The Olfactory Receptor OR51E1 Is Present along the Gastrointestinal Tract of Pigs, Co-Localizes with Enteroendocrine Cells and Is Modulated by Intestinal Microbiota

• Published in: PloS one Vol. 10; no. 6; p. e0129501
• Main Authors: Priori, Davide, Colombo, Michela, Clavenzani, Paolo, Jansman, Alfons J M, Lallès, Jean-Paul, Trevisi, Paolo, Bosi, Paolo
• Format: Journal Article
• Language: English
• Published: United States Public Library of Science 15.06.2015; Public Library of Science (PLoS)
• Subjects: Age; Amoxicillin; Animals; Anti-Bacterial Agents - pharmacology; Antibiotics; Cecum; Diet; E coli; Enteroendocrine Cells - metabolism; Escherichia coli; Gastrointestinal Microbiome; Gastrointestinal system; Gastrointestinal tract; Gastrointestinal Tract - cytology; Gastrointestinal Tract - metabolism; Gene Expression; Hormones; Intestinal microflora; Intestine; Lactobacillus amylovorus; Life Sciences; Localization; Metabolites; Microbiota; Microbiota (Symbiotic organisms); Microorganisms; Offspring; Parturition; Peptides; Receptors, Odorant - metabolism; Rectum; Serotonin; Suckling behavior; Swine - metabolism; Tissues; Weaning; France; Italy; Netherlands
• ISSN: 1932-6203; 1932-6203
• DOI: 10.1371/journal.pone.0129501

The relevance of the butyrate-sensing olfactory receptor OR51E1 for gastrointestinal (GIT) functioning has not been considered so far. We investigated in young pigs the distribution of OR51E1 along the GIT, its relation with some endocrine markers, its variation with age and after interventions affecting the gut environment and intestinal microbiota. Immuno-reactive cells for OR51E1 and chromogranin A (CgA) were counted in cardial (CA), fundic (FU), pyloric (PL) duodenal (DU), jejunal (JE), ileal (IL), cecal (CE), colonic (CO) and rectal (RE) mucosae. OR51E1 co-localization with serotonin (5HT) and peptide YY (PYY) were evaluated in PL and CO respectively. FU and PL tissues were also sampled from 84 piglets reared from sows receiving either or not oral antibiotics (amoxicillin) around parturition, and sacrificed at days 14, 21, 28 (weaning) and 42 of age. JE samples were also obtained from 12 caesarean-derived piglets that were orally associated with simple (SA) or complex (CA) microbiota in the postnatal phase, and of which on days 26-37 of age jejunal loops were perfused for 8 h with enterotoxigenic Escherichia coli F4 (ETEC), Lactobacillus amylovorus or saline (CTRL). Tissue densities of OR51E1+ cells were in decreasing order: PL=DU>FU=CA>JE=IL=CE=CO=RE. OR51E1+ cells showed an enteroendocrine nature containing gastrointestinal hormones such as PYY or 5HT. OR51E1 gene expression in PL and FU increased during and after the suckling period (p<0.05). It was marginally reduced in offspring from antibiotic-treated sows (tendency, p=0.073), vs. Jejunal OR51E1 gene expression was reduced in piglets early associated with SA, compared with CA, and in ETEC-perfused loops vs. CTRL (p<0.01). Our results indicate that OR51E1 is related to GIT enteroendocrine activity. Moreover age, pathogen challenge and dietary manipulations influencing the gastrointestinal luminal microenvironment significantly affect the OR51E1 gene expression in GIT tissues presumably in association with the release of microbial metabolites.