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A Novel Role of Listeria monocytogenes Membrane Vesicles in Inhibition of Autophagy and Cell Death
Umeå University, Faculty of Medicine, Department of Molecular Biology (Faculty of Medicine). Umeå University, Faculty of Medicine, Molecular Infection Medicine Sweden (MIMS). Umeå University, Faculty of Medicine, Umeå Centre for Microbial Research (UCMR).
Umeå University, Faculty of Medicine, Molecular Infection Medicine Sweden (MIMS). Umeå University, Faculty of Medicine, Department of Medical Biochemistry and Biophysics.
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2017 (English)In: Frontiers in Cellular and Infection Microbiology, E-ISSN 2235-2988, Vol. 7, 154Article in journal (Refereed) Published
Abstract [en]

Bacterial membrane vesicle (MV) production has been mainly studied in Gram-negative species. In this study, we show that Listeria monocytogenes, a Gram-positive pathogen that causes the food-borne illness listeriosis, produces MVs both in vitro and in vivo. We found that a major virulence factor, the pore-forming hemolysin listeriolysin O (LLO), is tightly associated with the MVs, where it resides in an oxidized, inactive state. Previous studies have shown that LLO may induce cell death and autophagy. To monitor possible effects of LLO and MVs on autophagy, we performed assays for LC3 lipidation and LDH sequestration as well as analysis by confocal microscopy of HEK293 cells expressing GFP-LC3. The results revealed that MVs alone did not affect autophagy whereas they effectively abrogated autophagy induced by pure LLO or by another pore-forming toxin from Vibrio cholerae, VCC. Moreover, Listeria monocytogenes MVs significantly decreased Torin1-stimulated macroautophagy. In addition, MVs protected against necrosis of HEK293 cells caused by the lytic action of LLO. We explored the mechanisms of LLO-induced autophagy and cell death and demonstrated that the protective effect of MVs involves an inhibition of LLO-induced pore formation resulting in inhibition of autophagy and the lytic action on eukaryotic cells. Further, we determined that these MVs help bacteria to survive inside eukaryotic cells (mouse embryonic fibroblasts). Taken together, these findings suggest that intracellular release of MVs from L. monocytogenes may represent a bacterial strategy to survive inside host cells, by its control of LLO activity and by avoidance of destruction from the autophagy system during infection.

Place, publisher, year, edition, pages
FRONTIERS MEDIA SA , 2017. Vol. 7, 154
Keyword [en]
Listeria monocytogenes, membrane vesicles, autophagy, listeriolysin O, pore-forming toxin
National Category
Immunology in the medical area Cell and Molecular Biology
Identifiers
URN: urn:nbn:se:umu:diva-136187DOI: 10.3389/fcimb.2017.00154ISI: 000400405800001PubMedID: 28516064OAI: oai:DiVA.org:umu-136187DiVA: diva2:1120825
Available from: 2017-07-07 Created: 2017-07-07 Last updated: 2017-07-07Bibliographically approved

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Vdovikova, SvitlanaSkalman, Lars NygårdFrancis, Monika K.Lundmark, RichardJohansson, JörgenWai, Sun N.
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Department of Molecular Biology (Faculty of Medicine)Molecular Infection Medicine Sweden (MIMS)Umeå Centre for Microbial Research (UCMR)Department of Medical Biochemistry and BiophysicsDepartment of Integrative Medical Biology (IMB)
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Immunology in the medical areaCell and Molecular Biology

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CiteExportLink to record
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