Oxytocin Signaling in Mouse Taste Buds

Abstract

BackgroundThe neuropeptide, oxytocin (OXT), acts on brain circuits to inhibit food intake. Mutant mice lacking OXT (OXT knockout) overconsume salty and sweet (i.e. sucrose, saccharin) solutions. We asked if OXT might also act on taste buds via its receptor, OXTR.Methodology/Principal FindingsUsing RT-PCR, we detected the expression of OXTR in taste buds throughout the oral cavity, but not in adjacent non-taste lingual epithelium. By immunostaining tissues from OXTR-YFP knock-in mice, we found that OXTR is expressed in a subset of Glial-like (Type I) taste cells, and also in cells on the periphery of taste buds. Single-cell RT-PCR confirmed this cell-type assignment. Using Ca2+ imaging, we observed that physiologically appropriate concentrations of OXT evoked [Ca2+]i mobilization in a subset of taste cells (EC50 ∼33 nM). OXT-evoked responses were significantly inhibited by the OXTR antagonist, L-371,257. Isolated OXT-responsive taste cells were neither Receptor (Type II) nor Presynaptic (Type III) cells, consistent with our immunofluorescence observations. We also investigated the source of OXT peptide that may act on taste cells. Both RT-PCR and immunostaining suggest that the OXT peptide is not produced in taste buds or in their associated nerves. Finally, we also examined the morphology of taste buds from mice that lack OXTR. Taste buds and their constituent cell types appeared very similar in mice with two, one or no copies of the OXTR gene.Conclusions/SignificanceWe conclude that OXT elicits Ca2+ signals via OXTR in murine taste buds. OXT-responsive cells are most likely a subset of Glial-like (Type I) taste cells. OXT itself is not produced locally in taste tissue and is likely delivered through the circulation. Loss of OXTR does not grossly alter the morphology of any of the cell types contained in taste buds. Instead, we speculate that OXT-responsive Glial-like (Type I) taste bud cells modulate taste signaling and afferent sensory output. Such modulation would complement central pathways of appetite regulation that employ circulating homeostatic and satiety signals.

Oxytocin decreases sweet taste sensitivity in mice

“…The plasma [OXT] for mice injected with vehicle only was ∼0.1 nM, with a range of 0.01 to 0.49 nM, similar to the 0.02 to 0.1 nM value reported in other rodent studies [38, 40, 41]. On the other hand, the EC 50 for central OXT-responsive neurons is ∼22 nM and ∼33 nM for OXT-responsive taste cells [26, 41]. Thus, we selected an i.p.…”

“…We previously reported that OXT receptor is expressed in a subset of murine taste bud cells and that OXT elicits calcium responses from those same cells [26]. Other investigators have shown OXT receptor expression (and OXT-elicited calcium responses) in a cell line derived from human fungiform papillae [27].…”

Taste perception, associated hormonal modulation, and nutrient intake

“…Hormones that bind to receptors on taste cells alter the palatability of food and, therefore, intake. Current knowledge of the hormonal modulation of taste function is summarized in Table 1 [60][61][62][63][64][65][66][67][68][69][70][71][72][73][74][75][76][77] and described in greater detail below.…”

“…The oxytocin receptor, on the other hand, was found on type I taste cells. 72 Oxytocin is presumed to act as an endocrine hormone on taste buds by influencing type I cells and consequently the structure of the taste bud. However, mice deficient in the oxytocin receptor did not show any morphological alterations.…”

“…However, mice deficient in the oxytocin receptor did not show any morphological alterations. 72 Still, some studies suggest a role in the consumption of sweet and salty foods. 73,74 While these studies postulate an impact on food consumption, oxytocin has not been directly linked to modulation of a specific taste quality.…”