Skip to main content
PMC home page
The Journal of Physiology logoLink to The Journal of Physiology
. 1988 May;399:227–245. doi: 10.1113/jphysiol.1988.sp017077

Quisqualate- and kainate-activated channels in mouse central neurones in culture.

P Ascher 1, L Nowak 1
PMCID: PMC1191661  PMID: 2457088

Abstract

1. Quisqualate- and kainate-induced currents were recorded in mouse central neurones in culture, using both 'whole-cell' and 'outside-out' configurations. Experiments were made at room temperature. 2. Both quisqualate- and kainate-induced currents invert at 0 mV when the extracellular and intracellular solutions contain similar concentrations of monovalent cations. The changes of reversal potential produced by changes in the monovalent cation concentrations are consistent with the hypothesis that both agonists activate channels selectively permeable to cations. 3. The spectral analysis of the quisqualate- and kainate-induced currents recorded in the whole-cell mode indicates that the main component of the quisqualate noise has a time constant of 10-15 ms while the main component of the kainate noise has a time constant of 2-3 ms. 4. In outside-out patches most of the quisqualate-induced current was carried by channels with a conductance of about 8 pS. A small fraction of the quisqualate-induced current appears to be carried by two other channels: the 'NMDA channel' (40-50 pS) (Ascher, Bregestovski & Nowak, 1988) and a 'fast' channel, with a conductance of 15-35 pS, which was not activated by low concentrations of L-glutamate or by NMDA (N-methyl-D-aspartate). 5. Most of the kainate-induced current can be attributed to a channel characterized by a conductance of about 4 pS. Here again, outside-out patches revealed the presence of an additional channel, with a conductance of about 20 pS. 6. The results are consistent with the notion that there are at least three distinct receptors for excitatory amino acids, each preferentially activated by either NMDA, quisqualate or kainate, each opening channels with multiple conductance states. Other possibilities are discussed.

Full text

PDF
227

Selected References

These references are in PubMed. This may not be the complete list of references from this article.

