Metabotropic glutamate receptor in C6BU-1 glioma cell has NMDA receptor-ion channel complex-like properties and interacts with serotonin2 receptor-stimulated signal transduction

J Neurochem. 1994 Oct;63(4):1346-53. doi: 10.1046/j.1471-4159.1994.63041346.x.

Abstract

We found in cultured glioma (C6BU-1) cells that excitatory amino acids (EAAs) such as glutamate, N-methyl-D-aspartate (NMDA), aspartate, and metabotropic glutamate receptor agonist trans-(+/-)-1-amino-1,3-cyclopentanedicarboxylate caused an increase in the inositol 1,4,5-trisphosphate formation and the intracellular Ca2+ concentration ([Ca2+]i) in the absence of extracellular Mg2+ and Ca2+. Pertussis toxin treatment abolished this glutamate-induced [Ca2+]i increase. Various antagonists against NMDA receptor-ion channel complex, such as Mg2+, D-2-amino-5-phosphonovalerate (D-APV), HA-966, and MK-801, also inhibited the increase in [Ca2+]i induced by glutamate. These results indicate that these metabotropic EAA receptors coupled to pertussis toxin-susceptible GTP-binding protein and phospholipase C system in C6BU-1 glioma cells have the pharmacological properties of NMDA receptor-ion channel complexes. We also found that in the presence of Mg2+ these metabotropic receptors resemble the NMDA receptor-ion channel complex interacted with 5-hydroxytryptamine2 (5-HT2) receptor signaling. EAAs inhibited 5-HT2 receptor-mediated intracellular Ca2+ mobilization and inositol 1,4,5-trisphosphate formation in a concentration-dependent manner. The inhibitory effect of glutamate was reversed by various NMDA receptor antagonists (D-APV, MK-801, phencyclidine, and HA-966), but L-APV failed to block the inhibitory effect of glutamate. The same result was observed in the absence of extracellular Ca2+. In addition, this inhibitory effect on 5-HT2 receptor-mediated signal transduction was abolished by treatment of C6BU-1 cells with pertussis toxin, whereas 5-HT2 receptor-mediated [Ca2+]i increase was not abolished by pertussis toxin treatment. We can, therefore, conclude that the inhibitory effect of glutamate is not a result of the influx of Ca2+ through the ion channel and that it operates via metabotropic glutamate receptors, having NMDA receptor-ion channel complex-like properties and being coupled with pertussis toxin-sensitive GTP-binding protein and phospholipase C.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • 2-Amino-5-phosphonovalerate / pharmacology
  • Animals
  • Aspartic Acid / pharmacology
  • Calcium / metabolism*
  • Calcium / pharmacology
  • Cell Line
  • Cycloleucine / analogs & derivatives
  • Cycloleucine / pharmacology
  • Dizocilpine Maleate / pharmacology
  • Glioma
  • Glutamic Acid / pharmacology
  • Inositol 1,4,5-Trisphosphate / metabolism*
  • Ion Channels / metabolism*
  • Kainic Acid / pharmacology
  • Kinetics
  • Magnesium Chloride / pharmacology
  • N-Methylaspartate / pharmacology
  • Neurotoxins / pharmacology
  • Pyrrolidinones / pharmacology
  • Rats
  • Receptors, Metabotropic Glutamate / metabolism*
  • Receptors, N-Methyl-D-Aspartate / metabolism*
  • Receptors, Serotonin / physiology*
  • Signal Transduction*
  • Tumor Cells, Cultured

Substances

  • Ion Channels
  • Neurotoxins
  • Pyrrolidinones
  • Receptors, Metabotropic Glutamate
  • Receptors, N-Methyl-D-Aspartate
  • Receptors, Serotonin
  • Magnesium Chloride
  • Cycloleucine
  • 1-amino-1,3-dicarboxycyclopentane
  • Aspartic Acid
  • Glutamic Acid
  • N-Methylaspartate
  • Dizocilpine Maleate
  • 2-Amino-5-phosphonovalerate
  • Inositol 1,4,5-Trisphosphate
  • 1-hydroxy-3-amino-2-pyrrolidone
  • Kainic Acid
  • Calcium