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The Journal of Neuroscience, September 10, 2008, 28(37):9122-9132; doi:10.1523/JNEUROSCI.0040-08.2008

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Cellular/Molecular
Fast Subplasma Membrane Ca²⁺ Transients Control Exo-Endocytosis of Synaptic-Like Microvesicles in Astrocytes

Julie Marchaland,^1 * Corrado Calì,^1 * Susan M. Voglmaier,³ Haiyan Li,² Romano Regazzi,¹ Robert H. Edwards,² and Paola Bezzi¹

¹Department of Cell Biology and Morphology, Faculty of Biology and Medicine, University of Lausanne, 1005 Lausanne, Switzerland, and Departments of ²Neurology and Physiology and ³Psychiatry, University of California, San Francisco, San Francisco, California 94143

Correspondence should be addressed to Dr. Paola Bezzi, Department of Cell Biology and Morphology, Faculty of Biology and Medicine, University of Lausanne, Rue du Bugnon 9, 1005 Lausanne, Switzerland. Email: Paola.Bezzi{at}unil.ch

Astrocytes are the most abundant glial cell type in the brain. Although not apposite for long-range rapid electrical communication, astrocytes share with neurons the capacity of chemical signaling via Ca²⁺-dependent transmitter exocytosis. Despite this recent finding, little is known about the specific properties of regulated secretion and vesicle recycling in astrocytes. Important differences may exist with the neuronal exocytosis, starting from the fact that stimulus-secretion coupling in astrocytes is voltage independent, mediated by G-protein-coupled receptors and the release of Ca²⁺ from internal stores. Elucidating the spatiotemporal properties of astrocytic exo-endocytosis is, therefore, of primary importance for understanding the mode of communication of these cells and their role in brain signaling. We here take advantage of fluorescent tools recently developed for studying recycling of glutamatergic vesicles at synapses (Voglmaier et al., 2006; Balaji and Ryan, 2007); we combine epifluorescence and total internal reflection fluorescence imaging to investigate with unprecedented temporal and spatial resolution, the stimulus-secretion coupling underlying exo-endocytosis of glutamatergic synaptic-like microvesicles (SLMVs) in astrocytes. Our main findings indicate that (1) exo-endocytosis in astrocytes proceeds with a time course on the millisecond time scale (_exocytosis = 0.24 ± 0.017 s; _endocytosis = 0.26 ± 0.03 s) and (2) exocytosis is controlled by local Ca²⁺ microdomains. We identified submicrometer cytosolic compartments delimited by endoplasmic reticulum tubuli reaching beneath the plasma membrane and containing SLMVs at which fast (time-to-peak, 50 ms) Ca²⁺ events occurred in precise spatial-temporal correlation with exocytic fusion events. Overall, the above characteristics of transmitter exocytosis from astrocytes support a role of this process in fast synaptic modulation.

Key words: exocytosis; endocytosis; calcium; glutamate release; astrocytes; imaging

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Received Jan. 4, 2008; revised July 22, 2008; accepted July 28, 2008.

Correspondence should be addressed to Dr. Paola Bezzi, Department of Cell Biology and Morphology, Faculty of Biology and Medicine, University of Lausanne, Rue du Bugnon 9, 1005 Lausanne, Switzerland. Email: Paola.Bezzi{at}unil.ch

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