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MCPIP1 ribonuclease exhibits broad-spectrum antiviral effects through viral RNA binding and degradation
Monocyte chemoattractant protein 1-induced protein 1 (MCPIP1), belonging to the MCPIP family with highly conserved CCCH-type zinc finger and Nedd4-BP1, YacP Nuclease domains, has been implicated in negative regulation of the cellular inflammatory responses. In this report, we demonstrate for the fir...
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| Published in: | Nucleic acids research 2013-03, Vol.41 (5), p.3314-3326 |
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| Main Authors: | , , , , , , |
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| cites | cdi_FETCH-LOGICAL-c444t-f626c42bc4513aae89c13d7c609afc29d9b674960e877921468a123f5d02ffbf3 |
| container_end_page | 3326 |
| container_issue | 5 |
| container_start_page | 3314 |
| container_title | Nucleic acids research |
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| creator | Lin, Ren-Jye Chien, Hsu-Ling Lin, Shyr-Yi Chang, Bi-Lan Yu, Han-Pang Tang, Wei-Chun Lin, Yi-Ling |
| description | Monocyte chemoattractant protein 1-induced protein 1 (MCPIP1), belonging to the MCPIP family with highly conserved CCCH-type zinc finger and Nedd4-BP1, YacP Nuclease domains, has been implicated in negative regulation of the cellular inflammatory responses. In this report, we demonstrate for the first time that this RNA-binding nuclease also targets viral RNA and possesses potent antiviral activities. Overexpression of the human MCPIP1, but not MCPIP2, MCPIP3 or MCPIP4, inhibited Japanese encephalitis virus (JEV) and dengue virus (DEN) replication. The functional analysis of MCPIP1 revealed that the activities of RNase, RNA binding and oligomerization, but not deubiqutinase, are required for its antiviral potential. Furthermore, infection of other positive-sense RNA viruses, such as sindbis virus and encephalomyocarditis virus, and negative-sense RNA virus, such as influenza virus, as well as DNA virus, such as adenovirus, can also be blocked by MCPIP1. Moreover, the endogenous MCPIP1 gene expression was induced by JEV and DEN infection, and knockdown of MCPIP1 expression enhanced the replication of JEV and DEN in human cells. Thus, MCPIP1 can act as a host innate defense via RNase activity for targeting and degrading viral RNA. |
| doi_str_mv | 10.1093/nar/gkt019 |
| format | article |
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In this report, we demonstrate for the first time that this RNA-binding nuclease also targets viral RNA and possesses potent antiviral activities. Overexpression of the human MCPIP1, but not MCPIP2, MCPIP3 or MCPIP4, inhibited Japanese encephalitis virus (JEV) and dengue virus (DEN) replication. The functional analysis of MCPIP1 revealed that the activities of RNase, RNA binding and oligomerization, but not deubiqutinase, are required for its antiviral potential. Furthermore, infection of other positive-sense RNA viruses, such as sindbis virus and encephalomyocarditis virus, and negative-sense RNA virus, such as influenza virus, as well as DNA virus, such as adenovirus, can also be blocked by MCPIP1. Moreover, the endogenous MCPIP1 gene expression was induced by JEV and DEN infection, and knockdown of MCPIP1 expression enhanced the replication of JEV and DEN in human cells. Thus, MCPIP1 can act as a host innate defense via RNase activity for targeting and degrading viral RNA.