New insights into the not-so-new NR3 subunits of N-methyl-D-aspartate receptor: Localization, structure, and function

Molecular Pharmacology

Volumn 78, Issue 1, 2010, Pages 1-11

  Low, Chian Ming ^a,b   Wee, Karen Siaw Ling ^a  

^a NATIONAL UNIVERSITY OF SINGAPORE   (Singapore)

^b NATIONAL UNIVERSITY OF SINGAPORE   (Singapore)

Author keywords

[No Author keywords available]

Indexed keywords

N METHYL DEXTRO ASPARTIC ACID RECEPTOR; PROTEIN NR 1; PROTEIN NR 2; PROTEIN NR 3; UNCLASSIFIED DRUG;

BRAIN FUNCTION; BRAIN REGION; CELL TYPE; HUMAN; LIGAND BINDING; MOTONEURON; NONHUMAN; NUCLEOTIDE SEQUENCE; OOCYTE; PRIORITY JOURNAL; PROTEIN EXPRESSION; SHORT SURVEY; SYNAPTIC MEMBRANE; TRANSGENIC MOUSE;

ANIMALS; ANIMALS, GENETICALLY MODIFIED; PROTEIN CONFORMATION; RECEPTORS, N-METHYL-D-ASPARTATE;

EID: 77953741703     PISSN: 0026895X     EISSN: 15210111     Source Type: Journal    
DOI: 10.1124/mol.110.064006     Document Type: Short Survey

References (101)

