Dolphin-derived NETosis results in rapid Toxoplasma gondii tachyzoite ensnarement and different phenotypes of NETs

Imlau, Michelle; Conejeros, Iván; Muñoz-Caro, Tamara; Zhou, Ershun; Gärtner, Ulrich; Ternes, Kerstin; Taubert, Anja; Hermosilla, Carlos

doi:10.1016/j.dci.2019.103527

Cited by 16 publications

(22 citation statements)

References 70 publications

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“…We show here that the NET produced by cat neutrophils after 180 min of interaction with RH tachyzoites are very similar to sprNET. Imlau and colleagues show that neutrophils isolated from dolphins produce all three types of NET, with a predominance of sprNET and aggNET [32]. Here, we did not find large clusters of NET aggregating neutrophils, but eventually small clusters could be seen (Supplementary Figure S5), corroborating previous findings and suggesting a conserved mechanism of NET release in response to T. gondii.…”

Section: Discussionsupporting

confidence: 91%

“…Release of NET can be triggered by an uncountable number of biological stimuli, including bacteria, fungus, viruses, helminths, and protozoans such as the pathogenic parasite T. gondii [24][25][26][27][28]. 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].…”

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: Discussionsupporting

confidence: 91%

Section: Introductionmentioning

confidence: 99%

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

et al. 2020

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“…In the case of Toxoplasma, NETs cause the immobilization of entrapped parasites, leading to their death (Abdallah et al, 2012;Yildiz et al, 2017). This mechanism is conserved in mice, humans, farm animals and marine mammals (Abdallah et al, 2012;Yildiz et al, 2017;Imlau et al, 2020). After the initial sensing, immune activation and clearance of parasites within macrophages and other antigen presenting cells (APCs), the CD8 T cell response is initiated when they encounter epitopes presented by major histocompatibility complex (MHC) I on APCs.…”

Section: Elimination Of Parasites Within the Hostmentioning

confidence: 99%

Section: The Immune Response During Toxoplasmosismentioning

confidence: 99%

Influence of the Host and Parasite Strain on the Immune Response During Toxoplasma Infection

Mukhopadhyay

Arranz-Solís

Saeij

2020

Front. Cell. Infect. Microbiol.

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Toxoplasma gondii is an exceptionally successful parasite that infects a very broad host range, including humans, across the globe. The outcome of infection differs remarkably between hosts, ranging from acute death to sterile infection. These differential disease patterns are strongly influenced by both host-and parasite-specific genetic factors. In this review, we discuss how the clinical outcome of toxoplasmosis varies between hosts and the role of different immune genes and parasite virulence factors, with a special emphasis on Toxoplasma-induced ileitis and encephalitis.

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“…Since NETs were first discovered to entrap and kill extracellular bacteria (Brinkmann et al, 2004 ), this novel effector mechanism has also been reported to be involved in immune system response against several pathogens, such as viruses (Wardini et al, 2010 ; Saitoh et al, 2012 ), fungi (Jin et al, 2016 ; Urban and Nett, 2018 ), or parasites (Munoz-Caro et al, 2015a ; Wei et al, 2016 ). It also has been shown that NETs against T. gondii infection exist in a variety of species including humans (Abi Abdallah et al, 2012 ), sheep (Yildiz et al, 2017 ), mice (Abi Abdallah et al, 2012 ), cattle (Yildiz et al, 2017 ), cats (Lacerda et al, 2019 ), harbor seals (Reichel et al, 2015 ), and dolphins (Imlau et al, 2020 ). NETs release can damage or kill T. gondii , but whether the NETs-based effector mechanism during T. gondii infection also works in the innate immune system of dogs remains unknown.…”

Section: Introductionmentioning

confidence: 99%

Toxoplasma gondii Triggers Neutrophil Extracellular Traps Release in Dogs

Wei

Wang

Liu

et al. 2020

Front. Cell. Infect. Microbiol.

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Toxoplasma gondii (T. gondii) can cause zoonotic toxoplasmosis worldwide. Neutrophil extracellular traps (NETs) have been known as a novel effector mechanism against T. gondii infection in the innate system of humans, cats, and sheep. Dogs are the intermediate host of T. gondii, in which the use of NETs against T. gondii infection remains unclear. Thus, this study aims to examine the effects of T. gondii on NETs release in dogs, and to further investigate the mechanism involved in the process. T. gondii-triggered NETs were analyzed by scanning electron microscopy (SEM) and fluorescence confocal microscopy, and the mechanism of T. gondii-triggered NETs release was determined by using inhibitors and a fluorometric reader. The results showed that T. gondii tachyzoites significantly triggered NETs-like structures, which consisted of DNA decorated with neutrophil elastase (NE) and myeloperoxidase (MPO). Further investigations revealed that reactive oxygen species (ROS)-, NADPH oxidase-, Rac 1or p38 mitogen-activated protein kinase (MAPK)-signaling pathways were relevant to T. gondii tachyzoites-triggered NETs release. Moreover, zymosan-triggered NETs release was strikingly degraded by T. gondii tachyzoites treatment, indicating that T. gondii may escape from the NETs-based capture strategy. Taken together, promoting NETs release is suggested to limit motility and evade infection of T. gondii in dogs.

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Dolphin-derived NETosis results in rapid Toxoplasma gondii tachyzoite ensnarement and different phenotypes of NETs

Cited by 16 publications

References 70 publications

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

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

Influence of the Host and Parasite Strain on the Immune Response During Toxoplasma Infection

Toxoplasma gondii Triggers Neutrophil Extracellular Traps Release in Dogs

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