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The Journal of Neuroscience, February 25, 2009, 29(8):2654-2662; doi:10.1523/JNEUROSCI.4694-08.2009

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Behavioral/Systems/Cognitive
Sensory Attributes of Complex Tasting Divalent Salts Are Mediated by TRPM5 and TRPV1 Channels

Céline E. Riera,¹ Horst Vogel,² Sidney A. Simon,³ Sami Damak,¹ and Johannes le Coutre¹

¹Nestlé Research Center, Vers-chez-les-Blanc, CH-1000 Lausanne, Switzerland, ²Ecole Polytechnique Fédérale de Lausanne, Institut des Sciences et Ingénierie Chimiques, CH-1015 Lausanne, Switzerland, and ³Department of Neurobiology and Center for Neuroengineering, Duke University, Durham, North Carolina 27710

Correspondence should be addressed to either of the following: Johannes le Coutre or Céline E. Riera (for technical questions), Nestlé Research Center, P.O. Box 44, CH-1000 Lausanne 26, Switzerland, E-mails: Email: johannes.le-coutre{at}rdls.nestle.com or Email: celine.riera{at}epfl.ch

Complex tasting divalent salts (CTDS) are present in our daily diet, contributing to multiple poorly understood taste sensations. CTDS evoking metallic, bitter, salty, and astringent sensations include the divalent salts of iron, zinc, copper, and magnesium. To identify pathways involved with the complex perception of the above salts, taste preference tests (two bottles, brief access) were performed in wild-type (WT) mice and in mice lacking (1) the T1R3 receptor, (2) TRPV1, the capsaicin receptor, or (3) the TRPM5 channel, the latter being necessary for the perception of sweet, bitter, and umami tasting stimuli. At low concentrations, FeSO₄ and ZnSO₄ were perceived as pleasant stimuli by WT mice, and this effect was fully reversed in TRPM5 knock-out mice. In contrast, MgSO₄ and CuSO₄ were aversive to WT mice, but for MgSO₄ the aversion was abolished in TRPM5 knock-out animals, and for CuSO₄, aversion decreased in both TRPV1- and TRPM5-deficient animals. Behavioral tests revealed that the T1R3 subunit of the sweet and umami receptors is implicated in the hedonically positive perception of FeSO₄ and ZnSO₄. For high concentrations of CTDS, the omission of TRPV1 reduced aversion. Imaging studies on heterologously expressed TRPM5 and TRPV1 channels are consistent with the behavioral experiments. Together, these results rationalize the complexity of metallic taste by showing that at low concentrations, compounds such as FeSO₄ and ZnSO₄ stimulate the gustatory system through the hedonically positive T1R3–TRPM5 pathway, and at higher concentrations, their aversion is mediated, in part, by the activation of TRPV1.

Key words: metallic taste; divalent salts; taste preference; TRP channels; T1R3; calcium/voltage imaging

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Received Sept. 30, 2008; revised Dec. 20, 2008; accepted Jan. 13, 2009.

Correspondence should be addressed to either of the following: Johannes le Coutre or Céline E. Riera (for technical questions), Nestlé Research Center, P.O. Box 44, CH-1000 Lausanne 26, Switzerland, E-mails: Email: johannes.le-coutre{at}rdls.nestle.com or Email: celine.riera{at}epfl.ch

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