Structure of the zinc-bound amino-terminal domain of the NMDA receptor NR2B subunit

EMBO Journal

Volumn 28, Issue 24, 2009, Pages 3910-3920

  Karakas, Erkan ^a   Simorowski, Noriko ^a   Furukawa, Hiro ^a  

^a Howard Hughes Medical Institute Cold Spring Harbor Laboratory Cold Spring Harbor   (United States)

Author keywords

Allosteric inhibition; Crystallography; NMDA receptor; Zinc binding

Indexed keywords

METABOTROPIC RECEPTOR; N METHYL DEXTRO ASPARTIC ACID RECEPTOR 2B; ZINC BINDING PROTEIN;

AMINO TERMINAL SEQUENCE; ARTICLE; CRYSTAL STRUCTURE; LIGAND BINDING; NONHUMAN; PRIORITY JOURNAL; RAT;

ALLOSTERIC SITE; ANIMALS; BRAIN; CRYSTALLOGRAPHY, X-RAY; ELECTROPHYSIOLOGY; FEMALE; GLUTAMIC ACID; MOLECULAR CONFORMATION; OOCYTES; PROTEIN BINDING; PROTEIN STRUCTURE, TERTIARY; RATS; RECEPTORS, N-METHYL-D-ASPARTATE; XENOPUS LAEVIS; ZINC;

MAMMALIA;

EID: 72449151659     PISSN: 02614189     EISSN: 14602075     Source Type: Journal    
DOI: 10.1038/emboj.2009.338     Document Type: Article

References (52)

