Structure and function of the NMDA receptor

Structural And Functional Organization Of The Synapse

Volumn , Issue , 2008, Pages 289-316

  Yuan, Hongjie ^a   Geballe, Matthew T ^b   Hansen, Kasper B ^a   Traynelis, Stephen F ^a  

^a EMORY UNIVERSITY SCHOOL OF MEDICINE   (United States)

^b EMORY UNIVERSITY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

EID: 84880315250     PISSN: None     EISSN: None     Source Type: Book    
DOI: 10.1007/978-0-387-77232-5_11     Document Type: Chapter

References (159)

1. Aizenman E, Lipton SA and Loring RH. Selective modulation of NMDA responses by reduction and oxidation. Neuron 2: 1257-1263, 1989
2. Allison DW, Gelfand VI, Spector I and Craig AM. Role of actin in anchoring postsynaptic receptors in cultured hippocampal neurons: differential attachment of NMDA versus AMPA receptors. J Neurosci 18: 2423-2436, 1998
3. Anson LC, Chen PE, Wyllie DJ, Colquhoun D and Schoepfer R. Identification of amino acid residues of the NR2A subunit that control glutamate potency in recombinant NR1/NR2A NMDA receptors. J Neurosci 18: 581-589, 1998
4. Auerbach A and Zhou Y. Gating reaction mechanisms for NMDA receptor channels. J Neurosci 25: 7914-7923, 2005
5. Balestrino M and Somjen GG. Concentration of carbon dioxide, interstitial pH and synaptic transmission in hippocampal formation of the rat. J Physiol 396: 247-266, 1988
6. Banke TG, Dravid SM and Traynelis SF. Protons trap NR1/NR2B NMDA receptors in a nonconducting state. J Neurosci 25: 42-51, 2005
7. Banke TG and Traynelis SF. Activation of NR1/NR2B NMDA receptors. Nat Neurosci 6: 144-152, 2003
8. Beck C, Wollmuth LP, Seeburg PH, Sakmann B and Kuner T. NMDAR channel segments forming the extracellular vestibule inferred from the accessibility of substituted cysteines. Neuron 22: 559-570, 1999
9. Béhé P, Colquhoun D and Wyllie DJ. Activation of single AMPA- and NMDA-type glutamate-receptor channels. In: Ionotropic glutamate receptors in the CNS, edited by Jonas P and Monyer H. Springer, New York, 1999, pp. 175-218
10. Benveniste M, Clements J, Vyklicky L, Jr. and Mayer ML. A kinetic analysis of the modulation of N-methyl-D-aspartic acid receptors by glycine in mouse cultured hippocampal neurones. J Physiol 428: 333-357, 1990
11. Benveniste M and Mayer ML. Kinetic analysis of antagonist action at N-methyl-Daspartic acid receptors. Two binding sites each for glutamate and glycine. Biophys J 59: 560-573, 1991
12. Borza I and Domany G. NR2B selective NMDA antagonists: the evolution of the ifenprodil- type pharmacophore. Curr Top Med Chem 6: 687-695, 2006
13. Brickley SG, Misra C, Mok MH, Mishina M and Cull-Candy SG. NR2B and NR2D subunits coassemble in cerebellar Golgi cells to form a distinct NMDA receptor subtype restricted to extrasynaptic sites. J Neurosci 23: 4958-4966, 2003
14. Brimecombe JC, Gallagher MJ, Lynch DR and Aizenman E. An NR2B point mutation affecting haloperidol and CP101,606 sensitivity of single recombinant N-methyl-Daspartate receptors. J Pharmacol Exp Ther 286: 627-634, 1998
15. Burnashev N, Schoepfer R, Monyer H, Ruppersberg JP, Gunther W, Seeburg PH and Sakmann B. Control by asparagine residues of calcium permeability and magnesium blockade in the NMDA receptor. Science 257: 1415-1419, 1992
16. Chatterton JE, Awobuluyi M, Premkumar LS, Takahashi H, Talantova M, Shin Y, Cui J, Tu S, Sevarino KA, Nakanishi N, Tong G, Lipton SA and Zhang D. Excitatory glycine receptors containing the NR3 family of NMDA receptor subunits. Nature 415: 793-798, 2002
17. Chazot PL. The NMDA receptor NR2B subunit: a valid therapeutic target for multiple CNS pathologies. Curr Med Chem 11: 389-396, 2004
18. Cheffings CM and Colquhoun D. Single channel analysis of a novel NMDA channel from Xenopus oocytes expressing recombinant NR1a, NR2A and NR2D subunits. J Physiol 526 Pt 3: 481-491, 2000
19. Chen N, Li B, Murphy TH and Raymond LA. Site within N-Methyl-D-aspartate receptor pore modulates channel gating. Mol Pharmacol 65: 157-164, 2004
20. Chen N, Moshaver A and Raymond LA. Differential sensitivity of recombinant Nmethyl- D-aspartate receptor subtypes to zinc inhibition. Mol Pharmacol 51: 1015-1023, 1997
21. Chen PE, Geballe MT, Stansfeld PJ, Johnston AR, Yuan H, Jacob AL, Snyder JP, Traynelis SF and Wyllie DJ. Structural features of the glutamate binding site in recombinant NR1/NR2A N-methyl-D-aspartate receptors determined by site-directed mutagenesis and molecular modeling. Mol Pharmacol 67: 1470-1484, 2005
22. Chen PE and Wyllie DJ. Pharmacological insights obtained from structure-function studies of ionotropic glutamate receptors. Br J Pharmacol 147: 839853, 2006.
