Maternal prebiotic supplementation impacts colitis development in offspring mice
Background and aimsMaternal 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 permea...
| Main Authors: | , , , , , , , , , , , , |
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| Format: | Article |
| Language: | English |
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Frontiers Media S.A.
2023-01-01
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| Series: | Frontiers in Nutrition |
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| Online Access: | https://www.frontiersin.org/articles/10.3389/fnut.2022.988529/full |
| _version_ | 1797960393057894400 |
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| author | Amélie Lê Amandine Selle Philippe Aubert Tony Durand Carole Brosseau Philippe Bordron Erwan Delage Samuel Chaffron Camille Petitfils Nicolas Cenac Michel Neunlist Marie Bodinier Malvyne Rolli-Derkinderen |
| author_facet | Amélie Lê Amandine Selle Philippe Aubert Tony Durand Carole Brosseau Philippe Bordron Erwan Delage Samuel Chaffron Camille Petitfils Nicolas Cenac Michel Neunlist Marie Bodinier Malvyne Rolli-Derkinderen |
| author_sort | Amélie Lê |
| collection | DOAJ |
| description | Background and aimsMaternal 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 methodsOffspring 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.ResultsDSS-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.ConclusionMaternal 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. |
| first_indexed | 2024-04-11T00:45:17Z |
| format | Article |
| id | doaj.art-010b697830cc4bf8ab6b05556de68055 |
| institution | Directory Open Access Journal |
| issn | 2296-861X |
| language | English |
| last_indexed | 2024-04-11T00:45:17Z |
| publishDate | 2023-01-01 |
| publisher | Frontiers Media S.A. |
| record_format | Article |
| series | Frontiers in Nutrition |
| spelling | doaj.art-010b697830cc4bf8ab6b05556de680552023-01-05T16:54:39ZengFrontiers Media S.A.Frontiers in Nutrition2296-861X2023-01-01910.3389/fnut.2022.988529988529Maternal prebiotic supplementation impacts colitis development in offspring miceAmélie Lê0Amandine Selle1Philippe Aubert2Tony Durand3Carole Brosseau4Philippe Bordron5Erwan Delage6Samuel Chaffron7Camille Petitfils8Nicolas Cenac9Michel Neunlist10Marie Bodinier11Malvyne Rolli-Derkinderen12The Enteric Nervous System in Gut and Brain Disorders, Institut des Maladies de l’Appareil Digestif, Institut National Pour la Santé et la Recherche Médicale, Nantes Université, Nantes, FranceUnité de Recherche 1268 Biopolymères Interactions Assemblages, Institut National de Recherche pour l’Agriculture, l’Alimentation et l’Environnement, Nantes, FranceThe Enteric Nervous System in Gut and Brain Disorders, Institut des Maladies de l’Appareil Digestif, Institut National Pour la Santé et la Recherche Médicale, Nantes Université, Nantes, FranceThe Enteric Nervous System in Gut and Brain Disorders, Institut des Maladies de l’Appareil Digestif, Institut National Pour la Santé et la Recherche Médicale, Nantes Université, Nantes, FranceUnité de Recherche 1268 Biopolymères Interactions Assemblages, Institut National de Recherche pour l’Agriculture, l’Alimentation et l’Environnement, Nantes, FranceThe Enteric Nervous System in Gut and Brain Disorders, Institut des Maladies de l’Appareil Digestif, Institut National Pour la Santé et la Recherche Médicale, Nantes Université, Nantes, FranceUMR 6004, LS2N, Nantes Université, Ecole Centrale Nantes, CNRS, Nantes, FranceUMR 6004, LS2N, Nantes Université, Ecole Centrale Nantes, CNRS, Nantes, FranceUMR 1220, Institut de Recherche en Santé Digestive, Toulouse, FranceUMR 1220, Institut de Recherche en Santé Digestive, Toulouse, FranceThe Enteric Nervous System in Gut and Brain Disorders, Institut des Maladies de l’Appareil Digestif, Institut National Pour la Santé et la Recherche Médicale, Nantes Université, Nantes, FranceUnité de Recherche 1268 Biopolymères Interactions Assemblages, Institut National de Recherche pour l’Agriculture, l’Alimentation et l’Environnement, Nantes, FranceThe Enteric Nervous System in Gut and Brain Disorders, Institut des Maladies de l’Appareil Digestif, Institut National Pour la Santé et la Recherche Médicale, Nantes Université, Nantes, FranceBackground and aimsMaternal 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 methodsOffspring 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.ResultsDSS-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.ConclusionMaternal 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.https://www.frontiersin.org/articles/10.3389/fnut.2022.988529/fullprebioticsIBDmicrobiotacolitisDOHaDoffspring |
| spellingShingle | Amélie Lê Amandine Selle Philippe Aubert Tony Durand Carole Brosseau Philippe Bordron Erwan Delage Samuel Chaffron Camille Petitfils Nicolas Cenac Michel Neunlist Marie Bodinier Malvyne Rolli-Derkinderen Maternal prebiotic supplementation impacts colitis development in offspring mice Frontiers in Nutrition prebiotics IBD microbiota colitis DOHaD offspring |
| 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 | prebiotics IBD microbiota colitis DOHaD offspring |
| url | https://www.frontiersin.org/articles/10.3389/fnut.2022.988529/full |
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