Transforming growth factor-β1b: a second TGF-β1 paralogue in the rainbow trout (Oncorhynchus mykiss) that has a lower constitutive expression but is more responsive to immune stimulation

Tanja Maehr, Maria M Costa, Jose L González Vecino, Simon Wadsworth, Samuel A M Martin, Tiehui Wang, Christopher J Secombes

Research output: Contribution to journalArticle

33 Citations (Scopus)

Abstract

The rainbow trout (Oncorhynchus mykiss) TGF-β1 sequence was one of the first fish cytokines described. Studies of its expression suggest it is constitutively expressed but displays refractory inducibility. Here we describe a second TGF-β1 (TGF-β1b) gene that is novel in several respects. TGF-β1b possesses typical TGF-β features, including a CXC motif and an integrin binding site, a tetrabasic cut site and a mature peptide of 112 amino acids (aa) containing nine conserved cysteine residues. The mature peptide is 83% identical to the first TGF-β1 sequence described in rainbow trout, that we designate TGF-β1a, and relative to TGF-β1a shows higher homology to Atlantic salmon TGF-β1b, zebrafish TGF-β1a, and sea bass and seabream TGF-β1. The gene organisation of salmonid TGF-β1b genes, as inferred from Atlantic salmon whole genome shotgun contigs, is a 6 exon/5 intron structure with exons 3 and 4 of salmonid TGF-β1a genes apparently fused together. The two trout TGF-β1 genes have a wide distribution in vivo, with highest expression found in immune tissues for both isoforms indicating that TGF-β1 has a predominant role in immunity of fish. Expression of both genes was also seen during the ontogeny of trout, with TGF-β1a relatively constant in expression level but TGF-β1b increasing over time. Immune responses in head kidney (HK) macrophages induced by pathogen associated molecular patterns (PAMPs), pro-inflammatory cytokines, mitogens and pathway activators highly elevated the expression level of TGF-β1b but not that of TGF-β1a. TGF-β1b expression was also increased by polyinosinic:polycytidylic acid (poly(I:C)) and/or lipopolysaccharide (LPS) stimulation in three different trout cell lines studied. Finally we show that TGF-β1b is potentially involved in defense against infection with viral haemorrhagic septicemia virus (VHSV), which had no effect on TGF-β1a expression. Thus, it is likely the TGF-β1b gene represents a copy which fulfils the major immune orchestrating functions of TGF-β1 as seen in other vertebrates.
Original languageEnglish
Pages (from-to)420-432
Number of pages13
JournalFish & Shellfish Immunology
Volume34
Issue number2
Early online date23 Nov 2012
DOIs
Publication statusPublished - Feb 2013

Keywords

  • animals
  • base sequence
  • cytokines
  • fish diseases
  • gene components
  • gene expression profiling
  • gene expression regulation, developmental
  • head kidney
  • lipopolysaccharides
  • mitogens
  • molecular sequence data
  • novirhabdovirus
  • Oncorhynchus mykiss
  • poly I-C
  • rhabdoviridae infections
  • sequence analysis, DNA
  • species specificity
  • transforming growth factor beta1
  • rainbow trout
  • TGF-β
  • macrophage
  • LPS
  • VHSV

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