Excitation and Adaptation in the Detection of Hydrogen Ions by Taste Receptor Cells: A Role for cAMP and Ca2+

2002 ◽  
Vol 87 (1) ◽  
pp. 399-408 ◽  
Author(s):  
Vijay Lyall ◽  
Rammy I. Alam ◽  
Tam-Hao T. Phan ◽  
Duy Q. Phan ◽  
Gerard L. Heck ◽  
...  
Keyword(s):  
Voltage Clamp ◽  
Basolateral Membrane ◽  
Taste Receptor ◽  
Intracellular Camp ◽  
Receptor Cells ◽  
Zero Current ◽  
Taste Receptor Cells ◽  
Hcl Concentration ◽  
Nerve Recordings ◽  
Strong Acids

The role of intracellular cAMP and Ca2+ in the excitation and adaptation of taste responses by HCl was investigated by direct measurement of intracellular pH (pHi) in polarized taste receptor cells (TRCs) and by chorda tympani (CT) nerve recordings. Stimulating the tongue with HCl concentrations between 1 and 30 mM caused a dose-dependent increase in CT responses that were insensitive to voltage clamp of the lingual receptive field and to amiloride. At a fixed HCl concentration (20 mM) topical lingual application of 8-chlorophenylthio(CPT)-cAMP increased the magnitude of HCl-induced CT response by twofold under zero current clamp. The magnitude of the CT response increased further at −60 mV and decreased at +60 mV lingual voltage clamp but remained amiloride insensitive. In untreated polarized TRCs, apical stimulation with HCl concentrations between 1 and 30 mM HCl induced sustained decreases in TRC pHi. The magnitude of pHidecrease increased with increasing HCl concentration. Following treatment of the basolateral membrane with 8-CPT-cAMP the decrease in pHi due to apical 1 mM HCl application was significantly increased. Treatment with cAMP alone decreased resting TRC pHi and inhibited the recovery of pHi from a basolateral NH4Cl pulse by 46%. Topical lingual application of ionomycin, a Ca2+ ionophore, did not affect the initial CT response to 20 mM HCl +10 mM CaCl2, but the response declined rapidly to 50% of its initial level within 2 min. In polarized TRCs, basolateral exposure to ionomycin increased TRC pHi and activated pHi recovery from NH4Cl pulse by 388%. Apical HCl stimulation induced a transient decrease in resting TRC pHifollowed by spontaneous recovery. The data suggest that cAMP enhances the sour taste of strong acids by activating a Ca2+- and amiloride-insensitive H+ conductance and inhibiting pHi recovery in TRCs. However, an increase in [Ca2+]i stimulates pHi recovery, which, in turn, increases sensory adaptation to acids.

scholarly journals Modulation of Rat Chorda Tympani NaCl Responses and Intracellular Na+ Activity in Polarized Taste Receptor Cells by pH

2002 ◽  
Vol 120 (6) ◽  
pp. 793-815 ◽  
Author(s):  
Vijay Lyall ◽  
Rammy I. Alam ◽  
Tam-Hao T. Phan ◽  
Oneal F. Russell ◽  
Shahbaz A. Malik ◽  
...  
Keyword(s):  
Apical Membrane ◽  
Taste Receptor ◽  
Potassium Acetate ◽  
Chorda Tympani ◽  
Receptor Cells ◽  
Intracellular Na Activity ◽  
Taste Receptor Cells ◽  
Nerve Recordings ◽  
Acid Loading ◽  
External Ph

