system and provide protection against viral pathogens. How breach of the skin barrier influences inn...
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| Veröffentlicht in: | Journal of investigative dermatology 2022-08, Vol.142 (8), p.2249-2259.e9 |
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| creator | Lei, Vivian Handfield, Chelsea Kwock, Jeffery T. Kirchner, Stephen J. Lee, Min Jin Coates, Margaret Wang, Kaiyuan Han, Qingjian Wang, Zilong Powers, Jennifer G. Wolfe, Sarah Corcoran, David L. Fanelli, Brian Dadlani, Manoj Ji, Ru-Rong Zhang, Jennifer Y. MacLeod, Amanda S. |
| description | The skin serves as the interface between the body and the environment and plays a fundamental role in innate antimicrobial host immunity. Antiviral proteins (AVPs) are part of the innate host defense system and provide protection against viral pathogens. How breach of the skin barrier influences innate AVP production remains largely unknown. In this study, we characterized the induction and regulation of AVPs after skin injury and identified a key role of TRPV1 in this process. Transcriptional and phenotypic profiling of cutaneous wounds revealed that skin injury induces high levels of AVPs in both mice and humans. Remarkably, pharmacologic and genetic ablation of TRPV1-mediated nociception abrogated the induction of AVPs, including Oas2, Oasl2, and Isg15 after skin injury in mice. Conversely, stimulation of TRPV1 nociceptors was sufficient to induce AVP production involving the CD301b+ cells‒IL-27‒mediated signaling pathway. Using IL-27 receptor‒knockout mice, we show that IL-27 signaling is required in the induction of AVPs after skin injury. Finally, loss of TRPV1 signaling leads to increased viral infectivity of herpes simplex virus. Together, our data indicate that TRPV1 signaling ensures skin antiviral competence on wounding. |
| doi_str_mv | 10.1016/j.jid.2021.11.041 |
| format | Article |
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Antiviral proteins (AVPs) are part of the innate host defense system and provide protection against viral pathogens. How breach of the skin barrier influences innate AVP production remains largely unknown. In this study, we characterized the induction and regulation of AVPs after skin injury and identified a key role of TRPV1 in this process. Transcriptional and phenotypic profiling of cutaneous wounds revealed that skin injury induces high levels of AVPs in both mice and humans. Remarkably, pharmacologic and genetic ablation of TRPV1-mediated nociception abrogated the induction of AVPs, including Oas2, Oasl2, and Isg15 after skin injury in mice. Conversely, stimulation of TRPV1 nociceptors was sufficient to induce AVP production involving the CD301b+ cells‒IL-27‒mediated signaling pathway. Using IL-27 receptor‒knockout mice, we show that IL-27 signaling is required in the induction of AVPs after skin injury. Finally, loss of TRPV1 signaling leads to increased viral infectivity of herpes simplex virus. Together, our data indicate that TRPV1 signaling ensures skin antiviral competence on wounding.</description><identifier>ISSN: 0022-202X</identifier><identifier>EISSN: 1523-1747</identifier><identifier>DOI: 10.1016/j.jid.2021.11.041</identifier><identifier>PMID: 35007556</identifier><language>eng</language><publisher>United States: Elsevier Inc</publisher><subject>Animals ; Antiviral Restriction Factors - immunology ; Herpes Simplex - immunology ; Humans ; Immunity, Innate ; Interleukin-27 - immunology ; Mice ; Nociceptors - metabolism ; Skin - injuries ; TRPV Cation Channels - genetics ; TRPV Cation Channels - metabolism</subject><ispartof>Journal of investigative dermatology, 2022-08, Vol.142 (8), p.2249-2259.e9</ispartof><rights>2021 The Authors</rights><rights>Copyright © 2021 The Authors. Published by Elsevier Inc. All rights reserved.