  1. Ascher P., Bregestovski P., Nowak L. N-methyl-D-aspartate-activated channels of mouse central neurones in magnesium-free solutions. J Physiol. 1988 May;399:207–226. doi: 10.1113/jphysiol.1988.sp017076. [DOI] [PMC free article] [PubMed] [Google Scholar]
  2. Ault B., Evans R. H., Francis A. A., Oakes D. J., Watkins J. C. Selective depression of excitatory amino acid induced depolarizations by magnesium ions in isolated spinal cord preparations. J Physiol. 1980 Oct;307:413–428. doi: 10.1113/jphysiol.1980.sp013443. [DOI] [PMC free article] [PubMed] [Google Scholar]
  3. Bormann J., Hamill O. P., Sakmann B. Mechanism of anion permeation through channels gated by glycine and gamma-aminobutyric acid in mouse cultured spinal neurones. J Physiol. 1987 Apr;385:243–286. doi: 10.1113/jphysiol.1987.sp016493. [DOI] [PMC free article] [PubMed] [Google Scholar]
  4. Crepel F., Dhanjal S. S., Sears T. A. Effect of glutamate, aspartate and related derivatives on cerebellar purkinje cell dendrites in the rat: an in vitro study. J Physiol. 1982 Aug;329:297–317. doi: 10.1113/jphysiol.1982.sp014304. [DOI] [PMC free article] [PubMed] [Google Scholar]
  5. Cull-Candy S. G., Ogden D. C. Ion channels activated by L-glutamate and GABA in cultured cerebellar neurons of the rat. Proc R Soc Lond B Biol Sci. 1985 May 22;224(1236):367–373. doi: 10.1098/rspb.1985.0038. [DOI] [PubMed] [Google Scholar]
  6. Cull-Candy S. G., Usowicz M. M. Multiple-conductance channels activated by excitatory amino acids in cerebellar neurons. Nature. 1987 Feb 5;325(6104):525–528. doi: 10.1038/325525a0. [DOI] [PubMed] [Google Scholar]
  7. Davies J., Watkins J. C. Depressant actions of gamma-D-glutamylaminomethyl sulfonate (GAMS) on amino acid-induced and synaptic excitation in the cat spinal cord. Brain Res. 1985 Feb 18;327(1-2):113–120. doi: 10.1016/0006-8993(85)91505-7. [DOI] [PubMed] [Google Scholar]
  8. Fagni L., Baudry M., Lynch G. Classification and properties of acidic amino acid receptors in hippocampus. I. Electrophysiological studies of an apparent desensitization and interactions with drugs which block transmission. J Neurosci. 1983 Aug;3(8):1538–1546. doi: 10.1523/JNEUROSCI.03-08-01538.1983. [DOI] [PMC free article] [PubMed] [Google Scholar]
  9. Fenwick E. M., Marty A., Neher E. A patch-clamp study of bovine chromaffin cells and of their sensitivity to acetylcholine. J Physiol. 1982 Oct;331:577–597. doi: 10.1113/jphysiol.1982.sp014393. [DOI] [PMC free article] [PubMed] [Google Scholar]
  10. Greenamyre J. T., Olson J. M., Penney J. B., Jr, Young A. B. Autoradiographic characterization of N-methyl-D-aspartate-, quisqualate- and kainate-sensitive glutamate binding sites. J Pharmacol Exp Ther. 1985 Apr;233(1):254–263. [PubMed] [Google Scholar]
  11. Grenningloh G., Rienitz A., Schmitt B., Methfessel C., Zensen M., Beyreuther K., Gundelfinger E. D., Betz H. The strychnine-binding subunit of the glycine receptor shows homology with nicotinic acetylcholine receptors. Nature. 1987 Jul 16;328(6127):215–220. doi: 10.1038/328215a0. [DOI] [PubMed] [Google Scholar]
  12. Gundersen C. B., Miledi R., Parker I. Messenger RNA from human brain induces drug- and voltage-operated channels in Xenopus oocytes. 1984 Mar 29-Apr 4Nature. 308(5958):421–424. doi: 10.1038/308421a0. [DOI] [PubMed] [Google Scholar]
  13. Hamill O. P., Bormann J., Sakmann B. Activation of multiple-conductance state chloride channels in spinal neurones by glycine and GABA. 1983 Oct 27-Nov 2Nature. 305(5937):805–808. doi: 10.1038/305805a0. [DOI] [PubMed] [Google Scholar]
  14. Hamill O. P., Marty A., Neher E., Sakmann B., Sigworth F. J. Improved patch-clamp techniques for high-resolution current recording from cells and cell-free membrane patches. Pflugers Arch. 1981 Aug;391(2):85–100. doi: 10.1007/BF00656997. [DOI] [PubMed] [Google Scholar]
  15. Hamill O. P., Sakmann B. Multiple conductance states of single acetylcholine receptor channels in embryonic muscle cells. Nature. 1981 Dec 3;294(5840):462–464. doi: 10.1038/294462a0. [DOI] [PubMed] [Google Scholar]
  16. Honoré T., Drejer J., Nielsen M. Calcium discriminates two [3H]kainate binding sites with different molecular target sizes in rat cortex. Neurosci Lett. 1986 Mar 28;65(1):47–52. doi: 10.1016/0304-3940(86)90118-7. [DOI] [PubMed] [Google Scholar]
  17. Jahr C. E., Stevens C. F. Glutamate activates multiple single channel conductances in hippocampal neurons. Nature. 1987 Feb 5;325(6104):522–525. doi: 10.1038/325522a0. [DOI] [PubMed] [Google Scholar]
  18. Johnson J. W., Ascher P. Glycine potentiates the NMDA response in cultured mouse brain neurons. Nature. 1987 Feb 5;325(6104):529–531. doi: 10.1038/325529a0. [DOI] [PubMed] [Google Scholar]
  19. Kiskin N. I., Krishtal O. A., Tsyndrenko AYa Excitatory amino acid receptors in hippocampal neurons: kainate fails to desensitize them. Neurosci Lett. 1986 Jan 30;63(3):225–230. doi: 10.1016/0304-3940(86)90360-5. [DOI] [PubMed] [Google Scholar]
  20. Krishtal O. A., Pidoplichko V. I. A receptor for protons in the nerve cell membrane. Neuroscience. 1980;5(12):2325–2327. doi: 10.1016/0306-4522(80)90149-9. [DOI] [PubMed] [Google Scholar]
  21. Luini A., Goldberg O., Teichberg V. I. Distinct pharmacological properties of excitatory amino acid receptors in the rat striatum: study by Na+ efflux assay. Proc Natl Acad Sci U S A. 1981 May;78(5):3250–3254. doi: 10.1073/pnas.78.5.3250. [DOI] [PMC free article] [PubMed] [Google Scholar]
  22. Mayer M. L., Westbrook G. L. The physiology of excitatory amino acids in the vertebrate central nervous system. Prog Neurobiol. 1987;28(3):197–276. doi: 10.1016/0301-0082(87)90011-6. [DOI] [PubMed] [Google Scholar]
  23. Nowak L., Bregestovski P., Ascher P., Herbet A., Prochiantz A. Magnesium gates glutamate-activated channels in mouse central neurones. Nature. 1984 Feb 2;307(5950):462–465. doi: 10.1038/307462a0. [DOI] [PubMed] [Google Scholar]
  24. Olverman H. J., Jones A. W., Watkins J. C. L-glutamate has higher affinity than other amino acids for [3H]-D-AP5 binding sites in rat brain membranes. Nature. 1984 Feb 2;307(5950):460–462. doi: 10.1038/307460a0. [DOI] [PubMed] [Google Scholar]
  25. Sawada S., Yamamoto C. Fast and slow depolarizing potentials induced by short pulses of kainic acid in hippocampal neurons. Brain Res. 1984 Dec 24;324(2):279–287. doi: 10.1016/0006-8993(84)90038-6. [DOI] [PubMed] [Google Scholar]
  26. Schofield P. R., Darlison M. G., Fujita N., Burt D. R., Stephenson F. A., Rodriguez H., Rhee L. M., Ramachandran J., Reale V., Glencorse T. A. Sequence and functional expression of the GABA A receptor shows a ligand-gated receptor super-family. Nature. 1987 Jul 16;328(6127):221–227. doi: 10.1038/328221a0. [DOI] [PubMed] [Google Scholar]
  27. Surtees L., Collins G. G. Receptor types mediating the excitatory actions of exogenous L-aspartate and L-glutamate in rat olfactory cortex. Brain Res. 1985 May 20;334(2):287–295. doi: 10.1016/0006-8993(85)90220-3. [DOI] [PubMed] [Google Scholar]
  28. Watkins J. C., Evans R. H. Excitatory amino acid transmitters. Annu Rev Pharmacol Toxicol. 1981;21:165–204. doi: 10.1146/annurev.pa.21.040181.001121. [DOI] [PubMed] [Google Scholar]

Articles from The Journal of Physiology are provided here courtesy of The Physiological Society

RESOURCES