Molecular determinants of agonist discrimination by NMDA receptor subunits: Analysis of the glutamate binding site on the NR2B subunit

Neuron

Volumn 18, Issue 3, 1997, Pages 493-503

  Laube, Bodo ^a   Hirai, Hirokazu ^c   Sturgess, Mike ^b   Betz, Heinrich ^a   Kuhse, Jochen ^a  

^a MAX PLANCK INSTITUTE FOR BRAIN RESEARCH   (Germany)

^b Symphony Pharmaceuticals   (United States)

^c INST OF PHYS AND CHEMICAL RESEARCH   (Japan)

Author keywords

[No Author keywords available]

Indexed keywords

MUTANT PROTEIN; N METHYL DEXTRO ASPARTIC ACID RECEPTOR; RECEPTOR SUBUNIT;

ARTICLE; BINDING SITE; GENE MUTATION; NONHUMAN; PRIORITY JOURNAL; PROTEIN DOMAIN; RECEPTOR BINDING; RECEPTOR BLOCKING;

EID: 0030991790     PISSN: 08966273     EISSN: None     Source Type: Journal    
DOI: 10.1016/S0896-6273(00)81249-0     Document Type: Article

References (55)

1. Arvola, M., and Keinänen, K. (1996). Characterization of the ligand-binding domains of glutamate receptor (GIuR-B and GIuR-D) subunits expressed in Escherichia coli as periplasmic proteins. J. Biol. Chem. 271, 15527-15532.
2. Bennett, J.A.,and Dingledine, R. (1995). Topology profile for a glutamate receptor: three transmembrane domains and a channel-lining reentrant membrane loop. Neuron 14, 373-384.
3. Benveniste, M., and Mayer, M.L. (1991). Kinetic analysis of antagonist action at N-methyl-D-aspartic acid receptors. Two binding sites each for glutamate and glycine. Biophys. J. 59, 560-573.
4. Chamberlin, R., and Bridges, R. (1993). Conformationally constrained acidic amino acids as probes of glutamate receptors and transporters. In Drug Design for Neuroscience, A. P. Kozikowski, ed. (New York: Raven Press, Ltd.).
5. Choi, D.W. (1988). Glutamate neurotoxicity and diseases of the nervous system. Neuron 1, 623-634.
6. Clements, J.D., and Westbrook, G.L. (1991). Activation kinetics reveal the number of glutamate and glycine binding sites on the N-methyl-D-aspartate receptor. Neuron 7, 605-613.
7. Durand, G.M., Gregor, P., Zheng, X., Bennett, M.V., Uhl, G.R., and Zukin, R.S. (1992). Cloning of an apparent splice variant of the rat N-methyl-D-aspartate receptor NMDAR1 with altered sensitivity to polyamines and activators of protein kinase C. Proc. Natl. Acad. Sci. USA 89, 9359-9363.
8. Fasman, G.D. (1989). Prediction of Protein Structure and the Principles of Protein Conformation. (New York: Plenum Press).
9. Grimwood, S., Le Bourdellès, B., and Whiting, P.J. (1995). Recombinant human NMDA homomeric NMDAR1 receptors expressed in mammalian cells form a high affinity glycine antagonist binding site. J. Neurochem. 64, 525-530.
10. Henderson, G., Johnson, J.W., and Ascher, P. (1990). Competitive antagonists and partial agonists at the glycine modulatory site of the mouse N-methyl-D-aspartate receptor. J. Physiol. (Lond.) 430, 189-212.
11. Hirai, H., Kirsch, J., Laube, B., Betz, H., and Kuhse, J. (1996). The glycine binding site of the N-methyl-D-aspartate receptor subunit NR1: identification of novel determinants of coagonist potentiation in the extracellular M3-M4 loop region. Proc. Natl. Acad. Sci. USA 93, 6031-6036.
12. Hollmann, M., and Heinemann, S. (1994). Cloned glutamate receptors. Annu. Rev. Neurosci. 17, 31-108.
13. Hollmann, M., Boulter, J., Maron, C., Beasley, L., Sullivan, J., Pecht, G., and Heinemann, S. (1993). Zinc potentiates agonist-induced currents at certain splice variants of the NMDA receptor. Neuron 10, 943-954.
14. Johnson, J.W., and Ascher, P. (1987). Glycine potentiates the NMDA response in cultured mouse brain neurons. Nature 325, 529-531.
15. Kang, C.-H., Shin, W.-C., Yamagata, Y., Gokcen, S., Ames, G.F.-L., and Kim, S.-H. (1991). Crystal structure for the lysine-, arginine-, ornithine-binding protein (LAO) from Salmonella typhimurium at 2.7-Å resolution. J. Biol. Chem. 266, 23893-23899.
