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Ryanodine stores and calcium regulation in the inner segments of salamander rods and cones

David Krizaj, F. Anthony Lai* and David R. Copenhagen

Despite the prominent role played by intracellular Ca²⁺ stores in the regulation of neuronal Ca²⁺ homeostasis and in invertebrate photoreception, little is known about their contribution to the control of free Ca²⁺ concentration ([Ca²⁺]_i) in the inner segments of vertebrate photoreceptors. Previously, caffeine-sensitive intracellular Ca²⁺ stores were shown to play a role in regulating glutamate release from photoreceptors. To understand the properties of these intracellular stores better we used pharmacological approaches that alter the dynamics of storage and release of Ca²⁺ from intracellular compartments. Caffeine evoked readily discernible changes in [Ca²⁺]_i in the inner segments of rods, but not cones. Caffeine-evoked Ca²⁺ responses in cone inner segments were unmasked in the presence of inhibitors of the plasma membrane Ca²⁺ ATPases (PMCAs) and mitochondrial Ca²⁺ sequestration. Caffeine-evoked responses were blocked by ryanodine, a selective blocker of Ca²⁺ release and by cyclopiazonic acid, a blocker of Ca²⁺ sequestration into the endoplasmic reticulum. These two inhibitors also substantially reduced the amplitude of depolarization-evoked [Ca²⁺]_i increases, providing evidence for Ca²⁺-induced Ca²⁺ release (CICR) in rods and cones. The magnitude and kinetics of caffeine-evoked Ca²⁺ elevation depended on the basal [Ca²⁺]_i, PMCA activity and on mitochondrial function. These results reveal an intimate interaction between the endoplasmic reticulum, voltage-gated Ca²⁺ channels, PMCAs and mitochondrial Ca²⁺ stores in photoreceptor inner segments, and suggest a role for CICR in the regulation of synaptic transmission.

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