Skip to main content
PMC home page
The Journal of Physiology logoLink to The Journal of Physiology
. 1996 Oct 1;496(Pt 1):165–173. doi: 10.1113/jphysiol.1996.sp021674

Dimensions and ion selectivity of recombinant AMPA and kainate receptor channels and their dependence on Q/R site residues.

N Burnashev 1, A Villarroel 1, B Sakmann 1
PMCID: PMC1160833  PMID: 8910205

Abstract

1. Recombinant alpha-amino-3-hydroxy-5-methyl-4-isoxazolepropionate receptor (AMPAR) subunits (GluR-A or GluR-B) and kainate receptor (KAR) subunit (GluR-6) in their unedited (Q)- and edited (R)-forms were expressed in HEK 293 cells. To estimate the dimensions of the narrow portion of these channels, biionic reversal potentials for organic cations of different mean diameters were determined with Cs+ as the internal reference ion. 2. Homomeric channels assembled from Q-form subunits were cation selective. The relation between the relative permeability and the mean size of different organic cations suggests that the diameter of the narrow portion of Q-form channels is approximately 0.78 nm for AMPAR and 0.75 nm for KAR channels. 3. Homomeric channels assembled from R-form subunits were permeant for anions and cations. When probed with CsC1 gradients the relative chloride permeability (PC1/PCs) was estimated as 0.14 for GluR-B(R) and 0.74 for GluR-6(R)-subunit channels. The permeability versus mean size relation for large cations measured with the weakly permeant F- as anion, indicates that for the R-form KAR channels the apparent pore diameter is close to 0.76 nm. 4. Heteromeric AMPAR and KAR channels co-assembled from Q- and R-form subunits were cation selective. The diameter of the narrow portion of these channels is estimated to be in the range between 0.70 and 0.74 nm. 5. The results indicated that the diameters of the narrow portion of AMPAR and KAR channels of different subunit composition and of widely different ion selectivity are comparable. Therefore, the differences in the anion versus cation selectivity, in Ca2+ permeability and in channel conductance are likely to be determined by the difference in charge density of the channel.