23. Chenard BL and Menniti FS. Antagonists selective for NMDA receptors containing the NR2B subunit. Curr Pharm Des 5: 381-404, 1999.
24. Chesler M. Regulation and modulation of pH in the brain. Physiol Rev 83: 1183-1221, 2003.
25. Chesler M and Kaila K. Modulation of pH by neuronal activity. Trends Neurosci 15: 396-402, 1992.
26. Choi YB and Lipton SA. Identification and mechanism of action of two histidine residues underlying high-affinity Zn2+ inhibition of the NMDA receptor. Neuron 23: 171- 180, 1999.
27. Ciabarra AM, Sullivan JM, Gahn LG, Pecht G, Heinemann S and Sevarino KA. Cloning and characterization of chi-1: a developmentally regulated member of a novel class of the ionotropic glutamate receptor family. J Neurosci 15: 6498-6508, 1995.
28. Clark GD, Clifford DB and Zorumski CF. The effect of agonist concentration, membrane voltage and calcium on N-methyl-D-aspartate receptor desensitization. Neuroscience 39: 787-797, 1990.
29. Clarke RJ and Johnson JW. NMDA receptor NR2 subunit dependence of the slow component of magnesium unblock. J Neurosci 26: 5825-5834, 2006.
30. Das S, Sasaki YF, Rothe T, Premkumar LS, Takasu M, Crandall JE, Dikkes P, Conner DA, Rayudu PV, Cheung W, Chen HS, Lipton SA and Nakanishi N. Increased NMDA current and spine density in mice lacking the NMDA receptor subunit NR3A. Nature 393: 377-381, 1998.
31. Dingledine R, Borges K, Bowie D and Traynelis SF. The glutamate receptor ion channels. Pharmacol Rev 51: 7-61, 1999.
32. Dingledine R and McBain CJ. Glutamate and Aspartate. In: Basic Neurochemistry: Molecular, Cellular and Medical Aspects, edited by Siegel GJ, Agranoff BW, Albers RW, Fisher SK and Uhler MD. 1999, p. 315-334.
33. Doyle DA, Morais CJ, Pfuetzner RA, Kuo A, Gulbis JM, Cohen SL, Chait BT and MacKinnon R. The structure of the potassium channel: molecular basis of K+ conduction and selectivity. Science 280: 69-77, 1998.
34. Dravid SM and Traynelis SF. Activation of NR1/NR2C NMDA receptors. The 35th Annual Meeting Society for Neuroscience, 2005.
