Nuclear hnRNPA2B1 initiates and amplifies the innate immune response to DNA viruses
DNA viruses typically eject genomic DNA into the nuclei of host cells after entry. It is unclear, however, how nuclear pathogen-derived DNA triggers innate immune responses. We report that heterogeneous nuclear ribonucleoprotein A2B1 (hnRNPA2B1) recognizes pathogenic DNA and amplifies interferon-α/β...
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| Veröffentlicht in: | Science (American Association for the Advancement of Science) 2019-08, Vol.365 (6454), p.656-656 |
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| creator | Wang, Lei Wen, Mingyue Cao, Xuetao |
| description | DNA viruses typically eject genomic DNA into the nuclei of host cells after entry. It is unclear, however, how nuclear pathogen-derived DNA triggers innate immune responses. We report that heterogeneous nuclear ribonucleoprotein A2B1 (hnRNPA2B1) recognizes pathogenic DNA and amplifies interferon-α/β (IFN-α/β) production. Upon DNA virus infection, nuclear-localized hnRNPA2B1 senses viral DNA, homodimerizes, and is then demethylated at arginine-226 by the arginine demethylase JMJD6. This results in hnRNPA2B1 translocation to the cytoplasm where it activates the TANK-binding kinase 1-interferon regulatory factor 3 (TBK1-IRF3) pathway, leading to IFN-α/β production. Additionally, hnRNPA2B1 facilitates
-methyladenosine (m
A) modification and nucleocytoplasmic trafficking of
,
, and
messenger RNAs. This, in turn, amplifies the activation of cytoplasmic TBK1-IRF3 mediated by these factors. Thus, hnRNPA2B1 plays important roles in initiating IFN-α/β production and enhancing stimulator of interferon genes (STING)-dependent cytoplasmic antiviral signaling. |
| doi_str_mv | 10.1126/science.aav0758 |
| format | Article |
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-methyladenosine (m
A) modification and nucleocytoplasmic trafficking of
,
, and
messenger RNAs. This, in turn, amplifies the activation of cytoplasmic TBK1-IRF3 mediated by these factors. Thus, hnRNPA2B1 plays important roles in initiating IFN-α/β production and enhancing stimulator of interferon genes (STING)-dependent cytoplasmic antiviral signaling.</description><identifier>ISSN: 0036-8075</identifier><identifier>EISSN: 1095-9203</identifier><identifier>DOI: 10.1126/science.aav0758</identifier><identifier>PMID: 31320558</identifier><language>eng</language><publisher>United States: American Association for the Advancement of Science</publisher><subject>Activation ; Adenosine - analogs & derivatives ; Adenosine - metabolism ; Amplification ; Animals ; Arginine ; Binding ; Body fat ; Cell Nucleus - immunology ; Cell Nucleus - virology ; Cytokines ; Cytoplasm ; Cytoplasm - metabolism ; Cytosol ; Demethylation ; Deoxyribonucleic acid ; Dimerization ; Dimers ; DNA ; DNA Virus Infections - immunology ; DNA viruses ; DNA, Viral - immunology ; Eukaryotes ; Feedback (Response) ; Gene expression ; Genes ; HEK293 Cells ; Herpes simplex ; Herpes viruses ; Herpesvirus 1, Human - immunology ; Heterogeneous-Nuclear Ribonucleoprotein Group A-B - genetics ; Heterogeneous-Nuclear Ribonucleoprotein Group A-B - metabolism ; Humans ; Immune response ; Immune system ; Immunity, Innate ; Infections ; Inflammation ; Innate immunity ; Interferon ; Interferon regulatory factor ; Interferon Regulatory Factor-3 ; Interferon-alpha - metabolism ; Interferon-beta - metabolism ; Interleukin 6 ; Jumonji Domain-Containing Histone Demethylases - metabolism ; Kinases ; Macrophages ; Membrane