Lactose and Fructo-oligosaccharides Increase Visceral Sensitivity in Mice via Glycation Processes, Increasing Mast Cell Density in Colonic Mucosa.


Journal

Gastroenterology
ISSN: 1528-0012
Titre abrégé: Gastroenterology
Pays: United States
ID NLM: 0374630

Informations de publication

Date de publication:
02 2020
Historique:
received: 15 04 2019
revised: 28 10 2019
accepted: 31 10 2019
pubmed: 13 11 2019
medline: 9 4 2020
entrez: 13 11 2019
Statut: ppublish

Résumé

Irritable bowel syndrome (IBS) is characterized by abdominal pain, bloating, and erratic bowel habits. A diet low in fermentable oligosaccharides, disaccharides, monosaccharides, and polyols (FODMAPs) can reduce symptoms of IBS, possibly by reducing microbial fermentation products. We investigated whether ingestion of FODMAPs can induce IBS-like visceral hypersensitivity mediated by fermentation products of intestinal microbes in mice. C57Bl/6 mice were gavaged with lactose, with or without the antiglycation agent pyridoxamine, or saline (controls) daily for 3 weeks. A separate group of mice were fed a diet containing fructo-oligosaccharides, with or without pyridoxamine in drinking water, or a normal chow diet (controls) for 6 weeks. Feces were collected and analyzed by 16S ribosomal RNA gene sequencing and bacterial community analyses. Abdominal sensitivity was measured by electromyography and mechanical von Frey filament assays. Colon tissues were collected from some mice and analyzed by histology and immunofluorescence to quantify mast cells and expression of advanced glycosylation end-product specific receptor (AGER). Mice gavaged with lactose or fed fructo-oligosaccharides had increased abdominal sensitivity compared with controls, associated with increased numbers of mast cells in colon and expression of the receptor for AGER in proximal colon epithelium. These effects were prevented by administration of pyridoxamine. Lactose and/or pyridoxamine did not induce significant alterations in the composition of the fecal microbiota. Mass spectrometric analysis of carbonyl compounds in fecal samples identified signatures associated with mice given lactose or fructo-oligosaccharides vs controls. We found that oral administration of lactose or fructo-oligosaccharides to mice increases abdominal sensitivity, associated with increased numbers of mast cells in colon and expression of AGER; these can be prevented with an antiglycation agent. Lactose and/or pyridoxamine did not produce alterations in fecal microbiota of mice. Our findings indicate that preventing glycation reactions might reduce abdominal pain in patients with IBS with sensitivity to FODMAPs.

Sections du résumé

BACKGROUND & AIMS
Irritable bowel syndrome (IBS) is characterized by abdominal pain, bloating, and erratic bowel habits. A diet low in fermentable oligosaccharides, disaccharides, monosaccharides, and polyols (FODMAPs) can reduce symptoms of IBS, possibly by reducing microbial fermentation products. We investigated whether ingestion of FODMAPs can induce IBS-like visceral hypersensitivity mediated by fermentation products of intestinal microbes in mice.
METHODS
C57Bl/6 mice were gavaged with lactose, with or without the antiglycation agent pyridoxamine, or saline (controls) daily for 3 weeks. A separate group of mice were fed a diet containing fructo-oligosaccharides, with or without pyridoxamine in drinking water, or a normal chow diet (controls) for 6 weeks. Feces were collected and analyzed by 16S ribosomal RNA gene sequencing and bacterial community analyses. Abdominal sensitivity was measured by electromyography and mechanical von Frey filament assays. Colon tissues were collected from some mice and analyzed by histology and immunofluorescence to quantify mast cells and expression of advanced glycosylation end-product specific receptor (AGER).
RESULTS
Mice gavaged with lactose or fed fructo-oligosaccharides had increased abdominal sensitivity compared with controls, associated with increased numbers of mast cells in colon and expression of the receptor for AGER in proximal colon epithelium. These effects were prevented by administration of pyridoxamine. Lactose and/or pyridoxamine did not induce significant alterations in the composition of the fecal microbiota. Mass spectrometric analysis of carbonyl compounds in fecal samples identified signatures associated with mice given lactose or fructo-oligosaccharides vs controls.
CONCLUSIONS
We found that oral administration of lactose or fructo-oligosaccharides to mice increases abdominal sensitivity, associated with increased numbers of mast cells in colon and expression of AGER; these can be prevented with an antiglycation agent. Lactose and/or pyridoxamine did not produce alterations in fecal microbiota of mice. Our findings indicate that preventing glycation reactions might reduce abdominal pain in patients with IBS with sensitivity to FODMAPs.

