Glutamate receptor ion channel properties predict vulnerability to cytotoxicity in a transfected nonneuronal cell line

Molecular and Cellular Neurosciences

Volumn 7, Issue 2, 1996, Pages 102-115

  Raymond, Lynn A ^a   Moshaver, Ali ^a   Tingley, Whit G ^b   Shalaby, Ismail ^b   Huganir, Richard L ^b  

^a UNIVERSITY OF BRITISH COLUMBIA   (Canada)

^b DEPARTMENT OF PATHOLOGY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

AMPA RECEPTOR; EXCITOTOXIN; GLUTAMATE RECEPTOR AGONIST; KAINIC ACID RECEPTOR; N METHYL DEXTRO ASPARTIC ACID RECEPTOR;

ARTICLE; CALCIUM TRANSPORT; CELL CULTURE; CELL SURVIVAL; CONTROLLED STUDY; ELECTROPHYSIOLOGY; EMBRYO; GENETIC TRANSFECTION; HUMAN; HUMAN CELL; IMMUNOBLOTTING; KIDNEY CELL; PRIORITY JOURNAL;

EID: 0030004899     PISSN: 10447431     EISSN: None     Source Type: Journal    
DOI: 10.1006/mcne.1996.0008     Document Type: Article

References (72)

1. Albin, R. L., and Greenamyre, J. T. (1992). Alternative excitotoxic hypotheses. Neurology 42: 733-738.
2. Anegawa, N. J., Lynch, D. R., Verdoorn, T. A., and Pritchett, D. B. (1995). Transfection of N-methyl-D-aspartate receptors in a nonneuronal cell line leads to cell death. J. Neurochem. 64: 2004-2012.
3. Ascher, P., and Nowak, L. (1988). Quisqualate-and kainate-activated channels in mouse central neurones in culture. J. Physiol. 399: 227-245.
4. 2+ entry via AMPA/KA receptors and excitotoxicity in cultured cerebellar Purkinje cells. J. Neurosci. 14: 187-197.
5. Brorson, J. R., Manzolillo, P. A., Gibbons, S. J., and Miller, R. J. (1995). AMPA receptor desensitization predicts the selective vulnerability of cerebellar Purkinje cells to excitotoxicity. J. Neurosci. 15: 4515-4524.
6. Burnashev, N., Schoepfer, R., Monyer, H., Ruppersberg, J. P., G̈unther, W., Seeburg, P. H., and Sakmann, B. (1992a). Control by asparagine residues of calcium permeability and magnesium blockade in the NMDA receptor. Science 257: 1415-1419.
7. Burnashev, N., Monyer, H., Seeburg, P. H., and Sakmann, B. (1992b). Divalent ion permeability of AMPA receptor channels is dominated by the edited form of a single subunit. Neuron 8: 189-198.
8. Chen, C., and Okayama, H. (1987). High-efficiency transformation of mammalian cells by plasmid DNA. Mol. Cell. Biol. 7: 2745-2752.
9. Choi, D. W. (1987). Ionic dependence of glutamate neurotoxicity. J. Neurosci. 7: 369-379.
10. Choi, D. W. (1988). Glutamate neurotoxicity and diseases of the nervous system. Neuron 1: 623-634.
11. Choi, D. W. (1994). Glutamate receptors and the induction of excitotoxic neuronal death. Prog. Brain Res. 100: 47-51.
12. Choi, D. W., Koh, J.-y., and Peters, S. (1988). Pharmacology of glutamate neurotoxicity in cortical cell culture: Attenuation by NMDA antagonists. J. Neurosci. 8: 185-196.
13. Cik, M., Chazot, P. L., and Stephenson, F. A. (1993). Optimal expression of cloned NMDAR1/NMDAR2A heteromeric glutamate receptors: A biochemical characterization. Biochem. J. 296: 877-883.
14. Cik, M., Chazot, P. L., and Stephenson, F. A. (1994). Expression of NMDAR1-1a (N598Q)/NMDAR2A receptors results in decreased cell mortality. Eur. J. Pharmacol. 266: R1-R3.
15. Coyle, J. T., and Puttfarcken, P. (1993). Oxidative stress, glutamate, and neurodegenerative disorders. Science 262: 689-695.
