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Relationship between Inositol 1,4,5-Trisphosphate Receptor Isoforms and Subcellular Ca²⁺ Signaling Patterns in Nonpigmented Ciliary Epithelia

From the Departments of ¹ Ophthalmology and Visual Sciences, ² Medicine and Cell Biology, Yale University School of Medicine, New Haven, Connecticut.

Abstract

PURPOSE. Subcellular Ca²⁺ signaling patterns, such as Ca²⁺ waves, gradients, and oscillations, are an important aspect of cell regulation, but the molecular basis for these signaling patterns is not understood. Because Ca²⁺ release patterns differ among isoforms of the inositol 1,4,5-trisphosphate (InsP3) receptor, the relationship between the distribution of these isoforms and subcellular Ca²⁺ signaling patterns in nonpigmented epithelial (NPE) cells was investigated.

METHODS. The distributions of the types I, II, and III InsP3 receptors were determined in NPE cells by immunofluorescence, and subcellular Ca²⁺ signaling patterns in these cells were examined by confocal line scanning microscopy.

RESULTS. The type I InsP3 receptor was concentrated at the basal pole of NPE cells, whereas the type III receptor was localized to the apical pole. The type II InsP3 receptor was not expressed in detectable amounts. Acetylcholine induced increases in Ca²⁺ that were mediated by InsP3, and these Ca²⁺ increases began as Ca²⁺ waves that were initiated at the apical pole, in the region of the type III InsP3 receptor. Acetylcholine occasionally induced sustained or repetitive Ca²⁺ increases that were prominent at the basal pole, in the region of the type I InsP3 receptor, but only subtle or absent apically.

CONCLUSIONS. Because the type I InsP3 receptor is thought to be responsible for repetitive Ca²⁺ release events, and the type III InsP3 receptor instead is suited to initiate Ca²⁺ signals, the subcellular distribution of these two isoforms corresponds to the Ca²⁺ signaling patterns observed in this cell type. Differential subcellular expression of InsP3 receptor isoforms may be an important molecular mechanism by which NPE cells organize their Ca²⁺ signals in space and time.

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