Exopolysaccharide-Producing <i>Bifidobacterium adolescentis</i> Strains with Similar Adhesion Property Induce Differential Regulation of Inflammatory Immune Response in Treg/Th17 Axis of DSS-Colitis Mice

Intestinal bifidobacteria benefit human health by promoting and modulating the gut flora, and boosting therapeutic efficiency for chronic metabolic diseases and cancer. Recently, <i>Bifidobacterium adolescentis</i> strains with high adhesion to intestinal epithelial cells were associated...

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Main Authors: Rui Yu, Fanglei Zuo, Huiqin Ma, Shangwu Chen
Format: Article
Language:English
Published: MDPI AG 2019-04-01
Series:Nutrients
Subjects:
IBD
Online Access:https://www.mdpi.com/2072-6643/11/4/782
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spelling doaj-7ae5a681073f4a63ac7d713964ac35ba2020-11-25T00:14:41ZengMDPI AGNutrients2072-66432019-04-0111478210.3390/nu11040782nu11040782Exopolysaccharide-Producing <i>Bifidobacterium adolescentis</i> Strains with Similar Adhesion Property Induce Differential Regulation of Inflammatory Immune Response in Treg/Th17 Axis of DSS-Colitis MiceRui Yu0Fanglei Zuo1Huiqin Ma2Shangwu Chen3Key Laboratory of Functional Dairy Science, College of Food Science and Nutritional Engineering, China Agricultural University, Beijing 100083, ChinaKey Laboratory of Functional Dairy Science, College of Food Science and Nutritional Engineering, China Agricultural University, Beijing 100083, ChinaCollege of Horticulture, China Agricultural University, Beijing 100193, ChinaKey Laboratory of Functional Dairy Science, College of Food Science and Nutritional Engineering, China Agricultural University, Beijing 100083, ChinaIntestinal bifidobacteria benefit human health by promoting and modulating the gut flora, and boosting therapeutic efficiency for chronic metabolic diseases and cancer. Recently, <i>Bifidobacterium adolescentis</i> strains with high adhesion to intestinal epithelial cells were associated with induction of T-helper 17 (Th17) cells in humans and rodents. Here, two <i>B. adolescentis</i> strains with similar adhesive ability but different aggregation properties were investigated for specific immunoregulatory effects, including the underlying cellular pathway, on macrophage and T-regulatory (Treg)/Th17 axis activation in vitro and in the colon of dextran sodium sulfate (DSS)-colitis mice in vivo. In-vitro, the auto-aggregative <i>B</i>. <i>adolescentis</i> strain IF1-11 induced significantly higher IL-6 and lower IL-10 secretion from immune cells, and it induced abundant Th17 cells. The non-aggregating strain IF1-03 induced significantly higher IL-10, less IL-6 and a high proportion of Treg/Th17 cells compared to total T cells. In vivo, orally administered IF1-03 protected DSS-colitis mice via activation of dendritic cells or macrophages and skewing of Treg/Th17 cells, consistent with Treg cell induction in vitro. IF1-03 exopolysaccharides showed a functional recognition pattern similar to IF1-03 for IL-10 cytokine secretion and Treg cell-differentiation induction, both dependent on the toll-like receptor 2&#8211;ERK/p38 MAPK-signaling cascade for macrophage activation. We suggest that <i>B</i>. <i>adolescentis</i> exopolysaccharide-associated enterocyte adhesion/aggregation phenotypes determine strain-specific adaptive immune responses in the gut via the macrophage-regulated Treg/Th17 axis.https://www.mdpi.com/2072-6643/11/4/782<i>Bifidobacterium adolescentis</i>macrophageTreg/Th17 axisexopolysaccharideERK/p38 MAPK pathwayIBD
collection DOAJ
language English
format Article
sources DOAJ
author Rui Yu
Fanglei Zuo
Huiqin Ma
Shangwu Chen
spellingShingle Rui Yu
Fanglei Zuo
