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Signalling pathway for histamine activation of non-selective cation channels in equine tracheal myocytes

Yong-Xiao Wang and Michael I. Kotlikoff

1. The signalling pathway underlying histamine activation of non-selective cation channels was investigated in single equine tracheal myocytes. Application of histamine (100 µM) activated the transient calcium-activated chloride current (I_Cl(Ca)) and sustained, low amplitude non-selective cation current (I_Cat). The H₁ receptor antagonist pyrilamine (10 µM) blocked activation of I_Cl(Ca) and I_Cat. Simultaneous application of histamine (100 µM) and caffeine (8 mM) during H₁ receptor blockade activated I_Cl(Ca), but not I_Cat. Neither the H₂ receptor antagonist cimetidine (20 µM) nor the H₃ receptor antagonist thioperamide (20 µM) prevented activation of I_Cl(Ca) and I_Cat.

2. Intracellular dialysis of anti-G_i/G_o antibodies completely blocked activation of I_Cat by histamine, whereas I_Cl(Ca) was not affected. By contrast, anti-G_q/G₁₁ antibodies greatly inhibited I_Cl(Ca), but did not alter activation of I_Cat.

3. 1-Oleoyl-2-acetyl-sn-glycerol (OAG, 20-100 µM) did not induce any current or affect currents activated by histamine or methacholine (mACH). Simultaneous application of OAG and caffeine activated I_Cl(Ca), but not I_Cat, indicating that a rise in [Ca²⁺]_i and stimulation of diacylglycerol-sensitive protein kinase C (PKC) is not sufficient to activate I_Cat. The phospholipase C inhibitor U73122 (2 µM) blocked histamine activation of I_Cl(Ca) and I_Cat, but simultaneous exposure of myocytes to histamine and caffeine restored both I_Cl(Ca) and I_Cat in the presence of U73122.

4. Histamine and mACH activated currents with equivalent I-V relationships. The currents activated by these agonists were not additive; following activation of I_Cat by mACH, histamine failed to induce an additional membrane current. Similarly, mACH did not induce an additional current after full activation of I_Cat by histamine.

5. We conclude that H₁ histamine receptors activate I_Cat through coupling to G_i/G_o proteins. Activation of I_Cat also requires intracellular calcium release, mediated by H₁ receptors coupling to G_q/G₁₁ proteins. This coupling is analogous to the activation of I_Cat by co-stimulation of M₂ and M₃ receptors.

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