Identification of IL-34 in teleost fish: differential expression of rainbow trout IL-34, MCSF1 and MCSF2, ligands of the MCSF receptor

Tiehui Wang, Tomoya Kono, Milena M Monte, Haruka Kuse, Maria M Costa, Hiroki Korenaga, Tanja Maehr, Mansourah Husain, Masahiro Sakai, Christopher J Secombes

Research output: Contribution to journalArticle

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Abstract

The mononuclear phagocyte system is composed of monocytes, macrophages and dendritic cells and has crucial roles in inflammation, autoimmunity, infection, cancer, organ transplantation and in maintaining organismal homeostasis. Interleukin-34 (IL-34) and macrophage colony stimulating factor (MCSF), both signalling through the MCSF receptor, regulate the mononuclear phagocyte system. A single IL-34 and MCSF gene are present in tetrapods. Two types of MCSF exist in teleost fish which is resulted from teleost-wide whole genome duplication. In this report, we first identified and sequence analysed six IL-34 genes in five teleost fish, rainbow trout, fugu, Atlantic salmon, catfish and zebrafish. The fish IL-34 molecules had a higher identity within fish group but low identities to IL-34s from birds (27.2-33.8%) and mammals (22.2-31.4%). However, they grouped with tetrapod IL-34 molecules in phylogenetic tree analysis, had a similar 7 exon/6 intron gene organisation, and genes in the IL-34 loci were syntenically conserved. In addition, the regions of the four main helices, along with a critical N-glycosylation site were well conserved. Taken together these data suggest that the teleost IL-34 genes described in this report are orthologues of tetrapod IL-34. Comparative expression study of the three trout MCSFR ligands revealed that IL-34, MCSF1 and MCSF2 are differentially expressed in tissues and cell lines. The expression of MCSF1 and MCSF2 showed great variance in different tissues and cell lines, suggesting a role in the differentiation and maintenance of specific macrophage lineages in specific locations. The relatively high levels of IL-34 expression across different tissues suggests a homeostatic role of IL-34 for the macrophage lineage in fish. One striking observation in the present study was the lack of induction of MCSF1 and MCSF2 expression but the quick induction of IL-34 expression by PAMPs and inflammatory cytokines in cell lines and primary head kidney macrophages in rainbow trout. In a parasitic proliferative kidney disease (PKD) model, the expression of IL-34 but not the dominant MCSF2 was affected by PKD, suggesting an involvement of macrophage function in this disease model. Thus IL-34 expression is sensitive to inflammatory stimuli and may regulate macrophage biology once up-regulated.
Original languageEnglish
Pages (from-to)398-409
Number of pages12
JournalMolecular Immunology
Volume53
Issue number4
Early online date23 Oct 2012
DOIs
Publication statusPublished - Apr 2013

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Macrophage Colony-Stimulating Factor Receptors
Oncorhynchus mykiss
Interleukins
Fishes
Ligands
Macrophages
Macrophage Colony-Stimulating Factor
Mononuclear Phagocyte System
Genes
Kidney Diseases
Cell Line
Takifugu
Head Kidney
Salmo salar
Catfishes
Trout
Organ Transplantation
Zebrafish

Keywords

  • Phylogeny
  • Macrophages
  • Animals
  • Recombinant Proteins
  • Exons
  • Humans
  • Interleukins
  • Amino Acid Sequence
  • Oncorhynchus mykiss
  • Macrophage Colony-Stimulating Factor
  • Protein Isoforms
  • Receptor, Macrophage Colony-Stimulating Factor
  • Conserved Sequence
  • Introns
  • Molecular Sequence Data
  • Cytokines
  • Gene Expression Regulation
  • Sequence Homology, Amino Acid

Cite this

Identification of IL-34 in teleost fish : differential expression of rainbow trout IL-34, MCSF1 and MCSF2, ligands of the MCSF receptor. / Wang, Tiehui; Kono, Tomoya; Monte, Milena M; Kuse, Haruka; Costa, Maria M; Korenaga, Hiroki; Maehr, Tanja; Husain, Mansourah; Sakai, Masahiro; Secombes, Christopher J.

In: Molecular Immunology, Vol. 53, No. 4, 04.2013, p. 398-409.

Research output: Contribution to journalArticle

Wang, Tiehui ; Kono, Tomoya ; Monte, Milena M ; Kuse, Haruka ; Costa, Maria M ; Korenaga, Hiroki ; Maehr, Tanja ; Husain, Mansourah ; Sakai, Masahiro ; Secombes, Christopher J. / Identification of IL-34 in teleost fish : differential expression of rainbow trout IL-34, MCSF1 and MCSF2, ligands of the MCSF receptor. In: Molecular Immunology. 2013 ; Vol. 53, No. 4. pp. 398-409.
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TY - JOUR

T1 - Identification of IL-34 in teleost fish

T2 - differential expression of rainbow trout IL-34, MCSF1 and MCSF2, ligands of the MCSF receptor

AU - Wang, Tiehui

AU - Kono, Tomoya

AU - Monte, Milena M

AU - Kuse, Haruka

AU - Costa, Maria M

AU - Korenaga, Hiroki

AU - Maehr, Tanja

AU - Husain, Mansourah

AU - Sakai, Masahiro

AU - Secombes, Christopher J

N1 - Copyright © 2012 Elsevier Ltd. All rights reserved.

