Gut Microbiota Remodeling and Intestinal Adaptation to Lipid Malabsorption After Enteroendocrine Cell Loss in Adult Mice.


Journal

Cellular and molecular gastroenterology and hepatology
ISSN: 2352-345X
Titre abrégé: Cell Mol Gastroenterol Hepatol
Pays: United States
ID NLM: 101648302

Informations de publication

Date de publication:
2023
Historique:
received: 04 12 2022
revised: 16 02 2023
accepted: 16 02 2023
medline: 22 5 2023
pubmed: 2 3 2023
entrez: 1 3 2023
Statut: ppublish

Résumé

Enteroendocrine cells (EECs) and their hormones are essential regulators of whole-body energy homeostasis. EECs sense luminal nutrients and microbial metabolites and subsequently secrete various hormones acting locally or at a distance. Impaired development of EECs during embryogenesis is life-threatening in newborn mice and humans due to compromised nutrient absorption. However, the physiological importance of the EEC system in adult mice has yet to be directedly studied. Herein, we aimed to determine the long-term consequences of a total loss of EECs in healthy adults on energy metabolism, intestinal transcriptome, and microbiota. We depleted intestinal EECs by tamoxifen treatment of adult Neurog3 Induction of EEC deficiency in adults is not life-threatening unless fed with a high-fat diet. Under a standard chow diet, mice lose 10% of weight due to impaired food efficiency. Blood concentrations of cholesterol, triglycerides, and free fatty acids are reduced, and lipid absorption is impaired and delayed in the distal small intestine. Genes controlling lipogenesis, carbohydrate metabolism, and neoglucogenesis are upregulated. Microbiota composition is rapidly altered after EECs depletion and is characterized by decreased α-diversity. Bacteroides and Lactobacillus were progressively enriched, whereas Lachnospiraceae declined without impacting fecal short-chain fatty acid concentrations. EECs are dispensable for survival in adult male mice under a standard chow diet. The absence of EECs impairs intestinal lipid absorption, leading to transcriptomic and metabolic adaptations and remodeling of the gut microbiota.

Sections du résumé

BACKGROUND & AIMS
Enteroendocrine cells (EECs) and their hormones are essential regulators of whole-body energy homeostasis. EECs sense luminal nutrients and microbial metabolites and subsequently secrete various hormones acting locally or at a distance. Impaired development of EECs during embryogenesis is life-threatening in newborn mice and humans due to compromised nutrient absorption. However, the physiological importance of the EEC system in adult mice has yet to be directedly studied. Herein, we aimed to determine the long-term consequences of a total loss of EECs in healthy adults on energy metabolism, intestinal transcriptome, and microbiota.
METHODS
We depleted intestinal EECs by tamoxifen treatment of adult Neurog3
RESULTS
Induction of EEC deficiency in adults is not life-threatening unless fed with a high-fat diet. Under a standard chow diet, mice lose 10% of weight due to impaired food efficiency. Blood concentrations of cholesterol, triglycerides, and free fatty acids are reduced, and lipid absorption is impaired and delayed in the distal small intestine. Genes controlling lipogenesis, carbohydrate metabolism, and neoglucogenesis are upregulated. Microbiota composition is rapidly altered after EECs depletion and is characterized by decreased α-diversity. Bacteroides and Lactobacillus were progressively enriched, whereas Lachnospiraceae declined without impacting fecal short-chain fatty acid concentrations.
CONCLUSIONS
EECs are dispensable for survival in adult male mice under a standard chow diet. The absence of EECs impairs intestinal lipid absorption, leading to transcriptomic and metabolic adaptations and remodeling of the gut microbiota.

Identifiants

pubmed: 36858136
pii: S2352-345X(23)00032-2
doi: 10.1016/j.jcmgh.2023.02.013
pmc: PMC10149283
pii:
doi:

Substances chimiques

Hormones 0
Cholesterol 97C5T2UQ7J

Types de publication

Journal Article Research Support, Non-U.S. Gov't

Langues

eng

Sous-ensembles de citation

IM

Pagination

1443-1461

Commentaires et corrections

Type : CommentIn

Informations de copyright

Copyright © 2023 The Authors. Published by Elsevier Inc. All rights reserved.

