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The Journal of Neuroscience, June 1, 2003, 23(11):4737-4745

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Transient Receptor Potential Channel Activation Causes a Novel Form of [Ca ²⁺]_i Oscillations and Is Not Involved in Capacitative Ca ²⁺ Entry in Glial Cells

Maurizio Grimaldi, Marina Maratos, and Ajay Verma

Department of Neurology, Uniformed Services University of the Health Sciences, Bethesda, Maryland 20814

Astrocytes express transient receptor potential channels (TRPCs), which have been implicated in Ca ²⁺ influx triggered by intracellular Ca ²⁺ stores depletion, a phenomenon known as capacitative Ca ²⁺ entry. We studied the properties of capacitative Ca ²⁺ entry in astrocytes by means of single-cell Ca ²⁺ imaging with the aim of understanding the involvement of TRPCs in this function. We found that, in astrocytes, capacitative Ca ²⁺ entry is not attributable to TRPC opening because the TRPC-permeable ions Sr²⁺ and Ba²⁺ do not enter astrocytes during capacitative Ca ²⁺ entry. Instead, natively expressed oleyl-acetyl-glycerol (OAG) (a structural analog of DAG) -sensitive TRPCs, when activated, initiate oscillations of cytosolic Ca ²⁺ concentration ([Ca ²⁺]_i) pharmacologically and molecularly consistent with TRPC3 activation. OAG-induced [Ca ²⁺]_i oscillations are not affected by inhibition of inositol trisphosphate (InsP₃) production or blockade of the InsP₃ receptor, therefore representing a novel form of [Ca ²⁺]_i signaling. Instead, high [Ca ²⁺]_i inhibited oscillations, by closing the OAG-sensitive channel. Also, treatment of astrocytes with antisense against TRPC3 caused a consistent decrease of the cells responding to OAG. Exogenous OAG but not endogenous DAG seems to activate TRPC3. In conclusion, in glial cells, natively expressed TRPC3s mediates a novel form of Ca ²⁺ signaling, distinct from capacitative Ca ²⁺ entry, which suggests a specific signaling function for this channel in glial cells.

Key words: astrocyte; transient receptor potential channel; store-operated Ca ²⁺ channels; [Ca ²⁺]_i oscillations; capacitative Ca ²⁺ entry; C6 glioma cells

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Received Dec. 2, 2002; revised Mar. 12, 2003; accepted Mar. 12, 2003.

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