Sequence and Expression Analysis of Interferon Regulatory Factor 10 (IRF10) in Three Diverse Teleost Fish Reveals Its Role in Antiviral Defense

Qiaoqing Xu, Yousheng Jiang, Eakapol Wangkahart, Jun Zou, Mingxian Chang, Daiqin Yang, Chris J. Secombes, Pin Nie, Tiehui Wang

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Abstract

Background

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.

Molecular Characterization of IRF10 in Three Fish Species

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.

Expression Analysis of IRF10 In Vivo and In Vitro

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.
Original languageEnglish
Article number0147181
Pages (from-to)1-22
Number of pages22
JournalPloS ONE
Volume11
Issue number1
DOIs
Publication statusPublished - 19 Jan 2016

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Fish
Antiviral Agents
Sequence Analysis
Fishes
fish
Trout
trout
Monopterus albus
Genes
Ctenopharyngodon idella
Oncorhynchus mykiss
Introns
fins
Vertebrates
introns
Gallus gallus interferon regulatory factor-10
interferon regulatory factors
Complementary DNA
vertebrates
kidneys

Cite this

Sequence and Expression Analysis of Interferon Regulatory Factor 10 (IRF10) in Three Diverse Teleost Fish Reveals Its Role in Antiviral Defense. / Xu, Qiaoqing; Jiang, Yousheng; Wangkahart, Eakapol; Zou, Jun; Chang, Mingxian; Yang, Daiqin; Secombes, Chris J.; Nie, Pin; Wang, Tiehui.

In: PloS ONE, Vol. 11, No. 1, 0147181, 19.01.2016, p. 1-22.

Research output: Contribution to journalArticle

Xu, Qiaoqing ; Jiang, Yousheng ; Wangkahart, Eakapol ; Zou, Jun ; Chang, Mingxian ; Yang, Daiqin ; Secombes, Chris J. ; Nie, Pin ; Wang, Tiehui. / Sequence and Expression Analysis of Interferon Regulatory Factor 10 (IRF10) in Three Diverse Teleost Fish Reveals Its Role in Antiviral Defense. In: PloS ONE. 2016 ; Vol. 11, No. 1. pp. 1-22.
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abstract = "BackgroundInterferon 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.Molecular Characterization of IRF10 in Three Fish SpeciesIn 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.Expression Analysis of IRF10 In Vivo and In VitroBoth 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.",
author = "Qiaoqing Xu and Yousheng Jiang and Eakapol Wangkahart and Jun Zou and Mingxian Chang and Daiqin Yang and Secombes, {Chris J.} and Pin Nie and Tiehui Wang",
note = "Acknowledgments This research was supported financially by the National Natural Science Foundation of China (31101928), the National Science and Technology Support Program of China (2013BAD20B06), the State Key Laboratory of Freshwater Ecology and Biotechnology (2010FB02) and the MASTS pooling initiative (The Marine Alliance for Science and Technology for Scotland) funded by the Scottish Funding Council (grant reference HR09011). Q.X. and Y.J. were supported financially by the National Scholarship Council of China. Funding: This research was supported financially by the National Natural Science Foundation of China (31101928), the National Science and Technology Support Program of China (2013BAD20B06), the State Key Laboratory of Freshwater Ecology and Biotechnology (2010FB02) and the MASTS pooling initiative (The Marine Alliance for Science and Technology for Scotland) funded by the Scottish Funding Council (grant reference HR09011). Q.X. and Y.J. were supported financially by the National Scholarship Council of China. The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript.",
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T1 - Sequence and Expression Analysis of Interferon Regulatory Factor 10 (IRF10) in Three Diverse Teleost Fish Reveals Its Role in Antiviral Defense

AU - Xu, Qiaoqing

AU - Jiang, Yousheng

AU - Wangkahart, Eakapol

AU - Zou, Jun

AU - Chang, Mingxian

AU - Yang, Daiqin

AU - Secombes, Chris J.

AU - Nie, Pin

AU - Wang, Tiehui

N1 - Acknowledgments This research was supported financially by the National Natural Science Foundation of China (31101928), the National Science and Technology Support Program of China (2013BAD20B06), the State Key Laboratory of Freshwater Ecology and Biotechnology (2010FB02) and the MASTS pooling initiative (The Marine Alliance for Science and Technology for Scotland) funded by the Scottish Funding Council (grant reference HR09011). Q.X. and Y.J. were supported financially by the National Scholarship Council of China. Funding: This research was supported financially by the National Natural Science Foundation of China (31101928), the National Science and Technology Support Program of China (2013BAD20B06), the State Key Laboratory of Freshwater Ecology and Biotechnology (2010FB02) and the MASTS pooling initiative (The Marine Alliance for Science and Technology for Scotland) funded by the Scottish Funding Council (grant reference HR09011). Q.X. and Y.J. were supported financially by the National Scholarship Council of China. The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript.

PY - 2016/1/19

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N2 - BackgroundInterferon 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.Molecular Characterization of IRF10 in Three Fish SpeciesIn 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.Expression Analysis of IRF10 In Vivo and In VitroBoth 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.

AB - BackgroundInterferon 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.Molecular Characterization of IRF10 in Three Fish SpeciesIn 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.Expression Analysis of IRF10 In Vivo and In VitroBoth 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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