Prebiotic Supplementation During Gestation Induces a Tolerogenic Environment and a Protective Microbiota in Offspring Mitigating Food Allergy

Food allergy is associated with alterations in the gut microbiota, epithelial barrier, and immune tolerance. These dysfunctions are observed within the first months of life, indicating that early intervention is crucial for disease prevention. Preventive nutritional strategies with prebiotics are an...

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Main Authors: Amandine Selle, Carole Brosseau, Wieneke Dijk, Angéline Duval, Grégory Bouchaud, Anais Rousseaux, Aurélia Bruneau, Claire Cherbuy, Mahendra Mariadassou, Véronique Cariou, Sebastien Barbarot, Marie Bodinier
Format: Article
Language:English
Published: Frontiers Media S.A. 2022-01-01
Series:Frontiers in Immunology
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Online Access:https://www.frontiersin.org/articles/10.3389/fimmu.2021.745535/full
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author Amandine Selle
Carole Brosseau
Wieneke Dijk
Angéline Duval
Grégory Bouchaud
Anais Rousseaux
Aurélia Bruneau
Claire Cherbuy
Mahendra Mariadassou
Véronique Cariou
Sebastien Barbarot
Sebastien Barbarot
Marie Bodinier
author_facet Amandine Selle
Carole Brosseau
Wieneke Dijk
Angéline Duval
Grégory Bouchaud
Anais Rousseaux
Aurélia Bruneau
Claire Cherbuy
Mahendra Mariadassou
Véronique Cariou
Sebastien Barbarot
Sebastien Barbarot
Marie Bodinier
author_sort Amandine Selle
collection DOAJ
description Food allergy is associated with alterations in the gut microbiota, epithelial barrier, and immune tolerance. These dysfunctions are observed within the first months of life, indicating that early intervention is crucial for disease prevention. Preventive nutritional strategies with prebiotics are an attractive option, as prebiotics such as galacto-oligosaccharides and inulin can promote tolerance, epithelial barrier reinforcement, and gut microbiota modulation. Nonetheless, the ideal period for intervention remains unknown. Here, we investigated whether galacto-oligosaccharide/inulin supplementation during gestation could protect offspring from wheat allergy development in BALB/cJRj mice. We demonstrated that gestational prebiotic supplementation promoted the presence of beneficial strains in the fecal microbiota of dams during gestation and partially during mid-lactation. This specific microbiota was transferred to their offspring and maintained to adulthood. The presence of B and T regulatory immune cell subsets was also increased in the lymph nodes of offspring born from supplemented mothers, suggestive of a more tolerogenic immune environment. Indeed, antenatal prebiotic supplementation reduced the development of wheat allergy symptoms in offspring. Our study thus demonstrates that prebiotic supplementation during pregnancy induces, in the offspring, a tolerogenic environment and a microbial imprint that mitigates food allergy development.
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spelling doaj.art-353848a6665a4f978d69d365ddcf18812022-12-22T04:04:11ZengFrontiers Media S.A.Frontiers in Immunology1664-32242022-01-011210.3389/fimmu.2021.745535745535Prebiotic Supplementation During Gestation Induces a Tolerogenic Environment and a Protective Microbiota in Offspring Mitigating Food AllergyAmandine Selle0Carole Brosseau1Wieneke Dijk2Angéline Duval3Grégory Bouchaud4Anais Rousseaux5Aurélia Bruneau6Claire Cherbuy7Mahendra Mariadassou8Véronique Cariou9Sebastien Barbarot10Sebastien Barbarot11Marie Bodinier12Institut National de Recherche pour l’Agriculture, l’alimentation et l’Environnement (INRAE), UR1268 Biopolymères Interactions Assemblages (BIA), Nantes, FranceInstitut National de Recherche pour l’Agriculture, l’alimentation et l’Environnement (INRAE), UR1268 Biopolymères Interactions Assemblages (BIA), Nantes, FranceInstitut National de Recherche pour l’Agriculture, l’alimentation et l’Environnement (INRAE), UR1268 Biopolymères Interactions Assemblages (BIA), Nantes, FranceInstitut National de Recherche pour l’Agriculture, l’alimentation et l’Environnement (INRAE), UR1268 Biopolymères Interactions Assemblages (BIA), Nantes, FranceInstitut National de Recherche pour l’Agriculture, l’alimentation et l’Environnement (INRAE), UR1268 Biopolymères Interactions Assemblages (BIA), Nantes, FranceInstitut National de Recherche