Abstract
The nasal cavity hosts an array of chemoresponsive cells, including the extended olfactory system and several other cells involved in detection of and responses to irritants. Solitary chemosensory cells (SCCs), which respond to irritants and bacteria, express the transient receptor potential channel TRPM5 an essential element of the taste transduction-signaling cascade. Microvillous cells (MVCs), non-neuronal cells situated in the apical layer of the main olfactory epithelium, also express TRPM5, but their function has not yet been clarified. TRPM5-positive MVCs, like SCCs, show a cholinergic phenotype expressing choline acetyl transferase (ChAT), but none of the other elements of the bitter taste transduction cascade could be detected. We reexamined TRPM5-positive MVCs with more sensitive gene expression and staining techniques to clarify whether they rely only on TRPM5 and ChAT or express other elements of the taste/SCC transduction cascade. Analyzing existing RNA sequencing data from whole olfactory mucosa and isolated olfactory sensory neurons, we determined that several elements of the taste/SCC transduction cascade, including taste receptors, are expressed in the olfactory mucosa in cells other than olfactory sensory neurons. Immunostaining confirmed the presence TRPM5 and ChAT in a subset of cells of the olfactory mucosa, which also showed the expression of PLCB2, gustducin, and T1R3. Specifically, these cells were identified as TRPM5-positive MVCs. Furthermore, we examined whether MVCs are innervated by trigeminal fibers, similarly to SCCs. Using antibodies against trigeminal nerve markers calcitonin gene-related peptide and substance P, we determined that, despite the cholinergic phenotype, most MVCs in the olfactory mucosa lacked consistent trigeminal innervation. Our findings indicate that MVCs, like SCCs, express all the elements of the bitter taste transduction cascade but that, unlike SCCs, they possess only sparse trigeminal innervation. The cholinergic phenotype of MVCs suggests a modulatory function of the surrounding olfactory epithelium, through the release of acetylcholine.
Highlights
In the last few decades, a wide range of different chemoresponsive cells have been described in rodents, including olfactory sensory neurons (OSNs), taste receptor cells, vomeronasal organ neurons, and trigeminal neurons, responsible, respectively, for the detection of odors, tastants, pheromones, and noxious stimuli [1,2,3,4,5,6,7]
solitary chemosensory cells (SCCs) were initially identified in the respiratory epithelium (RE) and vomeronasal organ, Transient receptor channel M5 (TRPM5)-expressing cells were reported in the main olfactory epithelium (MOE), including a small subset of OSNs [17] and the microvillous cells (MVCs) [18,19]
Taking advantage of four genetically modified TrpM5-green fluorescent protein (GFP), Plcb2-GFP, Chat-GFP, and Tas1R3-GFP mice, existing RNA sequencing (RNA-seq) data of olfactory mucosa and single neurons transcriptomes [21], and a different tissue fixation procedure than the one previously used [18,19], we characterized the population of TRPM5-positive MVCs in the MOE
Summary
In the last few decades, a wide range of different chemoresponsive cells have been described in rodents, including olfactory sensory neurons (OSNs), taste receptor cells, vomeronasal organ neurons, and trigeminal neurons, responsible, respectively, for the detection of odors, tastants, pheromones, and noxious stimuli [1,2,3,4,5,6,7]. SCCs express molecular markers of the taste transduction signaling cascade, including taste receptors (T1Rs and T2Rs), transient receptor potential channel 5 (TRPM5), the G protein α-gustducin, phospholipase C beta 2 (PLCB2) and the inositol 1,4,5-trisphosphate receptor, type 3 [10,11]. SCCs were initially identified in the RE and vomeronasal organ, TRPM5-expressing cells were reported in the main olfactory epithelium (MOE), including a small subset of OSNs [17] and the microvillous cells (MVCs) [18,19]
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