Saccharomyces boulardii alleviates ulcerative colitis carcinogenesis in mice by reducing TNF-α and IL-6 levels and functions and by rebalancing intestinal microbiota

Abstract Background and Aims To explore the inhibition mechanism of Saccharomyces boulardii (S. boulardii) on ulcerative colitis (UC) carcinogenesis. Methods C57BL/6 mice were treated with azoxymethane and dextran sulfate sodium (AOM/DSS) to develop a UC carcinogenesis model. The treatment group was...

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Main Authors: Chunsaier Wang, Wenbin Li, Hongying Wang, Yiming Ma, Xinhua Zhao, Xudong Zhang, Hong Yang, Jiaming Qian, Jingnan Li
Format: Article
Language:English
Published: BMC 2019-11-01
Series:BMC Microbiology
Subjects:
Online Access:http://link.springer.com/article/10.1186/s12866-019-1610-8
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author Chunsaier Wang
Wenbin Li
Hongying Wang
Yiming Ma
Xinhua Zhao
Xudong Zhang
Hong Yang
Jiaming Qian
Jingnan Li
author_facet Chunsaier Wang
Wenbin Li
Hongying Wang
Yiming Ma
Xinhua Zhao
Xudong Zhang
Hong Yang
Jiaming Qian
Jingnan Li
author_sort Chunsaier Wang
collection DOAJ
description Abstract Background and Aims To explore the inhibition mechanism of Saccharomyces boulardii (S. boulardii) on ulcerative colitis (UC) carcinogenesis. Methods C57BL/6 mice were treated with azoxymethane and dextran sulfate sodium (AOM/DSS) to develop a UC carcinogenesis model. The treatment group was lavaged with S. boulardii (5 × 107 CFU/d) for 12 weeks. The mice were sacrificed and the tumor load in the treatment group was compared with that of a control group. The levels of TNF-α and IL-6 in colon tissue were measured by enzyme-linked immunosorbent assays. The influence of S. boulardii on TNF-α and IL-6 regulation was also investigated using different colon cell lines. Differences in intestinal microbiota in both stool and intestinal mucosa samples were assessed using 16S rDNA sequencing. Results S. boulardii treatment reduced AOM/DSS-induced UC carcinogenesis in mice, as indicated by the reduced tumor load and reduced TNF-α and IL-6 levels in vivo, as well its effects on TNF-α and IL-6 activities in vitro. Significant changes in both fecal and mucosal microbiota were observed among the control, the AOM/DSS treated, and AOM/DSS plus S. boulardii treated groups. For fecal microbiota, the AOM/DSS treated group was lower in Lactobacillus, but higher in Oscillibacter and Lachnoclostridium than the control group. After intervention with S. boulardii, the percentage of Bacillus and Lactococcus increased, but Lachnoclostridium, Oscillibacter, Bacteroides, and Pseudomonas decreased. For the intestinal mucosal microbiota, the AOM/DSS treated group was lower in Bifidobacterium and Ruminococcaceae_UCG-014 and higher in Alloprevotella than the control group. After S. boulardii exposure, the percentage contributions of Lachnoclostridium and Lachnospiraceae_NK4A136 increased. Conclusions S. boulardii effectively reduced UC carcinogenesis in an AOM/DSS induced mice model. This positive result can likely be attributed to the reduction of TNF-α and IL-6 levels or the blockade of their function combined with alterations to the intestinal microbiota.
