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

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Abstract

Staphylococcus aureus is a major pathogen responsible for bovine mastitis, the most common and costly disease affecting dairy cattle. S. aureus naturally releases extracellular vesicles (EVs) during its growth. EVs play an important role in the bacteria-bacteria and bacteria-host interactions and are notably considered as nanocarriers that deliver virulence factors to the host tissues. Whether EVs play a role in a mastitis context is still unknown. In this work, we showed that S. aureus Newbould 305 (N305), a bovine mastitis isolate, has the ability to generate EVs in vitro with a designated protein content. Purified S. aureus N305-secreted EVs were not cytotoxic when tested in vitro on MAC-T and PS, two bovine mammary epithelial cell lines. However, they induced the gene expression of inflammatory cytokines at levels similar to those induced by live S. aureus N305. The in vivo immune response to purified S. aureus N305-secreted EVs was tested in a mouse model for bovine mastitis and their immunogenic effect was compared to that of live S. aureus N305, heat-killed S. aureus N305 and to S. aureus lipoteichoic acid (LTA). Clinical and histopathological signs were evaluated and pro-inflammatory and chemotactic cytokine levels were measured in the mammary gland 24 h post-inoculation. Live S. aureus induced a significantly stronger inflammatory response than that of any other condition tested. Nevertheless, S. aureus N305-secreted EVs induced a dose-dependent neutrophil recruitment and the production of a selected set of pro-inflammatory mediators as well as chemokines. This immune response elicited by intramammary S. aureus N305-secreted EVs was comparable to that of heat-killed S. aureus N305 and, partly, by LTA. These results demonstrated that S. aureus N305-secreted EVs induce a mild inflammatory response distinct from the live pathogen after intramammary injection. Overall, our combined in vitro and in vivo data suggest that EVs are worth to be investigated to better understand the S. aureus pathogenesis and are relevant tools to develop strategies against bovine S. aureus mastitis.

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Chemokines: a new classification system and their role in immunity.

A Zlotnik, O Yoshie (2000)

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Non-classical protein secretion in bacteria

Jannick Bendtsen, Lars Kiemer, Anders Fausbøll … (2005)

Background We present an overview of bacterial non-classical secretion and a prediction method for identification of proteins following signal peptide independent secretion pathways. We have compiled a list of proteins found extracellularly despite the absence of a signal peptide. Some of these proteins also have known roles in the cytoplasm, which means they could be so-called "moon-lightning" proteins having more than one function. Results A thorough literature search was conducted to compile a list of currently known bacterial non-classically secreted proteins. Pattern finding methods were applied to the sequences in order to identify putative signal sequences or motifs responsible for their secretion. We have found no signal or motif characteristic to any majority of the proteins in the compiled list of non-classically secreted proteins, and conclude that these proteins, indeed, seem to be secreted in a novel fashion. However, we also show that the apparently non-classically secreted proteins are still distinguished from cellular proteins by properties such as amino acid composition, secondary structure and disordered regions. Specifically, prediction of disorder reveals that bacterial secretory proteins are more structurally disordered than their cytoplasmic counterparts. Finally, artificial neural networks were used to construct protein feature based methods for identification of non-classically secreted proteins in both Gram-positive and Gram-negative bacteria. Conclusion We present a publicly available prediction method capable of discriminating between this group of proteins and other proteins, thus allowing for the identification of novel non-classically secreted proteins. We suggest candidates for non-classically secreted proteins in Escherichia coli and Bacillus subtilis. The prediction method is available online.

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Gram-positive bacteria produce membrane vesicles: proteomics-based characterization of Staphylococcus aureus-derived membrane vesicles.

