Epithelial cell invasion by salmonella typhimurium induces modulation of genes controlled by aryl hydrocarbon receptor signaling and involved in extracellular matrix biogenesis

Salmonella is the only bacterium able to enter a host cell by the two known mechanisms: trigger and zipper. The trigger mechanism relies on the injection of bacterial effectors into the host cell through the Salmonella type III secretion system 1. In the zipper mechanism, mediated by the invasins Rc...

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Main Authors: Anne-Marie Chaussé, Sylvie M. Roche, Marco Moroldo, Christelle Hennequet-Antier, Sébastien Holbert, Florent Kempf, Emilie Barilleau, Jérome Trotereau, Philippe Velge
Format: Article
Language:English
Published: Taylor & Francis Group 2023-12-01
Series:Virulence
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Online Access:https://www.tandfonline.com/doi/10.1080/21505594.2022.2158663
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author Anne-Marie Chaussé
Sylvie M. Roche
Marco Moroldo
Christelle Hennequet-Antier
Sébastien Holbert
Florent Kempf
Emilie Barilleau
Jérome Trotereau
Philippe Velge
author_facet Anne-Marie Chaussé
Sylvie M. Roche
Marco Moroldo
Christelle Hennequet-Antier
Sébastien Holbert
Florent Kempf
Emilie Barilleau
Jérome Trotereau
Philippe Velge
author_sort Anne-Marie Chaussé
collection DOAJ
description Salmonella is the only bacterium able to enter a host cell by the two known mechanisms: trigger and zipper. The trigger mechanism relies on the injection of bacterial effectors into the host cell through the Salmonella type III secretion system 1. In the zipper mechanism, mediated by the invasins Rck and PagN, the bacterium takes advantage of a cellular receptor for invasion. This study describes the transcriptomic reprogramming of the IEC-6 intestinal epithelial cell line to Salmonella Typhimurium strains that invaded cells by a trigger, a zipper, or both mechanisms. Using S. Typhimurium strains invalidated for one or other entry mechanism, we have shown that IEC-6 cells could support both entries. Comparison of the gene expression profiles of exposed cells showed that irrespective of the mechanism used for entry, the transcriptomic reprogramming of the cell was nearly the same. On the other hand, when gene expression was compared between cells unexposed or exposed to the bacterium, the transcriptomic reprogramming of exposed cells was significantly different. It is particularly interesting to note the modulation of expression of numerous target genes of the aryl hydrocarbon receptor showing that this transcription factor was activated by S. Typhimurium infection. Numerous genes associated with the extracellular matrix were also modified. This was confirmed at the protein level by western-blotting showing a dramatic modification in some extracellular matrix proteins. Analysis of a selected set of modulated genes showed that the expression of the majority of these genes was modulated during the intracellular life of S. Typhimurium.
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spelling doaj-art-ca76997886d74f2994a5f16b31db8fe22025-08-20T02:38:22ZengTaylor & Francis GroupVirulence2150-55942150-56082023-12-0114110.1080/21505594.2022.2158663Epithelial cell invasion by salmonella typhimurium induces modulation of genes controlled by aryl hydrocarbon receptor signaling and involved in extracellular matrix biogenesisAnne-Marie Chaussé0Sylvie M. Roche1Marco Moroldo2Christelle Hennequet-Antier3Sébastien Holbert4Florent Kempf5Emilie Barilleau6Jérome Trotereau7Philippe Velge8INRAE, ISP, Université de Tours, Nouzilly, FranceINRAE, ISP, Université de Tours, Nouzilly, FranceINRAE, AgroParisTech, Université Paris Saclay, Jouy-en-Josas, FranceINRAE, BOA, Université de Tours, Nouzilly, FranceINRAE, ISP, Université de Tours, Nouzilly, FranceINRAE, ISP, Université de Tours, Nouzilly, FranceINRAE, ISP, Université de Tours, Nouzilly, FranceINRAE, ISP, Université de Tours, Nouzilly, FranceINRAE, ISP, Université de Tours, Nouzilly, FranceSalmonella is the only bacterium able to enter a host cell by the two known mechanisms: trigger and zipper. The trigger mechanism relies on the injection of bacterial effectors into the host cell through the Salmonella type III secretion system 1. In the zipper mechanism, mediated by the invasins Rck and PagN, the bacterium takes advantage of a cellular receptor for invasion. This study describes the transcriptomic reprogramming of the IEC-6 intestinal epithelial cell line to Salmonella Typhimurium strains that invaded cells by a trigger, a zipper, or both mechanisms. Using S. Typhimurium strains invalidated for one or other entry mechanism, we have shown that IEC-6 cells could support both entries. Comparison of the gene expression profiles of exposed cells showed that irrespective of the mechanism used for entry, the transcriptomic reprogramming of the cell was nearly the same. On the other hand, when gene expression was compared between cells unexposed or exposed to the bacterium, the transcriptomic reprogramming of exposed cells was significantly different. It is particularly interesting to note the modulation of expression of numerous target genes of the aryl hydrocarbon receptor showing that this transcription factor was activated by S. Typhimurium infection. Numerous genes associated with the extracellular matrix were also modified. This was confirmed at the protein level by western-blotting showing a dramatic modification in some extracellular matrix proteins. Analysis of a selected set of modulated genes showed that the expression of the majority of these genes was modulated during the intracellular life of S. Typhimurium.https://www.tandfonline.com/doi/10.1080/21505594.2022.2158663Salmonella Typhimuriumgene expressionextracellular matrixaryl hydrocarbon receptorcell invasion
spellingShingle Anne-Marie Chaussé
Sylvie M. Roche
Marco Moroldo
Christelle Hennequet-Antier
Sébastien Holbert
Florent Kempf
Emilie Barilleau
Jérome Trotereau
Philippe Velge
Epithelial cell invasion by salmonella typhimurium induces modulation of genes controlled by aryl hydrocarbon receptor signaling and involved in extracellular matrix biogenesis
Virulence
Salmonella Typhimurium
gene expression
extracellular matrix
aryl hydrocarbon receptor
cell invasion
title Epithelial cell invasion by salmonella typhimurium induces modulation of genes controlled by aryl hydrocarbon receptor signaling and involved in extracellular matrix biogenesis
title_full Epithelial cell invasion by salmonella typhimurium induces modulation of genes controlled by aryl hydrocarbon receptor signaling and involved in extracellular matrix biogenesis
title_fullStr Epithelial cell invasion by salmonella typhimurium induces modulation of genes controlled by aryl hydrocarbon receptor signaling and involved in extracellular matrix biogenesis
title_full_unstemmed Epithelial cell invasion by salmonella typhimurium induces modulation of genes controlled by aryl hydrocarbon receptor signaling and involved in extracellular matrix biogenesis
title_short Epithelial cell invasion by salmonella typhimurium induces modulation of genes controlled by aryl hydrocarbon receptor signaling and involved in extracellular matrix biogenesis
title_sort epithelial cell invasion by salmonella typhimurium induces modulation of genes controlled by aryl hydrocarbon receptor signaling and involved in extracellular matrix biogenesis
topic Salmonella Typhimurium
gene expression
extracellular matrix
aryl hydrocarbon receptor
cell invasion
url https://www.tandfonline.com/doi/10.1080/21505594.2022.2158663
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