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spelling doaj.art-3c8f9cc5ce544aa380db789c818b9cca2022-12-21T23:58:23ZengBMCBMC Microbiology1471-21802019-11-0119111210.1186/s12866-019-1610-8Saccharomyces boulardii alleviates ulcerative colitis carcinogenesis in mice by reducing TNF-α and IL-6 levels and functions and by rebalancing intestinal microbiotaChunsaier Wang0Wenbin Li1Hongying Wang2Yiming Ma3Xinhua Zhao4Xudong Zhang5Hong Yang6Jiaming Qian7Jingnan Li8Department of Gastroenterology, Peking Union Medical College Hospital, Chinese Academy of Medical Sciences and Peking Union Medical CollegeDepartment of Gastroenterology, Peking Union Medical College Hospital, Chinese Academy of Medical Sciences and Peking Union Medical CollegeNational Cancer Center/Cancer Hospital, Chinese Academy of Medical Sciences and Peking Union Medical CollegeNational Cancer Center/Cancer Hospital, Chinese Academy of Medical Sciences and Peking Union Medical CollegeNational Cancer Center/Cancer Hospital, Chinese Academy of Medical Sciences and Peking Union Medical CollegeSchool of Biomedical Sciences and Pharmacy, University of Newcastle, Newcastle, New Lambton HeightsDepartment of Gastroenterology, Peking Union Medical College Hospital, Chinese Academy of Medical Sciences and Peking Union Medical CollegeDepartment of Gastroenterology, Peking Union Medical College Hospital, Chinese Academy of Medical Sciences and Peking Union Medical CollegeDepartment of Gastroenterology, Peking Union Medical College Hospital, Chinese Academy of Medical Sciences and Peking Union Medical CollegeAbstract Background and Aims To explore the inhibition mechanism of Saccharomyces boulardii (S. boulardii) on ulcerative colitis (UC) carcinogenesis. Methods C57BL/6 mice were treated with azoxymethane and dextran sulfate sodium (AOM/DSS) to develop a UC carcinogenesis model. The treatment group was lavaged with S. boulardii (5 × 107 CFU/d) for 12 weeks. The mice were sacrificed and the tumor load in the treatment group was compared with that of a control group. The levels of TNF-α and IL-6 in colon tissue were measured by enzyme-linked immunosorbent assays. The influence of S. boulardii on TNF-α and IL-6 regulation was also investigated using different colon cell lines. Differences in intestinal microbiota in both stool and intestinal mucosa samples were assessed using 16S rDNA sequencing. Results S. boulardii treatment reduced AOM/DSS-induced UC carcinogenesis in mice, as indicated by the reduced tumor load and reduced TNF-α and IL-6 levels in vivo, as well its effects on TNF-α and IL-6 activities in vitro. Significant changes in both fecal and mucosal microbiota were observed among the control, the AOM/DSS treated, and AOM/DSS plus S. boulardii treated groups. For fecal microbiota, the AOM/DSS treated group was lower in Lactobacillus, but higher in Oscillibacter and Lachnoclostridium than the control group. After intervention with S. boulardii, the percentage of Bacillus and Lactococcus increased, but Lachnoclostridium, Oscillibacter, Bacteroides, and Pseudomonas decreased. For the intestinal mucosal microbiota, the AOM/DSS treated group was lower in Bifidobacterium and Ruminococcaceae_UCG-014 and higher in Alloprevotella than the control group. After S. boulardii exposure, the percentage contributions of Lachnoclostridium and Lachnospiraceae_NK4A136 increased. Conclusions S. boulardii effectively reduced UC carcinogenesis in an AOM/DSS induced mice model. This positive result can likely be attributed to the reduction of TNF-α and IL-6 levels or the blockade of their function combined with alterations to the intestinal microbiota.http://link.springer.com/article/10.1186/s12866-019-1610-8Ulcerative colitis carcinogenesisTNF-αIL-6Saccharomyces boulardiiIntestinal microbiota
spellingShingle Chunsaier Wang
Wenbin Li
Hongying Wang
Yiming Ma
Xinhua Zhao
Xudong Zhang
Hong Yang
Jiaming Qian
Jingnan Li
Saccharomyces boulardii alleviates ulcerative colitis carcinogenesis in mice by reducing TNF-α and IL-6 levels and functions and by rebalancing intestinal microbiota
BMC Microbiology
Ulcerative colitis carcinogenesis
TNF-α
IL-6
Saccharomyces boulardii
Intestinal microbiota
title Saccharomyces boulardii alleviates ulcerative colitis carcinogenesis in mice by reducing TNF-α and IL-6 levels and functions and by rebalancing intestinal microbiota
title_full Saccharomyces boulardii alleviates ulcerative colitis carcinogenesis in mice by reducing TNF-α and IL-6 levels and functions and by rebalancing intestinal microbiota
title_fullStr Saccharomyces boulardii alleviates ulcerative colitis carcinogenesis in mice by reducing TNF-α and IL-6 levels and functions and by rebalancing intestinal microbiota
title_full_unstemmed Saccharomyces boulardii alleviates ulcerative colitis carcinogenesis in mice by reducing TNF-α and IL-6 levels and functions and by rebalancing intestinal microbiota
title_short Saccharomyces boulardii alleviates ulcerative colitis carcinogenesis in mice by reducing TNF-α and IL-6 levels and functions and by rebalancing intestinal microbiota
title_sort saccharomyces boulardii alleviates ulcerative colitis carcinogenesis in mice by reducing tnf α and il 6 levels and functions and by rebalancing intestinal microbiota
topic Ulcerative colitis carcinogenesis
TNF-α
IL-6
Saccharomyces boulardii
Intestinal microbiota
url http://link.springer.com/article/10.1186/s12866-019-1610-8
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