</description><identifier>ISSN: 0305-1048</identifier><identifier>EISSN: 1362-4962</identifier><identifier>DOI: 10.1093/nar/gkt019</identifier><identifier>PMID: 23355615</identifier><language>eng</language><publisher>England: Oxford University Press</publisher><subject>Amino Acid Sequence ; Conserved Sequence ; Dengue Virus - genetics ; Dengue Virus - immunology ; Dengue Virus - physiology ; Encephalitis Virus, Japanese - genetics ; Encephalitis Virus, Japanese - immunology ; Encephalitis Virus, Japanese - physiology ; HEK293 Cells ; Host-Pathogen Interactions ; Humans ; Immunity, Innate ; Molecular Sequence Data ; Nucleic Acid Enzymes ; Protein Binding ; Protein Multimerization ; Protein Structure, Tertiary ; Ribonucleases ; RNA Stability ; RNA, Viral - metabolism ; Transcription Factors - chemistry ; Transcription Factors - metabolism ; Transcription Factors - physiology ; Virus Replication ; Zinc Fingers</subject><ispartof>Nucleic acids research, 2013-03, Vol.41 (5), p.3314-3326</ispartof><rights>The Author(s) 2013. Published by Oxford University Press. 2013</rights><lds50>peer_reviewed</lds50><oa>free_for_read</oa><woscitedreferencessubscribed>false</woscitedreferencessubscribed><citedby>FETCH-LOGICAL-c444t-f626c42bc4513aae89c13d7c609afc29d9b674960e877921468a123f5d02ffbf3</citedby><cites>FETCH-LOGICAL-c444t-f626c42bc4513aae89c13d7c609afc29d9b674960e877921468a123f5d02ffbf3</cites></display><links><openurl>$$Topenurl_article</openurl><openurlfulltext>$$Topenurlfull_article</openurlfulltext><thumbnail>$$Tsyndetics_thumb_exl</thumbnail><linktopdf>$$Uhttps://www.ncbi.nlm.nih.gov/pmc/articles/PMC3597685/pdf/$$EPDF$$P50$$Gpubmedcentral$$Hfree_for_read</linktopdf><linktohtml>$$Uhttps://www.ncbi.nlm.nih.gov/pmc/articles/PMC3597685/$$EHTML$$P50$$Gpubmedcentral$$Hfree_for_read</linktohtml><link.rule.ids>230,315,730,783,787,888,27938,27939,53806,53808</link.rule.ids><backlink>$$Uhttps://www.ncbi.nlm.nih.gov/pubmed/23355615$$D View this record in MEDLINE/PubMed$$Hfree_for_read</backlink></links><search><creatorcontrib>Lin, Ren-Jye</creatorcontrib><creatorcontrib>Chien, Hsu-Ling</creatorcontrib><creatorcontrib>Lin, Shyr-Yi</creatorcontrib><creatorcontrib>Chang, Bi-Lan</creatorcontrib><creatorcontrib>Yu, Han-Pang</creatorcontrib><creatorcontrib>Tang, Wei-Chun</creatorcontrib><creatorcontrib>Lin, Yi-Ling</creatorcontrib><title>MCPIP1 ribonuclease exhibits broad-spectrum antiviral effects through viral RNA binding and degradation</title><title>Nucleic acids research</title><addtitle>Nucleic Acids Res</addtitle><description>Monocyte chemoattractant protein 1-induced protein 1 (MCPIP1), belonging to the MCPIP family with highly conserved CCCH-type zinc finger and Nedd4-BP1, YacP Nuclease domains, has been implicated in negative regulation of the cellular inflammatory responses. In this report, we demonstrate for the first time that this RNA-binding nuclease also targets viral RNA and possesses potent antiviral activities. Overexpression of the human MCPIP1, but not MCPIP2, MCPIP3 or MCPIP4, inhibited Japanese encephalitis virus (JEV) and dengue virus (DEN) replication. The functional analysis of MCPIP1 revealed that the activities of RNase, RNA binding and oligomerization, but not deubiqutinase, are required for its antiviral potential. Furthermore, infection of other positive-sense RNA viruses, such as sindbis virus and encephalomyocarditis virus, and negative-sense RNA virus, such as influenza virus, as well as DNA virus, such as adenovirus, can also be blocked by MCPIP1. Moreover, the endogenous MCPIP1 gene expression was induced by JEV and DEN infection, and knockdown of MCPIP1 expression enhanced the replication of JEV and DEN in human cells. Thus, MCPIP1 can act as a host innate defense via RNase activity for targeting and degrading viral RNA.