Sequence and expression analysis of two T helper master transcription factors, T-bet and GATA3, in rainbow trout Oncorhynchus mykiss and analysis of their expression during bacterial and parasitic infection

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Abstract

The polarization of naïve CD4+ T cells to T helper (Th)1 or Th2 cells is specified by two master transcription factors, T-bet and GATA3, and is an essential feature of mammalian adaptive immune responses to pathogens and the development of long-lasting immunity. We report here the cloning of rainbow trout Oncorhynchus mykiss T-bet and GATA3, to allow the future evaluation of the existence of Th1 and Th2 cells in salmonid fish. The trout T-bet translation shares high amino acid identities to other fish T-bet molecules (71-72%) but low identities to mammalian T-bet genes (41-42%), although the middle T-box DNA binding domain is highly conserved among all the T-bet proteins from fish and mammals. The trout GATA3 has high amino acid sequence identities (73-88%) to all known vertebrate molecules, with two highly conserved zinc finger motifs. The identity of the trout T-bet and GATA3 molecules was confirmed by phylogenetic tree analysis.A comparable expression level of T-bet and GATA3 was seen in the spleen, head kidney and muscle in healthy trout, but a higher expression level of GATA3 was seen in the gills, brain, skin and intestine relative to that of T-bet. T-bet and GATA3 expression was modulated by different stimulants. The T cell stimulant PHA up-regulated the expression of both T-bet and GATA3 in splenocytes, suggesting that they may be mainly expressed by activated T cells. The expression of T-bet and GATA3 in the spleen was increased by acute stress, but their expression was inhibited by bacterial (Yersinia ruckeri) infection. In a parasitic infection model, Tetracapsuloides bryosalmonae infection induced a biased gene expression profile where a large increase in the expression of T-bet, IFN-¿ and IL-2 was seen, suggesting that a Th1-like response is likely induced by this disease. A better understanding of pathogen modulated expression of T-bet and GATA3, and the potential underlying host immune responses elicited as a consequence of their expression, may allow novel future control measures against disease in fish to be developed.
Original languageEnglish
Pages (from-to)705-715
Number of pages11
JournalFish & Shellfish Immunology
Volume29
Issue number5
Early online date13 Jul 2010
DOIs
Publication statusPublished - Nov 2010

Fingerprint

T-cells
parasitoses
bacterial infections
Fish
trout
rainbow
Oncorhynchus mykiss
transcription factors
Pathogens
Molecules
T-lymphocytes
fish
immune response
Fish Proteins
Amino Acids
spleen
Mammals
pathogen
amino acid
Cloning

Keywords

  • Animals
  • Base Sequence
  • CD4-Positive T-Lymphocytes
  • Cloning, Molecular
  • Cluster Analysis
  • DNA Primers
  • Fish Diseases
  • GATA3 Transcription Factor
  • Gene Expression Profiling
  • Molecular Sequence Data
  • Myxozoa
  • Oncorhynchus mykiss
  • Parasitic Diseases, Animal
  • Phylogeny
  • Sequence Alignment
  • Sequence Analysis, DNA
  • Sequence Homology
  • Species Specificity
  • T-Box Domain Proteins
  • Yersinia Infections
  • Yersinia ruckeri