Proteins - metabolism ; Methylation ; Mice ; Mice, Knockout ; Microorganisms ; Mutation ; N6-methyladenosine ; Nuclear Proteins - metabolism ; Nuclei ; Nuclei (cytology) ; Nucleic acids ; Nucleotidyltransferases - metabolism ; Obesity ; Pathogens ; Phosphoproteins - metabolism ; Protein Transport ; Protein-Serine-Threonine Kinases - metabolism ; Protein-tyrosine kinase ; Proteins ; RAW 264.7 Cells ; RESEARCH ARTICLE SUMMARY ; RNA viruses ; Sensors ; Signal transduction ; Translocation ; Tyrosine ; Viral infections ; Viruses ; α-Interferon ; β-Interferon ; γ-Interferon</subject><ispartof>Science (American Association for the Advancement of Science), 2019-08, Vol.365 (6454), p.656-656</ispartof><rights>Copyright © 2019 The Authors, some rights reserved; exclusive licensee American Association for the Advancement of Science. No claim to original U.S. Government Works.</rights><rights>Copyright © 2019 The Authors, some rights reserved; exclusive licensee American Association for the Advancement of Science. No claim to original U.S. Government Works</rights><lds50>peer_reviewed</lds50><oa>free_for_read</oa><woscitedreferencessubscribed>false</woscitedreferencessubscribed><citedby>FETCH-LOGICAL-c454t-864663050c8184c0c6672c85600d7af57826844ae402b90037e8aacf86ba23da3</citedby><cites>FETCH-LOGICAL-c454t-864663050c8184c0c6672c85600d7af57826844ae402b90037e8aacf86ba23da3</cites><orcidid>0000-0001-9372-2579 ; 0000-0001-5943-3386 ; 0000-0001-9677-7647</orcidid></display><links><openurl>$$Topenurl_article</openurl><openurlfulltext>$$Topenurlfull_article</openurlfulltext><thumbnail>$$Tsyndetics_thumb_exl</thumbnail><link.rule.ids>314,776,780,2871,2872,27901,27902</link.rule.ids><backlink>$$Uhttps://www.ncbi.nlm.nih.gov/pubmed/31320558$$D View this record in MEDLINE/PubMed$$Hfree_for_read</backlink></links><search><creatorcontrib>Wang, Lei</creatorcontrib><creatorcontrib>Wen, Mingyue</creatorcontrib><creatorcontrib>Cao, Xuetao</creatorcontrib><title>Nuclear hnRNPA2B1 initiates and amplifies the innate immune response to DNA viruses</title><title>Science (American Association for the Advancement of Science)</title><addtitle>Science</addtitle><description>DNA viruses typically eject genomic DNA into the nuclei of host cells after entry. It is unclear, however, how nuclear pathogen-derived DNA triggers innate immune responses. We report that heterogeneous nuclear ribonucleoprotein A2B1 (hnRNPA2B1) recognizes pathogenic DNA and amplifies interferon-α/β (IFN-α/β) production. Upon DNA virus infection, nuclear-localized hnRNPA2B1 senses viral DNA, homodimerizes, and is then demethylated at arginine-226 by the arginine demethylase JMJD6. This results in hnRNPA2B1 translocation to the cytoplasm where it activates the TANK-binding kinase 1-interferon regulatory factor 3 (TBK1-IRF3) pathway, leading to IFN-α/β production. Additionally, hnRNPA2B1 facilitates
-methyladenosine (m
A) modification and nucleocytoplasmic trafficking of
,
, and
messenger RNAs. This, in turn, amplifies the activation of cytoplasmic TBK1-IRF3 mediated by these factors. Thus, hnRNPA2B1 plays important roles in initiating IFN-α/β production and enhancing stimulator of interferon genes (STING)-dependent cytoplasmic antiviral signaling.</description><subject>Activation</subject><subject>Adenosine - analogs & derivatives</subject><subject>Adenosine - metabolism</subject><subject>Amplification</subject><subject>Animals</subject><subject>Arginine</subject><subject>Binding</subject><subject>Body fat</subject><subject>Cell Nucleus - immunology</subject><subject>Cell Nucleus - virology</subject><subject>Cytokines</subject><subject>Cytoplasm</subject><subject>Cytoplasm - metabolism</subject><subject>Cytosol</subject><subject>Demethylation</subject><subject>Deoxyribonucleic acid</subject><subject>Dimerization</subject><subject>Dimers</subject><subject>DNA</subject><subject>DNA Virus Infections - immunology</subject><subject>DNA viruses</subject><subject>DNA, Viral - immunology</subject><subject>Eukaryotes</subject><subject>Feedback (Response)</subject><subject>Gene expression</subject><subject>Genes</subject><subject>HEK293 Cells</subject><subject>Herpes simplex</subject><subject>Herpes viruses</subject><subject>Herpesvirus 1, Human - immunology</subject><subject>Heterogeneous-Nuclear Ribonucleoprotein Group A-B - genetics</subject><subject>Heterogeneous-Nuclear Ribonucleoprotein Group A-B - metabolism</subject><subject>Humans</subject><subject>Immune response</subject><subject>Immune system</subject><subject>Immunity, Innate</subject><subject>Infections</subject><subject>Inflammation</subject><subject>Innate immunity</subject><subject>Interferon</subject><subject>Interferon regulatory factor</subject><subject>Interferon Regulatory Factor-3</subject><subject>Interferon-alpha - metabolism</subject><subject>Interferon-beta - metabolism</subject><subject>Interleukin 6</subject><subject>Jumonji Domain-Containing Histone Demethylases - metabolism</subject><subject>Kinases</subject><subject>Macrophages</subject><subject>Membrane Proteins - metabolism</subject><subject>Methylation</subject><subject>Mice</subject><subject>Mice, Knockout</subject><subject>Microorganisms</subject><subject>Mutation</subject><subject>N6-methyladenosine</subject><subject>Nuclear Proteins - metabolism</subject><subject>Nuclei</subject><subject>Nuclei (cytology)</subject><subject>Nucleic acids</subject><subject>Nucleotidyltransferases - metabolism</subject><subject>Obesity</subject><subject>Pathogens</subject><subject>Phosphoproteins - metabolism</subject><subject>Protein Transport</subject><subject>Protein-Serine-Threonine Kinases - metabolism</subject><subject>Protein-tyrosine kinase</subject><subject>Proteins</subject><subject>RAW 264.7 Cells</subject><subject>RESEARCH ARTICLE SUMMARY</subject><subject>RNA viruses</subject><subject>Sensors</subject><subject>Signal transduction</subject><subject>Translocation</subject><subject>Tyrosine</subject><subject>Viral infections</subject><subject>Viruses</subject><subject>α-Interferon</subject><subject>β-Interferon</subject><subject>γ-Interferon</subject><issn>0036-8075</issn><issn>1095-9203</issn><fulltext>true</fulltext><rsrctype>article</rsrctype><creationdate>2019</creationdate><recordtype>article</recordtype><sourceid>EIF</sourceid><recordid>eNpdkElPwzAQRi0EgrKcOYEsceGSMl7iOMeyI1UFsZwj150IV4lT7ASJf49RCwdOo9F7M5r5CDlmMGaMq4toHXqLY2M-ocj1FhkxKPOs5CC2yQhAqEwnsEf2Y1wCJFaKXbInmOCQ53pEXmaDbdAE-u6fZ08Tfsmo8653psdIjV9Q064aV7vU9e-YmE-EurYdPNKAcdX5iLTv6PVsQj9dGCLGQ7JTmybi0aYekLfbm9er-2z6ePdwNZlmVuayz7SSSgnIwWqmpQWrVMGtzhXAojB1XmiutJQGJfB5mX4pUBtja63mhouFEQfkfL13FbqPAWNftS5abBrjsRtixblinDMlyqSe_VOX3RB8ui5ZhdCSFRKSdbG2bOhiDFhXq-BaE74qBtVP3tUm72qTd5o43ewd5i0u_vzfgJNwshaWse_CH-cqfcdBim_Y-IUL</recordid><startdate>20190816</startdate><enddate>20190816</enddate><creator>Wang, Lei</creator><creator>Wen, Mingyue</creator><creator>Cao, Xuetao</creator><general>American Association for the Advancement of Science</general><general>The American Association for the Advancement of