GPR35 activation reduces Ca2+ transients and contributes to the kynurenic acid-dependent reduction of synaptic activity at CA3-CA1 synapses

PLoS One. 2013 Nov 29;8(11):e82180. doi: 10.1371/journal.pone.0082180. eCollection 2013.

Abstract

Limited information is available on the brain expression and role of GPR35, a Gi/o coupled receptor activated by kynurenic acid (KYNA). In mouse cultured astrocytes, we detected GPR35 transcript using RT-PCR and we found that KYNA (0.1 to 100 µM) decreased forskolin (FRSK)-induced cAMP production (p<0.05). Both CID2745687 (3 µM, CID), a recently described GPR35 antagonist, and GPR35 gene silencing significantly prevented the action of KYNA on FRSK-induced cAMP production. In these cultures, we then evaluated whether GPR35 activation was able to modulate intracellular Ca(2+) concentration ([Ca(2+)]i ) and [Ca(2+)]i fluxes. We found that both KYNA and zaprinast, a phosphodiesterase (PDE) inhibitor and GPR35 agonist, did not modify either basal or peaks of [Ca(2+)]i induced by challenging the cells with ATP (30 µM). However, the [Ca(2+)]i plateau phase following peak was significantly attenuated by these compounds in a store-operated Ca(2+) channel (SOC)-independent manner. The activation of GPR35 by KYNA and zaprinast was also studied at the CA3-CA1 synapse in the rat hippocampus. Evoked excitatory post synaptic currents (eEPSCs) were recorded from CA1 pyramidal neurons in acute brain slices. The action of KYNA on GPR35 was pharmacologically isolated by using NMDA and α7 nicotinic receptor blockers and resulted in a significant reduction of eEPSC amplitude. This effect was prevented in the presence of CID. Moreover, zaprinast reduced eEPSC amplitude in a PDE5- and cGMP-independent mechanism, thus suggesting that glutamatergic transmission in this area is modulated by GPR35. In conclusion, GPR35 is expressed in cultured astrocytes and its activation modulates cAMP production and [Ca(2+)]i. GPR35 activation may contribute to KYNA effects on the previously reported decrease of brain extracellular glutamate levels and reduction of excitatory transmission.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Animals
  • Astrocytes / cytology
  • Astrocytes / metabolism
  • Base Sequence
  • Calcium / metabolism*
  • Cells, Cultured
  • DNA Primers
  • Hippocampus / metabolism*
  • Kynurenic Acid / metabolism*
  • Mice
  • Real-Time Polymerase Chain Reaction
  • Receptors, G-Protein-Coupled / metabolism*
  • Synapses / metabolism*
  • Synapses / physiology
  • Synaptic Transmission

Substances

  • DNA Primers
  • GPR35 protein, mouse
  • Receptors, G-Protein-Coupled
  • Kynurenic Acid
  • Calcium

Grants and funding

The work was supported by Grant by Ente Cassa di Risparmio di Firenze and by PRIN Programmi di Ricerca Scientifica di Rilevante Interesse Nazionale (Guido Mannaioni). The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript.