Selective gamma-hydroxybutyric acid receptor ligands increase extracellular glutamate in the hippocampus, but fail to activate G protein and to produce the sedative/hypnotic effect of gamma-hydroxybutyric acid

J Neurochem. 2003 Nov;87(3):722-32. doi: 10.1046/j.1471-4159.2003.02037.x.

Abstract

Two gamma-hydroxybutyric acid (GHB) analogues, trans-gamma-hydroxycrotonic acid (t-HCA) and gamma-(p-methoxybenzyl)-gamma-hydroxybutyric acid (NCS-435) displaced [3H]GHB from GHB receptors with the same affinity as GHB but, unlike GHB, failed to displace [3H]baclofen from GABAB receptors. The effect of the GHB analogues, GHB and baclofen, on G protein activity and hippocampal extracellular glutamate levels was compared. While GHB and baclofen stimulated 5'-O-(3-[35S]thiotriphospate) [35S]GTPgammaS binding both in cortex homogenate and cortical slices, t-HCA and NCS-435 were ineffective up to 1 mm concentration. GHB and baclofen effect was suppressed by the GABAB antagonist CGP 35348 but not by the GHB receptor antagonist NCS-382. Perfused into rat hippocampus, 500 nm and 1 mm GHB increased and decreased extracellular glutamate levels, respectively. GHB stimulation was suppressed by NCS-382, while GHB inhibition by CGP 35348. t-HCA and NCS-435 (0.1-1000 microm) locally perfused into hippocampus increased extracellular glutamate; this effect was inhibited by NCS-382 (10 microm) but not by CGP 35348 (500 microm). The results indicate that GHB-induced G protein activation and reduction of glutamate levels are GABAB-mediated effects, while the increase of glutamate levels is a GHB-mediated effect. Neither t-HCA nor NCS-435 reproduced GHB sedative/hypnotic effect in mice, confirming that this effect is GABAB-mediated. The GHB analogues constitute important tools for understanding the physiological role of endogenous GHB and its receptor.

MeSH terms

  • Animals
  • Autoradiography
  • Benzocycloheptenes / pharmacology
  • Binding, Competitive / drug effects
  • Brain Chemistry
  • Extracellular Space / metabolism
  • GABA Antagonists / pharmacology
  • GTP-Binding Proteins / drug effects
  • GTP-Binding Proteins / metabolism*
  • Glutamic Acid / metabolism*
  • Guanosine 5'-O-(3-Thiotriphosphate) / pharmacokinetics
  • Hippocampus / drug effects
  • Hippocampus / metabolism*
  • Hydroxybutyrates / pharmacology*
  • Hypnotics and Sedatives / pharmacology
  • Ligands
  • Male
  • Mice
  • Mice, Inbred DBA
  • Microdialysis
  • Organophosphorus Compounds / pharmacology
  • Rats
  • Rats, Sprague-Dawley
  • Receptors, Cell Surface / drug effects
  • Receptors, Cell Surface / metabolism*
  • Reflex / drug effects

Substances

  • 4-hydroxybutyric acid receptor
  • Benzocycloheptenes
  • GABA Antagonists
  • Hydroxybutyrates
  • Hypnotics and Sedatives
  • Ligands
  • Organophosphorus Compounds
  • Receptors, Cell Surface
  • gamma-(4-methoxybenzyl)-gamma-hydroxybutyric acid
  • NCS 382
  • 4-hydroxybutyric acid
  • Guanosine 5'-O-(3-Thiotriphosphate)
  • Glutamic Acid
  • 4-hydroxy-2-butenoic acid
  • CGP 35348
  • GTP-Binding Proteins