Understanding the tonifying and the detoxifying properties of Chinese medicines from their impacts on gut microbiota and host metabolism: a case study with four medicinal herbs in experimental colitis rat model

Abstract Background Chinese medicines (CMs) have emerged as an alternative therapy for ulcerative colitis through reinforcing the vital qi and/or eliminating the pathogenic factors according to the traditional Chinese medicinal theory. Presystemic interactions of CMs with gut microbiota and the asso...

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Main Authors: Ting Li, Xuejiao Gao, Zhixiang Yan, Tai-Seng Wai, Wei Yang, Junru Chen, Ru Yan
Format: Article
Language:English
Published: BMC 2022-10-01
Series:Chinese Medicine
Subjects:
Online Access:https://doi.org/10.1186/s13020-022-00673-w
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author Ting Li
Xuejiao Gao
Zhixiang Yan
Tai-Seng Wai
Wei Yang
Junru Chen
Ru Yan
author_facet Ting Li
Xuejiao Gao
Zhixiang Yan
Tai-Seng Wai
Wei Yang
Junru Chen
Ru Yan
author_sort Ting Li
collection DOAJ
description Abstract Background Chinese medicines (CMs) have emerged as an alternative therapy for ulcerative colitis through reinforcing the vital qi and/or eliminating the pathogenic factors according to the traditional Chinese medicinal theory. Presystemic interactions of CMs with gut microbiota and the associated metabolic network shift are believed to be essential to achieve their holistic health benefits in traditional oral application. Methods This study first employed 16S rDNA-based microbial profiling and mass spectrometry-based urinary metabolomics to simultaneously evaluate four single CMs frequently prescribed as main constituent herbs for alleviating UC, the tonic ginseng and Astragali Radix (AR) and the detoxifying Scutellaria Radix (SR) and Rhubarb, on a dextran sodium sulfate (DSS)-induced colitis rat model, with aims to understanding the tonifying or detoxifying properties of CMs through clinical phenotypes, the common features and herb-specific signatures in gut microbial alterations and the associated host metabolic shifts. Colitis was induced in rats receiving 5% DSS for consecutive 7 days. Control group received water alone. Herbal groups received 5% DSS and respective herbal preparation by gavage once daily. Body weight, stool consistency, and rectal bleeding were recorded daily. Feces and urine were freshly collected at multiple time points. On day 7, blood and colon tissues were collected to determine anti-/pro-inflammatory cytokines levels, colonic myeloperoxidase activity, and histopathologic alterations. Results Gut microbiome was more prone to herb intervention than metabolome and displayed increasing associations with metabolic dynamics. Although both the tonic and the detoxifying herbs alleviated colitis and caused some similar changes in DSS-induced microbiome and metabolome disturbance, the tonic herbs were more effective and shared more common microbial and metabolic signatures. The detoxifying herbs elicited herb-specific changes. Rhubarb uniquely affected phenylalanine metabolism and established high correlations between Akkermansia muciniphila and Parasutterella and hydroxyphenylacetylglycine and phenylbutyrylglycine, while SR caused significant elevation of steroidal glucuronides dehydropregnenolone glucuronide and estriol glucuronide, both displaying exclusive correlations with genus Acetatifactor. Conclusion Both tonic and detoxifying herbs tested ameliorated experimental colitis and elicited alternative microbial and host metabolic reprogramming. The findings highlight the importance of presystemic interactions with gut microbiota to host metabolic shifts and promote modern translation of tonic and detoxifying properties of CMs.
