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Tuning activation of the AMPA-sensitive GluR2 ion channel by genetic adjustment of agonist-induced conformational changes.

Armstrong N, Mayer M, Gouaux E
Proc Natl Acad Sci U S A 100 5736-41 (2003)
Related entries: 1p1o, 1p1q, 1p1u, 1p1w

Cited: 111 times
EuropePMC logo PMID: 12730367

Abstract

The (S)-2-amino-3-(3-hydroxy-5-methyl-4-isoxazole) propionic acid (AMPA) receptor discriminates between agonists in terms of binding and channel gating; AMPA is a high-affinity full agonist, whereas kainate is a low-affinity partial agonist. Although there is extensive literature on the functional characterization of partial agonist activity in ion channels, structure-based mechanisms are scarce. Here we investigate the role of Leu-650, a binding cleft residue conserved among AMPA receptors, in maintaining agonist specificity and regulating agonist binding and channel gating by using physiological, x-ray crystallographic, and biochemical techniques. Changing Leu-650 to Thr yields a receptor that responds more potently and efficaciously to kainate and less potently and efficaciously to AMPA relative to the WT receptor. Crystal structures of the Leu-650 to Thr mutant reveal an increase in domain closure in the kainate-bound state and a partially closed and a fully closed conformation in the AMPA-bound form. Our results indicate that agonists can induce a range of conformations in the GluR2 ligand-binding core and that domain closure is directly correlated to channel activation. The partially closed, AMPA-bound conformation of the L650T mutant likely captures the structure of an agonist-bound, inactive state of the receptor. Together with previously solved structures, we have determined a mechanism of agonist binding and subsequent conformational rearrangements.

Articles - 1p1n mentioned but not cited (5)

  1. Molecular crowding enhances native state stability and refolding rates of globular proteins. Cheung MS, Klimov D, Thirumalai D. Proc Natl Acad Sci U S A 102 4753-4758 (2005)
  2. Tuning activation of the AMPA-sensitive GluR2 ion channel by genetic adjustment of agonist-induced conformational changes. Armstrong N, Mayer M, Gouaux E. Proc Natl Acad Sci U S A 100 5736-5741 (2003)
  3. Enhanced efficacy without further cleft closure: reevaluating twist as a source of agonist efficacy in AMPA receptors. Birdsey-Benson A, Gill A, Henderson LP, Madden DR. J Neurosci 30 1463-1470 (2010)
  4. Divide-and-conquer strategy for large-scale Eulerian solvent excluded surface. Zhao R, Wang M, Tong Y, Wei GW. Commun Inf Syst 18 299-329 (2018)
  5. Diversity-guided Lamarckian random drift particle swarm optimization for flexible ligand docking. Li C, Sun J, Palade V. BMC Bioinformatics 21 286 (2020)


Reviews citing this publication (21)

