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All classes of calcium channel couple with equal efficiency to exocytosis in rat melanotropes, inducing linear stimulus-secretion coupling

Huibert D. Mansvelder and Karel S. Kits

1. The contribution of low voltage-activated (LVA) T-type Ca²⁺ channels and four different types of high voltage-activated (HVA) Ca²⁺ channel to exocytosis, and the relationship between calcium influx and exocytosis during action potentials (APs) were studied in pituitary melanotropes.

2. Selective HVA Ca²⁺ channel blockers reduced exocytosis, monitored by membrane capacitance measurements, proportional to the reduction in Ca²⁺ influx. The efficacy of Ca²⁺ in stimulating exocytosis did not change in the presence of the Ca²⁺ channel blockers, indicating that all HVA Ca²⁺ channels act together in stimulating exocytosis.

3. The relationship between Ca²⁺ influx and exocytosis during the AP was examined using APs recorded from spontaneously active melanotropes as command templates under voltage clamp. Under voltage clamp, multiphasic Ca²⁺ currents were activated over the entire duration of the APs, i.e. during the rising phase as well as the plateau phase. The maximum amplitude of the Ca²⁺ current coincided with the peak of the AP.

4. The relationship between Ca²⁺ entry and exocytosis was linear for the different phases of the AP. Also, the influx of Ca²⁺ through LVA T-type channels stimulated exocytosis with the same efficacy as through the HVA channels.

5. APs of increasing duration (~50 to ~300 ms) evoked increasing amounts of exocytosis. The number of entering Ca²⁺ ions and the capacitance change were linearly related to AP duration, resulting in a fixed relationship between Ca²⁺ entry and exocytosis.

6. The results show that Ca²⁺ ions, entering a melanotrope, couple with equal strength to exocytosis regardless of the channel type involved. We suggest that the linear relationship between Ca²⁺ entry and secretion observed under physiological conditions (during APs), results from the equal strength with which LVA and HVA channels in melanotropes couple to exocytosis. This guarantees that secretion takes place over the entire duration of the AP.

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