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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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–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–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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