Identification and expression analysis of two interleukin-23α (p19) isoforms, in rainbow trout Oncorhynchus mykiss and Atlantic salmon Salmo salar

Yousheng Jiang, Mansourah Husain, Zhitao Qi, Steve Bird, Tiehui Wang

Research output: Contribution to journalArticle

15 Citations (Scopus)

Abstract

Interleukin (IL)-23 is a heterodimeric IL-12 family cytokine composed of a p19 α-chain, linked to a p40 β-chain that is shared with IL-12. IL-23 is distinguished functionally from IL-12 by its ability to induce the production of IL-17, and differentiation of Th17 cells in mammals. Three isoforms of p40 (p40a, p40b and p40c) have been found in some 3R teleosts. Salmonids also possess three p40 isoforms (p40b1, p40b2 and p40c) although p40a is missing, and two copies (paralogues) of p40b are present that have presumably been retained following the 4R duplication in this fish lineage. Teleost p19 has been discovered recently in zebrafish, but to date there is limited information on expression and modulation of this molecule. 

In this report we have cloned two p19 paralogues (p19a and p19b) in salmonids, suggesting that a salmonid can possess six potential IL-23 isoforms. Whilst Atlantic salmon has two active p19 genes, the rainbow trout p19b gene may have been pseudogenized. The salmonid p19 translations share moderate identities (22.8-29.9%) to zebrafish and mammalian p19 molecules, but their identity was supported by structural features, a conserved 4 exon/3 intron gene organisation, and phylogenetic tree analysis. The active salmonid p19 genes are highly expressed in blood and gonad. Bacterial (Yersinia ruckeri) and viral infection in rainbow trout induces the expression of p19a, suggesting pathogen-specific induction of IL-23 isoforms. Trout p19a expression was also induced by PAMPs (poly IC and peptidoglycan) and the proinflammatory cytokine IL-1β in primary head kidney macrophages. These data may indicate diverse functional roles of trout IL-23 isoforms in regulating the immune response in fish.

Original languageEnglish
Pages (from-to)216-228
Number of pages13
JournalMolecular Immunology
Volume66
Issue number2
Early online date1 Apr 2015
DOIs
Publication statusPublished - Aug 2015

Fingerprint

Interleukin-23
Salmo salar
Oncorhynchus mykiss
Protein Isoforms
Interleukin-12
Salmonidae
Trout
Zebrafish
Genes
Yersinia ruckeri
Fishes
Yersinia Infections
Head Kidney
Cytokines
Th17 Cells
Interleukin-17
Peptidoglycan
Gonads
Virus Diseases
Interleukin-1

Keywords

  • Amino Acid Sequence
  • Animals
  • Exons
  • Fish Diseases
  • Fish Proteins
  • Gene Expression
  • Gonads
  • Humans
  • Interleukin-1beta
  • Interleukin-23 Subunit p19
  • Introns
  • Macrophages
  • Molecular Sequence Data
  • Oncorhynchus mykiss
  • Peptidoglycan
  • Phylogeny
  • Poly I-C
  • Primary Cell Culture
  • Protein Isoforms
  • Salmo salar
  • Sequence Alignment
  • Sequence Homology, Amino Acid
  • Yersinia Infections
  • Yersinia ruckeri
  • Zebrafish

Cite this

Identification and expression analysis of two interleukin-23α (p19) isoforms, in rainbow trout Oncorhynchus mykiss and Atlantic salmon Salmo salar. / Jiang, Yousheng; Husain, Mansourah; Qi, Zhitao; Bird, Steve; Wang, Tiehui.

In: Molecular Immunology, Vol. 66, No. 2, 08.2015, p. 216-228.

Research output: Contribution to journalArticle

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abstract = "Interleukin (IL)-23 is a heterodimeric IL-12 family cytokine composed of a p19 α-chain, linked to a p40 β-chain that is shared with IL-12. IL-23 is distinguished functionally from IL-12 by its ability to induce the production of IL-17, and differentiation of Th17 cells in mammals. Three isoforms of p40 (p40a, p40b and p40c) have been found in some 3R teleosts. Salmonids also possess three p40 isoforms (p40b1, p40b2 and p40c) although p40a is missing, and two copies (paralogues) of p40b are present that have presumably been retained following the 4R duplication in this fish lineage. Teleost p19 has been discovered recently in zebrafish, but to date there is limited information on expression and modulation of this molecule. In this report we have cloned two p19 paralogues (p19a and p19b) in salmonids, suggesting that a salmonid can possess six potential IL-23 isoforms. Whilst Atlantic salmon has two active p19 genes, the rainbow trout p19b gene may have been pseudogenized. The salmonid p19 translations share moderate identities (22.8-29.9{\%}) to zebrafish and mammalian p19 molecules, but their identity was supported by structural features, a conserved 4 exon/3 intron gene organisation, and phylogenetic tree analysis. The active salmonid p19 genes are highly expressed in blood and gonad. Bacterial (Yersinia ruckeri) and viral infection in rainbow trout induces the expression of p19a, suggesting pathogen-specific induction of IL-23 isoforms. Trout p19a expression was also induced by PAMPs (poly IC and peptidoglycan) and the proinflammatory cytokine IL-1β in primary head kidney macrophages. These data may indicate diverse functional roles of trout IL-23 isoforms in regulating the immune response in fish.",
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AU - Bird, Steve