  1. Glutamate receptor ion channels: structure, regulation, and function. Traynelis SF, Wollmuth LP, McBain CJ, Menniti FS, Vance KM, Ogden KK, Hansen KB, Yuan H, Myers SJ, Dingledine R. Pharmacol Rev 62 405-496 (2010)
  2. Computations of standard binding free energies with molecular dynamics simulations. Deng Y, Roux B. J Phys Chem B 113 2234-2246 (2009)
  3. Glutamate receptor ion channels. Mayer ML. Curr Opin Neurobiol 15 282-288 (2005)
  4. Emerging models of glutamate receptor ion channel structure and function. Mayer ML. Structure 19 1370-1380 (2011)
  5. New insights into the not-so-new NR3 subunits of N-methyl-D-aspartate receptor: localization, structure, and function. Low CM, Wee KS. Mol Pharmacol 78 1-11 (2010)
  6. Pharmacological insights obtained from structure-function studies of ionotropic glutamate receptors. Chen PE, Wyllie DJ. Br J Pharmacol 147 839-853 (2006)
  7. The biochemistry, ultrastructure, and subunit assembly mechanism of AMPA receptors. Nakagawa T. Mol Neurobiol 42 161-184 (2010)
  8. Lessons from more than 80 structures of the GluA2 ligand-binding domain in complex with agonists, antagonists and allosteric modulators. Pøhlsgaard J, Frydenvang K, Madsen U, Kastrup JS. Neuropharmacology 60 135-150 (2011)
  9. Structural aspects of AMPA receptor activation, desensitization and deactivation. Hansen KB, Yuan H, Traynelis SF. Curr Opin Neurobiol 17 281-288 (2007)
  10. AMPA receptor ligands: synthetic and pharmacological studies of polyamines and polyamine toxins. Strømgaard K, Mellor I. Med Res Rev 24 589-620 (2004)
  11. Amino terminal domain regulation of NMDA receptor function. Herin GA, Aizenman E. Eur J Pharmacol 500 101-111 (2004)
  12. Emerging structural explanations of ionotropic glutamate receptor function. McFeeters RL, Oswald RE. FASEB J 18 428-438 (2004)
  13. 2,3-benzodiazepine-type AMPA receptor antagonists and their neuroprotective effects. Szénási G, Vegh M, Szabo G, Kertesz S, Kapus G, Albert M, Greff Z, Ling I, Barkoczy J, Simig G, Spedding M, Harsing LG. Neurochem Int 52 166-183 (2008)
  14. Structural dynamics of an ionotropic glutamate receptor. Kubo M, Ito E. Proteins 56 411-419 (2004)
  15. Size matters in activation/inhibition of ligand-gated ion channels. Du J, Dong H, Zhou HX. Trends Pharmacol Sci 33 482-493 (2012)
  16. Structure, Function, and Pharmacology of Glutamate Receptor Ion Channels. Hansen KB, Wollmuth LP, Bowie D, Furukawa H, Menniti FS, Sobolevsky AI, Swanson GT, Swanger SA, Greger IH, Nakagawa T, McBain CJ, Jayaraman V, Low CM, Dell'Acqua ML, Diamond JS, Camp CR, Perszyk RE, Yuan H, Traynelis SF. Pharmacol Rev 73 298-487 (2021)
  17. Never at rest: insights into the conformational dynamics of ion channels from cryo-electron microscopy. Lau C, Hunter MJ, Stewart A, Perozo E, Vandenberg JI. J Physiol 596 1107-1119 (2018)
  18. Mapping the Conformational Landscape of Glutamate Receptors Using Single Molecule FRET. MacLean DM, Durham RJ, Jayaraman V. Trends Neurosci 42 128-139 (2019)
  19. Glutamate receptors as seen by light: spectroscopic studies of structure-function relationships. Mankiewicz KA, Jayaraman V. Braz J Med Biol Res 40 1419-1427 (2007)
  20. Retour aux sources: defining the structural basis of glutamate receptor activation. Dawe GB, Aurousseau MR, Daniels BA, Bowie D. J Physiol 593 97-110 (2015)
  21. Structural Dynamics of Glutamate Signaling Systems by smFRET. Durham RJ, Latham DR, Sanabria H, Jayaraman V. Biophys J 119 1929-1936 (2020)

Articles citing this publication (85)

