Structure and mechanism of glutamate receptor ion channel assembly, activation and modulation

Current Opinion in Neurobiology

Volumn 21, Issue 2, 2011, Pages 283-290

  Mayer, Mark L ^a  

^a EUNICE KENNEDY SHRIVER NATIONAL INSTITUTE OF CHILD HEALTH AND HUMAN DEVELOPMENT   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

AMPA RECEPTOR; GLUTAMATE RECEPTOR; ION CHANNEL; IONOTROPIC RECEPTOR; KAINIC ACID RECEPTOR; N METHYL DEXTRO ASPARTIC ACID RECEPTOR; N METHYL DEXTRO ASPARTIC ACID RECEPTOR 2A; N METHYL DEXTRO ASPARTIC ACID RECEPTOR 2D; TETRAMER;

ALLOSTERISM; CHANNEL GATING; CRYSTAL STRUCTURE; LIGAND BINDING; MOLECULAR DYNAMICS; NONHUMAN; PRIORITY JOURNAL; PROTEIN ASSEMBLY; PROTEIN CONFORMATION; PROTEIN DOMAIN; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN STRUCTURE; REVIEW; THERMODYNAMICS;

ANIMALS; HUMANS; PROTEIN STRUCTURE, QUATERNARY; RECEPTORS, GLUTAMATE;

EID: 79955673392     PISSN: 09594388     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.conb.2011.02.001     Document Type: Review

References (64)

