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Effect of a loss of the mda5/ifih1 gene on the antiviral resistance in a Chinook salmon Oncorhynchus tshawytscha cell line
Cells are equipped with intracellular RIG-like Receptors (RLRs) detecting double stranded (ds)RNA, a molecule with Pathogen-Associated Molecular Pattern (PAMPs) generated during the life cycle of many viruses. Melanoma Differentiation-Associated protein 5 (MDA5), a helicase enzyme member of the RLRs...
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Published in: | PloS one 2024-10, Vol.19 (10), p.e0311283 |
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description | Cells are equipped with intracellular RIG-like Receptors (RLRs) detecting double stranded (ds)RNA, a molecule with Pathogen-Associated Molecular Pattern (PAMPs) generated during the life cycle of many viruses. Melanoma Differentiation-Associated protein 5 (MDA5), a helicase enzyme member of the RLRs encoded by the ifih1 gene, binds to long dsRNA molecules during a viral infection and initiates production of type I interferon (IFN1) which orchestrates the antiviral response. In order to understand the contribution of MDA5 to viral resistance in fish cells, we have isolated a clonal Chinook salmon Oncorhynchus tshawytscha epithelial-like cell line invalidated for the ifih1 gene by CRISPR/Cas9 genome editing. We demonstrated that IFN1 induction is impaired in this cell line after infection with the Snakehead Rhabdovirus (SHRV), the Salmon Alphavirus (SAV) or Nervous Necrosis Virus (NNV). The cell line, however, did not show any increase in cytopathic effect when infected with SHRV or SAV. Similarly, no cytopathic effect was observed in the ifih1-/- cell line when infected with Infectious Pancreatic Necrosis Virus (IPNV), Infectious Haemorrhagic Necrotic Virus (IHNV). These results indicate the redundancy of the antiviral innate defence system in CHSE-derived cells, which helps with circumventing viral evasion strategies. |
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Melanoma Differentiation-Associated protein 5 (MDA5), a helicase enzyme member of the RLRs encoded by the ifih1 gene, binds to long dsRNA molecules during a viral infection and initiates production of type I interferon (IFN1) which orchestrates the antiviral response. In order to understand the contribution of MDA5 to viral resistance in fish cells, we have isolated a clonal Chinook salmon Oncorhynchus tshawytscha epithelial-like cell line invalidated for the ifih1 gene by CRISPR/Cas9 genome editing. We demonstrated that IFN1 induction is impaired in this cell line after infection with the Snakehead Rhabdovirus (SHRV), the Salmon Alphavirus (SAV) or Nervous Necrosis Virus (NNV). The cell line, however, did not show any increase in cytopathic effect when infected with SHRV or SAV. Similarly, no cytopathic effect was observed in the ifih1-/- cell line when infected with Infectious Pancreatic Necrosis Virus (IPNV), Infectious Haemorrhagic Necrotic Virus (IHNV). These results indicate the redundancy of the antiviral innate defence system in CHSE-derived cells, which helps with circumventing viral evasion strategies.