pour l’Agriculture, l’alimentation et l’Environnement (INRAE), UR1268 Biopolymères Interactions Assemblages (BIA), Nantes, FranceMicalis Institute, Institut National de Recherche pour l’Agriculture, l’alimentation et l’Environnement (INRAE), AgroParisTech, Université Paris-Saclay, Jouy-en-Josas, FranceMicalis Institute, Institut National de Recherche pour l’Agriculture, l’alimentation et l’Environnement (INRAE), AgroParisTech, Université Paris-Saclay, Jouy-en-Josas, FranceMaIAGE, UR1404, Institut National de Recherche pour l’Agriculture, l’alimentation et l’Environnement (INRAE), Jouy-en-Josas, FranceStatSC, École nationale vétérinaire, agroalimentaire et de l'alimentation de Nantes-Atlantique (ONIRIS), Institut National de Recherche pour l’Agriculture, l’alimentation et l’Environnement (INRAE), Nantes, FranceDepartment of Dermatology, Centre Hospitalier Universitaire (CHU) Nantes, Nantes, FranceInstitut National de Recherche pour l’Agriculture, l’alimentation et l’Environnement (INRAE) Pays de la Loire, UMR1280 PhAN, Nantes, FranceInstitut National de Recherche pour l’Agriculture, l’alimentation et l’Environnement (INRAE), UR1268 Biopolymères Interactions Assemblages (BIA), Nantes, FranceFood allergy is associated with alterations in the gut microbiota, epithelial barrier, and immune tolerance. These dysfunctions are observed within the first months of life, indicating that early intervention is crucial for disease prevention. Preventive nutritional strategies with prebiotics are an attractive option, as prebiotics such as galacto-oligosaccharides and inulin can promote tolerance, epithelial barrier reinforcement, and gut microbiota modulation. Nonetheless, the ideal period for intervention remains unknown. Here, we investigated whether galacto-oligosaccharide/inulin supplementation during gestation could protect offspring from wheat allergy development in BALB/cJRj mice. We demonstrated that gestational prebiotic supplementation promoted the presence of beneficial strains in the fecal microbiota of dams during gestation and partially during mid-lactation. This specific microbiota was transferred to their offspring and maintained to adulthood. The presence of B and T regulatory immune cell subsets was also increased in the lymph nodes of offspring born from supplemented mothers, suggestive of a more tolerogenic immune environment. Indeed, antenatal prebiotic supplementation reduced the development of wheat allergy symptoms in offspring. Our study thus demonstrates that prebiotic supplementation during pregnancy induces, in the offspring, a tolerogenic environment and a microbial imprint that mitigates food allergy development.https://www.frontiersin.org/articles/10.3389/fimmu.2021.745535/fullfood allergygut microbiotaimmune toleranceprebioticspregnancy
spellingShingle Amandine Selle
Carole Brosseau
Wieneke Dijk
Angéline Duval
Grégory Bouchaud
Anais Rousseaux
Aurélia Bruneau
Claire Cherbuy
Mahendra Mariadassou
Véronique Cariou
Sebastien Barbarot
Sebastien Barbarot
Marie Bodinier
Prebiotic Supplementation During Gestation Induces a Tolerogenic Environment and a Protective Microbiota in Offspring Mitigating Food Allergy
Frontiers in Immunology
food allergy
gut microbiota
immune tolerance
prebiotics
pregnancy
title Prebiotic Supplementation During Gestation Induces a Tolerogenic Environment and a Protective Microbiota in Offspring Mitigating Food Allergy
title_full Prebiotic Supplementation During Gestation Induces a Tolerogenic Environment and a Protective Microbiota in Offspring Mitigating Food Allergy
title_fullStr Prebiotic Supplementation During Gestation Induces a Tolerogenic Environment and a Protective Microbiota in Offspring Mitigating Food Allergy
title_full_unstemmed Prebiotic Supplementation During Gestation Induces a Tolerogenic Environment and a Protective Microbiota in Offspring Mitigating Food Allergy
title_short Prebiotic Supplementation During Gestation Induces a Tolerogenic Environment and a Protective Microbiota in Offspring Mitigating Food Allergy
title_sort prebiotic supplementation during gestation induces a tolerogenic environment and a protective microbiota in offspring mitigating food allergy
topic food allergy
gut microbiota
immune tolerance
prebiotics
pregnancy
url https://www.frontiersin.org/articles/10.3389/fimmu.2021.745535/full
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