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The Journal of Neuroscience, December 15, 2000, 20(24):9059-9070

Origin Sites of Calcium Release and Calcium Oscillations in Frog Sympathetic Neurons

Stefan I. McDonough, Zoltán Cseresnyés, and Martin F. Schneider

Department of Biochemistry and Molecular Biology, University of Maryland Medical School, Baltimore, Maryland 21201

In many neurons, Ca²⁺ signaling depends on efflux of Ca²⁺ from intracellular stores into the cytoplasm via caffeine-sensitive ryanodine receptors (RyRs) of the endoplasmic reticulum. We have used high-speed confocal microscopy to image depolarization- and caffeine-evoked increases in cytoplasmic Ca²⁺ levels in individual cultured frog sympathetic neurons. Although caffeine-evoked Ca²⁺ wave fronts propagated throughout the cell, in most cells the initial Ca²⁺ release was from one or more discrete sites that were several micrometers wide and located at the cell edge, even in Ca²⁺-free external solution. During cell-wide cytoplasmic [Ca²⁺] oscillations triggered by continual caffeine application, the initial Ca²⁺ release that began each Ca²⁺ peak was from the same subcellular site or sites. The Ca²⁺ wave fronts propagated with constant amplitude; the spread was mostly via calcium-induced calcium release. Propagation was faster around the cell periphery than radially inward. Local Ca²⁺ levels within the cell body could increase or decrease independently of neighboring regions, suggesting independent action of spatially separate Ca²⁺ stores. Confocal imaging of fluorescent analogs of ryanodine and thapsigargin, and of MitoTracker, showed potential structural correlates to the patterns of Ca²⁺ release and propagation. High densities of RyRs were found in a ring around the cell periphery, mitochondria in a broader ring just inside the RyRs, and sarco-endoplasmic reticulum Ca²⁺ ATPase pumps in hot spots at the cell edge. Discrete sites at the cell edge primed to release Ca²⁺ from intracellular stores might preferentially convert Ca²⁺ influx through a local area of plasma membrane into a cell-wide Ca²⁺ increase.

Key words: ryanodine receptor; sympathetic neuron; caffeine; confocal microscopy; calcium; calcium wave; calcium oscillations; calcium-induced calcium release; subsurface cistern; fluo-4

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Copyright © 2000 Society for Neuroscience  0270-6474/00/20249059-12$05.00/0

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