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Outer membrane vesicles produced by pathogenic strains of Escherichia coli block autophagic flux and exacerbate inflammasome activation

Laure David, View ORCID ProfileFrédéric Taieb, Marie Pénary, Pierre-Jean Bordignon, Rémi Planès, Valérie Duplan-Eche, Etienne Meunier, View ORCID ProfileEric Oswald
doi: https://doi.org/10.1101/2021.04.20.440604
Laure David
aIRSD, INSERM, ENVT, INRAE, Université de Toulouse, UPS, Toulouse, France
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Frédéric Taieb
aIRSD, INSERM, ENVT, INRAE, Université de Toulouse, UPS, Toulouse, France
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  • ORCID record for Frédéric Taieb
Marie Pénary
aIRSD, INSERM, ENVT, INRAE, Université de Toulouse, UPS, Toulouse, France
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Pierre-Jean Bordignon
bInstitute of Pharmacology and Structural Biology (IPBS), University of Toulouse, 9 CNRS, Toulouse, France
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Rémi Planès
bInstitute of Pharmacology and Structural Biology (IPBS), University of Toulouse, 9 CNRS, Toulouse, France
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Valérie Duplan-Eche
cINFINITy, Université de Toulouse, CNRS, INSERM, UPS, Toulouse, France
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Etienne Meunier
bInstitute of Pharmacology and Structural Biology (IPBS), University of Toulouse, 9 CNRS, Toulouse, France
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Eric Oswald
aIRSD, INSERM, ENVT, INRAE, Université de Toulouse, UPS, Toulouse, France
dCHU Toulouse, Hôpital Purpan, Service de Bactériologie-Hygiène, Toulouse, France
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  • ORCID record for Eric Oswald
  • For correspondence: eric.oswald@inserm.fr
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Abstract

Escherichia coli (E. coli) strains are responsible for a majority of human extra-intestinal infections, resulting in huge medical, economic and social costs. We had previously shown that HlyF encoded by a large virulence plasmid harbored by pathogenic E. coli is not a hemolysin but a cytoplasmic enzyme leading to the overproduction of outer membrane vesicles (OMVs). Here, we show that these specific OMVs inhibit the autophagic flux by impairing the autophagosome – lysosome fusion, thus preventing the formation of acidic autolysosome and autophagosome clearance. Furthermore, OMVs from E. coli producing HlyF are much more prone to activate the non-canonical inflammasome pathway. Since autophagy and inflammation are crucial in the host’s response to infection especially during sepsis, our findings reveal an unsuspected role of OMVs in the crosstalk between bacteria and their host, highlighting the fact that these extracellular vesicles have exacerbated pathogenic properties compared to OMVs produced by isogenic strains unable to produce a functional HlyF.

Competing Interest Statement

The authors have declared no competing interest.

  • Abbreviations
    AIEC
    adherent-invasive E. coli
    BDI
    Bright Detail Intensity
    BMDM
    bone marrow-derived macrophages
    Casp
    Caspase
    E. coli
    Escherichia coli
    EHEC
    enterohemorrhagic E. coli
    ExPEC
    extra-intestinal pathogenic E. coli
    GSDM-D
    Gasdermin-D
    GFP
    Green Fluorescent Protein
    HBSS
    Hanks’balanced salt solution
    HlyF
    Hemolysin F
    IL-1β
    interleukin-1β
    ISX
    ImageStreamX system
    LPS
    Lipopolysaccharide
    OMV
    outer membrane vesicle
    RFP
    Red Fluorescent Protein
    TEM
    transmission electron microscopy
    WT
    Wild type
    Mut
    Mutated
  • Copyright 
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    Posted April 20, 2021.
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    Outer membrane vesicles produced by pathogenic strains of Escherichia coli block autophagic flux and exacerbate inflammasome activation
    Laure David, Frédéric Taieb, Marie Pénary, Pierre-Jean Bordignon, Rémi Planès, Valérie Duplan-Eche, Etienne Meunier, Eric Oswald
    bioRxiv 2021.04.20.440604; doi: https://doi.org/10.1101/2021.04.20.440604
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    Outer membrane vesicles produced by pathogenic strains of Escherichia coli block autophagic flux and exacerbate inflammasome activation
    Laure David, Frédéric Taieb, Marie Pénary, Pierre-Jean Bordignon, Rémi Planès, Valérie Duplan-Eche, Etienne Meunier, Eric Oswald
    bioRxiv 2021.04.20.440604; doi: https://doi.org/10.1101/2021.04.20.440604

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