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J Neurophysiol 83: 1435-1442, 2000;
0022-3077/00 $5.00
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The Journal of Neurophysiology Vol. 83 No. 3 March 2000, pp. 1435-1442
Copyright ©2000 by the American Physiological Society

Voltage-Dependent, Pertussis Toxin Insensitive Inhibition of Calcium Currents by Histamine in Bovine Adrenal Chromaffin Cells

Kevin P. M. Currie and Aaron P. Fox

Department of Neurobiology, Pharmacology and Physiology, The University of Chicago, Chicago, Illinois 60637

Currie, Kevin P. M. and Aaron P. Fox. Voltage-Dependent, Pertussis Toxin Insensitive Inhibition of Calcium Currents by Histamine in Bovine Adrenal Chromaffin Cells. J. Neurophysiol. 83: 1435-1442, 2000. Histamine is a known secretagogue in adrenal chromaffin cells. Activation of G-protein linked H1 receptors stimulates phospholipase C, which generates inositol trisphosphate leading to release of intracellular calcium stores and stimulation of calcium influx through store operated and other channels. This calcium leads to the release of catecholamines. In chromaffin cells, the main physiological trigger for catecholamine release is calcium influx through voltage-gated calcium channels (ICa). Therefore, these channels are important targets for the regulation of secretion. In particular N- and P/Q-type ICa are subject to inhibition by transmitter/hormone receptor activation of heterotrimeric G-proteins. However, the direct effect of histamine on ICa in chromaffin cells is unknown. This paper reports that histamine inhibited ICa in cultured bovine adrenal chromaffin cells and this response was blocked by the H1 antagonist mepyramine. With high levels of calcium buffering in the patch pipette solution (10 mM EGTA), histamine slowed the activation kinetics and inhibited the amplitude of ICa. A conditioning prepulse to +100 mV reversed the kinetic slowing and partially relieved the inhibition. These features are characteristic of a membrane delimited, voltage-dependent pathway which is thought to involve direct binding of G-protein beta gamma subunits to the Ca channels. However, unlike virtually every other example of this type of inhibition, the response to histamine was not blocked by pretreating the cells with pertussis toxin (PTX). The voltage-dependent, PTX insensitive inhibition produced by histamine was modest compared with the PTX sensitive inhibition produced by ATP (28% vs. 53%). When histamine and ATP were applied concomitantly there was no additivity of the inhibition beyond that produced by ATP alone (even though the agonists appear to activate distinct G-proteins) suggesting that the inhibition produced by ATP is maximal. When experiments were carried out under conditions of low levels of calcium buffering in the patch pipette solution (0.1 mM EGTA), histamine inhibited ICa in some cells using an entirely voltage insensitive pathway. We demonstrate that activation of PTX insensitive G-proteins (most likely Gq) by H1 receptors inhibits ICa. This may represent a mechanism by which histamine exerts inhibitory (in addition to previously identified stimulatory) effects on catecholamine release.




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