Two members of the TRPP family of ion channels, <i>Pkd1l3</i> and <i>Pkd2l1</i>, are co‐expressed in a subset of taste receptor cells

LopezJimenez, Nelson D.; Cavenagh, Margaret M.; Sainz, Eduardo; Cruz-Ithier, Mayra A.; Battey, James F.; Sullivan, Stephen N.

doi:10.1111/j.1471-4159.2006.03842.x

Cited by 165 publications

(126 citation statements)

References 71 publications

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“…Salty and sour stimuli are likely transduced by different cells than are bitter, sweet, and umami tastants because they are not believed to be transduced through cells expressing G-proteincoupled taste receptors and PLC␤2 (Huang et al, 2006;Ishimaru et al, 2006;Lopez-Jimenez et al, 2006). It is not confidently known which class of taste cells (i.e., receptor, presynaptic) is involved in salty and sour taste transduction.…”

Section: Presynaptic Cells Respond To Sour and Salty Stimulimentioning

confidence: 99%

Breadth of Tuning and Taste Coding in Mammalian Taste Buds

Tomchik¹,

Berg²,

Kim³

et al. 2007

J. Neurosci.

215

270

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A longstanding question in taste research concerns taste coding and, in particular, how broadly are individual taste bud cells tuned to taste qualities (sweet, bitter, umami, salty, and sour). Taste bud cells express G-protein-coupled receptors for sweet, bitter, or umami tastes but not in combination. However, responses to multiple taste qualities have been recorded in individual taste cells. We and others have shown previously there are two classes of taste bud cells directly involved in gustatory signaling: "receptor" (type II) cells that detect and transduce sweet, bitter, and umami compounds, and "presynaptic" (type III) cells. We hypothesize that receptor cells transmit their signals to presynaptic cells. This communication between taste cells could represent a potential convergence of taste information in the taste bud, resulting in taste cells that would respond broadly to multiple taste stimuli. We tested this hypothesis using calcium imaging in a lingual slice preparation. Here, we show that receptor cells are indeed narrowly tuned: 82% responded to only one taste stimulus. In contrast, presynaptic cells are broadly tuned: 83% responded to two or more different taste qualities. Receptor cells responded to bitter, sweet, or umami stimuli but rarely to sour or salty stimuli. Presynaptic cells responded to all taste qualities, including sour and salty. These data further elaborate functional differences between receptor cells and presynaptic cells, provide strong evidence for communication within the taste bud, and resolve the paradox of broad taste cell tuning despite mutually exclusive receptor expression.

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Section: Presynaptic Cells Respond To Sour and Salty Stimulimentioning

confidence: 99%

Breadth of Tuning and Taste Coding in Mammalian Taste Buds

Tomchik¹,

Berg²,

Kim³

et al. 2007

J. Neurosci.

215

270

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“…Lopez Jimenez et al [25] first reported the expression of these channels in a subset of mouse taste cells. Later, Ishimaru et al [26] confirmed and extended those findings by expressing PKD1L3 and PKD2L1 in HEK293 cells and showing that the transfected cells generated an inward current upon acid stimulation.…”

Section: Sour Transduction Mechanismsmentioning

confidence: 99%

Signal transduction and information processing in mammalian taste buds

Roper

2007

Pflugers Arch - Eur J Physiol

266

215

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The molecular machinery for chemosensory transduction in taste buds has received considerable attention within the last decade. Consequently, we now know a great deal about sweet, bitter, and umami taste mechanisms and are gaining ground rapidly on salty and sour transduction. Sweet, bitter, and umami tastes are transduced by G-protein-coupled receptors. Salty taste may be transduced by epithelial Na channels similar to those found in renal tissues. Sour transduction appears to be initiated by intracellular acidification acting on acidsensitive membrane proteins. Once a taste signal is generated in a taste cell, the subsequent steps involve secretion of neurotransmitters, including ATP and serotonin. It is now recognized that the cells responding to sweet, bitter, and umami taste stimuli do not possess synapses and instead secrete the neurotransmitter ATP via a novel mechanism not involving conventional vesicular exocytosis. ATP is believed to excite primary sensory afferent fibers that convey gustatory signals to the brain. In contrast, taste cells that do have synapses release serotonin in response to gustatory stimulation. The postsynaptic targets of serotonin have not yet been identified. Finally, ATP secreted from receptor cells also acts on neighboring taste cells to stimulate their release of serotonin. This suggests that there is important information processing and signal coding taking place in the mammalian taste bud after gustatory stimulation.

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“…Both strong acids, such as hydrochloric acid, and weak acids, such as acetic or citric acid, produce a sour sensation in humans and evoke sensory responses in nerve recordings in a variety of model organisms, including rat, mouse, and hamster (4)(5)(6)(7). A number of molecules have been proposed to transduce sour taste, most recently the ion channel PKD2L1/PKD1L3 (8)(9)(10)(11)(12), but their role in taste transduction remains unclear as subsequent studies using knockout mouse strains have failed to identify significant effects on sour taste (13)(14)(15). Nonetheless, the Pkd2l1 gene serves as a useful marker for sour taste cells (also designated type III cells), which account for ∼10% of the ∼50-100 taste cells found in each taste bud (1,9,11,16,17).…”

mentioning

confidence: 99%

“…A number of molecules have been proposed to transduce sour taste, most recently the ion channel PKD2L1/PKD1L3 (8)(9)(10)(11)(12), but their role in taste transduction remains unclear as subsequent studies using knockout mouse strains have failed to identify significant effects on sour taste (13)(14)(15). Nonetheless, the Pkd2l1 gene serves as a useful marker for sour taste cells (also designated type III cells), which account for ∼10% of the ∼50-100 taste cells found in each taste bud (1,9,11,16,17). Previously, using a Pkd2l1-YFP mouse, we showed that sour cells express a unique Zn 2+ -sensitive proton conductance, of unknown identity, that is likely to mediate the initial event in taste transduction (16).…”

mentioning

confidence: 99%

The K ⁺ channel K _IR 2.1 functions in tandem with proton influx to mediate sour taste transduction

Chang

Bushman

et al. 2015

Proc. Natl. Acad. Sci. U.S.A.

111

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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.

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Two members of the TRPP family of ion channels, Pkd1l3 and Pkd2l1, are co‐expressed in a subset of taste receptor cells

Cited by 165 publications

References 71 publications

Breadth of Tuning and Taste Coding in Mammalian Taste Buds

Breadth of Tuning and Taste Coding in Mammalian Taste Buds

Signal transduction and information processing in mammalian taste buds

The K ⁺ channel K _IR 2.1 functions in tandem with proton influx to mediate sour taste transduction

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Two members of the TRPP family of ion channels, Pkd1l3 and Pkd2l1, are co‐expressed in a subset of taste receptor cells

Cited by 165 publications

References 71 publications

Breadth of Tuning and Taste Coding in Mammalian Taste Buds

Breadth of Tuning and Taste Coding in Mammalian Taste Buds

Signal transduction and information processing in mammalian taste buds

The K + channel K IR 2.1 functions in tandem with proton influx to mediate sour taste transduction

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The K ⁺ channel K _IR 2.1 functions in tandem with proton influx to mediate sour taste transduction