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Structure and function of inhibitory glycine receptors

Published online by Cambridge University Press:  17 March 2009

Heinrich Betz
Heinrich Betz
Affiliation:
Department of Neurochemistry, Max-Planck-Institute for Brain Research, Deutschordenstrasse 46, 6000 Frankfurt/M. 71, Germany
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Extract

Ion transport by peptide channels has been the major theme in the work of the late P. Läuger. His theoretical and experimental approaches provided the basis for a deeper understanding of pore-mediated ion permeation through biological membranes. This review on a ligand–gated ion channel protein from the mammalian brain is dedicated to the memory of this outstanding scientist.

Type
Research Article
Information
Quarterly Reviews of Biophysics , Volume 25 , Issue 4 , November 1992 , pp. 381 - 394
Copyright
Copyright © Cambridge University Press 1992

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References

Akagi, H., Hirai, K. & Hishinuma, F. (1991). Cloning of a glycine receptor subtype expressed in rat brain and spinal cord during a specific period of neuronal development. FEBS Lett. 281, 160–166.CrossRefGoogle ScholarPubMed
Akagi, T. & Miledi, R. (1988). Heterogeneity of glycine receptors and their RNAs in rat brain and spinal cord. Science 242, 270–273.CrossRefGoogle ScholarPubMed
Akagi, T., Patton, D. E. & Miledi, R. (1989). Discrimination of heterogeneous mRNA encoding strychnine-sensitive glycine receptors in Xenopus oocytes by antisense oligonucleotides. Proc. Natl. Acad. Sci. USA 86, 8103–8107.CrossRefGoogle ScholarPubMed
Altschuler, R. A., Betz, H., Parakkal, M. H., Reeks, K. A. & Wenthold, R. J. (1986). Identification of glycinergic synapses in the cochlear nucleus through immunocytochemical localization of the postsynaptic receptor. Brain Res. 369,316–320.CrossRefGoogle ScholarPubMed
Aprison, M. H. & Daly, E. C. (1978). Biochemical aspects of transmitter at inhibitory synapses: the role of glycine. Adv. Neurochem. 3, 203–294.CrossRefGoogle Scholar
Becker, C.-M. (1992). Convulsants acting at the inhibitory glycine receptor. In Handbook of Experimental Pharmacology, vol 102 Selective Neurotoxicity (ed. Herken, H. and Hucho, F.). Berlin, Heidelberg: Springer-Verlag.Google Scholar
Becker, C.-M., Hermans-Borgmeyer, I., Schmitt, B. & Betz, H. (1986). The glycine receptor deficiency of the mutant mouse spastic: evidence for normal glycine receptor structure and localization. J. Neurosci. 6, 1358–1364.CrossRefGoogle ScholarPubMed
Becker, C.-M., Hoch, W. & Betz, H. (1988). Glycine receptor heterogeneity in rat spinal cord during postnatal development. EMBO J. 7, 3717–3726.CrossRefGoogle ScholarPubMed
Becker, C.-M., Schmieden, V., Tarroni, P., Strasser, U. & Betz, H. (1992). Isoform-selective deficit of glycine receptors in the mouse mutant spastic. Neuron 8, 283–289.CrossRefGoogle ScholarPubMed
Betz, H. (1990 a). Homology and analogy in transmembrane channel design: lessons from synaptic membrane proteins. Biochemistry 29, 3591–3599.CrossRefGoogle ScholarPubMed
Betz, H. (1990 b). Ligand-gated ion channels in the brain: the amino acid receptor family. Neuron 5, 383–392.CrossRefGoogle Scholar
Betz, H. (1991). Glycine receptors: heterogeneous and wide-spread in the mammalian brain. Trends Neurosci. 14, 458–461.CrossRefGoogle Scholar
Bormann, J., Hamill, O. P. & Sakmann, B. (1987). Mechanism of anion permeation through channels gated by glycine and γ-aminobutyric acid in mouse cultured spinal neurones. J. Physiol. 385, 243–286.CrossRefGoogle ScholarPubMed
Bormann, J., Rundström, N., Betz, H. & Langosch, D. (1992). Properties of recombinant glycine receptors: role of β subunit. Submitted.Google Scholar
