Heterogeneity of macrophage activation in fish

Forlenza, Maria; Fink, I.R.; Raes, Geert; Wiegertjes, G.F.

doi:10.1016/j.dci.2011.03.008

Cited by 89 publications

(69 citation statements)

References 116 publications

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“…A question that is very relevant both for infectious diseases and for cancer biology concerns the presence of different pro- and anti-inflammatory macrophage subtypes in zebrafish. Classically activated (M1) and alternatively activated (M2) macrophages, resembling the phenotypes of mammalian macrophages, have been identified in different fish species (Forlenza et al, 2011). That different macrophage subtypes might already be present in early zebrafish larvae has been suggested, but this remains to be further investigated (Feng et al, 2010).…”

Section: Discussionmentioning

confidence: 99%

Macrophage-pathogen interactions in infectious diseases: new therapeutic insights from the zebrafish host model

Torraca

Masud

Spaink

et al. 2014

Disease Models &Amp; Mechanisms

138

112

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Studying macrophage biology in the context of a whole living organism provides unique possibilities to understand the contribution of this extremely dynamic cell subset in the reaction to infections, and has revealed the relevance of cellular and molecular processes that are fundamental to the cell-mediated innate immune response. In particular, various recently established zebrafish infectious disease models are contributing substantially to our understanding of the mechanisms by which different pathogens interact with macrophages and evade host innate immunity. Transgenic zebrafish lines with fluorescently labeled macrophages and other leukocyte populations enable non-invasive imaging at the optically transparent early life stages. Furthermore, there is a continuously expanding availability of vital reporters for subcellular compartments and for probing activation of immune defense mechanisms. These are powerful tools to visualize the activity of phagocytic cells in real time and shed light on the intriguing paradoxical roles of these cells in both limiting infection and supporting the dissemination of intracellular pathogens. This Review will discuss how several bacterial and fungal infection models in zebrafish embryos have led to new insights into the dynamic molecular and cellular mechanisms at play when pathogens encounter host macrophages. We also describe how these insights are inspiring novel therapeutic strategies for infectious disease treatment.

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Section: Discussionmentioning

confidence: 99%

Macrophage-pathogen interactions in infectious diseases: new therapeutic insights from the zebrafish host model

Torraca

Masud

Spaink

et al. 2014

Disease Models &Amp; Mechanisms

138

112

View full text Add to dashboard Cite

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“…It remains unknown, to what degree invertebrate analogs of IFNγ would be able to enhance LPS-induced NO production, as no experimental data about enhancement of NO production by IFNγ-like cytokine in Drosophila are available. Presumably, the ability of M1 macrophages to produce large amounts of NO in response to microbial infection is a vertebrate evolutionary invention, known to be present already at the fish grade (132). At this stage the arginase function in M2 macrophages, inherited after invertebrate ancestors, was to deliver ornithine for processes of extracellular matrix synthesis, of importance in organogenesis and wound healing.…”

Section: Discussionmentioning

confidence: 99%

Evolutionary Roots of Arginase Expression and Regulation

Dzik

2014

Front. Immunol.

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Two main types of macrophage functions are known: classical (M1), producing nitric oxide, NO, and M2, in which arginase activity is primarily expressed. Ornithine, the product of arginase, is a substrate for synthesis of polyamines and collagen, important for growth and ontogeny of animals. M2 macrophages, expressing high level of mitochondrial arginase, have been implicated in promoting cell division and deposition of collagen during ontogeny and wound repair. Arginase expression is the default mode of tissue macrophages, but can also be amplified by signals, such as IL-4/13 or transforming growth factor-β (TGF-β) that accelerates wound healing and tissue repair. In worms, the induction of collagen gene is coupled with induction of immune response genes, both depending on the same TGF-β-like pathway. This suggests that the main function of M2 “heal” type macrophages is originally connected with the TGF-β superfamily of proteins, which are involved in regulation of tissue and organ differentiation in embryogenesis. Excretory–secretory products of metazoan parasites are able to induce M2-type of macrophage responses promoting wound healing without participation of Th2 cytokines IL-4/IL-13. The expression of arginase in lower animals can be induced by the presence of parasite antigens and TGF-β signals leading to collagen synthesis. This also means that the main proteins, which, in primitive metazoans, are involved in regulation of tissue and organ differentiation in embryogenesis are produced by innate immunity. The signaling function of NO is known already from the sponge stage of animal evolution. The cytotoxic role of NO molecule appeared later, as documented in immunity of marine mollusks and some insects. This implies that the M2-wound healing promoting function predates the defensive role of NO, a characteristic of M1 macrophages. Understanding when and how the M1 and M2 activities came to be in animals is useful for understanding how macrophage immunity, and immune responses operate.

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“…For instance, the common carp can yield sufficient numbers of blood cells for cell sorting of various subtypes of immune cells [8][9][10][11] and subsequent transcriptome analyses. [12][13][14][15] Since common carp and zebrafish both belong to the cyprinid family, we believe that the combined use of these animal models will yield results that are easily translated between these species and thereby will give the ''best of both worlds'' of a small genetically highly versatile model (zebrafish) and a fish model with a very large body size for which well-defined genetically highly inbred lines are available, as is the case with common carp. [16][17][18] This combination can also be highly successful for future screens at the embryo level since the small clutch size of zebrafish (up to a few hundred eggs per female) can be complemented with the very large clutch size of common carp (up to several hundreds of thousands of eggs per female).…”

Section: Introductionmentioning

confidence: 99%

Comparison of the Exomes of Common Carp (Cyprinus carpio) and Zebrafish (Danio rerio)

et al. 2012

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Research on common carp, Cyprinus carpio, is beneficial for zebrafish research because of resources available owing to its large body size, such as the availability of sufficient organ material for transcriptomics, proteomics, and metabolomics. Here we describe the shot gun sequencing of a clonal double-haploid common carp line. The assembly consists of 511891 scaffolds with an N50 of 17 kb, predicting a total genome size of 1.4-1.5 Gb. A detailed analysis of the ten largest scaffolds indicates that the carp genome has a considerably lower repeat coverage than zebrafish, whilst the average intron size is significantly smaller, making it comparable to the fugu genome. The quality of the scaffolding was confirmed by comparisons with RNA deep sequencing data sets and a manual analysis for synteny with the zebrafish, especially the Hox gene clusters. In the ten largest scaffolds analyzed, the synteny of genes is almost complete. Comparisons of predicted exons of common carp with those of the zebrafish revealed only few genes specific for either zebrafish or carp, most of these being of unknown function. This supports the hypothesis of an additional genome duplication event in the carp evolutionary history, which-due to a higher degree of compactness-did not result in a genome larger than that of zebrafish.

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Heterogeneity of macrophage activation in fish

Cited by 89 publications

References 116 publications

Macrophage-pathogen interactions in infectious diseases: new therapeutic insights from the zebrafish host model

Macrophage-pathogen interactions in infectious diseases: new therapeutic insights from the zebrafish host model

Evolutionary Roots of Arginase Expression and Regulation

Comparison of the Exomes of Common Carp (Cyprinus carpio) and Zebrafish (Danio rerio)

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