Mitochondrial damage elicits a TCDD-inducible poly(ADP-ribose) polymerase-mediated antiviral response
The innate immune system senses RNA viruses by pattern recognition receptors (PRRs) and protects the host from virus infection. PRRs mediate the production of immune modulatory factors and direct the elimination of RNA viruses. Here, we show a unique PRR that mediates antiviral response. Tetrachloro...
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| Veröffentlicht in: | Proceedings of the National Academy of Sciences - PNAS 2017-03, Vol.114 (10), p.2681-2686 |
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| creator | Kozaki, Tatsuya Komano, Jun Kanbayashi, Daiki Takahama, Michihiro Misawa, Takuma Satoh, Takashi Takeuchi, Osamu Kawai, Taro Shimizu, Shigeomi Matsuura, Yoshiharu Akira, Shizuo Saitoh, Tatsuya |
| description | The innate immune system senses RNA viruses by pattern recognition receptors (PRRs) and protects the host from virus infection. PRRs mediate the production of immune modulatory factors and direct the elimination of RNA viruses. Here, we show a unique PRR that mediates antiviral response. Tetrachlorodibenzo-p-dioxin (TCDD)-inducible poly(ADP ribose) polymerase (TIPARP), a Cysteine3 Histidine (CCCH)-type zinc finger-containing protein, binds to Sindbis virus (SINV) RNA via its zinc finger domain and recruits an exosome to induce viral RNA degradation. TIPARP typically localizes in the nucleus, but it accumulates in the cytoplasm after SINV infection, allowing targeting of cytoplasmic SINV RNA. Redistribution of TIPARP is induced by reactive oxygen species (ROS)-dependent oxidization of the nuclear pore that affects cytoplasmic-nuclear transport. BCL2-associated X protein (BAX) and BCL2 antagonist/killer 1 (BAK1), B-cell leukemia/lymphoma 2 (BCL2) family members, mediate mitochondrial damage to generate ROS after SINV infection. Thus, TIPARP is a viral RNA-sensing PRR that mediates antiviral responses triggered by BAX- and BAK1-dependent mitochondrial damage. |
| doi_str_mv | 10.1073/pnas.1621508114 |
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PRRs mediate the production of immune modulatory factors and direct the elimination of RNA viruses. Here, we show a unique PRR that mediates antiviral response. Tetrachlorodibenzo-p-dioxin (TCDD)-inducible poly(ADP ribose) polymerase (TIPARP), a Cysteine3 Histidine (CCCH)-type zinc finger-containing protein, binds to Sindbis virus (SINV) RNA via its zinc finger domain and recruits an exosome to induce viral RNA degradation. TIPARP typically localizes in the nucleus, but it accumulates in the cytoplasm after SINV infection, allowing targeting of cytoplasmic SINV RNA. Redistribution of TIPARP is induced by reactive oxygen species (ROS)-dependent oxidization of the nuclear pore that affects cytoplasmic-nuclear transport. BCL2-associated X protein (BAX) and BCL2 antagonist/killer 1 (BAK1), B-cell leukemia/lymphoma 2 (BCL2) family members, mediate mitochondrial damage to generate ROS after SINV infection. Thus, TIPARP is a viral RNA-sensing PRR that mediates antiviral responses triggered by BAX- and BAK1-dependent mitochondrial damage.