16. Durand, G. M., Bennett, M. V. L., and Zukin, R. S. (1993). 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. USA 90: 6731-6735.
17. 2+ permeability of unedited and edited versions of the kainate selective glutamate receptor GluR6. Proc. Natl. Acad. Sci. USA 90: 755-759.
18. Egebjerg, J., Bettler, B., Hermans-Borgmeyer, I., and Heinemann, S. (1991). Cloning of cDNA for a glutamate receptor subunit activated by kainate but not AMPA. Nature 351: 745-748.
19. 2+ and the potentiation by serum albumin. Brain Res. 560: 282-290.
20. Frandsen, A., and Schousboe, A. (1993). Excitatory amino acid-mediated cytotoxicity and calcium homeostasis in cultured neurons. J. Neurochem. 60: 1202-1211.
21. 2+ of N-methyl-D-aspartate and quisqualate neurotoxicity in young rat hippocampal slices. Neurosci. Lett. 97: 316-322.
22. Garthwaite, G., Hajós, F., and Garthwaite, J. (1986). Ionic requirements for neurotoxic effects of excitatory amino acid analogues in rat cerebellar slices. Neuroscience 18: 437-447.
23. Gasic, G. P., and Hollmann, M. (1992). Molecular neurobiology of glutamate receptors. Annu. Rev. Physiol. 54: 507-536.
24. Hamill, O. P., Marty, A., Neher, E., Sakmann, B., and Sigworth, F. J. (1981). Improved patch-clamp techniques for high resolution current recording from cells and cell-free membrane patches. Pflugers Arch. 391: 85-100.
25. 2+ accumulation in cortical cell culture correlates with subsequent neuronal degeneration. J. Neurosci. 13: 1993-2000.
26. Hollmann, M., and Heinemann, S. (1994). Cloned glutamate receptors. Annu. Rev. Neurosci. 17: 31-108.
27. 2+ permeability of KA-AMPA-gated glutamate receptor channels depends on subunit composition. Science 252: 851-853.
28. Ishii, T., Moriyoshi, K., Sugihara, H., Sakurada, K., Kadotani, H., Yokoi, M., Akazawa, C., Shigemoto, R., Mizuno, N., Masu, M., and Nakanishi, S. (1993). Molecular characterization of the family of the N-methyl-D-aspartate receptor subunits. J. Biol. Chem. 268: 2836-2843.
29. Kanai, Y., and Hediger, M. A. (1992). Primary structure and functional characterization of a high-affinity glutamate transporter. Nature 360: 467-471.
30. Kochhar, A., Zivin, J. A., Lyden, P. D., and Mazzarella, V. (1988). Glutamate antagonist therapy reduces neurologic deficits produced by focal central nervous system ischemia. Arch. Neurol. 45: 148-153.
31. 2+ permeability in both TM1 and TM2 of high affinity kainate receptor channels: Diversity by RNA editing. Neuron 10: 491-500.
32. Kowall, N. W., Ferrante, R. J., and Martin, J. B. (1987). Patterns of cell loss in Huntington's disease. Trends Neurosci. 10: 24-29.
33. Kunkel, T. A., Roberts, J. D., and Zabour, D. L. (1987). Rapid and efficient site-specific mutagenesis without phenotypic selection. Methods Enzymol. 154: 367-382.
34. Kutsuwada, T., Kashiwabuchi, N., Mori, H., Sakimura, K., Kushiya, E., Araki, K., Meguro, H., Masaki, H., Kumanishi, T., Arakawa, M., and Mishina, M. (1992). Molecular diversity of the NMDA receptor channel. Nature 358: 36-41.
35. Lynch, D. R., Lawrence, J. J., Lenz, S., Anegawa, N. J., Dichter, M., and Pritchett, D. B. (1995). Pharmacological characterization of heterodimeric NMDA receptors composed of NR 1a and 2B subunits: Differences with receptors formed from NR 1a and 2A. J. Neurochem. 64: 1462-1468.
