Amiloride-Insensitive Salt Taste Is Mediated by Two Populations of Type III Taste Cells with Distinct Transduction Mechanisms

Overview

Journal J Neurosci

Specialty Neurology

Date 2016 Feb 12

PMID 26865617

Citations 69

Authors

Brian C Lewandowski

Sunil K Sukumaran

Robert F Margolskee

Alexander A Bachmanov

Affiliations

Soon will be listed here.

Abstract

Significance Statement: Understanding the mechanisms underlying salty taste will help inform strategies to combat the health problems associated with NaCl overconsumption by humans. Of the two pathways underlying salty taste in mammals, the amiloride-insensitive (AI) pathway is the least understood. Using calcium imaging of isolated mouse taste cells, we identify two separate populations of AI salt-responsive type III taste cells distinguished by their sensitivity to anion size and show that these cells compose subpopulations of acid-responsive taste cells. We also find evidence that a sodium-conducting osmotically sensitive mechanism contributes to salt responses in type III taste cells. Our data not only provide new insights into the transduction mechanisms of AI salt taste but also have important implications for general theories of taste encoding.

Citing Articles

Nutrient Sensing by Lingual G-Protein-Coupled Taste Receptors.

Dutta Banik D, Medler K Methods Mol Biol. 2025; 2882:317-327.

PMID: 39992517 DOI: 10.1007/978-1-0716-4284-9_16.

Differential Effect of TRPV1 Modulators on Neural and Behavioral Responses to Taste Stimuli.

Rhyu M, Ozdener M, Lyall V Nutrients. 2024; 16(22).

PMID: 39599644 PMC: 11597080. DOI: 10.3390/nu16223858.

The complexities of salt taste reception: insights into the role of TMC4 in chloride taste detection.

Kasahara Y, Narukawa M, Saito Y, Abe K, Asakura T Front Mol Neurosci. 2024; 17:1468438.

PMID: 39386048 PMC: 11461469. DOI: 10.3389/fnmol.2024.1468438.

Deciphering Peripheral Taste Neuron Diversity: Using Genetic Identity to Bridge Taste Bud Innervation Patterns and Functional Responses.

Ohman L, Huang T, Unwin V, Singh A, Walters B, Whiddon Z J Neurosci. 2024; 44(46).

PMID: 39379155 PMC: 11561867. DOI: 10.1523/JNEUROSCI.0583-24.2024.

Novel Perspective on the Plasticity of Taste Perception: Is Food- and Exercise-Induced Inflammation Associated with Sweet Taste Sensitivity and Preference?.

Kimmeswenger I, Lieder B J Agric Food Chem. 2024; 72(27):15122-15127.

PMID: 38941285 PMC: 11247480. DOI: 10.1021/acs.jafc.3c09028.

References

Nelson G, Finger T . Immunolocalization of different forms of neural cell adhesion molecule (NCAM) in rat taste buds. J Comp Neurol. 1993; 336(4):507-16. DOI: 10.1002/cne.903360404. View

Ye Q, Heck G, DeSimone J . Effects of voltage perturbation of the lingual receptive field on chorda tympani responses to Na+ and K+ salts in the rat: implications for gustatory transduction. J Gen Physiol. 1994; 104(5):885-907. PMC: 2229243. DOI: 10.1085/jgp.104.5.885. View

Kitada Y . Anions modulate cation-induced responses of single units of the frog glossopharyngeal nerve. Brain Res. 1995; 694(1-2):253-63. DOI: 10.1016/0006-8993(95)00779-p. View

Gutierrez R, Carroll R, Wang N, Lee G, Taylor B . Analysis of tomato root initiation using a normal mixture distribution. Biometrics. 1995; 51(4):1461-8. View

Ruiz C, Gutknecht S, Delay E, Kinnamon S . Detection of NaCl and KCl in TRPV1 knockout mice. Chem Senses. 2006; 31(9):813-20. DOI: 10.1093/chemse/bjl024. View

