Journal Article

Bacteroides thetaiotaomicron and Faecalibacterium prausnitzii influence the production of mucus glycans and the development of goblet cells in the colonic epithelium of a gnotobiotic model rodent

Philippe, Catherine, C, Génétique Animale et Biologie Intégrative (GABI) ; Institut National de la Recherche Agronomique (INRA)-AgroParisTech, Robert, Veronique, V, Thomas, Muriel, Bridonneau, Chantal, C, French Ministry of Education and Research; Vitagora Competitive Cluster; French FUI (Fond Unique Interministeriel, FUI) [F1010012D]; FEDER (Fonds Europeen de Developpement Regional, Bourgogne) ; Burgundy Region; Conseil General 21; Grand Dijon; Merck Medication Familiale (Dijon, France); Biovitis (Saint Etienne de Chomeil, France), Robbe-Masselot, Catherine, C, MICrobiologie de l'ALImentation au Service de la Santé (MICALIS) ; Institut National de la Recherche Agronomique (INRA)-AgroParisTech, Noordine, Marie-Louise, M.-L, Chevalier-Curt, Marie Joncquel, M. J, Miquel, Sylvie, S, Langella, Philippe, P, Unité de Glycobiologie Structurale et Fonctionnelle - UMR 8576 (UGSF) ; Université de Lille-Centre National de la Recherche Scientifique (CNRS), Cherbuy, Claire, Bouet, Stephan, S, Wrzosek, Laura, L

2013

Overview

Background: The intestinal mucus layer plays a key role in the maintenance of host-microbiota homeostasis. To document the crosstalk between the host and microbiota, we used gnotobiotic models to study the influence of two major commensal bacteria, Bacteroides thetaiotaomicron and Faecalibacterium prausnitzii, on this intestinal mucus layer. B. thetaiotaomicron is known to use polysaccharides from mucus, but its effect on goblet cells has not been addressed so far. F. prausnitzii is of particular physiological importance because it can be considered as a sensor and a marker of human health. We determined whether B. thetaiotaomicron affected goblet cell differentiation, mucin synthesis and glycosylation in the colonic epithelium. We then investigated how F. prausnitzii influenced the colonic epithelial responses to B. thetaiotaomicron.[br/] Results: B. thetaiotaomicron, an acetate producer, increased goblet cell differentiation, expression of mucus-related genes and the ratio of sialylated to sulfated mucins in mono-associated rats. B. thetaiotaomicron, therefore, stimulates the secretory lineage, favoring mucus production. When B. thetaiotaomicron was associated with F. prausnitzii, an acetate consumer and a butyrate producer, the effects on goblet cells and mucin glycosylation were diminished. F. prausnitzii, by attenuating the effects of B. thetaiotaomicron on mucus, may help the epithelium to maintain appropriate proportions of different cell types of the secretory lineage. Using a mucus-producing cell line, we showed that acetate up-regulated KLF4, a transcription factor involved in goblet cell differentiation.[br/] Conclusions: B. thetaiotaomicron and F. prausnitzii, which are metabolically complementary, modulate, in vivo, the intestinal mucus barrier by modifying goblet cells and mucin glycosylation. Our study reveals the importance of the balance between two main commensal bacteria in maintaining colonic epithelial homeostasis via their respective effects on mucus.

• Publisher: HAL CCSD,BioMed Central,Springer Nature B.V
• Subject: Acetates - metabolism / Agricultural sciences / Animals / Bacteria / Bacteroides - physiology / Bacteroides - ultrastructure / Bacteroides Infections - microbiology / Bacteroides Infections - pathology / Bacteroides thetaiotaomicron / Cell Differentiation / Colon - metabolism / Colon - microbiology / Colon - pathology / Disease Models, Animal / Faecalibacterium prausnitzii / Gene Expression Regulation / Germ-Free Life / Glycosylation / Goblet Cells - metabolism / Goblet Cells - microbiology / Goblet Cells - pathology / Gram-Positive Bacterial Infections - microbiology / Gram-Positive Bacterial Infections - pathology / Host-Pathogen Interactions - genetics / HT29 Cells / Humans / Immunization / Intestinal Mucosa - metabolism / Intestinal Mucosa - microbiology / Intestinal Mucosa - pathology / Life Sciences / Mucus - metabolism / Mucus - microbiology / Polysaccharides - biosynthesis / Rats / Rodents / Ruminococcus - physiology / Signal Transduction / Small intestine / Time Factors
• ISBN: 0003199106000