Mixture interactions between sour and salt taste modalities were investigated in rats by direct measurement of intracellular pH (pHi) and Na+ activity ([Na+]i) in polarized fungiform taste receptor cells (TRCs) and by chorda tympani (CT) nerve recordings. Stimulating the lingual surface with NaCl solutions adjusted to pHs ranging between 2.0 and 10.3 increased the magnitude of NaCl CT responses linearly with increasing external pH (pHo). At pH 7.0, the epithelial sodium channel (ENaC) blocker, benzamil, decreased NaCl CT responses and inhibited further changes in CT responses induced by varying pHo to 2.0 or 10.3. At constant pHo, buffering NaCl solutions with potassium acetate/acetic acid (KA/AA) or HCO3−/CO2 inhibited NaCl CT responses relative to CT responses obtained with NaCl solutions buffered with HEPES. The carbonic anhydrase blockers, MK-507 and MK-417, attenuated the inhibition of NaCl CT responses in HCO3−/CO2 buffer, suggesting a regulatory role for pHi. In polarized TRCs step changes in apical pHo from 10.3 to 2.0 induced a linear decrease in pHi that remained within the physiological range (slope = 0.035; r2 = 0.98). At constant pHo, perfusing the apical membrane with Ringer's solutions buffered with KA/AA or HCO3−/CO2 decreased resting TRC pHi, and MK-507 or MK-417 attenuated the decrease in pHi in TRCs perfused with HCO3−/CO2 buffer. In parallel experiments, TRC [Na+]i decreased with (a) a decrease in apical pH, (b) exposing the apical membrane to amiloride or benzamil, (c) removal of apical Na+, and (d) acid loading the cells with NH4Cl or sodium acetate at constant pHo. Diethylpyrocarbonate and Zn2+, modification reagents for histidine residues in proteins, attenuated the CO2-induced inhibition of NaCl CT responses and the pHi-induced inhibition of apical Na+ influx in TRCs. We conclude that TRC pHi regulates Na+-influx through amiloride-sensitive apical ENaCs and hence modulates NaCl CT responses in acid/salt mixtures.

scholarly journals Responses to Di-Sodium Guanosine 5′-Monophosphate and Monosodiuml-Glutamate in Taste Receptor Cells of Rat Fungiform Papillae

2003 ◽  
Vol 89 (3) ◽  
pp. 1434-1439 ◽  
Author(s):  
Weihong Lin ◽  
Tatsuya Ogura ◽  
Sue C. Kinnamon
Keyword(s):  
Patch Clamp ◽  
Monosodium Glutamate ◽  
Taste Receptor ◽  
Intracellular Camp ◽  
Fungiform Papillae ◽  
Simultaneous Application ◽  
Umami Taste ◽  
Receptor Cells ◽  
Imaging Results ◽  
Taste Receptor Cells

The 5′-ribonucleotide guanosine 5′-monophosphate (GMP) is used widely as an umami taste stimulus and a potent flavor enhancer as it synergistically increases the umami taste elicited by monosodium glutamate. Transduction mechanisms for GMP and its synergy with glutamate are largely unknown. Using whole-cell patch-clamp and Ca2+ imaging, we examined responses to GMP, glutamate, and a mixture of GMP and glutamate in taste-receptor cells of rat fungiform papillae. Our electrophysiological results showed that GMP induces responses that are similar to those of glutamate, e.g., an outward current, an inward current, or a biphasic response. Our Ca2+ imaging results showed that applications of GMP, glutamate, and the mixture increased intracellular Ca2+ levels. Interestingly, both patch-clamp and Ca2+ imaging showed that some taste cells can respond to GMP and glutamate independently, indicating that glutamate and GMP likely activate different receptors. Simultaneous application of GMP and glutamate resulted in synergistic responses in a subset of cells; both response intensity and number of responding cells were increased. Most responses to GMP, as well as the synergy between GMP and glutamate, were suppressed by 8bromo-adenosine 3′,5′-cyclic monophosphate (8-bromo-cAMP) in patch-clamp recordings. Together, our results suggest that intracellular cAMP- and Ca2+-mediated pathways are involved in umami taste transduction for GMP and its synergistic responses with glutamate.

