The N-terminal domains of both NR1 and NR2 subunits determine allosteric Zn2+ inhibition and glycine affinity of N-methyl-D-aspartate receptors

Molecular Pharmacology

Volumn 72, Issue 6, 2007, Pages 1535-1544

  Madry, Christian ^a   Mesic, Ivana ^a,b   Betz, Heinrich ^a   Laube, Bodo ^a,b  

^a MAX PLANCK INSTITUTE FOR BRAIN RESEARCH   (Germany)

^b DARMSTADT UNIVERSITY OF TECHNOLOGY   (Germany)

Author keywords

[No Author keywords available]

Indexed keywords

3 (2 CARBOXY 4,6 DICHLORO 3 INDOLYL)PROPIONIC ACID; BACTERIAL PROTEIN; BINDING PROTEIN; DIZOCILPINE; GLUTAMATE RECEPTOR; GLYCINE; IFENPRODIL; N METHYL DEXTRO ASPARTIC ACID RECEPTOR; N METHYL DEXTRO ASPARTIC ACID RECEPTOR 1; N METHYL DEXTRO ASPARTIC ACID RECEPTOR 2; THROMBIN; UNCLASSIFIED DRUG; ZINC ION;

AMINO TERMINAL SEQUENCE; ARTICLE; CELL STRAIN HEK293; CONTROLLED STUDY; HUMAN; HUMAN CELL; PRIORITY JOURNAL; PROTEIN DEGRADATION; PROTEIN DOMAIN; PROTEIN EXPRESSION; WILD TYPE;

ALLOSTERIC REGULATION; ANIMALS; BINDING SITES; CELL LINE; FEMALE; GLYCINE; HUMANS; PROTEIN STRUCTURE, TERTIARY; PROTEIN SUBUNITS; RECEPTORS, N-METHYL-D-ASPARTATE; XENOPUS LAEVIS; ZINC;

EID: 36348946416     PISSN: 0026895X     EISSN: 15210111     Source Type: Journal    
DOI: 10.1124/mol.107.040071     Document Type: Article

References (40)

