Harbour seal (Phoca vitulina) PMN and monocytes release extracellular traps to capture the apicomplexan parasite Toxoplasma gondii

Reichel, Maria; Muñoz-Caro, Tamara; Contreras, Guillermo Sanchez; García, Ana Rubio; Magdowski, Gerd; Gärtner, Ulrich; Taubert, Anja; Hermosilla, Carlos

doi:10.1016/j.dci.2015.02.002

Cited by 60 publications

(82 citation statements)

References 66 publications

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“…Quantitative assays also revealed that N. caninum tachyzoite-induced NETs formation was a time- and dose- dependent process. These results confirmed that N. caninum tachyzoites can clearly induce NETs in vitro , which is in accordance to NETs-related data for T. gondii, E. bovis , and L. donovani (17–19). However, we do not know the effects of NETs on N. caninum infection in bovine, and whether neutrophils would also be able to recognize and attack N. caninum by NETs formation in vivo need to be further investigated.…”

Section: Discussionsupporting

confidence: 89%

“…Furthermore, inhibitors of NE and MPO significantly inhibited N. caninum tachyzoite-induced NETs formation, which suggest the critical role of NE and MPO in N. caninum tachyzoite-induced NETs. These proteins were also previously observed as key molecules in T. gondii-, Besnoitia besnoiti -, and E. bovis -triggered ETs (17, 23, 24). Previous studies showed that NETs formation was a NADPH oxidase-dependent process, which resulted in the production of ROS (25).…”

Section: Discussionsupporting

confidence: 59%

“…It has been demonstrated that several stimuli, including bacteria, fungi, viruses, and crystal salts can induce the activation of this novel mechanism-NETs in activated PMN (14–16). While most researches concentrated on the effects of NETs on bacteria, fungi, and viral pathogens, increasing evidence on NETs formation triggered by parasites was reported recently, such as T. gondii, Eimeria bovis , and Leishmania donovani (17–19). However, the effects of N. caninum on NETs formation have not been investigated.…”

Section: Discussionmentioning

confidence: 99%

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Canine Neutrophil Extracellular Traps Release Induced by the Apicomplexan Parasite Neospora caninum In Vitro

et al. 2016

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Neosporosis is considered as one of the main causes of abortion and severe economic losses in dairy industry. The Canis genus serving as one of the confirmed definitive hosts of the apicomplexan parasite Neospora caninum (N. caninum) plays a critical role in its life cycle. However, the effects of N. caninum on its definitive hosts of neutrophils extracellular traps (NETs) formation remain unclear. In the present study, N. caninum tachyzoite-induced canine NETs formation was observed by scanning electron microscopy (SEM). Visualization of DNA decorated with H3, neutrophil elastase (NE), and myeloperoxidase (MPO) within N. caninum tachyzoite-induced NETs were examined using fluorescence confocal microscopy analyses. Furthermore, the formation of canine NETs was quantified using Sytox Green staining, and the LDH levels in supernatants were examined by an LDH Cytotoxicity Assay® kit. The results clearly showed that NETs-like structures were induced by N. caninum tachyzoites, and the major components within these structures induced by N. caninum tachyzoite were further confirmed by fluorescence confocal microscopy visualization. These results suggest that N. caninum tachyzoites strongly induced NETs formation in canine polymorphonuclear neutrophils (PMN). In functional inhibition assays, the blockings of NADPH oxidase, NE, MPO, SOCE, ERK 1/2, and p38 MAPK signaling pathways significantly inhibited N. caninum tachyzoite-induced NETs formation. To our knowledge, this study is the first to report the formation of NETs in canine PMN against N. caninum infection.

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Section: Discussionsupporting

confidence: 89%

Section: Discussionsupporting

confidence: 59%

Section: Discussionmentioning

confidence: 99%

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Canine Neutrophil Extracellular Traps Release Induced by the Apicomplexan Parasite Neospora caninum In Vitro

et al. 2016

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“…Several protozoan parasites have been identified as potent NET inducers as well (11, 12, 29, 30, 32–35). To the best of our knowledge, we here describe, for the first time, the release of bovine NETs in response to the apicomplexan parasite N. caninum , which is known as an important abortive agent affecting not only beef and dairy cattle but also small ruminants worldwide (52–57).…”

Section: Discussionmentioning

confidence: 99%

“…By now, NETosis has been described to be triggered by different protozoan parasites in vitro and in vivo , such as Plasmodium falciparum (29), Leishmania spp. (30, 31), Eimeria bovis (12, 32), Eimeria arloingi (33), T. gondii (34, 35), Besnoitia besnoiti (11), Cryptosporidium parvum (13), Trypanosoma cruzii (36), and Entamoeba histolytica (37). In addition, monocyte-derived extracellular traps have recently been reported in response to tachyzoites of B. besnoiti (11) and T. gondii in vitro (35).…”

