Calcium-permeable AMPA receptors trigger vesicular glutamate release from Bergmann gliosomes

Chiara Cervetto, Daniela Frattaroli, Arianna Venturini, Mario Passalacqua, Mario Nobile, Susanna Alloisio, Carlo Tacchetti, Guido Maura, Luigi Francesco Agnati, Manuela Marcoli

Research output: Contribution to journalArticle

Abstract

The Bergmann glia is equipped with Ca2+-permeable AMPA receptors for glutamate, indispensable for structural and functional relations between the Bergmann glia and parallel/climbing fibers-Purkinje cell synapses. To better understand roles for the Bergmann AMPA receptors, herein we investigate on gliotransmitter release and Ca2+ signals in isolated Bergmann glia processes obtained from adult rat cerebellum. We found that: 1) the rat cerebellar purified astrocyte processes (gliosomes) expressed astrocytic and Bergmann markers and exhibited negligible contamination by nerve terminals, microglia, or oligodendrocytes; 2) activation of Ca2+-permeable AMPA receptors caused Ca2+ signals in the processes, and the release of glutamate from the processes; 3) effectiveness of rose bengal, trypan blue or bafilomycin A1, indicated that activation of the AMPA receptors evoked vesicular glutamate release. Cerebellar purified nerve terminals appeared devoid of glutamate-releasing Ca2+-permeable AMPA receptors, indicating that neuronal contamination may not be the source of the signals detected. Ultrastructural analysis indicated the presence of vesicles in the cytoplasm of the processes; confocal imaging confirmed the presence of vesicular glutamate transporters in Bergmann glia processes. We conclude that: a vesicular mechanism for release of the gliotransmitter glutamate is present in mature Bergmann processes; entry of Ca2+ through the AMPA receptors located on Bergmann processes is coupled with vesicular glutamate release. The findings would add a new role for a well-known Bergmann target for glutamate (the Ca2+-permeable AMPA receptors) and a new actor (the gliotransmitter glutamate) at the cerebellar excitatory synapses onto Purkinje cells.

Original languageEnglish
Article number5957
Pages (from-to)396-407
Number of pages12
JournalNeuropharmacology
Volume99
DOIs
Publication statusPublished - Dec 1 2015

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Keywords

  • Cerebellum
  • Gliosomes
  • Gliotransmitter release
  • GluA2-lacking AMPA receptor
  • Neuroglia

ASJC Scopus subject areas

  • Cellular and Molecular Neuroscience
  • Pharmacology

Cite this

Cervetto, C., Frattaroli, D., Venturini, A., Passalacqua, M., Nobile, M., Alloisio, S., Tacchetti, C., Maura, G., Agnati, L. F., & Marcoli, M. (2015). Calcium-permeable AMPA receptors trigger vesicular glutamate release from Bergmann gliosomes. Neuropharmacology, 99, 396-407. [5957]. https://doi.org/10.1016/j.neuropharm.2015.08.011