  1. Structural basis for partial agonist action at ionotropic glutamate receptors. Jin R, Banke TG, Mayer ML, Traynelis SF, Gouaux E. Nat Neurosci 6 803-810 (2003)
  2. Crystal structures of the GluR5 and GluR6 ligand binding cores: molecular mechanisms underlying kainate receptor selectivity. Mayer ML. Neuron 45 539-552 (2005)
  3. Glutamate receptors at atomic resolution. Mayer ML. Nature 440 456-462 (2006)
  4. Measurement of conformational changes accompanying desensitization in an ionotropic glutamate receptor. Armstrong N, Jasti J, Beich-Frandsen M, Gouaux E. Cell 127 85-97 (2006)
  5. Stargazin modulates native AMPA receptor functional properties by two distinct mechanisms. Turetsky D, Garringer E, Patneau DK. J Neurosci 25 7438-7448 (2005)
  6. Mechanism of partial agonist action at the NR1 subunit of NMDA receptors. Inanobe A, Furukawa H, Gouaux E. Neuron 47 71-84 (2005)
  7. Regulation of AMPA receptor gating by ligand binding core dimers. Horning MS, Mayer ML. Neuron 41 379-388 (2004)
  8. TARP auxiliary subunits switch AMPA receptor antagonists into partial agonists. Menuz K, Stroud RM, Nicoll RA, Hays FA. Science 318 815-817 (2007)
  9. AMPA receptor binding cleft mutations that alter affinity, efficacy, and recovery from desensitization. Robert A, Armstrong N, Gouaux JE, Howe JR. J Neurosci 25 3752-3762 (2005)
  10. Conformational restriction blocks glutamate receptor desensitization. Weston MC, Schuck P, Ghosal A, Rosenmund C, Mayer ML. Nat Struct Mol Biol 13 1120-1127 (2006)
  11. ATP binding at human P2X1 receptors. Contribution of aromatic and basic amino acids revealed using mutagenesis and partial agonists. Roberts JA, Evans RJ. J Biol Chem 279 9043-9055 (2004)
  12. X-ray structures of AMPA receptor-cone snail toxin complexes illuminate activation mechanism. Chen L, Dürr KL, Gouaux E. Science 345 1021-1026 (2014)
  13. Crystal structures of the kainate receptor GluR5 ligand binding core dimer with novel GluR5-selective antagonists. Mayer ML, Ghosal A, Dolman NP, Jane DE. J Neurosci 26 2852-2861 (2006)
  14. The free energy landscapes governing conformational changes in a glutamate receptor ligand-binding domain. Lau AY, Roux B. Structure 15 1203-1214 (2007)
  15. Structural landscape of isolated agonist-binding domains from single AMPA receptors. Landes CF, Rambhadran A, Taylor JN, Salatan F, Jayaraman V. Nat Chem Biol 7 168-173 (2011)
  16. Molecular mechanism of AMPA receptor noncompetitive antagonism. Balannik V, Menniti FS, Paternain AV, Lerma J, Stern-Bach Y. Neuron 48 279-288 (2005)
  17. Structural and single-channel results indicate that the rates of ligand binding domain closing and opening directly impact AMPA receptor gating. Zhang W, Cho Y, Lolis E, Howe JR. J Neurosci 28 932-943 (2008)
  18. Label-free microscale thermophoresis discriminates sites and affinity of protein-ligand binding. Seidel SA, Wienken CJ, Geissler S, Jerabek-Willemsen M, Duhr S, Reiter A, Trauner D, Braun D, Baaske P. Angew Chem Int Ed Engl 51 10656-10659 (2012)
  19. Locking the dimeric GABA(B) G-protein-coupled receptor in its active state. Kniazeff J, Saintot PP, Goudet C, Liu J, Charnet A, Guillon G, Pin JP. J Neurosci 24 370-377 (2004)
  20. Molecular mechanism of ligand recognition by NR3 subtype glutamate receptors. Yao Y, Harrison CB, Freddolino PL, Schulten K, Mayer ML. EMBO J 27 2158-2170 (2008)
  21. Crystal structure of the kainate receptor GluR5 ligand-binding core in complex with (S)-glutamate. Naur P, Vestergaard B, Skov LK, Egebjerg J, Gajhede M, Kastrup JS. FEBS Lett 579 1154-1160 (2005)
  22. Allosteric mechanism in AMPA receptors: a FRET-based investigation of conformational changes. Ramanoudjame G, Du M, Mankiewicz KA, Jayaraman V. Proc Natl Acad Sci U S A 103 10473-10478 (2006)
  23. Effects of the lurcher mutation on GluR1 desensitization and activation kinetics. Klein RM, Howe JR. J Neurosci 24 4941-4951 (2004)
  24. The relationship between agonist potency and AMPA receptor kinetics. Zhang W, Robert A, Vogensen SB, Howe JR. Biophys J 91 1336-1346 (2006)