</rights><lds50>peer_reviewed</lds50><oa>free_for_read</oa><woscitedreferencessubscribed>false</woscitedreferencessubscribed><citedby>FETCH-LOGICAL-c451t-e0d503940ea39c9d9cda452978abcbed8c0b0e54a04dc38021bed65a0468d28a3</citedby><cites>FETCH-LOGICAL-c451t-e0d503940ea39c9d9cda452978abcbed8c0b0e54a04dc38021bed65a0468d28a3</cites><orcidid>0000-0002-6773-272X ; 0000-0002-8045-5747 ; 0000-0002-9355-3688 ; 0000-0002-4485-1750 ; 0000-0001-7473-0354 ; 0000-0002-0343-2453 ; 0000-0002-9804-3193 ; 0000-0003-2693-5085 ; 0000-0003-1582-8452 ; 0000-0001-5406-151X ; 0000-0001-8139-9110 ; 0000-0001-6439-828X ; 0000-0003-3451-4803 ; 0000-0002-8223-7006 ; 0000-0002-8374-6427 ; 0000-0001-7460-9247 ; 0000-0003-4162-578X</orcidid></display><links><openurl>$$Topenurl_article</openurl><openurlfulltext>$$Topenurlfull_article</openurlfulltext><thumbnail>$$Tsyndetics_thumb_exl</thumbnail><link.rule.ids>230,314,777,781,882,27905,27906</link.rule.ids><backlink>$$Uhttps://www.ncbi.nlm.nih.gov/pubmed/35007556$$D View this record in MEDLINE/PubMed$$Hfree_for_read</backlink></links><search><creatorcontrib>Lei, Vivian</creatorcontrib><creatorcontrib>Handfield, Chelsea</creatorcontrib><creatorcontrib>Kwock, Jeffery T.</creatorcontrib><creatorcontrib>Kirchner, Stephen J.</creatorcontrib><creatorcontrib>Lee, Min Jin</creatorcontrib><creatorcontrib>Coates, Margaret</creatorcontrib><creatorcontrib>Wang, Kaiyuan</creatorcontrib><creatorcontrib>Han, Qingjian</creatorcontrib><creatorcontrib>Wang, Zilong</creatorcontrib><creatorcontrib>Powers, Jennifer G.</creatorcontrib><creatorcontrib>Wolfe, Sarah</creatorcontrib><creatorcontrib>Corcoran, David L.</creatorcontrib><creatorcontrib>Fanelli, Brian</creatorcontrib><creatorcontrib>Dadlani, Manoj</creatorcontrib><creatorcontrib>Ji, Ru-Rong</creatorcontrib><creatorcontrib>Zhang, Jennifer Y.</creatorcontrib><creatorcontrib>MacLeod, Amanda S.</creatorcontrib><title>Skin Injury Activates a Rapid TRPV1-Dependent Antiviral Protein Response</title><title>Journal of investigative dermatology</title><addtitle>J Invest Dermatol</addtitle><description>The skin serves as the interface between the body and the environment and plays a fundamental role in innate antimicrobial host immunity. Antiviral proteins (AVPs) are part of the innate host defense system and provide protection against viral pathogens. How breach of the skin barrier influences innate AVP production remains largely unknown. In this study, we characterized the induction and regulation of AVPs after skin injury and identified a key role of TRPV1 in this process. Transcriptional and phenotypic profiling of cutaneous wounds revealed that skin injury induces high levels of AVPs in both mice and humans. Remarkably, pharmacologic and genetic ablation of TRPV1-mediated nociception abrogated the induction of AVPs, including Oas2, Oasl2, and Isg15 after skin injury in mice. Conversely, stimulation of TRPV1 nociceptors was sufficient to induce AVP production involving the CD301b+ cells‒IL-27‒mediated signaling pathway. Using IL-27 receptor‒knockout mice, we show that IL-27 signaling is required in the induction of AVPs after skin injury. Finally, loss of TRPV1 signaling leads to increased viral infectivity of herpes simplex virus. Together, our data indicate that TRPV1 signaling ensures skin antiviral competence on wounding.