Eun-Young Lee, Do-Young Choi, Dae-Kyum Kim … (2009)

Although archaea, Gram-negative bacteria, and mammalian cells constitutively secrete membrane vesicles (MVs) as a mechanism for cell-free intercellular communication, this cellular process has been overlooked in Gram-positive bacteria. Here, we found for the first time that Gram-positive bacteria naturally produce MVs into the extracellular milieu. Further characterizations showed that the density and size of Staphylococcus aureus-derived MVs are both similar to those of Gram-negative bacteria. With a proteomics approach, we identified with high confidence a total of 90 protein components of S. aureus-derived MVs. In the group of identified proteins, the highly enriched extracellular proteins suggested that a specific sorting mechanism for vesicular proteins exists. We also identified proteins that facilitate the transfer of proteins to other bacteria, as well to eliminate competing organisms, antibiotic resistance, pathological functions in systemic infections, and MV biogenesis. Taken together, these observations suggest that the secretion of MVs is an evolutionally conserved, universal process that occurs from simple organisms to complex multicellular organisms. This information will help us not only to elucidate the biogenesis and functions of MVs, but also to develop therapeutic tools for vaccines, diagnosis, and antibiotics effective against pathogenic strains of Gram-positive bacteria.

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Author and article information

Contributors

Natayme R. Tartaglia: URI : http://loop.frontiersin.org/people/568574/overview

Koen Breyne: URI : http://loop.frontiersin.org/people/428473/overview

Evelyne Meyer: URI : http://loop.frontiersin.org/people/65051/overview

Julien Jardin: URI : http://loop.frontiersin.org/people/425974/overview

Kristel Demeyere: URI : http://loop.frontiersin.org/people/459410/overview

Nadia Berkova: URI : http://loop.frontiersin.org/people/395088/overview

Vasco Azevedo: URI : http://loop.frontiersin.org/people/34672/overview

Eric Guédon: URI : http://loop.frontiersin.org/people/481717/overview

Yves Le Loir: URI : http://loop.frontiersin.org/people/42854/overview

Journal

Journal ID (nlm-ta): Front Cell Infect Microbiol

Journal ID (iso-abbrev): Front Cell Infect Microbiol

Journal ID (publisher-id): Front. Cell. Infect. Microbiol.

Title: Frontiers in Cellular and Infection Microbiology

Publisher: Frontiers Media S.A.

ISSN (Electronic): 2235-2988

Publication date (Electronic): 22 August 2018

Publication date Collection: 2018

Volume: 8

Electronic Location Identifier: 277

Affiliations

[1] ¹STLO, INRA, Agrocampus Ouest , Rennes, France

[2] ²Federal University of Minas Gerais , Belo Horizonte, Brazil

[3] ³Department of Pharmacology, Toxicology and Biochemistry, Faculty of Veterinary Medicine, Ghent University , Merelbeke, Belgium

[4] ⁴CNRS, Institut de Génétique et Développement de Rennes - UMR 6290, Université de Rennes , Rennes, France

[5] ⁵CNRS, INSERM, Biologie, Santé, Innovation Technologique de Rennes - UMS 3480, Université de Rennes , Rennes, France

Author notes

Edited by: Eric Ghigo, IHU Mediterranee Infection, France

Reviewed by: Francis Alonzo, Loyola University Chicago, United States; Nina M. Van Sorge, University Medical Center Utrecht, Netherlands

*Correspondence: Eric Guédon eric.guedon@ 123456inra.fr

†These authors have contributed equally to this work

‡These authors share senior co-authorship

Article

DOI: 10.3389/fcimb.2018.00277

PMC ID: 6113362

PubMed ID: 30186772

SO-VID: 08a1ab14-e5e4-40ef-b3a4-f38363ad454e

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This is an open-access article distributed under the terms of the Creative Commons Attribution License (CC BY). The use, distribution or reproduction in other forums is permitted, provided the original author(s) and the copyright owner(s) are credited and that the original publication in this journal is cited, in accordance with accepted academic practice. No use, distribution or reproduction is permitted which does not comply with these terms.

History

Date received : 17 May 2018

Date accepted : 25 July 2018

Page count

Figures: 6, Tables: 1, Equations: 0, References: 120, Pages: 17, Words: 11976

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

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Bacterial extracellular vesicles

Most cited references 89

Chemokines: a new classification system and their role in immunity.

Non-classical protein secretion in bacteria

Gram-positive bacteria produce membrane vesicles: proteomics-based characterization of Staphylococcus aureus-derived membrane vesicles.

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