Changeux, J.-P., Giraudat, J. & Dennis, M. (1987). The nicotinic acetylcholine receptor: molecular architecture of a ligand-regulated ion channel. Trends Biochem. 8, 259–465.Google Scholar
Faber, D. S. & Korn, H. (1986). Instantaneous inward rectification in the Mauthner cell: a postsynaptic booster for excitatory inputs. Neuroscience 9, 1037–1043.CrossRefGoogle Scholar
Garcia-Calvo, M., Ruiz-Gómez, A., Vazquez, J., Morato, E., Valdivieso, F. & Major, F. Jr., (1989). Functional reconstitution of the glycine receptor. Biochemistry 28, 6405–6409.CrossRefGoogle ScholarPubMed
Giraudat, J., Dennis, M., Heidmann, T., Chang, J.-Y. & Changeux, J.-P. (1986). Structure of the high-affinity binding site for noncompetitive blockers of the acetylcholine receptor: serine 262 of the δ subunit is labeled by [3H]chlorpromazine. Proc. Natl. Acad. Sci. USA 83, 2719–2723.CrossRefGoogle ScholarPubMed
Graham, D., Pfeiffer, F. & Betz, H. (1981). UV light-induced crosslinking of strychnine to the glycine receptor of rat spinal cord membranes. Biochem. Biophys. Res. Commun. 102, 1330–1335.CrossRefGoogle Scholar
Graham, D., Pfeiffer, F. & Betz, H. (1983). Photoaffinity-labeling of the glycine receptor of rat spinal cord. Eur. J. Biochem. 131, 519–525.CrossRefGoogle ScholarPubMed
Graham, D., Pfeiffer, F., Simler, R. & Betz, H. (1985). Purification and characterization of the glycine receptor of pig spinal cord. Biochemistry 24, 990–994.CrossRefGoogle ScholarPubMed
Grenningloh, G., Rienitz, A., Schmitt, B., Methfessel, C., Zensen, M., Beyreuther, K., Gundelfinger, E. D. & Betz, H. (1987). The strychnine-binding subunit of the glycine receptor shows homology with nicotinic acetylcholine receptors. Nature 328, 215–220.CrossRefGoogle ScholarPubMed
Grenningloh, G., Pribilla, I., Prior, P., Multhaup, G., Beyreuther, K., Taleb, O. & Betz, H. (1990 a). Cloning and expression of the 58 kd β subunit of the inhibitory glycine receptor. Neuron 4, 963–970.CrossRefGoogle ScholarPubMed
Grenningloh, G., Schmieden, V., Schofield, P. R., Seeburg, P. H., Siddique, T., Mohandas, T. K., Becker, C.-M. & Betz, H. (1990 b). Alpha subunit variants of the human glycine receptor: primary structures, functional expression and chromosomal localization of the corresponding genes. EMBO J. 9, 771–776.CrossRefGoogle ScholarPubMed
Gundersen, C. B., Miledi, R. & Parker, I. (1984). Properties of human brain glycine receptors expressed in Xenopus oocytes. Proc. R. Soc. Lond. Ser. B 221, 235–244.Google ScholarPubMed
Hamill, O. P., Bormann, J. & Sakmann, B. (1983). Activation of multipleconductance state chloride channels in spinal neurones by glycine and GABA. Nature 305, 805–808.CrossRefGoogle ScholarPubMed
Hoch, W., Betz, H. & Becker, C.-M. (1989). Primary cultures of mouse spinal cord express the neonatal isoform of the inhibitory glycine receptor. Neuron 3, 339–348.CrossRefGoogle ScholarPubMed
Horikoshi, T., Asanuma, A., Yanagisawa, K. & Goto, S. (1988). Taurine modulates glycine response in Xenopus oocytes injected with messenger RNA from mouse brain. Mol. Brain Res. 4, 243–246.CrossRefGoogle Scholar
Hucho, F. (1986). The nicotinic acetylcholine receptor and its ion channel. Eur. J. Biochem. 158, 211–226.CrossRefGoogle ScholarPubMed
Hucho, F., Oberthür, W. & Lottspeich, F. (1986). The ion channel of the nicotinic acetylcholine receptor is formed by the homologous helices M II of the receptor subunits. FEBS Lett. 205, 137–141.CrossRefGoogle ScholarPubMed
Imoto, K., Busch, C., Sakmann, B., Mishina, M., Konno, T., Nakai, J., Bujo, H., Mori, Y., Fukuda, K. & Numa, S. (1988). Rings of negatively charged amino acids determine the acetylcholine receptor channel conductance. Nature 355, 645–648.CrossRefGoogle Scholar
Imoto, K., Methfessel, C., Sakmann, B., Mishina, M., Mori, Y., Konno, T., Fukuda, K., Kurasaki, M., Bujo, H., Fujita, Y. & Numa, S. (1986). Location of a δ-subunit region determining ion transport through the acetylcholine receptor channel. Nature 324, 670–674.CrossRefGoogle ScholarPubMed