Full text

PDF
165

Selected References

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

  1. Brusa R., Zimmermann F., Koh D. S., Feldmeyer D., Gass P., Seeburg P. H., Sprengel R. Early-onset epilepsy and postnatal lethality associated with an editing-deficient GluR-B allele in mice. Science. 1995 Dec 8;270(5242):1677–1680. doi: 10.1126/science.270.5242.1677. [DOI] [PubMed] [Google Scholar]
  2. Burnashev N., Zhou Z., Neher E., Sakmann B. Fractional calcium currents through recombinant GluR channels of the NMDA, AMPA and kainate receptor subtypes. J Physiol. 1995 Jun 1;485(Pt 2):403–418. doi: 10.1113/jphysiol.1995.sp020738. [DOI] [PMC free article] [PubMed] [Google Scholar]
  3. Cully D. F., Vassilatis D. K., Liu K. K., Paress P. S., Van der Ploeg L. H., Schaeffer J. M., Arena J. P. Cloning of an avermectin-sensitive glutamate-gated chloride channel from Caenorhabditis elegans. Nature. 1994 Oct 20;371(6499):707–711. doi: 10.1038/371707a0. [DOI] [PubMed] [Google Scholar]
  4. Dingledine R., Boland L. M., Chamberlin N. L., Kawasaki K., Kleckner N. W., Traynelis S. F., Verdoorn T. A. Amino acid receptors and uptake systems in the mammalian central nervous system. Crit Rev Neurobiol. 1988;4(1):1–96. [PubMed] [Google Scholar]
  5. Dwyer T. M., Adams D. J., Hille B. The permeability of the endplate channel to organic cations in frog muscle. J Gen Physiol. 1980 May;75(5):469–492. doi: 10.1085/jgp.75.5.469. [DOI] [PMC free article] [PubMed] [Google Scholar]
  6. Egebjerg J., Heinemann S. F. Ca2+ permeability of unedited and edited versions of the kainate selective glutamate receptor GluR6. Proc Natl Acad Sci U S A. 1993 Jan 15;90(2):755–759. doi: 10.1073/pnas.90.2.755. [DOI] [PMC free article] [PubMed] [Google Scholar]
  7. Franciolini F., Nonner W. Anion and cation permeability of a chloride channel in rat hippocampal neurons. J Gen Physiol. 1987 Oct;90(4):453–478. doi: 10.1085/jgp.90.4.453. [DOI] [PMC free article] [PubMed] [Google Scholar]
  8. Hollmann M., Heinemann S. Cloned glutamate receptors. Annu Rev Neurosci. 1994;17:31–108. doi: 10.1146/annurev.ne.17.030194.000335. [DOI] [PubMed] [Google Scholar]
  9. Horn R. Statistical methods for model discrimination. Applications to gating kinetics and permeation of the acetylcholine receptor channel. Biophys J. 1987 Feb;51(2):255–263. doi: 10.1016/S0006-3495(87)83331-3. [DOI] [PMC free article] [PubMed] [Google Scholar]
  10. Iino M., Ozawa S., Tsuzuki K. Permeation of calcium through excitatory amino acid receptor channels in cultured rat hippocampal neurones. J Physiol. 1990 May;424:151–165. doi: 10.1113/jphysiol.1990.sp018060. [DOI] [PMC free article] [PubMed] [Google Scholar]
  11. Köhler M., Burnashev N., Sakmann B., Seeburg P. H. Determinants of Ca2+ permeability in both TM1 and TM2 of high affinity kainate receptor channels: diversity by RNA editing. Neuron. 1993 Mar;10(3):491–500. doi: 10.1016/0896-6273(93)90336-p. [DOI] [PubMed] [Google Scholar]
  12. Lewis C. A. Ion-concentration dependence of the reversal potential and the single channel conductance of ion channels at the frog neuromuscular junction. J Physiol. 1979 Jan;286:417–445. doi: 10.1113/jphysiol.1979.sp012629. [DOI] [PMC free article] [PubMed] [Google Scholar]
  13. 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]
  14. Sommer B., Köhler M., Sprengel R., Seeburg P. H. RNA editing in brain controls a determinant of ion flow in glutamate-gated channels. Cell. 1991 Oct 4;67(1):11–19. doi: 10.1016/0092-8674(91)90568-j. [DOI] [PubMed] [Google Scholar]
  15. Swanson G. T., Feldmeyer D., Kaneda M., Cull-Candy S. G. Effect of RNA editing and subunit co-assembly single-channel properties of recombinant kainate receptors. J Physiol. 1996 Apr 1;492(Pt 1):129–142. doi: 10.1113/jphysiol.1996.sp021295. [DOI] [PMC free article] [PubMed] [Google Scholar]
  16. Villarroel A., Burnashev N., Sakmann B. Dimensions of the narrow portion of a recombinant NMDA receptor channel. Biophys J. 1995 Mar;68(3):866–875. doi: 10.1016/S0006-3495(95)80263-8. [DOI] [PMC free article] [PubMed] [Google Scholar]
  17. Vyklicky L., Jr, Krusek J., Edwards C. Differences in the pore sizes of the N-methyl-D-aspartate and kainate cation channels. Neurosci Lett. 1988 Jul 8;89(3):313–318. doi: 10.1016/0304-3940(88)90545-9. [DOI] [PubMed] [Google Scholar]
  18. Wollmuth L. P., Kuner T., Seeburg P. H., Sakmann B. Differential contribution of the NR1- and NR2A-subunits to the selectivity filter of recombinant NMDA receptor channels. J Physiol. 1996 Mar 15;491(Pt 3):779–797. doi: 10.1113/jphysiol.1996.sp021257. [DOI] [PMC free article] [PubMed] [Google Scholar]

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

RESOURCES