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Fasting increases microbiome-based colonization resistance and reduces host inflammatory responses during an enteric bacterial infection

Reducing food intake is a common host response to infection, yet it remains unclear whether fasting is detrimental or beneficial to an infected host. Despite the gastrointestinal tract being the primary site of nutrient uptake and a common route for infection, studies have yet to examine how fasting...

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Autores principales: Graef, Franziska A., Celiberto, Larissa S., Allaire, Joannie M., Kuan, Mimi T. Y., Bosman, Else S., Crowley, Shauna M., Yang, Hyungjun, Chan, Justin H., Stahl, Martin, Yu, Hongbing, Quin, Candice, Gibson, Deanna L., Verdu, Elena F., Jacobson, Kevan, Vallance, Bruce A.
Formato: Online Artículo Texto
Lenguaje:English
Publicado: Public Library of Science 2021
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC8341583/
https://www.ncbi.nlm.nih.gov/pubmed/34352037
http://dx.doi.org/10.1371/journal.ppat.1009719
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author Graef, Franziska A.
Celiberto, Larissa S.
Allaire, Joannie M.
Kuan, Mimi T. Y.
Bosman, Else S.
Crowley, Shauna M.
Yang, Hyungjun
Chan, Justin H.
Stahl, Martin
Yu, Hongbing
Quin, Candice
Gibson, Deanna L.
Verdu, Elena F.
Jacobson, Kevan
Vallance, Bruce A.
author_facet Graef, Franziska A.
Celiberto, Larissa S.
Allaire, Joannie M.
Kuan, Mimi T. Y.
Bosman, Else S.
Crowley, Shauna M.
Yang, Hyungjun
Chan, Justin H.
Stahl, Martin
Yu, Hongbing
Quin, Candice
Gibson, Deanna L.
Verdu, Elena F.
Jacobson, Kevan
Vallance, Bruce A.
author_sort Graef, Franziska A.
collection PubMed
description Reducing food intake is a common host response to infection, yet it remains unclear whether fasting is detrimental or beneficial to an infected host. Despite the gastrointestinal tract being the primary site of nutrient uptake and a common route for infection, studies have yet to examine how fasting alters the host’s response to an enteric infection. To test this, mice were fasted before and during oral infection with the invasive bacterium Salmonella enterica serovar Typhimurium. Fasting dramatically interrupted infection and subsequent gastroenteritis by suppressing Salmonella’s SPI-1 virulence program, preventing invasion of the gut epithelium. Virulence suppression depended on the gut microbiota, as Salmonella’s invasion of the epithelium proceeded in fasting gnotobiotic mice. Despite Salmonella’s restored virulence within the intestines of gnotobiotic mice, fasting downregulated pro-inflammatory signaling, greatly reducing intestinal pathology. Our study highlights how food intake controls the complex relationship between host, pathogen and gut microbiota during an enteric infection.
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spelling pubmed-83415832021-08-06 Fasting increases microbiome-based colonization resistance and reduces host inflammatory responses during an enteric bacterial infection Graef, Franziska A. Celiberto, Larissa S. Allaire, Joannie M. Kuan, Mimi T. Y. Bosman, Else S. Crowley, Shauna M. Yang, Hyungjun Chan, Justin H. Stahl, Martin Yu, Hongbing Quin, Candice Gibson, Deanna L. Verdu, Elena F. Jacobson, Kevan Vallance, Bruce A. PLoS Pathog Research Article Reducing food intake is a common host response to infection, yet it remains unclear whether fasting is detrimental or beneficial to an infected host. Despite the gastrointestinal tract being the primary site of nutrient uptake and a common route for infection, studies have yet to examine how fasting alters the host’s response to an enteric infection. To test this, mice were fasted before and during oral infection with the invasive bacterium Salmonella enterica serovar Typhimurium. Fasting dramatically interrupted infection and subsequent gastroenteritis by suppressing Salmonella’s SPI-1 virulence program, preventing invasion of the gut epithelium. Virulence suppression depended on the gut microbiota, as Salmonella’s invasion of the epithelium proceeded in fasting gnotobiotic mice. Despite Salmonella’s restored virulence within the intestines of gnotobiotic mice, fasting downregulated pro-inflammatory signaling, greatly reducing intestinal pathology. Our study highlights how food intake controls the complex relationship between host, pathogen and gut microbiota during an enteric infection. Public Library of Science 2021-08-05 /pmc/articles/PMC8341583/ /pubmed/34352037 http://dx.doi.org/10.1371/journal.ppat.1009719 Text en © 2021 Graef et al https://creativecommons.org/licenses/by/4.0/This is an open access article distributed under the terms of the Creative Commons Attribution License (https://creativecommons.org/licenses/by/4.0/) , which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited.
spellingShingle Research Article
Graef, Franziska A.
Celiberto, Larissa S.
Allaire, Joannie M.
Kuan, Mimi T. Y.
Bosman, Else S.
Crowley, Shauna M.
Yang, Hyungjun
Chan, Justin H.
Stahl, Martin
Yu, Hongbing
Quin, Candice
Gibson, Deanna L.
Verdu, Elena F.
Jacobson, Kevan
Vallance, Bruce A.
Fasting increases microbiome-based colonization resistance and reduces host inflammatory responses during an enteric bacterial infection
title Fasting increases microbiome-based colonization resistance and reduces host inflammatory responses during an enteric bacterial infection
title_full Fasting increases microbiome-based colonization resistance and reduces host inflammatory responses during an enteric bacterial infection
title_fullStr Fasting increases microbiome-based colonization resistance and reduces host inflammatory responses during an enteric bacterial infection
title_full_unstemmed Fasting increases microbiome-based colonization resistance and reduces host inflammatory responses during an enteric bacterial infection
title_short Fasting increases microbiome-based colonization resistance and reduces host inflammatory responses during an enteric bacterial infection
title_sort fasting increases microbiome-based colonization resistance and reduces host inflammatory responses during an enteric bacterial infection
topic Research Article
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC8341583/
https://www.ncbi.nlm.nih.gov/pubmed/34352037
http://dx.doi.org/10.1371/journal.ppat.1009719
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