Sequence and Expression Analysis of Interferon Regulatory Factor 10 (IRF10) in Three Diverse Teleost Fish Reveals Its Role in Antiviral Defense
Interferon regulatory factor (IRF) 10 was first found in birds and is present in the genome of other tetrapods (but not humans and mice), as well as in teleost fish. The functional role of IRF10 in vertebrate immunity is relatively unknown compared to IRF1-9. The target of this research was to clone...
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description | Interferon regulatory factor (IRF) 10 was first found in birds and is present in the genome of other tetrapods (but not humans and mice), as well as in teleost fish. The functional role of IRF10 in vertebrate immunity is relatively unknown compared to IRF1-9. The target of this research was to clone and characterize the IRF10 genes in three economically important fish species that will facilitate future evaluation of this molecule in fish innate and adaptive immunity.
In the present study, a single IRF10 gene was cloned in grass carp Ctenopharyngodon idella and Asian swamp eel Monopterus albus, and two, named IRF10a and IRF10b, in rainbow trout Oncorhynchus mykiss. The fish IRF10 molecules share highest identities to other vertebrate IRF10s, and have a well conserved DNA binding domain, IRF-associated domain, and an 8 exon/7 intron structure with conserved intron phase. The presence of an upstream ATG or open reading frame (ORF) in the 5'-untranslated region of different fish IRF10 cDNA sequences suggests potential regulation at the translational level, and this has been verified by in vitro transcription/translation experiments of the trout IRF10a cDNA, but would still need to be validated in fish cells.
Both trout IRF10 paralogues are highly expressed in thymus, blood and spleen but are relatively low in head kidney and caudal kidney. Trout IRF10b expression is significantly higher than IRF10a in integumentary tissues i.e. gills, scales, skin, intestine, adipose fin and tail fins, suggesting that IRF10b may be more important in mucosal immunity. The expression of both trout IRF10 paralogues is up-regulated by recombinant IFN-γ. The expression of the IRF10 genes is highly induced by Poly I:C in vitro and in vivo, and by viral infection, but is less responsive to peptidoglycan and bacterial infection, suggesting an important role of fish IRF10 in antiviral defense. |
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In the present study, a single IRF10 gene was cloned in grass carp Ctenopharyngodon idella and Asian swamp eel Monopterus albus, and two, named IRF10a and IRF10b, in rainbow trout Oncorhynchus mykiss. The fish IRF10 molecules share highest identities to other vertebrate IRF10s, and have a well conserved DNA binding domain, IRF-associated domain, and an 8 exon/7 intron structure with conserved intron phase. The presence of an upstream ATG or open reading frame (ORF) in the 5'-untranslated region of different fish IRF10 cDNA sequences suggests potential regulation at the translational level, and this has been verified by in vitro transcription/translation experiments of the trout IRF10a cDNA, but would still need to be validated in fish cells.
Both trout IRF10 paralogues are highly expressed in thymus, blood and spleen but are relatively low in head kidney and caudal kidney. Trout IRF10b expression is significantly higher than IRF10a in integumentary tissues i.e. gills, scales, skin, intestine, adipose fin and tail fins, suggesting that IRF10b may be more important in mucosal immunity. The expression of both trout IRF10 paralogues is up-regulated by recombinant IFN-γ. The expression of the IRF10 genes is highly induced by Poly I:C in vitro and in vivo, and by viral infection, but is less responsive to peptidoglycan and bacterial infection, suggesting an important role of fish IRF10 in antiviral defense.