Kirsch, J., Langosch, D., Prior, P., Littauer, U. Z., Schmitt, B. & Betz, H. (1991). The 93 kDa glycine receptor-associated protein binds to tubulin. J. Biol. Chem. 266, 22242–22245.CrossRefGoogle ScholarPubMed
Krishtal, O. A., Osipchuk, Y. V. & Vrublevsky, S. V. (1988). Properties of glycineactivated conductances in rat brain neurones. Neurosci. Lett. 84, 271–276.CrossRefGoogle ScholarPubMed
Kuhse, J., Schmieden, V. & Betz, H. (1990 a). Identification and functional expression of a novel ligand-binding subunit of the inhibitory glycine receptor. J. Biol. Chem. 265, 22317–22320.CrossRefGoogle ScholarPubMed
Kuhse, J., Schmieden, V. & Betz, H. (1990 b). A single amino acid exchange alters the pharmacology of neonatal rat glycine receptor subunit. Neuron 5, 867–873.CrossRefGoogle ScholarPubMed
Kuhse, J., Kuryatov, A., Maulet, Y., Malosio, M.-L., Schmieden, V. & Betz, H. (1991). Alternative splicing generates two isoforms of the α2 subunit of the inhibitory glycine receptor. FEBS Lett. 283, 73–77.CrossRefGoogle Scholar
Kyte, J. & Dolittle, R. F. (1982). A method for displaying the hydrophobic character of a protein. J. Mol. Biol. 157, 105–132.CrossRefGoogle Scholar
Langosch, D., Becker, C.-M. & Betz, H. (1990). The inhibitory glycine receptor: a ligand-gated chloride channel of the central nervous system. Eur. J. Biochem. 194, 1–8.CrossRefGoogle ScholarPubMed
Langosch, D., Hartung, K., Grell, E., Bamberg, E. & Betz, H. (1991). Ion channel formation by synthetic transmembrane segments of the inhibitory glycine receptor – a model study. Biochim. Biophys. Acta 1063, 36–44.CrossRefGoogle ScholarPubMed
Langosch, D., Thomas, L. & Betz, H. (1988). Conserved quaternary structure of ligand-gated ion channels: the postsynaptic glycine receptor is a pentamer. Proc. Natl. Acad. Sci. USA 85, 7394–7398.CrossRefGoogle ScholarPubMed
Malosio, M.-L., Marqueze-Pouey, B., Kuhse, J. & Betz, H. (1991 a). Widespread expression of glycine receptor subunit mRNAs in the adult and developing rat brain. EMBO J. 10, 2401–2409.CrossRefGoogle ScholarPubMed
Malosio, M.-L., Grenningloh, G., Kuhse, J., Schmieden, V., Schmitt, B., Prior, P. & Betz, H. (1991 b). Alternative splicing generates two variants of the α1 subunit of the inhibitor glycine receptor. J. Biol. Chem. 266, 2048–2053.CrossRefGoogle Scholar
Marvizon, J. C.Vazquez, J., Garcia-Calvo, M., Major, F. Jr., Ruiz-Gómez, A., Valdivieso, F. & Benavides, J. (1986). The glycine receptor: pharmacological studies and mathematical modeling of the allosteric interaction between the glycine- and strychnine-binding sites. Mol. Pharmacol. 30, 590–597.Google ScholarPubMed
Miller, C. (1988). Genetic manipulation of ion channels: a new approach to structure and mechanism. Neuron 2, 1195–1205.CrossRefGoogle Scholar
Mishina, M., Tobimatsu, T., Imoto, K., Tanaka, K., Fujita, Y., Fukuda, K., Kurasaki, M., Takahashi, H., Morimoto, Y., Hrose, T., Inayama, S., Takahashi, T., Kuno, M. & Numa, S. (1985). Location of functional regions of acetylcholine receptor α-subunit by site-directed mutagenesis. Nature 313, 364–369.CrossRefGoogle ScholarPubMed
Noda, M., Takahashi, H., Tanabe, T., Toyosato, M., Kiyotani, S., Furutani, Y., Hirose, T., Takashima, H., Inayama, S., Miyata, T. & Numa, S. (1983). Structural homology of Torpedo californica acetylcholine receptor subunits. Nature 302, 528–532.CrossRefGoogle ScholarPubMed
Parker, I., Sumikawa, K. & Miledi, R. (1988). Responses to GABA, glycine and β-alanine induced in Xenopus oocytes by messenger RNA from chick and rat brain. Proc. R. Soc. Lond. B 233, 201–216.Google ScholarPubMed
Pfeiffer, F. & Betz, H. (1981). Solubilization of the glycine receptor from rat spinal cord. Brain Res. 226, 273–279.CrossRefGoogle ScholarPubMed
