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Research Article | Host-Microbe Biology

Mast Cell Cytonemes as a Defense Mechanism against Coxiella burnetii

Soraya Mezouar, Joana Vitte, Laurent Gorvel, Amira Ben Amara, Benoit Desnues, Jean-Louis Mege
Jon P. Boyle, Editor
Soraya Mezouar
aAix-Marseille Université, IRD, APHM, MEPHI, IHU-Méditerranée Infection, Marseille, France
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Joana Vitte
aAix-Marseille Université, IRD, APHM, MEPHI, IHU-Méditerranée Infection, Marseille, France
bAPHM, IHU-Méditerranée Infection, UF Immunologie, Marseille, France
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Laurent Gorvel
cCRCM, CNRS UMR7258, INSERM U1068, Institut Paoli-Calmettes, Aix-Marseille Université, UM105, Marseille, France
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Amira Ben Amara
cCRCM, CNRS UMR7258, INSERM U1068, Institut Paoli-Calmettes, Aix-Marseille Université, UM105, Marseille, France
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Benoit Desnues
aAix-Marseille Université, IRD, APHM, MEPHI, IHU-Méditerranée Infection, Marseille, France
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Jean-Louis Mege
aAix-Marseille Université, IRD, APHM, MEPHI, IHU-Méditerranée Infection, Marseille, France
bAPHM, IHU-Méditerranée Infection, UF Immunologie, Marseille, France
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Jon P. Boyle
University of Pittsburgh
Roles: Editor
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DOI: 10.1128/mBio.02669-18
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ABSTRACT

Mast cells (MCs) are critical mediators of inflammation; however, their microbicidal activity against invading pathogens remains largely unknown. Here, we describe a nonpreviously reported antibacterial mechanism used by MCs against Coxiella burnetii, the agent of Q fever. We show that C. burnetii interaction with MCs does not result in bacterial uptake but rather induces the formation of extracellular actin filaments named cytonemes. MC cytonemes express cathelicidin and neutrophil elastase and mediate the capture and destruction of entrapped bacteria. We provide evidence that MC cytoneme formation and microbicidal activity are dependent on the cooperation of the scavenger receptor CD36 and Toll-like receptor 4. Taken together, our results suggest that MCs use an extracellular sophisticated mechanism of defense to eliminate intracellular pathogens, such as C. burnetii, before their entry into host cells.

IMPORTANCE Mast cells (MCs) are found in tissues that are in close contact with external environment, such as skin, lungs, or intestinal mucosa but also in the placenta during pregnancy. If their role in mediating allergic conditions is established, several studies now highlight their importance during infection with extracellular pathogens. This study showed a new and effective antimicrobial mechanism of MCs against Coxiella burnetii, an intracellular bacterium whose infection during pregnancy is associated with abortion, preterm labor, and stillbirth. The data reveal that in response to C. burnetii, MCs release extracellular actin filaments that contain antimicrobial agents and are capable to trap and kill bacteria. We show that this mechanism is dependent on the cooperation of two membrane receptors, CD36 and Toll-like receptor 4, and may occur in the placenta during pregnancy by using ex vivo placental MCs. Overall, this study reports an unexpected role for MCs during infection with intracellular bacteria and suggests that MC response to C. burnetii infection is a protective defense mechanism during pregnancy.

  • Copyright © 2019 Mezouar et al.

This is an open-access article distributed under the terms of the Creative Commons Attribution 4.0 International license.

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Mast Cell Cytonemes as a Defense Mechanism against Coxiella burnetii
Soraya Mezouar, Joana Vitte, Laurent Gorvel, Amira Ben Amara, Benoit Desnues, Jean-Louis Mege
mBio Apr 2019, 10 (2) e02669-18; DOI: 10.1128/mBio.02669-18

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Mast Cell Cytonemes as a Defense Mechanism against Coxiella burnetii
Soraya Mezouar, Joana Vitte, Laurent Gorvel, Amira Ben Amara, Benoit Desnues, Jean-Louis Mege
mBio Apr 2019, 10 (2) e02669-18; DOI: 10.1128/mBio.02669-18
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KEYWORDS

CD36
Coxiella burnetii
mast cells
TLR4
cytonemes

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