1. Hollmann M. Structure of ionotropic glutamate receptors. Ionotropic Glutamate Receptors in the CNS 1999, 3-98. Springer-Verlag, [Handbook of Experimental Pharmacology, vol 141]. P. Jonas, H. Monyer (Eds.).
2. Traynelis S.F., Wollmuth L.P., McBain C.J., Menniti F.S., Vance K.M., Ogden K.K., Hansen K.B., Yuan H., Myers S.J., Dingledine R. Glutamate receptor ion channels: structure, regulation, and function. Pharmacol Rev 2010, 62:405-496.
3. Mayer M.L. Glutamate receptors at atomic resolution. Nature 2006, 440:456-462.
4. Sobolevsky A.I., Rosconi M.P., Gouaux E. X-ray structure, symmetry and mechamism of an AMPA-subtype glutamate receptor. Nature 2009, 462:745-756.
5. Nakagawa T., Cheng Y., Ramm E., Sheng M., Walz T. Structure and different conformational states of native AMPA receptor complexes. Nature 2005, 433:545-549.
6. Midgett C.R., Madden D.R. The quaternary structure of a calcium-permeable AMPA receptor: conservation of shape and symmetry across functionally distinct subunit assemblies. J Mol Biol 2008, 382:578-584.
7. Shanks N.F., Maruo T., Farina A.N., Ellisman M.H., Nakagawa T. Contribution of the global subunit structure and stargazin on the maturation of AMPA receptors. J Neurosci 2010, 30:2728-2740.
8. Weston M.C., Schuck P., Ghosal A., Rosenmund C., Mayer M.L. Conformational restriction blocks glutamate receptor desensitization. Nat Struct Mol Biol 2006, 13:1120-1127.
9. Priel A., Selak S., Lerma J., Stern-Bach Y. Block of kainate receptor desensitization uncovers a key trafficking checkpoint. Neuron 2006, 52:1037-1046.
10. Das U., Kumar J., Mayer M.L., Plested A.J. Domain organization and function in GluK2 subtype kainate receptors. Proc Natl Acad Sci USA 2010, 107:8463-8468.
11. Plested A.J., Mayer M.L. AMPA receptor ligand binding domain mobility revealed by functional cross linking. J Neurosci 2009, 29:11912-11923.
12. Plested A.J., Vijayan R., Biggin P.C., Mayer M.L. Molecular basis of kainate receptor modulation by sodium. Neuron 2008, 58:720-735.
13. Prieto M.L., Wollmuth L.P. Gating modes in AMPA receptors. J Neurosci 2010, 30:4449-4459.
14. Poon K., Nowak L.M., Oswald R.E. Characterizing single-channel behavior of GluA3 receptors. Biophys J 2010, 99:1437-1446.
15. Gonzalez J., Du M., Parameshwaran K., Suppiramaniam V., Jayaraman V. Role of dimer interface in activation and desensitization in AMPA receptors. Proc Natl Acad Sci USA 2010, 107:9891-9896.
16. Sun Y., Olson R., Horning M., Armstrong N., Mayer M., Gouaux E. Mechanism of glutamate receptor desensitization. Nature 2002, 417:245-253.
17. Chaudhry C., Weston M.C., Schuck P., Rosenmund C., Mayer M.L. Stability of ligand-binding domain dimer assembly controls kainate receptor desensitization. EMBO J 2009, 28:1518-1530.
18. Armstrong N., Gouaux E. Mechanisms for activation and antagonism of an AMPA-sensitive glutamate receptor: crystal structures of the GluR2 ligand binding core. Neuron 2000, 28:165-181.
19. Kussius C.L., Popescu G.K. NMDA receptors with locked glutamate-binding clefts open with high efficacy. J Neurosci 2010, 30:12474-12479.
20. Wilding T.J., Chen K., Huettner J.E. Fatty acid modulation and polyamine block of GluK2 kainate receptors analyzed by scanning mutagenesis. J Gen Physiol 2010, 136:339-352.
21. Jin R., Singh S.K., Gu S., Furukawa H., Sobolevsky A.I., Zhou J., Jin Y., Gouaux E. Crystal structure and association behaviour of the GluR2 amino-terminal domain. EMBO J 2009, 28:1812-1823.
22. Kumar J., Schuck P., Jin R., Mayer M.L. The N-terminal domain of GluR6-subtype glutamate receptor ion channels. Nat Struct Mol Biol 2009, 16:631-638.
23. Clayton A., Siebold C., Gilbert R.J., Sutton G.C., Harlos K., McIlhinney R.A., Jones E.Y., Aricescu A.R. Crystal structure of the GluR2 amino-terminal domain provides insights into the architecture and assembly of ionotropic glutamate receptors. J Mol Biol 2009, 392:1125-1132.
24. Karakas E., Simorowski N., Furukawa H. Structure of the zinc-bound amino-terminal domain of the NMDA receptor NR2B subunit. EMBO J 2009, 28:3910-3920.
25. Kumar J., Mayer M.L. Crystal structures of the glutamate receptor ion channel GluK3 and GluK5 amino-terminal domains. J Mol Biol 2010, 404:680-696.
26. Schuler T., Mesic I., Madry C., Bartholomaus I., Laube B. Formation of NR1/NR2 and NR1/NR3 heterodimers constitutes the initial step in N-methyl-D-aspartate receptor assembly. J Biol Chem 2008, 283:37-46.
