Chloride ions evoke taste sensations by binding to the extracellular ligand-binding domain of sweet/umami taste receptors

Author:

Atsumi Nanako1,Yasumatsu Keiko123ORCID,Takashina Yuriko4,Ito Chiaki1,Yasui Norihisa14ORCID,Margolskee Robert F3ORCID,Yamashita Atsuko14ORCID

Affiliation:

1. Graduate School of Medicine, Dentistry and Pharmaceutical Sciences, Okayama University

2. Tokyo Dental Junior College

3. Monell Chemical Senses Center

4. School of Pharmaceutical Sciences, Okayama University

Abstract

Salt taste sensation is multifaceted: NaCl at low or high concentrations is preferably or aversively perceived through distinct pathways. Cl is thought to participate in taste sensation through an unknown mechanism. Here, we describe Cl ion binding and the response of taste receptor type 1 (T1r), a receptor family composing sweet/umami receptors. The T1r2a/T1r3 heterodimer from the medaka fish, currently the sole T1r amenable to structural analyses, exhibited a specific Cl binding in the vicinity of the amino-acid-binding site in the ligand-binding domain (LBD) of T1r3, which is likely conserved across species, including human T1r3. The Cl binding induced a conformational change in T1r2a/T1r3LBD at sub- to low-mM concentrations, similar to canonical taste substances. Furthermore, oral Cl application to mice increased impulse frequencies of taste nerves connected to T1r-expressing taste cells and promoted their behavioral preferences attenuated by a T1r-specific blocker or T1r3 knock-out. These results suggest that the Cl evokes taste sensations by binding to T1r, thereby serving as another preferred salt taste pathway at a low concentration.

Funder

Japan Society for the Promotion of Science

Mishima Kaiun Memorial Foundation

Salt Science Research Foundation

Publisher

eLife Sciences Publications, Ltd

Subject

General Immunology and Microbiology,General Biochemistry, Genetics and Molecular Biology,General Medicine,General Neuroscience

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1. Progress in Multisensory Synergistic Salt Reduction;Foods;2024-05-25

2. Physiological Integration of Taste and Metabolism;New England Journal of Medicine;2024-05-09

3. Allosteric Sites and Allosteric Regulators of G Protein-Coupled Receptors: Gray Cardinals of Signal Transduction;Journal of Evolutionary Biochemistry and Physiology;2023-12

4. ALLOSTERIC SITES AND ALLOSTERIC REGULATORS OF G-PROTEIN-COUPLED RECEPTORS: GRAY CARDINALS OF SIGNAL TRANSDUCTION;Журнал эволюционной биохимии и физиологии;2023-12-01

5. Physiological roles of chloride ions in bodily and cellular functions;The Journal of Physiological Sciences;2023-11-15

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