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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Veröffentlicht in:PloS one 2016-01, Vol.11 (1), p.e0147181-e0147181
Hauptverfasser: Xu, Qiaoqing, Jiang, Yousheng, Wangkahart, Eakapol, Zou, Jun, Chang, Mingxian, Yang, Daiqin, Secombes, Chris J, Nie, Pin, Wang, Tiehui
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container_title PloS one
container_volume 11
creator Xu, Qiaoqing
Jiang, Yousheng
Wangkahart, Eakapol
Zou, Jun
Chang, Mingxian
Yang, Daiqin
Secombes, Chris J
Nie, Pin
Wang, Tiehui
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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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. 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metabolism</topic><topic>Interferon-gamma - pharmacology</topic><topic>Intestine</topic><topic>Kidneys</topic><topic>Molecular Sequence Data</topic><topic>Monopterus albus</topic><topic>Mucosal immunity</topic><topic>Oncorhynchus mykiss</topic><topic>Oncorhynchus mykiss - genetics</topic><topic>Oncorhynchus mykiss - immunology</topic><topic>Peptidoglycans</topic><topic>Phylogeny</topic><topic>Physiological aspects</topic><topic>Polyinosinic:polycytidylic acid</topic><topic>Regulatory sequences</topic><topic>Research and Analysis Methods</topic><topic>Salmon</topic><topic>Scales</topic><topic>Sequence Analysis, DNA - methods</topic><topic>Skin</topic><topic>Smegmamorpha - genetics</topic><topic>Smegmamorpha - immunology</topic><topic>Spleen</topic><topic>Thymus</topic><topic>Tissue Distribution</topic><topic>Transcription</topic><topic>Trout</topic><topic>Viral infections</topic><topic>Zebrafish</topic><topic>γ-Interferon</topic><toplevel>peer_reviewed</toplevel><toplevel>online_resources</toplevel><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><collection>Medline</collection><collection>MEDLINE</collection><collection>MEDLINE (Ovid)</collection><collection>MEDLINE</collection><collection>MEDLINE</collection><collection>PubMed</collection><collection>CrossRef</collection><collection>ProQuest Central (Corporate)</collection><collection>Animal Behavior Abstracts</collection><collection>Bacteriology Abstracts (Microbiology B)</collection><collection>Biotechnology Research Abstracts</collection><collection>Nursing &amp; Allied Health Database</collection><collection>Ecology Abstracts</collection><collection>Entomology Abstracts (Full archive)</collection><collection>Immunology Abstracts</collection><collection>Meteorological &amp; Geoastrophysical Abstracts</collection><collection>Nucleic Acids Abstracts</collection><collection>Virology and AIDS Abstracts</collection><collection>Agricultural Science Collection</collection><collection>Health &amp; Medical Collection</collection><collection>ProQuest Central (purchase pre-March 2016)</collection><collection>Medical Database (Alumni Edition)</collection><collection>ProQuest Pharma Collection</collection><collection>Public Health Database</collection><collection>Technology Research Database</collection><collection>ProQuest SciTech Collection</collection><collection>ProQuest Technology Collection</collection><collection>ProQuest Natural Science Collection</collection><collection>Hospital Premium Collection</collection><collection>Hospital Premium Collection (Alumni Edition)</collection><collection>ProQuest Central (Alumni) (purchase pre-March 2016)</collection><collection>Materials Science &amp; Engineering Collection</collection><collection>ProQuest Central (Alumni Edition)</collection><collection>ProQuest One Sustainability</collection><collection>ProQuest Central UK/Ireland</collection><collection>Advanced Technologies &amp; Aerospace Collection</collection><collection>Agricultural &amp; Environmental Science Collection</collection><collection>ProQuest Central Essentials</collection><collection>Biological Science Collection</collection><collection>ProQuest Central</collection><collection>Technology Collection</collection><collection>Natural Science Collection</collection><collection>Environmental Sciences and Pollution Management</collection><collection>ProQuest One Community College</collection><collection>ProQuest Materials Science Collection</collection><collection>ProQuest Central Korea</collection><collection>Engineering Research Database</collection><collection>Health Research Premium Collection</collection><collection>Health Research Premium Collection (Alumni)</collection><collection>ProQuest Central Student</collection><collection>AIDS and Cancer Research Abstracts</collection><collection>SciTech Premium Collection</collection><collection>ProQuest Health &amp; Medical Complete (Alumni)</collection><collection>Materials Science Database</collection><collection>Nursing &amp; Allied Health Database (Alumni Edition)</collection><collection>Meteorological &amp; Geoastrophysical Abstracts - 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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>
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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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