Vaccination against microbiota motility protects mice from the detrimental impact of dietary emulsifier consumption.

Dietary emulsifiers, including carboxymethylcellulose (CMC) and polysorbate 80 (P80), perturb gut microbiota composition and gene expression, resulting in a microbiota with enhanced capacity to activate host pro-inflammatory gene expression and invade the intestine's inner mucus layer. Such mic...

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Main Authors: Melissa C Kordahi, Clara Delaroque, Marie-Florence Bredèche, Andrew T Gewirtz, Benoit Chassaing
Format: Article
Language:English
Published: Public Library of Science (PLoS) 2023-09-01
Series:PLoS Biology
Online Access:https://doi.org/10.1371/journal.pbio.3002289
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author Melissa C Kordahi
Clara Delaroque
Marie-Florence Bredèche
Andrew T Gewirtz
Benoit Chassaing
author_facet Melissa C Kordahi
Clara Delaroque
Marie-Florence Bredèche
Andrew T Gewirtz
Benoit Chassaing
author_sort Melissa C Kordahi
collection DOAJ
description Dietary emulsifiers, including carboxymethylcellulose (CMC) and polysorbate 80 (P80), perturb gut microbiota composition and gene expression, resulting in a microbiota with enhanced capacity to activate host pro-inflammatory gene expression and invade the intestine's inner mucus layer. Such microbiota alterations promote intestinal inflammation, which can have a variety of phenotypic consequences including increased adiposity. Bacterial flagellin is a key mediator of emulsifiers' impact in that this molecule enables motility and is itself a pro-inflammatory agonist. Hence, we reasoned that training the adaptive mucosal immune system to exclude microbes that express flagellin might protect against emulsifiers. Investigating this notion found that immunizing mice with flagellin elicited an increase in mucosal anti-flagellin IgA and IgA-coated microbiota that would have otherwise developed in response to CMC and P80 consumption. Yet, eliciting these responses in advance via flagellin immunization prevented CMC/P80-induced increases in microbiota expression of pro-inflammatory agonists including LPS and flagellin. Furthermore, such immunization prevented CMC/P80-induced microbiota encroachment and deleterious pro-inflammatory consequences associated therewith, including colon shortening and increased adiposity. Hence, eliciting mucosal immune responses to pathobiont surface components, including flagellin, may be a means of combatting the array of inflammatory diseases that are promoted by emulsifiers and perhaps other modern microbiota stressors.
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spelling doaj.art-fc6309c79c9c4e5b9d4ca82d15c5d1112023-09-26T05:30:18ZengPublic Library of Science (PLoS)PLoS Biology1544-91731545-78852023-09-01219e300228910.1371/journal.pbio.3002289Vaccination against microbiota motility protects mice from the detrimental impact of dietary emulsifier consumption.Melissa C KordahiClara DelaroqueMarie-Florence BredècheAndrew T GewirtzBenoit ChassaingDietary emulsifiers, including carboxymethylcellulose (CMC) and polysorbate 80 (P80), perturb gut microbiota composition and gene expression, resulting in a microbiota with enhanced capacity to activate host pro-inflammatory gene expression and invade the intestine's inner mucus layer. Such microbiota alterations promote intestinal inflammation, which can have a variety of phenotypic consequences including increased adiposity. Bacterial flagellin is a key mediator of emulsifiers' impact in that this molecule enables motility and is itself a pro-inflammatory agonist. Hence, we reasoned that training the adaptive mucosal immune system to exclude microbes that express flagellin might protect against emulsifiers. Investigating this notion found that immunizing mice with flagellin elicited an increase in mucosal anti-flagellin IgA and IgA-coated microbiota that would have otherwise developed in response to CMC and P80 consumption. Yet, eliciting these responses in advance via flagellin immunization prevented CMC/P80-induced increases in microbiota expression of pro-inflammatory agonists including LPS and flagellin. Furthermore, such immunization prevented CMC/P80-induced microbiota encroachment and deleterious pro-inflammatory consequences associated therewith, including colon shortening and increased adiposity. Hence, eliciting mucosal immune responses to pathobiont surface components, including flagellin, may be a means of combatting the array of inflammatory diseases that are promoted by emulsifiers and perhaps other modern microbiota stressors.https://doi.org/10.1371/journal.pbio.3002289
spellingShingle Melissa C Kordahi
Clara Delaroque
Marie-Florence Bredèche
Andrew T Gewirtz
Benoit Chassaing
Vaccination against microbiota motility protects mice from the detrimental impact of dietary emulsifier consumption.
PLoS Biology
title Vaccination against microbiota motility protects mice from the detrimental impact of dietary emulsifier consumption.
title_full Vaccination against microbiota motility protects mice from the detrimental impact of dietary emulsifier consumption.
title_fullStr Vaccination against microbiota motility protects mice from the detrimental impact of dietary emulsifier consumption.
title_full_unstemmed Vaccination against microbiota motility protects mice from the detrimental impact of dietary emulsifier consumption.
title_short Vaccination against microbiota motility protects mice from the detrimental impact of dietary emulsifier consumption.
title_sort vaccination against microbiota motility protects mice from the detrimental impact of dietary emulsifier consumption
url https://doi.org/10.1371/journal.pbio.3002289
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