Treesukosol Y, Lyall V, Heck G, DeSimone J, Spector A . A psychophysical and electrophysiological analysis of salt taste in Trpv1 null mice. Am J Physiol Regul Integr Comp Physiol. 2007; 292(5):R1799-809. DOI: 10.1152/ajpregu.00587.2006. View

Tomchik S, Berg S, Kim J, Chaudhari N, Roper S . Breadth of tuning and taste coding in mammalian taste buds. J Neurosci. 2007; 27(40):10840-8. PMC: 3717408. DOI: 10.1523/JNEUROSCI.1863-07.2007. View

Vandenbeuch A, Clapp T, Kinnamon S . Amiloride-sensitive channels in type I fungiform taste cells in mouse. BMC Neurosci. 2008; 9:1. PMC: 2235881. DOI: 10.1186/1471-2202-9-1. View

Hacker K, Laskowski A, Feng L, Restrepo D, Medler K . Evidence for two populations of bitter responsive taste cells in mice. J Neurophysiol. 2008; 99(3):1503-14. DOI: 10.1152/jn.00892.2007. View

10.

Huang Y, Maruyama Y, Stimac R, Roper S . Presynaptic (Type III) cells in mouse taste buds sense sour (acid) taste. J Physiol. 2008; 586(12):2903-12. PMC: 2517205. DOI: 10.1113/jphysiol.2008.151233. View

11.

Frank M, Lundy Jr R, Contreras R . Cracking taste codes by tapping into sensory neuron impulse traffic. Prog Neurobiol. 2008; 86(3):245-63. PMC: 2680288. DOI: 10.1016/j.pneurobio.2008.09.003. View

12.

Yoshida R, Horio N, Murata Y, Yasumatsu K, Shigemura N, Ninomiya Y . NaCl responsive taste cells in the mouse fungiform taste buds. Neuroscience. 2009; 159(2):795-803. DOI: 10.1016/j.neuroscience.2008.12.052. View

13.

Doolin R, Gilbertson T . Distribution and characterization of functional amiloride-sensitive sodium channels in rat tongue. J Gen Physiol. 1996; 107(4):545-54. PMC: 2217005. DOI: 10.1085/jgp.107.4.545. View

14.

Kloub M, Heck G, DeSimone J . Self-inhibition in Ca2+ -evoked taste responses: a novel tool for functional dissection of salt taste transduction mechanisms. J Neurophysiol. 1998; 79(2):911-21. DOI: 10.1152/jn.1998.79.2.911. View

15.

Ninomiya Y . Reinnervation of cross-regenerated gustatory nerve fibers into amiloride-sensitive and amiloride-insensitive taste receptor cells. Proc Natl Acad Sci U S A. 1998; 95(9):5347-50. PMC: 20263. DOI: 10.1073/pnas.95.9.5347. View

16.

Kitada Y, Mitoh Y, Hill D . Salt taste responses of the IXth nerve in Sprague-Dawley rats: lack of sensitivity to amiloride. Physiol Behav. 1998; 63(5):945-9. DOI: 10.1016/s0031-9384(98)00009-2. View

17.

Halpern B . Amiloride and vertebrate gustatory responses to NaCl. Neurosci Biobehav Rev. 1998; 23(1):5-47. DOI: 10.1016/s0149-7634(97)00063-8. View

18.

Lyall V, Heck G, DeSimone J, FELDMAN G . Effects of osmolarity on taste receptor cell size and function. Am J Physiol. 1999; 277(4):C800-13. DOI: 10.1152/ajpcell.1999.277.4.C800. View

19.

Naeini R, Witty M, Seguela P, Bourque C . An N-terminal variant of Trpv1 channel is required for osmosensory transduction. Nat Neurosci. 2005; 9(1):93-8. DOI: 10.1038/nn1614. View

20.

DeFazio R, Dvoryanchikov G, Maruyama Y, Kim J, Pereira E, Roper S . Separate populations of receptor cells and presynaptic cells in mouse taste buds. J Neurosci. 2006; 26(15):3971-80. PMC: 3712837. DOI: 10.1523/JNEUROSCI.0515-06.2006. View