Identifiants

pubmed: 31711923
pii: S0016-5085(19)41528-X
doi: 10.1053/j.gastro.2019.10.037
pii:
doi:

Substances chimiques

Oligosaccharides 0
Receptor for Advanced Glycation End Products 0
Vitamin B Complex 12001-76-2
Pyridoxamine 6466NM3W93
Lactose J2B2A4N98G

Types de publication

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

Langues

eng

Sous-ensembles de citation

IM

Pagination

652-663.e6

Informations de copyright

Copyright © 2020 AGA Institute. Published by Elsevier Inc. All rights reserved.

Auteurs

Jasper B J Kamphuis (JBJ)

Institut National de Recherche pour l'Agriculture, l'Alimentation et l'Environnement, Toxalim, UMR1331, INRAE/INP/UPS, Toulouse, France; Neurogastroenterology and Nutrition, Toxalim, Toulouse.

Bruno Guiard (B)

Centre de Recherches sur la Cognition Animale, Centre de Biologie Intégrative, Université de Toulouse, CNRS, UPS, Toulouse, France.

Mathilde Leveque (M)

Institut National de Recherche pour l'Agriculture, l'Alimentation et l'Environnement, Toxalim, UMR1331, INRAE/INP/UPS, Toulouse, France; Neurogastroenterology and Nutrition, Toxalim, Toulouse.

Maiwenn Olier (M)

Institut National de Recherche pour l'Agriculture, l'Alimentation et l'Environnement, Toxalim, UMR1331, INRAE/INP/UPS, Toulouse, France; Neurogastroenterology and Nutrition, Toxalim, Toulouse.

Isabelle Jouanin (I)

Institut National de Recherche pour l'Agriculture, l'Alimentation et l'Environnement, Toxalim, UMR1331, INRAE/INP/UPS, Toulouse, France; AXIOM Platform, MetaToul MetaboHUB, National Infrastructure for Metabolomics and Fluxomics, Toulouse, France.

Sophie Yvon (S)

Institut National de Recherche pour l'Agriculture, l'Alimentation et l'Environnement, Toxalim, UMR1331, INRAE/INP/UPS, Toulouse, France; Neurogastroenterology and Nutrition, Toxalim, Toulouse.

Valerie Tondereau (V)

Institut National de Recherche pour l'Agriculture, l'Alimentation et l'Environnement, Toxalim, UMR1331, INRAE/INP/UPS, Toulouse, France; Neurogastroenterology and Nutrition, Toxalim, Toulouse.

Pauline Rivière (P)

Institut National de Recherche pour l'Agriculture, l'Alimentation et l'Environnement, Toxalim, UMR1331, INRAE/INP/UPS, Toulouse, France; Neurogastroenterology and Nutrition, Toxalim, Toulouse.

Françoise Guéraud (F)

Institut National de Recherche pour l'Agriculture, l'Alimentation et l'Environnement, Toxalim, UMR1331, INRAE/INP/UPS, Toulouse, France; Prevention and Promotion of Carcinogenesis by Food team, Toxalim, Toulouse, France.

Sylvie Chevolleau (S)

Institut National de Recherche pour l'Agriculture, l'Alimentation et l'Environnement, Toxalim, UMR1331, INRAE/INP/UPS, Toulouse, France; AXIOM Platform, MetaToul MetaboHUB, National Infrastructure for Metabolomics and Fluxomics, Toulouse, France.

Maria-Helena Noguer-Meireles (MH)

Institut National de Recherche pour l'Agriculture, l'Alimentation et l'Environnement, Toxalim, UMR1331, INRAE/INP/UPS, Toulouse, France; AXIOM Platform, MetaToul MetaboHUB, National Infrastructure for Metabolomics and Fluxomics, Toulouse, France.

Jean-François Martin (JF)

Institut National de Recherche pour l'Agriculture, l'Alimentation et l'Environnement, Toxalim, UMR1331, INRAE/INP/UPS, Toulouse, France; AXIOM Platform, MetaToul MetaboHUB, National Infrastructure for Metabolomics and Fluxomics, Toulouse, France.

Laurent Debrauwer (L)

Institut National de Recherche pour l'Agriculture, l'Alimentation et l'Environnement, Toxalim, UMR1331, INRAE/INP/UPS, Toulouse, France; AXIOM Platform, MetaToul MetaboHUB, National Infrastructure for Metabolomics and Fluxomics, Toulouse, France.

Helene Eutamène (H)

Institut National de Recherche pour l'Agriculture, l'Alimentation et l'Environnement, Toxalim, UMR1331, INRAE/INP/UPS, Toulouse, France; Neurogastroenterology and Nutrition, Toxalim, Toulouse. Electronic address: helene.eutamene@inra.fr.

Vassilia Theodorou (V)

Institut National de Recherche pour l'Agriculture, l'Alimentation et l'Environnement, Toxalim, UMR1331, INRAE/INP/UPS, Toulouse, France; Neurogastroenterology and Nutrition, Toxalim, Toulouse.

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Classifications MeSH