</description><subject>Amino Acid Sequence</subject><subject>Conserved Sequence</subject><subject>Dengue Virus - genetics</subject><subject>Dengue Virus - immunology</subject><subject>Dengue Virus - physiology</subject><subject>Encephalitis Virus, Japanese - genetics</subject><subject>Encephalitis Virus, Japanese - immunology</subject><subject>Encephalitis Virus, Japanese - physiology</subject><subject>HEK293 Cells</subject><subject>Host-Pathogen Interactions</subject><subject>Humans</subject><subject>Immunity, Innate</subject><subject>Molecular Sequence Data</subject><subject>Nucleic Acid Enzymes</subject><subject>Protein Binding</subject><subject>Protein Multimerization</subject><subject>Protein Structure, Tertiary</subject><subject>Ribonucleases</subject><subject>RNA Stability</subject><subject>RNA, Viral - metabolism</subject><subject>Transcription Factors - chemistry</subject><subject>Transcription Factors - metabolism</subject><subject>Transcription Factors - physiology</subject><subject>Virus Replication</subject><subject>Zinc Fingers</subject><issn>0305-1048</issn><issn>1362-4962</issn><fulltext>true</fulltext><rsrctype>article</rsrctype><creationdate>2013</creationdate><recordtype>article</recordtype><recordid>eNpVkVtLHTEUhYO06PHy4g-QPBZhNPeZvBTk4A1sK6LPIZPLnLRzktMkI-2_d-SotE8b1v5Ye20WAMcYnWEk6XnU-Xz4VRGWO2CBqSANk4J8AgtEEW8wYt0e2C_lJ0KYYc52wR6hlHOB-QIM35b3t_cY5tCnOJnR6eKg-7MKfagF9jlp25SNMzVPa6hjDc8h6xE672etwLrKaRpWcKs-fL-AfYg2xGFmLbRuyNrqGlI8BJ-9Hos7epsH4Onq8nF509z9uL5dXtw1hjFWGy-IMIz0hnFMtXadNJja1ggktTdEWtmLdv4Oua5tJcFMdBoT6rlFxPve0wPwdeu7mfq1s8bFOidTmxzWOv9VSQf1_yaGlRrSs6JctqLjs8GXN4Ocfk-uVLUOxbhx1NGlqShMccsQbTs5o6db1ORUSnb-4wxG6rUZNTejts3M8Mm_wT7Q9yroC4gCjMg</recordid><startdate>20130301</startdate><enddate>20130301</enddate><creator>Lin, Ren-Jye</creator><creator>Chien, Hsu-Ling</creator><creator>Lin, Shyr-Yi</creator><creator>Chang, Bi-Lan</creator><creator>Yu, Han-Pang</creator><creator>Tang, Wei-Chun</creator><creator>Lin, Yi-Ling</creator><general>Oxford University Press</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></search><sort><creationdate>20130301</creationdate><title>MCPIP1 ribonuclease exhibits broad-spectrum antiviral effects through viral RNA binding and degradation</title><author>Lin, Ren-Jye ; Chien, Hsu-Ling ; Lin, Shyr-Yi ; Chang, Bi-Lan ; Yu, Han-Pang ; Tang, Wei-Chun ; Lin, Yi-Ling</author></sort><facets><frbrtype>5</frbrtype><frbrgroupid>cdi_FETCH-LOGICAL-c444t-f626c42bc4513aae89c13d7c609afc29d9b674960e877921468a123f5d02ffbf3</frbrgroupid><rsrctype>articles</rsrctype><prefilter>articles</prefilter><language>eng</language><creationdate>2013</creationdate><topic>Amino Acid Sequence</topic><topic>Conserved Sequence</topic><topic>Dengue Virus - genetics</topic><topic>Dengue Virus - immunology</topic><topic>Dengue Virus - physiology</topic><topic>Encephalitis Virus, Japanese - genetics</topic><topic>Encephalitis Virus, Japanese - immunology</topic><topic>Encephalitis Virus, Japanese - physiology</topic><topic>HEK293 Cells</topic><topic>Host-Pathogen Interactions</topic><topic>Humans</topic><topic>Immunity, Innate</topic><topic>Molecular Sequence Data</topic><topic>Nucleic Acid Enzymes</topic><topic>Protein Binding</topic><topic>Protein Multimerization</topic><topic>Protein Structure, Tertiary</topic><topic>Ribonucleases</topic><topic>RNA Stability</topic><topic>RNA, Viral - metabolism</topic><topic>Transcription Factors - chemistry</topic><topic>Transcription Factors - metabolism</topic><topic>Transcription Factors - physiology</topic><topic>Virus Replication</topic><topic>Zinc