  25. AMPA receptor ligand binding domain mobility revealed by functional cross linking. Plested AJ, Mayer ML. J Neurosci 29 11912-11923 (2009)
  26. Reconstitution of invertebrate glutamate receptor function depends on stargazin-like proteins. Walker CS, Brockie PJ, Madsen DM, Francis MM, Zheng Y, Koduri S, Mellem JE, Strutz-Seebohm N, Maricq AV. Proc Natl Acad Sci U S A 103 10781-10786 (2006)
  27. Atomistic mechanism for the activation and desensitization of an AMPA-subtype glutamate receptor. Dong H, Zhou HX. Nat Commun 2 354 (2011)
  28. The transmembrane AMPA receptor regulatory protein gamma 4 is a more effective modulator of AMPA receptor function than stargazin (gamma 2). Körber C, Werner M, Kott S, Ma ZL, Hollmann M. J Neurosci 27 8442-8447 (2007)
  29. 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. Frydenvang K, Lash LL, Naur P, Postila PA, Pickering DS, Smith CM, Gajhede M, Sasaki M, Sakai R, Pentikaïnen OT, Swanson GT, Kastrup JS. J Biol Chem 284 14219-14229 (2009)
  30. Dynamics of the S1S2 glutamate binding domain of GluR2 measured using 19F NMR spectroscopy. Ahmed AH, Loh AP, Jane DE, Oswald RE. J Biol Chem 282 12773-12784 (2007)
  31. Role of conformational dynamics in α-amino-3-hydroxy-5-methylisoxazole-4-propionic acid (AMPA) receptor partial agonism. Ramaswamy S, Cooper D, Poddar N, MacLean DM, Rambhadran A, Taylor JN, Uhm H, Landes CF, Jayaraman V. J Biol Chem 287 43557-43564 (2012)
  32. Domain organization and function in GluK2 subtype kainate receptors. Das U, Kumar J, Mayer ML, Plested AJ. Proc Natl Acad Sci U S A 107 8463-8468 (2010)
  33. Stargazin promotes closure of the AMPA receptor ligand-binding domain. MacLean DM, Ramaswamy SS, Du M, Howe JR, Jayaraman V. J Gen Physiol 144 503-512 (2014)
  34. Evolution of glutamate interactions during binding to a glutamate receptor. Cheng Q, Du M, Ramanoudjame G, Jayaraman V. Nat Chem Biol 1 329-332 (2005)
  35. Pharmacological characterization of the allosteric modulator desformylflustrabromine and its interaction with alpha4beta2 neuronal nicotinic acetylcholine receptor orthosteric ligands. Weltzin MM, Schulte MK. J Pharmacol Exp Ther 334 917-926 (2010)
  36. SOL-1 is an auxiliary subunit that modulates the gating of GLR-1 glutamate receptors in Caenorhabditis elegans. Zheng Y, Brockie PJ, Mellem JE, Madsen DM, Walker CS, Francis MM, Maricq AV. Proc Natl Acad Sci U S A 103 1100-1105 (2006)
  37. Tyr702 is an important determinant of agonist binding and domain closure of the ligand-binding core of GluR2. Frandsen A, Pickering DS, Vestergaard B, Kasper C, Nielsen BB, Greenwood JR, Campiani G, Fattorusso C, Gajhede M, Schousboe A, Kastrup JS. Mol Pharmacol 67 703-713 (2005)
  38. Mechanism of partial agonism at the GluR2 AMPA receptor: Measurements of lobe orientation in solution. Maltsev AS, Ahmed AH, Fenwick MK, Jane DE, Oswald RE. Biochemistry 47 10600-10610 (2008)
  39. Conserved SOL-1 proteins regulate ionotropic glutamate receptor desensitization. Walker CS, Francis MM, Brockie PJ, Madsen DM, Zheng Y, Maricq AV. Proc Natl Acad Sci U S A 103 10787-10792 (2006)
  40. Mechanism of AMPA receptor activation by partial agonists: disulfide trapping of closed lobe conformations. Ahmed AH, Wang S, Chuang HH, Oswald RE. J Biol Chem 286 35257-35266 (2011)
  41. How fast does the GluR1Qflip channel open? Li G, Niu L. J Biol Chem 279 3990-3997 (2004)
  42. NMR spectroscopy of the ligand-binding core of ionotropic glutamate receptor 2 bound to 5-substituted willardiine partial agonists. Fenwick MK, Oswald RE. J Mol Biol 378 673-685 (2008)
  43. Mechanisms of antagonism of the GluR2 AMPA receptor: structure and dynamics of the complex of two willardiine antagonists with the glutamate binding domain. Ahmed AH, Thompson MD, Fenwick MK, Romero B, Loh AP, Jane DE, Sondermann H, Oswald RE. Biochemistry 48 3894-3903 (2009)
  44. Concanavalin-A reports agonist-induced conformational changes in the intact GluR6 kainate receptor. Fay AM, Bowie D. J Physiol 572 201-213 (2006)
  45. Interface interactions modulating desensitization of the kainate-selective ionotropic glutamate receptor subunit GluR6. Zhang Y, Nayeem N, Nanao MH, Green T. J Neurosci 26 10033-10042 (2006)
