Role of NETs in the difference in host susceptibility to Toxoplasma gondii between sheep and cattle

Yıldız, Kader; Gökpınar, Sami; Gazyağci, Aycan Nuriye; Babür, Cahit; Sürsal, Neslihan; Azkur, Ahmet Kürşat

doi:10.1016/j.vetimm.2017.05.005

Cited by 42 publications

(50 citation statements)

References 43 publications

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“…Interestingly, a similar EV-mediated export of deiminated histones, as observed in cow serum-EVs in the current study, was recently identified in the naked mole-rat, an animal with unusual immunological and metabolic traits [98], as well as in alligator, also an animal with unusual antimicrobial, including anti-viral responses [93]. Deiminated histone H3 is commonly used as an indicator for neutrophil extracellular trap formation (NETosis) [31,244], which has been related to PAD4 and implicated in anti-viral responses in cattle respiratory syncytial virus disease [42], in response to parasitic infections in cattle [245][246][247] as well as in response to certain antibiotics [248]. Interestingly, in crocodilians, extracellular histones H2A and H4 have been identified to act as inhibitors of viral (HIV) infection in vitro [249], although roles for post-translational deimination were not assessed.…”

Section: Discussionmentioning

confidence: 99%

Post-Translational Protein Deimination Signatures in Serum and Serum-Extracellular Vesicles of Bos taurus Reveal Immune, Anti-Pathogenic, Anti-Viral, Metabolic and Cancer-Related Pathways for Deimination

Criscitiello

Kraev

Lange

2020

IJMS

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The bovine immune system is known for its unusual traits relating to immunoglobulin and antiviral responses. Peptidylarginine deiminases (PADs) are phylogenetically conserved enzymes that cause post-translational deimination, contributing to protein moonlighting in health and disease. PADs also regulate extracellular vesicle (EV) release, forming a critical part of cellular communication. As PAD-mediated mechanisms in bovine immunology and physiology remain to be investigated, this study profiled deimination signatures in serum and serum-EVs in Bos taurus. Bos EVs were poly-dispersed in a 70-500 nm size range and showed differences in deiminated protein cargo, compared with whole sera. Key immune, metabolic and gene regulatory proteins were identified to be post-translationally deiminated with some overlapping hits in sera and EVs (e.g., immunoglobulins), while some were unique to either serum or serum-EVs (e.g., histones). Protein-protein interaction network analysis of deiminated proteins revealed KEGG pathways common for serum and serum-EVs, including complement and coagulation cascades, viral infection (enveloped viruses), viral myocarditis, bacterial and parasitic infections, autoimmune disease, immunodeficiency intestinal IgA production, B-cell receptor signalling, natural killer cell mediated cytotoxicity, platelet activation and hematopoiesis, alongside metabolic pathways including ferroptosis, vitamin digestion and absorption, cholesterol metabolism and mineral absorption. KEGG pathways specific to EVs related to HIF-1 signalling, oestrogen signalling and biosynthesis of amino acids. KEGG pathways specific for serum only, related to Epstein-Barr virus infection, transcription mis-regulation in cancer, bladder cancer, Rap1 signalling pathway, calcium signalling pathway and ECM-receptor interaction. This indicates differences in physiological and pathological pathways for deiminated proteins in serum-EVs, compared with serum. Our findings may shed light on pathways underlying a number of pathological and anti-pathogenic (viral, bacterial, parasitic) pathways, with putative translatable value to human pathologies, zoonotic diseases and development of therapies for infections, including anti-viral therapies.

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Section: Discussionmentioning

confidence: 99%

Post-Translational Protein Deimination Signatures in Serum and Serum-Extracellular Vesicles of Bos taurus Reveal Immune, Anti-Pathogenic, Anti-Viral, Metabolic and Cancer-Related Pathways for Deimination

Criscitiello

Kraev

Lange

2020

IJMS

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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: 81%

“…The aggregated NETs also covered most of the larvae, hampering the parasites' motility [59]. Although N. caninum and H. contortus viability was not affected by bovine neutrophils, another study showed T. gondii were killed by bovine NETs [60].…”

Section: Bovinaementioning

confidence: 99%

“…Histone citrullination could also be important in the formation of ETs in sheep; these NETs were found in mammary alveoli in response to S. uberis infection [4]. T. gondii, a parasite found to trigger NETs in human and murine neutrophils [28], was tested for its impact on ovine and bovine neutrophils [60]. The tachyzoites induced NETs in ovine neutrophils after 30 min of co-incubation in a time-dependent manner.…”

Section: Caprinaementioning

confidence: 99%

“…The tachyzoites induced NETs in ovine neutrophils after 30 min of co-incubation in a time-dependent manner. Additionally, the parasites were found entrapped within the meshwork [60].…”

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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Toxoplasma gondii-induced neutrophil extracellular traps are relevant to glycolysis, TLR2, and TLR4 MAPK signaling pathway in goats

Jin,

Chen

et al. 2023

Parasitol Res

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Role of NETs in the difference in host susceptibility to Toxoplasma gondii between sheep and cattle

Cited by 42 publications

References 43 publications

Post-Translational Protein Deimination Signatures in Serum and Serum-Extracellular Vesicles of Bos taurus Reveal Immune, Anti-Pathogenic, Anti-Viral, Metabolic and Cancer-Related Pathways for Deimination

Post-Translational Protein Deimination Signatures in Serum and Serum-Extracellular Vesicles of Bos taurus Reveal Immune, Anti-Pathogenic, Anti-Viral, Metabolic and Cancer-Related Pathways for Deimination

Extracellular Traps: An Ancient Weapon of Multiple Kingdoms

Toxoplasma gondii-induced neutrophil extracellular traps are relevant to glycolysis, TLR2, and TLR4 MAPK signaling pathway in goats

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