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Maternal Microbiota Transfer Programs Offspring Eating Behavior

Understanding the link between mother’s obesity and regulation of the child’s appetite is a prerequisite for the design of successful preventive strategies. Beyond the possible contributions of genetic heritage, family culture, and hormonal and metabolic environment during pregnancy, we investigate...

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Autores principales: Pocheron, Anne-Lise, Le Dréan, Gwenola, Billard, Helene, Moyon, Thomas, Pagniez, Anthony, Heberden, Christine, Le Chatelier, Emmanuelle, Darmaun, Dominique, Michel, Catherine, Parnet, Patricia
Formato: Online Artículo Texto
Lenguaje:English
Publicado: Frontiers Media S.A. 2021
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC8239415/
https://www.ncbi.nlm.nih.gov/pubmed/34211445
http://dx.doi.org/10.3389/fmicb.2021.672224
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author Pocheron, Anne-Lise
Le Dréan, Gwenola
Billard, Helene
Moyon, Thomas
Pagniez, Anthony
Heberden, Christine
Le Chatelier, Emmanuelle
Darmaun, Dominique
Michel, Catherine
Parnet, Patricia
author_facet Pocheron, Anne-Lise
Le Dréan, Gwenola
Billard, Helene
Moyon, Thomas
Pagniez, Anthony
Heberden, Christine
Le Chatelier, Emmanuelle
Darmaun, Dominique
Michel, Catherine
Parnet, Patricia
author_sort Pocheron, Anne-Lise
collection PubMed
description Understanding the link between mother’s obesity and regulation of the child’s appetite is a prerequisite for the design of successful preventive strategies. Beyond the possible contributions of genetic heritage, family culture, and hormonal and metabolic environment during pregnancy, we investigate in the present paper the causal role of the transmission of the maternal microbiotas in obesity as microbiotas differ between lean and obese mothers, maternal microbiotas are the main determinants of a baby’s gut colonization, and the intestinal microbiota resulting from the early colonization could impact the feeding behavior of the offspring with short- and long-term consequences on body weight. We thus investigated the potential role of vertical transfers of maternal microbiotas in programming the eating behavior of the offspring. Selectively bred obese-prone (OP)/obese-resistant (OR) Sprague-Dawley dams were used since differences in the cecal microbiota have been evidenced from males of that strain. Microbiota collected from vagina (at the end of gestation), feces, and milk (at postnatal days 1, 5, 10, and 15) of OP/OR dams were orally inoculated to conventional Fischer F344 recipient pups from birth to 15 days of age to create three groups of pups: F-OP, F-OR, and F-Sham group (that received the vehicle). We first checked microbiotal differences between inoculas. We then assessed the impact of transfer (from birth to adulthood) onto the intestinal microbiota of recipients rats, their growth, and their eating behavior by measuring their caloric intake, their anticipatory food reward responses, their preference for sweet and fat tastes in solutions, and the sensations that extend after food ingestion. Finally, we searched for correlation between microbiota composition and food intake parameters. We found that maternal transfer of microbiota differing in composition led to alterations in pups’ gut microbiota composition that did not last until adulthood but were associated with specific eating behavior characteristics that were predisposing F-OP rats to higher risk of over consuming at subsequent periods of their life. These findings support the view that neonatal gut microbiotal transfer can program eating behavior, even without a significant long-lasting impact on adulthood microbiota composition.
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spelling pubmed-82394152021-06-30 Maternal Microbiota Transfer Programs Offspring Eating Behavior Pocheron, Anne-Lise Le Dréan, Gwenola Billard, Helene Moyon, Thomas Pagniez, Anthony Heberden, Christine Le Chatelier, Emmanuelle Darmaun, Dominique Michel, Catherine Parnet, Patricia Front Microbiol Microbiology Understanding the link between mother’s obesity and regulation of the child’s appetite is a prerequisite for the design of successful preventive strategies. Beyond the possible contributions of genetic heritage, family culture, and hormonal and metabolic environment during pregnancy, we investigate in the present paper the causal role of the transmission of the maternal microbiotas in obesity as microbiotas differ between lean and obese mothers, maternal microbiotas are the main determinants of a baby’s gut colonization, and the intestinal microbiota resulting from the early colonization could impact the feeding behavior of the offspring with short- and long-term consequences on body weight. We thus investigated the potential role of vertical transfers of maternal microbiotas in programming the eating behavior of the offspring. Selectively bred obese-prone (OP)/obese-resistant (OR) Sprague-Dawley dams were used since differences in the cecal microbiota have been evidenced from males of that strain. Microbiota collected from vagina (at the end of gestation), feces, and milk (at postnatal days 1, 5, 10, and 15) of OP/OR dams were orally inoculated to conventional Fischer F344 recipient pups from birth to 15 days of age to create three groups of pups: F-OP, F-OR, and F-Sham group (that received the vehicle). We first checked microbiotal differences between inoculas. We then assessed the impact of transfer (from birth to adulthood) onto the intestinal microbiota of recipients rats, their growth, and their eating behavior by measuring their caloric intake, their anticipatory food reward responses, their preference for sweet and fat tastes in solutions, and the sensations that extend after food ingestion. Finally, we searched for correlation between microbiota composition and food intake parameters. We found that maternal transfer of microbiota differing in composition led to alterations in pups’ gut microbiota composition that did not last until adulthood but were associated with specific eating behavior characteristics that were predisposing F-OP rats to higher risk of over consuming at subsequent periods of their life. These findings support the view that neonatal gut microbiotal transfer can program eating behavior, even without a significant long-lasting impact on adulthood microbiota composition. Frontiers Media S.A. 2021-06-15 /pmc/articles/PMC8239415/ /pubmed/34211445 http://dx.doi.org/10.3389/fmicb.2021.672224 Text en Copyright © 2021 Pocheron, Le Dréan, Billard, Moyon, Pagniez, Heberden, Le Chatelier, Darmaun, Michel and Parnet. 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 Microbiology
Pocheron, Anne-Lise
Le Dréan, Gwenola
Billard, Helene
Moyon, Thomas
Pagniez, Anthony
Heberden, Christine
Le Chatelier, Emmanuelle
Darmaun, Dominique
Michel, Catherine
Parnet, Patricia
Maternal Microbiota Transfer Programs Offspring Eating Behavior
title Maternal Microbiota Transfer Programs Offspring Eating Behavior
title_full Maternal Microbiota Transfer Programs Offspring Eating Behavior
title_fullStr Maternal Microbiota Transfer Programs Offspring Eating Behavior
title_full_unstemmed Maternal Microbiota Transfer Programs Offspring Eating Behavior
title_short Maternal Microbiota Transfer Programs Offspring Eating Behavior
title_sort maternal microbiota transfer programs offspring eating behavior
topic Microbiology
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC8239415/
https://www.ncbi.nlm.nih.gov/pubmed/34211445
http://dx.doi.org/10.3389/fmicb.2021.672224
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