Molecular analyses on Neospora caninum -triggered NETosis in the caprine system

Villagra-Blanco, Rodolfo; Silva, Liliana; Gärtner, Ulrich; Wagner, Henrik; Failing, Klaus; Wehrend, Axel; Taubert, Anja; Hermosilla, Carlos

doi:10.1016/j.dci.2017.02.020

Cited by 26 publications

(35 citation statements)

References 93 publications

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“…Commonly in terrestrial susceptible hosts, such as cattle, goats, sheep, horses and dogs, infections of N. caninum underlie complex cellular as well as molecular immunological regulations (see Gazzinelli et al., 1998 ; Boysen et al., 2006 ; Taubert et al., 2006 , Taubert et al., 2010 ; Klevar et al., 2007 ; Wei et al., 2016 , Villagra-Blanco et al., 2017a , Villagra-Blanco et al., 2017b ). In bottlenose dolphins, the innate immune system comprehends also PMN and monocytes, which comprise between 22-72% and 0–11% of the circulating leukocytes, respectively ( Goldstein et al., 2006 , Hall et al., 2007 , Venn-Watson et al., 2007 , Schwacke et al., 2009 ).…”

Section: Introductionmentioning

confidence: 99%

Bottlenose dolphins (Tursiops truncatus) do also cast neutrophil extracellular traps against the apicomplexan parasite Neospora caninum

Villagra-Blanco

Silva

Aguilella-Segura

et al. 2017

International Journal for Parasitology: Parasites and Wildlife

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Neutrophil extracellular traps (NETs) are web-like structures composed of nuclear DNA decorated with histones and cytoplasmic peptides which antiparasitic properties have not previously been investigated in cetaceans. Polymorphonuclear neutrophils (PMN) were isolated from healthy bottlenose dolphins (Tursiops truncatus), and stimulated with Neospora caninum tachyzoites and the NETs-agonist zymosan. In vitro interactions of PMN with the tachyzoites resulted in rapid extrusion of NETs. For the demonstration and quantification of cetacean NETs, extracellular DNA was stained by using either Sytox Orange® or Pico Green®. Scanning electron microscopy (SEM) and fluorescence analyses demonstrated PMN-derived release of NETs upon exposure to tachyzoites of N. caninum. Co-localization studies of N. caninum induced cetacean NETs proved the presence of DNA adorned with histones (H1, H2A/H2B, H3, H4), neutrophil elastase (NE), myeloperoxidase (MPO) and pentraxin (PTX) confirming the molecular properties of mammalian NETosis. Dolphin-derived N. caninum-NETosis were efficiently suppressed by DNase I and diphenyleneiodonium (DPI) treatments. Our results indicate that cetacean-derived NETs represent an ancient, conserved and relevant defense effector mechanism of the host innate immune system against N. caninum and probably other related neozoan parasites circulating in the marine environment.

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Section: Introductionmentioning

confidence: 99%

Bottlenose dolphins (Tursiops truncatus) do also cast neutrophil extracellular traps against the apicomplexan parasite Neospora caninum

Villagra-Blanco

Silva

Aguilella-Segura

et al. 2017

International Journal for Parasitology: Parasites and Wildlife

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“…The parasites were found entrapped within the NET structures, which were positive for H1, H2A/B, H3, H4, NE, pentraxin, and cathepsin B [127]. The phenotype was blocked by the MPO-inhibitor ABAH but was independent of NADPH-oxidases [127]. In addition, caprine monocytes respond to parasite interaction with the release of extracellular traps, as reported by Perez et al [63].…”

Section: Caprinaementioning

confidence: 58%

“…The release of ETs from dolphins has been demonstrated recently by Villagra-Blanco and colleagues [81]. The apicomplexan parasite N. caninum, studied in the context of bovine, canine, and caprine NETs [57,74,127], was used in a study involving neutrophils derived from bottlenose dolphins (Tursiops truncates) [81]. After co-incubation with the parasite for 30 to 60 min, cetacean neutrophils released a fine network of DNA.…”

Section: Extracellular Traps In Delphinidaementioning

confidence: 96%

“…Other animals belonging to the Bovidae family, such as goats and sheep, have also been reported to release extracellular traps in response to bacterial or parasitic pathogens [4,62,127]. The intracellular protozoan parasite, Neospora caninum, induced NET formation in goat neutrophils after 60 min of exposure [127]. The parasites were found entrapped within the NET structures, which were positive for H1, H2A/B, H3, H4, NE, pentraxin, and cathepsin B [127].…”

Section: Caprinaementioning

confidence: 99%

“…The intracellular protozoan parasite, Neospora caninum, induced NET formation in goat neutrophils after 60 min of exposure [127]. The parasites were found entrapped within the NET structures, which were positive for H1, H2A/B, H3, H4, NE, pentraxin, and cathepsin B [127]. The phenotype was blocked by the MPO-inhibitor ABAH but was independent of NADPH-oxidases [127].…”

Section: Caprinaementioning

confidence: 99%

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Extracellular Traps: An Ancient Weapon of Multiple Kingdoms

Neumann

Brogden²,

Köckritz-Blickwede

2020

Biology

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The discovery, in 2004, of extracellular traps released by neutrophils has extended our understanding of the mode of action of various innate immune cells. This fascinating discovery demonstrated the extracellular trapping and killing of various pathogens by neutrophils. During the last decade, evidence has accumulated showing that extracellular traps play a crucial role in the defence mechanisms of various cell types present in vertebrates, invertebrates, and plants. The aim of this review is to summarise the relevant literature on the evolutionary history of extracellular traps used as a weapon in various kingdoms of life. Biology 2020, 9, 34 2 of 23On the basis of findings from several studies mostly performed with human and murine neutrophils, the following three different pathways that lead to the formation of ETs by innate immune cells have been identified: (1) Release of nuclear DNA by ETosis, a suicidal cell death associated with the rupture of the nuclear membrane prior to cell lysis [14,15]; (2) vesicular release of nuclear DNA by viable cells [16,17]; and (3) release of mitochondrial DNA [18,19]. However, the exact molecular mechanisms leading to one or the other phenotype of ET formation has still not been entirely clarified. A group of renowned scientists and experts on NETs has recently published an opinionated review on the subject due to the abundance of available data that has also led to some confusion in the NET/ET research community because of contradictory results and divergent scientific concepts, for example, the molecular pathways of ET formation or the origin of the DNA that forms the ET scaffold [20]. There is a strong consensus about the composition of ETs among the findings that NETs contain a high amount of granule proteins, for example, cell-type-specific proteases and other antibacterial molecules that are associated with DNA-histone complexes. However, it is still unclear how different triggers or pathways have led to phenotypical differences about the source of DNA or viability of the ET-releasing cell.Comparison of ET phenotypical differences between host species in relation to evolutionary aspects, especially by comparing data from phylogenetic groups, would help to understand the pathways of ET formation in more detail.

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