</description><identifier>ISSN: 1932-6203</identifier><identifier>EISSN: 1932-6203</identifier><identifier>DOI: 10.1371/journal.pone.0147181</identifier><identifier>PMID: 26783745</identifier><language>eng</language><publisher>United States: Public Library of Science</publisher><subject>Adaptive Immunity ; Animal diseases ; Animal tissues ; Animals ; Antiviral drugs ; Bacteria ; Biology and Life Sciences ; Birds ; Carp ; Carps - genetics ; Carps - immunology ; Cloning, Molecular ; Comparative analysis ; Ctenopharyngodon idella ; Deoxyribonucleic acid ; Diseases and pests ; DNA ; Earth Sciences ; Ecology and Environmental Sciences ; Epinephelus coioides ; Fins ; Fish ; Fish Proteins - genetics ; Fish Proteins - metabolism ; Fishes ; Gene expression ; Gene Expression Profiling - methods ; Gene Expression Regulation - drug effects ; Genes ; Genetic aspects ; Genomes ; Gills ; Immunity ; Immunity, Innate ; Infections ; Interferon ; Interferon regulatory factor ; Interferon regulatory factor 1 ; Interferon Regulatory Factors - genetics ; Interferon Regulatory Factors - metabolism ; Interferon-gamma - pharmacology ; Intestine ; Kidneys ; Molecular Sequence Data ; Monopterus albus ; Mucosal immunity ; Oncorhynchus mykiss ; Oncorhynchus mykiss - genetics ; Oncorhynchus mykiss - immunology ; Peptidoglycans ; Phylogeny ; Physiological aspects ; Polyinosinic:polycytidylic acid ; Regulatory sequences ; Research and Analysis Methods ; Salmon ; Scales ; Sequence Analysis, DNA - methods ; Skin ; Smegmamorpha - genetics ; Smegmamorpha - immunology ; Spleen ; Thymus ; Tissue Distribution ; Transcription ; Trout ; Viral infections ; Zebrafish ; γ-Interferon</subject><ispartof>PloS one, 2016-01, Vol.11 (1), p.e0147181-e0147181</ispartof><rights>COPYRIGHT 2016 Public Library of Science</rights><rights>2016 Xu 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>2016 Xu et al 2016 Xu et al</rights><lds50>peer_reviewed</lds50><oa>free_for_read</oa><woscitedreferencessubscribed>false</woscitedreferencessubscribed><citedby>FETCH-LOGICAL-c593t-4ce0777ba338c4103350058c302275cc8b975e1598bd12cb66f9bf7bbcdc2efe3</citedby><cites>FETCH-LOGICAL-c593t-4ce0777ba338c4103350058c302275cc8b975e1598bd12cb66f9bf7bbcdc2efe3</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/PMC4718558/pdf/$$EPDF$$P50$$Gpubmedcentral$$Hfree_for_read</linktopdf><linktohtml>$$Uhttps://www.ncbi.nlm.nih.gov/pmc/articles/PMC4718558/$$EHTML$$P50$$Gpubmedcentral$$Hfree_for_read</linktohtml><link.rule.ids>230,314,723,776,780,860,881,2095,2914,23846,27903,27904,53769,53771,79346,79347</link.rule.ids><backlink>$$Uhttps://www.ncbi.nlm.nih.gov/pubmed/26783745$$D View this record in MEDLINE/PubMed$$Hfree_for_read</backlink></links><search><contributor>Boudinot, Pierre</contributor><creatorcontrib>Xu, Qiaoqing</creatorcontrib><creatorcontrib>Jiang, Yousheng</creatorcontrib><creatorcontrib>Wangkahart, Eakapol</creatorcontrib><creatorcontrib>Zou, Jun</creatorcontrib><creatorcontrib>Chang, Mingxian</creatorcontrib><creatorcontrib>Yang, Daiqin</creatorcontrib><creatorcontrib>Secombes, Chris J</creatorcontrib><creatorcontrib>Nie, Pin</creatorcontrib><creatorcontrib>Wang, Tiehui</creatorcontrib><title>Sequence and Expression Analysis of Interferon Regulatory Factor 10 (IRF10) in Three Diverse Teleost Fish Reveals Its Role in Antiviral Defense</title><title>PloS one</title><addtitle>PLoS One</addtitle><description>Interferon regulatory factor (IRF) 10 was first found in birds and is present in the genome of other tetrapods (but not humans and mice), as well as in teleost fish. The functional role of IRF10 in vertebrate immunity is relatively unknown compared to IRF1-9. The target of this research was to clone and characterize the IRF10 genes in three economically important fish species that will facilitate future evaluation of this molecule in fish innate and adaptive immunity.
In the present study, a single IRF10 gene was cloned in grass carp Ctenopharyngodon idella and Asian swamp eel Monopterus albus, and two, named IRF10a and IRF10b, in rainbow trout Oncorhynchus mykiss. The fish IRF10 molecules share highest identities to other vertebrate IRF10s, and have a well conserved DNA binding domain, IRF-associated domain, and an 8 exon/7 intron structure with conserved intron phase. The presence of an upstream ATG or open reading frame (ORF) in the 5'-untranslated region of different fish IRF10 cDNA sequences suggests potential regulation at the translational level, and this has been verified by in vitro transcription/translation experiments of the trout IRF10a cDNA, but would still need to be validated in fish cells.