35. Durand GM, Bennett MV and Zukin RS. Splice variants of the N-methyl-D-aspartate receptor NR1 identify domains involved in regulation by polyamines and protein kinase C. Proc Natl Acad Sci U S A 90: 6731-6735, 1993
36. Durand GM, Gregor P, Zheng X, Bennett MV, Uhl GR and Zukin RS. 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 U S A 89: 9359-9363, 1992
37. Ehlers MD, Fung ET, O'Brien RJ and Huganir RL. Splice variant-specific interaction of the NMDA receptor subunit NR1 with neuronal intermediate filaments. J Neurosci 18: 720-730, 1998
38. Ehlers MD, Zhang S, Bernhadt JP and Huganir RL. Inactivation of NMDA receptors by direct interaction of calmodulin with the NR1 subunit. Cell 84: 745-755, 1996
39. Erreger K, Chen PE, Wyllie DJ and Traynelis SF. Glutamate receptor gating. Crit Rev Neurobiol 16: 187-224, 2004
40. Erreger K, Dravid SM, Banke TG, Wyllie DJ and Traynelis SF. Subunit-specific gating controls rat NR1/NR2A and NR1/NR2B NMDA channel kinetics and synaptic signaling profiles. J Physiol 563: 345-358, 2005
41. Erreger K, Geballe MT, Dravid SM, Snyder JP, Wyllie DJ and Traynelis SF. Mechanism of partial agonism at NMDA receptors for a conformationally restricted glutamate analog. J Neurosci 25: 7858-7866, 2005
42. Erreger K, Geballe MT, Kristensen AS, Chen PE, Hansen KB, Lee CJ, Yuan H, Le P, Lyuboslavsky P, Micale N, Jørgensen L, Clausen RP, Wyllie DJ, Snyder JP and Traynelis SF. Subunit-specific agonist activity for glutamate analogs at NR2A, NR2B
43. Erreger K and Traynelis SF. Allosteric interaction between zinc and glutamate binding domains on NR2A causes desensitization of NMDA receptors. J Physiol 569: 381-393, 2005
44. Farrant M, Feldmeyer D, Takahashi T and Cull-Candy SG. NMDA-receptor channel diversity in the developing cerebellum. Nature 368: 335-339, 1994
45. Fayyazuddin A, Villarroel A, Le GA, Lerma J and Neyton J. Four residues of the extracellular N-terminal domain of the NR2A subunit control high-affinity Zn2+ binding to NMDA receptors. Neuron 25: 683-694, 2000
46. Furukawa H and Gouaux E. Mechanisms of activation, inhibition and specificity: crystal structures of the NMDA receptor NR1 ligand-binding core. EMBO J 22: 2873-2885, 2003
47. Furukawa H, Singh SK, Mancusso R and Gouaux E. Subunit arrangement and function in NMDA receptors. Nature 438: 185-192, 2005
48. Gallagher MJ, Huang H, Pritchett DB and Lynch DR. Interactions between ifenprodil and the NR2B subunit of the N-methyl-D-aspartate receptor. J Biol Chem 271: 9603-9611, 1996
49. Giffard RG, Monyer H, Christine CW and Choi DW. Acidosis reduces NMDA receptor activation, glutamate neurotoxicity, and oxygen-glucose deprivation neuronal injury in cortical cultures. Brain Res 506: 339-342, 1990
50. Hansen KB, Yuan H and Traynelis SF. Structural aspects of AMPA receptor activation, desensitization, and deactivation. Curr Opin Neurobiol 17: 281-288, 2007
51. Hatton CJ and Paoletti P. Modulation of triheteromeric NMDA receptors by N-terminal domain ligands. Neuron 46: 261-274, 2005
52. Hollmann M, Boulter J, Maron C, Beasley L, Sullivan J, Pecht G and Heinemann S. Zinc potentiates agonist-induced currents at certain splice variants of the NMDA receptor. Neuron 10: 943-954, 1993
53. Hu B and Zheng F. Molecular determinants of glycine-independent desensitization of NR1/NR2A receptors. J Pharmacol Exp Ther 313: 563-569, 2005
54. Huggins DJ and Grant GH. The function of the amino terminal domain in NMDA receptor modulation. J Mol Graph Model 23: 381-388, 2005
55. Hume RI, Dingledine R and Heinemann SF. Identification of a site in glutamate receptor subunits that controls calcium permeability. Science 253: 1028-1031, 1991
