Toxoplasma gondii induces extracellular traps release in cat neutrophils

Lacerda, Luciana Carvalho; Santos, Jane Lima dos; Wardini, Amanda Brito; Silva, Aísla Nascimento da; Santos, Andrea; Freire, Herbert Pina Silva; Anjos, Danielle Oliveira dos; Romano, Carla Cristina; Mendes, Érica Araújo; Munhoz, Alexandre Dias

doi:10.1016/j.exppara.2019.107770

Cited by 9 publications

(13 citation statements)

References 42 publications

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“…Neutrophils from dog [35], sheep and cattle [31], donkey [34], harbour seal [30], and dolphin [33] all release NET induced by this parasite. Moreover, Lacerda and colleagues recently showed that neutrophils from cats also produce NET in response to T. gondii [36], although without exploring its mechanism or NET toxicity to the parasite. Here we show that cat neutrophils produce classical NET in response to tachyzoites of the virulent strain RH, corroborating previous findings [36].…”

Section: Discussionmentioning

confidence: 99%

“…Moreover, Lacerda and colleagues recently showed that neutrophils from cats also produce NET in response to T. gondii [36], although without exploring its mechanism or NET toxicity to the parasite. Here we show that cat neutrophils produce classical NET in response to tachyzoites of the virulent strain RH, corroborating previous findings [36]. Furthermore, we show that the cystogenic strain ME49 also induces NET release, and that production of NET by cat neutrophils in response to both virulent or cystogenic strains occurs either in a classical way, after a few hours, or in a rapid way, within the first 15 min of interaction with parasites.…”

Section: Discussionmentioning

confidence: 99%

“…Neutrophils from different organisms release NET upon interaction with T. gondii, including those of mice, humans, dogs, cattle, sheep, donkey, harbor seals, and dolphins [29][30][31][32][33][34][35], all of which are intermediate hosts for the parasite. Recently, extracellular traps were also shown to be produced by cat neutrophils [36]. However, the mechanisms behind NET formation in response to T. gondii are not completely understood.…”

Section: Introductionmentioning

confidence: 99%

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Extracellular Traps Released by Neutrophils from Cats are Detrimental to Toxoplasma gondii Infectivity

et al. 2020

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Toxoplasma gondii is the causative agent of toxoplasmosis, an infectious disease that affects over 30% of the human world population, causing fatal infections in immunocompromised individuals and neonates. The life cycle of T. gondii is complex, and involves intermediate hosts (birds and mammals) and definitive hosts (felines, including domestic cats). The innate immune repertoire against the parasite involves the production of neutrophil extracellular traps (NET), and neutrophils from several intermediate hosts produce NET induced by T. gondii. However, the mechanisms underlying NET release in response to the parasite have been poorly explored. Therefore, the aims of this study were to investigate whether neutrophils from cats produce NET triggered by T. gondii and to understand the mechanisms thereby involved. Neutrophils from cats were stimulated with T. gondii tachyzoites and NET-derived DNA in the supernatant was quantified during the time. The presence of histone H1 and myeloperoxidase was detected by immunofluorescence. We observed that cat neutrophils produce both classical and rapid/early NET stimulated by T. gondii. Inhibition of elastase, intracellular calcium, and phosphatidylinositol 3-kinase (PI3K)-δ partially blocked classical NET release in response to the parasite. Electron microscopy revealed strands and networks of DNA in close contact or completely entrapping parasites. Live imaging showed that tachyzoites are killed by NET. We conclude that the production of NET is a conserved strategy to control infection by T. gondii amongst intermediate and definitive hosts.

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Section: Discussionmentioning

confidence: 99%

Section: Discussionmentioning

confidence: 99%

Section: Introductionmentioning

confidence: 99%

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Extracellular Traps Released by Neutrophils from Cats are Detrimental to Toxoplasma gondii Infectivity

et al. 2020

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“…The co-incubation of live T. gondii tachyzoites with harbour seal PMNs resulted in net-like structures with the parasites attached to them [80]. In line with parasite-induced NET formation in other mammalian species [28,60,71] enzymatic activity of NADPH oxidase, NE, and MPO were reported and inhibition of those enzymes resulted in a significant reduction in NETosis [80]. The entrapment of the parasites by seal NETs prevented host cell invasion, thus, displaying a beneficial impact of NETs for the host organism [80].…”

Section: Extracellular Traps In Carnivores Such As Felidae Canidae mentioning

confidence: 69%

“…It was suggested that an infection with feline leukaemia virus (FeLV) leads to exacerbated neutrophil activation, and thus made these cells less susceptible to other stimuli [73]. Similar to other mammalian neutrophils, cat neutrophils also responded to tachyzoites of T. gondii in a ROS-dependent fashion by releasing NETs [71]. Recently, NETs were also found in the endometrium of queens and bitches, suffering from E. coli-mediated pyometra [72].…”

Section: Extracellular Traps In Carnivores Such As Felidae Canidae mentioning

confidence: 99%

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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