Section: Introductionmentioning

confidence: 99%

Bovine Polymorphonuclear Neutrophils Cast Neutrophil Extracellular Traps against the Abortive Parasite Neospora caninum

et al. 2017

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Neospora caninum represents a relevant apicomplexan parasite causing severe reproductive disorders in cattle worldwide. Neutrophil extracellular trap (NET) generation was recently described as an efficient defense mechanism of polymorphonuclear neutrophils (PMN) acting against different parasites. In vitro interactions of bovine PMN with N. caninum were analyzed at different ratios and time spans. Extracellular DNA staining was used to illustrate the typical molecules of NETs [i.e., histones (H3), neutrophil elastase (NE), myeloperoxidase (MPO), pentraxin] via antibody-based immunofluorescence analyses. Functional inhibitor treatments were applied to reveal the role of several enzymes [NADPH oxidase (NOX), NE, MPO, PAD4], ATP-dependent P2Y2 receptor, store-operated Ca++entry (SOCE), CD11b receptor, ERK1/2- and p38 MAPK-mediated signaling pathway in tachyzoite-triggered NETosis. N. caninum tachyzoites triggered NETosis in a time- and dose-dependent manner. Scanning electron microscopy analyses revealed NET structures being released by bovine PMN and entrapping tachyzoites. N. caninum-induced NET formation was found not to be NOX-, NE-, MPO-, PAD4-, ERK1/2-, and p38 MAP kinase-dependent process since inhibition of these enzymes led to a slight decrease of NET formation. CD11b was also identified as a neutrophil receptor being involved in NETosis. Furthermore, N. caninum-triggered NETosis depends on Ca++ influx as well as neutrophil metabolism since both the inhibition of SOCE and of P2Y2-mediated ATP uptake diminished NET formation. Host cell invasion assays indicated that PMN-derived NETosis hampered tachyzoites from active host cell invasion, thereby inhibiting further intracellular replication. NET formation represents an early and effective mechanism of response of the innate immune system, which might reduce initial infection rates during the acute phase of cattle neosporosis.

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Endoparasite survey of free-swimming baleen whales (Balaenoptera musculus, B. physalus, B. borealis) and sperm whales (Physeter macrocephalus) using non/minimally invasive methods

et al. 2015

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A number of parasitic diseases have gained importance as neozoan opportunistic infections in the marine environment. Here, we report on the gastrointestinal endoparasite fauna of three baleen whale species and one toothed whale: blue (Balaenoptera musculus), fin (Balaenoptera physalus), and sei whales (Balaenoptera borealis) and sperm whales (Physeter macrocephalus) from the Azores Islands, Portugal. In total, 17 individual whale fecal samples [n = 10 (B. physalus); n = 4 (P. macrocephalus); n = 2 (B. musculus); n = 1 (B. borealis)] were collected from free-swimming animals as part of ongoing studies on behavioral ecology. Furthermore, skin biopsies were collected from sperm whales (n = 5) using minimally invasive biopsy darting and tested for the presence of Toxoplasma gondii, Neospora caninum, and Besnoitia besnoiti DNA via PCR. Overall, more than ten taxa were detected in whale fecal samples. Within protozoan parasites, Entamoeba spp. occurred most frequently (64.7%), followed by Giardia spp. (17.6%) and Balantidium spp. (5.9%). The most prevalent metazoan parasites were Ascaridida indet. spp. (41.2%), followed by trematodes (17.7%), acanthocephalan spp., strongyles (11.8%), Diphyllobotrium spp. (5.9%), and spirurids (5.9%). Helminths were mainly found in sperm whales, while enteric protozoan parasites were exclusively detected in baleen whales, which might be related to dietary differences. No T. gondii, N. caninum, or B. besnoiti DNA was detected in any skin sample. This is the first record on Giardia and Balantidium infections in large baleen whales.

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Harbour seal (Phoca vitulina) PMN and monocytes release extracellular traps to capture the apicomplexan parasite Toxoplasma gondii

Cited by 60 publications

References 66 publications

Canine Neutrophil Extracellular Traps Release Induced by the Apicomplexan Parasite Neospora caninum In Vitro

Canine Neutrophil Extracellular Traps Release Induced by the Apicomplexan Parasite Neospora caninum In Vitro

Bovine Polymorphonuclear Neutrophils Cast Neutrophil Extracellular Traps against the Abortive Parasite Neospora caninum

Endoparasite survey of free-swimming baleen whales (Balaenoptera musculus, B. physalus, B. borealis) and sperm whales (Physeter macrocephalus) using non/minimally invasive methods

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