56. Inanobe A, Furukawa H and Gouaux E. Mechanism of Partial Agonist Action at the NR1 Subunit of NMDA Receptors. Neuron 47: 71-84, 2005
57. Jiang Y, Lee A, Chen J, Cadene M, Chait BT and MacKinnon R. Crystal structure and mechanism of a calcium-gated potassium channel. Nature 417: 515-522, 2002
58. Jin R, Banke TG, Mayer ML, Traynelis SF and Gouaux E. Structural basis for partial agonist action at ionotropic glutamate receptors. Nat Neurosci 6: 803-810, 2003
59. Jin R, Clark S, Weeks AM, Dudman JT, Gouaux E and Partin KM. Mechanism of positive allosteric modulators acting on AMPA receptors. J Neurosci 25: 9027-9036, 2005
60. Johnson JW and Ascher P. Glycine potentiates the NMDA response in cultured mouse brain neurons. Nature 325: 529-531, 1987
61. Johnson TD. Modulation of channel function by polyamines. Trends Pharmacol Sci 17: 22-27, 1996
62. Jones KS, VanDongen HM and VanDongen AM. The NMDA receptor M3 segment is a conserved transduction element coupling ligand binding to channel opening. J Neurosci 22: 2044-2053, 2002
63. Jones S and Gibb AJ. Functional NR2B- and NR2D-containing NMDA receptor channels in rat substantia nigra dopaminergic neurones. J Physiol 569: 209-221, 2005
64. Kashiwagi K, Fukuchi J, Chao J, Igarashi K and Williams K. An aspartate residue in the extracellular loop of the N-methyl-D-aspartate receptor controls sensitivity to spermine and protons. Mol Pharmacol 49: 1131-1141, 1996
65. Kashiwagi K, Pahk AJ, Masuko T, Igarashi K and Williams K. Block and modulation of N-methyl-D-aspartate receptors by polyamines and protons: role of amino acid residues in the transmembrane and pore-forming regions of NR1 and NR2 subunits. Mol Pharmacol 52: 701-713, 1997
66. Kawajiri S and Dingledine R. Multiple structural determinants of voltage-dependent magnesium block in recombinant NMDA receptors. Neuropharmacology 32: 1203-1211, 1993
67. Kew JN and Kemp JA. Ionotropic and metabotropic glutamate receptor structure and pharmacology. Psychopharmacology (Berl) 179: 4-29, 2005
68. Kew JN, Trube G and Kemp JA. A novel mechanism of activity-dependent NMDA receptor antagonism describes the effect of ifenprodil in rat cultured cortical neurones. J Physiol 497 (Pt 3): 761-772, 1996
69. Kew JN, Trube G and Kemp JA. State-dependent NMDA receptor antagonism by Ro 8- 4304, a novel NR2B selective, non-competitive, voltage-independent antagonist. Br J Pharmacol 123: 463-472, 1998
70. Kleckner NW and Dingledine R. Requirement for glycine in activation of NMDAreceptors expressed in Xenopus oocytes. Science 241: 835-837, 1988
71. Kristensen AS, Geballe MT, Snyder JP and Traynelis SF. Glutamate receptors: variation in structure-function coupling. Trends Pharmacol Sci 27: 65-69, 2006
72. Krupp JJ, Vissel B, Heinemann SF and Westbrook GL. Calcium-dependent inactivation of recombinant N-methyl-D-aspartate receptors is NR2 subunit specific. Mol Pharmacol 50: 1680-1688, 1996
73. Krupp JJ, Vissel B, Thomas CG, Heinemann SF and Westbrook GL. Interactions of calmodulin and alpha-actinin with the NR1 subunit modulate Ca2+-dependent inactivation of NMDA receptors. J Neurosci 19: 1165-1178, 1999
74. Kuner T and Schoepfer R. Multiple structural elements determine subunit specificity of Mg2+ block in NMDA receptor channels. J Neurosci 16: 3549-3558, 1996
75. Kuner T, Seeburg PH and Guy HR. A common architecture for K+ channels and ionotropic glutamate receptors? Trends Neurosci 26: 27-32, 2003
76. Kuner T, Wollmuth LP, Karlin A, Seeburg PH and Sakmann B. Structure of the NMDA receptor channel M2 segment inferred from the accessibility of substituted cysteines. Neuron 17: 343-352, 1996