</description><identifier>ISSN: 1932-6203</identifier><identifier>EISSN: 1932-6203</identifier><identifier>DOI: 10.1371/journal.pone.0311283</identifier><identifier>PMID: 39401233</identifier><language>eng</language><publisher>United States: Public Library of Science</publisher><subject>Analysis ; Animals ; Biological response modifiers ; Biology and Life Sciences ; Carp ; Cell Line ; Cells ; Chinook salmon ; Cloning ; CRISPR ; CRISPR-Cas Systems ; DNA helicase ; Double-stranded RNA ; Drug resistance ; Enzymes ; Fish diseases ; Fish Diseases - genetics ; Fish Diseases - immunology ; Fish Diseases - virology ; Fish Proteins - genetics ; Fish Proteins - metabolism ; Fishes ; Genes ; Genetic aspects ; Genome editing ; Genomes ; Genomics ; Health aspects ; Infection ; Infections ; Infectious pancreatic necrosis ; Interferon ; Interferon Type I - metabolism ; Interferon-Induced Helicase, IFIH1 - genetics ; Interferon-Induced Helicase, IFIH1 - metabolism ; Life Sciences ; Maximum likelihood method ; Melanoma ; Necrosis ; Oncorhynchus tshawytscha ; Plant virus diseases ; Plant viruses ; Proteins ; Redundancy ; Research and Analysis Methods ; RNA ; Salmon ; Salmon - virology ; Trout ; Viral infections ; Viruses</subject><ispartof>PloS one, 2024-10, Vol.19 (10), p.e0311283</ispartof><rights>Copyright: © 2024 Collins et al. This is an open access article distributed under the terms of the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited.</rights><rights>COPYRIGHT 2024 Public Library of Science</rights><rights>2024 Collins et al. This is an open access article distributed under the terms of the Creative Commons Attribution License: http://creativecommons.org/licenses/by/4.0/ (the “License”), which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited. Notwithstanding the ProQuest Terms and Conditions, you may use this content in accordance with the terms of the License.</rights><rights>Attribution</rights><rights>2024 Collins et al 2024 Collins et al</rights><rights>2024 Collins et al. This is an open access article distributed under the terms of the Creative Commons Attribution License: http://creativecommons.org/licenses/by/4.0/ (the “License”), which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited. 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These results indicate the redundancy of the antiviral innate defence system in CHSE-derived cells, which helps with circumventing viral evasion strategies.</description><subject>Analysis</subject><subject>Animals</subject><subject>Biological response modifiers</subject><subject>Biology and Life Sciences</subject><subject>Carp</subject><subject>Cell Line</subject><subject>Cells</subject><subject>Chinook salmon</subject><subject>Cloning</subject><subject>CRISPR</subject><subject>CRISPR-Cas Systems</subject><subject>DNA helicase</subject><subject>Double-stranded RNA</subject><subject>Drug resistance</subject><subject>Enzymes</subject><subject>Fish diseases</subject><subject>Fish Diseases - genetics</subject><subject>Fish Diseases - immunology</subject><subject>Fish Diseases - virology</subject><subject>Fish Proteins - genetics</subject><subject>Fish Proteins - metabolism</subject><subject>Fishes</subject><subject>Genes</subject><subject>Genetic aspects</subject><subject>Genome editing</subject><subject>Genomes</subject><subject>Genomics</subject><subject>Health aspects</subject><subject>Infection</subject><subject>Infections</subject><subject>Infectious pancreatic necrosis</subject><subject>Interferon</subject><subject>Interferon Type I - metabolism</subject><subject>Interferon-Induced Helicase, IFIH1 - genetics</subject><subject>Interferon-Induced Helicase, IFIH1 - metabolism</subject><subject>Life Sciences</subject><subject>Maximum