Two interleukin-17C-like genes exist in rainbow trout Oncorhynchus mykiss that are differentially expressed and modulated

Tiehui Wang, Samuel A M Martin, Christopher J Secombes

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48 Citations (Scopus)

Abstract

Interleukin (IL)-17 family members (IL-17A-F) are key players in adaptive immune responses and have a central role in coordinating innate and adaptive immunity. Here, we report on two novel IL-17 homologues in rainbow trout Oncorhynchus mykiss, trout (t) IL-17C1 and tIL-17C2, that share 73.7% amino acid identity. The two tIL-17C-like molecules have relatively higher sequence identities to IL-17Cs from fish and mammals and the fish IL-17C-like molecules phylogenetically form a specific clade that groups with the mammalian IL-17C and IL-17E clades. However, the gene organisation of the fish IL-17C-like molecules is closer to mammalian IL-17Es than to IL-17Cs, and this taken together with other factors suggest the fish IL-17C-like genes may have arisen from an ancestral gene that gave rise to mammalian IL-17C and IL-17E. The expression of tIL-17Cs was detectable in all the eight tissues examined, with the expression of tIL-17 mainly contributed by tIL-17C1 in gills and skin, and by tIL-17C2 in spleen, head kidney and brain. The expression of tIL-17Cs was modulated by inflammatory stimulants, including IL-1beta, interferon-gamma, LPS and PolyIC, in a trout macrophage cell line (RTS-11). IL-1beta was the most potent inducer of tIL-17C2 but only had a minor effect on the expression of tIL-17C1. LPS and PolyIC were also potent inducers of tIL-17C2. The expression of tIL-17Cs was also up-regulated by bacterial infection, with the extent and increase more dramatic for tIL-17C2. The broad distribution of expression and differential modulation of tIL-17Cs by inflammatory stimulants and infection suggest important roles of the two tIL-17Cs in the salmonid immune system.
Original languageEnglish
Pages (from-to)491-500
Number of pages10
JournalDevelopmental and Comparative Immunology
Volume34
Issue number5
Early online date10 Dec 2009
DOIs
Publication statusPublished - May 2010

Keywords

  • Adaptive Immunity
  • Amino Acid Sequence
  • Animals
  • Bacterial Infections
  • Cell Line
  • Evolution, Molecular
  • Gene Duplication
  • Gene Expression Profiling
  • Gene Expression Regulation
  • Gills
  • Inflammation Mediators
  • Interleukin-17
  • Macrophages
  • Mammals
  • Molecular Sequence Data
  • Oncorhynchus mykiss
  • Organ Specificity
  • Sequence Alignment
  • Sequence Homology, Amino Acid
  • Skin
  • Rainbow trout
  • IL-17C-like
  • Gene organisation
  • Bacterial infection
  • LPS
  • IL-1beta
  • Expression
  • Modulation
  • IL-17 cytokine family
  • Macrophages in-vitro
  • Functional-characterization
  • IFN-gamma
  • T-cell
  • Evolution
  • Member
  • Fish
  • Phytohemmaglutinin
  • Identification

Cite this

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title = "Two interleukin-17C-like genes exist in rainbow trout Oncorhynchus mykiss that are differentially expressed and modulated",
abstract = "Interleukin (IL)-17 family members (IL-17A-F) are key players in adaptive immune responses and have a central role in coordinating innate and adaptive immunity. Here, we report on two novel IL-17 homologues in rainbow trout Oncorhynchus mykiss, trout (t) IL-17C1 and tIL-17C2, that share 73.7{\%} amino acid identity. The two tIL-17C-like molecules have relatively higher sequence identities to IL-17Cs from fish and mammals and the fish IL-17C-like molecules phylogenetically form a specific clade that groups with the mammalian IL-17C and IL-17E clades. However, the gene organisation of the fish IL-17C-like molecules is closer to mammalian IL-17Es than to IL-17Cs, and this taken together with other factors suggest the fish IL-17C-like genes may have arisen from an ancestral gene that gave rise to mammalian IL-17C and IL-17E. The expression of tIL-17Cs was detectable in all the eight tissues examined, with the expression of tIL-17 mainly contributed by tIL-17C1 in gills and skin, and by tIL-17C2 in spleen, head kidney and brain. The expression of tIL-17Cs was modulated by inflammatory stimulants, including IL-1beta, interferon-gamma, LPS and PolyIC, in a trout macrophage cell line (RTS-11). IL-1beta was the most potent inducer of tIL-17C2 but only had a minor effect on the expression of tIL-17C1. LPS and PolyIC were also potent inducers of tIL-17C2. The expression of tIL-17Cs was also up-regulated by bacterial infection, with the extent and increase more dramatic for tIL-17C2. The broad distribution of expression and differential modulation of tIL-17Cs by inflammatory stimulants and infection suggest important roles of the two tIL-17Cs in the salmonid immune system.",
keywords = "Adaptive Immunity, Amino Acid Sequence, Animals, Bacterial Infections, Cell Line, Evolution, Molecular, Gene Duplication, Gene Expression Profiling, Gene Expression Regulation, Gills, Inflammation Mediators, Interleukin-17, Macrophages, Mammals, Molecular Sequence Data, Oncorhynchus mykiss, Organ Specificity, Sequence Alignment, Sequence Homology, Amino Acid, Skin, Rainbow trout, IL-17C-like, Gene organisation, Bacterial infection, LPS, IL-1beta, Expression , Modulation , IL-17 cytokine family, Macrophages in-vitro, Functional-characterization, IFN-gamma, T-cell, Evolution , Member , Fish, Phytohemmaglutinin, Identification",
author = "Tiehui Wang and Martin, {Samuel A M} and Secombes, {Christopher J}",
year = "2010",
month = "5",
doi = "10.1016/j.dci.2009.11.011",
language = "English",
volume = "34",
pages = "491--500",
journal = "Developmental and Comparative Immunology",
issn = "0145-305X",
publisher = "Elsevier Limited",
number = "5",