77. Kuryatov A, Laube B, Betz H and Kuhse J. Mutational analysis of the glycine-binding site of the NMDA receptor: structural similarity with bacterial amino acid-binding proteins. Neuron 12: 1291-1300, 1994
78. Laube B, Schemm R and Betz H. Molecular determinants of ligand discrimination in the glutamate-binding pocket of the NMDA receptor. Neuropharmacology 47: 994-1007, 2004
79. Layton ME, Kelly MJ, III and Rodzinak KJ. Recent advances in the development of NR2B subtype-selective NMDA receptor antagonists. Curr Top Med Chem 6: 697-709, 2006
80. Legendre P, Rosenmund C and Westbrook GL. Inactivation of NMDA channels in cultured hippocampal neurons by intracellular calcium. J Neurosci 13: 674-684, 1993
81. Lerma J, Zukin RS and Bennett MV. Glycine decreases desensitization of N-methyl-Daspartate (NMDA) receptors expressed in Xenopus oocytes and is required for NMDA responses. Proc Natl Acad Sci U S A 87: 2354-2358, 1990
82. Lester RA and Jahr CE. NMDA channel behavior depends on agonist affinity. J Neurosci 12: 635-643, 1992
83. Lester RA, Tong G and Jahr CE. Interactions between the glycine and glutamate binding sites of the NMDA receptor. J Neurosci 13: 1088-1096, 1993
84. Lipton SA. The molecular basis of memantine action in Alzheimer's disease and other neurologic disorders: low-affinity, uncompetitive antagonism. Curr Alzheimer Res 2: 155-165, 2005
85. Low CM, Lyuboslavsky P, French A, Le P, Wyatte K, Thiel WH, Marchan EM, Igarashi K, Kashiwagi K, Gernert K, Williams K, Traynelis SF and Zheng F. Molecular determinants of proton-sensitive N-methyl-D-aspartate receptor gating. Mol Pharmacol 63: 1212-1222, 2003
86. Low CM, Zheng F, Lyuboslavsky P and Traynelis SF. 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, 2000
87. Madry C, Mesic I, Bartholomaus I, Nicke A, Betz H and Laube B. Principal role of NR3 subunits in NR1/NR3 excitatory glycine receptor function. Biochem Biophys Res Commun 354: 102-108, 2007
88. Malherbe P, Mutel V, Broger C, Perin-Dureau F, Kemp JA, Neyton J, Paoletti P and Kew JN. Identification of critical residues in the amino terminal domain of the human NR2B subunit involved in the RO 25-6981 binding pocket. J Pharmacol Exp Ther 307: 897-905, 2003
89. Masuko T, Kuno T, Kashiwagi K, Kusama T, Williams K and Igarashi K. Stimulatory and inhibitory properties of aminoglycoside antibiotics at N-methyl-D-aspartate receptors. J Pharmacol Exp Ther 290: 1026-1033, 1999
90. Matsuda K, Kamiya Y, Matsuda S and Yuzaki M. Cloning and characterization of a novel NMDA receptor subunit NR3B: a dominant subunit that reduces calcium permeability. Brain Res Mol Brain Res 100: 43-52, 2002
91. Mayer ML and Armstrong N. Structure and function of glutamate receptor ion channels. Annu Rev Physiol 66: 161-181, 2004
92. Mayer ML, Olson R and Gouaux E. Mechanisms for ligand binding to GluR0 ion channels: crystal structures of the glutamate and serine complexes and a closed apo state. J Mol Biol 311: 815-836, 2001
93. Mayer ML, Vyklicky L, Jr. and Clements J. Regulation of NMDA receptor desensitization in mouse hippocampal neurons by glycine. Nature 338: 425-427, 1989
94. McFeeters RL and Oswald RE. Emerging structural explanations of ionotropic glutamate receptor function. FASEB J 18: 428-438, 2004
95. Medina I, Filippova N, Charton G, Rougeole S, Ben-Ari Y, Khrestchatisky M and Bregestovski P. Calcium-dependent inactivation of heteromeric NMDA receptorchannels expressed in human embryonic kidney cells. J Physiol 482 (Pt 3): 567-573, 1995
96. Mitchell NA and Fleck MW. Targeting of AMPA receptor gating processes by allosteric modulators and mutations. Biophys J 92: 2392-2402, 2007
