TRIM24 facilitates antiviral immunity through mediating K63-linked TRAF3 ubiquitination
Ubiquitination is an essential mechanism in the control of antiviral immunity upon virus infection. Here, we identify a series of ubiquitination-modulating enzymes that are modulated by vesicular stomatitis virus (VSV). Notably, TRIM24 is down-regulated through direct transcriptional suppression ind...
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| Veröffentlicht in: | The Journal of experimental medicine 2020-07, Vol.217 (7), Article 20192083 |
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| creator | Zhu, Qingchen Yu, Tao Gan, Shucheng Wang, Yan Pei, Yifei Zhao, Qifan Pei, Siyu Hao, Shumeng Yuan, Jia Xu, Jing Hou, Fajian Wu, Xuefeng Peng, Chao Wu, Ping Qin, Jun Xiao, Yichuan |
| description | Ubiquitination is an essential mechanism in the control of antiviral immunity upon virus infection. Here, we identify a series of ubiquitination-modulating enzymes that are modulated by vesicular stomatitis virus (VSV). Notably, TRIM24 is down-regulated through direct transcriptional suppression induced by VSV-activated IRF3. Reducing or ablating TRIM24 compromises type I IFN (IFN-I) induction upon RNA virus infection and thus renders mice more sensitive to VSV infection. Mechanistically, VSV infection induces abundant TRIM24 translocation to mitochondria, where TRIM24 binds with TRAF3 and directly mediates K63linked TRAF3 ubiquitination at K429/K436. This modification of TRAF3 enables its association with MAVS and TBK1, which consequently activates downstream antiviral signaling. Together, these findings establish TRIM24 as a critical positive regulator in controlling the activation of antiviral signaling and describe a previously unknown mechanism of TRIM24 function. |
| doi_str_mv | 10.1084/jem.20192083 |
| format | Article |
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Here, we identify a series of ubiquitination-modulating enzymes that are modulated by vesicular stomatitis virus (VSV). Notably, TRIM24 is down-regulated through direct transcriptional suppression induced by VSV-activated IRF3. Reducing or ablating TRIM24 compromises type I IFN (IFN-I) induction upon RNA virus infection and thus renders mice more sensitive to VSV infection. Mechanistically, VSV infection induces abundant TRIM24 translocation to mitochondria, where TRIM24 binds with TRAF3 and directly mediates K63linked TRAF3 ubiquitination at K429/K436. This modification of TRAF3 enables its association with MAVS and TBK1, which consequently activates downstream antiviral signaling. Together, these findings establish TRIM24 as a critical positive regulator in controlling the activation of antiviral signaling and describe a previously unknown mechanism of TRIM24 function.</description><identifier>ISSN: 0022-1007</identifier><identifier>EISSN: 1540-9538</identifier><identifier>DOI: 10.1084/jem.20192083</identifier><identifier>PMID: 32324863</identifier><language>eng</language><publisher>NEW YORK: Rockefeller Univ Press</publisher><subject>Adaptor Proteins, Signal Transducing - metabolism ; Amino Acid Sequence ; Animals ; Base Sequence ; Cell Nucleus - metabolism ; Down-Regulation ; HEK293 Cells ; Humans ; Immunity ; Immunology ; Infectious Disease and Host Defense ; Inflammation - genetics ; Innate Immunity and Inflammation ; Interferon Type I - metabolism ; Life Sciences & Biomedicine ; Lysine - metabolism ; Medicine, Research & Experimental ; Mice, Inbred C57BL ; Mice, Knockout ; Mitochondria - metabolism ; Models, Biological ; Nuclear Proteins - chemistry ; Nuclear Proteins - deficiency ; Nuclear Proteins - genetics ; Nuclear Proteins - metabolism ; Protein Serine-Threonine Kinases - metabolism ; Protein Transport ; Research & Experimental Medicine ; RING Finger Domains ; Science & Technology ; Signal Transduction ; TNF Receptor-Associated Factor 3 - chemistry ; TNF Receptor-Associated Factor 3 - genetics ; TNF Receptor-Associated Factor 3 - metabolism ; Transcription Factors - chemistry ; Transcription Factors - deficiency ; Transcription Factors - genetics ; Transcription Factors - metabolism ; Transcription, Genetic ; Ubiquitination ; Vesicular stomatitis Indiana virus - physiology</subject><ispartof>The Journal of experimental medicine, 2020-07, Vol.217 (7), Article 20192083</ispartof><rights>2020 Zhu et al.</rights><rights>2020 Zhu et al. 2020</rights><lds50>peer_reviewed</lds50><oa>free_for_read</oa><woscitedreferencessubscribed>true</woscitedreferencessubscribed><woscitedreferencescount>38</woscitedreferencescount><woscitedreferencesoriginalsourcerecordid>wos000574828600004</woscitedreferencesoriginalsourcerecordid><citedby>FETCH-LOGICAL-c384t-e4b43285624c202cb8294185b8cf1fac14f97c82d9a3f67c8edf1634caad2ba63</citedby><cites>FETCH-LOGICAL-c384t-e4b43285624c202cb8294185b8cf1fac14f97c82d9a3f67c8edf1634caad2ba63</cites><orcidid>0000-0002-2263-128X ; 0000-0001-7896-4625 ; 0000-0002-6814-2676 ; 0000-0001-7804-6971</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/PMC7336305/pdf/$$EPDF$$P50$$Gpubmedcentral$$Hfree_for_read</linktopdf><linktohtml>$$Uhttps://www.ncbi.nlm.nih.gov/pmc/articles/PMC7336305/$$EHTML$$P50$$Gpubmedcentral$$Hfree_for_read</linktohtml><link.rule.ids>230,315,728,781,785,886,27929,27930,28253,53796,53798</link.rule.ids><backlink>$$Uhttps://www.ncbi.nlm.nih.gov/pubmed/32324863$$D View this record in MEDLINE/PubMed$$Hfree_for_read</backlink></links><search><creatorcontrib>Zhu, Qingchen</creatorcontrib><creatorcontrib>Yu, Tao</creatorcontrib><creatorcontrib>Gan, Shucheng</creatorcontrib><creatorcontrib>Wang, Yan</creatorcontrib><creatorcontrib>Pei, Yifei</creatorcontrib><creatorcontrib>Zhao, Qifan</creatorcontrib><creatorcontrib>Pei, Siyu</creatorcontrib><creatorcontrib>Hao, Shumeng</creatorcontrib><creatorcontrib>Yuan, Jia</creatorcontrib><creatorcontrib>Xu, Jing</creatorcontrib><creatorcontrib>Hou, Fajian</creatorcontrib><creatorcontrib>Wu, Xuefeng</creatorcontrib><creatorcontrib>Peng, Chao</creatorcontrib><creatorcontrib>Wu, Ping</creatorcontrib><creatorcontrib>Qin, Jun</creatorcontrib><creatorcontrib>Xiao, Yichuan</creatorcontrib><title>TRIM24 facilitates antiviral immunity through mediating K63-linked TRAF3 ubiquitination</title><title>The Journal of experimental medicine</title><addtitle>J EXP MED</addtitle><addtitle>J Exp Med</addtitle><description>Ubiquitination is an essential mechanism in the control of antiviral immunity upon virus infection. Here, we identify a series of ubiquitination-modulating enzymes that are modulated by vesicular stomatitis virus (VSV). Notably, TRIM24 is down-regulated through direct transcriptional suppression induced by VSV-activated IRF3. Reducing or ablating TRIM24 compromises type I IFN (IFN-I) induction upon RNA virus infection and thus renders mice more sensitive to VSV infection. Mechanistically, VSV infection induces abundant TRIM24 translocation to mitochondria, where TRIM24 binds with TRAF3 and directly mediates K63linked TRAF3 ubiquitination at K429/K436. This modification of TRAF3 enables its association with MAVS and TBK1, which consequently activates downstream antiviral signaling. Together, these findings establish TRIM24 as a critical positive regulator in controlling the activation of antiviral signaling and describe a previously unknown mechanism of TRIM24 function.