Pfeiffer, F., Graham, D. & Betz, H. (1982). Purification by affinity chromatography of the glycine receptor of rat spinal cord. J. Biol. Chem. 257, 9389–9393.CrossRefGoogle ScholarPubMed
Pfeiffer, F., Simler, R., Grenningloh, G. & Betz, H. (1984). Monoclonal antibodies and peptide mapping reveal structural similarities between the subunits of the glycine receptor of rat spinal cord. Proc. Nad. Acad. Sci. USA 81, 7224–7227.CrossRefGoogle ScholarPubMed
Pribilla, I., Takagi, T., Langosch, D., Bormann, J. & Betz, H. (1992). The atypical M2 segment of the β subunit confers picrotoxinin resistance to inhibitory glycine receptor channels. EMBO J., in press.CrossRefGoogle Scholar
Prior, P., Schmitt, B., Grenningloh, G., Pribilla, I., Multhaup, G., Beyreuther, K., Maulet, Y., Werner, P., Langosch, D., Kirsch, J. & Betz, H. (1992). Primary structure and alternative splice variants of gephyrin, a putative glycine receptortubulin linker protein. Neuron 8, 1161–1170.CrossRefGoogle ScholarPubMed
Ruiz-Gómez, A., Morato, E., Garcia-Calvo, M., Valdivieso, F. & Major, F. Jr., (1990). Localization of the strychnine binding site on the 48-kilodalton subunit of the glycine receptor. Biochemistry 29, 7033–7040.CrossRefGoogle ScholarPubMed
Schmieden, V., Grenningloh, G., Schofield, P. R. & Betz, H. (1989). Functional expression in Xenopus oocytes of the strychnine binding 48 kd subunit of the glycine receptor. EMBO J. 8, 695–700.CrossRefGoogle ScholarPubMed
Schmieden, V., Kuhse, J. & Betz, H. (1992). Agonist pharmacology of neonatal and adult glycine receptor α subunits: identification of amino acid residues involved in taurine activation. EMBO J. 11, 2025–2032.CrossRefGoogle ScholarPubMed
Schmitt, B., Knaus, P., Becker, C.-M. & Betz, H. (1987). The M r 93,000 polypeptide of the postsynaptic glycine receptor is a peripheral membrane protein. Biochemistry 26, 805–811.CrossRefGoogle Scholar
Schofield, P. R., Darlison, M., Fujita, N., Burt, D., Stephenson, F., Rodriguez, H., Rhee, L., Ramachandran, J., Reale, V., Glencorse, T., Seeburg, P. H. & Barnard, E. A. (1987). Sequence and functional expression of the GABAA receptor shows a ligand-gated receptor super family. Nature 328, 221–227.CrossRefGoogle Scholar
Sontheimer, H., Becker, C.-M., Pritchett, D. B., Schofield, P. G., Grenningloh, G., Kettenmann, H., Betz, H. & Seeburg, P. H. (1989). Functional chloride channels by mammalian cell expression of rat glycine receptor subunit. Neuron 2, 1491–1497.CrossRefGoogle ScholarPubMed
Takahashi, T. & Momiyama, A. (1991). Single-channel currents underlying glycinergic inhibitory postsynaptic responses in spinal neurons. Neuron 7, 965–969.CrossRefGoogle ScholarPubMed
Triller, A., Cluzeaud, F., Pfeiffer, F., Betz, H. & Korn, H. (1985). Distribution of glycine receptors at central synapses: an immunoelectron microscopy study. J. Cell Biol. 101, 683–688.CrossRefGoogle ScholarPubMed
Twyman, R. E. & MacDonald, R. L. (1991). Kinetic properties of the glycine receptor main- and sub-conductance states of mouse spinal cord neurones in culture. J. Physiol. 435, 303–331.CrossRefGoogle ScholarPubMed
Unwin, N. (1989). The structure of ionic channels in membranes of excitable cells. Neuron 3, 665–676.CrossRefGoogle ScholarPubMed
Vandenberg, R. J., French, C. R., Barry, P. H., Shine, J. & Schofield, P. R. (1992). Antagonism of ligand-gated ion channel receptors: two domains of the glycine receptor α subunit form the strychnine-binding site. Proc. Natl. Acad. Set. USA 89, 1765–1769.CrossRefGoogle ScholarPubMed
Young, A. B. & Snyder, S. H. (1973). Strychnine binding associated with glycine receptors of the central nervous system. Proc. Natl. Acad. Sci. USA 70, 2832–2836.CrossRefGoogle ScholarPubMed
Young, A. B. & Snyder, S. H. (1974). Strychnine binding in rat spinal cord membranes associated with the synaptic glycine receptor: cooperativity of glycine interactions. Mol. Pharmacol. 10, 790–809.Google Scholar