Acid Stimulation (Sour Taste) Elicits GABA and Serotonin Release from Mouse Taste Cells

Yijen A Huang,Stephen D Roper,Elizabeth Pereira,Hiroaki Matsunami

doi:10.1371/journal.pone.0025471

Abstract

Several transmitter candidates including serotonin (5-HT), ATP, and norepinephrine (NE) have been identified in taste buds. Recently, γ-aminobutyric acid (GABA) as well as the associated synthetic enzymes and receptors have also been identified in taste cells. GABA reduces taste-evoked ATP secretion from Receptor cells and is considered to be an inhibitory transmitter in taste buds. However, to date, the identity of GABAergic taste cells and the specific stimulus for GABA release are not well understood. In the present study, we used genetically-engineered Chinese hamster ovary (CHO) cells stably co-expressing GABAB receptors and Gαqo5 proteins to measure GABA release from isolated taste buds. We recorded robust responses from GABA biosensors when they were positioned against taste buds isolated from mouse circumvallate papillae and the buds were depolarized with KCl or a stimulated with an acid (sour) taste. In contrast, a mixture of sweet and bitter taste stimuli did not trigger GABA release. KCl- or acid-evoked GABA secretion from taste buds was Ca2+-dependent; removing Ca2+ from the bathing medium eliminated GABA secretion. Finally, we isolated individual taste cells to identify the origin of GABA secretion. GABA was released only from Presynaptic (Type III) cells and not from Receptor (Type II) cells. Previously, we reported that 5-HT released from Presynaptic cells inhibits taste-evoked ATP secretion. Combined with the recent findings that GABA depresses taste-evoked ATP secretion [1], the present results indicate that GABA and 5-HT are inhibitory transmitters in mouse taste buds and both likely play an important role in modulating taste responses.

Highlights

When mammalian taste buds are stimulated, taste cells release neurotransmitters that excite primary afferent fibers and transmit gustatory signals to the CNS
We tested whether gustatory stimuli excite taste buds to release GABA and if so, which type(s) of taste cells were responsible for the release
We used CGP55845 to verify that biosensor responses were generated by activating GABA receptors, not endogenous ATP receptors (CGP, Figs. 1C, 1D). (Responses to ATP were unaffected by 10 mM CGP55845, but those to GABA were blocked)

Summary

Introduction

When mammalian taste buds are stimulated, taste cells release neurotransmitters that excite primary afferent fibers and transmit gustatory signals to the CNS. These transmitters mediate cellto-cell interactions within the taste bud that play important roles in shaping the output and generating the taste code for gustatory stimuli. Only 5-HT, ATP and NE have been so identified [3,7,11,12,13,14] These transmitters have been shown to be secreted by separate classes of taste cells. Sweet and bitter taste stimuli trigger Receptor (Type II) cells to secrete ATP [12,13]. ATP excites sensory afferents [11] as well as stimulates Presynaptic cells to release 5-HT [12]

Methods

Results

Conclusion