16. Kawamoto, S., Uchino, S., Hattori, S., Hamajima, K., Mishina, M., Nakajima-lijima, S.,and Okuda, K. (1995). Expression and characterization of the ζ1 subunit of the N-methyl-D-aspartate (NMDA) receptor channel in a baculovirus system. Mol. Brain Res. 30, 137-148.
17. Kemp, J.A., and Leeson, P.D. (1993). The glycine site of the NMDA receptor: five years on. Trends Pharmacol. Sci. 14, 20-25.
18. Kendrick, S.J., Lynch, D.R., and Pritchett, D.B. (1996). Characterization of glutamate binding sites in receptors assembled from transfected NMDA receptor subunits. J. Neurochem. 67, 608-616.
19. Kleckner, N.W., and Dingledine, R. (1988). Requirement for glycine in activation of NMDA-receptors expressed in Xenopus oocytes. Science 241, 835-837.
20. Kuner, T., Wollmuth, L.P., Karlin, A., Seeburg, P.H., and Sakmann, B. (1996). Structure of the NMDA receptor channel M2 segment inferred from the accessibility of substituted cysteines. Neuron 17, 343-352.
21. Kuryatov, A., Laube, B., Betz, H., and Kuhse, J. (1994). Mutational analysis of the glycine-binding site of the NMDA receptor: structural similarity with bacterial amino acid-binding proteins. Neuron 12, 1291-1300.
22. Kutsuwada, T., Kashiwabuchi, N., Mori, H., Sakimura, K., Kushiya, E., Araki, K., Meguro, H., Masaki, H., Kumanishi, T., Arakawa, M., and Mishina, M. (1992). Molecular diversity of the NMDA receptor channel. Nature 358, 36-41.
23. Kuusinen, A., Arvola, M., and Keinänen, K. (1995). Molecular dissection of the agonist binding site of an AMPA receptor. EMBO J. 14, 6327-6332.
24. Laube, B., Kuryatov, A., Kuhse, J., and Betz, H. (1993). Glycine-glutamate interactions at the NMDA receptor: role of cysteine residues. FEBS Lett. 335, 331-334.
25. Laurie, D.J., and Seeburg, P.H. (1994). Ligand affinities at recombinant N-methyl-D-aspartate receptors depend on subunit composition. Eur. J. Pharmacol. 268, 335-345.
26. Lynch, D.R., Anegawa, N.J., Verdoorn, T., and Pritchett, D.B. (1994). N-methyl-D-aspartate receptors: different subunit requirements for binding of glutamate antagonists, glycine antagonists, and channel-blocking agents. Mol. Pharmacol. 45, 540-545.
27. Madison, D.V. (1991). Mechanisms underlying long-term potentiation of synaptic transmission. Annu. Rev. Neurosci. 14, 379-397.
28. Mano, I., Lamed, Y., and Teichberg, V.I. (1996). A Venus flytrap mechanism for activation and desensitization of α-amino-3-hydroxy-5-methyl-4-isoxazole propionic acid receptors. J. Biol. Chem. 271, 15299-15302.
29. Mayer, M.L., and Westbrook, G.L. (1987). Permeation and block of N-methyl-D-aspartic acid receptor channels by divalent cations in mouse cultured central neurones. J. Physiol. (Lond.) 394, 501-527.
30. 2+ of NMDA responses in spinal cord neurones. Nature 309, 261-263.
31. Mayer, M.L., Vycklicky, L., and Clements, J. (1989). Regulation of NMDA receptor desensitization in mouse hippocampal neurons by glycine. Nature 338, 425-427.
32. Mcllhinney, R.A.J., Molnár, E., Atack, J.R., and Whiting, P.J. (1996). Cell surface expression of the human N-methyl-D-aspartate receptor subunit 1a requires the co-expression of the NR2A subunit in transfected cells. Neuroscience 70, 989-997.
33. Meguro, H., Mori, H., Araki, K., Kushiya, E., Kutsuwada, T., Yamazaki, M., Kumanishi, T., Arakawa, M., Sakimura, K., and Mishina, M. (1992). Functional characterization of a heteromeric NMDA receptor channel expressed from cloned cDNAs. Nature 357, 70-74.
34. Monyer, H., Sprengel, R., Schoepfer, R., Herb, A., Higuchi, M., Lomeli, H., Burnashev, N., Sakmann, B., and Seeburg, P.H. (1992). Heteromeric NMDA receptors: molecular and functional distinction of subtypes. Science 256, 1217-1221.
35. Moriyoshi, K., Masu, M., Ishii, T., Shigemoto, R., Mizuno, N., and Nakanishi, S. (1991). Molecular cloning and characterization of the rat NMDA receptor. Nature 354, 31-37.
36. Nakanishi, S. (1992). Molecular diversity of glutamate receptors and implications for brain function. Science 258, 597-603.