Fingers</topic><toplevel>peer_reviewed</toplevel><toplevel>online_resources</toplevel><creatorcontrib>Lin, Ren-Jye</creatorcontrib><creatorcontrib>Chien, Hsu-Ling</creatorcontrib><creatorcontrib>Lin, Shyr-Yi</creatorcontrib><creatorcontrib>Chang, Bi-Lan</creatorcontrib><creatorcontrib>Yu, Han-Pang</creatorcontrib><creatorcontrib>Tang, Wei-Chun</creatorcontrib><creatorcontrib>Lin, Yi-Ling</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>Nucleic acids research</jtitle></facets><delivery><delcategory>Remote Search Resource</delcategory><fulltext>fulltext</fulltext></delivery><addata><au>Lin, Ren-Jye</au><au>Chien, Hsu-Ling</au><au>Lin, Shyr-Yi</au><au>Chang, Bi-Lan</au><au>Yu, Han-Pang</au><au>Tang, Wei-Chun</au><au>Lin, Yi-Ling</au><format>journal</format><genre>article</genre><ristype>JOUR</ristype><atitle>MCPIP1 ribonuclease exhibits broad-spectrum antiviral effects through viral RNA binding and degradation</atitle><jtitle>Nucleic acids research</jtitle><addtitle>Nucleic Acids Res</addtitle><date>2013-03-01</date><risdate>2013</risdate><volume>41</volume><issue>5</issue><spage>3314</spage><epage>3326</epage><pages>3314-3326</pages><issn>0305-1048</issn><eissn>1362-4962</eissn><notes>ObjectType-Article-1</notes><notes>SourceType-Scholarly Journals-1</notes><notes>ObjectType-Feature-2</notes><notes>content type line 23</notes><abstract>Monocyte chemoattractant protein 1-induced protein 1 (MCPIP1), belonging to the MCPIP family with highly conserved CCCH-type zinc finger and Nedd4-BP1, YacP Nuclease domains, has been implicated in negative regulation of the cellular inflammatory responses. In this report, we demonstrate for the first time that this RNA-binding nuclease also targets viral RNA and possesses potent antiviral activities. Overexpression of the human MCPIP1, but not MCPIP2, MCPIP3 or MCPIP4, inhibited Japanese encephalitis virus (JEV) and dengue virus (DEN) replication. The functional analysis of MCPIP1 revealed that the activities of RNase, RNA binding and oligomerization, but not deubiqutinase, are required for its antiviral potential. Furthermore, infection of other positive-sense RNA viruses, such as sindbis virus and encephalomyocarditis virus, and negative-sense RNA virus, such as influenza virus, as well as DNA virus, such as adenovirus, can also be blocked by MCPIP1. Moreover, the endogenous MCPIP1 gene expression was induced by JEV and DEN infection, and knockdown of MCPIP1 expression enhanced the replication of JEV and DEN in human cells. Thus, MCPIP1 can act as a host innate defense via RNase activity for targeting and degrading viral RNA.</abstract><cop>England</cop><pub>Oxford University Press</pub><pmid>23355615</pmid><doi>10.1093/nar/gkt019</doi><tpages>13</tpages><oa>free_for_read</oa></addata></record> |
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| ispartof | Nucleic acids research, 2013-03, Vol.41 (5), p.3314-3326 |
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| source | PubMed Central; Oxford Journals |
| subjects | Amino Acid Sequence Conserved Sequence Dengue Virus - genetics Dengue Virus - immunology Dengue Virus - physiology Encephalitis Virus, Japanese - genetics Encephalitis Virus, Japanese - immunology Encephalitis Virus, Japanese - physiology HEK293 Cells Host-Pathogen Interactions Humans Immunity, Innate Molecular Sequence Data Nucleic Acid Enzymes Protein Binding Protein Multimerization Protein Structure, Tertiary Ribonucleases RNA Stability RNA, Viral - metabolism Transcription Factors - chemistry Transcription Factors - metabolism Transcription Factors - physiology Virus Replication Zinc Fingers |
| title | MCPIP1 ribonuclease exhibits broad-spectrum antiviral effects through viral RNA binding and degradation |
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