Stable expression and characterization of recombinant human heteromeric N-methyl-D-aspartate receptor subtypes NMDAR1A/2A and NMDAR1A/2B in mammalian cells

Journal of Pharmacology and Experimental Therapeutics

Volumn 279, Issue 1, 1996, Pages 367-378

  Varney, M A ^a   Jachec, C ^a   Deal, C ^a   Hess, S D ^a   Daggett, L P ^a   Skvoretz, R ^a   Urcan, M ^a   Morrison, J H ^b   Moran, T ^b   Johnson, E C ^a   Velicelebi G ^a  

^a MERCK RESEARCH LABORATORIES   (United States)

^b MOUNT SINAI SCHOOL OF MEDICINE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

4 PHOSPHONOMETHYLPIPECOLIC ACID; DIZOCILPINE; GLUTAMIC ACID; IFENPRODIL; N METHYL DEXTRO ASPARTIC ACID; N METHYL DEXTRO ASPARTIC ACID RECEPTOR; RECEPTOR SUBTYPE;

ARTICLE; CALCIUM CELL LEVEL; CELL LINE; DRUG POTENTIATION; DRUG SELECTIVITY; ELECTROPHYSIOLOGY; MEMBRANE POTENTIAL; PRIORITY JOURNAL;

ANIMALS; ANTIBODIES, MONOCLONAL; CALCIUM; CELL LINE; HUMANS; RATS; RECEPTORS, N-METHYL-D-ASPARTATE; RECOMBINANT PROTEINS; TRANSFECTION;

EID: 12644295056     PISSN: 00223565     EISSN: None     Source Type: Journal    
DOI: None     Document Type: Article

References (66)

