Abstract
The non-NMDA family of glutamate receptors comprises a growing number of structurally related subunits (GluR-A to -D or -1 to -4; GluR-5, -6; KA-1). GluR-A to -D appear to constitute the major AMPA receptor subtypes but the functional and pharmacological characteristics of the other subunits are unresolved. Using a mammalian expression system we demonstrate here that homomeric GluR-5 receptors exhibit properties of a high affinity domoate (KD approximately 2 nM) and kainate (KD approximately 70 nM) binding site. For these receptors, the rank order of ligands competing with [3H]kainate binding was domoate much greater than quisqualate approximately glutamate much greater than AMPA approximately CNQX. The respective receptor channels were gated in decreasing order of sensitivity by domoate, kainate, glutamate and AMPA. In contrast to recombinantly expressed GluR-A to -D channels, currents elicited at GluR-5 receptor desensitize channels to all agonists. This property is characteristic of currents in peripheral neurons on sensory ganglia. These findings suggest the existence of at least two distinct types of non-NMDA receptor channels, both gated by AMPA and kainate, but differing in pharmacology and current properties.
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- Agrawal S. G., Evans R. H. The primary afferent depolarizing action of kainate in the rat. Br J Pharmacol. 1986 Feb;87(2):345–355. doi: 10.1111/j.1476-5381.1986.tb10823.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Bettler B., Boulter J., Hermans-Borgmeyer I., O'Shea-Greenfield A., Deneris E. S., Moll C., Borgmeyer U., Hollmann M., Heinemann S. Cloning of a novel glutamate receptor subunit, GluR5: expression in the nervous system during development. Neuron. 1990 Nov;5(5):583–595. doi: 10.1016/0896-6273(90)90213-y. [DOI] [PubMed] [Google Scholar]
- Boulter J., Hollmann M., O'Shea-Greenfield A., Hartley M., Deneris E., Maron C., Heinemann S. Molecular cloning and functional expression of glutamate receptor subunit genes. Science. 1990 Aug 31;249(4972):1033–1037. doi: 10.1126/science.2168579. [DOI] [PubMed] [Google Scholar]
- Burnashev N., Monyer H., Seeburg P. H., Sakmann B. Divalent ion permeability of AMPA receptor channels is dominated by the edited form of a single subunit. Neuron. 1992 Jan;8(1):189–198. doi: 10.1016/0896-6273(92)90120-3. [DOI] [PubMed] [Google Scholar]
- Chen C., Okayama H. High-efficiency transformation of mammalian cells by plasmid DNA. Mol Cell Biol. 1987 Aug;7(8):2745–2752. doi: 10.1128/mcb.7.8.2745. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Egebjerg J., Bettler B., Hermans-Borgmeyer I., Heinemann S. Cloning of a cDNA for a glutamate receptor subunit activated by kainate but not AMPA. Nature. 1991 Jun 27;351(6329):745–748. doi: 10.1038/351745a0. [DOI] [PubMed] [Google Scholar]
- 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]
- Hampson D. R., Huie D., Wenthold R. J. Solubilization of kainic acid binding sites from rat brain. J Neurochem. 1987 Oct;49(4):1209–1215. doi: 10.1111/j.1471-4159.1987.tb10012.x. [DOI] [PubMed] [Google Scholar]
- Hollmann M., O'Shea-Greenfield A., Rogers S. W., Heinemann S. Cloning by functional expression of a member of the glutamate receptor family. Nature. 1989 Dec 7;342(6250):643–648. doi: 10.1038/342643a0. [DOI] [PubMed] [Google Scholar]
- Huettner J. E. Glutamate receptor channels in rat DRG neurons: activation by kainate and quisqualate and blockade of desensitization by Con A. Neuron. 1990 Sep;5(3):255–266. doi: 10.1016/0896-6273(90)90163-a. [DOI] [PubMed] [Google Scholar]
- Hume R. I., Dingledine R., Heinemann S. F. Identification of a site in glutamate receptor subunits that controls calcium permeability. Science. 1991 Aug 30;253(5023):1028–1031. doi: 10.1126/science.1653450. [DOI] [PubMed] [Google Scholar]
- Keinänen K., Wisden W., Sommer B., Werner P., Herb A., Verdoorn T. A., Sakmann B., Seeburg P. H. A family of AMPA-selective glutamate receptors. Science. 1990 Aug 3;249(4968):556–560. doi: 10.1126/science.2166337. [DOI] [PubMed] [Google Scholar]