97. Monyer H, Burnashev N, Laurie DJ, Sakmann B and Seeburg PH. Developmental and regional expression in the rat brain and functional properties of four NMDA receptors. Neuron 12: 529-540, 1994
98. Monyer H, Sprengel R, Schoepfer R, Herb A, Higuchi M, Lomeli H, Burnashev N, Sakmann B and Seeburg PH. Heteromeric NMDA receptors: molecular and functional distinction of subtypes. Science 256: 1217-1221, 1992
99. Mott DD, Doherty JJ, Zhang S, Washburn MS, Fendley MJ, Lyuboslavsky P, Traynelis SF and Dingledine R. Phenylethanolamines inhibit NMDA receptors by enhancing proton inhibition. Nat Neurosci 1: 659-667, 1998
100. Nahum-Levy R, Lipinski D, Shavit S and Benveniste M. Desensitization of NMDA receptor channels is modulated by glutamate agonists. Biophys J 80: 2152-2166, 2001
101. Nedergaard M, Kraig RP, Tanabe J and Pulsinelli WA. Dynamics of interstitial and intracellular pH in evolving brain infarct. Am J Physiol 260: R581-R588, 1991
102. Nishi M, Hinds H, Lu HP, Kawata M and Hayashi Y. Motoneuron-specific expression of NR3B, a novel NMDA-type glutamate receptor subunit that works in a dominantnegative manner. J Neurosci 21: RC185, 2001
103. Pahk AJ and Williams K. Influence of extracellular pH on inhibition by ifenprodil at Nmethyl- D-aspartate receptors in Xenopus oocytes. Neurosci Lett 225: 29-32, 1997
104. Paoletti P, Ascher P and Neyton J. High-affinity zinc inhibition of NMDA NR1-NR2A receptors. J Neurosci 17: 5711-5725, 1997
105. Paoletti P and Neyton J. NMDA receptor subunits: function and pharmacology. Curr Opin Pharmacol 7: 39-47, 2007
106. Paoletti P, Perin-Dureau F, Fayyazuddin A, Le GA, Callebaut I and Neyton J. Molecular organization of a zinc binding n-terminal modulatory domain in a NMDA receptor subunit. Neuron 28: 911-925, 2000
107. Partin KM, Fleck MW and Mayer ML. AMPA receptor flip/flop mutants affecting deactivation, desensitization, and modulation by cyclothiazide, aniracetam, and thiocyanate. J Neurosci 16: 6634-6647, 1996
108. Perez-Otano I, Schulteis CT, Contractor A, Lipton SA, Trimmer JS, Sucher NJ and Heinemann SF. Assembly with the NR1 subunit is required for surface expression of NR3A-containing NMDA receptors. J Neurosci 21: 1228-1237, 2001
109. Perin-Dureau F, Rachline J, Neyton J and Paoletti P. Mapping the binding site of the neuroprotectant ifenprodil on NMDA receptors. J Neurosci 22: 5955-5965, 2002
110. Peters S, Koh J and Choi DW. Zinc selectively blocks the action of N-methyl-Daspartate on cortical neurons. Science 236: 589-593, 1987
111. Pina-Crespo JC and Gibb AJ. Subtypes of NMDA receptors in new-born rat hippocampal granule cells. J Physiol 541: 41-64, 2002
112. Popescu G and Auerbach A. Modal gating of NMDA receptors and the shape of their synaptic response. Nat Neurosci 6: 476-483, 2003
113. Popescu G and Auerbach A. The NMDA receptor gating machine: lessons from single channels. Neuroscientist 10: 192-198, 2004
114. Popescu G, Robert A, Howe JR and Auerbach A. Reaction mechanism determines NMDA receptor response to repetitive stimulation. Nature 430: 790-793, 2004
115. Rachline J, Perin-Dureau F, Le GA, Neyton J and Paoletti P. The micromolar zincbinding domain on the NMDA receptor subunit NR2B. J Neurosci 25: 308-317, 2005
116. Rosenmund C, Feltz A and Westbrook GL. Calcium-dependent inactivation of synaptic NMDA receptors in hippocampal neurons. J Neurophysiol 73: 427-430, 1995
117. Rosenmund C, Stern-Bach Y and Stevens CF. The tetrameric structure of a glutamate receptor channel. Science 280: 1596-1599, 1998
118. Rosenmund C and Westbrook GL. Calcium-induced actin depolymerization reduces NMDA channel activity. Neuron 10: 805-814, 1993
