Fermented Astragalus and its metabolites regulate inflammatory status and gut microbiota to repair intestinal barrier damage in dextran sulfate sodium-induced ulcerative colitis

Fermentation represents an efficient biotechnological approach to increase the nutritional and functional potential of traditional Chinese medicine. In this study, Lactobacillus plantarum was used to ferment traditional Chinese medicine Astragalus, the differential metabolites in the fermented Astra...

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Main Authors: Junxiang Li, Yingchun Ma, Xiaofeng Li, Yafei Wang, Zeqi Huo, Yang Lin, Jiaru Li, Hui Yang, Zhiming Zhang, Pingrong Yang, Chunjiang Zhang
Format: Article
Language:English
Published: Frontiers Media S.A. 2022-11-01
Series:Frontiers in Nutrition
Subjects:
Online Access:https://www.frontiersin.org/articles/10.3389/fnut.2022.1035912/full
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author Junxiang Li
Yingchun Ma
Xiaofeng Li
Yafei Wang
Zeqi Huo
Zeqi Huo
Zeqi Huo
Yang Lin
Yang Lin
Yang Lin
Jiaru Li
Hui Yang
Zhiming Zhang
Pingrong Yang
Pingrong Yang
Chunjiang Zhang
Chunjiang Zhang
Chunjiang Zhang
author_facet Junxiang Li
Yingchun Ma
Xiaofeng Li
Yafei Wang
Zeqi Huo
Zeqi Huo
Zeqi Huo
Yang Lin
Yang Lin
Yang Lin
Jiaru Li
Hui Yang
Zhiming Zhang
Pingrong Yang
Pingrong Yang
Chunjiang Zhang
Chunjiang Zhang
Chunjiang Zhang
author_sort Junxiang Li
collection DOAJ
description Fermentation represents an efficient biotechnological approach to increase the nutritional and functional potential of traditional Chinese medicine. In this study, Lactobacillus plantarum was used to ferment traditional Chinese medicine Astragalus, the differential metabolites in the fermented Astragalus (FA) were identified by ultra-performance liquid chromatography-Q Exactive hybrid quadrupole-Orbitrap mass spectrometry (UPLC-Q-Exactive-MS), and the ameliorating effect of FA on dextran sulfate sodium (DSS)-induced colitis in mice were further explored. The results showed that 11 differential metabolites such as raffinose, progesterone and uridine were identified in FA, which may help improve the ability of FA to alleviate colitis. Prophylactic FA supplementation effectively improved DAI score, colon length and histopathological lesion in DSS-treated mice. The abnormal activation of the intestinal immune barrier in mice was controlled after FA supplementation, the contents of myeloperoxidase (MPO) and IgE were reduced and the contents of IgA were increased. The intestinal pro-inflammatory factors TNF-α, IL-1β, IL-6, and IL-17 were down-regulated and the anti-inflammatory factors IL-10 and TGF-β were up-regulated, suggesting that FA can intervene in inflammatory status by regulating the balance of Th1/Th2/Th17/Treg related cytokines. In addition, FA supplementation modified the structure of the intestinal microbiota and enriched the abundance of Akkermansia and Alistipes, which were positively associated with the production of short-chain fatty acids. These microbes and their metabolites induced by FA also be involved in maintaining the intestinal mucosal barrier integrity by affecting mucosal immunity. We observed that intestinal tight junction protein and mucous secreting protein ZO-1, occludin, and MUC2 genes expression were more pronounced in mice supplemented with FA compared to unfermented Astragalus, along with modulation of intestinal epithelial cells (IECs) apoptosis, verifying the intestinal mucosal barrier repaired by FA. This study is the first to suggest that FA as a potential modulator can more effectively regulate the inflammatory status and gut microbiota to repair the intestinal barrier damage caused by colitis.
