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Research Article

The K+ channel KIR2.1 functions in tandem with proton influx to mediate sour taste transduction

Wenlei Ye, Rui B. Chang, Jeremy D. Bushman, Yu-Hsiang Tu, Eric M. Mulhall, Courtney E. Wilson, Alexander J. Cooper, Wallace S. Chick, David C. Hill-Eubanks, Mark T. Nelson, Sue C. Kinnamon, and Emily R. Liman
PNAS January 12, 2016 113 (2) E229-E238; first published December 1, 2015; https://doi.org/10.1073/pnas.1514282112
Wenlei Ye
aSection of Neurobiology, Department of Biological Sciences, University of Southern California, Los Angeles, CA 90089;
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Rui B. Chang
aSection of Neurobiology, Department of Biological Sciences, University of Southern California, Los Angeles, CA 90089;
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Jeremy D. Bushman
aSection of Neurobiology, Department of Biological Sciences, University of Southern California, Los Angeles, CA 90089;
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Yu-Hsiang Tu
aSection of Neurobiology, Department of Biological Sciences, University of Southern California, Los Angeles, CA 90089;
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Eric M. Mulhall
aSection of Neurobiology, Department of Biological Sciences, University of Southern California, Los Angeles, CA 90089;
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Courtney E. Wilson
bDepartment of Otolaryngology, University of Colorado Medical School, Aurora, CO 80045;
cRocky Mountain Taste and Smell Center, University of Colorado Medical School, Aurora, CO 80045;
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Alexander J. Cooper
aSection of Neurobiology, Department of Biological Sciences, University of Southern California, Los Angeles, CA 90089;
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Wallace S. Chick
dDepartment of Cell and Developmental Biology, University of Colorado Medical School, Aurora, CO 80045;
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David C. Hill-Eubanks
eDepartment of Pharmacology, University of Vermont, Burlington, VT 05405;
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Mark T. Nelson
eDepartment of Pharmacology, University of Vermont, Burlington, VT 05405;
fInstitute of Cardiovascular Sciences, University of Manchester, Manchester M13 9PT, United Kingdom
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Sue C. Kinnamon
bDepartment of Otolaryngology, University of Colorado Medical School, Aurora, CO 80045;
cRocky Mountain Taste and Smell Center, University of Colorado Medical School, Aurora, CO 80045;
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Emily R. Liman
aSection of Neurobiology, Department of Biological Sciences, University of Southern California, Los Angeles, CA 90089;
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  • For correspondence: liman@USC.edu
  1. Edited by King-Wai Yau, Johns Hopkins University School of Medicine, Baltimore, MD, and approved October 21, 2015 (received for review July 20, 2015)

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    - Dec 30, 2015
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Significance

Among the five basic tastes, sour is one of the least understood. Notably, the sour receptor remains to be identified, and molecular mechanisms by which sour stimuli are detected are largely not known. Previous work has shown that H+ ions can directly enter sour taste cells, eliciting a change in membrane potential and acidification of the cell cytosol. In the present work, we identify a second element of sensory transduction, a K+ channel, KIR2.1, which is inhibited by intracellular acidification. The presence of an acid-sensitive K+ channel in sour taste cells allows for amplification of the sensory response and may explain why weak acids that produce intracellular acidification, such as acetic acid, taste more sour than strong acids.

Abstract

Sour taste is detected by a subset of taste cells on the tongue and palate epithelium that respond to acids with trains of action potentials. Entry of protons through a Zn2+-sensitive proton conductance that is specific to sour taste cells has been shown to be the initial event in sour taste transduction. Whether this conductance acts in concert with other channels sensitive to changes in intracellular pH, however, is not known. Here, we show that intracellular acidification generates excitatory responses in sour taste cells, which can be attributed to block of a resting K+ current. We identify KIR2.1 as the acid-sensitive K+ channel in sour taste cells using pharmacological and RNA expression profiling and confirm its contribution to sour taste with tissue-specific knockout of the Kcnj2 gene. Surprisingly, acid sensitivity is not conferred on sour taste cells by the specific expression of Kir2.1, but by the relatively small magnitude of the current, which makes the cells exquisitely sensitive to changes in intracellular pH. Consistent with a role of the K+ current in amplifying the sensory response, entry of protons through the Zn2+-sensitive conductance produces a transient block of the KIR2.1 current. The identification in sour taste cells of an acid-sensitive K+ channel suggests a mechanism for amplification of sour taste and may explain why weak acids that produce intracellular acidification, such as acetic acid, taste more sour than strong acids.

  • proton channel
  • taste cell
  • gustatory
  • inward rectifier
  • potassium channel

Footnotes

  • ↵1Present address: Department of Cell Biology, Harvard Medical School, Boston, MA 02115.

  • ↵2To whom correspondence should be addressed. Email: liman{at}USC.edu.
  • Author contributions: W.Y., R.B.C., J.D.B., Y.-H.T., E.M.M., C.E.W., A.J.C., M.T.N., S.C.K., and E.R.L. designed research; W.Y., R.B.C., J.D.B., Y.-H.T., E.M.M., C.E.W., A.J.C., and E.R.L. performed research; W.S.C., D.C.H.-E., M.T.N., and S.C.K. contributed new reagents/analytic tools; W.Y., R.B.C., J.D.B., Y.-H.T., E.M.M., C.E.W., A.J.C., M.T.N., S.C.K., and E.R.L. analyzed data; and W.Y., R.B.C., J.D.B., M.T.N., S.C.K., and E.R.L. wrote the paper.

  • The authors declare no conflict of interest.

  • This article is a PNAS Direct Submission.

  • See Commentary on page 246.

  • This article contains supporting information online at www.pnas.org/lookup/suppl/doi:10.1073/pnas.1514282112/-/DCSupplemental.

Freely available online through the PNAS open access option.

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KIR2.1 is a component of sour taste transduction
Wenlei Ye, Rui B. Chang, Jeremy D. Bushman, Yu-Hsiang Tu, Eric M. Mulhall, Courtney E. Wilson, Alexander J. Cooper, Wallace S. Chick, David C. Hill-Eubanks, Mark T. Nelson, Sue C. Kinnamon, Emily R. Liman
Proceedings of the National Academy of Sciences Jan 2016, 113 (2) E229-E238; DOI: 10.1073/pnas.1514282112

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KIR2.1 is a component of sour taste transduction
Wenlei Ye, Rui B. Chang, Jeremy D. Bushman, Yu-Hsiang Tu, Eric M. Mulhall, Courtney E. Wilson, Alexander J. Cooper, Wallace S. Chick, David C. Hill-Eubanks, Mark T. Nelson, Sue C. Kinnamon, Emily R. Liman
Proceedings of the National Academy of Sciences Jan 2016, 113 (2) E229-E238; DOI: 10.1073/pnas.1514282112
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