</description><identifier>ISSN: 0027-8424</identifier><identifier>EISSN: 1091-6490</identifier><identifier>DOI: 10.1073/pnas.1621508114</identifier><identifier>PMID: 28213497</identifier><language>eng</language><publisher>United States: National Academy of Sciences</publisher><subject>Active Transport, Cell Nucleus - genetics ; Active Transport, Cell Nucleus - immunology ; bcl-2 Homologous Antagonist-Killer Protein - genetics ; bcl-2 Homologous Antagonist-Killer Protein - immunology ; bcl-2-Associated X Protein - genetics ; bcl-2-Associated X Protein - immunology ; Biological Sciences ; Cytoplasm ; Cytoplasm - genetics ; Cytoplasm - immunology ; Host-Pathogen Interactions - genetics ; Host-Pathogen Interactions - immunology ; Humans ; Immune system ; Immunity, Innate - genetics ; Mitochondria - genetics ; Mitochondria - pathology ; Mitochondria - virology ; Poly(ADP-ribose) Polymerases - genetics ; Poly(ADP-ribose) Polymerases - immunology ; Proteins ; Reactive Oxygen Species - metabolism ; Receptors, Pattern Recognition - genetics ; Receptors, Pattern Recognition - immunology ; Ribonucleic acid ; RNA ; RNA Viruses - genetics ; RNA Viruses - immunology ; Sindbis virus ; Sindbis Virus - genetics ; Sindbis Virus - immunology ; Sindbis Virus - pathogenicity ; Viral infections</subject><ispartof>Proceedings of the National Academy of Sciences - PNAS, 2017-03, Vol.114 (10), p.2681-2686</ispartof><rights>Volumes 1–89 and 106–114, copyright as a collective work only; author(s) retains copyright to individual articles</rights><rights>Copyright National Academy of Sciences Mar 7, 2017</rights><lds50>peer_reviewed</lds50><oa>free_for_read</oa><woscitedreferencessubscribed>false</woscitedreferencessubscribed><citedby>FETCH-LOGICAL-c542t-b5c2001229f3a0243eb4842b5784d125e65fe1bac3158d3c6ea4d8565707835b3</citedby><cites>FETCH-LOGICAL-c542t-b5c2001229f3a0243eb4842b5784d125e65fe1bac3158d3c6ea4d8565707835b3</cites></display><links><openurl>$$Topenurl_article</openurl><openurlfulltext>$$Topenurlfull_article</openurlfulltext><thumbnail>$$Tsyndetics_thumb_exl</thumbnail><linktopdf>$$Uhttps://www.jstor.org/stable/pdf/26480089$$EPDF$$P50$$Gjstor$$H</linktopdf><linktohtml>$$Uhttps://www.jstor.org/stable/26480089$$EHTML$$P50$$Gjstor$$H</linktohtml><link.rule.ids>230,314,727,780,784,803,885,27924,27925,53791,53793,58017,58250</link.rule.ids><backlink>$$Uhttps://www.ncbi.nlm.nih.gov/pubmed/28213497$$D View this record in MEDLINE/PubMed$$Hfree_for_read</backlink></links><search><creatorcontrib>Kozaki, Tatsuya</creatorcontrib><creatorcontrib>Komano, Jun</creatorcontrib><creatorcontrib>Kanbayashi, Daiki</creatorcontrib><creatorcontrib>Takahama, Michihiro</creatorcontrib><creatorcontrib>Misawa, Takuma</creatorcontrib><creatorcontrib>Satoh, Takashi</creatorcontrib><creatorcontrib>Takeuchi, Osamu</creatorcontrib><creatorcontrib>Kawai, Taro</creatorcontrib><creatorcontrib>Shimizu, Shigeomi</creatorcontrib><creatorcontrib>Matsuura, Yoshiharu</creatorcontrib><creatorcontrib>Akira, Shizuo</creatorcontrib><creatorcontrib>Saitoh, Tatsuya</creatorcontrib><title>Mitochondrial damage elicits a TCDD-inducible poly(ADP-ribose) polymerase-mediated antiviral response</title><title>Proceedings of the National Academy of Sciences - PNAS</title><addtitle>Proc Natl Acad Sci U S A</addtitle><description>The innate immune system senses RNA viruses by pattern recognition receptors (PRRs) and protects the host from virus infection. PRRs mediate the production of immune modulatory factors and direct the elimination of RNA viruses. Here, we show a unique PRR that mediates antiviral response. Tetrachlorodibenzo-p-dioxin (TCDD)-inducible poly(ADP ribose) polymerase (TIPARP), a Cysteine3 Histidine (CCCH)-type zinc finger-containing protein, binds to Sindbis virus (SINV) RNA via its zinc finger domain and recruits an exosome to induce viral RNA degradation. TIPARP typically localizes in the nucleus, but it accumulates in the cytoplasm after SINV infection, allowing targeting of cytoplasmic SINV RNA. Redistribution of TIPARP is induced by reactive oxygen species (ROS)-dependent oxidization of the nuclear pore that affects cytoplasmic-nuclear transport. BCL2-associated X protein (BAX) and BCL2 antagonist/killer 1 (BAK1), B-cell leukemia/lymphoma 2 (BCL2) family members, mediate mitochondrial damage to generate ROS after SINV infection. Thus, TIPARP is a viral RNA-sensing PRR that mediates antiviral responses triggered by BAX- and BAK1-dependent mitochondrial damage.