1. Al-Hallaq RA, Jarabek BR, Fu Z, Vicini S, Wolfe BB, and Yasuda RP (2002) Association of NR3A with the N-methyl-D-aspartate receptor NR1 and NR2 subunits. Mol Pharmacol 62:1119-1127.
2. Allgaier C, Durmaz M, Müller D, Franke H, Poelchen W, Wirkner K, and Illes P (2001) Single-cell RT-PCR analysis of N-methyl-D-aspartate receptor subunit expression in rat locus coeruleus neurones. Naunyn Schmiedebergs Arch Pharmacol 363:120-123.
3. Andersson O, Stenqvist A, Attersand A, and von Euler G (2001) Nucleotide sequence, genomic organization, and chromosomal localization of genes encoding the human NMDA receptor subunits NR3A and NR3B. Genomics 78:178-184.
4. Armstrong N and 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.
5. Armstrong N, Mayer M, and Gouaux E (2003) Tuning activation of the AMPA-sensitive GluR2 ion channel by genetic adjustment of agonist-induced conformational changes. Proc Natl Acad Sci USA 100:5736-5741.
6. Armstrong N, Sun Y, Chen GQ, and Gouaux E (1998) Structure of a glutamate-receptor ligand-binding core in complex with kainate. Nature 395:913-917.
7. Awobuluyi M, Yang J, Ye Y, Chatterton JE, Godzik A, Lipton SA, and Zhang D (2007) Subunit-specific roles of glycine-binding domains in activation of NR1/NR3 N-methyl-D-aspartate receptors. Mol Pharmacol 71:112-122.
8. Barth AL and Malenka RC (2001) NMDAR EPSC kinetics do not regulate the critical period for LTP at thalamocortical synapses. Nat Neurosci 4:235-236.
9. Bendel O, Meijer B, Hurd Y, and von Euler G (2005) Cloning and expression of the human NMDA receptor subunit NR3B in the adult human hippocampus. Neurosci Lett 377:31-36.
10. Bendová Z, Sumová A, and Mikkelsen JD (2009) Circadian and developmental regulation of N-methyl-D-aspartate-receptor 1 mRNA splice variants and Nmethyl-D-aspartate-receptor 3 subunit expression within the rat suprachiasmatic nucleus. Neuroscience 159:599-609.
11. Blanpied TA, Scott DB, and Ehlers MD (2002) Dynamics and regulation of clathrin coats at specialized endocytic zones of dendrites and spines. Neuron 36:435-449.
12. Cavara NA and Hollmann M (2008) Shuffling the deck anew: how NR3 tweaks NMDA receptor function. Mol Neurobiol 38:16-26.
13. Chatterton JE, Awobuluyi M, Premkumar LS, Takahashi H, Talantova M, Shin Y, Cui J, Tu S, Sevarino KA, Nakanishi N, et al. (2002) Excitatory glycine receptors containing the NR3 family of NMDA receptor subunits. Nature 415:793-798. (Pubitemid 34150501)
14. Chen GQ and Gouaux E (1997) Overexpression of a glutamate receptor (GluR2) ligand binding domain in Escherichia coli: application of a novel protein folding screen. Proc Natl Acad Sci USA 94:13431-13436.
15. Ciabarra AM, Sullivan JM, Gahn LG, Pecht G, Heinemann S, and Sevarino KA (1995) 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. (Pubitemid 3001297)
16. Curtis DR, Hösli L, and Johnston GA (1967) Inhibition of spinal neurons by glycine. Nature 215:1502-1503.
17. Dalkara T, Erdemli G, Barun S, and Onur R (1992) Glycine is required for NMDA receptor activation: electrophysiological evidence from intact rat hippocampus. Brain Res 576:197-202.
18. Das S, Sasaki YF, Rothe T, Premkumar LS, Takasu M, Crandall JE, Dikkes P, Conner DA, Rayudu PV, Cheung W, et al. (1998) Increased NMDA current and spine density in mice lacking the NMDA receptor subunit NR3A. Nature 393:377-381.
19. Dingledine R, Borges K, Bowie D, and Traynelis SF (1999) The glutamate receptor ion channels. Pharmacol Rev 51:7-61.
20. Dunah AW, Yasuda RP, Wang YH, Luo J, Dávila-García M, Gbadegesin M, Vicini S, and Wolfe BB (1996) Regional and ontogenic expression of the NMDA receptor subunit NR2D protein in rat brain using a subunit-specific antibody. J Neurochem 67:2335-2345. (Pubitemid 26392503)
21. Eriksson M, Nilsson A, Froelich-Fabre S, Akesson E, Dunker J, Seiger A, Folkesson R, Benedikz E, and Sundström E (2002) Cloning and expression of the human N-methyl-D-aspartate receptor subunit NR3A. Neurosci Lett 321:177-181.
22. Farrant M, Feldmeyer D, Takahashi T, and Cull-Candy SG (1994) NMDA-receptor channel diversity in the developing cerebellum. Nature 368:335-339.
23. Forcina MS, Ciabarra AM, and Seravino KA (1995) Cloning of chi-2: a putative member of the ionotropic glutamate receptor superfamily. Soc Neurosci Abstr 21:438.3.
24. Fukaya M, Hayashi Y, and Watanabe M (2005) NR2 to NR3B subunit switchover of NMDA receptors in early postnatal motoneurons. Eur J Neurosci 21:1432-1436.