</description><subject>Adaptor Proteins, Signal Transducing - metabolism</subject><subject>Amino Acid Sequence</subject><subject>Animals</subject><subject>Base Sequence</subject><subject>Cell Nucleus - metabolism</subject><subject>Down-Regulation</subject><subject>HEK293 Cells</subject><subject>Humans</subject><subject>Immunity</subject><subject>Immunology</subject><subject>Infectious Disease and Host Defense</subject><subject>Inflammation - genetics</subject><subject>Innate Immunity and Inflammation</subject><subject>Interferon Type I - metabolism</subject><subject>Life Sciences & Biomedicine</subject><subject>Lysine - metabolism</subject><subject>Medicine, Research & Experimental</subject><subject>Mice, Inbred C57BL</subject><subject>Mice, Knockout</subject><subject>Mitochondria - metabolism</subject><subject>Models, Biological</subject><subject>Nuclear Proteins - chemistry</subject><subject>Nuclear Proteins - deficiency</subject><subject>Nuclear Proteins - genetics</subject><subject>Nuclear Proteins - metabolism</subject><subject>Protein Serine-Threonine Kinases - metabolism</subject><subject>Protein Transport</subject><subject>Research & Experimental Medicine</subject><subject>RING Finger Domains</subject><subject>Science & Technology</subject><subject>Signal Transduction</subject><subject>TNF Receptor-Associated Factor 3 - chemistry</subject><subject>TNF Receptor-Associated Factor 3 - genetics</subject><subject>TNF Receptor-Associated Factor 3 - metabolism</subject><subject>Transcription Factors - chemistry</subject><subject>Transcription Factors - deficiency</subject><subject>Transcription Factors - genetics</subject><subject>Transcription Factors - metabolism</subject><subject>Transcription, Genetic</subject><subject>Ubiquitination</subject><subject>Vesicular stomatitis Indiana virus - physiology</subject><issn>0022-1007</issn><issn>1540-9538</issn><fulltext>true</fulltext><rsrctype>article</rsrctype><creationdate>2020</creationdate><recordtype>article</recordtype><sourceid>AOWDO</sourceid><sourceid>EIF</sourceid><recordid>eNqNkc1r3DAQxUVoSbZJbjkXHwut05FG1sqXQFiaD5oSCFt6FLIs7yq1pcSSU_LfV8smS3PrSQPvN0-PeYScUDilIPnXezucMqA1A4l7ZEYrDmVdoXxHZgCMlRRgfkA-xHgPQDmvxD45QIaMS4Ez8mt5d_2D8aLTxvUu6WRjoX1yT27UfeGGYfIuPRdpPYZptS4G2zqdnF8V3wWWvfO_bVss784vsJga9zi5rGU9-CPyvtN9tMcv7yH5efFtubgqb24vrxfnN6VByVNpecORyUowbhgw00hWcyqrRpqO5kyUd_XcSNbWGjuRJ9t2VCA3Wres0QIPydnW92FqcjhjfcrB1cPoBj0-q6Cdeqt4t1ar8KTmiAKhygafXgzG8DjZmNTgorF9r70NU1QMay5roGKDftmiZgwxjrbbfUNBbbpQuQv12kXGP_4bbQe_Hj8Dcgv8sU3oonHWG7vDAKCac8mkyBPwxaacfNhFmHzKq5__fxX_AqY7pso</recordid><startdate>20200706</startdate><enddate>20200706</enddate><creator>Zhu, Qingchen</creator><creator>Yu, Tao</creator><creator>Gan, Shucheng</creator><creator>Wang, Yan</creator><creator>Pei, Yifei</creator><creator>Zhao, Qifan</creator><creator>Pei, Siyu</creator><creator>Hao, Shumeng</creator><creator>Yuan, Jia</creator><creator>Xu, Jing</creator><creator>Hou, Fajian</creator><creator>Wu, Xuefeng</creator><creator>Peng, Chao</creator><creator>Wu, Ping</creator><creator>Qin, Jun</creator><creator>Xiao, Yichuan</creator><general>Rockefeller