PY - 2013/4

Y1 - 2013/4

N2 - The mononuclear phagocyte system is composed of monocytes, macrophages and dendritic cells and has crucial roles in inflammation, autoimmunity, infection, cancer, organ transplantation and in maintaining organismal homeostasis. Interleukin-34 (IL-34) and macrophage colony stimulating factor (MCSF), both signalling through the MCSF receptor, regulate the mononuclear phagocyte system. A single IL-34 and MCSF gene are present in tetrapods. Two types of MCSF exist in teleost fish which is resulted from teleost-wide whole genome duplication. In this report, we first identified and sequence analysed six IL-34 genes in five teleost fish, rainbow trout, fugu, Atlantic salmon, catfish and zebrafish. The fish IL-34 molecules had a higher identity within fish group but low identities to IL-34s from birds (27.2-33.8%) and mammals (22.2-31.4%). However, they grouped with tetrapod IL-34 molecules in phylogenetic tree analysis, had a similar 7 exon/6 intron gene organisation, and genes in the IL-34 loci were syntenically conserved. In addition, the regions of the four main helices, along with a critical N-glycosylation site were well conserved. Taken together these data suggest that the teleost IL-34 genes described in this report are orthologues of tetrapod IL-34. Comparative expression study of the three trout MCSFR ligands revealed that IL-34, MCSF1 and MCSF2 are differentially expressed in tissues and cell lines. The expression of MCSF1 and MCSF2 showed great variance in different tissues and cell lines, suggesting a role in the differentiation and maintenance of specific macrophage lineages in specific locations. The relatively high levels of IL-34 expression across different tissues suggests a homeostatic role of IL-34 for the macrophage lineage in fish. One striking observation in the present study was the lack of induction of MCSF1 and MCSF2 expression but the quick induction of IL-34 expression by PAMPs and inflammatory cytokines in cell lines and primary head kidney macrophages in rainbow trout. In a parasitic proliferative kidney disease (PKD) model, the expression of IL-34 but not the dominant MCSF2 was affected by PKD, suggesting an involvement of macrophage function in this disease model. Thus IL-34 expression is sensitive to inflammatory stimuli and may regulate macrophage biology once up-regulated.

AB - The mononuclear phagocyte system is composed of monocytes, macrophages and dendritic cells and has crucial roles in inflammation, autoimmunity, infection, cancer, organ transplantation and in maintaining organismal homeostasis. Interleukin-34 (IL-34) and macrophage colony stimulating factor (MCSF), both signalling through the MCSF receptor, regulate the mononuclear phagocyte system. A single IL-34 and MCSF gene are present in tetrapods. Two types of MCSF exist in teleost fish which is resulted from teleost-wide whole genome duplication. In this report, we first identified and sequence analysed six IL-34 genes in five teleost fish, rainbow trout, fugu, Atlantic salmon, catfish and zebrafish. The fish IL-34 molecules had a higher identity within fish group but low identities to IL-34s from birds (27.2-33.8%) and mammals (22.2-31.4%). However, they grouped with tetrapod IL-34 molecules in phylogenetic tree analysis, had a similar 7 exon/6 intron gene organisation, and genes in the IL-34 loci were syntenically conserved. In addition, the regions of the four main helices, along with a critical N-glycosylation site were well conserved. Taken together these data suggest that the teleost IL-34 genes described in this report are orthologues of tetrapod IL-34. Comparative expression study of the three trout MCSFR ligands revealed that IL-34, MCSF1 and MCSF2 are differentially expressed in tissues and cell lines. The expression of MCSF1 and MCSF2 showed great variance in different tissues and cell lines, suggesting a role in the differentiation and maintenance of specific macrophage lineages in specific locations. The relatively high levels of IL-34 expression across different tissues suggests a homeostatic role of IL-34 for the macrophage lineage in fish. One striking observation in the present study was the lack of induction of MCSF1 and MCSF2 expression but the quick induction of IL-34 expression by PAMPs and inflammatory cytokines in cell lines and primary head kidney macrophages in rainbow trout. In a parasitic proliferative kidney disease (PKD) model, the expression of IL-34 but not the dominant MCSF2 was affected by PKD, suggesting an involvement of macrophage function in this disease model. Thus IL-34 expression is sensitive to inflammatory stimuli and may regulate macrophage biology once up-regulated.

KW - Phylogeny

KW - Macrophages

KW - Animals

KW - Recombinant Proteins

KW - Exons

KW - Humans

KW - Interleukins

KW - Amino Acid Sequence

KW - Oncorhynchus mykiss

KW - Macrophage Colony-Stimulating Factor

KW - Protein Isoforms

KW - Receptor, Macrophage Colony-Stimulating Factor

KW - Conserved Sequence

KW - Introns

KW - Molecular Sequence Data

KW - Cytokines

KW - Gene Expression Regulation

KW - Sequence Homology, Amino Acid

U2 - 10.1016/j.molimm.2012.09.008

DO - 10.1016/j.molimm.2012.09.008

M3 - Article

VL - 53

SP - 398

EP - 409

JO - Molecular Immunology

JF - Molecular Immunology

SN - 0161-5890

IS - 4

ER -