Astrocytic glutamate transport regulates a Drosophila CNS synapse that lacks astrocyte ensheathment

Sarah E. Macnamee, Kendra E. Liu, Stephan Gerhard, Cathy T. Tran, Richard D. Fetter, Albert Cardona, Leslie P Tolbert, Lynne A Oland

Research output: Contribution to journalArticle

12 Citations (Scopus)

Abstract

Anatomical, molecular, and physiological interactions between astrocytes and neuronal synapses regulate information processing in the brain. The fruit fly Drosophila melanogaster has become a valuable experimental system for genetic manipulation of the nervous system and has enormous potential for elucidating mechanisms that mediate neuron-glia interactions. Here, we show the first electrophysiological recordings from Drosophila astrocytes and characterize their spatial and physiological relationship with particular synapses. Astrocyte intrinsic properties were found to be strongly analogous to those of vertebrate astrocytes, including a passive current-voltage relationship, low membrane resistance, high capacitance, and dye-coupling to local astrocytes. Responses to optogenetic stimulation of glutamatergic premotor neurons were correlated directly with anatomy using serial electron microscopy reconstructions of homologous identified neurons and surrounding astrocytic processes. Robust bidirectional communication was present: neuronal activation triggered astrocytic glutamate transport via excitatory amino acid transporter 1 (Eaat1), and blocking Eaat1 extended glutamatergic interneuron-evoked inhibitory postsynaptic currents in motor neurons. The neuronal synapses were always located within 1 μm of an astrocytic process, but none were ensheathed by those processes. Thus, fly astrocytes can modulate fast synaptic transmission via neurotransmitter transport within these anatomical parameters. J. Comp. Neurol. 524:1979-1998, 2016.

Original languageEnglish (US)
Pages (from-to)1979-1998
Number of pages20
JournalJournal of Comparative Neurology
Volume524
Issue number10
DOIs
StatePublished - Jul 1 2016

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Astrocytes
Synapses
Drosophila
Glutamic Acid
Excitatory Amino Acid Transporter 1
Neurons
Diptera
Optogenetics
Inhibitory Postsynaptic Potentials
Motor Neurons
Interneurons
Drosophila melanogaster
Automatic Data Processing
Synaptic Transmission
Neuroglia
Nervous System
Neurotransmitter Agents
Vertebrates
Fruit
Anatomy

Keywords

  • Coupling
  • Electron microscopy
  • Electrophysiology
  • Optogenetics
  • RRID: AB_221477
  • RRID: AB_2313643
  • RRID: AB_2490070
  • RRID: AB_528122
  • RRID: AB_528235
  • RRID: SCR_007353

ASJC Scopus subject areas

  • Neuroscience(all)

Cite this

Astrocytic glutamate transport regulates a Drosophila CNS synapse that lacks astrocyte ensheathment. / Macnamee, Sarah E.; Liu, Kendra E.; Gerhard, Stephan; Tran, Cathy T.; Fetter, Richard D.; Cardona, Albert; Tolbert, Leslie P; Oland, Lynne A.

In: Journal of Comparative Neurology, Vol. 524, No. 10, 01.07.2016, p. 1979-1998.

Research output: Contribution to journalArticle

Macnamee, Sarah E. ; Liu, Kendra E. ; Gerhard, Stephan ; Tran, Cathy T. ; Fetter, Richard D. ; Cardona, Albert ; Tolbert, Leslie P ; Oland, Lynne A. / Astrocytic glutamate transport regulates a Drosophila CNS synapse that lacks astrocyte ensheathment. In: Journal of Comparative Neurology. 2016 ; Vol. 524, No. 10. pp. 1979-1998.
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