Mast Cell Cytonemes as a Defense Mechanism against <named-content content-type="genus-species">Coxiella burnetii</named-content>

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. b...

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Autores principales:	Soraya Mezouar, Joana Vitte, Laurent Gorvel, Amira Ben Amara, Benoit Desnues, Jean-Louis Mege
Formato:	article
Lenguaje:	EN
Publicado:	American Society for Microbiology 2019
Materias:	CD36 Coxiella burnetii mast cells TLR4 cytonemes Microbiology QR1-502
Acceso en línea:	https://doaj.org/article/feb44557171545bab6764bc0fac8dc01
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spelling	oai:doaj.org-article:feb44557171545bab6764bc0fac8dc012021-11-15T15:55:26ZMast Cell Cytonemes as a Defense Mechanism against <named-content content-type="genus-species">Coxiella burnetii</named-content>10.1128/mBio.02669-182150-7511https://doaj.org/article/feb44557171545bab6764bc0fac8dc012019-04-01T00:00:00Zhttps://journals.asm.org/doi/10.1128/mBio.02669-18https://doaj.org/toc/2150-7511ABSTRACT 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.Soraya MezouarJoana VitteLaurent GorvelAmira Ben AmaraBenoit DesnuesJean-Louis MegeAmerican Society for MicrobiologyarticleCD36Coxiella burnetiimast cellsTLR4cytonemesMicrobiologyQR1-502ENmBio, Vol 10, Iss 2 (2019)
institution	DOAJ
collection	DOAJ
language	EN
topic	CD36 Coxiella burnetii mast cells TLR4 cytonemes Microbiology QR1-502
spellingShingle	CD36 Coxiella burnetii mast cells TLR4 cytonemes Microbiology QR1-502 Soraya Mezouar Joana Vitte Laurent Gorvel Amira Ben Amara Benoit Desnues Jean-Louis Mege Mast Cell Cytonemes as a Defense Mechanism against <named-content content-type="genus-species">Coxiella burnetii</named-content>
description	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.
format	article
author	Soraya Mezouar Joana Vitte Laurent Gorvel Amira Ben Amara Benoit Desnues Jean-Louis Mege
author_facet	Soraya Mezouar Joana Vitte Laurent Gorvel Amira Ben Amara Benoit Desnues Jean-Louis Mege
author_sort	Soraya Mezouar
title	Mast Cell Cytonemes as a Defense Mechanism against <named-content content-type="genus-species">Coxiella burnetii</named-content>
title_short	Mast Cell Cytonemes as a Defense Mechanism against <named-content content-type="genus-species">Coxiella burnetii</named-content>
title_full	Mast Cell Cytonemes as a Defense Mechanism against <named-content content-type="genus-species">Coxiella burnetii</named-content>
title_fullStr	Mast Cell Cytonemes as a Defense Mechanism against <named-content content-type="genus-species">Coxiella burnetii</named-content>
title_full_unstemmed	Mast Cell Cytonemes as a Defense Mechanism against <named-content content-type="genus-species">Coxiella burnetii</named-content>
title_sort	mast cell cytonemes as a defense mechanism against <named-content content-type="genus-species">coxiella burnetii</named-content>
publisher	American Society for Microbiology
publishDate	2019
url	https://doaj.org/article/feb44557171545bab6764bc0fac8dc01
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Mast Cell Cytonemes as a Defense Mechanism against <named-content content-type="genus-species">Coxiella burnetii</named-content>

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