1. ADAMS, S.-L., FOLDES, R. L. AND KAMBOJ, R. K: Human N-methyl-D-aspartate receptor modulatory subunit hNR3: Cloning and sequencing of the cDNA and primary structure of the protein. Biochim. Biophys. Acta 1260: 105-108, 1995.
2. ANEGAWA, N. J., LYNCH, D. R., VERDOON, T. A. AND PRITCHETT, D. B.: Transfection of N-methyl-D-aspartate receptors in a non-neuronal cell line leads to cell death. J. Neurochem. 64: 2004-2012, 1995.
3. ASCHER, P., BREGESTOVSKI, P. AND NOWAK, L.: N-Methyl-D-aspartate-activated channels of mouse central neurones in magnesium-free solutions. J. Physiol. (Lond.) 399: 207-226, 1988.
4. AUSUBEL, F. M., BRENT, R., KINGSTON, R. E., MOORE, D. D., SEIDMAN, J. G., SMITH, J. A. AND STRUHL, K.: Calcium phosphate transfections. In Current Protocols in Molecular Biology, ed. by F. M. Ausubel, R. Brent, R. E. Kingston, D. D. Moore, J. G. Seidman, J. A. Smith and K. Struhl, pp. 9.1.1-9.1.4., Wiley-Greene Publishing, New York, 1990.
5. BOECKMAN, F. A. AND AIZENMAN, E.: Stable transfection of the NR1 subunit in Chinese hamster ovary cells fails to produce a functional N-methyl-D-aspartate receptor. Neurosci. Lett. 173: 189-192, 1994.
6. BULLER, A. L., LARSON, H. C., SCHNEIDER, B. E., BEATON, J. A., MORRISETT, R. A. AND MONAGHAN, D. T.: The molecular basis of NMDA receptor subtypes: Native receptor diversity is predicted by subunit composition. J. Neurosci. 14: 5471-5484, 1994.
7. BURNASHEV, N., SCHOEPFER, R., MONYER, H., RUPPERSBERG, J. P., GUNTHER, W., SEEBURG, P. H. AND SAKMANN, B.: Control by asparagine residues of calcium permeability and magnesium blockade in the NMDA receptor. Science (Wash. DC) 257: 1415-1419, 1992.
8. BURNASHEV, N., ZHOU, Z., NEHER, E. AND SAKMANN, B.: Fractional calcium currents through recombinant GluR channels of the NMDA, AMPA and kainate receptor subtypes. J. Physiol. (Lond.) 485: 403-418, 1995.
9. CHAZOT, P. L., CIK, M. AND STEPHENSON, F. A.: Immunological detection of the NMDAR1 glutamate receptor subunit expressed in human embryonic kidney 293 cells and in rat brain. J. Neurochem. 59: 1176-1178, 1992.
10. CHAZOT, P. L., COLEMAN, S. K., CIK, M. AND STEPHENSON, F. A.: Molecular characterization of N-methyl-D-aspartate receptors expressed in mammalian cells yields evidence for the coexistence of three subunit types within a discrete receptor molecule. J. Biol. Chem. 269: 24403-24409, 1994.
11. CHOI, D. W.: Glutamate neurotoxicity and diseases of the nervous system. Neuron 1: 623-634, 1988.
12. CIK, M., CHAZOT, P. L. AND STEPHENSON, F. A.: Optimal expression of cloned NMDAR1/NMDAR2A heteromeric glutamate receptors: A biochemical characterization. Biochem. J. 296: 877-883, 1993.
13. COLLINGRIDGE, G. L. AND SINGER, W.: Excitatory amino acid receptors and synaptic plasticity. Trends Pharmacol. Sci. 11: 290-296, 1990.
14. DAGGETT, L. P., SACAAN, A. I., AKONG, M., RAO, S. P., HESS, S. D., LIAW, C., URRUTIA, A., JACHEC, C., ELLIS, S. B., DREESSEN, J., KNOPFEL, T., LANDWEHRMEYER, G. B., TESTA, C. M., YOUNG, A. B., VARNEY, M., JOHNSON, E. C. AND VELIÇELEBI, G.: Molecular and functional characterization of recombinant human metabotropic glutamate receptor subtype 5. Neuropharmacology 34: 871-886, 1995.
15. DESAI, M. A., BURNETT, J. P., MAYNE, N. G. AND SCHOEPP, D. D.: Cloning and expression of a human metabotropic glutamate receptor 1a: Enhanced coupling on co-transfection with a glutamate transporter. Mol. Pharmacol. 48: 648-657, 1995.
