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J Biol Chem, Vol. 273, Issue 40, 25686-25694, October 2, 1998

Action Currents Generate Stepwise Intracellular Ca²⁺ Patterns in a Neuroendocrine Cell

From the Department of Cellular Animal Physiology, Institute of Cellular Signaling and Nijmegen Institute for Neurosciences, University of Nijmegen, Toernooiveld 1, 6525 ED Nijmegen, The Netherlands

It is believed that specific patterns of changes in the cytosolic-free calcium concentration ([Ca²⁺]_i) are used to control cellular processes such as gene transcription, cell proliferation, differentiation, and secretion. We recently showed that the Ca²⁺ oscillations in the neuroendocrine melanotrope cells of Xenopus laevis are built up by a number of discrete Ca²⁺ rises, the Ca²⁺ steps. The origin of the Ca²⁺ steps and their role in the generation of long-lasting Ca²⁺ patterns were unclear. By simultaneous, noninvasive measuring of melanotrope plasma membrane electrical activity and the [Ca²⁺]_i, we show that numbers, amplitude, and frequency of Ca²⁺ steps are variable among individual oscillations and are determined by the firing pattern and shape of the action currents. The general Na⁺ channel blocker tetrodotoxin had no effect on either action currents or the [Ca²⁺]_i. Under Na⁺-free conditions, a depolarizing pulse of 20 mM K⁺ induced repetitive action currents and stepwise increases in the [Ca²⁺]_i. The Ca²⁺ channel blocker CoCl₂ eliminated action currents and stepwise increases in the [Ca²⁺]_i in both the absence and presence of high K⁺. We furthermore demonstrate that the speed of Ca²⁺ removal from the cytoplasm depends on the [Ca²⁺]_i, also between Ca²⁺ steps during the rising phase of an oscillation. It is concluded that Ca²⁺ channels, and not Na⁺ channels, are essential for the generation of specific step patterns and, furthermore, that the frequency and shape of Ca²⁺ action currents in combination with the Ca²⁺ removal rate determine the oscillatory pattern.

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