Science</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>7QF</scope><scope>7QG</scope><scope>7QL</scope><scope>7QP</scope><scope>7QQ</scope><scope>7QR</scope><scope>7SC</scope><scope>7SE</scope><scope>7SN</scope><scope>7SP</scope><scope>7SR</scope><scope>7SS</scope><scope>7T7</scope><scope>7TA</scope><scope>7TB</scope><scope>7TK</scope><scope>7TM</scope><scope>7U5</scope><scope>7U9</scope><scope>8BQ</scope><scope>8FD</scope><scope>C1K</scope><scope>F28</scope><scope>FR3</scope><scope>H8D</scope><scope>H8G</scope><scope>H94</scope><scope>JG9</scope><scope>JQ2</scope><scope>K9.</scope><scope>KR7</scope><scope>L7M</scope><scope>L~C</scope><scope>L~D</scope><scope>M7N</scope><scope>P64</scope><scope>RC3</scope><scope>7X8</scope><orcidid>https://orcid.org/0000-0001-9372-2579</orcidid><orcidid>https://orcid.org/0000-0001-5943-3386</orcidid><orcidid>https://orcid.org/0000-0001-9677-7647</orcidid></search><sort><creationdate>20190816</creationdate><title>Nuclear hnRNPA2B1 initiates and amplifies the innate immune response to DNA viruses</title><author>Wang, Lei ; Wen, Mingyue ; Cao, Xuetao</author></sort><facets><frbrtype>5</frbrtype><frbrgroupid>cdi_FETCH-LOGICAL-c454t-864663050c8184c0c6672c85600d7af57826844ae402b90037e8aacf86ba23da3</frbrgroupid><rsrctype>articles</rsrctype><prefilter>articles</prefilter><language>eng</language><creationdate>2019</creationdate><topic>Activation</topic><topic>Adenosine - analogs & derivatives</topic><topic>Adenosine - metabolism</topic><topic>Amplification</topic><topic>Animals</topic><topic>Arginine</topic><topic>Binding</topic><topic>Body fat</topic><topic>Cell Nucleus - immunology</topic><topic>Cell Nucleus - virology</topic><topic>Cytokines</topic><topic>Cytoplasm</topic><topic>Cytoplasm - metabolism</topic><topic>Cytosol</topic><topic>Demethylation</topic><topic>Deoxyribonucleic acid</topic><topic>Dimerization</topic><topic>Dimers</topic><topic>DNA</topic><topic>DNA Virus Infections - immunology</topic><topic>DNA viruses</topic><topic>DNA, Viral - immunology</topic><topic>Eukaryotes</topic><topic>Feedback (Response)</topic><topic>Gene expression</topic><topic>Genes</topic><topic>HEK293 Cells</topic><topic>Herpes simplex</topic><topic>Herpes viruses</topic><topic>Herpesvirus 1, Human - immunology</topic><topic>Heterogeneous-Nuclear Ribonucleoprotein Group A-B - genetics</topic><topic>Heterogeneous-Nuclear Ribonucleoprotein Group A-B - metabolism</topic><topic>Humans</topic><topic>Immune response</topic><topic>Immune system</topic><topic>Immunity, Innate</topic><topic>Infections</topic><topic>Inflammation</topic><topic>Innate immunity</topic><topic>Interferon</topic><topic>Interferon regulatory factor</topic><topic>Interferon Regulatory Factor-3</topic><topic>Interferon-alpha - metabolism</topic><topic>Interferon-beta - metabolism</topic><topic>Interleukin 6</topic><topic>Jumonji Domain-Containing Histone Demethylases - metabolism</topic><topic>Kinases</topic><topic>Macrophages</topic><topic>Membrane Proteins - metabolism</topic><topic>Methylation</topic><topic>Mice</topic><topic>Mice, Knockout</topic><topic>Microorganisms</topic><topic>Mutation</topic><topic>N6-methyladenosine</topic><topic>Nuclear Proteins - metabolism</topic><topic>Nuclei</topic><topic>Nuclei (cytology)</topic><topic>Nucleic acids</topic><topic>Nucleotidyltransferases - metabolism</topic><topic>Obesity</topic><topic>Pathogens</topic><topic>Phosphoproteins - metabolism</topic><topic>Protein Transport</topic><topic>Protein-Serine-Threonine Kinases - metabolism</topic><topic>Protein-tyrosine kinase</topic><topic>Proteins</topic><topic>RAW 