AMPA receptor mediated excitotoxicity in neocortical neurons is developmentally regulated and dependent upon receptor desensitization

Neurochemistry International

Volumn 32, Issue 5-6, 1998, Pages 505-513

  Jensen, J B ^a   Schousboe, A ^a   Pickering, D S ^a  

^a UNIVERSITY OF COPENHAGEN   (Denmark)

Author keywords

[No Author keywords available]

Indexed keywords

1 (4 AMINOPHENYL) 3,4 DIHYDRO 4 METHYL 3 METHYLCARBAMOYL 7,8 METHYLENEDIOXY 5H 2,3 BENZODIAZEPINE; 1 (4 AMINOPHENYL) 4 METHYL 7,8 METHYLENEDIOXY 5H 2,3 BENZODIAZEPINE; 6 NITRO 7 SULFAMOYLBENZO[F]QUINOXALINE 2,3 DIONE; AMPA RECEPTOR; AMPA RECEPTOR ANTAGONIST; CYCLOTHIAZIDE; DIZOCILPINE; GLUTAMATE RECEPTOR ANTAGONIST; N METHYL DEXTRO ASPARTIC ACID RECEPTOR;

ANIMAL CELL; ARTICLE; CELL DEATH; CELL VIABILITY; CONTROLLED STUDY; FEMALE; MOUSE; NEOCORTEX; NERVE CELL CULTURE; NERVOUS SYSTEM DEVELOPMENT; NONHUMAN; PRIORITY JOURNAL; RECEPTOR DOWN REGULATION;

ALPHA-AMINO-3-HYDROXY-5-METHYL-4-ISOXAZOLEPROPIONIC ACID; ANIMALS; BENZOTHIADIAZINES; CELL AGING; CELLS, CULTURED; CEREBRAL CORTEX; EXCITATORY AMINO ACID ANTAGONISTS; MICE; MICE, INBRED STRAINS; NEURONS; NEUROTOXINS; RECEPTORS, AMPA; SODIUM AZIDE;

ANIMALIA;

EID: 0032078116     PISSN: 01970186     EISSN: None     Source Type: Journal    
DOI: 10.1016/S0197-0186(97)00130-7     Document Type: Article

References (58)

