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      Qingchang Wenzhong Decoction Accelerates Intestinal Mucosal Healing Through Modulation of Dysregulated Gut Microbiome, Intestinal Barrier and Immune Responses in Mice

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          Abstract

          Inflammatory bowel disease (IBD), a group of multifactorial and inflammatory infirmities, is closely associated with dysregulation of gut microbiota and host metabolome, but effective treatments are currently limited. Qingchang Wenzhong Decoction (QCWZD) is an effective and classical traditional herbal prescription for the treatment of IBD and has been proved to attenuate intestinal inflammation in a model of acute colitis. However, the role of QCWZD in recovery phase of colitis is unclear. Here, we demonstrated that mice treated with QCWZD showed a faster recovery from dextran sulfate sodium (DSS)-induced epithelial injury, accompanied by reduced mucosal inflammation and attenuated intestinal dysbiosis using bacterial 16S rRNA amplicon sequencing compared to those receiving sterile water. The protective effects of QCWZD are gut microbiota dependent, as demonstrated by fecal microbiome transplantation and antibiotics treatment. Gut microbes transferred from QCWZD-treated mice displayed a similar role in mucosal protection and epithelial regeneration as QCWZD on colitis in mice, and depletion of the gut microbiota through antibiotics treatments diminished the beneficial effects of QCWZD on colitis mice. Moreover, metabolomic analysis revealed metabolic profiles alternations in response to the gut microbiota reprogrammed by QCWZD intervention, especially enhanced tryptophan metabolism, which may further accelerate intestinal stem cells-mediated epithelial regeneration to protect the integrity of intestinal mucosa through activation of Wnt/β-catenin signals. Collectively, our results suggested that orally administrated QCWZD accelerates intestinal mucosal healing through the modulation of dysregulated gut microbiota and metabolism, thus regulating intestinal stem cells-mediated epithelial proliferation, and hold promise for novel microbial-based therapies in the treatment of IBD.

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          Most cited references54

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          Worldwide incidence and prevalence of inflammatory bowel disease in the 21st century: a systematic review of population-based studies.

          Inflammatory bowel disease is a global disease in the 21st century. We aimed to assess the changing incidence and prevalence of inflammatory bowel disease around the world.
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            Single Lgr5 stem cells build crypt-villus structures in vitro without a mesenchymal niche.

            The intestinal epithelium is the most rapidly self-renewing tissue in adult mammals. We have recently demonstrated the presence of about six cycling Lgr5(+) stem cells at the bottoms of small-intestinal crypts. Here we describe the establishment of long-term culture conditions under which single crypts undergo multiple crypt fission events, while simultanously generating villus-like epithelial domains in which all differentiated cell types are present. Single sorted Lgr5(+) stem cells can also initiate these cryptvillus organoids. Tracing experiments indicate that the Lgr5(+) stem-cell hierarchy is maintained in organoids. We conclude that intestinal cryptvillus units are self-organizing structures, which can be built from a single stem cell in the absence of a non-epithelial cellular niche.
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              Ulcerative colitis

              Ulcerative colitis is a chronic inflammatory disease affecting the colon, and its incidence is rising worldwide. The pathogenesis is multifactorial, involving genetic predisposition, epithelial barrier defects, dysregulated immune responses, and environmental factors. Patients with ulcerative colitis have mucosal inflammation starting in the rectum that can extend continuously to proximal segments of the colon. Ulcerative colitis usually presents with bloody diarrhoea and is diagnosed by colonoscopy and histological findings. The aim of management is to induce and then maintain remission, defined as resolution of symptoms and endoscopic healing. Treatments for ulcerative colitis include 5-aminosalicylic acid drugs, steroids, and immunosuppressants. Some patients can require colectomy for medically refractory disease or to treat colonic neoplasia. The therapeutic armamentarium for ulcerative colitis is expanding, and the number of drugs with new targets will rapidly increase in coming years.
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                Author and article information

                Contributors
                Journal
                Front Pharmacol
                Front Pharmacol
                Front. Pharmacol.
                Frontiers in Pharmacology
                Frontiers Media S.A.
                1663-9812
                07 September 2021
                2021
                : 12
                : 738152
                Affiliations
                [ 1 ]Department of Gastroenterology, Dongfang Hospital, Beijing University of Chinese Medicine, Beijing, China
                [ 2 ]Graduate School, Beijing University of Chinese Medicine, Beijing, China
                [ 3 ]Department of Traditional Chinese Medicine, Beijing Yangfangdian Hospital, Beijing, China
                [ 4 ]Department of Pathology, Dongfang Hospital, Beijing University of Chinese Medicine, Beijing, China
                [ 5 ]School of Chinese Materia Medica, Beijing University of Chinese Medicine, Beijing, China
                [ 6 ]Dongzhimen Hospital, Beijing University of Chinese Medicine, Beijing, China
                Author notes

                Edited by: Ralf Weiskirchen, RWTH Aachen University, Germany

                Reviewed by: Thomson Patrick Joseph, Laval University, Canada

                Helioswilton Sales-Campos, Universidade Federal de Goiás, Brazil

                Hao-Sen Chiang, National Taiwan University, Taiwan

                *Correspondence: Tangyou Mao, maotangyouqun@ 123456126.com
                [†]

                These authors have contributed equally to this work

                This article was submitted to Gastrointestinal and Hepatic Pharmacology, a section of the journal Frontiers in Pharmacology

                Article
                738152
                10.3389/fphar.2021.738152
                8452913
                34557102
                a5832b61-98f1-4969-baa9-0a9397c9d3b1
                Copyright © 2021 Sun, Li, Wang, Liu, Liu, Jiang, Lu, Ding, Shi, Zhao, Yuan, Tan, Shi, Xing and Mao.

                This is an open-access article distributed under the terms of the Creative Commons Attribution License (CC BY). The use, distribution or reproduction in other forums is permitted, provided the original author(s) and the copyright owner(s) are credited and that the original publication in this journal is cited, in accordance with accepted academic practice. No use, distribution or reproduction is permitted which does not comply with these terms.

                History
                : 08 July 2021
                : 24 August 2021
                Funding
                Funded by: National Natural Science Foundation of China - State Grid Corporation Joint Fund for Smart Grid 10.13039/501100019491
                Award ID: 81903990
                Categories
                Pharmacology
                Original Research

                Pharmacology & Pharmaceutical medicine
                inflammatory bowel disease,qingchang wenzhong decoction,mucosal healing,gut microbiota,tryptophan metabolism,intestinal stem cells

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