Cloning and expression of feline colony stimulating factor receptor (CSF-1R) and analysis of the species specificity of stimulation by colony stimulating factor-1 (CSF-1) and interleukin-34 (IL-34)

Gow, Deborah J.; Garceau, Valérie; Pridans, Clare; Gow, Adam; Simpson, Kerry; Gunn-Moore, Danièlle; Hume, David

doi:10.1016/j.cyto.2012.11.014

Cited by 17 publications

(16 citation statements)

References 66 publications

(29 reference statements)

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“…IL-34 orthologs have not only been found across all classes of vertebrates [24,51,53,54], but it would also seem that this gene actually predates CSF-1, as an IL-34 but no CSF-1 homolog has been recently identified in elasmobranchs [55]. At this time, it is difficult to speculate whether our findings pertaining to the functional differences between X. laevis IL-34-and CSF-1-derived tadpole macrophages extend to evolutionarily and physiologically distinct vertebrate species or reflect unique physiological and immunological strategies on the part of amphibians.…”

Section: Discussionmentioning

confidence: 99%

Divergent antiviral roles of amphibian (Xenopus laevis) macrophages elicited by colony-stimulating factor-1 and interleukin-34

Grayfer

Robert

2014

Journal of Leukocyte Biology

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Macrophages are integral to amphibian immunity against RVs, as well as to the infection strategies of these pathogens. Although CSF-1 was considered to be the principal mediator of macrophage development, the IL-34 cytokine, which shares no sequence identity with CSF-1, is now believed to contribute to vertebrate monopoiesis. However, the respective roles of CSF-1- and IL-34-derived macrophages are still poorly understood. To delineate the contribution of these macrophage populations to amphibian immunity against the RV FV3, we identified the Xenopus laevis IL-34 and transcriptionally and functionally compared this cytokine with the previously identified X. laevis CSF-1. The X. laevis CSF-1 and IL-34 displayed strikingly nonoverlapping developmental and tissue-specific gene-expression patterns. Furthermore, only CSF-1 but not IL-34 was up-regulated in the kidneys of FV3-challenged tadpoles. Intriguingly, recombinant forms of these cytokines (rXlCSF-1, rXlIL-34) elicited morphologically distinct tadpole macrophages, and whereas rXlCSF-1 pretreatment decreased the survival of FV3-infected tadpoles, rXlIL-34 administration significantly prolonged FV3-challenged animal survival. Compared with rXlIL-34-elicited macrophages, macrophages derived by rXlCSF-1 were more phagocytic but also significantly more susceptible to in vitro FV3 infections. By contrast, rXlIL-34-derived macrophages exhibited significantly greater in vitro antiranaviral activity and displayed substantially more robust gene expression of the NADPH oxidase components (p67(phox), gp91(phox)) and type I IFN. Moreover, FV3-challenged, rXlIL-34-derived macrophages exhibited several orders of magnitude greater up-regulation of the type I IFN gene expression. This marks the first report of the disparate roles of CSF-1 and IL-34 in vertebrate antiviral immunity.

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Section: Discussionmentioning

confidence: 99%

Divergent antiviral roles of amphibian (Xenopus laevis) macrophages elicited by colony-stimulating factor-1 and interleukin-34

Grayfer

Robert

2014

Journal of Leukocyte Biology

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“…IL‐34 exists in all types of vertebrates including fish, amphibians, birds, and mammals . These species show a similar gene organization of IL‐34, consisting of 7 exons and 6 introns.…”

Section: Il‐34 Biologymentioning

confidence: 99%

“…On the other hand, murine IL‐34 is capable of activating CSF‐1R in mouse, human, and pig but not in cats. Both human and mouse IL‐34 have similar activity on the pig and feline CSF‐1R . At the amino acid sequence level, IL‐34 is highly conserved among avian and mammalian species, in contrast to CSF‐1 .…”

Section: Il‐34 Biologymentioning

confidence: 99%

Interleukin-34, a comprehensive review

Baghdadi

Umeyama

Hama

et al. 2018

Journal of Leukocyte Biology

106

120

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IL-34 is a novel cytokine that was identified in 2008 in a comprehensive proteomic analysis as a tissue-specific ligand of CSF-1 receptor (CSF-1R). IL-34 exists in all vertebrates including fish, amphibians, birds, and mammals, showing high conservation among species. Structurally, IL-34 belongs to the short-chain helical hematopoietic cytokine family but shows no apparent consensus structural domains, motifs, or sequence homology with other cytokines. IL-34 is synthesized as a secreted homodimeric glycoprotein that binds to the extracellular domains of CSF-1R and receptor-type protein-tyrosine phosphatase-zeta (PTP-ζ) in addition to the chondroitin sulfate chains of syndecan-1. These interactions result in activating several signaling pathways that regulate major cellular functions, including proliferation, differentiation, survival, metabolism, and cytokine/chemokine expression in addition to cellular adhesion and migration. In the steady state, IL-34 contributes to the development and maintenance of specific myeloid cell subsets in a tissue-specific manner: Langerhans cells in the skin and microglia in the brain. In pathological conditions, changes in IL-34 expression-increased or decreased-are involved in disease pathogenesis and correlate with progression, severity, and chronicity. One decade after its discovery, IL-34 has been introduced as a newcomer to the big family of interleukins with specific physiological functions, critical pathological roles, and promising clinical applications in disease diagnosis and treatment. In this review, we celebrate the 10th anniversary of IL-34 discovery, introducing its biological characteristics, and discussing the importance of IL-34 signaling network in health and disease.

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“…Intriguingly, the X. laevis IL-34-derived macrophages possess elevated arginase-1 gene expression and yet also exhibit potent respiratory burst responses, typical of mammalian M1 macrophages. It is notable that IL-34 is found across all vertebrates (Garceau et al, 2010; Gow et al, 2012; Gow et al, 2013; Wang et al, 2013). In fact, this cytokine may even predate CSF-1, considering the presence of IL-34 and absence of CSF-1 in the elasmobranch genome (Venkatesh et al, 2014).…”

Section: Monopoiesis In Anuramentioning

confidence: 99%

Amphibian macrophage development and antiviral defenses

Grayfer

Robert

2016

Developmental & Comparative Immunology

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Macrophage lineage cells represent the cornerstone of vertebrate physiology and immune defenses. In turn, comparative studies using non-mammalian animal models have revealed that evolutionarily distinct species have adopted diverse molecular and physiological strategies for controlling macrophage development and functions. Notably, amphibian species present a rich array of physiological and environmental adaptations, not to mention the peculiarity of metamorphosis from larval to adult stages of development, involving drastic transformation and differentiation of multiple new tissues. Thus it is not surprising that different amphibian species and their respective tadpole and adult stages have adopted unique hematopoietic strategies. Accordingly and in order to establish a more comprehensive view of these processes, here we review the hematopoietic and monopoietic strategies observed across amphibians, describe the present understanding of the molecular mechanisms driving amphibian, an in particular Xenopus laevis macrophage development and functional polarization, and discuss the roles of macrophage-lineage cells during ranavirus infections.

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Cloning and expression of feline colony stimulating factor receptor (CSF-1R) and analysis of the species specificity of stimulation by colony stimulating factor-1 (CSF-1) and interleukin-34 (IL-34)

Cited by 17 publications

References 66 publications

Divergent antiviral roles of amphibian (Xenopus laevis) macrophages elicited by colony-stimulating factor-1 and interleukin-34

Divergent antiviral roles of amphibian (Xenopus laevis) macrophages elicited by colony-stimulating factor-1 and interleukin-34

Interleukin-34, a comprehensive review

Amphibian macrophage development and antiviral defenses

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