Identification of IL-34 in teleost fish: Differential expression of rainbow trout IL-34, MCSF1 and MCSF2, ligands of the MCSF receptor
- Authors
- Wang, T., Kono, T., Monte, M.M., Kuse, H., Costa, M.M., Korenaga, H., Maehr, T., Husain, M., Sakai, M., and Secombes, C.J.
- ID
- ZDB-PUB-121105-6
- Date
- 2013
- Source
- Molecular immunology 53(4): 398-409 (Journal)
- Registered Authors
- Keywords
- teleost fish, IL-34, MCSF, MCSFR, gene cloning, differential expression
- MeSH Terms
-
- Oncorhynchus mykiss/genetics*
- Oncorhynchus mykiss/immunology
- Macrophages/cytology
- Macrophages/immunology*
- Macrophages/metabolism
- Amino Acid Sequence
- Macrophage Colony-Stimulating Factor/genetics*
- Macrophage Colony-Stimulating Factor/immunology
- Humans
- Sequence Homology, Amino Acid
- Cytokines/pharmacology
- Exons
- Phylogeny
- Protein Isoforms/genetics
- Protein Isoforms/immunology
- Gene Expression Regulation/drug effects
- Gene Expression Regulation/immunology
- Introns
- Receptor, Macrophage Colony-Stimulating Factor/genetics
- Receptor, Macrophage Colony-Stimulating Factor/immunology
- Molecular Sequence Data
- Interleukins/genetics*
- Interleukins/immunology
- Recombinant Proteins/genetics
- Recombinant Proteins/immunology
- Animals
- Conserved Sequence
- PubMed
- 23099477 Full text @ Mol. Immunol.
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.