Identification and expression analysis of two fish-specific IL-6 cytokine family members, the ciliary neurotrophic factor (CNTF)-like and M17 genes, in rainbow trout Oncorhynchus mykiss

Tiehui Wang, Christopher J Secombes

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28 Citations (Scopus)

Abstract

The mammalian interleukin (IL)-6 family of cytokines consist of eight class-I helical cytokines and are major players in hematopoiesis, as well as in neuroendocrine and immune systems, and have pro- and anti-inflammatory properties. We have identified a novel fish CNTF-like molecule, for the first time, as well as the trout M17 gene. The trout CNTF-like gene encodes a putative 191 amino acid peptide without a signal peptide, and shares high amino acid sequence identities (39-99%) within the fish CNTF-like molecules that we have identified, but only limited identities (21-24%) to higher vertebrate CNTF molecules among the IL-6 family members. The fish CNTF-like gene has two phase 0 introns in the coding region whilst the mammalian CNTF gene has only one phase 0 intron. The trout M17 encodes a peptide of 227 amino acid residues which has a predicted signal peptide of 35 aa and shares the highest identities (38-95%) to other fish M17 molecules, but limited homology to other IL-6 family members. Both of the fish CNTF-like and M17 proteins have four predicted helices and their tertiary structure could be stabilised by multiple conserved disulphide bonds. Phylogenetic analysis suggests that the fish CNTF-like and M17 genes may have arisen from ancestral genes that have given rise to mammalian LIF/OSM, and CNTF/CLC/CT-1/CT-2 of the IL-6 family. The trout CNTF-like gene is highly expressed in brain and muscle, whilst the M17 is highly expressed in immune tissues, including gills, spleen and head kidney. Furthermore, immune stimulation of a macrophage cell line and bacterial infection in vivo up-regulated M17 expression but had little effect on CNTF-like expression. These results suggest a major role of the CNTF-like molecule in fish nervous and muscular systems and of M17 in the immune system.
Original languageEnglish
Pages (from-to)2290-2298
Number of pages9
JournalMolecular Immunology
Volume46
Issue number11-12
Early online date6 May 2009
DOIs
Publication statusPublished - Jul 2009

Fingerprint

Ciliary Neurotrophic Factor
Oncorhynchus mykiss
Interleukin-6
Fishes
Cytokines
Genes
Trout
Protein Sorting Signals
Introns
Immune System
Head Kidney
Amino Acids
Peptides
Neurosecretory Systems
Hematopoiesis
Bacterial Infections
Disulfides
Nervous System
Vertebrates
Amino Acid Sequence

Keywords

  • amino acid sequence
  • animals
  • base sequence
  • ciliary neurotrophic factor
  • interleukin-6
  • introns
  • molecular sequence data
  • Oncorhynchus mykiss
  • phylogeny
  • yersinia infections

Cite this

@article{3eb0523188104bee88c9d6e2c00ea23a,
title = "Identification and expression analysis of two fish-specific IL-6 cytokine family members, the ciliary neurotrophic factor (CNTF)-like and M17 genes, in rainbow trout Oncorhynchus mykiss",
abstract = "The mammalian interleukin (IL)-6 family of cytokines consist of eight class-I helical cytokines and are major players in hematopoiesis, as well as in neuroendocrine and immune systems, and have pro- and anti-inflammatory properties. We have identified a novel fish CNTF-like molecule, for the first time, as well as the trout M17 gene. The trout CNTF-like gene encodes a putative 191 amino acid peptide without a signal peptide, and shares high amino acid sequence identities (39-99{\%}) within the fish CNTF-like molecules that we have identified, but only limited identities (21-24{\%}) to higher vertebrate CNTF molecules among the IL-6 family members. The fish CNTF-like gene has two phase 0 introns in the coding region whilst the mammalian CNTF gene has only one phase 0 intron. The trout M17 encodes a peptide of 227 amino acid residues which has a predicted signal peptide of 35 aa and shares the highest identities (38-95{\%}) to other fish M17 molecules, but limited homology to other IL-6 family members. Both of the fish CNTF-like and M17 proteins have four predicted helices and their tertiary structure could be stabilised by multiple conserved disulphide bonds. Phylogenetic analysis suggests that the fish CNTF-like and M17 genes may have arisen from ancestral genes that have given rise to mammalian LIF/OSM, and CNTF/CLC/CT-1/CT-2 of the IL-6 family. The trout CNTF-like gene is highly expressed in brain and muscle, whilst the M17 is highly expressed in immune tissues, including gills, spleen and head kidney. Furthermore, immune stimulation of a macrophage cell line and bacterial infection in vivo up-regulated M17 expression but had little effect on CNTF-like expression. These results suggest a major role of the CNTF-like molecule in fish nervous and muscular systems and of M17 in the immune system.",
keywords = "amino acid sequence, animals, base sequence, ciliary neurotrophic factor, interleukin-6, introns, molecular sequence data , Oncorhynchus mykiss, phylogeny, yersinia infections",
author = "Tiehui Wang and Secombes, {Christopher J}",
year = "2009",
month = "7",
doi = "10.1016/j.molimm.2009.04.003",
language = "English",
volume = "46",
pages = "2290--2298",
journal = "Molecular Immunology",
issn = "0161-5890",
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number = "11-12",

