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Volume 17, Number 15, Issue of August 1, 1997 pp. 5772-5781
Copyright ©1997 Society for Neuroscience

Ca²⁺- and Voltage-Dependent Inactivation of Ca²⁺ Channels in Nerve Terminals of the Neurohypophysis

Received March 27, 1997; revised May 14, 1997; accepted May 20, 1997.

Janet L. Branchaw, Matthew I. Banks, and Meyer B. Jackson

Department of Physiology, University of Wisconsin Medical School, Madison, Wisconsin 53706

Ca²⁺ channel inactivation was investigated in neurohypophysial nerve terminals by using patch-clamp techniques. The contribution of intracellular Ca²⁺ to inactivation was evaluated by replacing Ca²⁺ with Ba²⁺ or by including BAPTA in the internal recording solution. Ca²⁺ channel inactivation during depolarizing pulses was primarily voltage-dependent. A contribution of intracellular Ca²⁺ was revealed by comparing steady-state inactivation of Ca²⁺ channels with Ca²⁺ current and with intracellular [Ca²⁺]. However, this contribution was small compared to that of voltage. In contrast to voltage-gated Ca²⁺ channels in other preparations, in the neurohypophysis Ba²⁺ substitution or intracellular BAPTA increased the speed of inactivation while reducing the steady-state level of inactivation. Ca²⁺ channel recovery from inactivation was studied by using a paired-pulse protocol. The rate of Ca²⁺ channel recovery from inactivation at negative potentials was increased dramatically by Ba²⁺ substitution or intracellular BAPTA, indicating that intracellular Ca²⁺ inhibits recovery. Stimulation with trains of brief pulses designed to mimic physiological bursts of electrical activity showed that Ca²⁺ channel inactivation was much greater with 20 Hz trains than with 14 Hz trains. Inactivation induced by 20 Hz trains was reduced by intracellular BAPTA, suggesting an important role for Ca²⁺-dependent inactivation during physiologically relevant forms of electrical activity. Inhibitors of calmodulin and calcineurin had no effect on Ca²⁺ channel inactivation, arguing against a mechanism of inactivation involving these Ca²⁺-dependent proteins. The inactivation behavior described here, in which voltage effects on Ca²⁺ channel inactivation predominate at positive potentials and Ca²⁺ effects predominate at negative potentials, may be relevant to the regulation of neuropeptide release.

Key words: posterior pituitary; Ca²⁺ channels; neurosecretion; oxytocin; vasopressin; fura-2; frequency-dependent depression; synaptic plasticity

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