Glutamate may be an efferent transmitter that elicits inhibition in mouse taste buds.

Yijen A Huang,Jeff Grant,Stephen Roper

doi:10.1371/journal.pone.0030662

Abstract

Recent studies suggest that l-glutamate may be an efferent transmitter released from axons innervating taste buds. In this report, we determined the types of ionotropic synaptic glutamate receptors present on taste cells and that underlie this postulated efferent transmission. We also studied what effect glutamate exerts on taste bud function. We isolated mouse taste buds and taste cells, conducted functional imaging using Fura 2, and used cellular biosensors to monitor taste-evoked transmitter release. The findings show that a large fraction of Presynaptic (Type III) taste bud cells (∼50%) respond to 100 µM glutamate, NMDA, or kainic acid (KA) with an increase in intracellular Ca2+. In contrast, Receptor (Type II) taste cells rarely (4%) responded to 100 µM glutamate. At this concentration and with these compounds, these agonists activate glutamatergic synaptic receptors, not glutamate taste (umami) receptors. Moreover, applying glutamate, NMDA, or KA caused taste buds to secrete 5-HT, a Presynaptic taste cell transmitter, but not ATP, a Receptor cell transmitter. Indeed, glutamate-evoked 5-HT release inhibited taste-evoked ATP secretion. The findings are consistent with a role for glutamate in taste buds as an inhibitory efferent transmitter that acts via ionotropic synaptic glutamate receptors.

Highlights

During taste stimulation, important synaptic interactions take place in the taste bud between the different cell types
Vandenbeuch et al [25] showed that kainate-type glutamate receptors are present on Presynaptic (Type III) taste cells
We conducted a series of experiments to test the effects of kainic acid (KA), an AMPA/Kainate receptor agonist, and NMDA on Presynaptic cells

Summary

Introduction

Important synaptic interactions (paracrine and autocrine) take place in the taste bud between the different cell types. It was recently reported that mouse taste buds express subunits for kainate-type glutamate receptors and that glutamate at 1 to 100 mM stimulated Presynaptic (Type III) taste cells, with the conclusion that this excitatory amino acid was an efferent transmitter onto those cells [25]. Consistent with that interpretation, vesicular glutamate transporters are found in fibers innervating mouse taste papillae, suggesting that glutamate is likely released from these fibers onto taste buds [25]. These studies point to a role for glutamate as a neurotransmitter in the peripheral taste pathway, the detailed actions of glutamate in the taste bud at concentrations that unambiguously discriminate synaptic versus taste receptors remains to be tested

Methods

Results

Conclusion