Huiqin Ma
Shangwu Chen
Exopolysaccharide-Producing <i>Bifidobacterium adolescentis</i> Strains with Similar Adhesion Property Induce Differential Regulation of Inflammatory Immune Response in Treg/Th17 Axis of DSS-Colitis Mice
Nutrients
<i>Bifidobacterium adolescentis</i>
macrophage
Treg/Th17 axis
exopolysaccharide
ERK/p38 MAPK pathway
IBD
author_facet Rui Yu
Fanglei Zuo
Huiqin Ma
Shangwu Chen
author_sort Rui Yu
title Exopolysaccharide-Producing <i>Bifidobacterium adolescentis</i> Strains with Similar Adhesion Property Induce Differential Regulation of Inflammatory Immune Response in Treg/Th17 Axis of DSS-Colitis Mice
title_short Exopolysaccharide-Producing <i>Bifidobacterium adolescentis</i> Strains with Similar Adhesion Property Induce Differential Regulation of Inflammatory Immune Response in Treg/Th17 Axis of DSS-Colitis Mice
title_full Exopolysaccharide-Producing <i>Bifidobacterium adolescentis</i> Strains with Similar Adhesion Property Induce Differential Regulation of Inflammatory Immune Response in Treg/Th17 Axis of DSS-Colitis Mice
title_fullStr Exopolysaccharide-Producing <i>Bifidobacterium adolescentis</i> Strains with Similar Adhesion Property Induce Differential Regulation of Inflammatory Immune Response in Treg/Th17 Axis of DSS-Colitis Mice
title_full_unstemmed Exopolysaccharide-Producing <i>Bifidobacterium adolescentis</i> Strains with Similar Adhesion Property Induce Differential Regulation of Inflammatory Immune Response in Treg/Th17 Axis of DSS-Colitis Mice
title_sort exopolysaccharide-producing <i>bifidobacterium adolescentis</i> strains with similar adhesion property induce differential regulation of inflammatory immune response in treg/th17 axis of dss-colitis mice
publisher MDPI AG
series Nutrients
issn 2072-6643
publishDate 2019-04-01
description Intestinal bifidobacteria benefit human health by promoting and modulating the gut flora, and boosting therapeutic efficiency for chronic metabolic diseases and cancer. Recently, <i>Bifidobacterium adolescentis</i> strains with high adhesion to intestinal epithelial cells were associated with induction of T-helper 17 (Th17) cells in humans and rodents. Here, two <i>B. adolescentis</i> strains with similar adhesive ability but different aggregation properties were investigated for specific immunoregulatory effects, including the underlying cellular pathway, on macrophage and T-regulatory (Treg)/Th17 axis activation in vitro and in the colon of dextran sodium sulfate (DSS)-colitis mice in vivo. In-vitro, the auto-aggregative <i>B</i>. <i>adolescentis</i> strain IF1-11 induced significantly higher IL-6 and lower IL-10 secretion from immune cells, and it induced abundant Th17 cells. The non-aggregating strain IF1-03 induced significantly higher IL-10, less IL-6 and a high proportion of Treg/Th17 cells compared to total T cells. In vivo, orally administered IF1-03 protected DSS-colitis mice via activation of dendritic cells or macrophages and skewing of Treg/Th17 cells, consistent with Treg cell induction in vitro. IF1-03 exopolysaccharides showed a functional recognition pattern similar to IF1-03 for IL-10 cytokine secretion and Treg cell-differentiation induction, both dependent on the toll-like receptor 2&#8211;ERK/p38 MAPK-signaling cascade for macrophage activation. We suggest that <i>B</i>. <i>adolescentis</i> exopolysaccharide-associated enterocyte adhesion/aggregation phenotypes determine strain-specific adaptive immune responses in the gut via the macrophage-regulated Treg/Th17 axis.
topic <i>Bifidobacterium adolescentis</i>
macrophage
Treg/Th17 axis
exopolysaccharide
ERK/p38 MAPK pathway
IBD
url https://www.mdpi.com/2072-6643/11/4/782
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