Cite this

@article{dd4aee3e2aa44242bbb738ec30edded2,
title = "Sequence and expression analysis of two T helper master transcription factors, T-bet and GATA3, in rainbow trout Oncorhynchus mykiss and analysis of their expression during bacterial and parasitic infection",
abstract = "The polarization of na{\"i}ve CD4+ T cells to T helper (Th)1 or Th2 cells is specified by two master transcription factors, T-bet and GATA3, and is an essential feature of mammalian adaptive immune responses to pathogens and the development of long-lasting immunity. We report here the cloning of rainbow trout Oncorhynchus mykiss T-bet and GATA3, to allow the future evaluation of the existence of Th1 and Th2 cells in salmonid fish. The trout T-bet translation shares high amino acid identities to other fish T-bet molecules (71-72{\%}) but low identities to mammalian T-bet genes (41-42{\%}), although the middle T-box DNA binding domain is highly conserved among all the T-bet proteins from fish and mammals. The trout GATA3 has high amino acid sequence identities (73-88{\%}) to all known vertebrate molecules, with two highly conserved zinc finger motifs. The identity of the trout T-bet and GATA3 molecules was confirmed by phylogenetic tree analysis.A comparable expression level of T-bet and GATA3 was seen in the spleen, head kidney and muscle in healthy trout, but a higher expression level of GATA3 was seen in the gills, brain, skin and intestine relative to that of T-bet. T-bet and GATA3 expression was modulated by different stimulants. The T cell stimulant PHA up-regulated the expression of both T-bet and GATA3 in splenocytes, suggesting that they may be mainly expressed by activated T cells. The expression of T-bet and GATA3 in the spleen was increased by acute stress, but their expression was inhibited by bacterial (Yersinia ruckeri) infection. In a parasitic infection model, Tetracapsuloides bryosalmonae infection induced a biased gene expression profile where a large increase in the expression of T-bet, IFN-¿ and IL-2 was seen, suggesting that a Th1-like response is likely induced by this disease. A better understanding of pathogen modulated expression of T-bet and GATA3, and the potential underlying host immune responses elicited as a consequence of their expression, may allow novel future control measures against disease in fish to be developed.",
keywords = "Animals, Base Sequence, CD4-Positive T-Lymphocytes, Cloning, Molecular, Cluster Analysis, DNA Primers, Fish Diseases, GATA3 Transcription Factor, Gene Expression Profiling, Molecular Sequence Data, Myxozoa, Oncorhynchus mykiss, Parasitic Diseases, Animal, Phylogeny, Sequence Alignment, Sequence Analysis, DNA, Sequence Homology, Species Specificity, T-Box Domain Proteins, Yersinia Infections, Yersinia ruckeri",
author = "Tiehui Wang and Holland, {Jason W.} and Martin, {Sam A.M.} and Secombes, {Christopher J.}",
note = "A paid open access option is available for this journal. Voluntary deposit by author of pre-print allowed on Institutions open scholarly website and pre-print servers Voluntary deposit by author of authors post-print allowed on institutions open scholarly website including Institutional Repository Deposit due to Funding Body, Institutional and Governmental mandate only allowed where separate agreement between repository and publisher exists Set statement to accompany deposit Published source must be acknowledged Must link to journal home page or articles' DOI Publisher's version/PDF cannot be used Articles in some journals can be made Open Access on payment of additional charge NIH Authors articles will be submitted to PubMed Central after 12 months Authors who are required to deposit in subject-based repositories may also use Sponsorship Option",
year = "2010",
month = "11",
doi = "10.1016/j.fsi.2010.06.016",
language = "English",
volume = "29",
pages = "705--715",
journal = "Fish & Shellfish Immunology",
issn = "1050-4648",
publisher = "ACADEMIC PRESS LTD- ELSEVIER SCIENCE LTD",
number = "5",

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TY - JOUR

T1 - Sequence and expression analysis of two T helper master transcription factors, T-bet and GATA3, in rainbow trout Oncorhynchus mykiss and analysis of their expression during bacterial and parasitic infection

AU - Wang, Tiehui

AU - Holland, Jason W.

AU - Martin, Sam A.M.

AU - Secombes, Christopher J.

N1 - A paid open access option is available for this journal. Voluntary deposit by author of pre-print allowed on Institutions open scholarly website and pre-print servers Voluntary deposit by author of authors post-print allowed on institutions open scholarly website including Institutional Repository Deposit due to Funding Body, Institutional and Governmental mandate only allowed where separate agreement between repository and publisher exists Set statement to accompany deposit Published source must be acknowledged Must link to journal home page or articles' DOI Publisher's version/PDF cannot be used Articles in some journals can be made Open Access on payment of additional charge NIH Authors articles will be submitted to PubMed Central after 12 months Authors who are required to deposit in subject-based repositories may also use Sponsorship Option