1. Armstrong N, Jasti J, Beich-Frandsen M, and Gouaux E (2006) Measurement of conformational changes accompanying desensitization in an ionotropic glutamate receptor. Cell 127:85-97.
2. Ayalon G and Stern-Bach Y (2001) Functional assembly of AMPA and kainate receptors is mediated by several discrete protein-protein interactions. Neuron 31:103-113.
3. Chen GQ, Cui C, Mayer ML, and Gouaux E (1999) Functional characterization of a potassium-selective prokaryotic glutamate receptor. Nature 402:817-821.
4. Chen N, Moshaver A, and Raymond LA (1997) Differential sensitivity of recombinant N-methyl-D-aspartate receptor subtypes to zinc inhibition. Mol Pharmacol 51:1015-1023.
5. 2+ modulation of the NMDA receptor. J Neurosci 21:392-400.
6. 2+ inhibition of the NMDA receptor. Neuron 23:171-180.
7. Cull-Candy S, Brickley S, and Farrant M (2001) NMDA receptor subunits: diversity, development and disease. Curr Opin Neurobiol 11:327-335.
8. Dingledine R, Borges K, Bowie D, and Traynelis SF (1999) The glutamate receptor ion channels. Pharmacol Rev 51:7-61.
9. 2+ binding to NMDA receptors. Neuron 25:683-694.
10. Fernández-Monreal M, López-Atalaya J, Benchenane K, Cacquevel M, Dulin F, Le Caer JP, Rossier J, Jarrige AC, MacKenzie E, Colloc'h N, et al. (2004) Arginine 260 of the amino-terminal domain of the NR1 subunit is critical for tissue-type plasminogen activator-mediated enhancement of N-methyl-D-aspartate receptor signalling. J Biol Chem 279:50850-50856.
11. Furukawa H, Singh SK, Mancusso R, and Gouaux E (2005) Subunit arrangement and function in NMDA receptors. Nature 438:185-192.
12. Herin GA and Aizenman E (2004) Amino-terminal domain regulation of NMDA receptor function. Eur J Pharmacol 500:101-111.
13. Hu B and Zheng F (2005) Molecular determinants of glycine-independent desensitization of NR1/NR2A receptors. J Pharmacol Exp Ther 313:563-569.
14. Krupp JJ, Vissel B, Heinemann SF, and Westbrook GL (1998) N-terminal domains in the NR2 subunit control desensitization of NMDA receptors. Neuron 20:317-327.
15. Kunishima N, Shimada Y, Tsuji Y, Sato T, Yamamoto M, Kumasaka T, Nakanishi S, Jingami H, and Morikawa K (2000) Structural basis of glutamate recognition by a dimeric metabotropic glutamate receptor. Nature 407:971-977.
16. 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.
17. Kuusinen A, Abele R, Madden DR, and Keinanen K (1999) Oligomerization and ligand-binding properties of the ectodomain of the α-amino-3-hydroxy-5- methyl-4-isoxazole propionic acid receptor subunit GluRD. J Biol Chem 274:28937-28943.
18. Laube B, Hirai H, Sturgess M, Betz H, and Kuhse J (1997) Molecular determinants of agonist discrimination by NMDA receptor subunits: analysis of the glutamate binding site on the NR2B subunit. Neuron 18:493-503.
19. Laube B, Kuhse J, and Betz H (1998) Evidence for a tetrameric structure of recombinant NMDA receptors. J Neurosci 18:2954-2961.
20. Laube B, Kuhse J, Rundstrom N, Kirsch J, Schmieden V, and Betz H (1995) Modulation by zinc ions of native rat and recombinant human inhibitory glycine receptors. J Physiol 483:613-619.
21. Laurie DJ and Seeburg PH (1994) Ligand affinities at recombinant N-methyl-D-aspartate receptors depend on subunit composition. Eur J Pharmacol 268:335-345.
22. Low CM, Zheng F, Lyuboslawsky P, and Traynelis SF (2000) Molecular determinants of coordinated proton and zinc inhibition of N-methyl- D-aspartate NR1/NR2A receptors. Proc Natl Acad Sci U S A 97:11062-11067.
23. Madden DR (2002) The structure and function of glutamate receptor ion channels. Nat Rev Neurosci 3:91-101.
24. Madry C, Mesic I, Bartholomäus I, Nicke A, Betz H, and Laube B (2007) Principal role of NR3 subunits in NR1/NR3 excitatory glycine receptor function. Biochem Biophys Res Commun 354:102-108.
25. Matsuda S, Kamiya Y, and Yuzaki M (2005) Roles of the N-terminal domain on the function and quaternary structure of the ionotropic glutamate receptor. J Biol Chem 280:20021-20029.
26. Mayer ML (2006) Glutamate receptors at atomic resolution. Nature 440:456-462.
27. Meddows E, Le Bourdelles B, Grimwood S, Wafford K, Sandhu S, Whiting P, and McIlhinney RA (2001) Identification of molecular determinants that are important in the assembly of N-methyl-D-aspartate receptors. J Biol Chem 276:18795-18803.
28. Nicole O, Docagne F, Ali C, Margaill I, Carmeliet P, MacKenzie ET, Vivien D, and Buisson A (2001) The proteolytic activity of tissue-plasminogen activator enhances NMDA receptor-mediated signaling. Nat Med 7:59-64.
29. Paoletti P, Ascher P, and Neyton J (1997) High-affinity zinc inhibition of NMDA NR1-NR2A receptors. J Neurosci 17:5711-5725.
30. Paoletti P, Perin-Dureau F, Fayyazuddin A, Le Goff A, Callebaut I, and Neyton J (2000) Molecular organization of a zinc binding N-terminal modulatory domain in a NMDA receptor subunit. Neuron 28:911-925.
31. Pasternack A, Coleman SK, Jouppila A, Mottershead DG, Lindfors M, Pasternack M, and Keinanen K (2002) α-Amino-3-hydroxy-5-methyl-4- isoxazolepropionic acid (AMPA) receptor channels lacking the N-terminal domain. J Biol Chem 277:49662-49667.
32. Perin-Dureau F, Rachline J, Neyton J, and Paoletti P (2002) Mapping the binding site of the neuroprotectant Ifenprodil on NMDA receptors. J Neurosci 22:5955-5965.
33. Priestley T, Laughton P, Myers J, Le Bourdelles B, Kerby J, and Whiting PJ (1995) Pharmacological properties of recombinant human N-methyl- D-aspartate receptors comprising NR1a/NR2A and NR1A/NR2B subunit assemblies expressed in permanent transfected mouse fibroblast cells. Mol Pharmacol 48:841-848.
34. Rachline J, Perin-Dureau F, Le Goff A, Neyton J, and Paoletti P (2005) The micromolar zinc-binding domain on the NMDA receptor subunit NR2B. J Neurosci 25:308-317.
35. Sadtler S, Laube B, Lashub A, Nicke A, Betz H, and Schmalzing G (2003) A basic cluster determines topology of the cytoplasmic M3-M4 loop of the glycine receptor α1 subunit. J Biol Chem 278:16782-16790.
36. Traynelis SF, Burgess MF, Zheng F, Lyuboslavsky P, and Powers JL (1998) Control of voltage-independent zinc inhibition of NMDA receptors by the NR1 subunit. J Neurosci 18:6163-6175.
37. Tsirka SE, Gualandris A, Amaral DG, and Strickland S (1995) Excitotoxin-induced neuronal degeneration and seizure are mediated by tissue plasminogen activator. Nature 377:340-344.
38. Williams K (1996) Separating dual effects of zinc at recombinant N-methyl-D-aspartate receptors. Neurosci Lett 215:9-12.
39. Yao Y and Mayer ML (2006) Characterization of a soluble ligand binding domain of the NMDA receptor regulatory subunit NR3A. J Neurosci 26:4559-4566.
40. Zheng F, Erreger K, Low CM, Banke T, Lee CJ, Conn PJ, and Traynelis SF (2001) Allosteric interaction between the amino terminal domain and the ligand binding domain of NR2A. Nat Neurosci 4:894-901.