1. Adams PD, Grosse-Kunstleve RW, Hung LW, Ioerger TR, McCoy AJ, Moriarty NW, Read RJ, Sacchettini JC, Sauter NK, Terwilliger TC (2002) PHENIX: building new software for automated crystal-lographic structure determination. Acta Crystallogr D Biol Crystallogr 58: 1948-1954
2. Alarcon K, Martz A, Mony L, Neyton J, Paoletti P, Goeldner M, Foucaud B (2008) Reactive derivatives for affinity labeling in the ifenprodil site of NMDA receptors. Bioorg Med Chem Lett 18: 2765-2770
3. Armstrong N, Gouaux E (2000) Mechanisms for activation and antagonism of an AMPA-sensitive glutamate receptor: crystal structures of the GluR2 ligand binding core. Neuron 28: 165-181
4. Choi YB, Lipton SA (1999) Identification and mechanism of action of two histidine residues underlying high-affinity Zn2+ inhibition of the NMDA receptor. Neuron 23: 171-180
5. Clayton A, Siebold C, Gilbert RJ, Sutton GC, Harlos K, McIlhinney RA, Jones EY, Aricescu AR (2009) Crystal structure of the GluR2 amino-terminal domain provides insights into the architecture and assembly of ionotropic glutamate receptors. J Mol Biol 392: 1125-1132
6. Cull-Candy S, Brickley S, Farrant M (2001) NMDA receptor sub-units: diversity, development and disease. Curr Opin Neurobiol 11: 327-335
7. de La Fortelle E, Bricogne G (1997) Maximum-likelihood heavy-atom parameter refinement for multiple isomorphous replacement and multiwavelength anomalous diffraction methods. Methods Enzymol 276: 472-492
8. Dingledine R, Borges K, Bowie D, Traynelis SF (1999) The glutamate receptor ion channels. Pharmacol Rev 51: 7-61
9. Emsley P, Cowtan K (2004) Coot: model-building tools for molecular graphics. Acta Crystallogr D Biol Crystallogr 60: 2126-2132
10. Fayyazuddin A, Villarroel A, Le Goff A, Lerma J, Neyton J (2000) Four residues of the extracellular N-terminal domain of the NR2A subunit control high-affinity Zn2+ binding to NMDA receptors. Neuron 25: 683-694
11. Fitzgerald DJ, Berger P, Schaffitzel C, Yamada K, Richmond TJ, Berger I (2006) Protein complex expression by using multigene baculoviral vectors. Nat Methods 3: 1021-1032
12. Furukawa H, Gouaux E (2003) Mechanisms of activation, inhibition and specificity: crystal structures of the NMDA receptor NR1 ligand-binding core. EMBO J 22: 2873-2885
13. Furukawa H, Singh SK, Mancusso R, Gouaux E (2005) Subunit arrangement and function in NMDA receptors. Nature 438: 185-192
14. Gielen M, Siegler Retchless B, Mony L, Johnson JW, Paoletti P (2009) Mechanism of differential control of NMDA receptor activity by NR2 subunits. Nature 459: 703-707
15. Gogas KR (2006) Glutamate-based therapeutic approaches: NR2B receptor antagonists. Curr Opin Pharmacol 6: 68-74
16. Han X, Tomitori H, Mizuno S, Higashi K, Full C, Fukiwake T, Terui Y, Leewanich P, Nishimura K, Toida T, Williams K, Kashiwagi K, Igarashi K (2008) Binding of spermine and ifenprodil to a purified, soluble regulatory domain of the N-methyl-D-aspartate receptor. J Neurochem 107: 1566-1577
17. Harding MM (2002) Metal-ligand geometry relevant to proteins and in proteins: sodium and potassium. Acta Crystallogr D Biol Crystallogr 58: 872-874
18. Jin R, Singh SK, Gu S, Furukawa H, Sobolevsky AI, Zhou J, Jin Y, Gouaux E (2009) Crystal structure and association behaviour of the GluR2 amino-terminal domain. EMBO J 28: 1812-1823
19. Johnson JW, Ascher P (1987) Glycine potentiates the NMDA response in cultured mouse brain neurons. Nature 325: 529-531
20. Jones TA, Kjeldgaard M (1997) Electron-density map interpretation. Methods Enzymol 277: 173-208
21. Kandel ER, Schwartz JH, Jessell TM (1995) Essentials of Neural Science and Behavior. East Norwalk: Appelton & Lange
22. Kerchner GA, Nicoll RA (2008) Silent synapses and the emergence of a postsynaptic mechanism for LTP. Nat Rev Neurosci 9: 813-825
23. Kumar J, Schuck P, Jin R, Mayer ML (2009) The N-terminal domain of GluR6-subtype glutamate receptor ion channels. Nat Struct Mol Biol 16: 631-638
24. Kunishima N, Shimada Y, Tsuji Y, Sato T, Yamamoto M, Kumasaka T, Nakanishi S, Jingami H, Morikawa K (2000) Structural basis of glutamate recognition by a dimeric metabotropic glutamate receptor. Nature 407: 971-977
25. Kuusinen A, Arvola M, Keinanen K (1995) Molecular dissection of the agonist binding site of an AMPA receptor. EMBO J 14: 6327-6332
26. Low CM, Zheng F, Lyuboslavsky P, Traynelis SF (2000) Molecular determinants of coordinated proton and zinc inhibition of N-methyl-D-aspartate NR1/NR2A receptors. Proc Natl Acad Sci USA 97: 11062-11067