</description><subject>Animals</subject><subject>Antiviral Restriction Factors - immunology</subject><subject>Herpes Simplex - immunology</subject><subject>Humans</subject><subject>Immunity, Innate</subject><subject>Interleukin-27 - immunology</subject><subject>Mice</subject><subject>Nociceptors - metabolism</subject><subject>Skin - injuries</subject><subject>TRPV Cation Channels - genetics</subject><subject>TRPV Cation Channels - metabolism</subject><issn>0022-202X</issn><issn>1523-1747</issn><fulltext>true</fulltext><rsrctype>article</rsrctype><creationdate>2022</creationdate><recordtype>article</recordtype><sourceid>EIF</sourceid><recordid>eNp9UU1LJDEQDbKis-oP2Iv0cS_dVqWT_kBYGNxdFQRl_MBbyCTlmnYm3SY9A_57I-PK7sVTkar3Xr3UY-wbQoGA1VFXdM4WHDgWiAUI3GITlLzMsRb1FzYB4DxP4_td9jXGDhJHyGaH7ZYSoJaymrCz6yfns3PfrcJLNjWjW-uRYqazmR6czW5mV3eY_6SBvCU_ZlOfEC7oRXYV-pESdUZx6H2kfbb9oBeRDt7rHrv9_evm5Cy_uDw9P5le5EZIHHMCK6FsBZAuW9Pa1lgtJG_rRs_NnGxjYA4khQZhTdmkr6VmJdOzaixvdLnHfmx0h9V8SdYkV8mOGoJb6vCieu3U_xPvHtWffq1aLtu6wiTw_V0g9M8riqNaumhosdCe-lVUvMKmhbopRYLiBmpCH2Ogh481COotAdWplIB6S0AhqpRA4hz-6--D8ffkCXC8AVC60tpRUNE48oasC2RGZXv3ifwr3_CXRg</recordid><startdate>20220801</startdate><enddate>20220801</enddate><creator>Lei, Vivian</creator><creator>Handfield, Chelsea</creator><creator>Kwock, Jeffery T.</creator><creator>Kirchner, Stephen J.</creator><creator>Lee, Min Jin</creator><creator>Coates, Margaret</creator><creator>Wang, Kaiyuan</creator><creator>Han, Qingjian</creator><creator>Wang, Zilong</creator><creator>Powers, Jennifer G.</creator><creator>Wolfe, Sarah</creator><creator>Corcoran, David L.</creator><creator>Fanelli, Brian</creator><creator>Dadlani, Manoj</creator><creator>Ji, Ru-Rong</creator><creator>Zhang, Jennifer Y.</creator><creator>MacLeod, Amanda S.</creator><general>Elsevier Inc</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>5PM</scope><orcidid>https://orcid.org/0000-0002-6773-272X</orcidid><orcidid>https://orcid.org/0000-0002-8045-5747</orcidid><orcidid>https://orcid.org/0000-0002-9355-3688</orcidid><orcidid>https://orcid.org/0000-0002-4485-1750</orcidid><orcidid>https://orcid.org/0000-0001-7473-0354</orcidid><orcidid>https://orcid.org/0000-0002-0343-2453</orcidid><orcidid>https://orcid.org/0000-0002-9804-3193</orcidid><orcidid>https://orcid.org/0000-0003-2693-5085</orcidid><orcidid>https://orcid.org/0000-0003-1582-8452</orcidid><orcidid>https://orcid.org/0000-0001-5406-151X</orcidid><orcidid>https://orcid.org/0000-0001-8139-9110</orcidid><orcidid>https://orcid.org/0000-0001-6439-828X</orcidid><orcidid>https://orcid.org/0000-0003-3451-4803</orcidid><orcidid>https://orcid.org/0000-0002-8223-7006</orcidid><orcidid>https://orcid.org/0000-0002-8374-6427</orcidid><orcidid>https://orcid.org/0000-0001-7460-9247</orcidid><orcidid>https://orcid.org/0000-0003-4162-578X</orcidid></search><sort><creationdate>20220801</creationdate><title>Skin Injury Activates a Rapid TRPV1-Dependent Antiviral Protein Response</title><author>Lei, Vivian ; Handfield, Chelsea ; Kwock, Jeffery T. ; Kirchner, Stephen J. ; Lee, Min Jin ; Coates, Margaret ; Wang, Kaiyuan ; Han, Qingjian ; Wang, Zilong ; Powers, Jennifer G. ; Wolfe, Sarah ; Corcoran, David L. ; Fanelli, Brian ; Dadlani, Manoj ; Ji, Ru-Rong ; Zhang, Jennifer Y. ; MacLeod, Amanda S.</author></sort><facets><frbrtype>5</frbrtype><frbrgroupid>cdi_FETCH-LOGICAL-c451t-e0d503940ea39c9d9cda452978abcbed8c0b0e54a04dc38021bed65a0468d28a3</frbrgroupid><rsrctype>articles</rsrctype><prefilter>articles</prefilter><language>eng</language><creationdate>2022</creationdate><topic>Animals</topic><topic>Antiviral Restriction Factors - immunology</topic><topic>Herpes Simplex - immunology</topic><topic>Humans</topic><topic>Immunity, Innate</topic><topic>Interleukin-27 - immunology</topic><topic>Mice</topic><topic>Nociceptors - metabolism</topic><topic>Skin - injuries</topic><topic>TRPV Cation Channels - genetics</topic><topic>TRPV Cation Channels - metabolism</topic><toplevel>peer_reviewed</toplevel><toplevel>online_resources</toplevel><creatorcontrib>Lei, Vivian</creatorcontrib><creatorcontrib>Handfield, Chelsea</creatorcontrib><creatorcontrib>Kwock, Jeffery T.