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Maternal prebiotic supplementation impacts colitis development in offspring mice

BACKGROUND AND AIMS: Maternal diet plays a key role in preventing or contributing to the development of chronic diseases, such as obesity, allergy, and brain disorders. Supplementation of maternal diet with prebiotics has been shown to reduce the risk of food allergies and affect the intestinal perm...

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Autores principales: Lê, Amélie, Selle, Amandine, Aubert, Philippe, Durand, Tony, Brosseau, Carole, Bordron, Philippe, Delage, Erwan, Chaffron, Samuel, Petitfils, Camille, Cenac, Nicolas, Neunlist, Michel, Bodinier, Marie, Rolli-Derkinderen, Malvyne
Formato: Online Artículo Texto
Lenguaje:English
Publicado: Frontiers Media S.A. 2023
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC9849907/
https://www.ncbi.nlm.nih.gov/pubmed/36687706
http://dx.doi.org/10.3389/fnut.2022.988529
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author Lê, Amélie
Selle, Amandine
Aubert, Philippe
Durand, Tony
Brosseau, Carole
Bordron, Philippe
Delage, Erwan
Chaffron, Samuel
Petitfils, Camille
Cenac, Nicolas
Neunlist, Michel
Bodinier, Marie
Rolli-Derkinderen, Malvyne
author_facet Lê, Amélie
Selle, Amandine
Aubert, Philippe
Durand, Tony
Brosseau, Carole
Bordron, Philippe
Delage, Erwan
Chaffron, Samuel
Petitfils, Camille
Cenac, Nicolas
Neunlist, Michel
Bodinier, Marie
Rolli-Derkinderen, Malvyne
author_sort Lê, Amélie
collection PubMed
description BACKGROUND AND AIMS: Maternal diet plays a key role in preventing or contributing to the development of chronic diseases, such as obesity, allergy, and brain disorders. Supplementation of maternal diet with prebiotics has been shown to reduce the risk of food allergies and affect the intestinal permeability in offspring later in life. However, its role in modulating the development of other intestinal disorders, such as colitis, remains unknown. Therefore, we investigated the effects of prebiotic supplementation in pregnant mice on the occurrence of colitis in their offspring. MATERIALS AND METHODS: Offspring from mothers, who were administered prebiotic galacto-oligosaccharides and inulin during gestation or fed a control diet, were subjected to three cycles of dextran sulphate sodium (DSS) treatment to induce chronic colitis, and their intestinal function and disease activity were evaluated. Colonic remodelling, gut microbiota composition, and lipidomic and transcriptomic profiles were also assessed. RESULTS: DSS-treated offspring from prebiotic-fed mothers presented a higher disease score, increased weight loss, and increased faecal humidity than those from standard diet-fed mothers. DSS-treated offspring from prebiotic-fed mothers also showed increased number of colonic mucosal lymphocytes and macrophages than the control group, associated with the increased colonic concentrations of resolvin D5, protectin DX, and 14-hydroxydocosahexaenoic acid, and modulation of colonic gene expression. In addition, maternal prebiotic supplementation induced an overabundance of eight bacterial families and a decrease in the butyrate caecal concentration in DSS-treated offspring. CONCLUSION: Maternal prebiotic exposure modified the microbiota composition and function, lipid content, and transcriptome of the colon of the offspring. These modifications did not protect against colitis, but rather sensitised the mice to colitis development.
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spelling pubmed-98499072023-01-20 Maternal prebiotic supplementation impacts colitis development in offspring mice Lê, Amélie Selle, Amandine Aubert, Philippe Durand, Tony Brosseau, Carole Bordron, Philippe Delage, Erwan Chaffron, Samuel Petitfils, Camille Cenac, Nicolas Neunlist, Michel Bodinier, Marie Rolli-Derkinderen, Malvyne Front Nutr Nutrition BACKGROUND AND AIMS: Maternal diet plays a key role in preventing or contributing to the development of chronic diseases, such as obesity, allergy, and brain disorders. Supplementation of maternal diet with prebiotics has been shown to reduce the risk of food allergies and affect the intestinal permeability in offspring later in life. However, its role in modulating the development of other intestinal disorders, such as colitis, remains unknown. Therefore, we investigated the effects of prebiotic supplementation in pregnant mice on the occurrence of colitis in their offspring. MATERIALS AND METHODS: Offspring from mothers, who were administered prebiotic galacto-oligosaccharides and inulin during gestation or fed a control diet, were subjected to three cycles of dextran sulphate sodium (DSS) treatment to induce chronic colitis, and their intestinal function and disease activity were evaluated. Colonic remodelling, gut microbiota composition, and lipidomic and transcriptomic profiles were also assessed. RESULTS: DSS-treated offspring from prebiotic-fed mothers presented a higher disease score, increased weight loss, and increased faecal humidity than those from standard diet-fed mothers. DSS-treated offspring from prebiotic-fed mothers also showed increased number of colonic mucosal lymphocytes and macrophages than the control group, associated with the increased colonic concentrations of resolvin D5, protectin DX, and 14-hydroxydocosahexaenoic acid, and modulation of colonic gene expression. In addition, maternal prebiotic supplementation induced an overabundance of eight bacterial families and a decrease in the butyrate caecal concentration in DSS-treated offspring. CONCLUSION: Maternal prebiotic exposure modified the microbiota composition and function, lipid content, and transcriptome of the colon of the offspring. These modifications did not protect against colitis, but rather sensitised the mice to colitis development. Frontiers Media S.A. 2023-01-05 /pmc/articles/PMC9849907/ /pubmed/36687706 http://dx.doi.org/10.3389/fnut.2022.988529 Text en Copyright © 2023 Lê, Selle, Aubert, Durand, Brosseau, Bordron, Delage, Chaffron, Petitfils, Cenac, Neunlist, Bodinier and Rolli-Derkinderen. https://creativecommons.org/licenses/by/4.0/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.
spellingShingle Nutrition
Lê, Amélie
Selle, Amandine
Aubert, Philippe
Durand, Tony
Brosseau, Carole
Bordron, Philippe
Delage, Erwan
Chaffron, Samuel
Petitfils, Camille
Cenac, Nicolas
Neunlist, Michel
Bodinier, Marie
Rolli-Derkinderen, Malvyne
Maternal prebiotic supplementation impacts colitis development in offspring mice
title Maternal prebiotic supplementation impacts colitis development in offspring mice
title_full Maternal prebiotic supplementation impacts colitis development in offspring mice
title_fullStr Maternal prebiotic supplementation impacts colitis development in offspring mice
title_full_unstemmed Maternal prebiotic supplementation impacts colitis development in offspring mice
title_short Maternal prebiotic supplementation impacts colitis development in offspring mice
title_sort maternal prebiotic supplementation impacts colitis development in offspring mice
topic Nutrition
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC9849907/
https://www.ncbi.nlm.nih.gov/pubmed/36687706
http://dx.doi.org/10.3389/fnut.2022.988529
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