Acid-induced responses in hamster chorda tympani and intracellular pH tracking by taste receptor cells

1998 ◽  
Vol 275 (1) ◽  
pp. C227-C238 ◽  
Author(s):  
Robert E. Stewart ◽  
Vijay Lyall ◽  
George M. Feldman ◽  
Gerard L. Heck ◽  
John A. DeSimone
Keyword(s):  
Voltage Clamp ◽  
Intracellular Ph ◽  
Imaging Techniques ◽  
Taste Receptor ◽  
Channel Blockers ◽  
Chorda Tympani ◽  
Chorda Tympani Nerve ◽  
Linear Change ◽  
Receptor Cells ◽  
Taste Receptor Cells

HCl- and NaCl-induced hamster chorda tympani nerve responses were recorded during voltage clamp of the lingual receptive field. Voltage perturbations did not influence responses to HCl. In contrast, responses to NaCl were decreased by submucosal-positive and increased by submucosal-negative voltage clamp. Responses to HCl were insensitive to the Na+ channel blockers, amiloride and benzamil, and to methylisobutylamiloride (MIA), an Na+/H+exchange blocker. Responses to NaCl were unaffected by MIA but were suppressed by benzamil. Microfluorometric and imaging techniques were used to monitor the relationship between external pH (pHo) and the intracellular pH (pHi) of fungiform papilla taste receptor cells (TRCs) following 2′,7′-bis(2-carboxyethyl)-5(6)-carboxyfluorescein loading. TRC pHi responded rapidly and monotonically to changes in pHo. This response was unaffected by Na+ removal or the presence of amiloride, benzamil, or MIA. The neural records and the data from isolated TRCs suggest that the principal transduction pathway for acid taste in hamster is similar to that in rat. This may involve the monitoring of changes in TRC pHimediated through amiloride-insensitive H+ transport across TRC membranes. This is an example of cell monitoring of environmental pH through pH tracking, i.e., a linear change in pHi in response to a change in pHo, as has been proposed for carotid bodies. In taste, the H+transport sites may be concentrated on the basolateral membranes of TRCs and, therefore, are responsive to an attenuated H+ concentration from diffusion of acids across the tight junctions.

Taste Transductions in Taste Receptor Cells: Basic Tastes and Moreover

2014 ◽  
Vol 20 (16) ◽  
pp. 2684-2692 ◽  
Author(s):  
Shusuke Iwata ◽  
Ryusuke Yoshida ◽  
Yuzo Ninomiya
Keyword(s):  
Taste Receptor ◽  
Receptor Cells ◽  
Taste Receptor Cells

scholarly journals Role for epithelial Na+channels and putative Na+/H+ exchangers in salt taste transduction in rats

1997 ◽  
Vol 273 (6) ◽  
pp. R1923-R1931 ◽  
Author(s):  
Robert F. Lundy ◽  
David W. Pittman ◽  
Robert J. Contreras
Keyword(s):  
Salt Concentration ◽  
Taste Receptor ◽  
Drug Dose ◽  
Chorda Tympani Nerve ◽  
Sprague Dawley ◽  
Salt Taste ◽  
Receptor Cells ◽  
Taste Transduction ◽  
Taste Receptor Cells ◽  
Dimethyl Amiloride

The effects of the epithelial Na+channel antagonists amiloride and benzamil and the Na+/H+exchange antagonist 5-( N, N-dimethyl)-amiloride (DMA)-Cl on the integrated responses of the chorda tympani nerve to 30, 75, 150, 300, and 500 mM concentrations of NaCl, KCl, and NH4Cl were assessed in male Sprague-Dawley rats. Based on evidence from other systems, 1 and 25 μM amiloride and benzamil were chosen to selectively inhibit epithelial Na+ channels and 1 μM DMA was chosen to selectively inhibit Na+/H+exchange. When added to stimulating salt solutions, amiloride, benzamil, and DMA were each effective in inhibiting responses to all three salts. The degree of inhibition varied with drug, salt, and salt concentration, but not drug dose. Amiloride suppressed NaCl responses to a greater degree than KCl and NH4Cl responses, whereas DMA suppressed NH4Cl responses to a greater degree than NaCl and KCl responses. In all but one case (25 μM amiloride added to KCl), drug suppression of taste nerve responses decreased with an increase in salt concentration. The present results suggest that 1) epithelial Na+ channels in rat taste receptor cells may play a role in KCl and NH4Cl taste transduction; 2) a Na+/H+exchange protein may be present in taste receptor cells, representing a putative component, in addition to epithelial Na+ channels, in salt taste transduction; and 3) salt taste detection and transduction may depend on the utilization of a combination of common and distinct transcellular pathways.

Sign in / Sign up

Export Citation Format

Share Document