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The Journal of Neuroscience, January 15, 2000, 20(2):666-673

SNARE Protein-Dependent Glutamate Release from Astrocytes

Alfonso Araque, Nianzhen Li, Robert T. Doyle, and Philip G. Haydon

Laboratory of Cellular Signaling, Department of Zoology and Genetics, Iowa State University, Ames, Iowa 50011

We investigated the cellular mechanisms underlying the Ca2+-dependent release of glutamate from cultured astrocytes isolated from rat hippocampus. Using Ca2+ imaging and electrophysiological techniques, we analyzed the effects of disrupting astrocytic vesicle proteins on the ability of astrocytes to release glutamate and to cause neuronal electrophysiological responses, i.e., a slow inward current (SIC) and/or an increase in the frequency of miniature synaptic currents. We found that the Ca2+-dependent glutamate release from astrocytes is not caused by the reverse operation of glutamate transporters, because the astrocyte-induced glutamate-mediated responses in neurons were affected neither by inhibitors of glutamate transporters (beta -threo-hydroxyaspartate, dihydrokainate, and L-trans-pyrrolidine-2,4-dicarboxylate) nor by replacement of extracellular sodium with lithium. We show that Ca2+-dependent glutamate release from astrocytes requires an electrochemical gradient necessary for glutamate uptake in vesicles, because bafilomycin A1, a vacuolar-type H+-ATPase inhibitor, reduced glutamate release from astrocytes. Injection of astrocytes with the light chain of the neurotoxin Botulinum B that selectively cleaves the vesicle-associated SNARE protein synaptobrevin inhibited the astrocyte-induced glutamate response in neurons. Therefore, the Ca2+-dependent glutamate release from astrocytes is a SNARE protein-dependent process that requires the presence of functional vesicle-associated proteins, suggesting that astrocytes store glutamate in vesicles and that it is released through an exocytotic pathway.

Key words: astrocyte-neuron signaling; astrocyte calcium waves; transmitter release; Botulinum neurotoxin; bafilomycin; exocytosis; SNARE protein; V-ATPase

Copyright © 2000 Society for Neuroscience  0270-6474/00/202666-08$05.00/0


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