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

Mol Immunol. 2015 Aug;66(2):216-28. doi: 10.1016/j.molimm.2015.03.014. Epub 2015 Apr 1.

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.

Keywords: Atlantic salmon Salmo salar; Cloning; Expression; IL-23; Rainbow trout Oncorhynchus mykiss; p19.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Amino Acid Sequence
  • Animals
  • Exons
  • Fish Diseases / genetics
  • Fish Diseases / immunology*
  • Fish Diseases / microbiology
  • Fish Proteins / blood
  • Fish Proteins / genetics*
  • Fish Proteins / immunology
  • Gene Expression
  • Gonads / immunology
  • Gonads / microbiology
  • Humans
  • Interleukin-1beta / pharmacology
  • Interleukin-23 Subunit p19 / blood
  • Interleukin-23 Subunit p19 / genetics*
  • Interleukin-23 Subunit p19 / immunology
  • Introns
  • Macrophages / cytology
  • Macrophages / drug effects
  • Macrophages / immunology
  • Molecular Sequence Data
  • Oncorhynchus mykiss / classification
  • Oncorhynchus mykiss / genetics
  • Oncorhynchus mykiss / immunology*
  • Oncorhynchus mykiss / microbiology
  • Peptidoglycan / pharmacology
  • Phylogeny
  • Poly I-C / pharmacology
  • Primary Cell Culture
  • Protein Isoforms / blood
  • Protein Isoforms / genetics
  • Protein Isoforms / immunology
  • Salmo salar / classification
  • Salmo salar / genetics
  • Salmo salar / immunology*
  • Salmo salar / microbiology
  • Sequence Alignment
  • Sequence Homology, Amino Acid
  • Yersinia Infections / immunology
  • Yersinia Infections / microbiology
  • Yersinia Infections / veterinary*
  • Yersinia ruckeri / immunology
  • Zebrafish / genetics
  • Zebrafish / immunology
  • Zebrafish / microbiology

Substances

  • Fish Proteins
  • Interleukin-1beta
  • Interleukin-23 Subunit p19
  • Peptidoglycan
  • Protein Isoforms
  • Poly I-C