likelihood method</subject><subject>Melanoma</subject><subject>Necrosis</subject><subject>Oncorhynchus tshawytscha</subject><subject>Plant virus diseases</subject><subject>Plant viruses</subject><subject>Proteins</subject><subject>Redundancy</subject><subject>Research and Analysis Methods</subject><subject>RNA</subject><subject>Salmon</subject><subject>Salmon - virology</subject><subject>Trout</subject><subject>Viral infections</subject><subject>Viruses</subject><issn>1932-6203</issn><issn>1932-6203</issn><fulltext>true</fulltext><rsrctype>article</rsrctype><creationdate>2024</creationdate><recordtype>article</recordtype><sourceid>COVID</sourceid><sourceid>PIMPY</sourceid><recordid>eNqNk21r2zAQx83YWLts32BsgsFYXyTVgy3br0YI3VoIBPb0VijyKVZnS5klZ8s-_eTWLUnpi2GBxen3vzud7pLkNcEzwnJyfu36zspmtnUWZpgRQgv2JDklJaNTTjF7erA_SV54f41xxgrOnycnrEwxoYydJn8vtAYVkNNIosZ5P-xCDaitZHZutKkJ2oAF5OyNWdpgdqaTDerAGx-kVYCMjeJFbaxzP5GXTRvhlVWuq_dW1b1Hwdfy9z54VUukoGlQYyy8TJ5p2Xh4Nf4nyfdPF98Wl9Pl6vPVYr6cqizFYcoxrjhIXlQ5XVO9rgqlK5Ix4ERhRYsSZF4wnZdlSUoiKU-lZrKCnNFSa7Jmk-Ttrd9tvJ8Yy-YFiwXIc87imiQfR6Jft1ApsCHeUGw708puL5w04vjEmlps3E4QkuY0ho0ezm491A90l_OlGGw4LSjNU7Ijkf0wRuvcrx58EK3xQ1WkBdcPiRHO84zfJPbuAfp4-iO1kQ0IY7WLSarBqZgXhFKaZWwIO3uEil8FrVGxibSJ9iPB2ZEgMgH-hI3svRdXX7_8P7v6ccy-P2BrkE2ovWv6YJz1x2B6C6ouNmYH-r6yBIthBu6qIYYZEOMMRNmbw9e8F901PfsH92QAvA</recordid><startdate>20241014</startdate><enddate>20241014</enddate><creator>Collins, Catherine</creator><creator>Chaumont, Lise</creator><creator>Peruzzi, Mathilde</creator><creator>Jamak, Nedim</creator><creator>Boudinot, Pierre</creator><creator>Béjar, Julia</creator><creator>Moreno, Patricia</creator><creator>Álvarez Torres, Daniel</creator><creator>Collet, Bertrand</creator><general>Public Library 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>IOV</scope><scope>ISR</scope><scope>3V.</scope><scope>7QG</scope><scope>7QL</scope><scope>7QO</scope><scope>7RV</scope><scope>7SN</scope><scope>7SS</scope><scope>7T5</scope><scope>7TG</scope><scope>7TM</scope><scope>7U9</scope><scope>7X2</scope><scope>7X7</scope><scope>7XB</scope><scope>88E</scope><scope>8AO</scope><scope>8C1</scope><scope>8FD</scope><scope>8FE</scope><scope>8FG</scope><scope>8FH</scope><scope>8FI</scope><scope>8FJ</scope><scope>8FK</scope><scope>ABJCF</scope><scope>ABUWG</scope><scope>AFKRA</scope><scope>ARAPS</scope><scope>ATCPS</scope><scope>AZQEC</scope><scope>BBNVY</scope><scope>BENPR</scope><scope>BGLVJ</scope><scope>BHPHI</scope><scope>C1K</scope><scope>CCPQU</scope><scope>COVID</scope><scope>D1I</scope><scope>DWQXO</scope><scope>FR3</scope><scope>FYUFA</scope><scope>GHDGH</scope><scope>GNUQQ</scope><scope>H94</scope><scope>HCIFZ</scope><scope>K9.</scope><scope>KB.</scope><scope>KB0</scope><scope>KL.</scope><scope>L6V</scope><scope>LK8</scope><scope>M0K</scope><scope>M0S</scope><scope>M1P</scope><scope>M7N</scope><scope>M7P</scope><scope>M7S</scope><scope>NAPCQ</scope><scope>P5Z</scope><scope>P62</scope><scope>P64</scope><scope>PATMY</scope><scope>PDBOC</scope><scope>PIMPY</scope><scope>PQEST</scope><scope>PQQKQ</scope><scope>PQUKI</scope><scope>PRINS</scope><scope>PTHSS</scope><scope>PYCSY</scope><scope>RC3</scope><scope>7X8</scope><scope>1XC</scope><scope>VOOES</scope><scope>5PM</scope><orcidid>https://orcid.org/0000-0003-2795-2653</orcidid></search><sort><creationdate>20241014</creationdate><title>Effect of a loss of the mda5/ifih1 gene on the antiviral resistance in a Chinook salmon Oncorhynchus