}

TY - JOUR

T1 - Two interleukin-17C-like genes exist in rainbow trout Oncorhynchus mykiss that are differentially expressed and modulated

AU - Wang, Tiehui

AU - Martin, Samuel A M

AU - Secombes, Christopher J

PY - 2010/5

Y1 - 2010/5

N2 - Interleukin (IL)-17 family members (IL-17A-F) are key players in adaptive immune responses and have a central role in coordinating innate and adaptive immunity. Here, we report on two novel IL-17 homologues in rainbow trout Oncorhynchus mykiss, trout (t) IL-17C1 and tIL-17C2, that share 73.7% amino acid identity. The two tIL-17C-like molecules have relatively higher sequence identities to IL-17Cs from fish and mammals and the fish IL-17C-like molecules phylogenetically form a specific clade that groups with the mammalian IL-17C and IL-17E clades. However, the gene organisation of the fish IL-17C-like molecules is closer to mammalian IL-17Es than to IL-17Cs, and this taken together with other factors suggest the fish IL-17C-like genes may have arisen from an ancestral gene that gave rise to mammalian IL-17C and IL-17E. The expression of tIL-17Cs was detectable in all the eight tissues examined, with the expression of tIL-17 mainly contributed by tIL-17C1 in gills and skin, and by tIL-17C2 in spleen, head kidney and brain. The expression of tIL-17Cs was modulated by inflammatory stimulants, including IL-1beta, interferon-gamma, LPS and PolyIC, in a trout macrophage cell line (RTS-11). IL-1beta was the most potent inducer of tIL-17C2 but only had a minor effect on the expression of tIL-17C1. LPS and PolyIC were also potent inducers of tIL-17C2. The expression of tIL-17Cs was also up-regulated by bacterial infection, with the extent and increase more dramatic for tIL-17C2. The broad distribution of expression and differential modulation of tIL-17Cs by inflammatory stimulants and infection suggest important roles of the two tIL-17Cs in the salmonid immune system.

AB - Interleukin (IL)-17 family members (IL-17A-F) are key players in adaptive immune responses and have a central role in coordinating innate and adaptive immunity. Here, we report on two novel IL-17 homologues in rainbow trout Oncorhynchus mykiss, trout (t) IL-17C1 and tIL-17C2, that share 73.7% amino acid identity. The two tIL-17C-like molecules have relatively higher sequence identities to IL-17Cs from fish and mammals and the fish IL-17C-like molecules phylogenetically form a specific clade that groups with the mammalian IL-17C and IL-17E clades. However, the gene organisation of the fish IL-17C-like molecules is closer to mammalian IL-17Es than to IL-17Cs, and this taken together with other factors suggest the fish IL-17C-like genes may have arisen from an ancestral gene that gave rise to mammalian IL-17C and IL-17E. The expression of tIL-17Cs was detectable in all the eight tissues examined, with the expression of tIL-17 mainly contributed by tIL-17C1 in gills and skin, and by tIL-17C2 in spleen, head kidney and brain. The expression of tIL-17Cs was modulated by inflammatory stimulants, including IL-1beta, interferon-gamma, LPS and PolyIC, in a trout macrophage cell line (RTS-11). IL-1beta was the most potent inducer of tIL-17C2 but only had a minor effect on the expression of tIL-17C1. LPS and PolyIC were also potent inducers of tIL-17C2. The expression of tIL-17Cs was also up-regulated by bacterial infection, with the extent and increase more dramatic for tIL-17C2. The broad distribution of expression and differential modulation of tIL-17Cs by inflammatory stimulants and infection suggest important roles of the two tIL-17Cs in the salmonid immune system.

KW - Adaptive Immunity

KW - Amino Acid Sequence

KW - Animals

KW - Bacterial Infections

KW - Cell Line

KW - Evolution, Molecular

KW - Gene Duplication

KW - Gene Expression Profiling

KW - Gene Expression Regulation

KW - Gills

KW - Inflammation Mediators

KW - Interleukin-17

KW - Macrophages

KW - Mammals

KW - Molecular Sequence Data

KW - Oncorhynchus mykiss

KW - Organ Specificity

KW - Sequence Alignment

KW - Sequence Homology, Amino Acid

KW - Skin

KW - Rainbow trout

KW - IL-17C-like

KW - Gene organisation

KW - Bacterial infection

KW - LPS

KW - IL-1beta

KW - Expression

KW - Modulation

KW - IL-17 cytokine family

KW - Macrophages in-vitro

KW - Functional-characterization

KW - IFN-gamma

KW - T-cell

KW - Evolution

KW - Member

KW - Fish

KW - Phytohemmaglutinin

KW - Identification

U2 - 10.1016/j.dci.2009.11.011

DO - 10.1016/j.dci.2009.11.011

M3 - Article

C2 - 19961871

VL - 34

SP - 491

EP - 500

JO - Developmental and Comparative Immunology

JF - Developmental and Comparative Immunology

SN - 0145-305X

IS - 5

ER -