The expression of immune-regulatory genes in rainbow trout, Oncorhynchus mykiss, during a natural outbreak of proliferative kidney disease (PKD)

J W Holland, C R W Gould, C S Jones, L R Noble, C J Secombes

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46 Citations (Scopus)

Abstract

Proliferative kidney disease (PKD) is a parasitic infection of salmonid fish characterized by an apparently abnormal immune response to the presence of the myxozoan parasite, Tetracapsuloides bryosalmonae. In order to examine the nature of the immune response at the molecular level, the expression of a range of immune regulatory genes, including cytokines and cyclooxygenase (COX)-2 was examined in naive unexposed fish and in naive fish exposed to parasite-infected water at three points during the course of a natural outbreak of PKD. Since fish with advanced PKD pathology generally exhibit increased susceptibility to secondary infections which is typical of stress/cortisol-mediated immune suppression, a further aim of this work was to examine in vitro the influence of the glucocorticoid cortisol on the bacterial lipopolysaccharide (LPS)-induced expression of the trout cytokine genes studied. Two weeks after the initial sampling, naive exposed fish showed a specific profile of up-regulated tumor necrosis factor (TNF)-alpha2, COX-2 and, to a lesser extent, transforming growth factor (TGF)-beta1 expression. As the disease pathology increased, TNF-alpha2 and COX-2 expression returned to normal levels. Stress levels of cortisol suppressed the LPS inducibility of pro-inflammatory cytokine genes, although TGF-beta1 and TNF-alpha2 appeared to be refractory. These data demonstrate that specific immune responses at the molecular level are affected during PKD infection, with the cortisol suppression of cytokine expression in vitro providing a possible link to PKD-mediated cytokine down-regulation and immune suppression.

Original languageEnglish
Pages (from-to)S95-102
Number of pages8
JournalParasitology
Volume126
DOIs
Publication statusPublished - 2003

Fingerprint

Oncorhynchus mykiss
Kidney Diseases
Regulator Genes
regulator genes
kidney diseases
Disease Outbreaks
Fishes
cytokines
cortisol
Hydrocortisone
Cytokines
tumor necrosis factors
prostaglandin synthase
Cyclooxygenase 2
transforming growth factor beta 1
Transforming Growth Factor beta1
fish
Tumor Necrosis Factor-alpha
immune response
lipopolysaccharides

Keywords

  • rainbow trout
  • cytokine
  • expression
  • PKD
  • cortisol
  • stress
  • SALMO-GAIRDNERI RICHARDSON
  • TUMOR-NECROSIS-FACTOR
  • TETRACAPSULA-BRYOSALMONAE
  • PARASITIC INFECTION
  • VIRUS-INFECTION
  • HANDLING STRESS
  • TNF-ALPHA
  • TGF-BETA
  • SUSCEPTIBILITY
  • INTERLEUKIN-1-BETA

Cite this

@article{0250a21cac3043f89912054ac1595218,
title = "The expression of immune-regulatory genes in rainbow trout, Oncorhynchus mykiss, during a natural outbreak of proliferative kidney disease (PKD)",
abstract = "Proliferative kidney disease (PKD) is a parasitic infection of salmonid fish characterized by an apparently abnormal immune response to the presence of the myxozoan parasite, Tetracapsuloides bryosalmonae. In order to examine the nature of the immune response at the molecular level, the expression of a range of immune regulatory genes, including cytokines and cyclooxygenase (COX)-2 was examined in naive unexposed fish and in naive fish exposed to parasite-infected water at three points during the course of a natural outbreak of PKD. Since fish with advanced PKD pathology generally exhibit increased susceptibility to secondary infections which is typical of stress/cortisol-mediated immune suppression, a further aim of this work was to examine in vitro the influence of the glucocorticoid cortisol on the bacterial lipopolysaccharide (LPS)-induced expression of the trout cytokine genes studied. Two weeks after the initial sampling, naive exposed fish showed a specific profile of up-regulated tumor necrosis factor (TNF)-alpha2, COX-2 and, to a lesser extent, transforming growth factor (TGF)-beta1 expression. As the disease pathology increased, TNF-alpha2 and COX-2 expression returned to normal levels. Stress levels of cortisol suppressed the LPS inducibility of pro-inflammatory cytokine genes, although TGF-beta1 and TNF-alpha2 appeared to be refractory. These data demonstrate that specific immune responses at the molecular level are affected during PKD infection, with the cortisol suppression of cytokine expression in vitro providing a possible link to PKD-mediated cytokine down-regulation and immune suppression.",
keywords = "rainbow trout, cytokine, expression, PKD, cortisol, stress, SALMO-GAIRDNERI RICHARDSON, TUMOR-NECROSIS-FACTOR, TETRACAPSULA-BRYOSALMONAE, PARASITIC INFECTION, VIRUS-INFECTION, HANDLING STRESS, TNF-ALPHA, TGF-BETA, SUSCEPTIBILITY, INTERLEUKIN-1-BETA",
author = "Holland, {J W} and Gould, {C R W} and Jones, {C S} and Noble, {L R} and Secombes, {C J}",
year = "2003",
doi = "10.1017/S0031182003003767",
language = "English",
volume = "126",
pages = "S95--102",
journal = "Parasitology",
issn = "0031-1820",
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TY - JOUR