36. MacDermott, A. B., and Dale, N. (1987). Receptors, ion channels and synaptic potentials underlying the integrative actions of excitatory amino acids. Trends Neurosci. 10: 280-284.
37. May, P. C., and Robison, P. M. (1993). Cyclothiazide treatment unmasks AMPA excitotoxicity in rat primary hippocampal cultures. J. Neurochem. 60: 1171-1174.
38. Mayer, M. L., and Westbrook, G. L. (1987). The physiology of excitatory amino acids in the vertebrate nervous system. Prog. Neurobiol. 28: 197-276.
39. Meldrum, B., and Garthwaite, J. (1990). Excitatory amino acid neurotoxicity and neurodegenerative disease. Trends Pharmacol. Sci. 11: 379-387.
40. Michaels, R. L., and Rothman, S. M. (1990). Glutamate neurotoxicity in vitro: Antagonist pharmacology and intracellular calcium concentrations. J. Neurosci. 10: 283-292.
41. Monaghan, D. T., Bridges, R. J., and Cotman, C. W. (1989). The excitatory amino acid receptors: Their classes, pharmacology, and distinct properties in the function of the central nervous system. Annu. Rev. Pharmacol. Toxicol. 29: 365-402.
42. Monyer, H., Sprengel, R., Schoepfer, R., Herb, A., Higuchi, M., Lomeli, H., Burnashev, N, Sakmann, B., and Seeburg, P. H. (1992). Heteromeric NMDA receptors: molecular and functional distinction of subtypes. Science 256: 1217-1221.
43. 2+-block site of the NMDA receptor channel. Nature 358: 673-675.
44. Moudy, A. M., Yamada, K. A., and Rothman, S. M. (1994). Rapid desensitization determines the pharmacology of glutamate neurotoxicity. Neuropharmacology 33: 953-962.
45. Nakanishi, S. (1992). Molecular diversity of glutamate receptors and implications for brain function. Science 258: 597-603.
46. 2+ in toxic cell killing. Trends Pharmacol. Sci. 10: 281-285.
47. Park, C. K., Nehls, D. G., Graham, D. I., Teasdale, G. M., and McCulloch, J. (1988). The glutamate antagonist MK-801 reduces focal ischemic brain damage in the rat. Ann. Neurol. 24: 543-551.
48. Partin, K. M., Patneau, D. K., Winters, C. A., Mayer, M. L., and Buonanno, A. (1993). Selective modulation of densensitization at AMPA versus kainate receptors by cyclothiazide and concanavalin A. Neuron 11: 1069-1082.
49. Partin, K. M., Bowie, D., and Mayer, M. L. (1995). Structural determinants of allosteric regulation in alternatively spliced AMPA receptors. Neuron 14: 833-843.
50. Randall, R. D., and Thayer, S. A. (1992). Glutamate-induced calcium transient triggers delayed calcium overload and neurotoxicity in rat hippocampal neurons. J. Neurosci. 12: 1882-1895.
51. Raymond, L. A., Blackstone, C. D., and Huganir, R. L. (1993). Phosphorylation and modulation of recombinant GluR6 glutamate receptors by cAMP-dependent protein kinase. Nature 361: 637-641.
52. Roche, K. W., Raymond, L. A., Blackstone, C., and Huganir, R. L. (1994). Transmembrane topology of the glutamate receptor subunit GluR6. J. Biol. Chem. 269: 11679-11682.
53. Rothman, S. M., Thurston, J. H., and Hauhart, R. E. (1987). Delayed neurotoxicity of excitatory amino acids in vitro. Neuroscience 22: 471 -480.
54. 2+ and channel blockers by a single amino acid substitution in the N-methyl-D-aspartate receptor. J. Biol. Chem. 268: 410-415.
