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Dietary Fiber-Induced Microbial Short Chain Fatty Acids Suppress ILC2-Dependent Airway Inflammation

Group 2 Innate lymphoid cells (ILC2) contribute significantly to allergic inflammation. However, the role of microbiota on ILC2s remains to be unraveled. Here we show that short chain fatty acids (SCFAs), such as butyrate, derived from fermentation of dietary fibers by the gut microbiota inhibit pul...

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Autores principales: Lewis, Gavin, Wang, Bowen, Shafiei Jahani, Pedram, Hurrell, Benjamin P., Banie, Homayon, Aleman Muench, German R., Maazi, Hadi, Helou, Doumet Georges, Howard, Emily, Galle-Treger, Lauriane, Lo, Richard, Santosh, Swetha, Baltus, Andrew, Bongers, Gerrold, San-Mateo, Lani, Gilliland, Frank D., Rehan, Virender K., Soroosh, Pejman, Akbari, Omid
Formato: Online Artículo Texto
Lenguaje:English
Publicado: Frontiers Media S.A. 2019
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC6760365/
https://www.ncbi.nlm.nih.gov/pubmed/31620118
http://dx.doi.org/10.3389/fimmu.2019.02051
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author Lewis, Gavin
Wang, Bowen
Shafiei Jahani, Pedram
Hurrell, Benjamin P.
Banie, Homayon
Aleman Muench, German R.
Maazi, Hadi
Helou, Doumet Georges
Howard, Emily
Galle-Treger, Lauriane
Lo, Richard
Santosh, Swetha
Baltus, Andrew
Bongers, Gerrold
San-Mateo, Lani
Gilliland, Frank D.
Rehan, Virender K.
Soroosh, Pejman
Akbari, Omid
author_facet Lewis, Gavin
Wang, Bowen
Shafiei Jahani, Pedram
Hurrell, Benjamin P.
Banie, Homayon
Aleman Muench, German R.
Maazi, Hadi
Helou, Doumet Georges
Howard, Emily
Galle-Treger, Lauriane
Lo, Richard
Santosh, Swetha
Baltus, Andrew
Bongers, Gerrold
San-Mateo, Lani
Gilliland, Frank D.
Rehan, Virender K.
Soroosh, Pejman
Akbari, Omid
author_sort Lewis, Gavin
collection PubMed
description Group 2 Innate lymphoid cells (ILC2) contribute significantly to allergic inflammation. However, the role of microbiota on ILC2s remains to be unraveled. Here we show that short chain fatty acids (SCFAs), such as butyrate, derived from fermentation of dietary fibers by the gut microbiota inhibit pulmonary ILC2 functions and subsequent development of airway hyperreactivity (AHR). We further show that SCFAs modulate GATA3, oxidative phosphorylation, and glycolytic metabolic pathways in pulmonary ILC2s. The observed phenotype is associated with increased IL-17a secretion by lung ILC2s and linked to enhanced neutrophil recruitment to the airways. Finally, we show that butyrate-producing gut bacteria in germ-free mice effectively suppress ILC2-driven AHR. Collectively, our results demonstrate a previously unrecognized role for microbial-derived SCFAs on pulmonary ILC2s in the context of AHR. The data suggest strategies aimed at modulating metabolomics and microbiota in the gut, not only to treat, but to prevent lung inflammation and asthma.
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spelling pubmed-67603652019-10-16 Dietary Fiber-Induced Microbial Short Chain Fatty Acids Suppress ILC2-Dependent Airway Inflammation Lewis, Gavin Wang, Bowen Shafiei Jahani, Pedram Hurrell, Benjamin P. Banie, Homayon Aleman Muench, German R. Maazi, Hadi Helou, Doumet Georges Howard, Emily Galle-Treger, Lauriane Lo, Richard Santosh, Swetha Baltus, Andrew Bongers, Gerrold San-Mateo, Lani Gilliland, Frank D. Rehan, Virender K. Soroosh, Pejman Akbari, Omid Front Immunol Immunology Group 2 Innate lymphoid cells (ILC2) contribute significantly to allergic inflammation. However, the role of microbiota on ILC2s remains to be unraveled. Here we show that short chain fatty acids (SCFAs), such as butyrate, derived from fermentation of dietary fibers by the gut microbiota inhibit pulmonary ILC2 functions and subsequent development of airway hyperreactivity (AHR). We further show that SCFAs modulate GATA3, oxidative phosphorylation, and glycolytic metabolic pathways in pulmonary ILC2s. The observed phenotype is associated with increased IL-17a secretion by lung ILC2s and linked to enhanced neutrophil recruitment to the airways. Finally, we show that butyrate-producing gut bacteria in germ-free mice effectively suppress ILC2-driven AHR. Collectively, our results demonstrate a previously unrecognized role for microbial-derived SCFAs on pulmonary ILC2s in the context of AHR. The data suggest strategies aimed at modulating metabolomics and microbiota in the gut, not only to treat, but to prevent lung inflammation and asthma. Frontiers Media S.A. 2019-09-18 /pmc/articles/PMC6760365/ /pubmed/31620118 http://dx.doi.org/10.3389/fimmu.2019.02051 Text en Copyright © 2019 Lewis, Wang, Shafiei Jahani, Hurrell, Banie, Aleman Muench, Maazi, Howard, Galle-Treger, Lo, Santosh, Baltus, Bongers, San-Mateo, Gilliland, Rehan, Soroosh and Akbari. http://creativecommons.org/licenses/by/4.0/ This is an open-access article distributed under the terms of the Creative Commons Attribution License (CC BY). The use, distribution or reproduction in other forums is permitted, provided the original author(s) and the copyright owner(s) are credited and that the original publication in this journal is cited, in accordance with accepted academic practice. No use, distribution or reproduction is permitted which does not comply with these terms.
spellingShingle Immunology
Lewis, Gavin
Wang, Bowen
Shafiei Jahani, Pedram
Hurrell, Benjamin P.
Banie, Homayon
Aleman Muench, German R.
Maazi, Hadi
Helou, Doumet Georges
Howard, Emily
Galle-Treger, Lauriane
Lo, Richard
Santosh, Swetha
Baltus, Andrew
Bongers, Gerrold
San-Mateo, Lani
Gilliland, Frank D.
Rehan, Virender K.
Soroosh, Pejman
Akbari, Omid
Dietary Fiber-Induced Microbial Short Chain Fatty Acids Suppress ILC2-Dependent Airway Inflammation
title Dietary Fiber-Induced Microbial Short Chain Fatty Acids Suppress ILC2-Dependent Airway Inflammation
title_full Dietary Fiber-Induced Microbial Short Chain Fatty Acids Suppress ILC2-Dependent Airway Inflammation
title_fullStr Dietary Fiber-Induced Microbial Short Chain Fatty Acids Suppress ILC2-Dependent Airway Inflammation
title_full_unstemmed Dietary Fiber-Induced Microbial Short Chain Fatty Acids Suppress ILC2-Dependent Airway Inflammation
title_short Dietary Fiber-Induced Microbial Short Chain Fatty Acids Suppress ILC2-Dependent Airway Inflammation
title_sort dietary fiber-induced microbial short chain fatty acids suppress ilc2-dependent airway inflammation
topic Immunology
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC6760365/
https://www.ncbi.nlm.nih.gov/pubmed/31620118
http://dx.doi.org/10.3389/fimmu.2019.02051
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