Murine AML12 hepatocytes allow Salmonella Typhimurium T3SS1-independent invasion and intracellular fate

Abstract Numerous studies have demonstrated the key role of the Salmonella Pathogenicity Island 1-encoded type III secretion system (T3SS1) apparatus as well as its associated effectors in the invasion and intracellular fate of Salmonella in the host cell. Several T3SS1 effectors work together to co...

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Main Authors: S. Holbert, E. Barilleau, S. M. Roche, J. Trotereau, S. Georgeault, J. Burlaud-Gaillard, A. Wiedemann, S. Méresse, I. Virlogeux-Payant, P. Velge
Format: Article
Language:English
Published: Nature Portfolio 2021-11-01
Series:Scientific Reports
Online Access:https://doi.org/10.1038/s41598-021-02054-z
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author S. Holbert
E. Barilleau
S. M. Roche
J. Trotereau
S. Georgeault
J. Burlaud-Gaillard
A. Wiedemann
S. Méresse
I. Virlogeux-Payant
P. Velge
author_facet S. Holbert
E. Barilleau
S. M. Roche
J. Trotereau
S. Georgeault
J. Burlaud-Gaillard
A. Wiedemann
S. Méresse
I. Virlogeux-Payant
P. Velge
author_sort S. Holbert
collection DOAJ
description Abstract Numerous studies have demonstrated the key role of the Salmonella Pathogenicity Island 1-encoded type III secretion system (T3SS1) apparatus as well as its associated effectors in the invasion and intracellular fate of Salmonella in the host cell. Several T3SS1 effectors work together to control cytoskeleton networks and induce massive membrane ruffles, allowing pathogen internalization. Salmonella resides in a vacuole whose maturation requires that the activity of T3SS1 subverts early stages of cell signaling. Recently, we identified five cell lines in which Salmonella Typhimurium enters without using its three known invasion factors: T3SS1, Rck and PagN. The present study investigated the intracellular fate of Salmonella Typhimurium in one of these models, the murine hepatocyte cell line AML12. We demonstrated that both wild-type Salmonella and T3SS1-invalidated Salmonella followed a common pathway leading to the formation of a Salmonella containing vacuole (SCV) without classical recruitment of Rho-GTPases. Maturation of the SCV continued through an acidified phase that led to Salmonella multiplication as well as the formation of a tubular network resembling Salmonella induced filaments (SIF). The fact that in the murine AML12 hepatocyte, the T3SS1 mutant induced an intracellular fate resembling to the wild-type strain highlights the fact that Salmonella Typhimurium invasion and intracellular survival can be completely independent of T3SS1.
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spelling doaj.art-4b7786ed7b0e4066a893b52e5a309af92022-12-21T22:43:28ZengNature PortfolioScientific Reports2045-23222021-11-0111111610.1038/s41598-021-02054-zMurine AML12 hepatocytes allow Salmonella Typhimurium T3SS1-independent invasion and intracellular fateS. Holbert0E. Barilleau1S. M. Roche2J. Trotereau3S. Georgeault4J. Burlaud-Gaillard5A. Wiedemann6S. Méresse7I. Virlogeux-Payant8P. Velge9ISP, INRAE, Université de ToursISP, INRAE, Université de ToursISP, INRAE, Université de ToursISP, INRAE, Université de ToursPlateforme IBiSA de Microscopie Electronique, Université de Tours et CHRU de ToursPlateforme IBiSA de Microscopie Electronique, Université de Tours et CHRU de ToursISP, INRAE, Université de ToursCNRS, INSERM, CIML, Aix Marseille UnivISP, INRAE, Université de ToursISP, INRAE, Université de ToursAbstract Numerous studies have demonstrated the key role of the Salmonella Pathogenicity Island 1-encoded type III secretion system (T3SS1) apparatus as well as its associated effectors in the invasion and intracellular fate of Salmonella in the host cell. Several T3SS1 effectors work together to control cytoskeleton networks and induce massive membrane ruffles, allowing pathogen internalization. Salmonella resides in a vacuole whose maturation requires that the activity of T3SS1 subverts early stages of cell signaling. Recently, we identified five cell lines in which Salmonella Typhimurium enters without using its three known invasion factors: T3SS1, Rck and PagN. The present study investigated the intracellular fate of Salmonella Typhimurium in one of these models, the murine hepatocyte cell line AML12. We demonstrated that both wild-type Salmonella and T3SS1-invalidated Salmonella followed a common pathway leading to the formation of a Salmonella containing vacuole (SCV) without classical recruitment of Rho-GTPases. Maturation of the SCV continued through an acidified phase that led to Salmonella multiplication as well as the formation of a tubular network resembling Salmonella induced filaments (SIF). The fact that in the murine AML12 hepatocyte, the T3SS1 mutant induced an intracellular fate resembling to the wild-type strain highlights the fact that Salmonella Typhimurium invasion and intracellular survival can be completely independent of T3SS1.https://doi.org/10.1038/s41598-021-02054-z
spellingShingle S. Holbert
E. Barilleau
S. M. Roche
J. Trotereau
S. Georgeault
J. Burlaud-Gaillard
A. Wiedemann
S. Méresse
I. Virlogeux-Payant
P. Velge
Murine AML12 hepatocytes allow Salmonella Typhimurium T3SS1-independent invasion and intracellular fate
Scientific Reports
title Murine AML12 hepatocytes allow Salmonella Typhimurium T3SS1-independent invasion and intracellular fate
title_full Murine AML12 hepatocytes allow Salmonella Typhimurium T3SS1-independent invasion and intracellular fate
title_fullStr Murine AML12 hepatocytes allow Salmonella Typhimurium T3SS1-independent invasion and intracellular fate
title_full_unstemmed Murine AML12 hepatocytes allow Salmonella Typhimurium T3SS1-independent invasion and intracellular fate
title_short Murine AML12 hepatocytes allow Salmonella Typhimurium T3SS1-independent invasion and intracellular fate
title_sort murine aml12 hepatocytes allow salmonella typhimurium t3ss1 independent invasion and intracellular fate
url https://doi.org/10.1038/s41598-021-02054-z
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