T1 - The expression of immune-regulatory genes in rainbow trout, Oncorhynchus mykiss, during a natural outbreak of proliferative kidney disease (PKD)

AU - Holland, J W

AU - Gould, C R W

AU - Jones, C S

AU - Noble, L R

AU - Secombes, C J

PY - 2003

Y1 - 2003

N2 - Proliferative kidney disease (PKD) is a parasitic infection of salmonid fish characterized by an apparently abnormal immune response to the presence of the myxozoan parasite, Tetracapsuloides bryosalmonae. In order to examine the nature of the immune response at the molecular level, the expression of a range of immune regulatory genes, including cytokines and cyclooxygenase (COX)-2 was examined in naive unexposed fish and in naive fish exposed to parasite-infected water at three points during the course of a natural outbreak of PKD. Since fish with advanced PKD pathology generally exhibit increased susceptibility to secondary infections which is typical of stress/cortisol-mediated immune suppression, a further aim of this work was to examine in vitro the influence of the glucocorticoid cortisol on the bacterial lipopolysaccharide (LPS)-induced expression of the trout cytokine genes studied. Two weeks after the initial sampling, naive exposed fish showed a specific profile of up-regulated tumor necrosis factor (TNF)-alpha2, COX-2 and, to a lesser extent, transforming growth factor (TGF)-beta1 expression. As the disease pathology increased, TNF-alpha2 and COX-2 expression returned to normal levels. Stress levels of cortisol suppressed the LPS inducibility of pro-inflammatory cytokine genes, although TGF-beta1 and TNF-alpha2 appeared to be refractory. These data demonstrate that specific immune responses at the molecular level are affected during PKD infection, with the cortisol suppression of cytokine expression in vitro providing a possible link to PKD-mediated cytokine down-regulation and immune suppression.

AB - Proliferative kidney disease (PKD) is a parasitic infection of salmonid fish characterized by an apparently abnormal immune response to the presence of the myxozoan parasite, Tetracapsuloides bryosalmonae. In order to examine the nature of the immune response at the molecular level, the expression of a range of immune regulatory genes, including cytokines and cyclooxygenase (COX)-2 was examined in naive unexposed fish and in naive fish exposed to parasite-infected water at three points during the course of a natural outbreak of PKD. Since fish with advanced PKD pathology generally exhibit increased susceptibility to secondary infections which is typical of stress/cortisol-mediated immune suppression, a further aim of this work was to examine in vitro the influence of the glucocorticoid cortisol on the bacterial lipopolysaccharide (LPS)-induced expression of the trout cytokine genes studied. Two weeks after the initial sampling, naive exposed fish showed a specific profile of up-regulated tumor necrosis factor (TNF)-alpha2, COX-2 and, to a lesser extent, transforming growth factor (TGF)-beta1 expression. As the disease pathology increased, TNF-alpha2 and COX-2 expression returned to normal levels. Stress levels of cortisol suppressed the LPS inducibility of pro-inflammatory cytokine genes, although TGF-beta1 and TNF-alpha2 appeared to be refractory. These data demonstrate that specific immune responses at the molecular level are affected during PKD infection, with the cortisol suppression of cytokine expression in vitro providing a possible link to PKD-mediated cytokine down-regulation and immune suppression.

KW - rainbow trout

KW - cytokine

KW - expression

KW - PKD

KW - cortisol

KW - stress

KW - SALMO-GAIRDNERI RICHARDSON

KW - TUMOR-NECROSIS-FACTOR

KW - TETRACAPSULA-BRYOSALMONAE

KW - PARASITIC INFECTION

KW - VIRUS-INFECTION

KW - HANDLING STRESS

KW - TNF-ALPHA

KW - TGF-BETA

KW - SUSCEPTIBILITY

KW - INTERLEUKIN-1-BETA

U2 - 10.1017/S0031182003003767

DO - 10.1017/S0031182003003767

M3 - Article

VL - 126

SP - S95-102

JO - Parasitology

JF - Parasitology

SN - 0031-1820

ER -