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spelling doaj.art-27ac5458287b4007bfa247216e1020b22023-09-03T11:25:09ZengBMCChinese Medicine1749-85462022-10-0117111710.1186/s13020-022-00673-wUnderstanding the tonifying and the detoxifying properties of Chinese medicines from their impacts on gut microbiota and host metabolism: a case study with four medicinal herbs in experimental colitis rat modelTing Li0Xuejiao Gao1Zhixiang Yan2Tai-Seng Wai3Wei Yang4Junru Chen5Ru Yan6State Key Laboratory of Quality Research in Chinese Medicine, Institute of Chinese Medical Sciences, University of MacauState Key Laboratory of Quality Research in Chinese Medicine, Institute of Chinese Medical Sciences, University of MacauState Key Laboratory of Quality Research in Chinese Medicine, Institute of Chinese Medical Sciences, University of MacauState Key Laboratory of Quality Research in Chinese Medicine, Institute of Chinese Medical Sciences, University of MacauState Key Laboratory of Quality Research in Chinese Medicine, Institute of Chinese Medical Sciences, University of MacauState Key Laboratory of Quality Research in Chinese Medicine, Institute of Chinese Medical Sciences, University of MacauState Key Laboratory of Quality Research in Chinese Medicine, Institute of Chinese Medical Sciences, University of MacauAbstract Background Chinese medicines (CMs) have emerged as an alternative therapy for ulcerative colitis through reinforcing the vital qi and/or eliminating the pathogenic factors according to the traditional Chinese medicinal theory. Presystemic interactions of CMs with gut microbiota and the associated metabolic network shift are believed to be essential to achieve their holistic health benefits in traditional oral application. Methods This study first employed 16S rDNA-based microbial profiling and mass spectrometry-based urinary metabolomics to simultaneously evaluate four single CMs frequently prescribed as main constituent herbs for alleviating UC, the tonic ginseng and Astragali Radix (AR) and the detoxifying Scutellaria Radix (SR) and Rhubarb, on a dextran sodium sulfate (DSS)-induced colitis rat model, with aims to understanding the tonifying or detoxifying properties of CMs through clinical phenotypes, the common features and herb-specific signatures in gut microbial alterations and the associated host metabolic shifts. Colitis was induced in rats receiving 5% DSS for consecutive 7 days. Control group received water alone. Herbal groups received 5% DSS and respective herbal preparation by gavage once daily. Body weight, stool consistency, and rectal bleeding were recorded daily. Feces and urine were freshly collected at multiple time points. On day 7, blood and colon tissues were collected to determine anti-/pro-inflammatory cytokines levels, colonic myeloperoxidase activity, and histopathologic alterations. Results Gut microbiome was more prone to herb intervention than metabolome and displayed increasing associations with metabolic dynamics. Although both the tonic and the detoxifying herbs alleviated colitis and caused some similar changes in DSS-induced microbiome and metabolome disturbance, the tonic herbs were more effective and shared more common microbial and metabolic signatures. The detoxifying herbs elicited herb-specific changes. Rhubarb uniquely affected phenylalanine metabolism and established high correlations between Akkermansia muciniphila and Parasutterella and hydroxyphenylacetylglycine and phenylbutyrylglycine, while SR caused significant elevation of steroidal glucuronides dehydropregnenolone glucuronide and estriol glucuronide, both displaying exclusive correlations with genus Acetatifactor. Conclusion Both tonic and detoxifying herbs tested ameliorated experimental colitis and elicited alternative microbial and host metabolic reprogramming. The findings highlight the importance of presystemic interactions with gut microbiota to host metabolic shifts and promote modern translation of tonic and detoxifying properties of CMs.https://doi.org/10.1186/s13020-022-00673-wChinese medicinesTonic herbDetoxifying herbExperimental colitisGut microbiotaHost metabolism
spellingShingle Ting Li
Xuejiao Gao
Zhixiang Yan
Tai-Seng Wai
Wei Yang
Junru Chen
Ru Yan
Understanding the tonifying and the detoxifying properties of Chinese medicines from their impacts on gut microbiota and host metabolism: a case study with four medicinal herbs in experimental colitis rat model
Chinese Medicine
Chinese medicines
Tonic herb
Detoxifying herb
Experimental colitis
Gut microbiota
Host metabolism
title Understanding the tonifying and the detoxifying properties of Chinese medicines from their impacts on gut microbiota and host metabolism: a case study with four medicinal herbs in experimental colitis rat model
title_full Understanding the tonifying and the detoxifying properties of Chinese medicines from their impacts on gut microbiota and host metabolism: a case study with four medicinal herbs in experimental colitis rat model
title_fullStr Understanding the tonifying and the detoxifying properties of Chinese medicines from their impacts on gut microbiota and host metabolism: a case study with four medicinal herbs in experimental colitis rat model
title_full_unstemmed Understanding the tonifying and the detoxifying properties of Chinese medicines from their impacts on gut microbiota and host metabolism: a case study with four medicinal herbs in experimental colitis rat model
title_short Understanding the tonifying and the detoxifying properties of Chinese medicines from their impacts on gut microbiota and host metabolism: a case study with four medicinal herbs in experimental colitis rat model
title_sort understanding the tonifying and the detoxifying properties of chinese medicines from their impacts on gut microbiota and host metabolism a case study with four medicinal herbs in experimental colitis rat model
topic Chinese medicines
Tonic herb
Detoxifying herb
Experimental colitis
Gut microbiota
Host metabolism
url https://doi.org/10.1186/s13020-022-00673-w
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