Molecular and Functional Characterization of IL-15 in Rainbow Trout Oncorhynchus mykiss: A Potent Inducer of IFN-¿ Expression in Spleen Leukocytes

Tiehui Wang, Jason W Holland, Allison Carrington, Jun Zou, Christopher J Secombes

Research output: Contribution to journalArticle

71 Citations (Scopus)

Abstract

IL-15 is a member of the common gamma-chain family of cytokines that possess a heterogeneous repertoire of activities on various cells of the immune system. We report here the first functional characterization of a fish IL-15 in rainbow trout. The trout IL-15 gene is 6-kb long and contains six exons and five introns that transcribe into a 1.2-kb mRNA containing seven out-of-frame AUG initiation codons and translate into a 193-aa peptide. Potential sites for transcriptional activators and repressors have been identified in the trout IL-15 gene. Like IL-15 from other species, trout IL-15 is closely linked to an INPP4B gene, but there is also a BCL10 gene located between the IL-15 and INPP4B genes. Three alternative splicing variants of the trout IL-15 gene have also been identified and their expression in vivo was studied. Trout IL-15 expression is present in all the tissues and cell lines studied. Recombinant trout IFN-gamma selectively increased IL-15 expression but had little effect on other cytokines such as IL-1 beta and IL-11. Recombinant trout IL-15 preferentially stimulated splenic leukocytes from healthy fish, where it induced a large increase in IFN-gamma expression, with little, if any, effect on IL-1 beta expression. This effect was quite long-lived, and was still apparent 24 h poststimulation. Although the exact cell types being affected have still to be determined, it is clear that once produced IL-15 will have a profound affect on the ability of the fish immune system to activate antimicrobial defenses and genes induced themselves by IFN-gamma.

Original languageEnglish
Pages (from-to)1475-1488
Number of pages14
JournalThe Journal of Immunology
Volume179
Issue number3
Publication statusPublished - 1 Aug 2007

Keywords

  • Amino Acid Sequence
  • Animals
  • Base Sequence
  • Cell Line
  • Cloning, Molecular
  • Female
  • Interferon-gamma
  • Interleukin-15
  • Leukocytes
  • Molecular Sequence Data
  • Oncorhynchus mykiss
  • Organ Specificity
  • Sequence Alignment
  • Sequence Homology, Amino Acid
  • Spleen
  • Interleukin-15 messenger-RNA
  • Natural-killer-cells
  • KAPPA-B
  • Signal peptides
  • Dendritic cells
  • Human monocytes
  • Intracellular trafficking
  • Transcription factor
  • Langerhans Cells

Cite this

Molecular and Functional Characterization of IL-15 in Rainbow Trout Oncorhynchus mykiss : A Potent Inducer of IFN-¿ Expression in Spleen Leukocytes. / Wang, Tiehui; Holland, Jason W; Carrington, Allison; Zou, Jun; Secombes, Christopher J.

In: The Journal of Immunology, Vol. 179, No. 3, 01.08.2007, p. 1475-1488.

Research output: Contribution to journalArticle

@article{9473204e8ea04ccc9cf840d69c9b4c86,
title = "Molecular and Functional Characterization of IL-15 in Rainbow Trout Oncorhynchus mykiss: A Potent Inducer of IFN-¿ Expression in Spleen Leukocytes",
abstract = "IL-15 is a member of the common gamma-chain family of cytokines that possess a heterogeneous repertoire of activities on various cells of the immune system. We report here the first functional characterization of a fish IL-15 in rainbow trout. The trout IL-15 gene is 6-kb long and contains six exons and five introns that transcribe into a 1.2-kb mRNA containing seven out-of-frame AUG initiation codons and translate into a 193-aa peptide. Potential sites for transcriptional activators and repressors have been identified in the trout IL-15 gene. Like IL-15 from other species, trout IL-15 is closely linked to an INPP4B gene, but there is also a BCL10 gene located between the IL-15 and INPP4B genes. Three alternative splicing variants of the trout IL-15 gene have also been identified and their expression in vivo was studied. Trout IL-15 expression is present in all the tissues and cell lines studied. Recombinant trout IFN-gamma selectively increased IL-15 expression but had little effect on other cytokines such as IL-1 beta and IL-11. Recombinant trout IL-15 preferentially stimulated splenic leukocytes from healthy fish, where it induced a large increase in IFN-gamma expression, with little, if any, effect on IL-1 beta expression. This effect was quite long-lived, and was still apparent 24 h poststimulation. Although the exact cell types being affected have still to be determined, it is clear that once produced IL-15 will have a profound affect on the ability of the fish immune system to activate antimicrobial defenses and genes induced themselves by IFN-gamma.",
keywords = "Amino Acid Sequence, Animals, Base Sequence, Cell Line, Cloning, Molecular, Female, Interferon-gamma, Interleukin-15, Leukocytes, Molecular Sequence Data, Oncorhynchus mykiss, Organ Specificity, Sequence Alignment, Sequence Homology, Amino Acid, Spleen, Interleukin-15 messenger-RNA, Natural-killer-cells, KAPPA-B, Signal peptides, Dendritic cells, Human monocytes, Intracellular trafficking, Transcription factor, Langerhans Cells",
author = "Tiehui Wang and Holland, {Jason W} and Allison Carrington and Jun Zou and Secombes, {Christopher J}",
year = "2007",
month = "8",
day = "1",
language = "English",
volume = "179",
pages = "1475--1488",
journal = "The Journal of Immunology",
issn = "0022-1767",
publisher = "American Association of Immunologists",
number = "3",