27. MacDermott AB, Mayer ML, Westbrook GL, Smith SJ, Barker JL (1986) NMDA-receptor activation increases cytoplasmic calcium concentration in cultured spinal cord neurones. Nature 321: 519-522
28. Marinelli L, Cosconati S, Steinbrecher T, Limongelli V, Bertamino A, Novellino E, Case DA (2007) Homology modeling of NR2B modulatory domain of NMDA receptor and analysis of ifenprodil binding. Chem Med Chem 2: 1498-1510
29. Masuko T, Kashiwagi K, Kuno T, Nguyen ND, Pahk AJ, Fukuchi J, Igarashi K, Williams K (1999) A regulatory domain (R1-R2) in the amino terminus of the N-methyl-D-aspartate receptor: effects of spermine, protons, and ifenprodil, and structural similarity to bacterial leucine/isoleucine/valine binding protein. Mol Pharmacol 55: 957-969
30. Mayer ML (2005) Crystal structures of the GluR5 and GluR6 ligand binding cores: molecular mechanisms underlying kainate receptor selectivity. Neuron 45: 539-552
31. Mayer ML, Westbrook GL, Guthrie PB (1984) Voltage-dependent block by Mg2+ of NMDA responses in spinal cord neurones. Nature 309: 261-263
32. McCoy AJ, Grosse-Kunstleve RW, Adams PD, Winn MD, Storoni LC, Read RJ (2007) Phaser crystallographic software. J Appl Cryst 40: 658-674
33. Mony L, Krzaczkowski L, Leonetti M, Le Goff A, Alarcon K, Neyton J, Bertrand HO, Acher F, Paoletti P (2009) Structural basis of NR2B-selective antagonist recognition by N-methyl-D-aspartate receptors. Mol Pharmacol 75: 60-74
34. Monyer H, Burnashev N, Laurie DJ, Sakmann B, Seeburg PH (1994) Developmental and regional expression in the rat brain and functional properties of four NMDA receptors. Neuron 12: 529-540
35. Murshudov GN, Vagin AA, Dodson EJ (1997) Refinement of macro-molecular structures by the maximum-likelihood method. Acta Crystallogr D Biol Crystallogr 53: 240-255
36. O'Hara PJ, Sheppard PO, Thogersen H, Venezia D, Haldeman BA, McGrane V, Houamed KM, Thomsen C, Gilbert TL, Mulvihill ER (1993) The ligand-binding domain in metabotropic glutamate receptors is related to bacterial periplasmic binding proteins. Neuron 11: 41-52
37. Otwinowski Z, Minor W (1997) Processing of X-ray diffraction data collected in oscillation mode. Methods Enzymol 276: 307-326
38. Paoletti P, Ascher P, Neyton J (1997) High-affinity zinc inhibition of NMDA NR1-NR2A receptors. J Neurosci 17: 5711-5725
39. Paoletti P, Neyton J (2007) NMDA receptor subunits: function and pharmacology. Curr Opin Pharmacol 7: 39-47
40. Paoletti P, Perin-Dureau F, Fayyazuddin A, Le Goff A, Callebaut I, Neyton J (2000) Molecular organization of a zinc binding N-terminal modulatory domain in a NMDA receptor subunit. Neuron 28: 911-925
41. Paoletti P, Vergnano AM, Barbour B, Casado M (2009) Zinc at glutamatergic synapses. Neuroscience 158: 126-136
42. Perin-Dureau F, Rachline J, Neyton J, Paoletti P (2002) Mapping the binding site of the neuroprotectant ifenprodil on NMDA receptors. J Neurosci 22: 5955-5965
43. Plested AJ, Mayer ML (2007) Structure and mechanism of kainate receptor modulation by anions. Neuron 53: 829-841
44. Plested AJ, Vijayan R, Biggin PC, Mayer ML (2008) Molecular basis of kainate receptor modulation by sodium. Neuron 58: 720-735
45. Rachline J, Perin-Dureau F, Le Goff A, Neyton J, Paoletti P (2005) The micromolar zinc-binding domain on the NMDA receptor subunit NR2B. J Neurosci 25: 308-317
46. Sudhof TC, Malenka RC (2008) Understanding synapses: past, present, and future. Neuron 60: 469-476
47. Terwilliger T (2004) SOLVE and RESOLVE: automated structure solution, density modification and model building. J Synchrotron Radiat 11: 49-52
48. Trakhanov S, Vyas NK, Luecke H, Kristensen DM, Ma J, Quiocho FA (2005) Ligand-free and-bound structures of the binding protein (LivJ) of the Escherichia coli ABC leucine/isoleucine/valine transport system: trajectory and dynamics of the interdomain rotation and ligand specificity. Biochemistry 44: 6597-6608
49. Traynelis SF, Hartley M, Heinemann SF (1995) Control of proton sensitivity of the NMDA receptor by RNA splicing and polya-mines. Science 268: 873-876
50. Williams K (1993) Ifenprodil discriminates subtypes of the N-methyl-D-aspartate receptor: selectivity and mechanisms at recombinant heteromeric receptors. Mol Pharmacol 44: 851-859
51. Wong E, Ng FM, Yu CY, Lim P, Lim LH, Traynelis SF, Low CM (2005) Expression and characterization of soluble amino-terminal domain of NR2B subunit of N-methyl-D-aspartate receptor. Protein Sci 14: 2275-2283
52. Yao Y, Harrison CB, Freddolino PL, Schulten K, Mayer ML (2008) Molecular mechanism of ligand recognition by NR3 subtype glutamate receptors. EMBO J 27: 2158-2170