</description><subject>Active Transport, Cell Nucleus - genetics</subject><subject>Active Transport, Cell Nucleus - immunology</subject><subject>bcl-2 Homologous Antagonist-Killer Protein - genetics</subject><subject>bcl-2 Homologous Antagonist-Killer Protein - immunology</subject><subject>bcl-2-Associated X Protein - genetics</subject><subject>bcl-2-Associated X Protein - immunology</subject><subject>Biological Sciences</subject><subject>Cytoplasm</subject><subject>Cytoplasm - genetics</subject><subject>Cytoplasm - immunology</subject><subject>Host-Pathogen Interactions - genetics</subject><subject>Host-Pathogen Interactions - immunology</subject><subject>Humans</subject><subject>Immune system</subject><subject>Immunity, Innate - genetics</subject><subject>Mitochondria - genetics</subject><subject>Mitochondria - pathology</subject><subject>Mitochondria - virology</subject><subject>Poly(ADP-ribose) Polymerases - genetics</subject><subject>Poly(ADP-ribose) Polymerases - immunology</subject><subject>Proteins</subject><subject>Reactive Oxygen Species - metabolism</subject><subject>Receptors, Pattern Recognition - genetics</subject><subject>Receptors, Pattern Recognition - immunology</subject><subject>Ribonucleic acid</subject><subject>RNA</subject><subject>RNA Viruses - genetics</subject><subject>RNA Viruses - immunology</subject><subject>Sindbis virus</subject><subject>Sindbis Virus - genetics</subject><subject>Sindbis Virus - immunology</subject><subject>Sindbis Virus - pathogenicity</subject><subject>Viral infections</subject><issn>0027-8424</issn><issn>1091-6490</issn><fulltext>true</fulltext><rsrctype>article</rsrctype><creationdate>2017</creationdate><recordtype>article</recordtype><sourceid>EIF</sourceid><recordid>eNqNkc1v1DAQxS0EokvhzAkUiUs5pB1_xr4gVbstIBXBoZwtx5ltvUriYCeV-t_jsqUFTpws-f38_GYeIa8pHFNo-Mk0unxMFaMSNKXiCVlRMLRWwsBTsgJgTa0FEwfkRc47ADBSw3NywDSjXJhmRfBLmKO_jmOXguurzg3uCivsgw9zrlx1ud5s6jB2iw9tj9UU-9uj0823OoU2Znz_62LA5DLWA3bBzdhVbpzDTUjFLmGe4pjxJXm2dX3GV_fnIfl-fna5_lRffP34eX16UXsp2Fy30jMAypjZcgdMcGxFid_KRouOMolKbpG2znMqdce9Qic6LZVsoNFctvyQfNj7Tktb4ngc5xLDTikMLt3a6IL9WxnDtb2KN1Zy0Siqi8HRvUGKPxbMsx1C9tj3bsS4ZEu1oeVDYf4HVcYoaYwp6Lt_0F1c0lg2UShNjTKgeKFO9pRPMeeE24fcFOxd2_aubfvYdnnx9s9xH_jf9RbgzR7Y5TmmR10JDaAN_wmqJa-e</recordid><startdate>20170307</startdate><enddate>20170307</enddate><creator>Kozaki, Tatsuya</creator><creator>Komano, Jun</creator><creator>Kanbayashi, Daiki</creator><creator>Takahama, Michihiro</creator><creator>Misawa, Takuma</creator><creator>Satoh, Takashi</creator><creator>Takeuchi, Osamu</creator><creator>Kawai, Taro</creator><creator>Shimizu, Shigeomi</creator><creator>Matsuura, Yoshiharu</creator><creator>Akira, Shizuo</creator><creator>Saitoh, Tatsuya</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>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>7X8</scope><scope>5PM</scope></search><sort><creationdate>20170307</creationdate><title>Mitochondrial damage elicits a TCDD-inducible poly(ADP-ribose) polymerase-mediated antiviral response</title><author>Kozaki, Tatsuya ; Komano, Jun ; Kanbayashi, Daiki ; Takahama, Michihiro ; Misawa, Takuma ; Satoh, Takashi ; Takeuchi, Osamu ; Kawai, Taro ; Shimizu, Shigeomi ; Matsuura, Yoshiharu ; Akira, Shizuo ; Saitoh, Tatsuya</author></sort><facets><frbrtype>5</frbrtype><frbrgroupid>cdi_FETCH-LOGICAL-c542t-b5c2001229f3a0243eb4842b5784d125e65fe1bac3158d3c6ea4d8565707835b3</frbrgroupid><rsrctype>articles</rsrctype><prefilter>articles</prefilter><language>eng</language><creationdate>2017</creationdate><topic>Active Transport, Cell Nucleus - genetics</topic><topic>Active Transport, Cell Nucleus - immunology</topic><topic>bcl-2 Homologous Antagonist-Killer Protein - genetics</topic><topic>bcl-2 Homologous Antagonist-Killer Protein - immunology</topic><topic>bcl-2-Associated X Protein - genetics</topic><topic>bcl-2-Associated X Protein - immunology</topic><topic>Biological Sciences</topic><topic>Cytoplasm</topic><topic>Cytoplasm - genetics</topic><topic>Cytoplasm - immunology</topic><topic>Host-Pathogen Interactions - genetics</topic><topic>Host-Pathogen Interactions - immunology</topic><topic>Humans</topic><topic>Immune system</topic><topic>Immunity, Innate - genetics</topic><topic>Mitochondria - genetics</topic><topic>Mitochondria - pathology</topic><topic>Mitochondria - virology</topic><topic>Poly(ADP-ribose) Polymerases - genetics</topic><topic>Poly(ADP-ribose) Polymerases - immunology</topic><topic>Proteins</topic><topic>Reactive Oxygen Species - metabolism</topic><topic>Receptors, Pattern Recognition - genetics</topic><topic>Receptors, Pattern Recognition - immunology</topic><topic>Ribonucleic acid</topic><topic>RNA</topic><topic>RNA Viruses - genetics</topic><topic>RNA Viruses - immunology</topic><topic>Sindbis virus</topic><topic>Sindbis Virus - genetics</topic><topic>Sindbis Virus - immunology</topic><topic>Sindbis Virus - pathogenicity</topic><topic>Viral infections</topic><toplevel>peer_reviewed</toplevel><toplevel>online_resources</toplevel><creatorcontrib>Kozaki, Tatsuya</creatorcontrib><creatorcontrib>Komano, Jun</creatorcontrib><creatorcontrib>Kanbayashi, Daiki</creatorcontrib><creatorcontrib>Takahama, Michihiro</creatorcontrib><creatorcontrib>Misawa, Takuma</creatorcontrib><creatorcontrib>Satoh, Takashi</creatorcontrib><creatorcontrib>Takeuchi, Osamu</creatorcontrib><creatorcontrib>Kawai, Taro</creatorcontrib><creatorcontrib>Shimizu, Shigeomi</creatorcontrib><creatorcontrib>Matsuura, Yoshiharu</creatorcontrib><creatorcontrib>Akira, Shizuo</creatorcontrib><creatorcontrib>Saitoh, Tatsuya</creatorcontrib><collection>Medline</collection><collection>MEDLINE</collection><collection>MEDLINE (Ovid)</collection><collection>MEDLINE</collection><collection>MEDLINE</collection><collection>PubMed</collection><collection>CrossRef</collection><collection>Animal Behavior Abstracts</collection><collection>Bacteriology Abstracts (Microbiology B)</collection><collection>Calcium & Calcified Tissue Abstracts</collection><collection>Chemoreception Abstracts</collection><collection>Ecology Abstracts</collection><collection>Entomology Abstracts (Full archive)</collection><collection>Immunology Abstracts</collection><collection>Neurosciences Abstracts</collection><collection>Nucleic Acids Abstracts</collection><collection>Oncogenes and Growth Factors Abstracts</collection><collection>Virology and AIDS Abstracts</collection><collection>Technology Research Database</collection><collection>Environmental Sciences and Pollution Management</collection><collection>Engineering Research Database</collection><collection>AIDS and Cancer Research Abstracts</collection><collection>Algology Mycology and Protozoology Abstracts (Microbiology C)</collection><collection>Biotechnology and BioEngineering Abstracts</collection><collection>Genetics Abstracts</collection><collection>MEDLINE - Academic</collection><collection>PubMed Central (Full Participant titles)</collection><jtitle>Proceedings of the National Academy of Sciences - PNAS</jtitle></facets><delivery><delcategory>Remote Search Resource</delcategory><fulltext>fulltext</fulltext></delivery><addata><au>Kozaki, Tatsuya</au><au>Komano, Jun</au><au>Kanbayashi, Daiki</au><au>Takahama, Michihiro</au><au>Misawa, Takuma</au><au>Satoh, Takashi</au><au>Takeuchi, Osamu</au><au>Kawai, Taro</au><au>Shimizu, Shigeomi</au><au>Matsuura, Yoshiharu</au><au>Akira, Shizuo</au><au>Saitoh, Tatsuya</au><format>journal</format><genre>article</genre><ristype>JOUR</ristype><atitle>Mitochondrial damage elicits a TCDD-inducible poly(ADP-ribose) polymerase-mediated antiviral response</atitle><jtitle>Proceedings of the National Academy of Sciences - PNAS</jtitle><addtitle>Proc Natl Acad Sci U S A</addtitle><date>2017-03-07</date><risdate>2017</risdate><volume>114</volume><issue>10</issue><spage>2681</spage><epage>2686</epage><pages>2681-2686</pages><issn>0027-8424</issn><eissn>1091-6490</eissn><abstract>The innate immune system senses RNA viruses by pattern recognition receptors (PRRs) and protects the host from virus infection. PRRs mediate the production of immune modulatory factors and direct the elimination of RNA viruses. Here, we show a unique PRR that mediates antiviral response. Tetrachlorodibenzo-p-dioxin (TCDD)-inducible poly(ADP ribose) polymerase (TIPARP), a Cysteine3 Histidine (CCCH)-type zinc finger-containing protein, binds to Sindbis virus (SINV) RNA via its zinc finger domain and recruits an exosome to induce viral RNA degradation. TIPARP typically localizes in the nucleus, but it accumulates in the cytoplasm after SINV infection, allowing targeting of cytoplasmic SINV RNA. Redistribution of TIPARP is induced by reactive oxygen species (ROS)-dependent oxidization of the nuclear pore that affects cytoplasmic-nuclear transport. BCL2-associated X protein (BAX) and BCL2 antagonist/killer 1 (BAK1), B-cell leukemia/lymphoma 2 (BCL2) family members, mediate mitochondrial damage to generate ROS after SINV infection. Thus, TIPARP is a viral RNA-sensing PRR that mediates antiviral responses triggered by BAX- and BAK1-dependent mitochondrial damage.</abstract><cop>United States</cop><pub>National Academy of Sciences</pub><pmid>28213497</pmid><doi>10.1073/pnas.1621508114</doi><tpages>6</tpages><oa>free_for_read</oa></addata></record> |
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| subjects | Active Transport, Cell Nucleus - genetics Active Transport, Cell Nucleus - immunology bcl-2 Homologous Antagonist-Killer Protein - genetics bcl-2 Homologous Antagonist-Killer Protein - immunology bcl-2-Associated X Protein - genetics bcl-2-Associated X Protein - immunology Biological Sciences Cytoplasm Cytoplasm - genetics Cytoplasm - immunology Host-Pathogen Interactions - genetics Host-Pathogen Interactions - immunology Humans Immune system Immunity, Innate - genetics Mitochondria - genetics Mitochondria - pathology Mitochondria - virology Poly(ADP-ribose) Polymerases - genetics Poly(ADP-ribose) Polymerases - immunology Proteins Reactive Oxygen Species - metabolism Receptors, Pattern Recognition - genetics Receptors, Pattern Recognition - immunology Ribonucleic acid RNA RNA Viruses - genetics RNA Viruses - immunology Sindbis virus Sindbis Virus - genetics Sindbis Virus - immunology Sindbis Virus - pathogenicity Viral infections |
| title | Mitochondrial damage elicits a TCDD-inducible poly(ADP-ribose) polymerase-mediated antiviral response |
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