- London E. D., Coyle J. T. Specific binding of [3H]kainic acid to receptor sites in rat brain. Mol Pharmacol. 1979 May;15(3):492–505. [PubMed] [Google Scholar]
- Monaghan D. T., Bridges R. J., Cotman C. W. The excitatory amino acid receptors: their classes, pharmacology, and distinct properties in the function of the central nervous system. Annu Rev Pharmacol Toxicol. 1989;29:365–402. doi: 10.1146/annurev.pa.29.040189.002053. [DOI] [PubMed] [Google Scholar]
- Monaghan D. T., Cotman C. W. The distribution of [3H]kainic acid binding sites in rat CNS as determined by autoradiography. Brain Res. 1982 Dec 2;252(1):91–100. doi: 10.1016/0006-8993(82)90981-7. [DOI] [PubMed] [Google Scholar]
- Monyer H., Seeburg P. H., Wisden W. Glutamate-operated channels: developmentally early and mature forms arise by alternative splicing. Neuron. 1991 May;6(5):799–810. doi: 10.1016/0896-6273(91)90176-z. [DOI] [PubMed] [Google Scholar]
- Moriyoshi K., Masu M., Ishii T., Shigemoto R., Mizuno N., Nakanishi S. Molecular cloning and characterization of the rat NMDA receptor. Nature. 1991 Nov 7;354(6348):31–37. doi: 10.1038/354031a0. [DOI] [PubMed] [Google Scholar]
- Mullis K. B., Faloona F. A. Specific synthesis of DNA in vitro via a polymerase-catalyzed chain reaction. Methods Enzymol. 1987;155:335–350. doi: 10.1016/0076-6879(87)55023-6. [DOI] [PubMed] [Google Scholar]
- Pritchett D. B., Lüddens H., Seeburg P. H. Type I and type II GABAA-benzodiazepine receptors produced in transfected cells. Science. 1989 Sep 22;245(4924):1389–1392. doi: 10.1126/science.2551039. [DOI] [PubMed] [Google Scholar]
- Robinson J. H., Deadwyler S. A. Kainic acid produces depolarization of CA3 pyramidal cells in the vitro hippocampal slice. Brain Res. 1981 Sep 21;221(1):117–127. doi: 10.1016/0006-8993(81)91067-2. [DOI] [PubMed] [Google Scholar]
- Sanger F., Nicklen S., Coulson A. R. DNA sequencing with chain-terminating inhibitors. Proc Natl Acad Sci U S A. 1977 Dec;74(12):5463–5467. doi: 10.1073/pnas.74.12.5463. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Slevin J. T., Collins J. F., Coyle J. T. Analogue interactions with the brain receptor labeled by [3H]kainic acid. Brain Res. 1983 Apr 11;265(1):169–172. doi: 10.1016/0006-8993(83)91351-3. [DOI] [PubMed] [Google Scholar]
- Sommer B., Keinänen K., Verdoorn T. A., Wisden W., Burnashev N., Herb A., Köhler M., Takagi T., Sakmann B., Seeburg P. H. Flip and flop: a cell-specific functional switch in glutamate-operated channels of the CNS. Science. 1990 Sep 28;249(4976):1580–1585. doi: 10.1126/science.1699275. [DOI] [PubMed] [Google Scholar]
- 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]
- Unnerstall J. R., Wamsley J. K. Autoradiographic localization of high-affinity [3H]kainic acid binding sites in the rat forebrain. Eur J Pharmacol. 1983 Jan 21;86(3-4):361–371. doi: 10.1016/0014-2999(83)90185-1. [DOI] [PubMed] [Google Scholar]
- Verdoorn T. A., Burnashev N., Monyer H., Seeburg P. H., Sakmann B. Structural determinants of ion flow through recombinant glutamate receptor channels. Science. 1991 Jun 21;252(5013):1715–1718. doi: 10.1126/science.1710829. [DOI] [PubMed] [Google Scholar]
- Werner P., Voigt M., Keinänen K., Wisden W., Seeburg P. H. Cloning of a putative high-affinity kainate receptor expressed predominantly in hippocampal CA3 cells. Nature. 1991 Jun 27;351(6329):742–744. doi: 10.1038/351742a0. [DOI] [PubMed] [Google Scholar]
- Westbrook G. L., Lothman E. W. Cellular and synaptic basis of kainic acid-induced hippocampal epileptiform activity. Brain Res. 1983 Aug 22;273(1):97–109. doi: 10.1016/0006-8993(83)91098-3. [DOI] [PubMed] [Google Scholar]
- Yanisch-Perron C., Vieira J., Messing J. Improved M13 phage cloning vectors and host strains: nucleotide sequences of the M13mp18 and pUC19 vectors. Gene. 1985;33(1):103–119. doi: 10.1016/0378-1119(85)90120-9. [DOI] [PubMed] [Google Scholar]