Changes of the biophysical properties of voltage-gated Na+ currents during maturation of the sodium-taste cells in rat fungiform papillae.

Abstract

Taste cells are a heterogeneous population of sensory receptors that undergo continuous turnover. Different chemo-sensitive cell lines rely on action potentials to release the neurotransmitter onto nerve endings. The electrical excitability is due to the presence of a tetrodotoxin-sensitive, voltage-gated sodium current (INa ) similar to that found in neurons. Since the biophysical properties of neuronal INa change during development, we wondered whether the same also occurred in taste cells. Here, we used the patch-clamp recording technique to study INa in salt-sensing cells (sodium cells) of rat fungiform papillae. We identified these cells by exploiting the known blocking effect of amiloride on ENaC, the sodium (salt) receptor. Based on the amplitude of INa , which is known to increase during development, we subdivided sodium cells into two groups: cells with small sodium current (SSC cells; INa <1nA) and cells with large sodium current (LSC cells; INa >1nA). We found that: the voltage dependence of activation and inactivation significantly differed between these subsets; a slowly inactivating sodium current was more prominent in LSC cells; membrane capacitance in SSC cells was larger than in LSC cells. mRNA expression analysis of the α-subunits of voltage-gated sodium channels in fungiform taste buds supported the functional data. Lucifer Yellow labelling of recorded cells revealed that our electrophysiological criterion for distinguishing two broad groups of taste cells was in good agreement with morphological observations for cell maturity. Thus, all these findings are consistent with developmental changes in the voltage-dependent properties of sodium-taste cells. KEY POINTS: Taste cells are sensory receptors that undergo continuous turnover while they detect food chemicals and communicate with afferent nerve fibres. The voltage-gated sodium current (INa ) is a key ion current for generating action potentials in fully differentiated and chemo-sensitive taste cells, which use electrical signalling to release neurotransmitters. Here we show that, during the maturation of rat taste cells involved in salt detection (sodium cells), the biophysical properties of INa , such as voltage dependence of activation and inactivation, change significantly. Our results help reveal how taste cells gain electrical excitability during turnover, a property critical to their operation as chemical detectors that relay sensory information to nerve fibres.