Maternal gestational Bifidobacterium bifidum TMC3115 treatment shapes construction of offspring gut microbiota and development of immune system and induces immune tolerance to food allergen

In this study we aimed to determine whether treatment with maternal Bifidobacterium bifidum TMC3115 could affect the composition of the gut microbiota and the development of the immune system and intestinal tract of offspring, and protect the offspring from IgE-mediated allergic disease. Pregnant BA...

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Main Authors: Ruyue Cheng, Yujie Zhang, Yang Yang, Lei Ren, Jinxing Li, Yimei Wang, Xi Shen, Fang He
Format: Article
Language:English
Published: Frontiers Media S.A. 2022-11-01
Series:Frontiers in Cellular and Infection Microbiology
Subjects:
Online Access:https://www.frontiersin.org/articles/10.3389/fcimb.2022.1045109/full
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author Ruyue Cheng
Yujie Zhang
Yang Yang
Lei Ren
Jinxing Li
Yimei Wang
Xi Shen
Fang He
author_facet Ruyue Cheng
Yujie Zhang
Yang Yang
Lei Ren
Jinxing Li
Yimei Wang
Xi Shen
Fang He
author_sort Ruyue Cheng
collection DOAJ
description In this study we aimed to determine whether treatment with maternal Bifidobacterium bifidum TMC3115 could affect the composition of the gut microbiota and the development of the immune system and intestinal tract of offspring, and protect the offspring from IgE-mediated allergic disease. Pregnant BALB/c mice were gavaged with TMC3115 until delivery. Offspring were sensitized with ovalbumin from postnatal days 21 to 49. After maternal treatment with TMC3115, the microbiota of the offspring’s feces, intestinal contents, and stomach contents (a proxy for breast milk) at the newborn and weaning stages exhibited the most change, and levels of immunoglobulin in the sera and stomach contents and of splenic cytokines, as well as the mRNA levels of colonic intestinal development indicators were all significantly altered in offspring at different stages. After sensitization with ovalbumin, there were no significant changes in the levels of serum IgE or ovalbumin-specific IgE/IgG1 in the TMC3115 group; however, IgM, the expression of intestinal development indicators, and the production of fecal short chain fatty acid (SCFA) were significantly increased, as were the relative abundances of Lactobacillus and the Lachnospiraceae NK4A136 group. Our results suggested that maternal treatment with TMC3115 could have a profound modulatory effect on the composition of the gut microbiota and the development of the immune system and intestinal tissue in offspring at different stages of development, and may induce immune tolerance to allergens in ovalbumin-stimulated offspring by modulating the gut microbiota and SCFA production.
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spelling doaj.art-caf41026d49746b28d3a98b0640dd3272022-12-22T04:16:06ZengFrontiers Media S.A.Frontiers in Cellular and Infection Microbiology2235-29882022-11-011210.3389/fcimb.2022.10451091045109Maternal gestational Bifidobacterium bifidum TMC3115 treatment shapes construction of offspring gut microbiota and development of immune system and induces immune tolerance to food allergenRuyue Cheng0Yujie Zhang1Yang Yang2Lei Ren3Jinxing Li4Yimei Wang5Xi Shen6Fang He7Department of Nutrition and Food Hygiene, West China School of Public Health and West China Fourth Hospital, Sichuan University, Chengdu, Sichuan, ChinaDepartment of Nutrition and Food Hygiene, West China School of Public Health and West China Fourth Hospital, Sichuan University, Chengdu, Sichuan, ChinaDepartment of Nutrition and Food Hygiene, West China School of Public Health and West China Fourth Hospital, Sichuan University, Chengdu, Sichuan, ChinaDepartment of Research and Development, Hebei Inatural Bio-tech Co., Ltd, Shijiazhuang, Hebei, ChinaDepartment of Nutrition and Food Hygiene, West China School of Public Health and West China Fourth Hospital, Sichuan University, Chengdu, Sichuan, ChinaDepartment of Nutrition and Food Hygiene, West China School of Public Health and West China Fourth Hospital, Sichuan University, Chengdu, Sichuan, ChinaDepartment of Nutrition and Food Hygiene, West China School of Public Health and West China Fourth Hospital, Sichuan University, Chengdu, Sichuan, ChinaDepartment of Nutrition and Food Hygiene, West China School of Public Health and West China Fourth Hospital, Sichuan University, Chengdu, Sichuan, ChinaIn this study we aimed to determine whether treatment with maternal Bifidobacterium bifidum TMC3115 could affect the composition of the gut microbiota and the development of the immune system and intestinal tract of offspring, and protect the offspring from IgE-mediated allergic disease. Pregnant BALB/c mice were gavaged with TMC3115 until delivery. Offspring were sensitized with ovalbumin from postnatal days 21 to 49. After maternal treatment with TMC3115, the microbiota of the offspring’s feces, intestinal contents, and stomach contents (a proxy for breast milk) at the newborn and weaning stages exhibited the most change, and levels of immunoglobulin in the sera and stomach contents and of splenic cytokines, as well as the mRNA levels of colonic intestinal development indicators were all significantly altered in offspring at different stages. After sensitization with ovalbumin, there were no significant changes in the levels of serum IgE or ovalbumin-specific IgE/IgG1 in the TMC3115 group; however, IgM, the expression of intestinal development indicators, and the production of fecal short chain fatty acid (SCFA) were significantly increased, as were the relative abundances of Lactobacillus and the Lachnospiraceae NK4A136 group. Our results suggested that maternal treatment with TMC3115 could have a profound modulatory effect on the composition of the gut microbiota and the development of the immune system and intestinal tissue in offspring at different stages of development, and may induce immune tolerance to allergens in ovalbumin-stimulated offspring by modulating the gut microbiota and SCFA production.https://www.frontiersin.org/articles/10.3389/fcimb.2022.1045109/fullallergyBifidobacteriumgut microbiotaimmune functionSCFA
spellingShingle Ruyue Cheng
Yujie Zhang
Yang Yang
Lei Ren
Jinxing Li
Yimei Wang
Xi Shen
Fang He
Maternal gestational Bifidobacterium bifidum TMC3115 treatment shapes construction of offspring gut microbiota and development of immune system and induces immune tolerance to food allergen
Frontiers in Cellular and Infection Microbiology
allergy
Bifidobacterium
gut microbiota
immune function
SCFA
title Maternal gestational Bifidobacterium bifidum TMC3115 treatment shapes construction of offspring gut microbiota and development of immune system and induces immune tolerance to food allergen
title_full Maternal gestational Bifidobacterium bifidum TMC3115 treatment shapes construction of offspring gut microbiota and development of immune system and induces immune tolerance to food allergen
title_fullStr Maternal gestational Bifidobacterium bifidum TMC3115 treatment shapes construction of offspring gut microbiota and development of immune system and induces immune tolerance to food allergen
title_full_unstemmed Maternal gestational Bifidobacterium bifidum TMC3115 treatment shapes construction of offspring gut microbiota and development of immune system and induces immune tolerance to food allergen
title_short Maternal gestational Bifidobacterium bifidum TMC3115 treatment shapes construction of offspring gut microbiota and development of immune system and induces immune tolerance to food allergen
title_sort maternal gestational bifidobacterium bifidum tmc3115 treatment shapes construction of offspring gut microbiota and development of immune system and induces immune tolerance to food allergen
topic allergy
Bifidobacterium
gut microbiota
immune function
SCFA
url https://www.frontiersin.org/articles/10.3389/fcimb.2022.1045109/full
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