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A Store-Operated Ca²⁺ Influx Pathway in the Bag Cell Neurons of Aplysia

¹Department of Physiology, Queen's University, Kingston, Ontario, Canada; ²Department of Pharmacology, Yale University, New Haven, Connecticut; and ³Department of Physiology and Biophysics, Boston University, Boston, Massachusetts

Submitted 2 February 2006; accepted in final form 24 July 2006

Although store-operated Ca²⁺ influx has been well-studied in nonneuronal cells, an understanding of its nature in neurons remains poor. In the bag cell neurons of Aplysia californica, prior work has suggested that a Ca²⁺ entry pathway can be activated by Ca²⁺ store depletion. Using fura-based imaging of intracellular Ca²⁺ in cultured bag cell neurons, we now characterize this pathway as store-operated Ca²⁺ influx. In the absence of extracellular Ca²⁺, the endoplasmic reticulum Ca²⁺-ATPase inhibitors, cyclopiazonic acid (CPA) or thapsigargin, depleted intracellular stores and elevated intracellular free Ca²⁺. With the subsequent addition of extracellular Ca²⁺, a prominent Ca²⁺ influx was observed. The ryanodine receptor agonist, chloroethylphenol (CEP), also increased intracellular Ca²⁺ but did not initiate store-operated Ca²⁺ influx, despite overlap between CEP- and CPA-sensitive stores. Bafilomycin A, a vesicular H⁺-ATPase inhibitor, liberated intracellular Ca²⁺ from acidic stores and attenuated subsequent Ca²⁺ influx, presumably by replenishing CPA-depleted stores. Store-operated Ca²⁺ influx was partially blocked by low concentrations of La³⁺ or BTP2, and strongly inhibited by either 1-[b-[3-(4-methoxyphenyl)propoxy]-4-methoxyphenethyl]-1H-imidazole (SKF-96365) or a high concentration of Ni²⁺. Regarding IP₃ receptor blockers, 2-aminoethyldiphenyl borate, but not xestospongin C, prevented store-operated Ca²⁺ influx. However, jasplakinolide, an actin stabilizer reported to inhibit this pathway in smooth muscle cell lines, was ineffective. The bag cell neurons initiate reproductive behavior through a prolonged afterdischarge associated with intracellular Ca²⁺ release and neuropeptide secretion. Store-operated Ca²⁺ influx may serve to replenish stores depleted during the afterdischarge or participate in the release of peptide that triggers behavior.

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