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Ca²⁺ influx in resting rat sensory neurones that regulates and is regulated by ryanodine-sensitive Ca²⁺ stores

Yuriy M. Usachev and Stanley A. Thayer

Store-operated, voltage-independent Ca²⁺ channels are activated by depletion of intracellular Ca²⁺ stores and mediate Ca²⁺ influx into non-excitable cells at resting membrane potential. We used microfluorimetry, patch-clamp and Mn²⁺-quench techniques to explore the possibility that a similar mechanism exists in rat dorsal root ganglion (DRG) neurones in primary culture.

Following caffeine-induced depletion, ryanodine-sensitive Ca²⁺ stores refilled with Ca²⁺ at resting membrane potential. The refilling process required extracellular Ca²⁺, was blocked by 2 mM Ni²⁺, and was facilitated by membrane hyperpolarization from -55 to -80 mV, indicating a key role for Ca²⁺ influx. This influx of Ca²⁺ was not affected by the voltage-operated Ca²⁺ channel (VOCC) antagonists nicardipine (10 µM), nimodipine (10 µM) or -grammotoxin SIA (1 µM).

When ryanodine-sensitive Ca²⁺ stores were depleted in Ca²⁺-free media, a return to 2 mM external Ca²⁺ resulted in a pronounced [Ca²⁺]_i overshoot, indicating an increased permeability to Ca²⁺. Depletion of Ca²⁺ stores also produced a 2-fold increase in the rate of Mn²⁺ influx. The [Ca²⁺]_i overshoot and Mn²⁺ entry were both inhibited by Ni²⁺, but not by VOCC antagonists.

Caffeine induced periodic Ca²⁺ release from, and reuptake into, ryanodine-sensitive stores. The [Ca²⁺]_i oscillations were arrested by removal of extracellular Ca²⁺ or by addition of Ni²⁺, but they were not affected by VOCC antagonists. Hyperpolarization increased the frequency of this rhythmic activity.

These data suggest the presence of a Ca²⁺ entry pathway in mammalian sensory neurones that is distinct from VOCCs and is regulated by ryanodine-sensitive Ca²⁺ stores. This pathway participates in refilling intracellular Ca²⁺ stores and maintaining [Ca²⁺]_i oscillations and thus controls the balance between intra- and extracellular Ca²⁺ reservoirs in resting DRG neurones.

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