tshawytscha cell line</title><author>Collins, Catherine ; Chaumont, Lise ; Peruzzi, Mathilde ; Jamak, Nedim ; Boudinot, Pierre ; Béjar, Julia ; Moreno, Patricia ; Álvarez Torres, Daniel ; Collet, Bertrand</author></sort><facets><frbrtype>5</frbrtype><frbrgroupid>cdi_FETCH-LOGICAL-c540t-600d6ea68d72b2fbd8cfd153e61c0c289ea783f7999191a264af3ade7329ff1b3</frbrgroupid><rsrctype>articles</rsrctype><prefilter>articles</prefilter><language>eng</language><creationdate>2024</creationdate><topic>Analysis</topic><topic>Animals</topic><topic>Biological response modifiers</topic><topic>Biology and Life Sciences</topic><topic>Carp</topic><topic>Cell Line</topic><topic>Cells</topic><topic>Chinook salmon</topic><topic>Cloning</topic><topic>CRISPR</topic><topic>CRISPR-Cas Systems</topic><topic>DNA helicase</topic><topic>Double-stranded RNA</topic><topic>Drug resistance</topic><topic>Enzymes</topic><topic>Fish diseases</topic><topic>Fish Diseases - 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Melanoma Differentiation-Associated protein 5 (MDA5), a helicase enzyme member of the RLRs encoded by the ifih1 gene, binds to long dsRNA molecules during a viral infection and initiates production of type I interferon (IFN1) which orchestrates the antiviral response. In order to understand the contribution of MDA5 to viral resistance in fish cells, we have isolated a clonal Chinook salmon Oncorhynchus tshawytscha epithelial-like cell line invalidated for the ifih1 gene by CRISPR/Cas9 genome editing. We demonstrated that IFN1 induction is impaired in this cell line after infection with the Snakehead Rhabdovirus (SHRV), the Salmon Alphavirus (SAV) or Nervous Necrosis Virus (NNV). The cell line, however, did not show any increase in cytopathic effect when infected with SHRV or SAV. Similarly, no cytopathic effect was observed in the ifih1-/- cell line when infected with Infectious Pancreatic Necrosis Virus (IPNV), Infectious Haemorrhagic Necrotic Virus (IHNV). These results indicate the redundancy of the antiviral innate defence system in CHSE-derived cells, which helps with circumventing viral evasion strategies.</abstract><cop>United States</cop><pub>Public Library of Science</pub><pmid>39401233</pmid><doi>10.1371/journal.pone.0311283</doi><tpages>e0311283</tpages><orcidid>https://orcid.org/0000-0003-2795-2653</orcidid><oa>free_for_read</oa></addata></record> |
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subjects | Analysis Animals Biological response modifiers Biology and Life Sciences Carp Cell Line Cells Chinook salmon Cloning CRISPR CRISPR-Cas Systems DNA helicase Double-stranded RNA Drug resistance Enzymes Fish diseases Fish Diseases - genetics Fish Diseases - immunology Fish Diseases - virology Fish Proteins - genetics Fish Proteins - metabolism Fishes Genes Genetic aspects Genome editing Genomes Genomics Health aspects Infection Infections Infectious pancreatic necrosis Interferon Interferon Type I - metabolism Interferon-Induced Helicase, IFIH1 - genetics Interferon-Induced Helicase, IFIH1 - metabolism Life Sciences Maximum likelihood method Melanoma Necrosis Oncorhynchus tshawytscha Plant virus diseases Plant viruses Proteins Redundancy Research and Analysis Methods RNA Salmon Salmon - virology Trout Viral infections Viruses |
title | Effect of a loss of the mda5/ifih1 gene on the antiviral resistance in a Chinook salmon Oncorhynchus tshawytscha cell line |
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