Both trout IRF10 paralogues are highly expressed in thymus, blood and spleen but are relatively low in head kidney and caudal kidney. Trout IRF10b expression is significantly higher than IRF10a in integumentary tissues i.e. gills, scales, skin, intestine, adipose fin and tail fins, suggesting that IRF10b may be more important in mucosal immunity. The expression of both trout IRF10 paralogues is up-regulated by recombinant IFN-γ. The expression of the IRF10 genes is highly induced by Poly I:C in vitro and in vivo, and by viral infection, but is less responsive to peptidoglycan and bacterial infection, suggesting an important role of fish IRF10 in antiviral defense.</description><subject>Adaptive Immunity</subject><subject>Animal diseases</subject><subject>Animal tissues</subject><subject>Animals</subject><subject>Antiviral drugs</subject><subject>Bacteria</subject><subject>Biology and Life Sciences</subject><subject>Birds</subject><subject>Carp</subject><subject>Carps - genetics</subject><subject>Carps - immunology</subject><subject>Cloning, Molecular</subject><subject>Comparative analysis</subject><subject>Ctenopharyngodon idella</subject><subject>Deoxyribonucleic acid</subject><subject>Diseases and pests</subject><subject>DNA</subject><subject>Earth Sciences</subject><subject>Ecology and Environmental Sciences</subject><subject>Epinephelus coioides</subject><subject>Fins</subject><subject>Fish</subject><subject>Fish Proteins - genetics</subject><subject>Fish Proteins - metabolism</subject><subject>Fishes</subject><subject>Gene expression</subject><subject>Gene Expression Profiling - methods</subject><subject>Gene Expression Regulation - drug effects</subject><subject>Genes</subject><subject>Genetic aspects</subject><subject>Genomes</subject><subject>Gills</subject><subject>Immunity</subject><subject>Immunity, Innate</subject><subject>Infections</subject><subject>Interferon</subject><subject>Interferon regulatory factor</subject><subject>Interferon regulatory factor 1</subject><subject>Interferon Regulatory Factors - genetics</subject><subject>Interferon Regulatory Factors - metabolism</subject><subject>Interferon-gamma - pharmacology</subject><subject>Intestine</subject><subject>Kidneys</subject><subject>Molecular Sequence Data</subject><subject>Monopterus albus</subject><subject>Mucosal immunity</subject><subject>Oncorhynchus mykiss</subject><subject>Oncorhynchus mykiss - genetics</subject><subject>Oncorhynchus mykiss - immunology</subject><subject>Peptidoglycans</subject><subject>Phylogeny</subject><subject>Physiological aspects</subject><subject>Polyinosinic:polycytidylic acid</subject><subject>Regulatory sequences</subject><subject>Research and Analysis Methods</subject><subject>Salmon</subject><subject>Scales</subject><subject>Sequence Analysis, DNA - methods</subject><subject>Skin</subject><subject>Smegmamorpha - genetics</subject><subject>Smegmamorpha - immunology</subject><subject>Spleen</subject><subject>Thymus</subject><subject>Tissue Distribution</subject><subject>Transcription</subject><subject>Trout</subject><subject>Viral infections</subject><subject>Zebrafish</subject><subject>γ-Interferon</subject><issn>1932-6203</issn><issn>1932-6203</issn><fulltext>true</fulltext><rsrctype>article</rsrctype><creationdate>2016</creationdate><recordtype>article</recordtype><sourceid>EIF</sourceid><sourceid>BENPR</sourceid><sourceid>DOA</sourceid><recordid>eNptUtFu0zAUjRCIjcEfILDEy3hoseM4dl4mVdsKlSYhlfJsOc516yq1i51W9Cv45TlrNq1oyoOj63POvcf3ZNlHgseEcvJt7XfBqXa89Q7GmBScCPIqOycVzUdljunrZ_9n2bsY1xgzKsrybXaWl1xQXrDz7N8v-LMDpwEp16Dbv9sAMVrv0CRpH6KNyBs0cx0EAyGV57Dctarz4YCmSqcTEYwuZ_MpwV-RdWixCgDoxu4hREALaMHHDk1tXCXqHlQb0ayLaO5b6OET19m9DapFN2DARXifvTEJBB-G8yL7Pb1dXP8Y3f38Prue3I00q2g3KjRgznmtKBW6IJhSltwJTXGec6a1qCvOgLBK1A3JdV2WpqoNr2vd6Dx1ohfZ56PutvVRDm8ZJeFMkKIqGUmI2RHReLWW22A3KhykV1Y-FHxYShU6q1uQmLOqJqYUlLGCNFoJSNuoDTVEVKzASetq6LarN9BocF3yfCJ6euPsSi79XvZbZUwkgctBIPi0r9jJjY0a2lY58Lt-7hILXuQiT9Av_0FfdjeglioZsM741Ff3onJSFJhVOWH93OMXUOlrYGN1Cp6xqX5CKI4EHXyMAcyTR4JlH9vHYWQfWznENtE-PX-fJ9JjTuk9TNnpTw</recordid><startdate>20160101</startdate><enddate>20160101</enddate><creator>Xu, Qiaoqing</creator><creator>Jiang, Yousheng</creator><creator>Wangkahart, Eakapol</creator><creator>Zou, Jun</creator><creator>Chang, Mingxian</creator><creator>Yang, Daiqin</creator><creator>Secombes, Chris