25. Furukawa H and Gouaux E (2003) Mechanisms of activation, inhibition and specificity: crystal structures of the NMDA receptor NR1 ligand-binding core. EMBO J 22:2873-2885.
26. Furukawa H, Singh SK, Mancusso R, and Gouaux E (2005) Subunit arrangement and function in NMDA receptors. Nature 438:185-192.
27. Com, NR2A, NR2B, NR2C, NR2D and NR3A. Brain Res Mol Brain Res 69:164-170.
28. Han X, Tomitori H, Mizuno S, Higashi K, Füll C, Fukiwake T, Terui Y, Leewanich P, Nishimura K, Toida T, et al. (2008) Binding of spermine and ifenprodil to a purified, soluble regulatory domain of the N-methyl-D-aspartate receptor. J Neurochem 107:1566-1577.
29. Hatten ME (1999) Central nervous system neuronal migration. Annu Rev Neurosci 22:511-539.
30. Hogner A, Kastrup JS, Jin R, Liljefors T, Mayer ML, Egebjerg J, Larsen IK, and Gouaux E (2002) Structural basis for AMPA receptor activation and ligand selectivity: crystal structures of five agonist complexes with the GluR2 ligand-binding core. J Mol Biol 322:93-109.
31. Hollmann M and Heinemann S (1994) Cloned glutamate receptors. Annu Rev Neurosci 17:31-108.
32. Inanobe A, Furukawa H, and Gouaux E (2005) Mechanism of partial agonist action at the NR1 subunit of NMDA receptors. Neuron 47:71-84.
33. Jin R, Banke TG, Mayer ML, Traynelis SF, and Gouaux E (2003) Structural basis for partial agonist action at ionotropic glutamate receptors. Nat Neurosci 6:803-810.
34. Jin R, Singh SK, Gu S, Furukawa H, Sobolevsky AI, Zhou J, Jin Y, and Gouaux E (2009) Crystal structure and association behaviour of the GluR2 amino-terminal domain. EMBO J 28:1812-1823.
35. Johnson JW and Ascher P (1987) Glycine potentiates the NMDA response in cultured mouse brain neurons. Nature 325:529-531.
36. Káradóttir R, Cavelier P, Bergersen LH, and Attwell D (2005) NMDA receptors are expressed in oligodendrocytes and activated in ischaemia. Nature 438:1162-1166.
37. Karakas E, Simorowski N, and Furukawa H (2009) Structure of the zinc-bound amino-terminal domain of the NMDA receptor NR2B subunit. EMBO J 28:3910-3920.
38. Kemp JA and Leeson PD (1993) The glycine site of the NMDA receptor-five years on. Trends Pharmacol Sci 14:20-25.
39. Kirson ED, Schirra C, Konnerth A, and Yaari Y (1999) Early postnatal switch in magnesium sensitivity of NMDA receptors in rat CA1 pyramidal cells. J Physiol 521:99-111.
40. Kleckner NW and Dingledine R (1988) Requirement for glycine in activation of NMDA-receptors expressed in Xenopus oocytes. Science 241:835-837.
41. Kumar J, Schuck P, Jin R, and Mayer ML (2009) The N-terminal domain of GluR6-subtype glutamate receptor ion channels. Nat Struct Mol Biol 16:631-638.
42. 2+ block of recombinant NMDA channels mutated within the selectivity filter and expressed in Xenopus oocytes. J Physiol 507:1-12.
43. Laurie DJ, Bartke I, Schoepfer R, Naujoks K, and Seeburg PH (1997) Regional, developmental and interspecies expression of the four NMDAR2 subunits, examined using monoclonal antibodies. Brain Res Mol Brain Res 51:23-32.
44. Liu XB, Murray KD, and Jones EG (2004) Switching of NMDA receptor 2A and 2B subunits at thalamic and cortical synapses during early postnatal development. J Neurosci 24:8885-8895.
45. Luo J, Bosy TZ, Wang Y, Yasuda RP, and Wolfe BB (1996) Ontogeny of NMDA R1 subunit protein expression in five regions of rat brain. Brain Res Dev Brain Res 92:10-17.
46. 2+ and NR1 antagonist. Proc Natl Acad Sci USA 105:12563-12568.
47. 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.
48. Matsuda K, Fletcher M, Kamiya Y, and Yuzaki M (2003) Specific assembly with the NMDA receptor 3B subunit controls surface expression and calcium permeability of NMDA receptors. J Neurosci 23:10064-10073. (Pubitemid 37392553)
49. Matsuda K, Kamiya Y, Matsuda S, and Yuzaki M (2002) 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.
50. Mayer ML and Armstrong N (2004) Structure and function of glutamate receptor ion channels. Annu Rev Physiol 66:161-181.
51. Mayer ML, Olson R, and Gouaux E (2001) 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.
52. 2+ of NMDA responses in spinal cord neurones. Nature 309:261-263.
53. Medina AE, Liao DS, Mower AF, and Ramoa AS (2001) Do NMDA receptor kinetics regulate the end of critical periods of plasticity? Neuron 32:553-555.
54. Monyer H, Burnashev N, Laurie DJ, Sakmann B, and Seeburg PH (1994) Developmental and regional expression in the rat brain and functional properties of four NMDA receptors. Neuron 12:529-540.
