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Accumulated caveolae constitute subcellular compartments for glial calcium signaling in lanceolate sensory endings innervating rat vibrissae

The terminal Schwann cells that accompany lanceolate sensory endings in the rat vibrissal follicle are known to display the small plasma membrane invaginations termed caveolae, which concentrate Ca2+ signaling molecules. We have previously shown that these cells generate Ca2+ signals at the lamellar processes covering the receptor axons through activation of the metabotropic purinoceptor P2Y2. To investigate the roles of caveolae in the spatiotemporal organization of Ca2+ signals, terminal Schwann cells were observed by immunohistochemistry for the caveola protein caveolin‐1, and by transmission and scanning electron microscopy. In addition, immunohistochemical detection of P2Y2 and its coupling partner Gq/11 along with confocal image analysis of the purinergically induced glial Ca2+ responses was performed in isolated tissue preparations either treated or untreated with the caveolae eliminator methyl‐β‐cyclodextrin. Results showed the Schwann lamellae to be characterized by the presence of dense caveolae accompanying a fine tubular network of the endoplasmic reticulum Ca2+ store and by intense expression of the signaling molecules P2Y2 and Gq/11. Loss of caveolae diffusely redistributed these molecules throughout the entire cell and impaired the lamellar Ca2+ signals, both in chronological priority (preceding the global cell response) and in spatial integrity (involving the entire length of the processes). To our knowledge, this is the first report of a subcellular accumulation of caveolae underlying compartmentalized glial Ca2+ signals that can couple with local effects on the accompanying axon terminals. J. Comp. Neurol. 520:2053–2066, 2012. © 2011 Wiley Periodicals, Inc.