J</creator><creator>Nie, Pin</creator><creator>Wang, Tiehui</creator><general>Public Library of Science</general><general>Public Library of Science (PLoS)</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>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>AEUYN</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>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>5PM</scope><scope>DOA</scope></search><sort><creationdate>20160101</creationdate><title>Sequence and Expression Analysis of Interferon Regulatory Factor 10 (IRF10) in Three Diverse Teleost Fish Reveals Its Role in Antiviral Defense</title><author>Xu, Qiaoqing ; Jiang, Yousheng ; Wangkahart, Eakapol ; Zou, Jun ; Chang, Mingxian ; Yang, Daiqin ; Secombes, Chris J ; Nie, Pin ; Wang, Tiehui</author></sort><facets><frbrtype>5</frbrtype><frbrgroupid>cdi_FETCH-LOGICAL-c593t-4ce0777ba338c4103350058c302275cc8b975e1598bd12cb66f9bf7bbcdc2efe3</frbrgroupid><rsrctype>articles</rsrctype><prefilter>articles</prefilter><language>eng</language><creationdate>2016</creationdate><topic>Adaptive Immunity</topic><topic>Animal diseases</topic><topic>Animal tissues</topic><topic>Animals</topic><topic>Antiviral drugs</topic><topic>Bacteria</topic><topic>Biology and Life Sciences</topic><topic>Birds</topic><topic>Carp</topic><topic>Carps - 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Academic</collection><collection>ProQuest Engineering Collection</collection><collection>ProQuest Biological Science Collection</collection><collection>Agricultural Science Database</collection><collection>Health & Medical Collection (Alumni Edition)</collection><collection>Medical Database</collection><collection>Algology Mycology and Protozoology Abstracts (Microbiology C)</collection><collection>Biological Science Database</collection><collection>Engineering Database</collection><collection>Nursing & Allied Health Premium</collection><collection>Advanced Technologies & Aerospace Database</collection><collection>ProQuest Advanced Technologies & Aerospace Collection</collection><collection>Biotechnology and BioEngineering Abstracts</collection><collection>Environmental Science Database</collection><collection>Materials Science Collection</collection><collection>Publicly Available Content Database</collection><collection>ProQuest One Academic Eastern Edition (DO NOT USE)</collection><collection>ProQuest One Academic</collection><collection>ProQuest One Academic UKI Edition</collection><collection>ProQuest Central China</collection><collection>Engineering Collection</collection><collection>Environmental Science Collection</collection><collection>Genetics Abstracts</collection><collection>MEDLINE - Academic</collection><collection>PubMed Central (Full Participant titles)</collection><collection>DOAJ Directory of Open Access Journals</collection><jtitle>PloS one</jtitle></facets><delivery><delcategory>Remote Search Resource</delcategory><fulltext>fulltext</fulltext></delivery><addata><au>Xu, Qiaoqing</au><au>Jiang, Yousheng</au><au>Wangkahart, Eakapol</au><au>Zou, Jun</au><au>Chang, Mingxian</au><au>Yang, Daiqin</au><au>Secombes, Chris J</au><au>Nie, Pin</au><au>Wang, Tiehui</au><au>Boudinot, Pierre</au><format>journal</format><genre>article</genre><ristype>JOUR</ristype><atitle>Sequence and Expression Analysis of Interferon Regulatory Factor 10 (IRF10) in Three Diverse Teleost Fish Reveals Its Role in Antiviral Defense</atitle><jtitle>PloS one</jtitle><addtitle>PLoS One</addtitle><date>2016-01-01</date><risdate>2016</risdate><volume>11</volume><issue>1</issue><spage>e0147181</spage><epage>e0147181</epage><pages>e0147181-e0147181</pages><issn>1932-6203</issn><eissn>1932-6203</eissn><abstract>Interferon regulatory factor (IRF) 10 was first found in birds and is present in the genome of other tetrapods (but not humans and mice), as well as in teleost fish. The functional role of IRF10 in vertebrate immunity is relatively unknown compared to IRF1-9. The target of this research was to clone and characterize the IRF10 genes in three economically important fish species that will facilitate future evaluation of this molecule in fish innate and adaptive immunity.
