Staphylococcus aureus Extracellular Vesicles Elicit an Immunostimulatory Response in vivo on the Murine Mammary Gland

Tartaglia, Natayme Rocha; Breyne, Koen; Meyer, Evelyne; Cauty, Chantal; Jardin, Julien; Chrétien, Denis; Dupont, Aurélien; Demeyere, Kristel; Berkova, Nadejda; Azevedo, Vasco; Guédon, Éric; Loir, Yves Le

doi:10.3389/fcimb.2018.00277

Cited by 61 publications

(76 citation statements)

References 122 publications

(148 reference statements)

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“…F95-enrichment for deiminated proteins from serum and serum-EVs revealed a range of immunological, metabolic and gene regulatory proteins as candidates for this post-translational modification, therefore indicating hitherto under-recognized modes for protein-moonlighting of these proteins in bovine immunity and physiology. Few studies have hitherto assessed roles for PADs and deimination in cattle [22,23,42], while a range of studies have been carried out on EVs in relation to cattle immunity, fertility and development [54,57,60,61,63,65,68,74,78,83,85,88,90]. Export of post-translationally modified proteins, such as deiminated proteins in the current study, has not been assessed before in cattle serum.…”

Section: Discussionmentioning

confidence: 93%

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: 93%

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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“…These can originate from all the cells present in the mammary gland (Lasser et al., ), including epithelial and immune cells. Milk EVs could also be secreted by the bacteria colonizing the mammary gland or found in milk (Andreas et al., ; Le Doare et al., ; Tartaglia et al., ), which can also secrete small RNA sequences (Choi, Kim, Hong, & Lee, ; Choi, Kwon, Hong, & Lee, ) in outer membrane vesicles (Kulp & Kuehn, ) and transfer their nucleic acid content to human cells (Bitto et al., ). Therefore, it is most likely that milk is a complex carrier of a multitude of small EVs with different proteins, RNA, mRNA, and microRNA cargo originating from a multitude of cell types.…”

Section: Cellular Origin Of Milk Micrornasmentioning

confidence: 99%

Milk MicroRNAs in Health and Disease

Benmoussa

Provost

2019

Comp Rev Food Sci Food Safe

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MicroRNAs are small noncoding RNAs responsible for regulating 40% to 60% of gene expression at the posttranscriptional level. The discovery of circulating microRNAs in several biological fluids opened the path for their study as biomarkers and long‐range cell‐to‐cell communication mediators. Their transfer between individuals in the case of blood transfusion, for example, and their high enrichment in milk have sparked the interest for microRNA transfer through diet, especially from mothers to infants during breastfeeding. The extension of such paradigm led to the study of milk microRNAs in the case of cow or goat milk consumption in adults. Here we provide a comprehensive critical review of the key findings surrounding milk microRNAs in human, cow, and goat milk among other species. We discuss the data on their biological properties, their use as disease biomarkers, their transfer between individuals or species, and their putative or verified functions in health and disease of infants and adult consumers. This work is based on all the literature available and integrates all the results, theories, debates, and validation studies available so far on milk microRNAs and related areas of investigations. We critically discuss the limitations and outline future aspects and avenues to explore in this rapidly growing field of research that could impact public health through infant milk formulations or new therapies. We hope that this comprehensive review of the literature will provide insight for all teams investigating milk RNAs’ biological activities and help ensure the quality of future reports.

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“…The broad spectrum of activities associated with S. aureus-derived EVs, as well as their strain-dependency, is mainly related to their protein content 12 . The EV cargo includes a variety of proteins, such as virulence factors and lipoproteins, some of which are known to be potent antigens 12,17,18,[21][22][23][24] . The EV protein cargo has been shown to vary as a function of environmental conditions 21 and the producer strains 12,17 .…”

mentioning

confidence: 99%

Extracellular vesicles produced by human and animal Staphylococcus aureus strains share a highly conserved core proteome

Tartaglia

Nicolas

Rodovalho

et al. 2020

Sci Rep

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Staphylococcus aureus is an important opportunistic pathogen of humans and animals. it produces extracellular vesicles (EVs) that are involved in cellular communication and enable inter-kingdom crosstalk, the delivery of virulence factors and modulation of the host immune response. The protein content of EVs determines their biological functions. Clarifying which proteins are selected, and how, is of crucial value to understanding the role of EVs in pathogenesis and the development of molecular delivery systems. Here, we postulated that S. aureus EVs share a common proteome containing components involved in cargo sorting. The EV proteomes of five S. aureus strains originating from human, bovine, and ovine hosts were characterised. The clustering of EV proteomes reflected the diversity of the producing strains. A total of 253 proteins were identified, 119 of which composed a core EV proteome with functions in bacterial survival, pathogenesis, and putatively in EV biology. We also identified features in the sequences of EV proteins and the corresponding genes that could account for their packaging into EVs. Our findings corroborate the hypothesis of a selective sorting of proteins into EVs and offer new perspectives concerning the roles of EVs in S. aureus pathogenesis in specific host niches. Staphylococcus aureus is a Gram-positive opportunistic pathogen that causes a broad spectrum of infections in humans and animals. In humans, these diseases range from superficial skin and soft tissue infections to life-threatening conditions that require hospitalisation and extensive medical support 1,2. This bacterium is also one of the main causative agents of nosocomial infections. In animals, S. aureus is notably responsible for ruminant mastitis, an inflammation of the mammary glands that dramatically affects animal health and welfare, milk quality and the economics of milk production 3. Mastitis is also the principal reason for the use of antibiotics in dairy herds 4. The wide range of clinical manifestations of S. aureus infections is likely associated with its huge arsenal of virulence factors, which include structural components and extracellular factors such as enzymes and toxins 5. Despite considerable efforts, the precise mechanisms underlying host adaptation, colonisation and interactions are not yet fully understood 6. Extracellular vesicles (EVs) are used by many pathogenic bacteria as a secretory route to deliver toxic compounds to infected cells 7,8. EVs are lipid bilayer nanoparticles that range in size from 20 to 300 nm and are released by almost all cells in all domains of life 9. In Gram-positive bacteria, they are formed by budding and shedding of the cytoplasmic membrane. They play a pivotal role in cell-to-cell communication through their ability to transport bioactive molecules (proteins, nucleic acids, lipids, metabolites) from donor to recipient cells. The EVs produced by S. aureus can mediate the pathogenesis of infection in a variety of ways. They may be cytotoxic to host cells 10-12 , induce the ...

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Staphylococcus aureus Extracellular Vesicles Elicit an Immunostimulatory Response in vivo on the Murine Mammary Gland

Cited by 61 publications

References 122 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

Milk MicroRNAs in Health and Disease

Extracellular vesicles produced by human and animal Staphylococcus aureus strains share a highly conserved core proteome

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