119. Rumbaugh G, Prybylowski K, Wang JF and Vicini S. Exon 5 and spermine regulate deactivation of NMDA receptor subtypes. J Neurophysiol 83: 1300-1306, 2000
120. Sasaki YF, Rothe T, Premkumar LS, Das S, Cui J, Talantova MV, Wong HK, Gong X, Chan SF, Zhang D, Nakanishi N, Sucher NJ and Lipton SA. Characterization and comparison of the NR3A subunit of the NMDA receptor in recombinant systems and primary cortical neurons. J Neurophysiol 87: 2052-2063, 2002
121. Sather W, Dieudonne S, MacDonald JF and Ascher P. Activation and desensitization of N-methyl-D-aspartate receptors in nucleated outside-out patches from mouse neurones. J Physiol 450: 643-672, 1992
122. Sather W, Johnson JW, Henderson G and Ascher P. Glycine-insensitive desensitization of NMDA responses in cultured mouse embryonic neurons. Neuron 4: 725-731, 1990
123. Schorge S, Elenes S and Colquhoun D. Maximum likelihood fitting of single channel NMDA activity with a mechanism composed of independent dimers of subunits. J Physiol 569: 395-418, 2005
124. Schulte U, Hahn H, Konrad M, Jeck N, Derst C, Wild K, Weidemann S, Ruppersberg JP, Fakler B and Ludwig J. pH gating of ROMK (K(ir)1.1) channels: control by an Arg-Lys- Arg triad disrupted in antenatal Bartter syndrome. Proc Natl Acad Sci U S A 96: 15298- 15303, 1999
125. Sessoms-Sikes S, Honse Y, Lovinger DM and Colbran RJ. CaMKIIalpha enhances the desensitization of NR2B-containing NMDA receptors by an autophosphorylationdependent mechanism. Mol Cell Neurosci 29: 139-147, 2005
126. Sharma G and Stevens CF. A mutation that alters magnesium block of N-methyl-Daspartate receptor channels. Proc Natl Acad Sci U S A 93: 9259-9263, 1996
127. Siesjo BK. Acid-base homeostasis in the brain: physiology, chemistry, and neurochemical pathology. Prog Brain Res 63: 121-154, 1985
128. Smith TC and Howe JR. Concentration-dependent substate behavior of native AMPA receptors. Nat Neurosci 3: 992-997, 2000
129. Sobolevsky AI, Prodromou ML, Yelshansky MV and Wollmuth LP. Subunit-specific contribution of pore-forming domains to NMDA receptor channel structure and gating. J Gen Physiol 129: 509-525, 2007
130. Sobolevsky AI, Rooney L and Wollmuth LP. Staggering of subunits in NMDAR channels. Biophys J 83: 3304-3314, 2002
131. Stern P, Behe P, Schoepfer R and Colquhoun D. Single-channel conductances of NMDA receptors expressed from cloned cDNAs: comparison with native receptors. Proc Biol Sci 250: 271-277, 1992
132. Sucher NJ, Akbarian S, Chi CL, Leclerc CL, Awobuluyi M, Deitcher DL, Wu MK, Yuan JP, Jones EG and Lipton SA. Developmental and regional expression pattern of a novel NMDA receptor-like subunit (NMDAR-L) in the rodent brain. J Neurosci 15: 6509-6520, 1995
133. Sullivan JM, Traynelis SF, Chen HS, Escobar W, Heinemann SF and Lipton SA. Identification of two cysteine residues that are required for redox modulation of the NMDA subtype of glutamate receptor. Neuron 13: 929-936, 1994
134. Tang CM, Dichter M and Morad M. Modulation of the N-methyl-D-aspartate channel by extracellular H+. Proc Natl Acad Sci U S A 87: 6445-6449, 1990
135. Tang LH and Aizenman E. The modulation of N-methyl-D-aspartate receptors by redox and alkylating reagents in rat cortical neurones in vitro. J Physiol 465: 303-323, 1993
136. Traynelis SF. pH modulation of ligand-gated channels. In: pH and brain function, edited by Kaila K and Ransom. BR. NY: Wiley Liss, 1998
137. Traynelis SF, Burgess MF, Zheng F, Lyuboslavsky P and Powers JL. Control of voltageindependent zinc inhibition of NMDA receptors by the NR1 subunit. J Neurosci 18: 6163-6175, 1998
138. Traynelis SF and Cull-Candy SG. Pharmacological properties and H+ sensitivity of excitatory amino acid receptor channels in rat cerebellar granule neurones. J Physiol 433: 727-763, 1991