16. DINGLEDINE, R., MCBAIN, C. J. AND MCNAMARA, J. O.: Excitatory amino acid receptors in epilepsy. Trends Pharmacol. Sci. 11: 334-338, 1990.
17. FOLDES, R. L., ADAMS, S. L., FANTASKE, R. P. AND KAMBOJ, R. K.: Human N-methyl-D-aspartate receptor modulatory subunit hNR2A: Cloning and sequencing of the cDNA and primary structure of the protein. Biochim. Biophys. Acta 1223: 155-159, 1994a.
18. FOLDES, R. L., RAMPERSAD, V. AND KAMBOJ, R. K.: Cloning and sequence analysis of additional splice variants encoding human N-methyl-D-aspartate receptor (hNR1) subunits. Gene 147: 303-304, 1994b.
19. GIBB, A. J. AND COLQUHOUN, D.: Activation of N-methyl-D-aspartate receptors by 1-glutamate in cells dissociated from adult rat hippocampus. J. Physiol. (Lond.) 456: 143-179, 1992.
20. GRIMWOOD, S., LE BOURDELLÈS, B. AND WHITING, P. J.: Recombinant human NMDA homomeric NR1 receptors expressed in mammalian cells form a high-affinity glycine antagonist binding site. J. Neurochem. 64: 525-530, 1995.
21. 2+ indicators with greatly improved fluorescence properties. J. Biol. Chem. 260: 3440-3450, 1985.
22. HESS, S. D., DAGGETT, L. P., CRONA, J., DEAL, C., LU, C.-C., URRUTIA, A., CHAVEZ-NORIEGA, L., ELLIS, S. B., JOHNSON, E. C. AND VELIÇELEBI, G.: Cloning and functional characterization of human heteromeric N-methyl-D-aspartate receptors. J. Pharmacol. Exp. Ther. 278: 808-816, 1996.
23. IKEDA, K., NAGASAWA, M., MORI, H., ARAKI, K., SAKIMURA, K., WATANABE, M., INOUE, Y. AND MISHINA, M.: Cloning and expression of the epsilon 4 subunit of the NMDA receptor channel. FEBS Lett. 313: 34-38, 1992.
24. ISHII, T., MORIYOSHI, K., SUGIHARA, H., SAKURADA, K., KADOTANI, H., YOKOI, M., AKAZAWA, C., SHIGEMOTO, R., MIZUNO, N., MASU, M. AND NAKANISHI, S.: Molecular characterization of the family of the N-methyl-D-aspartate receptor subunits. J. Biol. Chem. 268: 2836-2843, 1993.
25. KAO, J. P. Y., HAROOTUNIAN, A. T. AND TSIEN, R. Y.: Photochemically generated cytosolic calcium pulses and their detection by fluo-3. J. Biol. Chem. 264: 8179-8184, 1989.
26. KARP, S. J., MASU, M., EKI, T., OZAWA, K. AND NAKANISHI, S.: Molecular cloning and chromosomal localization of the key subunit of the human N-methyl-D-aspartate receptor. J. Biol. Chem. 268: 3728-3733, 1993.
27. KOH, J. Y. AND CHOI, D. W.: Quantitative determination of glutamate-mediated cortical neuronal injury in cell culture by lactate dehydrogenase efflux assay. J. Neurosci. Methods 20: 83-90, 1987.
28. 2+-permeable AMPA and NMDA receptor channels in basket cells of rat hippocampal dentate gyrus. J. Physiol. (Lond.) 485: 383-402, 1995.
29. KUTSUWADA, T., KASHIWABUCHI, N., MORI, H., SAKIMURA, K., KUSHIYA, E., ARAKI, K., MEGURO, H., MASAKI, H., KUMANISHI, T., ARAKAWA, M. AND MISHINA, M.: Molecular diversity of the NMDA receptor channel. Nature (Lond.) 358: 36-41, 1992.
30. LAURIE, D. J. AND SEEBURG, P. H.: Ligand affinities at recombinant N-methyl-d-aspartate receptors depend on subunit composition. Eur. J. Pharmacol. 268: 335-345, 1994.
31. LE BOURDELLÈS, B., WAFFORD, K. A., KEMP, J. A., MARSHALL, G., BAIN, C., WILCOX, A. S., SIKELA, J. M. AND WHITING, P. J.: Cloning, functional coexpression, and pharmacological characterization of human cDNAs encoding NMDA receptor NR1 and NR2A subunits. J. Neurochem. 62: 2091-2098, 1994.
