Microvillous cells in the olfactory epithelium express elements of the solitary chemosensory cell transduction signaling cascade

PLoS One. 2018 Sep 13;13(9):e0202754. doi: 10.1371/journal.pone.0202754. eCollection 2018.

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.

Publication types

  • Research Support, N.I.H., Extramural
  • Research Support, Non-U.S. Gov't

MeSH terms

  • Animals
  • Biomarkers / metabolism
  • Chemoreceptor Cells / metabolism*
  • Choline O-Acetyltransferase / genetics*
  • Choline O-Acetyltransferase / metabolism
  • Gene Expression Profiling
  • Mice
  • Mice, Transgenic
  • Microvilli / metabolism
  • Olfactory Mucosa / metabolism*
  • Olfactory Mucosa / ultrastructure
  • Sequence Analysis, RNA
  • Signal Transduction*
  • TRPM Cation Channels / genetics*
  • TRPM Cation Channels / metabolism
  • Taste / genetics
  • Trigeminal Nerve / metabolism

Substances

  • Biomarkers
  • TRPM Cation Channels
  • Trpm5 protein, mouse
  • Choline O-Acetyltransferase