Inwardly rectifying potassium (Kir) channels play key roles in functions, including maintaining the resting membrane potential and regulating the action potential duration in excitable cells. Using in situ whole-cell recordings, we investigated Kir currents in mouse fungiform taste bud cells (TBCs) and immunologically identified the cell types (type I-III) expressing these currents. We demonstrated that Kir currents occur in a cell-type-independent manner. The activation potentials we measured were -80 to -90 mV, and the magnitude of the currents increased as the membrane potentials decreased, irrespective of the cell types. The maximum current densities at -120 mV showed no significant differences among cell types (p>0.05, one-way ANOVA). The density of Kir currents was not correlated with the density of either transient inward currents or outwardly rectifying currents, although there was significant correlation between transient inward and outwardly rectifying current densities (p<0.05, test for no correlation). RT-PCR studies employing total RNA extracted from peeled lingual epithelia detected mRNAs for Kir1, Kir2, Kir4, Kir6, and Kir7 families. These findings indicate that TBCs express several types of Kir channels functionally, which may contribute to regulation of the resting membrane potential and signal transduction of taste.

Department of Human Intelligence Systems Graduate School of Life Science and Systems Engineering Kyushu Institute of Technology Kitakyushu Japan

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ADLER E, HOON MA, MUELLER KL, CHANDRASHEKAR J, RYBA NJ, ZUKER CS. A novel family of mammalian taste receptors. Cell. 2000;100:693–702. doi: 10.1016/s0092-8674(00)80705-9. PubMed DOI

BEBAROVA M, MATEJOVIC P, SIMURDOVA M, SIMURDA J. Acetaldehyde at clinically relevant concentrations inhibits inward rectifier potassium current I(K1) in rat ventricular myocytes. Physiol Res. 2015;64:939–943. doi: 10.1007/s00210-017-1341-z. PubMed DOI

CHANDRASHEKAR J, MUELLER KL, HOON MA, ADLER E, FENG L, GUO W, ZUKER CS, RYBA NJ. T2Rs function as bitter taste receptors. Cell. 2000;100:703–711. doi: 10.1016/s0092-8674(00)80706-0. PubMed DOI

CLAPP TR, MEDLER KF, DAMAK S, MARGOLSKEE RF, KINNAMON SC. Mouse taste cells with G protein-coupled taste receptors lack voltage-gated calcium channels and SNAP-25. BMC Biol. 2006;4:7. doi: 10.1186/1741-7007-4-7. PubMed DOI PMC

CLAPP TR, STONE LM, MARGOLSKEE RF, KINNAMON SC. Immunocytochemical evidence for co-expression of Type III IP3 receptor with signaling components of bitter taste transduction. BMC Neurosci. 2001;2:6. doi: 10.1186/1471-2202-2-6. PubMed DOI PMC

DeFAZIO RA, DVORYANCHIKOV G, MARUYAMA Y, KIM JW, PEREIRA E, ROPER SD, CHAUDHARI N. Separate populations of receptor cells and presynaptic cells in mouse taste buds. J Neurosci. 2006;26:3971–3980. doi: 10.1523/jneurosci.0515-06.2006. PubMed DOI PMC

EGUCHI K, OHTUBO Y, YOSHII K. Functional expression of M3, a muscarinic acetylcholine receptor subtype, in taste bud cells of mouse fungiform papillae. Chem Senses. 2008;33:47–55. doi: 10.1093/chemse/bjm065. PubMed DOI

FURUE H, YOSHII K. In situ tight-seal recordings of taste substance-elicited action currents and voltage-gated Ba currents from single taste bud cells in the peeled epithelium of mouse tongue. Brain Res. 1997;776:133–139. doi: 10.1016/s0006-8993(97)00974-8. PubMed DOI

FURUE H, YOSHII K. A method for in-situ tight-seal recordings from single taste bud cells of mice. J Neurosci Methods. 1998;84:109–114. doi: 10.1016/s0165-0270(98)00104-6. PubMed DOI

HAYATO R, OHTUBO Y, YOSHII K. Functional expression of ionotropic purinergic receptors on mouse taste bud cells. J Physiol. 2007;584:473–488. doi: 10.1113/jphysiol.2007.138370. PubMed DOI PMC

HIBINO H, INANOBE A, FURUTANI K, MURAKAMI S, FINDLAY I, KURACHI Y. Inwardly rectifying potassium channels: their structure, function, and physiological roles. Physiol Rev. 2010;90:291–366. doi: 10.1152/physrev.00021.2009. PubMed DOI