55. Monyer H, Sprengel R, Schoepfer R, Herb A, Higuchi M, Lomeli H, Burnashev N, Sakmann B, and Seeburg PH (1992) Heteromeric NMDA receptors: molecular and functional distinction of subtypes. Science 256:1217-1221.
56. Mori H and Mishina M (1995) Structure and function of the NMDA receptor channel. Neuropharmacology 34:1219-1237.
57. Moriyoshi K, Masu M, Ishii T, Shigemoto R, Mizuno N, and Nakanishi S (1991) Molecular cloning and characterization of the rat NMDA receptor. Nature 354:31-37. (Pubitemid 21896774)
58. Nakanishi N, Tu S, Shin Y, Cui J, Kurokawa T, Zhang D, Chen HS, Tong G, and Lipton SA (2009) Neuroprotection by the NR3A subunit of the NMDA receptor. J Neurosci 29:5260-5265.
59. Ng FM, Geballe MT, Snyder JP, Traynelis SF, and Low CM (2008) Structural insights into phenylethanolamines high-affinity binding site in NR2B from binding and molecular modeling studies. Mol Brain 1:16.
60. Ng FM, Soh W, Geballe MT, and Low CM (2007) Improving solubility of NR2B amino-terminal domain of N-methyl-D-aspartate receptor expressed in Escherichia coli. Biochem Biophys Res Commun 362:69-74.
61. Niemann S, Kanki H, Fukui Y, Takao K, Fukaya M, Hynynen MN, Churchill MJ, Shefner JM, Bronson RT, Brown RH Jr, et al. (2007) Genetic ablation of NMDA receptor subunit NR3B in mouse reveals motoneuronal and nonmotoneuronal phenotypes. Eur J Neurosci 26:1407-1420.
62. Niemann S, Landers JE, Churchill MJ, Hosler B, Sapp P, Speed WC, Lahn BT, Kidd KK, Brown RH Jr, and Hayashi Y (2008) Motoneuron-specific NR3B gene: no association with ALS and evidence for a common null allele. Neurology 70:666-676.
63. Nishi M, Hinds H, Lu HP, Kawata M, and Hayashi Y (2001) Motoneuron-specific expression of NR3B, a novel NMDA-type glutamate receptor subunit that works in a dominant-negative manner. J Neurosci 21:RC185.
64. Nowak L, Bregestovski P, Ascher P, Herbet A, and Prochiantz A (1984) Magnesium gates glutamate-activated channels in mouse central neurones. Nature 307:462-465. (Pubitemid 14132062)
65. Pérez-Otaño I, Luján R, Tavalin SJ, Plomann M, Modregger J, Liu XB, Jones EG, Heinemann SF, Lo DC, and Ehlers MD (2006) Endocytosis and synaptic removal of NR3A-containing NMDA receptors by PACSIN1/syndapin1. Nat Neurosci 9:611-621.
66. Perez-Otano I, Schulteis CT, Contractor A, Lipton SA, Trimmer JS, Sucher NJ, and Heinemann SF (2001) Assembly with the NR1 subunit is required for surface expression of NR3A-containing NMDA receptors. J Neurosci 21:1228-1237.
67. 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.
68. Petralia RS, Wang YX, and Wenthold RJ (1994b) The NMDA receptor subunits NR2A and NR2B show histological and ultrastructural localization patterns similar to those of NR1. J Neurosci 14:6102-6120.
69. Petralia RS, Yokotani N, and Wenthold RJ (1994a) Light and electron microscope distribution of the NMDA receptor subunit NMDAR1 in the rat nervous system using a selective anti-peptide antibody. J Neurosci 14:667-696. (Pubitemid 24043923)
70. Pina-Crespo JC, and Heinemann SF (2004) Physiological and pharmacological properties of recombinant NR3-containing receptors expressed in mammalian cells. Soc Neurosci Abstr 30:957.
71. Prithviraj R and Inglis FM (2008) Expression of the N-methyl-D-aspartate receptor subunit NR3B regulates dendrite morphogenesis in spinal motor neurons. Neuroscience 155:145-153.
72. Pujic Z, Matsumoto I, and Wilce PA (1993) Expression of the gene coding for the NR1 subunit of the NMDA receptor during rat brain development. Neurosci Lett 162: 67-70.
73. Rácz B, Blanpied TA, Ehlers MD, and Weinberg RJ (2004) Lateral organization of endocytic machinery in dendritic spines. Nat Neurosci 7:917-918.
74. Riva MA, Tascedda F, Molteni R, and Racagni G (1994) Regulation of NMDA receptor subunit mRNA expression in the rat brain during postnatal development. Brain Res Mol Brain Res 25:209-216.
75. Roberts AC, Díez-García J, Rodriguiz RM, López IP, Luján R, Martínez-Turrillas R, Picó E, Henson MA, Bernardo DR, Jarrett TM, et al. (2009) Downregulation of NR3A-containing NMDARs is required for synapse maturation and memory consolidation. Neuron 63:342-356.
76. Sasaki YF, Rothe T, Premkumar LS, Das S, Cui J, Talantova MV, Wong HK, Gong X, Chan SF, Zhang D, et al. (2002) Characterization and comparison of the NR3A subunit of the NMDA receptor in recombinant systems and primary cortical neurons. J Neurophysiol 87:2052-2063.
77. Schell MJ, Molliver ME, and Snyder SH (1995) D-Serine, an endogenous synaptic modulator: localization to astrocytes and glutamate-stimulated release. Proc Natl Acad Sci USA 92:3948-3952.