32. LEGENDRE, P., ROSENMUND, C. AND WESTBROOK, G. L.: Inactivation of NMDA channels in cultured hippocampal neurons by intracellular calcium. J. Neurosci. 13: 674-684, 1993.
33. LEGENDRE, P. AND WESTBROOK, G.L.: Ifenprodil blocks N-methyl-d-aspartate receptors by a two-component mechanism. Mol. Pharmacol. 40: 289-298, 1991.
34. LOWRY, O. H., ROSEBROUGH, N. J., FARR, A. L. AND RANDALL, R. J.: Protein measurement with the Folin phenol reagent. J. Biol. Chem. 193: 265-275, 1951.
35. MAYER, M. L. AND WESTBROOK, G. L.: The physiology of excitatory amino acids in the vertebrate central nervous system. Prog. Neurobiol. 28: 197-276, 1987.
36. 2+ of NMDA responses in spinal cord neurones. Nature (Lond.) 309: 261-263, 1984.
37. MAYER, M. L., WESTBROOK, G. L. AND VYKLICKY, L., JR.: Sites of antagonist action on N-methyl-D-aspartic acid receptors studied using fluctuation analysis and a rapid perfusion technique. J. Neurophysiol. 60: 645-663, 1988.
38. 2+ in hippocampal neurones. J. Neurophysiol. 72: 456-465, 1994.
39. MEDINA, I., FILIPPOVA, N., CHARTON, G., ROUGEOLE, S., BEN-ARI, Y., KHRESTCHATISKY, M. AND BRECESTOVSKI, P.: Calcium-dependent inactivation of heteromeric NMDA receptor-channels expressed in human embryonic kidney cells. J. Physiol. (Lond.) 482: 567-573, 1995.
40. MEGURO, H., MORI, H., ARAKI, K., KUSHIYA, E., KUTSUWADA, T., YAMAZAKI, M., KUMANISHI, T., ARAKAWA, M., SAKIMURA, K. AND MISHINA, M.: Functional characterization of a heteromeric NMDA receptor channel expressed from cloned cDNAs. Nature (Lond.) 357: 70-74, 1992.
41. 3H]MK-801 binding to subpopulations of NMDA receptors. Neurosci. Lett. 122: 21-24, 1991.
42. MONAGHAN, D. T., OLVERMAN, H. J., HGUYEN, L., WATKINS, J. C. AND COTMAN, C. W.: Two classes of N-methyl-D-aspartate recognition sites: Differential distribution and differential regulation by glycine. Proc. Natl. Acad. Sci. U.S.A. 85: 9836-9840, 1988.
43. MONYER, H., BURNASHEV, N., LAURIE, D. J., SAKMANN, B. AND SEEBURG, P. H.: Developmental and regional expression in the rat brain and functional properties of four NMDA receptors. Neuron 12: 529-540, 1994.
44. MONYER, H., SPRENGEL, R., SCHOEPFER, R., HERB, A., HIGUCHI, M., LOMELI, H., BURNASHEV, N., SAKMANN, B. AND SEEBURG, P. H.: Heteromeric NMDA receptors: Molecular and functional distinction of subtypes. Science (Wash. DC) 256: 1217-1221, 1992.
45. MORIYOSHI, K., MASU, M., ISHII, T., SHIGEMOTO, R., MIZUNO, N. AND NAKANISHI, S.: Molecular cloning and characterization of the rat NMDA receptor. Nature (Lond.) 354: 31-37, 1991.
46. NAKANISHI, S.: Molecular diversity of glutamate receptors and implications for brain function. Science (Wash. DC) 258: 597-603, 1992.
47. NAKANISHI, N., AXEL, R. AND SHNEIDER, N. A.: Alternative splicing generates functionally distinct N-methyl-D-aspartate receptors. Proc. Natl. Acad. Sci. U.S.A. 89: 8552-8556, 1992.
48. NICOLL, R. A., KAUER, J. A. AND MALENKA, R. C.: The current excitement in long-term potentiation. Neuron 1: 97-103, 1988.
49. NOWAK, L., BREGESTOVSKI, P., ASCHER, P., HERBET, A. AND PROCHIANTZ, A.: Magnesium gates glutamate-activated channels in mouse central neurones. Nature (Lond.) 307: 462-465, 1984.
50. PARSONS, C. G., GRUNER, R., ROZENTAL, J., MILLAR, J. AND LODGE, D.: Patch clamp studies on the kinetics and selectivity of N-methyl-D-aspartate receptor antagonism by memantine (1-amino-3,5-dimethyladamantan). Neuropharmacology 32: 1337-1350, 1993.