1. Angulo, M.C., Lambolez, B., Audinat, E., Hestrin, S., Rossier, J., 1997. Subunit composition, kinetic, and permeation properties of AMPA receptors in single neocortical nonpyramidal cells. J. Neurosci. 17, 6685-6696.
2. Berman, F.W., Murray, T.F., 1997. Domoic acid neurotoxicity in cultured cerebellar granule neurons is mediated predominantly by NMDA receptors that are activated as a consequence of excitatory amino acid release. J. Neurochem. 69, 693-703.
3. Berridge, M.V., Tan, A.S., 1993. Characterization of the cellular reduction of 3-(4,5-dimethylthiazol-2-yl)-2,5-diphenyltetrazolium bromide (MTT): subcellular localization, substrate dependence, and involvement of mitochondrial electron transport in MTT reduction. Arch. Biochem. Biophys. 303, 474-482.
4. Bleakman, D., Ballyk, B.A., Schoepp, D.D., Palmer, A.J., Bath, C.P., Sharpe, E.F., Woolley, M.L., Bufton, H.R., Kamboj, R.K., Tarnawa, I., Lodge, D., 1996. Activity of 2,3-benzodiazepines at native rat and recombinant human glutamate receptors in vitro: stereospecificity and selectivity profiles. Neuropharmacol. 35, 1689-1702.
5. Burnashev, N., 1993. Recombinant ionotropic glutamate receptors: functional distinctions imparted by different subunits. Cell Physiol. Biochem. 3, 318-331.
6. Burnashev, N., Monyer, H., Seeburg, P.H., Sakmann, B., 1992. Divalent ion permeability of AMPA receptor channels is dominated by the edited form of a single subunit. Neuron 8, 189-198.
7. 2+ uptake in brain neurons. Eur. J. Pharmacol. 290, 105-115.
8. Cebers, G., Zhivotovsky, B., Ankarcrona, M., Liljequist, S., 1997. AMPA neurotoxicity in cultured cerebellar granule neurons: mode of cell death. Brain Res. Bull. 43, 393-403.
9. Choi, D.W., 1985. Glutamate neurotoxicity in cortical cell culture is calcium dependent. Neurosci. Lett. 58, 293-297.
10. Choi, D.W., 1992. Excitotoxic cell death. J. Neurobiol. 23, 1261-1276.
11. Choi, D.W., Koh, J.-Y., Peters, S., 1988. Pharmacology of glutamate neurotoxicity in cortical cell culture: attenuation by NMDA antagonists. J. Neurosci. 8, 185-196.
12. Dichter, M.A., 1978. Rat cortical neurons in culture: methods, cell morphology, electrophysiology and synapse formation. Brain Res. 149, 279-293.
13. Donevan, S.D., Rogawski, M.A., 1993. GYKI 52466, a 2,3-benzodiazepine, is a highly selective, noncompetitive antagonist of AMPA/kainate receptor responses. Neuron 10, 51-59.
14. Donevan, S.D., Yamaguchi, S-I., Rogawski, M.A., 1994. Non-N-methyl-D-aspartate receptor antagonism by 3-N-substituted 2,3-benzodiazepines: relationship to anticonvulsant activity. J. Pharmacol. Exp. Therap. 271, 25-29.
15. Dugan, L.L., Bruno, V.M.G., Amagasu, S.M., Giffard, R.G., 1995. Glia modulate the response of murine cortical neurons to excitotoxicity: Glia exacerbate AMPA neurotoxicity. J. Neurosci. 15, 4545-4555.
16. Frandsen, A., Schousboe, A., 1987. Time and concentration dependency of the toxicity of excitatory amino acids on cerebral neurons in primary culture. Neurochem. Int. 10, 583-591.
17. Frandsen, A., Schousboe, A., 1990. Development of excitatory amino acid induced cytotoxicity in cultured neurons. Int. J. Devl. Neurosci. 8, 209-216.
18. 2+ release from intracellular stores in cultured cerebral cortical neurons. J. Neurochem. 56, 1075-1078.
19. Frandsen, A., Schousboe, A., 1992. Mobilization of dantrolene-sensitive intracellular calcium pools is involved in the cytotoxicity induced by quisqualate and N-methyl-D-aspartate but not by 2-amino-3-(3-hydroxy-5-methylisoxazol-4-yl)propionate and kainate in cultured cerebral cortical neurons. Proc. Natl. Acad. Sci. U.S.A. 89, 2590-2594.