HIGURE Y, KATAYAMA Y, TAKEUCHI K, OHTUBO Y, YOSHII K. Lucifer Yellow slows voltage-gated Na+ current inactivation in a light-dependent manner in mice. J Physiol. 2003;550:159–167. doi: 10.1113/jphysiol.2003.040733. PubMed DOI PMC

HUANG YA, MARUYAMA Y, STIMAC R, ROPER SD. Presynaptic (Type III) cells in mouse taste buds sense sour (acid) taste. J Physiol. 2008;586:2903–2912. doi: 10.1113/jphysiol.2008.151233. PubMed DOI PMC

IWAMOTO M, TAKASHIMA M, OHTUBO Y. A subset of taste receptor cells express biocytin-permeable channels activated by reducing extracellular Ca(2+) concentration. Eur J Neurosci. 2020;51:1605–1623. doi: 10.1111/ejn.14672. PubMed DOI

KASHIO M, WEI-QI G, OHSAKI Y, KIDO MA, TARUNO A. CALHM1/CALHM3 channel is intrinsically sorted to the basolateral membrane of epithelial cells including taste cells. Sci Rep. 2019;9:2681. doi: 10.1038/s41598-019-39593-5. PubMed DOI PMC

KATAOKA S, YANG R, ISHIMARU Y, MATSUNAMI H, SÉVIGNY J, KINNAMON JC, FINGER TE. The candidate sour taste receptor, PKD2L1, is expressed by type III taste cells in the mouse. Chem Senses. 2008;33:243–254. doi: 10.1093/chemse/bjm083. PubMed DOI PMC

KIMURA K, OHTUBO Y, TATENO K, TAKEUCHI K, KUMAZAWA T, YOSHII K. Cell-type-dependent action potentials and voltage-gated currents in mouse fungiform taste buds. Eur J Neurosci. 2014;39:24–34. doi: 10.1111/ejn.12388. PubMed DOI

MA Z, SAUNG WT, FOSKETT JK. Action potentials and ion conductances in wild-type and CALHM1-knockout type II taste cells. J Neurophysiol. 2017;117:1865–1876. doi: 10.1152/jn.00835.2016. PubMed DOI PMC

MA Z, TARUNO A, OHMOTO M, JYOTAKI M, LIM JC, MIYAZAKI H, NIISATO N, MARUNAKA Y, LEE RJ, HOFF H, PAYNE R, DEMURO A, PARKER I, MITCHELL CH, HENAO-MEJIA J, TANIS JE, MATSUMOTO I, TORDOFF MG, FOSKETT JK. CALHM3 is essential for rapid ion channel-mediated purinergic neurotransmission of GPCR-mediated tastes. Neuron. 2018;98:547–561.e10. doi: 10.1016/j.neuron.2018.03.043. PubMed DOI PMC

MORI Y, EGUCHI K, YOSHII K, OHTUBO Y. Selective expression of muscarinic acetylcholine receptor subtype M3 by mouse type III taste bud cells. Pflugers Arch. 2016;468:2053–2059. doi: 10.1007/s00424-016-1879-5. PubMed DOI PMC

MURRAY RG. The ultrastructure of taste buds. In: FRIEDMANN I, editor. The Ultrastructure of Sensory Organs. Amsterdam: North-Holland Publishing Company; 1973. pp. 1–81.

NELSON G, CHANDRASHEKAR J, HOON MA, FENG L, ZHAO G, RYBA NJP, ZUKER CS. An amino-acid taste receptor. Nature. 2002;416:199–202. doi: 10.1038/nature726. PubMed DOI

NELSON G, HOON MA, CHANDRASHEKAR J, ZHANG Y, RYBA NJ, ZUKER CS. Mammalian sweet taste receptors. Cell. 2001;106:381–390. doi: 10.1016/s0092-8674(01)00451-2. PubMed DOI

NICHOLS CG. KATP channels as molecular sensors of cellular metabolism. Nature. 2006;440:470–476. doi: 10.1038/nature04711. PubMed DOI

NOGUCHI T, IKEDA Y, MIYAJIMA M, YOSHII K. Voltage-gated channels involved in taste responses and characterizing taste bud cells in mouse soft palates. Brain Res. 2003;982:241–259. doi: 10.1016/s0006-8993(03)03013-0. PubMed DOI

OHTUBO Y, IWAMOTO M, YOSHII K. Subtype-dependent postnatal development of taste receptor cells in mouse fungiform taste buds. Eur J Neurosci. 2012;35:1661–1671. doi: 10.1111/j.1460-9568.2012.08068.x. PubMed DOI