Auteurs

Florence Blot (F)

Institut de Génétique et de Biologie Moléculaire et Cellulaire (IGBMC), Illkirch, France; Institut National de la Santé et de la Recherche Médicale (INSERM) U1258, Illkirch, France; Centre National de Recherche Scientifique (CNRS) UMR7104, Illkirch, France; Université de Strasbourg, Illkirch, France.

Justine Marchix (J)

Nantes Université, CHU Nantes, Inserm, TENS, The Enteric Nervous System in Gut and Brain Diseases, IMAD, Nantes, France.

Miriam Ejarque (M)

Institut de Génétique et de Biologie Moléculaire et Cellulaire (IGBMC), Illkirch, France; Institut National de la Santé et de la Recherche Médicale (INSERM) U1258, Illkirch, France; Centre National de Recherche Scientifique (CNRS) UMR7104, Illkirch, France; Université de Strasbourg, Illkirch, France.

Sara Jimenez (S)

Institut de Génétique et de Biologie Moléculaire et Cellulaire (IGBMC), Illkirch, France; Institut National de la Santé et de la Recherche Médicale (INSERM) U1258, Illkirch, France; Centre National de Recherche Scientifique (CNRS) UMR7104, Illkirch, France; Université de Strasbourg, Illkirch, France.

Aline Meunier (A)

Institut de Génétique et de Biologie Moléculaire et Cellulaire (IGBMC), Illkirch, France; Institut National de la Santé et de la Recherche Médicale (INSERM) U1258, Illkirch, France; Centre National de Recherche Scientifique (CNRS) UMR7104, Illkirch, France; Université de Strasbourg, Illkirch, France.

Céline Keime (C)

Institut de Génétique et de Biologie Moléculaire et Cellulaire (IGBMC), Illkirch, France; Institut National de la Santé et de la Recherche Médicale (INSERM) U1258, Illkirch, France; Centre National de Recherche Scientifique (CNRS) UMR7104, Illkirch, France; Université de Strasbourg, Illkirch, France.

Camille Trottier (C)

Nantes Université, CHU Nantes, Inserm, TENS, The Enteric Nervous System in Gut and Brain Diseases, IMAD, Nantes, France.

Mikaël Croyal (M)

L'Institut du Thorax, INSERM UMR_S1087, CNRS UMR_6291, Université de Nantes, Nantes, France; CRNH-Ouest Mass Spectrometry Core Facility, Nantes, France; Nantes Université, CHU Nantes, Inserm, CNRS, SFR Santé, Inserm UMS 016, CNRS UMS 3556, Nantes, France.

Céline Lapp (C)

Institut de Génétique et de Biologie Moléculaire et Cellulaire (IGBMC), Illkirch, France; Institut National de la Santé et de la Recherche Médicale (INSERM) U1258, Illkirch, France; Centre National de Recherche Scientifique (CNRS) UMR7104, Illkirch, France; Université de Strasbourg, Illkirch, France.

Maxime M Mahe (MM)

Nantes Université, CHU Nantes, Inserm, TENS, The Enteric Nervous System in Gut and Brain Diseases, IMAD, Nantes, France; Department of Pediatric General and Thoracic Surgery, Cincinnati Children's Hospital Medical Center, Cincinnati, Ohio; Department of Pediatrics, University of Cincinnati, Cincinnati, Ohio.

Adèle De Arcangelis (A)

Institut de Génétique et de Biologie Moléculaire et Cellulaire (IGBMC), Illkirch, France; Institut National de la Santé et de la Recherche Médicale (INSERM) U1258, Illkirch, France; Centre National de Recherche Scientifique (CNRS) UMR7104, Illkirch, France; Université de Strasbourg, Illkirch, France. Electronic address: adele@igbmc.fr.

Gérard Gradwohl (G)

Institut de Génétique et de Biologie Moléculaire et Cellulaire (IGBMC), Illkirch, France; Institut National de la Santé et de la Recherche Médicale (INSERM) U1258, Illkirch, France; Centre National de Recherche Scientifique (CNRS) UMR7104, Illkirch, France; Université de Strasbourg, Illkirch, France. Electronic address: gradwohl@igbmc.fr.

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Classifications MeSH