55. Schanne, F. A. X., Kane, A. B., Young, E. E., and Farber, J. L. (1979). Calcium dependence of toxic cell death: A final common pathway. Science 206: 700-702.
56. Schramm, M., Eimerl, S., and Costa, E. (1990). Serum and depolarizing agents cause acute neurotoxicity in cultured cerebellar granule cells: Role of the glutamate receptor responsive to N-methyl-D-aspartate. Proc. Natl. Acad. Sci. USA 87: 1193-1197.
57. Seeburg, P. H. (1993). The molecular biology of mammalian glutamate receptor channels. Trends Neurosci. 16: 359-365.
58. Sheardown, M. J., Nielsen, E. O., Hansen, A. J., Jacobsen, P., and Honoré, T. (1990). 2,3-Dihydroxy-6-nitro-7-sulfamoyl-benzo(F)quinoxaline: A neuroprotectant for cerebral ischemia. Science 247: 571-574.
59. Simon, R. P., Swan, J. H., Griffiths, T., and Meldrum, B. S. (1984). Blockade of N-methyl-D-aspartate receptors may protect against ischemic damage in the brain. Science 226: 850-852.
60. Sommer, B., Keinänen, K., Verdoorn, T. A., Wisden, W., Burnashev, N., Herb, A., Köhler, M., Takagi, T., Sakmann, B., and Seeburg, P. H. (1990). Flip and flop: A cell-specific functional switch in glutamate-operated channels of the CNS. Science 249: 1580-1585.
61. Stern, P., Béhé, P., Schoepfer, R., and Colquhoun, D. (1992). Single-channel conductances of NMDA receptors expressed from cloned cDNAs: comparison with native receptors. Proc. R. Soc. London B 250: 271-277.
62. Sugihara, H., Moriyoshi, K., Ishii, T., Masu, M., and Nakanishi, S. (1992). Structures and properties of seven isoforms of the NMDA receptor generated by alternative splicing. Biochem. Biophys. Res. Commun. 185: 826-832.
63. Tingley, W. G., Roche, K. W., Thompson, A. K., and Huganir, R. L. (1993). Regulation of NMDA receptor phosphorylation by alternative splicing of the C-terminal domain. Nature 364: 70-73.
64. Traynelis, S. F., Hartley, M., and Heinemann, S. F. (1995). Control of proton sensitivity of the NMDA receptor by RNA splicing and polyamines. Science 268: 873-876.
65. 2+ chelators reduce early excitotoxic and ischemic neuronal injury in vitro and in vivo. Neuron 11: 221-235.
66. Uematsu, D., Araki, N., Greenberg, J. H., Sladky, J., and Reivich, M. (1991). Combined therapy with MK-801 and nimodipine for protection of ischemic brain damage. Neurology 41: 88-94.
67. Weiss, J. H., Hartley, D. M., Koh, J., and Choi, D. W. (1990). The calcium channel blocker nifedipine attenuates slow excitatory amino acid neurotoxicity. Science 247: 1474-1477.
68. Weiss, J. H., Yin, H.-Z., and Choi, D. W. (1994a). Basal forebrain cholinergic neurons are selectively vulnerable to AMPA/kainate receptor-mediated neurotoxicity. Neuroscience 60: 659-664.
69. 2+ dependent. Neurosci. Lett. 167: 93-96.
70. Wyllie, D. J., Traynelis, S. F., and Cull-Candy, S. G. (1993). Evidence for more than one type of non-NMDA receptor in outside-out patches from cerebellar granule cells of the rat. J. Physiol. 463: 193-226.
71. 2+ dependent. NeuroReport 5: 1477-1480.
72. Zorumski, C. F., Thio, L. L., Clark, G. D., and Clifford ,D. B. (1990). Blockade of desensitization augments quisqualate excitotoxicity in hippocampal neurons. Neuron 5: 61-66.