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Activation by bitter substances of a cationic channel in membrane patches excised from the bullfrog taste receptor cell

Takashi Tsunenari *, Takashi Kurahashi ¹ ² and Akimichi Kaneko *

The response to bitter-tasting substances was recorded in outside-out membrane patches excised from the taste receptor cell of the bullfrog fungiform papilla.

Application of a bitter-tasting substance, quinine or denatonium, induced channel openings under conditions in which none of the second messenger candidates or their precursors (e.g. cyclic nucleotide, inositol 1,4,5-trisphosphate, Ca²⁺, ATP and GTP) were present on either side of the membrane. The response could be recorded > 10 min after excision of the patch membrane. These data suggest that the channel was directly gated by the bitter-tasting substances.

No change in response was detected upon addition to the cytoplasmic side of either GDPS (1 mM) or GTPS (1 mM), suggesting that the G protein cascade has no direct relation to response generation.

The quinine-induced current was dose dependent. The lowest effective concentration was approximately 0·1 mM, and the saturating concentration was near 1 mM. The dose-response curve was fitted by the Hill equation with a K_½ of 0·52 mM and a Hill coefficient of 3·8.

The single channel conductance measured in 120 mM NaCl solution was 10 pS. The channel was cation selective, and the ratio of the permeabilities for Na⁺, K⁺ and Cs⁺ (P_Na : P_K : P_Cs) was 1 : 0·48 : 0·39. The unitary conductance was dependent on the extracellular Ca²⁺ concentration ([Ca²⁺]_o); 9·2 pS in a nominally Ca²⁺-free solution, and 4·5 pS in 1·8 mM [Ca²⁺]_o.

The dose dependence, the ion selectivity and the dependence of the unitary conductance on [Ca²⁺]_o were almost identical to those of the quinine-induced whole-cell current reported previously, indicating that the channel activity observed in the excised membrane is the basis of the whole-cell current.

The present observations suggest the new possibility that the cationic channel directly gated by bitter substances is involved in the bitter taste transduction mechanism.

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