20. 2+ permeability of AMPA receptors in principal neurons and interneurons in rat CNS. Neuron 15, 193-204.
21. Hack, N.J., Sluiter, A.A., Balázs, R., 1995. AMPA receptors in cerebellar granule cells during development in culture. Dev. Brain Res. 87, 55-61.
22. Hertz, E., Yu, A.C.H., Hertz, L., Juurlink, B.H.J., Schousboe, A., 1989. Preparation of primary cultures of mouse cortical neurons. In Shahar, A., de Vellis, J., Vernadakis, A., Haber, B. (Eds), A dissection and tissue culture manual of the nervous system, chapter 40. Alan R. Liss. Inc, New York, pp. 183-186.
23. Hertz, L., Juurlink, B.H.J., Fosmark, H., Schousboe, A., 1982. Astrocytes in primary cultures. In Pfeiffer, K.S.E. (Ed.), Neuroscience approached through cell culture, Vol. 1, CRC Press, Boca Raton, Fl, U.S.A. pp. 175-186.
24. 2+ permeability of KA-AMPA-gated glutamate receptor channels depends on subunit composition. Science 252, 851-853.
25. 2+ in cultured neurons from rat brain. J. Neurochem. 64, 2049-2056.
26. Impagnatiello, F., Oberto, A., Longone, P., Costa, E., Guidotti, A., 1997. 7-cloro-3-methyl-3,4-dihydro-2H-1,2,4-benzothiadiazine S,S-dioxide: a partial modulator of AMPA receptor desensitization devoid of neurotoxicity. Proc. Natl. Acad. Sci. U.S.A. 94, 7053-7058.
27. Kim, J.P., Koh, J., Choi, D.W., 1987. L-Homocysteate is a potent neurotoxin on cultured cortical neurons. Brain Res. 437, 103-110.
28. Kiskin, N.I., Krishtal, O.A., Tsyndrenko, A.Y., 1986. Excitatory amino acid receptors in hippocampal neurons: kainate fails to desensitize them. Neurosci. Lett. 63, 225-230.
29. Koh, J.-Y., Goldberg, M.P., Hartley, D.M., Choi, D.W., 1990. NonNMDA receptor-mediated neurotoxicity in cortical culture. J. Neurosci. 10, 693-705.
30. Kovács, A.D., Szabó, G., 1997. GYKI 53655, a 2,3-benzodiazepine, non-competitively protects cultured neurons against AMPA toxicity. Eur. J. Pharmacol. 331, 93-96.
31. Lambolez, B., Ropert, N., Perrais, D., Rossier, J., Hestrin, S., 1996. Correlation between kinetics and RNA splicing of α-amino-3-hydroxy-5-methylisoxazole-4-propionic acid receptors in neocortical neurons. Proc. Natl. Acad. Sci. U.S.A. 93, 1797-1802.
32. Larm, J.A., Cheung, N.S., Beart, P.M., 1996. (S)-5-fluorowillardiine-mediated neurotoxicity in cultured murine cortical neurons occurs via AMPA and kainate receptors. Eur. J. Pharmacol. 314, 249-254.
33. Larm, J.A., Cheung, N.S., Beart, P.M., 1997. Apoptosis induced via AMPA-selective glutamate receptors in cultured murine cortical neurons. J. Neurochem. 69, 617-622.
34. Larsson, O.M., Drejer, J., Kvamme, E., Svenneby, G., Hertz, L., Schousboe, A., 1985. Ontogenetic development of glutamate and GABA metabolizing enzymes in cultured cerebral cortex interneurons and in cerebral cortex in vivo. Int. J. Devl. Neurosci. 3, 177-185.
35. Liu, Y., Peterson, D.A., Kimura, H., Schubert, D., 1997. Mechanism of cellular 3-(4,5-dimethylthiazol-2-yl)-2,5-diphenyltetrazolium bromide (MTT) reduction. J. Neurochem. 69, 5811-5593.
36. Lomeli, H., Mosbacher, J., Melcher, T., Höger, T., Geiger, J.R.P., Kuner, T., Monyer, H., Higuchi, M., Bach, A., Seeburg, P., 1994. Control of kinetic properties of AMPA receptor channels by nuclear RNA editing. Science 266, 1709-1713.
37. May, P.C., Robison, P.M., 1993. Cyclothiazide treatment unmasks AMPA excitotoxicity in rat primary hippocampal cultures. J. Neurochem. 60, 1171-1174.
38. Mosbacher, J., Schoepfer, R., Monyer, H., Burnashev, N., Seeburg, P.H., Ruppersberg, J.P., 1994. A molecular determinant for submillisecond desensitization in glutamate receptors. Science 266, 1059-1062.