OHTUBO Y, SUEMITSU T, SHIOBARA S, MATSUMOTO T, KUMAZAWA T, YOSHII KY. Optical recordings of taste responses from fungiform papillae of mouse in situ. J Physiol. 2001;530:287–293. doi: 10.1111/j.1469-7793.2001.0287l.x. PubMed DOI PMC

OHTUBO Y, YOSHII K. Quantitative analysis of taste bud cell numbers in fungiform and soft palate taste buds of mice. Brain Res. 2011;1367:13–21. doi: 10.1016/j.brainres.2010.10.060. PubMed DOI

PODZIMEK S, DUSKOVA M, BROUKAL Z, RACZ B, STARKA L, DUSKOVA J. The evolution of taste and perinatal programming of taste preferences. Physiol Res. 2018;67(Suppl 3):S421–S429. doi: 10.33549/physiolres.934026. PubMed DOI

REIMANN F, ASHCROFT FM. Inwardly rectifying potassium channels. Curr Opin Cell Biol. 1999;11:503–508. doi: 10.1016/s0955-0674(99)80073-8. PubMed DOI

ROMANOV RA, LASHER RS, HIGH B, SAVIDGE LE, LAWSON A, ROGACHEVSKAJA OA, ZHAO H, ROGACHEVSKY VV, BYSTROVA MF, CHURBANOV GD, ADAMEYKO I, HARKANY T, YANG R, KIDD GJ, MARAMBAUD P, KINNAMON JC, KOLESNIKOV SV, FINGER TE. Chemical synapses without synaptic vesicles: Purinergic neurotransmission through a CALHM1 channel-mitochondrial signaling complex. Sci Signal. 2018;11:529. doi: 10.1126/scisignal.aao1815. PubMed DOI PMC

ROMANOV RA, ROGACHEVSKAJA OA, BYSTROVA MF, JIANG P, MARGOLSKEE RF, KOLESNIKOV SS. Afferent neurotransmission mediated by hemichannels in mammalian taste cells. EMBO J. 2007;26:657–667. doi: 10.1038/sj.emboj.7601526. PubMed DOI PMC

ROPER SD. Taste buds as peripheral chemosensory processors. Semin Cell Dev Biol. 2013;24:71–79. doi: 10.1016/j.semcdb.2012.12.002. PubMed DOI PMC

SUN XD, HERNESS MS. Characterization of inwardly rectifying potassium currents from dissociated rat taste receptor cells. Am J Physiol. 1996;271:C1221–C1232. doi: 10.1152/ajpcell.1996.271.4.c1221. PubMed DOI

WEN RJ, HUANG D, ZHANG Y, LIU YW. Bis(3)-tacrine inhibits the sustained potassium current in cultured rat hippocampal neurons. Physiol Res. 2017;66:539–544. doi: 10.33549/physiolres.933354. PubMed DOI

YANG R, CROWLEY HH, ROCK ME, KINNAMON JC. Taste cells with synapses in rat circumvallate papillae display SNAP-25-like immunoreactivity. J Comp Neurol. 2000;424:205–215. doi: 10.1002/1096-9861(20000821)424:2<205::aid-cne2>3.0.co;2-f. PubMed DOI

YE W, CHANG RB, BUSHMAN JD, TU YH, MULHALL EM, WILSON CE, COOPER AJ, CHICK WS, HILL-EUBANKS DC, NELSON MT, KINNAMON SC, LIMAN ER. The K+ channel KIR2.1 functions in tandem with proton influx to mediate sour taste transduction. Proc Natl Acad Sci U S A. 2016;113:E229–E238. doi: 10.1073/pnas.1514282112. PubMed DOI PMC

YEE KK, SUKUMARAN SK, KOTHA R, GILBERTSON TA, MARGOLSKEE RF. Glucose transporters and ATP-gated K+ (KATP) metabolic sensors are present in type 1 taste receptor 3 (T1r3)-expressing taste cells. Proc Natl Acad Sci U S A. 2011;108:5431–5436. doi: 10.1073/pnas.1100495108. PubMed DOI PMC

YOSHIDA R, MIYAUCHI A, YASUO T, JYOTAKI M, MURATA Y, YASUMATSU K, SHIGEMURA N, YANAGAWA Y, OBATA K, UENO H, MARGOLSKEE RF, NINOMIYA Y. Discrimination of taste qualities among mouse fungiform taste bud cells. J Physiol. 2009;587:4425–4439. doi: 10.1113/jphysiol.2009.175075. PubMed DOI PMC