37. Nakanishi, N., Shneider, N.A., and Axel, R. (1990). A family of glutamate receptor genes: evidence for the formation of heteromultimeric receptors with distinct channel properties. Neuron 5, 569-581.
38. Nakanishi, N., Axel, R., and Shneider, N.A. (1992). Alternative splicing generates functionally distinct N-methyl-D-aspartate receptors. Proc. Natl. Acad. Sci. USA 89, 8552-8556.
39. Oh, B.H., Pandit, J., Kang, C.H., Nikaido, K., Gokcen, S., Ames, G.F.L., and Kim, S.H. (1993). Three-dimensional structures of the periplasmic lysine/arginine/ornithine-binding protein with and withshy; out a ligand. J. Biol. Chem. 268, 11348-11355.
40. O'Hara, P.J., Sheppard, P.O., Thogersen, H., Venezia, D., Haldemann, B.A., McGrane, V., Houamed, K.M.,Thomsen, C., Gilber, T.L., and Mulvihill, E.R. (1993). The ligand-binding domain in metabotropic glutamate receptors is related to bacterial periplasmic binding proteins. Neuron 11, 41-52.
41. Olney, J.W. (1990). Excitotoxic amino acids and neuropsychiatric disorders. Annu. Rev. Pharmacol. Toxicol. 30, 47-71.
42. Paas, Y., Devillers-Thiéry, A., Changeux, J.-P., Medevielle, F., and Teichberg, V. (1996a). Identification of an extracellular motif involved in the binding of guanine nucleotides by a glutamate receptor. EMBO J. 15, 1548-1556.
43. Paas, Y., Eisenstein, M., Medevielle, F., Teichberg, V.I., and Devillers-Thiéry, A. (1996b). Identification of the amino acid subsets accounting for the ligand binding specificity of a glutamate receptor. Neuron 17, 979-990.
44. Priestley, T., Laughton, P., Myers, J., Le Bourdellès, B., Kerby, J., and Whiting, P.J. (1995). Pharmacological properties of recombinant human NMDA receptors comprising NR1a/NR2A and NR1a/NR2B subunit assemblies expressed in permanently transfected mouse fibroblast cells. Mol. Pharmacol. 48, 841-848.
45. 3H-labeled MK-801 binding to the excitatory amino acid receptor complex from rat brain is enhanced by glycine. Proc. Natl. Acad. Sci. USA 84, 7744-7748.
46. Schmieden, V., Grenningloh, G., Schofield, P.R., and Betz, H. (1989). Functional expression in Xenopusoocytes of the strychnine binding 48 kd subunit of the glycine receptor. EMBO J. 8, 695-700.
47. Shimamoto, K., and Ohfune, Y. (1996). Syntheses and conformational analyses of glutamate analogs: 2-(2-carboxy-3-substituted-cyclopropyl)glycines as useful probes for excitatory amino acid receptors. J. Med. Chem. 39, 407-423.
48. Stern-Bach, Y., Bettler, B., Hartley, M., Sheppard, P.O., O'Hara, J., and Heinemann, S.F. (1994). Agonist selectivity of glutamate receptors is specified by two domains structurally related to bacterial amino-acid binding proteins. Neuron 13, 1345-1357.
49. Sugihara, H., Moriyoshi, K., Ishii, T., Masu, M., and Nakanishi, S. (1992). Structures and properties of seven isoforms of the NMDA receptor generated by alternative splicing. Biochem. Biophys. Res. Comm. 185, 826-832.
50. Sullivan, J.M., Traynelis, S.F., Chen, H.S.V., Escobar, W., Heinemann, S.F., and Lipton, S.A. (1994). Identification of two cysteine residues that are required for redox modulation of the NMDA subtype of glutamate receptor. Neuron 13, 929-936.
51. Uchino, S., Sakimura, K., Nagahari, K., and Mishina, M. (1992). Mutations in a putative agonist binding region of the AMPA-selective glutamate receptor channel. FEBS Lett. 308, 253-257.
52. Wafford, K.A., Kathoria, M., Bain, C.J., Marshall, G., Le Bourdellès, B., Kemp, J.A., and Whiting, P.J. (1995). Identification of amino acids in the N-methyl-D-aspartate receptor NR1 subunit that contribute to the glycine binding site. Mol. Pharmacol. 47, 374-380.
53. Wo, Z.G., and Oswald, E. (1994). Transmembrane topology of two kainate receptors revealed by N-glycosylation. Proc. Natl. Acad. Sci. USA 91, 7154-7158.
54. Wo, Z.G., and Oswald, E. (1995). Unraveling the modular design of glutamate-gated ion channels. Trends Neurosci. 18, 161-168.
55. 2+ potentiation of recombinant NMDA receptors. Neuron 12, 811-818.