39. Mosman, T., 1983. Rapid colorimetric assay for cellular growth and survival: application to proliferation and cytotoxicity assays. J. Immun. Meth. 65, 55-63.
40. Moudy, A.M., Yamada, K.A., Rothman, S.M., 1994. Rapid desensitization determines the pharmacology of glutamate neurotoxicity. Neuropharmacol. 33, 953-962.
41. Olney, J.W., 1988. Endogenous excitotoxins and neuropathological disorders. In Lodge, D. (Ed.), Excitatory Amino Acids in Health and Disease, Wiley, London, pp. 297-320.
42. Partin, K.M., Fleck, M.W., Mayer, M.L., 1996. AMPA receptor flip/ flop mutants affecting deactivation, desensitization, and modulation by cyclothiazide, aniracetam, and thiocyanate. J. Neurosci. 16, 6634-6647.
43. Paternain, A.V., Morales, M., Lerma, J., 1995. Selective antagonism of AMPA receptor unmasks kainate receptor-mediated responses in hippocampal neurons. Neuron 14, 185-189.
44. Paternain, A.V., Vicente, A., Nielsen, E.Ø., Lerma J., 1996. Comparative antagonism of kainate-activated kainate and AMPA receptors in hippocampal neurons. Eur. J. Neurosci. 8, 2129-2136.
45. Patneau, D.K., Mayer, M.L., 1991. Kinetic analysis of interactions between kainate and AMPA: evidence for activation of a single receptor in mouse hippocampal neurons. Neuron 6, 785-798.
46. 2+-permeable AMPA receptors among cultured rat cerebellar granule cells. Neuro Report 8, 1877-1882.
47. 2+ homeostasis. In Ascher, P., Choi, D.W., Christen, Y. (Eds), Glutamate, Cell Death and Memory, Springer-Verlag, Berlin, Heidelberg, pp. 137-152.
48. Sensenbrenner, M., Maderspach, K., Latzkovits, L., Jarós, G., 1978. Neuronal cells from chick embryo cerebral hemispheres cultivated on polylysine-coated surfaces. Devl. Neurosci. 1, 91-101.
49. Sheardown, M.J., Nielsen, E.Ø., Hansen, A.J., Jacobsen, P., Honore, T., 1990. 2,3-dihydroxy-6-nitro-7-sulfamoyl-benzo(F)quinoxaline: a neuroprotectant for cerebral ischemia. Science 247, 571-574.
50. Slater, T.F., Sawyer, B., Sträuli U., 1963. Studies on succinate-tetrazolium reductase systems. III. Points of coupling of four different tetrazolium salts. Biochim Biophys. Acta 77, 383-393.
51. Swanson, G.T., Kamboj, S.K., Cull-Candy, S.G., 1997. Single-channel properties of recombinant AMPA receptors depend on RNA editing, splice variation, and subunit composition. J. Neurosci. 17, 58-69.
52. Tang, C.-M., Shi, Q.-Y., Katchman, A., Lynch, G., 1991. Modulation of the time course of fast EPSCs and glutamate channel kinetics by aniracetam. Science 254, 288-290.
53. Thio, L.L., Clifford, D.B., Zorumski, C.F., 1992. Blockade of ionotropic quisqualate receptor desensitization by wheat germ agglutinin in cultured postnatal rat hippocampal neurons. J. Neurophysiol. 68, 1917-1929.
54. Varming, T., Drejer, J., Frandsen, A., Schousboe, A., 1996. Characterization of a chemical anoxia model in cerebellar granule neurons using sodium azide: protection by nifedipine and MK-801. J. Neurosci. Res. 44, 40-46.
55. Vizi, E.S., Mike, A., Tarnawa, L, 1996. 2,3-Benzodiazepines (GYKI 52466 and analogs): negative allosteric modulators of AMPA receptors. CNS Drug Reviews 2, 91-126.
56. Weiss, J.H., Hartley, D.M., Koh, J., Choi, D.W., 1990. The calcium channel blocker nifedipine attenuates slow excitatory amino acid neurotoxicity. Science 247, 1474-1477.
57. Wong, E.H., Kemp, J.A., Priestley, T., Knight, A.R., Woodruff, G.N., Iversen L.L., 1986. The anticonvulsant MK-801 is a potent N-methyl-D-aspartate antagonist. Proc. Natl. Acad. Sci. U.S.A. 83, 7104-7108.
58. Yamada, K.A., Tang, C.-M., 1993. Benzothiadiazides inhibit rapid glutamate receptor desensitization and enhance glutamatergic synaptic currents. J. Neurosci. 13, 3904-3915.