In the present study, a single IRF10 gene was cloned in grass carp Ctenopharyngodon idella and Asian swamp eel Monopterus albus, and two, named IRF10a and IRF10b, in rainbow trout Oncorhynchus mykiss. The fish IRF10 molecules share highest identities to other vertebrate IRF10s, and have a well conserved DNA binding domain, IRF-associated domain, and an 8 exon/7 intron structure with conserved intron phase. The presence of an upstream ATG or open reading frame (ORF) in the 5'-untranslated region of different fish IRF10 cDNA sequences suggests potential regulation at the translational level, and this has been verified by in vitro transcription/translation experiments of the trout IRF10a cDNA, but would still need to be validated in fish cells.
Both trout IRF10 paralogues are highly expressed in thymus, blood and spleen but are relatively low in head kidney and caudal kidney. Trout IRF10b expression is significantly higher than IRF10a in integumentary tissues i.e. gills, scales, skin, intestine, adipose fin and tail fins, suggesting that IRF10b may be more important in mucosal immunity. The expression of both trout IRF10 paralogues is up-regulated by recombinant IFN-γ. The expression of the IRF10 genes is highly induced by Poly I:C in vitro and in vivo, and by viral infection, but is less responsive to peptidoglycan and bacterial infection, suggesting an important role of fish IRF10 in antiviral defense.</abstract><cop>United States</cop><pub>Public Library of Science</pub><pmid>26783745</pmid><doi>10.1371/journal.pone.0147181</doi><oa>free_for_read</oa></addata></record> |
fulltext | fulltext |
identifier | ISSN: 1932-6203 |
ispartof | PloS one, 2016-01, Vol.11 (1), p.e0147181-e0147181 |
issn | 1932-6203 1932-6203 |
language | eng |
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source | MEDLINE; DOAJ Directory of Open Access Journals; Elektronische Zeitschriftenbibliothek - Frei zugängliche E-Journals; PubMed Central; Free Full-Text Journals in Chemistry; Public Library of Science (PLoS) |
subjects | Adaptive Immunity Animal diseases Animal tissues Animals Antiviral drugs Bacteria Biology and Life Sciences Birds Carp Carps - genetics Carps - immunology Cloning, Molecular Comparative analysis Ctenopharyngodon idella Deoxyribonucleic acid Diseases and pests DNA Earth Sciences Ecology and Environmental Sciences Epinephelus coioides Fins Fish Fish Proteins - genetics Fish Proteins - metabolism Fishes Gene expression Gene Expression Profiling - methods Gene Expression Regulation - drug effects Genes Genetic aspects Genomes Gills Immunity Immunity, Innate Infections Interferon Interferon regulatory factor Interferon regulatory factor 1 Interferon Regulatory Factors - genetics Interferon Regulatory Factors - metabolism Interferon-gamma - pharmacology Intestine Kidneys Molecular Sequence Data Monopterus albus Mucosal immunity Oncorhynchus mykiss Oncorhynchus mykiss - genetics Oncorhynchus mykiss - immunology Peptidoglycans Phylogeny Physiological aspects Polyinosinic:polycytidylic acid Regulatory sequences Research and Analysis Methods Salmon Scales Sequence Analysis, DNA - methods Skin Smegmamorpha - genetics Smegmamorpha - immunology Spleen Thymus Tissue Distribution Transcription Trout Viral infections Zebrafish γ-Interferon |
title | Sequence and Expression Analysis of Interferon Regulatory Factor 10 (IRF10) in Three Diverse Teleost Fish Reveals Its Role in Antiviral Defense |
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