  46. LRET investigations of conformational changes in the ligand binding domain of a functional AMPA receptor. Gonzalez J, Rambhadran A, Du M, Jayaraman V. Biochemistry 47 10027-10032 (2008)
  47. On the mechanisms of alpha-amino-3-hydroxy-5-methylisoxazole-4-propionic acid (AMPA) receptor binding to glutamate and kainate. Fenwick MK, Oswald RE. J Biol Chem 285 12334-12343 (2010)
  48. Structural determinants of agonist-specific kinetics at the ionotropic glutamate receptor 2. Holm MM, Lunn ML, Traynelis SF, Kastrup JS, Egebjerg J. Proc Natl Acad Sci U S A 102 12053-12058 (2005)
  49. Constitutive activation of the N-methyl-D-aspartate receptor via cleft-spanning disulfide bonds. Blanke ML, VanDongen AM. J Biol Chem 283 21519-21529 (2008)
  50. A binding site tyrosine shapes desensitization kinetics and agonist potency at GluR2. A mutagenic, kinetic, and crystallographic study. Holm MM, Naur P, Vestergaard B, Geballe MT, Gajhede M, Kastrup JS, Traynelis SF, Egebjerg J. J Biol Chem 280 35469-35476 (2005)
  51. Ligand discrimination and gating in cyclic nucleotide-gated ion channels from apo and partial agonist-bound cryo-EM structures. Rheinberger J, Gao X, Schmidpeter PA, Nimigean CM. Elife 7 (2018)
  52. Chemistry and conformation of the ligand-binding domain of GluR2 subtype of glutamate receptors. Cheng Q, Jayaraman V. J Biol Chem 279 26346-26350 (2004)
  53. Correlating AMPA receptor activation and cleft closure across subunits: crystal structures of the GluR4 ligand-binding domain in complex with full and partial agonists. Gill A, Birdsey-Benson A, Jones BL, Henderson LP, Madden DR. Biochemistry 47 13831-13841 (2008)
  54. Solution X-ray scattering evidence for agonist- and antagonist-induced modulation of cleft closure in a glutamate receptor ligand-binding domain. Madden DR, Armstrong N, Svergun D, Pérez J, Vachette P. J Biol Chem 280 23637-23642 (2005)
  55. Rigid body essential X-ray crystallography: distinguishing the bend and twist of glutamate receptor ligand binding domains. Bjerrum EJ, Biggin PC. Proteins 72 434-446 (2008)
  56. Role of the chemical interactions of the agonist in controlling alpha-amino-3-hydroxy-5-methyl-4-isoxazolepropionic acid receptor activation. Mankiewicz KA, Rambhadran A, Du M, Ramanoudjame G, Jayaraman V. Biochemistry 46 1343-1349 (2007)
  57. Selective agonist binding of (S)-2-amino-3-(3-hydroxy-5-methyl-4-isoxazolyl)propionic acid (AMPA) and 2S-(2alpha,3beta,4beta)-2-carboxy-4-(1-methylethenyl)-3-pyrrolidineacetic acid (kainate) receptors: a molecular modeling study. Pentikäinen OT, Settimo L, Keinänen K, Johnson MS. Biochem Pharmacol 66 2413-2425 (2003)
  58. Autoantibodies against an extracellular peptide of the GluR3 subtype of AMPA receptors activate both homomeric and heteromeric AMPA receptor channels. Cohen-Kashi Malina K, Ganor Y, Levite M, Teichberg VI. Neurochem Res 31 1181-1190 (2006)
  59. Effects of buffer composition and dilution on nanowire field-effect biosensors. Lloret N, Frederiksen RS, Møller TC, Rieben NI, Upadhyay S, De Vico L, Jensen JH, Nygård J, Martinez KL. Nanotechnology 24 035501 (2013)
  60. Binding site flexibility: molecular simulation of partial and full agonists within a glutamate receptor. Arinaminpathy Y, Sansom MS, Biggin PC. Mol Pharmacol 69 11-18 (2006)
  61. Chemical interplay in the mechanism of partial agonist activation in alpha-amino-3-hydroxy-5-methyl-4-isoxazolepropionic acid receptors. Mankiewicz KA, Rambhadran A, Wathen L, Jayaraman V. Biochemistry 47 398-404 (2008)
  62. Amino-pyrrolidine tricarboxylic acids give new insight into group III metabotropic glutamate receptor activation mechanism. Frauli M, Hubert N, Schann S, Triballeau N, Bertrand HO, Acher F, Neuville P, Pin JP, Prézeau L. Mol Pharmacol 71 704-712 (2007)
  63. Comparison of taurine- and glycine-induced conformational changes in the M2-M3 domain of the glycine receptor. Han NL, Clements JD, Lynch JW. J Biol Chem 279 19559-19565 (2004)