27. Gielen M., Siegler Retchless B., Mony L., Johnson J.W., Paoletti P. Mechanism of differential control of NMDA receptor activity by NR2 subunits. Nature 2009, 459:703-707.
28. Yuan H., Hansen K.B., Vance K.M., Ogden K.K., Traynelis S.F. Control of NMDA receptor function by the NR2 subunit amino-terminal domain. J Neurosci 2009, 29:12045-12058.
29. Gielen M., Le Goff A., Stroebel D., Johnson J.W., Neyton J., Paoletti P. Structural rearrangements of NR1/NR2A NMDA receptors during allosteric inhibition. Neuron 2008, 57:80-93.
30. Mony L., Krzaczkowski L., Leonetti M., Le Goff A., Alarcon K., Neyton J., Bertrand H.O., Acher F., Paoletti P. Structural basis of NR2B-selective antagonist recognition by NMDA receptors. Mol Pharmacol 2009, 75:60-74.
31. Mosley C.A., Myers S.J., Murray E.E., Santangelo R., Tahirovic Y.A., Kurtkaya N., Mullasseril P., Yuan H., Lyuboslavsky P., Le P., et al. Synthesis, structural activity-relationships, and biological evaluation of novel amide-based allosteric binding site antagonists in NR1A/NR2B N-methyl-D-aspartate receptors. Bioorg Med Chem 2009, 17:6463-6480.
32. Yao Y., Harrison C.B., Freddolino P.L., Schulten K., Mayer M.L. Molecular mechanism of ligand recognition by NR3 subtype glutamate receptors. EMBO J 2008, 27:2158-2170.
33. Ahmed A.H., Wang Q., Sondermann H., Oswald R.E. Structure of the S1S2 glutamate binding domain of GLuR3. Proteins 2009, 75:628-637.
34. Kasper C., Frydenvang K., Naur P., Gajhede M., Pickering D.S., Kastrup J.S. Molecular mechanism of agonist recognition by the ligand-binding core of the ionotropic glutamate receptor 4. FEBS Lett 2008, 582:4089-4094.
35. Gill A., Birdsey-Benson A., Jones B.L., Henderson L.P., Madden D.R. Correlating AMPA receptor activation and cleft closure across subunits: crystal structures of the GluR4 ligand-binding domain in complex with full and partial agonists. Biochemistry 2008, 47:13831-13841.
36. Pohlsgaard J., Frydenvang K., Madsen U., Kastrup J.S. Lessons from more than 80 structures of the GluA2 ligand-binding domain in complex with agonists, antagonists and allosteric modulators. Neuropharmacology 2010.
37. Ahmed A.H., Thompson M.D., Fenwick M.K., Romero B., Loh A.P., Jane D.E., Sondermann H., Oswald R.E. Mechanisms of antagonism of the GluR2 AMPA receptor: structure and dynamics of the complex of two willardiine antagonists with the glutamate binding domain. Biochemistry 2009, 48:3894-3903.
38. Clausen R.P., Naur P., Kristensen A.S., Greenwood J.R., Strange M., Brauner-Osborne H., Jensen A.A., Nielsen A.S., Geneser U., Ringgaard L.M., et al. The glutamate receptor GluR5 agonist (S)-2-amino-3-(3-hydroxy-7,8-dihydro-6H-cyclohepta[d]isoxazol-4-yl)propion ic acid and the 8-methyl analogue: synthesis, molecular pharmacology, and biostructural characterization. J Med Chem 2009, 52:4911-4922.
39. Frydenvang K., Lash L.L., Naur P., Postila P.A., Pickering D.S., Smith C.M., Gajhede M., Sasaki M., Sakai R., Pentikainen O.T., et al. Full domain closure of the ligand-binding core of the ionotropic glutamate receptor iGluR5 induced by the high affinity agonist dysiherbaine and the functional antagonist 8,9-dideoxyneodysiherbaine. J Biol Chem 2009, 284:14219-14229.
40. Alushin G.M., Jane D., Mayer M.L. Binding site and ligand flexibility revealed by high resolution crystal structures of GluK1 competitive antagonists. Neuropharmacology 2010, 60:126-134.
41. Cruz L.A., Estebanez-Perpina E., Pfaff S., Borngraeber S., Bao N., Blethrow J., Fletterick R.J., England P.M. 6-Azido-7-nitro-1,4-dihydroquinoxaline-2,3-dione (ANQX) forms an irreversible bond to the active site of the GluR2 AMPA receptor. J Med Chem 2008, 51:5856-5860.
42. Numano R., Szobota S., Lau A.Y., Gorostiza P., Volgraf M., Roux B., Trauner D., Isacoff E.Y. Nanosculpting reversed wavelength sensitivity into a photoswitchable iGluR. Proc Natl Acad Sci USA 2009, 106:6814-6819.
43. Janovjak H., Szobota S., Wyart C., Trauner D., Isacoff E.Y. A light-gated, potassium-selective glutamate receptor for the optical inhibition of neuronal firing. Nat Neurosci 2010, 13:1027-1032.
44. Fenwick M.K., Oswald R.E. On the mechanisms of alpha-amino-3-hydroxy-5-methylisoxazole-4-propionic acid (AMPA) receptor binding to glutamate and kainate. J Biol Chem 2010, 285:12334-12343.