Univ Press</general><general>Rockefeller University Press</general><scope>AOWDO</scope><scope>BLEPL</scope><scope>DTL</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>7X8</scope><scope>5PM</scope><orcidid>https://orcid.org/0000-0002-2263-128X</orcidid><orcidid>https://orcid.org/0000-0001-7896-4625</orcidid><orcidid>https://orcid.org/0000-0002-6814-2676</orcidid><orcidid>https://orcid.org/0000-0001-7804-6971</orcidid></search><sort><creationdate>20200706</creationdate><title>TRIM24 facilitates antiviral immunity through mediating K63-linked TRAF3 ubiquitination</title><author>Zhu, Qingchen ; 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Here, we identify a series of ubiquitination-modulating enzymes that are modulated by vesicular stomatitis virus (VSV). Notably, TRIM24 is down-regulated through direct transcriptional suppression induced by VSV-activated IRF3. Reducing or ablating TRIM24 compromises type I IFN (IFN-I) induction upon RNA virus infection and thus renders mice more sensitive to VSV infection. Mechanistically, VSV infection induces abundant TRIM24 translocation to mitochondria, where TRIM24 binds with TRAF3 and directly mediates K63linked TRAF3 ubiquitination at K429/K436. This modification of TRAF3 enables its association with MAVS and TBK1, which consequently activates downstream antiviral signaling. Together, these findings establish TRIM24 as a critical positive regulator in controlling the activation of antiviral signaling and describe a previously unknown mechanism of TRIM24 function.</abstract><cop>NEW YORK</cop><pub>Rockefeller Univ Press</pub><pmid>32324863</pmid><doi>10.1084/jem.20192083</doi><tpages>21</tpages><orcidid>https://orcid.org/0000-0002-2263-128X</orcidid><orcidid>https://orcid.org/0000-0001-7896-4625</orcidid><orcidid>https://orcid.org/0000-0002-6814-2676</orcidid><orcidid>https://orcid.org/0000-0001-7804-6971</orcidid><oa>free_for_read</oa></addata></record> |
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| subjects | Adaptor Proteins, Signal Transducing - metabolism Amino Acid Sequence Animals Base Sequence Cell Nucleus - metabolism Down-Regulation HEK293 Cells Humans Immunity Immunology Infectious Disease and Host Defense Inflammation - genetics Innate Immunity and Inflammation Interferon Type I - metabolism Life Sciences & Biomedicine Lysine - metabolism Medicine, Research & Experimental Mice, Inbred C57BL Mice, Knockout Mitochondria - metabolism Models, Biological Nuclear Proteins - chemistry Nuclear Proteins - deficiency Nuclear Proteins - genetics Nuclear Proteins - metabolism Protein Serine-Threonine Kinases - metabolism Protein Transport Research & Experimental Medicine RING Finger Domains Science & Technology Signal Transduction TNF Receptor-Associated Factor 3 - chemistry TNF Receptor-Associated Factor 3 - genetics TNF Receptor-Associated Factor 3 - metabolism Transcription Factors - chemistry Transcription Factors - deficiency Transcription Factors - genetics Transcription Factors - metabolism Transcription, Genetic Ubiquitination Vesicular stomatitis Indiana virus - physiology |
| title | TRIM24 facilitates antiviral immunity through mediating K63-linked TRAF3 ubiquitination |
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