  64. Exploring kainate receptor pharmacology using molecular dynamics simulations. Postila PA, Swanson GT, Pentikäinen OT. Neuropharmacology 58 515-527 (2010)
  65. Exploring the GluR2 ligand-binding core in complex with the bicyclical AMPA analogue (S)-4-AHCP. Nielsen BB, Pickering DS, Greenwood JR, Brehm L, Gajhede M, Schousboe A, Kastrup JS. FEBS J 272 1639-1648 (2005)
  66. Identification of a neurosteroid binding site contained within the GluR2-S1S2 domain. Spivak V, Lin A, Beebe P, Stoll L, Gentile L. Lipids 39 811-819 (2004)
  67. Subtype selectivity and flexibility of ionotropic glutamate receptors upon antagonist ligand binding. Pentikäinen U, Settimo L, Johnson MS, Pentikäinen OT. Org Biomol Chem 4 1058-1070 (2006)
  68. Not all desensitizations are created equal: physiological evidence that AMPA receptor desensitization differs for kainate and glutamate. Levchenko-Lambert Y, Turetsky DM, Patneau DK. J Neurosci 31 9359-9367 (2011)
  69. Mutations to the kainate receptor subunit GluR6 binding pocket that selectively affect domoate binding. Zhang Y, Nayeem N, Green T. Mol Pharmacol 74 1163-1169 (2008)
  70. Computational study of synthetic agonist ligands of ionotropic glutamate receptors. Wolter T, Steinbrecher T, Elstner M. PLoS One 8 e58774 (2013)
  71. Quantifying water-mediated protein-ligand interactions in a glutamate receptor: a DFT study. Sahai MA, Biggin PC. J Phys Chem B 115 7085-7096 (2011)
  72. Pharmacological and structural characterization of conformationally restricted (S)-glutamate analogues at ionotropic glutamate receptors. Juknaitė L, Venskutonytė R, Assaf Z, Faure S, Gefflaut T, Aitken DJ, Nielsen B, Gajhede M, Kastrup JS, Bunch L, Frydenvang K, Pickering DS. J Struct Biol 180 39-46 (2012)
  73. Water soluble RNA based antagonist of AMPA receptors. Du M, Ulrich H, Zhao X, Aronowski J, Jayaraman V. Neuropharmacology 53 242-251 (2007)
  74. A quantum biochemistry investigation of willardiine partial agonism in AMPA receptors. Lima Neto JX, Fulco UL, Albuquerque EL, Corso G, Bezerra EM, Caetano EW, da Costa RF, Freire VN. Phys Chem Chem Phys 17 13092-13103 (2015)
  75. Measurement of multiple torsional angles from one-dimensional solid-state NMR spectra: application to the conformational analysis of a ligand in its biological receptor site. Edwards R, Madine J, Fielding L, Middleton DA. Phys Chem Chem Phys 12 13999-14008 (2010)
  76. Computational Investigation into the Interactions of Traditional Chinese Medicine Molecules of WenQingYin with GluR2. Tseng YH, Chuang PH, Huang YR, Chen CL. Int J Mol Sci 18 (2017)
  77. Low-mode docking search in iGluR homology models implicates three residues in the control of ligand selectivity. Rodriguez J, Carcache L, Rein KS. J Mol Recognit 18 183-189 (2005)
  78. Population Shift Mechanism for Partial Agonism of AMPA Receptor. Oshima H, Re S, Sakakura M, Takahashi H, Sugita Y. Biophys J 116 57-68 (2019)
  79. Structure of the Arabidopsis Glutamate Receptor-like Channel GLR3.2 Ligand-Binding Domain. Gangwar SP, Green MN, Michard E, Simon AA, Feijó JA, Sobolevsky AI. Structure 29 161-169.e4 (2021)
  80. Subunit-selective iGluR antagonists can potentiate heteromeric receptor responses by blocking desensitization. Pollok S, Reiner A. Proc Natl Acad Sci U S A 117 25851-25858 (2020)
  81. The IGF-derived tripeptide Gly-Pro-Glu is a weak NMDA receptor agonist. Vaaga CE, Tovar KR, Westbrook GL. J Neurophysiol 112 1241-1245 (2014)
  82. Disruption of agonist and ligand activity in an AMPA glutamate receptor splice-variable domain deletion mutant. Johnson WD, Parandaman V, Onaivi ES, Taylor RE, Akinshola BE. Brain Res 1222 18-30 (2008)
  83. Comment New light on an open-and-shut case. Madden DR. Nat Chem Biol 1 317-319 (2005)
  84. The Route to 'Chemobrain' - Computational probing of neuronal LTP pathway. Fahim A, Rehman Z, Bhatti MF, Virk N, Ali A, Rashid A, Paracha RZ. Sci Rep 9 9630 (2019)
  85. Vibrational spectroscopic investigation of the ligand binding domain of kainate receptors. Du M, Rambhadran A, Jayaraman V. Protein Sci 18 1585-1591 (2009)


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