Dietary cellulose induces anti-inflammatory immunity and transcriptional programs via maturation of the intestinal microbiota

Although it is generally accepted that dietary fiber is health promoting, the underlying immunological and molecular mechanisms are not well defined, especially with respect to cellulose, the most ubiquitous dietary fiber. Here, the impact of dietary cellulose on intestinal microbiota, immune respon...

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Main Authors: Florence Fischer, Rossana Romero, Anne Hellhund, Uwe Linne, Wilhelm Bertrams, Olaf Pinkenburg, Hosam Shams Eldin, Kai Binder, Ralf Jacob, Alesia Walker, Bärbel Stecher, Marijana Basic, Maik Luu, Rouzbeh Mahdavi, Anna Heintz-Buschart, Alexander Visekruna, Ulrich Steinhoff
Format: Article
Language:English
Published: Taylor & Francis Group 2020-11-01
Series:Gut Microbes
Subjects:
Online Access:http://dx.doi.org/10.1080/19490976.2020.1829962
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spelling doaj-66994b12046c4d7c80be7dcfafb708582021-03-18T15:12:50ZengTaylor & Francis GroupGut Microbes1949-09761949-09842020-11-0112110.1080/19490976.2020.18299621829962Dietary cellulose induces anti-inflammatory immunity and transcriptional programs via maturation of the intestinal microbiotaFlorence Fischer0Rossana Romero1Anne Hellhund2Uwe Linne3Wilhelm Bertrams4Olaf Pinkenburg5Hosam Shams Eldin6Kai Binder7Ralf Jacob8Alesia Walker9Bärbel Stecher10Marijana Basic11Maik Luu12Rouzbeh Mahdavi13Anna Heintz-Buschart14Alexander Visekruna15Ulrich Steinhoff16Philipps UniversityPhilipps UniversityPhilipps UniversityPhilipps UniversityUniversities of Giessen and Marburg Lung Center, Philipps UniversityPhilipps UniversityPhilipps UniversityPhilipps UniversityPhilipps UniversityHelmholtz Zentrum MünchenLudwig Maximilians-University München and German Center for Infection Research (DZIF), Partner Site MunichHannover Medical SchoolPhilipps UniversityPhilipps UniversityHelmholtz Centre for Environmental Research - UFZPhilipps UniversityPhilipps UniversityAlthough it is generally accepted that dietary fiber is health promoting, the underlying immunological and molecular mechanisms are not well defined, especially with respect to cellulose, the most ubiquitous dietary fiber. Here, the impact of dietary cellulose on intestinal microbiota, immune responses and gene expression in health and disease was examined. Lack of dietary cellulose disrupted the age-related diversification of the intestinal microbiota, which subsequently remained in an immature state. Interestingly, one of the most affected microbial genera was Alistipes which is equipped with enzymes to degrade cellulose. Absence of cellulose changed the microbial metabolome, skewed intestinal immune responses toward inflammation, altered the gene expression of intestinal epithelial cells and mice showed increased sensitivity to colitis induction. In contrast, mice with a defined microbiota including A. finegoldii showed enhanced colonic expression of intestinal IL-22 and Reg3γ restoring intestinal barrier function. This study supports the epidemiological observations and adds a causal explanation for the health promoting effects of the most common biopolymer on earth.http://dx.doi.org/10.1080/19490976.2020.1829962celluloseinsoluble fibermicrobiota maturationmicrobial diversitybile acidsmucosal homeostasisinflammationalistipesreg3γil-22
collection DOAJ
language English
format Article
sources DOAJ
author Florence Fischer
Rossana Romero
Anne Hellhund
Uwe Linne
Wilhelm Bertrams
Olaf Pinkenburg
Hosam Shams Eldin
Kai Binder
Ralf Jacob
Alesia Walker
Bärbel Stecher
Marijana Basic
Maik Luu
Rouzbeh Mahdavi
Anna Heintz-Buschart
Alexander Visekruna
Ulrich Steinhoff
spellingShingle Florence Fischer
Rossana Romero
Anne Hellhund
Uwe Linne
Wilhelm Bertrams
Olaf Pinkenburg
Hosam Shams Eldin
Kai Binder
Ralf Jacob
Alesia Walker
Bärbel Stecher
Marijana Basic
Maik Luu
Rouzbeh Mahdavi
Anna Heintz-Buschart
Alexander Visekruna
Ulrich Steinhoff
Dietary cellulose induces anti-inflammatory immunity and transcriptional programs via maturation of the intestinal microbiota
Gut Microbes
cellulose
insoluble fiber
microbiota maturation
microbial diversity
bile acids
mucosal homeostasis
inflammation
alistipes
reg3γ
il-22
author_facet Florence Fischer
Rossana Romero
Anne Hellhund
Uwe Linne
Wilhelm Bertrams
Olaf Pinkenburg
Hosam Shams Eldin
Kai Binder
Ralf Jacob
Alesia Walker
Bärbel Stecher
Marijana Basic
Maik Luu
Rouzbeh Mahdavi
Anna Heintz-Buschart
Alexander Visekruna
Ulrich Steinhoff
author_sort Florence Fischer
title Dietary cellulose induces anti-inflammatory immunity and transcriptional programs via maturation of the intestinal microbiota
title_short Dietary cellulose induces anti-inflammatory immunity and transcriptional programs via maturation of the intestinal microbiota
title_full Dietary cellulose induces anti-inflammatory immunity and transcriptional programs via maturation of the intestinal microbiota
title_fullStr Dietary cellulose induces anti-inflammatory immunity and transcriptional programs via maturation of the intestinal microbiota
title_full_unstemmed Dietary cellulose induces anti-inflammatory immunity and transcriptional programs via maturation of the intestinal microbiota
title_sort dietary cellulose induces anti-inflammatory immunity and transcriptional programs via maturation of the intestinal microbiota
publisher Taylor & Francis Group
series Gut Microbes
issn 1949-0976
1949-0984
publishDate 2020-11-01
description Although it is generally accepted that dietary fiber is health promoting, the underlying immunological and molecular mechanisms are not well defined, especially with respect to cellulose, the most ubiquitous dietary fiber. Here, the impact of dietary cellulose on intestinal microbiota, immune responses and gene expression in health and disease was examined. Lack of dietary cellulose disrupted the age-related diversification of the intestinal microbiota, which subsequently remained in an immature state. Interestingly, one of the most affected microbial genera was Alistipes which is equipped with enzymes to degrade cellulose. Absence of cellulose changed the microbial metabolome, skewed intestinal immune responses toward inflammation, altered the gene expression of intestinal epithelial cells and mice showed increased sensitivity to colitis induction. In contrast, mice with a defined microbiota including A. finegoldii showed enhanced colonic expression of intestinal IL-22 and Reg3γ restoring intestinal barrier function. This study supports the epidemiological observations and adds a causal explanation for the health promoting effects of the most common biopolymer on earth.
topic cellulose
insoluble fiber
microbiota maturation
microbial diversity
bile acids
mucosal homeostasis
inflammation
alistipes
reg3γ
il-22
url http://dx.doi.org/10.1080/19490976.2020.1829962
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