Neurosteroid dehydroepiandrosterone enhances activity and trafficking of astrocytic GLT-1 via σ1 receptor-mediated PKC activation in the hippocampal dentate gyrus of rats

Glia. 2017 Sep;65(9):1491-1503. doi: 10.1002/glia.23175. Epub 2017 Jun 5.

Abstract

Neurosteroid dehydroepiandrosterone (DHEA) has been reported to exert a potent neuroprotective effect against glutamate-induced excitotoxicity. However, the underlying mechanism remains to be elucidated. One of the possible mechanisms may be an involvement of astrocytic glutamate transporter subtype-1 (GLT-1) that can quickly clear spilled glutamate at the synapse to prevent excitotoxicity. To examine the effect of DHEA on GLT-1 activity, we measured synaptically induced glial depolarization (SIGD) in the dentate gyrus (DG) of adult rats by applying an optical recording technique to the hippocampal slices stained with voltage-sensitive dye RH155. Bath-application of DHEA for 10 min dose-dependently increased SIGD without changing presynaptic glutamate releases, which was sensitive to the GLT-1 blocker DHK. Patch-clamp recordings in astrocytes showed that an application of 50 μM DHEA increased glutamate-evoked inward currents (Iglu) by approximately 1.5-fold, which was dependent on the GLT-1 activity. In addition, the level of biotinylated GLT-1 protein in the surface of astrocytes was significantly elevated by DHEA. The DHEA-increased SIGD, Iglu, and GLT-1 translocation to the cell surface were blocked by the σ1 R antagonist NE100 and mimicked by the σ1 R agonist PRE084. DHEA elevated the phosphorylation level of PKC in a σ1 R-dependent manner. Furthermore, the PKC inhibitor chelerythrine could prevent the DHEA-increased SIGD, Iglu, and GLT-1 translocation. Collectively, present results suggest that DHEA enhances the activity and translocation to cell surface of astrocytic GLT-1 mainly via σ1 R-mediated PKC cascade.

Keywords: dehydroepiandrosterone; glutamate transporter 1; protein kinase C; sigma-1 receptor; synaptically induced glial depolarization.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Animals
  • Astrocytes / drug effects
  • Astrocytes / metabolism*
  • Central Nervous System Agents / administration & dosage
  • Cyclic AMP-Dependent Protein Kinases / antagonists & inhibitors
  • Cyclic AMP-Dependent Protein Kinases / metabolism
  • Dehydroepiandrosterone / administration & dosage
  • Dehydroepiandrosterone / metabolism*
  • Dentate Gyrus / drug effects
  • Dentate Gyrus / metabolism*
  • Excitatory Amino Acid Transporter 2 / metabolism*
  • Glutamic Acid / drug effects
  • Glutamic Acid / metabolism
  • Inositol 1,4,5-Trisphosphate Receptors / metabolism
  • Male
  • Membrane Potentials / drug effects
  • Membrane Potentials / physiology
  • Phosphorylation / drug effects
  • Phosphorylation / physiology
  • Protein Kinase C / antagonists & inhibitors
  • Protein Kinase C / metabolism*
  • Protein Transport / drug effects
  • Protein Transport / physiology
  • Proto-Oncogene Proteins c-akt / metabolism
  • Rats, Wistar
  • Receptors, sigma / agonists
  • Receptors, sigma / antagonists & inhibitors
  • Receptors, sigma / metabolism*
  • Tissue Culture Techniques

Substances

  • Central Nervous System Agents
  • Excitatory Amino Acid Transporter 2
  • Inositol 1,4,5-Trisphosphate Receptors
  • Receptors, sigma
  • Slc1a2 protein, rat
  • Glutamic Acid
  • Dehydroepiandrosterone
  • Proto-Oncogene Proteins c-akt
  • Cyclic AMP-Dependent Protein Kinases
  • Protein Kinase C