78. Schüler T, Mesic I, Madry C, Bartholomäus I, and Laube B (2008) Formation of NR1/NR2 and NR1/NR3 heterodimers constitutes the initial step in N-methyl-Daspartate receptor assembly. J Biol Chem 283:37-46.
79. χ-2, members of a novel class of the glutamate receptor superfamily. Soc Neurosci Abstr 22:59219.
80. Smothers CT and Woodward JJ (2007) Pharmacological characterization of glycineactivated currents in HEK 293 cells expressing N-methyl-D-aspartate NR1 and NR3 subunits. J Pharmacol Exp Ther 322:739-748.
81. Sobolevsky AI, Rosconi MP, and Gouaux E (2009) X-ray structure, symmetry and mechanism of an AMPA-subtype glutamate receptor. Nature 462:745-756.
82. Standaert DG, Friberg IK, Landwehrmeyer GB, Young AB, and Penney JB Jr (1999) Expression of NMDA glutamate receptor subunit mRNAs in neurochemically identified projection and interneurons in the striatum of the rat. Brain Res Mol Brain Res 64:11-23.
83. Standaert DG, Landwehrmeyer GB, Kerner JA, Penney JB Jr, and Young AB (1996) Expression of NMDAR2D glutamate receptor subunit mRNA in neurochemically identified interneurons in the rat neostriatum, neocortex and hippocampus. Brain Res Mol Brain Res 42:89-102.
84. Stone TW (1993) Subtypes of NMDA receptors. Gen Pharmacol 24:825-832.
85. Sucher NJ, Akbarian S, Chi CL, Leclerc CL, Awobuluyi M, Deitcher DL, Wu MK, Yuan JP, Jones EG, and Lipton SA (1995) Developmental and regional expression pattern of a novel NMDA receptor-like subunit (NMDAR-L) in the rodent brain. J Neurosci 15:6509-6520.
86. Sun L, Margolis FL, Shipley MT, and Lidow MS (1998) Identification of a long variant of mRNA encoding the NR3 subunit of the NMDA receptor: its regional distribution and developmental expression in the rat brain. FEBS Lett 441:392-396.
87. Talantova M, Piña-Crespo JC, States B, Chen VH-S, Tong G, Zhang D, Heinemann SF, and Lipton SA (2007) Unique functional properties of NR3-containing "NMDA" receptors expressed in mammalian cells. Soc Neurosci Abstr 33:875.27.
88. Tang W, Wesley M, Freeman WM, Liang B, and Hemby SE (2004) Alterations in ionotropic glutamate receptor subunits during binge cocaine self-administration and withdrawal in rats. J Neurochem 89:1021-1033.
89. Tong G, Takahashi H, Tu S, Shin Y, Talantova M, Zago W, Xia P, Nie Z, Goetz T, Zhang D, et al. (2008) Modulation of NMDA receptor properties and synaptic transmission by the NR3A subunit in mouse hippocampal and cerebrocortical neurons. J Neurophysiol 99:122-132.
90. Ulbrich MH and Isacoff EY (2008) Rules of engagement for NMDA receptor subunits. Proc Natl Acad Sci USA 105:14163-14168.
91. van Zundert B, Yoshii A, and Constantine-Paton M (2004) Receptor compartmentalization and trafficking at glutamate synapses: a developmental proposal. Trends Neurosci 27:428-437.
92. Wada A, Takahashi H, Lipton SA, and Chen HS (2006) NR3A modulates the outer vestibule of the "NMDA" receptor channel. J Neurosci 26:13156-13166.
93. Wee KS, Zhang Y, Khanna S, and Low CM (2008) Immunolocalization of NMDA receptor subunit NR3B in selected structures in the rat forebrain, cerebellum, and lumbar spinal cord. J Comp Neurol 509:118-135.
94. Williams K, Chao J, Kashiwagi K, Masuko T, and Igarashi K (1996) Activation of N-methyl-D-aspartate receptors by glycine: role of an aspartate residue in the M3-M4 loop of the NR1 subunit. Mol Pharmacol 50:701-708. (Pubitemid 26347688)
95. Williams K, Russell SL, Shen YM, and Molinoff PB (1993) Developmental switch in the expression of NMDA receptors occurs in vivo and in vitro. Neuron 10:267-278.
96. Wong E, Ng FM, Yu CY, Lim P, Lim LH, Traynelis SF, and 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.
97. Wong HK, Liu XB, Matos MF, Chan SF, Pérez-Otaño I, Boysen M, Cui J, Nakanishi N, Trimmer JS, Jones EG, et al. (2002) Temporal and regional expression of NMDA receptor subunit NR3A in the mammalian brain. J Comp Neurol 450:303-317.
98. Yamakura T, Askalany AR, Petrenko AB, Kohno T, Baba H, and Sakimura K (2005) The NR3B subunit does not alter the anesthetic sensitivities of recombinant N-methyl-D-aspartate receptors. Anesth Analg 100:1687-1692.
99. Yao Y, Harrison CB, Freddolino PL, Schulten K, and Mayer ML (2008) Molecular mechanism of ligand recognition by NR3 subtype glutamate receptors. EMBO J 27:2158-2170.
100. 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.
101. Zatorre RJ, Jones-Gotman M, Evans AC, and Meyer E (1992) Functional localization and lateralization of human olfactory cortex. Nature 360:339-340.