51. PLANELLS-CASES, R., SUN, W., FERRER-MONTIEL, A. V. AND MONTAL, M.: Molecular cloning, functional expression, and pharmacological characterization of an N-methyl-D-aspartate receptor subunit from human brain. Proc. Natl. Acad. Sci. U.S.A. 90: 5057-5061, 1993.
52. PRIESTLEY, T. AND KEMP, J. A.: Agonist response kinetics of N-methyl-D-aspartate receptors in neurons cultured from rat cerebral cortex and cerebellum: Evidence for receptor heterogeneity. Mol. Pharmacol. 44: 1252-1257, 1994.
53. PRIESTLEY, T., LAUGHTON, P., MYERS, J., LE BOURDELLÈS, B., KERRY, J. AND WHITING, P.: Pharmacological properties of recombinant human N-methyl-D-aspartate receptors comprising NR1a/NR2A and NR1a/NR2B subunit assemblies expressed in permanently transfected mouse fibroblast cells. Mol. Pharmacol. 48: 841-848, 1995.
54. SCHNEGGENBERGER, R., ZHOU, Z., KONNERTH, A. AND NEHER, E.: Fractional contribution of calcium to the cation current through glutamate receptor channels. Neuron 11: 133-143, 1993.
55. SHENG, M., CUMMINGS, J., ROLDAN, L. A., JAN, Y. N. AND JAN, L. Y.: Changing subunit composition of heteromeric NMDA receptors during development of rat cortex. Nature (Lond.) 368: 144-147, 1994.
56. SIEGEL, S. J., BROSE, N., JANSSEN, W. G., GASIC, G. P., JAHN, R., HEINEMANN, S. F. AND MORRISON, J. H.: Regional, cellular, and ultrastructural distribution of the N-methyl-D-aspartate receptor subunit 1 in monkey hippocampus. Proc. Natl. Acad. Sci. U.S.A. 91: 564-568, 1994
57. STERN, P., BÉHÉ, P., SCHOEPFER, R. AND COLQUHOUN, D.: Single-channel conductances of NMDA receptors expressed from cloned cDNAs: Comparison with native receptors. Proc. R. Soc. Lond. 250: 271-277, 1992.
58. STERN, P., CIK, M., COLQUHOUN, D. AND STEPHENSON, F. A.: Single channel properties of cloned NMDA receptors in a human cell line: Comparison with results from Xenopus oocytes. J. Physiol. (Lond.) 476: 391-397, 1994.
59. SUGIHARA, H., MORIYOSHI, K., ISHII, T., MASU, M. AND NAKANISHI, S.: Structures and properties of seven isoforms of the NMDA receptor generated by alternative splicing. Biochem. Biophys. Res. Commun. 185: 826-832, 1992.
60. SULLIVAN, J. M., TRAYNELIS, S. F., CHEN, H. S., ESCOBAR, W., HEINEMANN, S. F. AND LIPTON, S. A.: Identification of two cysteine residues that are required for redox modulation of the NMDA subtype of glutamate receptor. Neuron 13: 929-936, 1994.
61. SZATKOWSKI, M. AND ATTWELL, D.: Triggering and execution of neuronal death in brain ischaemia: Two phases of glutamate release by different mechanisms. Trends Neurosci. 17: 359-365, 1994.
62. WAFFORD, K. A., BAIN, C. J., LE BOURDELLÈS, B., WHITING, P. J. AND KEMP, J. A.: Preferential co-assembly of recombinant NMDA receptors composed of three different subunits. NeuroReport 4: 1347-1349, 1993.
63. WHITING, P., SCHOEPFER, R., LINDSTROM, J. AND PRIESTLEY, T.: Structural and pharmacological characterization of the major brain nicotinic acetylcholine receptor subtype stably expressed in mouse fibroblasts. Mol. Pharmacol. 40: 463-472, 1991.
64. 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.
65. WILLIAMS, K., RUSSELL, S. L., SHEN, Y. M. AND MOLINOFF, P. B.: Developmental switch in the expression of NMDA receptors occurs in vivo and in vitro. Neuron 10: 267-278, 1993.
66. YAMAZAKI, M., MORI, H., ARAKI, K., MORI, K. J. AND MISHINA, M.: Cloning, expression and modulation of a mouse NMDA receptor subunit. FEBS Lett. 300: 39-45, 1992.