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The cells and logic for mammalian sour taste detection

Abstract

Mammals taste many compounds yet use a sensory palette consisting of only five basic taste modalities: sweet, bitter, sour, salty and umami (the taste of monosodium glutamate)1,2. Although this repertoire may seem modest, it provides animals with critical information about the nature and quality of food. Sour taste detection functions as an important sensory input to warn against the ingestion of acidic (for example, spoiled or unripe) food sources1,2,3. We have used a combination of bioinformatics, genetic and functional studies to identify PKD2L1, a polycystic-kidney-disease-like ion channel4, as a candidate mammalian sour taste sensor. In the tongue, PKD2L1 is expressed in a subset of taste receptor cells distinct from those responsible for sweet, bitter and umami taste. To examine the role of PKD2L1-expressing taste cells in vivo, we engineered mice with targeted genetic ablations of selected populations of taste receptor cells. Animals lacking PKD2L1-expressing cells are completely devoid of taste responses to sour stimuli. Notably, responses to all other tastants remained unaffected, proving that the segregation of taste qualities even extends to ionic stimuli. Our results now establish independent cellular substrates for four of the five basic taste modalities, and support a comprehensive labelled-line mode of taste coding at the periphery5,6,7,8,9,10. Notably, PKD2L1 is also expressed in specific neurons surrounding the central canal of the spinal cord. Here we demonstrate that these PKD2L1-expressing neurons send projections to the central canal, and selectively trigger action potentials in response to decreases in extracellular pH. We propose that these cells correspond to the long-sought components of the cerebrospinal fluid chemosensory system11. Taken together, our results suggest a common basis for acid sensing in disparate physiological settings.

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Figure 1: PKD2L1 is expressed in a novel population of TRCs.
Figure 2: PKD2L1-expressing TRCs are the mediators of sour taste.
Figure 3: PKD2L1 is expressed in neurons contacting the central canal of the spinal cord.
Figure 4: PKD2L1-expressing neurons of the central canal fire action potentials in response to pH stimulation.

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Acknowledgements

We thank L. Feng for help with expression studies, A. Becker for generation of antibodies, D. Cowan for sequencing, and K. Briedis for bioinformatics. We especially thank Y. Zhang for introducing us to the spinal cord slice preparation, and superb technical guidance and help with equipment and animals. We thank members of the Zuker laboratory for valuable comments. This research was supported in part by a grant from the National Institute on Deafness and Other Communication Disorders to C.S.Z. and the intramural research program of the NIH, NIDCR (N.J.P.R.). X.C. is a fellow of the HFS program and D.T. is supported by an Emmy-Noether grant of the Deutsche Forschungsgemeinschaft. C.S.Z. is an investigator of the Howard Hughes Medical Institute.

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Correspondence to Charles S. Zuker.

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Huang, A., Chen, X., Hoon, M. et al. The cells and logic for mammalian sour taste detection. Nature 442, 934–938 (2006). https://doi.org/10.1038/nature05084

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