Septins restrict inflammation and protect zebrafish larvae from Shigella infection.

Shigella flexneri, a Gram-negative enteroinvasive pathogen, causes inflammatory destruction of the human intestinal epithelium. Infection by S. flexneri has been well-studied in vitro and is a paradigm for bacterial interactions with the host immune system. Recent work has revealed that components o...

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Main Authors: Maria J Mazon-Moya, Alexandra R Willis, Vincenzo Torraca, Laurent Boucontet, Avinash R Shenoy, Emma Colucci-Guyon, Serge Mostowy
Format: Article
Language:English
Published: Public Library of Science (PLoS) 2017-06-01
Series:PLoS Pathogens
Online Access:https://journals.plos.org/plospathogens/article/file?id=10.1371/journal.ppat.1006467&type=printable
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author Maria J Mazon-Moya
Alexandra R Willis
Vincenzo Torraca
Laurent Boucontet
Avinash R Shenoy
Emma Colucci-Guyon
Serge Mostowy
author_facet Maria J Mazon-Moya
Alexandra R Willis
Vincenzo Torraca
Laurent Boucontet
Avinash R Shenoy
Emma Colucci-Guyon
Serge Mostowy
author_sort Maria J Mazon-Moya
collection DOAJ
description Shigella flexneri, a Gram-negative enteroinvasive pathogen, causes inflammatory destruction of the human intestinal epithelium. Infection by S. flexneri has been well-studied in vitro and is a paradigm for bacterial interactions with the host immune system. Recent work has revealed that components of the cytoskeleton have important functions in innate immunity and inflammation control. Septins, highly conserved cytoskeletal proteins, have emerged as key players in innate immunity to bacterial infection, yet septin function in vivo is poorly understood. Here, we use S. flexneri infection of zebrafish (Danio rerio) larvae to study in vivo the role of septins in inflammation and infection control. We found that depletion of Sept15 or Sept7b, zebrafish orthologs of human SEPT7, significantly increased host susceptibility to bacterial infection. Live-cell imaging of Sept15-depleted larvae revealed increasing bacterial burdens and a failure of neutrophils to control infection. Strikingly, Sept15-depleted larvae present significantly increased activity of Caspase-1 and more cell death upon S. flexneri infection. Dampening of the inflammatory response with anakinra, an antagonist of interleukin-1 receptor (IL-1R), counteracts Sept15 deficiency in vivo by protecting zebrafish from hyper-inflammation and S. flexneri infection. These findings highlight a new role for septins in host defence against bacterial infection, and suggest that septin dysfunction may be an underlying factor in cases of hyper-inflammation.
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spelling doaj-art-cbc5f72660c24379a1acddcf231f36fa2025-08-20T03:19:52ZengPublic Library of Science (PLoS)PLoS Pathogens1553-73661553-73742017-06-01136e100646710.1371/journal.ppat.1006467Septins restrict inflammation and protect zebrafish larvae from Shigella infection.Maria J Mazon-MoyaAlexandra R WillisVincenzo TorracaLaurent BoucontetAvinash R ShenoyEmma Colucci-GuyonSerge MostowyShigella flexneri, a Gram-negative enteroinvasive pathogen, causes inflammatory destruction of the human intestinal epithelium. Infection by S. flexneri has been well-studied in vitro and is a paradigm for bacterial interactions with the host immune system. Recent work has revealed that components of the cytoskeleton have important functions in innate immunity and inflammation control. Septins, highly conserved cytoskeletal proteins, have emerged as key players in innate immunity to bacterial infection, yet septin function in vivo is poorly understood. Here, we use S. flexneri infection of zebrafish (Danio rerio) larvae to study in vivo the role of septins in inflammation and infection control. We found that depletion of Sept15 or Sept7b, zebrafish orthologs of human SEPT7, significantly increased host susceptibility to bacterial infection. Live-cell imaging of Sept15-depleted larvae revealed increasing bacterial burdens and a failure of neutrophils to control infection. Strikingly, Sept15-depleted larvae present significantly increased activity of Caspase-1 and more cell death upon S. flexneri infection. Dampening of the inflammatory response with anakinra, an antagonist of interleukin-1 receptor (IL-1R), counteracts Sept15 deficiency in vivo by protecting zebrafish from hyper-inflammation and S. flexneri infection. These findings highlight a new role for septins in host defence against bacterial infection, and suggest that septin dysfunction may be an underlying factor in cases of hyper-inflammation.https://journals.plos.org/plospathogens/article/file?id=10.1371/journal.ppat.1006467&type=printable
spellingShingle Maria J Mazon-Moya
Alexandra R Willis
Vincenzo Torraca
Laurent Boucontet
Avinash R Shenoy
Emma Colucci-Guyon
Serge Mostowy
Septins restrict inflammation and protect zebrafish larvae from Shigella infection.
PLoS Pathogens
title Septins restrict inflammation and protect zebrafish larvae from Shigella infection.
title_full Septins restrict inflammation and protect zebrafish larvae from Shigella infection.
title_fullStr Septins restrict inflammation and protect zebrafish larvae from Shigella infection.
title_full_unstemmed Septins restrict inflammation and protect zebrafish larvae from Shigella infection.
title_short Septins restrict inflammation and protect zebrafish larvae from Shigella infection.
title_sort septins restrict inflammation and protect zebrafish larvae from shigella infection
url https://journals.plos.org/plospathogens/article/file?id=10.1371/journal.ppat.1006467&type=printable
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AT vincenzotorraca septinsrestrictinflammationandprotectzebrafishlarvaefromshigellainfection
AT laurentboucontet septinsrestrictinflammationandprotectzebrafishlarvaefromshigellainfection
AT avinashrshenoy septinsrestrictinflammationandprotectzebrafishlarvaefromshigellainfection
AT emmacolucciguyon septinsrestrictinflammationandprotectzebrafishlarvaefromshigellainfection
AT sergemostowy septinsrestrictinflammationandprotectzebrafishlarvaefromshigellainfection