}

TY - JOUR

T1 - Molecular and Functional Characterization of IL-15 in Rainbow Trout Oncorhynchus mykiss

T2 - A Potent Inducer of IFN-¿ Expression in Spleen Leukocytes

AU - Wang, Tiehui

AU - Holland, Jason W

AU - Carrington, Allison

AU - Zou, Jun

AU - Secombes, Christopher J

PY - 2007/8/1

Y1 - 2007/8/1

N2 - IL-15 is a member of the common gamma-chain family of cytokines that possess a heterogeneous repertoire of activities on various cells of the immune system. We report here the first functional characterization of a fish IL-15 in rainbow trout. The trout IL-15 gene is 6-kb long and contains six exons and five introns that transcribe into a 1.2-kb mRNA containing seven out-of-frame AUG initiation codons and translate into a 193-aa peptide. Potential sites for transcriptional activators and repressors have been identified in the trout IL-15 gene. Like IL-15 from other species, trout IL-15 is closely linked to an INPP4B gene, but there is also a BCL10 gene located between the IL-15 and INPP4B genes. Three alternative splicing variants of the trout IL-15 gene have also been identified and their expression in vivo was studied. Trout IL-15 expression is present in all the tissues and cell lines studied. Recombinant trout IFN-gamma selectively increased IL-15 expression but had little effect on other cytokines such as IL-1 beta and IL-11. Recombinant trout IL-15 preferentially stimulated splenic leukocytes from healthy fish, where it induced a large increase in IFN-gamma expression, with little, if any, effect on IL-1 beta expression. This effect was quite long-lived, and was still apparent 24 h poststimulation. Although the exact cell types being affected have still to be determined, it is clear that once produced IL-15 will have a profound affect on the ability of the fish immune system to activate antimicrobial defenses and genes induced themselves by IFN-gamma.

AB - IL-15 is a member of the common gamma-chain family of cytokines that possess a heterogeneous repertoire of activities on various cells of the immune system. We report here the first functional characterization of a fish IL-15 in rainbow trout. The trout IL-15 gene is 6-kb long and contains six exons and five introns that transcribe into a 1.2-kb mRNA containing seven out-of-frame AUG initiation codons and translate into a 193-aa peptide. Potential sites for transcriptional activators and repressors have been identified in the trout IL-15 gene. Like IL-15 from other species, trout IL-15 is closely linked to an INPP4B gene, but there is also a BCL10 gene located between the IL-15 and INPP4B genes. Three alternative splicing variants of the trout IL-15 gene have also been identified and their expression in vivo was studied. Trout IL-15 expression is present in all the tissues and cell lines studied. Recombinant trout IFN-gamma selectively increased IL-15 expression but had little effect on other cytokines such as IL-1 beta and IL-11. Recombinant trout IL-15 preferentially stimulated splenic leukocytes from healthy fish, where it induced a large increase in IFN-gamma expression, with little, if any, effect on IL-1 beta expression. This effect was quite long-lived, and was still apparent 24 h poststimulation. Although the exact cell types being affected have still to be determined, it is clear that once produced IL-15 will have a profound affect on the ability of the fish immune system to activate antimicrobial defenses and genes induced themselves by IFN-gamma.

KW - Amino Acid Sequence

KW - Animals

KW - Base Sequence

KW - Cell Line

KW - Cloning, Molecular

KW - Female

KW - Interferon-gamma

KW - Interleukin-15

KW - Leukocytes

KW - Molecular Sequence Data

KW - Oncorhynchus mykiss

KW - Organ Specificity

KW - Sequence Alignment

KW - Sequence Homology, Amino Acid

KW - Spleen

KW - Interleukin-15 messenger-RNA

KW - Natural-killer-cells

KW - KAPPA-B

KW - Signal peptides

KW - Dendritic cells

KW - Human monocytes

KW - Intracellular trafficking

KW - Transcription factor

KW - Langerhans Cells

M3 - Article

C2 - 17641013

VL - 179

SP - 1475

EP - 1488

JO - The Journal of Immunology

JF - The Journal of Immunology

SN - 0022-1767

IS - 3

ER -