</creatorcontrib><creatorcontrib>Kirchner, Stephen J.</creatorcontrib><creatorcontrib>Lee, Min Jin</creatorcontrib><creatorcontrib>Coates, Margaret</creatorcontrib><creatorcontrib>Wang, Kaiyuan</creatorcontrib><creatorcontrib>Han, Qingjian</creatorcontrib><creatorcontrib>Wang, Zilong</creatorcontrib><creatorcontrib>Powers, Jennifer G.</creatorcontrib><creatorcontrib>Wolfe, Sarah</creatorcontrib><creatorcontrib>Corcoran, David L.</creatorcontrib><creatorcontrib>Fanelli, Brian</creatorcontrib><creatorcontrib>Dadlani, Manoj</creatorcontrib><creatorcontrib>Ji, Ru-Rong</creatorcontrib><creatorcontrib>Zhang, Jennifer Y.</creatorcontrib><creatorcontrib>MacLeod, Amanda S.</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>PubMed Central (Full Participant titles)</collection><jtitle>Journal of investigative dermatology</jtitle></facets><delivery><delcategory>Remote Search Resource</delcategory><fulltext>fulltext</fulltext></delivery><addata><au>Lei, Vivian</au><au>Handfield, Chelsea</au><au>Kwock, Jeffery T.</au><au>Kirchner, Stephen J.</au><au>Lee, Min Jin</au><au>Coates, Margaret</au><au>Wang, Kaiyuan</au><au>Han, Qingjian</au><au>Wang, Zilong</au><au>Powers, Jennifer G.</au><au>Wolfe, Sarah</au><au>Corcoran, David L.</au><au>Fanelli, Brian</au><au>Dadlani, Manoj</au><au>Ji, Ru-Rong</au><au>Zhang, Jennifer Y.</au><au>MacLeod, Amanda S.</au><format>journal</format><genre>article</genre><ristype>JOUR</ristype><atitle>Skin Injury Activates a Rapid TRPV1-Dependent Antiviral Protein Response</atitle><jtitle>Journal of investigative dermatology</jtitle><addtitle>J Invest Dermatol</addtitle><date>2022-08-01</date><risdate>2022</risdate><volume>142</volume><issue>8</issue><spage>2249</spage><epage>2259.e9</epage><pages>2249-2259.e9</pages><issn>0022-202X</issn><eissn>1523-1747</eissn><abstract>The skin serves as the interface between the body and the environment and plays a fundamental role in innate antimicrobial host immunity. Antiviral proteins (AVPs) are part of the innate host defense system and provide protection against viral pathogens. How breach of the skin barrier influences innate AVP production remains largely unknown. In this study, we characterized the induction and regulation of AVPs after skin injury and identified a key role of TRPV1 in this process. Transcriptional and phenotypic profiling of cutaneous wounds revealed that skin injury induces high levels of AVPs in both mice and humans. Remarkably, pharmacologic and genetic ablation of TRPV1-mediated nociception abrogated the induction of AVPs, including Oas2, Oasl2, and Isg15 after skin injury in mice. Conversely, stimulation of TRPV1 nociceptors was sufficient to induce AVP production involving the CD301b+ cells‒IL-27‒mediated signaling pathway. Using IL-27 receptor‒knockout mice, we show that IL-27 signaling is required in the induction of AVPs after skin injury. Finally, loss of TRPV1 signaling leads to increased viral infectivity of herpes simplex virus. 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| ispartof | Journal of investigative dermatology, 2022-08, Vol.142 (8), p.2249-2259.e9 |
| issn | 0022-202X 1523-1747 |
| language | eng |
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| source | MEDLINE; Elektronische Zeitschriftenbibliothek - Frei zugängliche E-Journals; Alma/SFX Local Collection |
| subjects | Animals Antiviral Restriction Factors - immunology Herpes Simplex - immunology Humans Immunity, Innate Interleukin-27 - immunology Mice Nociceptors - metabolism Skin - injuries TRPV Cation Channels - genetics TRPV Cation Channels - metabolism |
| title | Skin Injury Activates a Rapid TRPV1-Dependent Antiviral Protein Response |
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