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The Journal of Neuroscience, March 17, 2004, 24(11):2633-2642; doi:10.1523/JNEUROSCI.3770-03.2004

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Cellular/Molecular
Vesicular Glutamate Transporter-Dependent Glutamate Release from Astrocytes

Vedrana Montana,¹ Yingchun Ni,¹ Vice Sunjara,² Xue Hua,¹ and Vladimir Parpura¹

¹Department of Cell Biology and Neuroscience and Center for Nanoscale Science and Engineering, ²International Scholars Program, University of California, Riverside, California 92521

Astrocytes exhibit excitability based on variations of their intracellular Ca²⁺ concentrations, which leads to glutamate release, that in turn can signal to adjacent neurons. This glutamate-mediated astrocyte–neuron signaling occurs at physiological intracellular Ca²⁺ levels in astrocytes and includes modulation of synaptic transmission. The mechanism underlying Ca²⁺-dependent glutamate release from astrocytes is most likely exocytosis, because astrocytes express the protein components of the soluble N-ethyl maleimide-sensitive fusion protein attachment protein receptors complex, including synaptobrevin 2, syntaxin, and synaptosome-associated protein of 23 kDa. Although these proteins mediate Ca²⁺-dependent glutamate release from astrocytes, it is not well understood whether astrocytes express functional vesicular glutamate transporters (VGLUTs) that are critical for vesicle refilling. Here, we find in cultured and freshly isolated astrocytes the presence of brain-specific Na⁺-dependent inorganic phosphate cotransporter and differentiation-associated Na⁺-dependent inorganic phosphate cotransporter that have recently been identified as VGLUTs 1 and 2. Indirect immunocytochemistry showed a punctate pattern of VGLUT immunoreactivity throughout the entire cell body and processes, whereas pharmacological inhibition of VGLUTs abolished mechanically and agonist-evoked Ca²⁺-dependent glutamate release from astrocytes. Taken together, these data indicate that VGLUTs play a functional role in exocytotic glutamate release from astrocytes.

Key words: astrocytes; vesicular glutamate transporters; SNAREs; V-ATPase; calcium-dependent glutamate release; exocytosis; signaling; synapse

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Received Aug 12, 2003; revised January 30, 2004; accepted January 30, 2004.

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