AU - Wang, Tiehui

N1 - Copyright © 2015 Elsevier Ltd. All rights reserved. Acknowledgements: TW received funding from the MASTS pooling initiative (The Marine Alliance for Science and Technology for Scotland, Scottish Funding Council grant no. HR09011). M.H. was supported financially by the Public Authority of Applied Education and Training, Kuwait. YJ were supported financially by the National Scholarship Council of Shanghai City, China. We thank Marine Scotland staff for providing samples from VHSV-infected trout generated within the Scottish Government-funded Research Project FC1996, and Prof. C.J. Secombes (University of Aberdeen) for his support and critical reading of this manuscript.

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N2 - Interleukin (IL)-23 is a heterodimeric IL-12 family cytokine composed of a p19 α-chain, linked to a p40 β-chain that is shared with IL-12. IL-23 is distinguished functionally from IL-12 by its ability to induce the production of IL-17, and differentiation of Th17 cells in mammals. Three isoforms of p40 (p40a, p40b and p40c) have been found in some 3R teleosts. Salmonids also possess three p40 isoforms (p40b1, p40b2 and p40c) although p40a is missing, and two copies (paralogues) of p40b are present that have presumably been retained following the 4R duplication in this fish lineage. Teleost p19 has been discovered recently in zebrafish, but to date there is limited information on expression and modulation of this molecule. In this report we have cloned two p19 paralogues (p19a and p19b) in salmonids, suggesting that a salmonid can possess six potential IL-23 isoforms. Whilst Atlantic salmon has two active p19 genes, the rainbow trout p19b gene may have been pseudogenized. The salmonid p19 translations share moderate identities (22.8-29.9%) to zebrafish and mammalian p19 molecules, but their identity was supported by structural features, a conserved 4 exon/3 intron gene organisation, and phylogenetic tree analysis. The active salmonid p19 genes are highly expressed in blood and gonad. Bacterial (Yersinia ruckeri) and viral infection in rainbow trout induces the expression of p19a, suggesting pathogen-specific induction of IL-23 isoforms. Trout p19a expression was also induced by PAMPs (poly IC and peptidoglycan) and the proinflammatory cytokine IL-1β in primary head kidney macrophages. These data may indicate diverse functional roles of trout IL-23 isoforms in regulating the immune response in fish.

AB - Interleukin (IL)-23 is a heterodimeric IL-12 family cytokine composed of a p19 α-chain, linked to a p40 β-chain that is shared with IL-12. IL-23 is distinguished functionally from IL-12 by its ability to induce the production of IL-17, and differentiation of Th17 cells in mammals. Three isoforms of p40 (p40a, p40b and p40c) have been found in some 3R teleosts. Salmonids also possess three p40 isoforms (p40b1, p40b2 and p40c) although p40a is missing, and two copies (paralogues) of p40b are present that have presumably been retained following the 4R duplication in this fish lineage. Teleost p19 has been discovered recently in zebrafish, but to date there is limited information on expression and modulation of this molecule. In this report we have cloned two p19 paralogues (p19a and p19b) in salmonids, suggesting that a salmonid can possess six potential IL-23 isoforms. Whilst Atlantic salmon has two active p19 genes, the rainbow trout p19b gene may have been pseudogenized. The salmonid p19 translations share moderate identities (22.8-29.9%) to zebrafish and mammalian p19 molecules, but their identity was supported by structural features, a conserved 4 exon/3 intron gene organisation, and phylogenetic tree analysis. The active salmonid p19 genes are highly expressed in blood and gonad. Bacterial (Yersinia ruckeri) and viral infection in rainbow trout induces the expression of p19a, suggesting pathogen-specific induction of IL-23 isoforms. Trout p19a expression was also induced by PAMPs (poly IC and peptidoglycan) and the proinflammatory cytokine IL-1β in primary head kidney macrophages. These data may indicate diverse functional roles of trout IL-23 isoforms in regulating the immune response in fish.

KW - Amino Acid Sequence

KW - Animals

KW - Exons

KW - Fish Diseases

KW - Fish Proteins

KW - Gene Expression

KW - Gonads

KW - Humans

KW - Interleukin-1beta

KW - Interleukin-23 Subunit p19

KW - Introns

KW - Macrophages

KW - Molecular Sequence Data

KW - Oncorhynchus mykiss

KW - Peptidoglycan

KW - Phylogeny

KW - Poly I-C

KW - Primary Cell Culture

KW - Protein Isoforms

KW - Salmo salar

KW - Sequence Alignment

KW - Sequence Homology, Amino Acid

KW - Yersinia Infections

KW - Yersinia ruckeri

KW - Zebrafish

U2 - 10.1016/j.molimm.2015.03.014

DO - 10.1016/j.molimm.2015.03.014

M3 - Article

VL - 66

SP - 216

EP - 228

JO - Molecular Immunology

JF - Molecular Immunology

SN - 0161-5890

IS - 2

ER -