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TY - JOUR

T1 - Identification and expression analysis of two fish-specific IL-6 cytokine family members, the ciliary neurotrophic factor (CNTF)-like and M17 genes, in rainbow trout Oncorhynchus mykiss

AU - Wang, Tiehui

AU - Secombes, Christopher J

PY - 2009/7

Y1 - 2009/7

N2 - The mammalian interleukin (IL)-6 family of cytokines consist of eight class-I helical cytokines and are major players in hematopoiesis, as well as in neuroendocrine and immune systems, and have pro- and anti-inflammatory properties. We have identified a novel fish CNTF-like molecule, for the first time, as well as the trout M17 gene. The trout CNTF-like gene encodes a putative 191 amino acid peptide without a signal peptide, and shares high amino acid sequence identities (39-99%) within the fish CNTF-like molecules that we have identified, but only limited identities (21-24%) to higher vertebrate CNTF molecules among the IL-6 family members. The fish CNTF-like gene has two phase 0 introns in the coding region whilst the mammalian CNTF gene has only one phase 0 intron. The trout M17 encodes a peptide of 227 amino acid residues which has a predicted signal peptide of 35 aa and shares the highest identities (38-95%) to other fish M17 molecules, but limited homology to other IL-6 family members. Both of the fish CNTF-like and M17 proteins have four predicted helices and their tertiary structure could be stabilised by multiple conserved disulphide bonds. Phylogenetic analysis suggests that the fish CNTF-like and M17 genes may have arisen from ancestral genes that have given rise to mammalian LIF/OSM, and CNTF/CLC/CT-1/CT-2 of the IL-6 family. The trout CNTF-like gene is highly expressed in brain and muscle, whilst the M17 is highly expressed in immune tissues, including gills, spleen and head kidney. Furthermore, immune stimulation of a macrophage cell line and bacterial infection in vivo up-regulated M17 expression but had little effect on CNTF-like expression. These results suggest a major role of the CNTF-like molecule in fish nervous and muscular systems and of M17 in the immune system.

AB - The mammalian interleukin (IL)-6 family of cytokines consist of eight class-I helical cytokines and are major players in hematopoiesis, as well as in neuroendocrine and immune systems, and have pro- and anti-inflammatory properties. We have identified a novel fish CNTF-like molecule, for the first time, as well as the trout M17 gene. The trout CNTF-like gene encodes a putative 191 amino acid peptide without a signal peptide, and shares high amino acid sequence identities (39-99%) within the fish CNTF-like molecules that we have identified, but only limited identities (21-24%) to higher vertebrate CNTF molecules among the IL-6 family members. The fish CNTF-like gene has two phase 0 introns in the coding region whilst the mammalian CNTF gene has only one phase 0 intron. The trout M17 encodes a peptide of 227 amino acid residues which has a predicted signal peptide of 35 aa and shares the highest identities (38-95%) to other fish M17 molecules, but limited homology to other IL-6 family members. Both of the fish CNTF-like and M17 proteins have four predicted helices and their tertiary structure could be stabilised by multiple conserved disulphide bonds. Phylogenetic analysis suggests that the fish CNTF-like and M17 genes may have arisen from ancestral genes that have given rise to mammalian LIF/OSM, and CNTF/CLC/CT-1/CT-2 of the IL-6 family. The trout CNTF-like gene is highly expressed in brain and muscle, whilst the M17 is highly expressed in immune tissues, including gills, spleen and head kidney. Furthermore, immune stimulation of a macrophage cell line and bacterial infection in vivo up-regulated M17 expression but had little effect on CNTF-like expression. These results suggest a major role of the CNTF-like molecule in fish nervous and muscular systems and of M17 in the immune system.

KW - amino acid sequence

KW - animals

KW - base sequence

KW - ciliary neurotrophic factor

KW - interleukin-6

KW - introns

KW - molecular sequence data

KW - Oncorhynchus mykiss

KW - phylogeny

KW - yersinia infections

U2 - 10.1016/j.molimm.2009.04.003

DO - 10.1016/j.molimm.2009.04.003

M3 - Article

C2 - 19419770

VL - 46

SP - 2290

EP - 2298

JO - Molecular Immunology

JF - Molecular Immunology

SN - 0161-5890

IS - 11-12

ER -