264.7 Cells</topic><topic>RESEARCH ARTICLE SUMMARY</topic><topic>RNA viruses</topic><topic>Sensors</topic><topic>Signal transduction</topic><topic>Translocation</topic><topic>Tyrosine</topic><topic>Viral infections</topic><topic>Viruses</topic><topic>α-Interferon</topic><topic>β-Interferon</topic><topic>γ-Interferon</topic><toplevel>peer_reviewed</toplevel><toplevel>online_resources</toplevel><creatorcontrib>Wang, Lei</creatorcontrib><creatorcontrib>Wen, Mingyue</creatorcontrib><creatorcontrib>Cao, Xuetao</creatorcontrib><collection>Medline</collection><collection>MEDLINE</collection><collection>MEDLINE (Ovid)</collection><collection>MEDLINE</collection><collection>MEDLINE</collection><collection>PubMed</collection><collection>CrossRef</collection><collection>Aluminium Industry Abstracts</collection><collection>Animal Behavior Abstracts</collection><collection>Bacteriology Abstracts (Microbiology B)</collection><collection>Calcium & Calcified Tissue Abstracts</collection><collection>Ceramic Abstracts</collection><collection>Chemoreception Abstracts</collection><collection>Computer and Information Systems Abstracts</collection><collection>Corrosion Abstracts</collection><collection>Ecology Abstracts</collection><collection>Electronics & Communications Abstracts</collection><collection>Engineered Materials Abstracts</collection><collection>Entomology Abstracts (Full archive)</collection><collection>Industrial and Applied Microbiology Abstracts (Microbiology A)</collection><collection>Materials Business File</collection><collection>Mechanical & Transportation Engineering Abstracts</collection><collection>Neurosciences Abstracts</collection><collection>Nucleic Acids Abstracts</collection><collection>Solid State and Superconductivity Abstracts</collection><collection>Virology and AIDS Abstracts</collection><collection>METADEX</collection><collection>Technology Research Database</collection><collection>Environmental Sciences and Pollution Management</collection><collection>ANTE: Abstracts in New Technology & Engineering</collection><collection>Engineering Research Database</collection><collection>Aerospace Database</collection><collection>Copper Technical Reference Library</collection><collection>AIDS and Cancer Research Abstracts</collection><collection>Materials Research Database</collection><collection>ProQuest Computer Science Collection</collection><collection>ProQuest Health & Medical Complete (Alumni)</collection><collection>Civil Engineering Abstracts</collection><collection>Advanced Technologies Database with Aerospace</collection><collection>Computer and Information Systems Abstracts Academic</collection><collection>Computer and Information Systems Abstracts Professional</collection><collection>Algology Mycology and Protozoology Abstracts (Microbiology C)</collection><collection>Biotechnology and BioEngineering Abstracts</collection><collection>Genetics Abstracts</collection><collection>MEDLINE - Academic</collection><jtitle>Science (American Association for the Advancement of Science)</jtitle></facets><delivery><delcategory>Remote Search Resource</delcategory><fulltext>fulltext</fulltext></delivery><addata><au>Wang, Lei</au><au>Wen, Mingyue</au><au>Cao, Xuetao</au><format>journal</format><genre>article</genre><ristype>JOUR</ristype><atitle>Nuclear hnRNPA2B1 initiates and amplifies the innate immune response to DNA viruses</atitle><jtitle>Science (American Association for the Advancement of