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spelling doaj.art-d4e04a8c07cc4365b117ed591486a5d02022-12-22T02:30:49ZengFrontiers Media S.A.Frontiers in Nutrition2296-861X2022-11-01910.3389/fnut.2022.10359121035912Fermented Astragalus and its metabolites regulate inflammatory status and gut microbiota to repair intestinal barrier damage in dextran sulfate sodium-induced ulcerative colitisJunxiang Li0Yingchun Ma1Xiaofeng Li2Yafei Wang3Zeqi Huo4Zeqi Huo5Zeqi Huo6Yang Lin7Yang Lin8Yang Lin9Jiaru Li10Hui Yang11Zhiming Zhang12Pingrong Yang13Pingrong Yang14Chunjiang Zhang15Chunjiang Zhang16Chunjiang Zhang17School of Pharmacy, Lanzhou University, Lanzhou, ChinaGansu Institute for Drug Control, Lanzhou, ChinaSchool of Life Sciences, Lanzhou University, Lanzhou, ChinaSchool of Pharmacy, Lanzhou University, Lanzhou, ChinaSchool of Life Sciences, Lanzhou University, Lanzhou, ChinaKey Laboratory of Cell Activities and Stress Adaptations, Ministry of Education, Lanzhou University, Lanzhou, ChinaGansu Key Laboratory of Biomonitoring and Bioremediation for Environmental Pollution, Lanzhou University, Lanzhou, ChinaSchool of Life Sciences, Lanzhou University, Lanzhou, ChinaKey Laboratory of Cell Activities and Stress Adaptations, Ministry of Education, Lanzhou University, Lanzhou, ChinaGansu Key Laboratory of Biomonitoring and Bioremediation for Environmental Pollution, Lanzhou University, Lanzhou, ChinaSchool of Pharmacy, Lanzhou University, Lanzhou, ChinaSchool of Pharmacy, Lanzhou University, Lanzhou, ChinaGansu Provincial Hospital of Traditional Chinese Medicine (TCM), Lanzhou, ChinaSchool of Pharmacy, Lanzhou University, Lanzhou, ChinaGansu Institute for Drug Control, Lanzhou, ChinaSchool of Life Sciences, Lanzhou University, Lanzhou, ChinaKey Laboratory of Cell Activities and Stress Adaptations, Ministry of Education, Lanzhou University, Lanzhou, ChinaGansu Key Laboratory of Biomonitoring and Bioremediation for Environmental Pollution, Lanzhou University, Lanzhou, ChinaFermentation represents an efficient biotechnological approach to increase the nutritional and functional potential of traditional Chinese medicine. In this study, Lactobacillus plantarum was used to ferment traditional Chinese medicine Astragalus, the differential metabolites in the fermented Astragalus (FA) were identified by ultra-performance liquid chromatography-Q Exactive hybrid quadrupole-Orbitrap mass spectrometry (UPLC-Q-Exactive-MS), and the ameliorating effect of FA on dextran sulfate sodium (DSS)-induced colitis in mice were further explored. The results showed that 11 differential metabolites such as raffinose, progesterone and uridine were identified in FA, which may help improve the ability of FA to alleviate colitis. Prophylactic FA supplementation effectively improved DAI score, colon length and histopathological lesion in DSS-treated mice. The abnormal activation of the intestinal immune barrier in mice was controlled after FA supplementation, the contents of myeloperoxidase (MPO) and IgE were reduced and the contents of IgA were increased. The intestinal pro-inflammatory factors TNF-α, IL-1β, IL-6, and IL-17 were down-regulated and the anti-inflammatory factors IL-10 and TGF-β were up-regulated, suggesting that FA can intervene in inflammatory status by regulating the balance of Th1/Th2/Th17/Treg related cytokines. In addition, FA supplementation modified the structure of the intestinal microbiota and enriched the abundance of Akkermansia and Alistipes, which were positively associated with the production of short-chain fatty acids. These microbes and their metabolites induced by FA also be involved in maintaining the intestinal mucosal barrier integrity by affecting mucosal immunity. We observed that intestinal tight junction protein and mucous secreting protein ZO-1, occludin, and MUC2 genes expression were more pronounced in mice supplemented with FA compared to unfermented Astragalus, along with modulation of intestinal epithelial cells (IECs) apoptosis, verifying the intestinal mucosal barrier repaired by FA. This study is the first to suggest that FA as a potential modulator can more effectively regulate the inflammatory status and gut microbiota to repair the intestinal barrier damage caused by colitis.https://www.frontiersin.org/articles/10.3389/fnut.2022.1035912/fullAstragalusfermentationinflammationintestinal barriergut microbiota
spellingShingle Junxiang Li
Yingchun Ma
Xiaofeng Li
Yafei Wang
Zeqi Huo
Zeqi Huo
Zeqi Huo
Yang Lin
Yang Lin
Yang Lin
Jiaru Li
Hui Yang
Zhiming Zhang
Pingrong Yang
Pingrong Yang
Chunjiang Zhang
Chunjiang Zhang
Chunjiang Zhang
Fermented Astragalus and its metabolites regulate inflammatory status and gut microbiota to repair intestinal barrier damage in dextran sulfate sodium-induced ulcerative colitis
Frontiers in Nutrition
Astragalus
fermentation
inflammation
intestinal barrier
gut microbiota
title Fermented Astragalus and its metabolites regulate inflammatory status and gut microbiota to repair intestinal barrier damage in dextran sulfate sodium-induced ulcerative colitis
title_full Fermented Astragalus and its metabolites regulate inflammatory status and gut microbiota to repair intestinal barrier damage in dextran sulfate sodium-induced ulcerative colitis
title_fullStr Fermented Astragalus and its metabolites regulate inflammatory status and gut microbiota to repair intestinal barrier damage in dextran sulfate sodium-induced ulcerative colitis
title_full_unstemmed Fermented Astragalus and its metabolites regulate inflammatory status and gut microbiota to repair intestinal barrier damage in dextran sulfate sodium-induced ulcerative colitis
title_short Fermented Astragalus and its metabolites regulate inflammatory status and gut microbiota to repair intestinal barrier damage in dextran sulfate sodium-induced ulcerative colitis
title_sort fermented astragalus and its metabolites regulate inflammatory status and gut microbiota to repair intestinal barrier damage in dextran sulfate sodium induced ulcerative colitis
topic Astragalus
fermentation
inflammation
intestinal barrier
gut microbiota
url https://www.frontiersin.org/articles/10.3389/fnut.2022.1035912/full
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