45. Maltsev A.S., Oswald R.E. Hydrophobic side chain dynamics of a glutamate receptor ligand binding domain. J Biol Chem 2010, 285:10154-10162.
46. Chaudhry C., Plested A.J., Schuck P., Mayer M.L. Energetics of glutamate receptor ligand binding domain dimer assembly are modulated by allosteric ions. Proc Natl Acad Sci USA 2009, 106:12329-12334.
47. Vijayan R., Plested A.J., Mayer M.L., Biggin P.C. Selectivity and cooperativity of modulatory ions in a neurotransmitter receptor. Biophys J 2009, 96:1751-1760.
48. Plested A.J., Mayer M.L. Engineering a high-affinity allosteric binding site for divalent cations in kainate receptors. Neuropharmacology 2009, 56:114-120.
49. Hansen K.B., Naur P., Kurtkaya N.L., Kristensen A.S., Gajhede M., Kastrup J.S., Traynelis S.F. Modulation of the dimer interface at ionotropic glutamate-like receptor delta2 by D-serine and extracellular calcium. J Neurosci 2009, 29:907-917.
50. Nayeem N., Zhang Y., Schweppe D.K., Madden D.R., Green T. A nondesensitizing kainate receptor point mutant. Mol Pharmacol 2009, 76:534-542.
51. Ptak C.P., Ahmed A.H., Oswald R.E. Probing the allosteric modulator binding site of GluR2 with thiazide derivatives. Biochemistry 2009, 48:8594-8602.
52. Ahmed A.H., Oswald R.E. Piracetam defines a new binding site for allosteric modulators of alpha-amino-3-hydroxy-5-methyl-4-isoxazole-propionic acid (AMPA) receptors. J Med Chem 2010, 53:2197-2203.
53. Jamieson C., Campbell R.A., Cumming I.A., Gillen K.J., Gillespie J., Kazemier B., Kiczun M., Lamont Y., Lyons A.J., Maclean J.K., et al. A novel series of positive modulators of the AMPA receptor: structure-based lead optimization. Bioorg Med Chem Lett 2010, 20:6072-6075.
54. Jamieson C., Basten S., Campbell R.A., Cumming I.A., Gillen K.J., Gillespie J., Kazemier B., Kiczun M., Lamont Y., Lyons A.J., et al. A novel series of positive modulators of the AMPA receptor: discovery and structure based hit-to-lead studies. Bioorg Med Chem Lett 2010, 20:5753-5756.
55. Ward S.E., Harries M., Aldegheri L., Andreotti D., Ballantine S., Bax B.D., Harris A.J., Harker A.J., Lund J., Melarange R., et al. Discovery of N-[(2S)-5-(6-fluoro-3-pyridinyl)-2,3-dihydro-1H-inden-2-yl]-2-propanesulfo namide, a novel clinical AMPA receptor positive modulator. J Med Chem 2010, 53:5801-5812.
56. Ward S.E., Bax B.D., Harries M. Challenges for and current status of research into positive modulators of AMPA receptors. Br J Pharmacol 2010, 160:181-190.
57. Ahmed A.H., Ptak C.P., Oswald R.E. Molecular mechanism of flop selectivity and subsite recognition for an AMPA receptor allosteric modulator: structures of GluA2 and GluA3 in complexes with PEPA. Biochemistry 2010, 49:2843-2850.
58. Zhang W., St-Gelais F., Grabner C.P., Trinidad J.C., Sumioka A., Morimoto-Tomita M., Kim K.S., Straub C., Burlingame A.L., Howe J.R., et al. A transmembrane accessory subunit that modulates kainate-type glutamate receptors. Neuron 2009, 61:385-396.
59. von Engelhardt J., Mack V., Sprengel R., Kavenstock N., Li K.W., Stern-Bach Y., Smit A.B., Seeburg P.H., Monyer H. CKAMP44: a brain-specific protein attenuating short-term synaptic plasticity in the dentate gyrus. Science 2010, 327:1518-1522.
60. Schwenk J., Harmel N., Zolles G., Bildl W., Kulik A., Heimrich B., Chisaka O., Jonas P., Schulte U., Fakler B., et al. Functional proteomics identify cornichon proteins as auxiliary subunits of AMPA receptors. Science 2009, 323:1313-1319.
61. Shi Y., Suh Y.H., Milstein A.D., Isozaki K., Schmid S.M., Roche K.W., Nicoll R.A. Functional comparison of the effects of TARPs and cornichons on AMPA receptor trafficking and gating. Proc Natl Acad Sci USA 2010, 107:16315-16319.
62. Kato A.S., Gill M.B., Ho M.T., Yu H., Tu Y., Siuda E.R., Wang H., Qian Y.W., Nisenbaum E.S., Tomita S., et al. Hippocampal AMPA receptor gating controlled by both TARP and cornichon proteins. Neuron 2010, 68:1082-1096.
63. Lau A.Y., Roux B. The free energy landscapes governing conformational changes in a glutamate receptor ligand-binding domain. Structure 2007, 15:1203-1214.
64. Vijayan R., Sahai M.A., Czajkowski T., Biggin P.C. A comparative analysis of the role of water in the binding pockets of ionotropic glutamate receptors. Phys Chem Chem Phys 2010.