Science)</jtitle><addtitle>Science</addtitle><date>2019-08-16</date><risdate>2019</risdate><volume>365</volume><issue>6454</issue><spage>656</spage><epage>656</epage><pages>656-656</pages><issn>0036-8075</issn><eissn>1095-9203</eissn><abstract>DNA viruses typically eject genomic DNA into the nuclei of host cells after entry. It is unclear, however, how nuclear pathogen-derived DNA triggers innate immune responses. We report that heterogeneous nuclear ribonucleoprotein A2B1 (hnRNPA2B1) recognizes pathogenic DNA and amplifies interferon-α/β (IFN-α/β) production. Upon DNA virus infection, nuclear-localized hnRNPA2B1 senses viral DNA, homodimerizes, and is then demethylated at arginine-226 by the arginine demethylase JMJD6. This results in hnRNPA2B1 translocation to the cytoplasm where it activates the TANK-binding kinase 1-interferon regulatory factor 3 (TBK1-IRF3) pathway, leading to IFN-α/β production. Additionally, hnRNPA2B1 facilitates
-methyladenosine (m
A) modification and nucleocytoplasmic trafficking of
,
, and
messenger RNAs. This, in turn, amplifies the activation of cytoplasmic TBK1-IRF3 mediated by these factors. Thus, hnRNPA2B1 plays important roles in initiating IFN-α/β production and enhancing stimulator of interferon genes (STING)-dependent cytoplasmic antiviral signaling.</abstract><cop>United States</cop><pub>American Association for the Advancement of Science</pub><pmid>31320558</pmid><doi>10.1126/science.aav0758</doi><tpages>1</tpages><orcidid>https://orcid.org/0000-0001-9372-2579</orcidid><orcidid>https://orcid.org/0000-0001-5943-3386</orcidid><orcidid>https://orcid.org/0000-0001-9677-7647</orcidid><oa>free_for_read</oa></addata></record> |
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| ispartof | Science (American Association for the Advancement of Science), 2019-08, Vol.365 (6454), p.656-656 |
| issn | 0036-8075 1095-9203 |
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| source | American Association for the Advancement of Science; MEDLINE |
| subjects | Activation Adenosine - analogs & derivatives Adenosine - metabolism Amplification Animals Arginine Binding Body fat Cell Nucleus - immunology Cell Nucleus - virology Cytokines Cytoplasm Cytoplasm - metabolism Cytosol Demethylation Deoxyribonucleic acid Dimerization Dimers DNA DNA Virus Infections - immunology DNA viruses DNA, Viral - immunology Eukaryotes Feedback (Response) Gene expression Genes HEK293 Cells Herpes simplex Herpes viruses Herpesvirus 1, Human - immunology Heterogeneous-Nuclear Ribonucleoprotein Group A-B - genetics Heterogeneous-Nuclear Ribonucleoprotein Group A-B - metabolism Humans Immune response Immune system Immunity, Innate Infections Inflammation Innate immunity Interferon Interferon regulatory factor Interferon Regulatory Factor-3 Interferon-alpha - metabolism Interferon-beta - metabolism Interleukin 6 Jumonji Domain-Containing Histone Demethylases - metabolism Kinases Macrophages Membrane Proteins - metabolism Methylation Mice Mice, Knockout Microorganisms Mutation N6-methyladenosine Nuclear Proteins - metabolism Nuclei Nuclei (cytology) Nucleic acids Nucleotidyltransferases - metabolism Obesity Pathogens Phosphoproteins - metabolism Protein Transport Protein-Serine-Threonine Kinases - metabolism Protein-tyrosine kinase Proteins RAW 264.7 Cells RESEARCH ARTICLE SUMMARY RNA viruses Sensors Signal transduction Translocation Tyrosine Viral infections Viruses α-Interferon β-Interferon γ-Interferon |
| title | Nuclear hnRNPA2B1 initiates and amplifies the innate immune response to DNA viruses |
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