PY - 2010/11

Y1 - 2010/11

N2 - The polarization of naïve CD4+ T cells to T helper (Th)1 or Th2 cells is specified by two master transcription factors, T-bet and GATA3, and is an essential feature of mammalian adaptive immune responses to pathogens and the development of long-lasting immunity. We report here the cloning of rainbow trout Oncorhynchus mykiss T-bet and GATA3, to allow the future evaluation of the existence of Th1 and Th2 cells in salmonid fish. The trout T-bet translation shares high amino acid identities to other fish T-bet molecules (71-72%) but low identities to mammalian T-bet genes (41-42%), although the middle T-box DNA binding domain is highly conserved among all the T-bet proteins from fish and mammals. The trout GATA3 has high amino acid sequence identities (73-88%) to all known vertebrate molecules, with two highly conserved zinc finger motifs. The identity of the trout T-bet and GATA3 molecules was confirmed by phylogenetic tree analysis.A comparable expression level of T-bet and GATA3 was seen in the spleen, head kidney and muscle in healthy trout, but a higher expression level of GATA3 was seen in the gills, brain, skin and intestine relative to that of T-bet. T-bet and GATA3 expression was modulated by different stimulants. The T cell stimulant PHA up-regulated the expression of both T-bet and GATA3 in splenocytes, suggesting that they may be mainly expressed by activated T cells. The expression of T-bet and GATA3 in the spleen was increased by acute stress, but their expression was inhibited by bacterial (Yersinia ruckeri) infection. In a parasitic infection model, Tetracapsuloides bryosalmonae infection induced a biased gene expression profile where a large increase in the expression of T-bet, IFN-¿ and IL-2 was seen, suggesting that a Th1-like response is likely induced by this disease. A better understanding of pathogen modulated expression of T-bet and GATA3, and the potential underlying host immune responses elicited as a consequence of their expression, may allow novel future control measures against disease in fish to be developed.

AB - The polarization of naïve CD4+ T cells to T helper (Th)1 or Th2 cells is specified by two master transcription factors, T-bet and GATA3, and is an essential feature of mammalian adaptive immune responses to pathogens and the development of long-lasting immunity. We report here the cloning of rainbow trout Oncorhynchus mykiss T-bet and GATA3, to allow the future evaluation of the existence of Th1 and Th2 cells in salmonid fish. The trout T-bet translation shares high amino acid identities to other fish T-bet molecules (71-72%) but low identities to mammalian T-bet genes (41-42%), although the middle T-box DNA binding domain is highly conserved among all the T-bet proteins from fish and mammals. The trout GATA3 has high amino acid sequence identities (73-88%) to all known vertebrate molecules, with two highly conserved zinc finger motifs. The identity of the trout T-bet and GATA3 molecules was confirmed by phylogenetic tree analysis.A comparable expression level of T-bet and GATA3 was seen in the spleen, head kidney and muscle in healthy trout, but a higher expression level of GATA3 was seen in the gills, brain, skin and intestine relative to that of T-bet. T-bet and GATA3 expression was modulated by different stimulants. The T cell stimulant PHA up-regulated the expression of both T-bet and GATA3 in splenocytes, suggesting that they may be mainly expressed by activated T cells. The expression of T-bet and GATA3 in the spleen was increased by acute stress, but their expression was inhibited by bacterial (Yersinia ruckeri) infection. In a parasitic infection model, Tetracapsuloides bryosalmonae infection induced a biased gene expression profile where a large increase in the expression of T-bet, IFN-¿ and IL-2 was seen, suggesting that a Th1-like response is likely induced by this disease. A better understanding of pathogen modulated expression of T-bet and GATA3, and the potential underlying host immune responses elicited as a consequence of their expression, may allow novel future control measures against disease in fish to be developed.

KW - Animals

KW - Base Sequence

KW - CD4-Positive T-Lymphocytes

KW - Cloning, Molecular

KW - Cluster Analysis

KW - DNA Primers

KW - Fish Diseases

KW - GATA3 Transcription Factor

KW - Gene Expression Profiling

KW - Molecular Sequence Data

KW - Myxozoa

KW - Oncorhynchus mykiss

KW - Parasitic Diseases, Animal

KW - Phylogeny

KW - Sequence Alignment

KW - Sequence Analysis, DNA

KW - Sequence Homology

KW - Species Specificity

KW - T-Box Domain Proteins

KW - Yersinia Infections

KW - Yersinia ruckeri

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U2 - 10.1016/j.fsi.2010.06.016

DO - 10.1016/j.fsi.2010.06.016

M3 - Article

VL - 29

SP - 705

EP - 715

JO - Fish & Shellfish Immunology

JF - Fish & Shellfish Immunology

SN - 1050-4648

IS - 5

ER -