139. Traynelis SF and Cull-Candy SG. Proton inhibition of N-methyl-D-aspartate receptors in cerebellar neurons. Nature 345: 347-350, 1990
140. Traynelis SF, Hartley M and Heinemann SF. Control of proton sensitivity of the NMDA receptor by RNA splicing and polyamines. Science 268: 873-876, 1995
141. Vicini S, Wang JF, Li JH, Zhu WJ, Wang YH, Luo JH, Wolfe BB and Grayson DR. Functional and pharmacological differences between recombinant N-methyl-D-aspartate receptors. J Neurophysiol 79: 555-566, 1998
142. Villarroel A, Burnashev N and Sakmann B. Dimensions of the narrow portion of a recombinant NMDA receptor channel. Biophys J 68: 866-875, 1995
143. Vyklicky L, Jr. Calcium-mediated modulation of N-methyl-D-aspartate (NMDA) responses in cultured rat hippocampal neurones. J Physiol 470: 575-600, 1993
144. Vyklicky L, Jr., Vlachova V and Krusek J. The effect of external pH changes on responses to excitatory amino acids in mouse hippocampal neurones. J Physiol 430: 497- 517, 1990
145. Wafford KA, Kathoria M, Bain CJ, Marshall G, Le BB, Kemp JA and Whiting PJ. 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, 1995
146. Westbrook GL and Mayer ML. Micromolar concentrations of Zn2+ antagonize NMDA and GABA responses of hippocampal neurons. Nature 328: 640-643, 1987
147. Williams K. Separating dual effects of zinc at recombinant N-methyl-D-aspartate receptors. Neurosci Lett 215: 9-12, 1996
148. Williams K. Interactions of polyamines with ion channels. Biochem J 325 (Pt 2): 289-297, 1997
149. Williams K. Ifenprodil discriminates subtypes of the N-methyl-D-aspartate receptor: selectivity and mechanisms at recombinant heteromeric receptors. Mol Pharmacol 44: 851-859, 1993
150. Williams K, Chao J, Kashiwagi K, Masuko T and Igarashi K. Activation of N-methyl-Daspartate receptors by glycine: role of an aspartate residue in the M3-M4 loop of the NR1 subunit. Mol Pharmacol 50: 701-708, 1996
151. Williams K, Kashiwagi K, Fukuchi J and Igarashi K. An acidic amino acid in the Nmethyl- D-aspartate receptor that is important for spermine stimulation. Mol Pharmacol 48: 1087-1098, 1995
152. Wollmuth LP, Kuner T and Sakmann B. Adjacent asparagines in the NR2-subunit of the NMDA receptor channel control the voltage-dependent block by extracellular Mg2+. J Physiol 506 (Pt 1): 13-32, 1998
153. Wollmuth LP, Kuner T, Seeburg PH and Sakmann B. Differential contribution of the NR1- and NR2A-subunits to the selectivity filter of recombinant NMDA receptor channels. J Physiol 491 (Pt 3): 779-797, 1996
154. Wong E, Ng FM, Yu CY, Lim P, Lim LH, Traynelis SF and Low CM. Expression and characterization of soluble amino-terminal domain of NR2B subunit of N-methyl-Daspartate receptor. Protein Sci 14: 2275-2283, 2005
155. Wyllie DJ, Behe P and Colquhoun D. Single-channel activations and concentration jumps: comparison of recombinant NR1a/NR2A and NR1a/NR2D NMDA receptors. J Physiol 510 (Pt 1): 1-18, 1998
156. Wyszynski M, Lin J, Rao A, Nigh E, Beggs AH, Craig AM and Sheng M. Competitive binding of alpha-actinin and calmodulin to the NMDA receptor. Nature 385: 439-442, 1997
157. Yao Y and Mayer ML. Characterization of a soluble ligand binding domain of the NMDA receptor regulatory subunit NR3A. J Neurosci 26: 4559-4566, 2006
158. Zhang S, Ehlers MD, Bernhardt JP, Su CT and Huganir RL. Calmodulin mediates calcium- dependent inactivation of N-methyl-D-aspartate receptors. Neuron 21: 443-453, 1998
159. Zheng F, Erreger K, Low CM, Banke T, Lee CJ, Conn PJ and Traynelis SF. Allosteric interaction between the amino terminal domain and the ligand binding domain of NR2A. Nat Neurosci 4: 894-901, 2001