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Distinct Intracellular Calcium Profiles Following Influx Through N- Versus L-Type Calcium Channels: Role of Ca²⁺-Induced Ca²⁺ Release

Program in Neuroscience, Department of Neurobiology, University of Massachusetts Medical School, Worcester, Massachusetts 01605

Submitted 8 December 2003; accepted in final form 22 February 2004

Selective activation of neuronal functions by Ca²⁺ is determined by the kinetic profile of the intracellular calcium ([Ca²⁺]_i) signal in addition to its amplitude. Concurrent electrophysiology and ratiometric calcium imaging were used to measure transmembrane Ca²⁺ current and the resulting rise and decay of [Ca²⁺]_i in differentiated pheochromocytoma (PC12) cells. We show that equal amounts of Ca²⁺ entering through N-type and L-type voltage-gated Ca²⁺ channels result in significantly different [Ca²⁺]_i temporal profiles. When the contribution of N-type channels was reduced by -conotoxin MVIIA treatment, a faster [Ca²⁺]_i decay was observed. Conversely, when the contribution of L-type channels was reduced by nifedipine treatment, [Ca²⁺]_i decay was slower. Potentiating L-type current with BayK8644, or inactivating N-type channels by shifting the holding potential to –40 mV, both resulted in a more rapid decay of [Ca²⁺]_i. Channel-specific differences in [Ca²⁺]_i decay rates were abolished by depleting intracellular Ca²⁺ stores with thapsigargin or by blocking ryanodine receptors with ryanodine, suggesting the involvement of Ca²⁺-induced Ca²⁺ release (CICR). Further support for involvement of CICR is provided by the demonstration that caffeine slowed [Ca²⁺]_i decay while ryanodine at high concentrations increased the rate of [Ca²⁺]_i decay. We conclude that Ca²⁺ entering through N-type channels is amplified by ryanodine receptor mediated CICR. Channel-specific activation of CICR provides a mechanism whereby the kinetics of intracellular Ca²⁺ leaves a fingerprint of the route of entry, potentially encoding the selective activation of a subset of Ca²⁺-sensitive processes within the neuron.

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