Abstract
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. control. 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.
Highlights
The superfamily of olfactory receptors (ORs) is formed by a very large number of G-protein coupled receptor proteins that detect volatile odorant molecules
The immunohistochemical visualizations for OR51E1 staining in each tissue and for co-localizations with chromogranin A (CgA), 5HT and peptide YY (PYY) are presented in Figs 1 and 2, respectively
Our results show that OR51E1 co-localizes with the enteroendocrine cell marker CgA all along the gastrointestinal tract (GIT) for a percentage varying from 78% to 100% (Fig 3B)
Summary
The superfamily of olfactory receptors (ORs) is formed by a very large number of G-protein coupled receptor proteins that detect volatile odorant molecules. They were initially discovered in the olfactory epithelium, but recent evidence shows that several of them are well expressed in the respiratory tract and in other tissues [1], where their function is still unclear. Deorphanization studies by cell-reporter systems evidenced that 3- and 4- methyl-valeric acids [5], nonanoic acid [6] and butyric acid [7] are agonists of this receptor. The sensitivity of OR51E1 to butyrate is of particular interest due to the multiple implications of this enteric bacterial metabolite in regulating GIT tissues in normal and pathological states [8]
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