Kainate-induced excitotoxicity is dependent upon extracellular potassium concentrations that regulate the activity of AMPA/KA type glutamate receptors

Journal of Neurochemistry

Volumn 83, Issue 4, 2002, Pages 934-945

  Ha, Byeong Keun ^a   Vicini, Stefano ^b   Rogers, Richard C ^a,d   Bresnahan, Jacqueline C ^a   Burry, Richard W ^a   Beattie, Michael S ^a,c  

^a OHIO STATE UNIVERSITY   (United States)

^b GEORGETOWN UNIVERSITY   (United States)

^c THE OHIO STATE UNIVERSITY COLLEGE OF MEDICINE   (United States)

^d PENNINGTON BIOMEDICAL RESEARCH CENTER   (United States)

Author keywords

AMPA KA receptors; Cerebellar granule cell; Excitotoxicity; GluR1; Potassium

Indexed keywords

AMPA RECEPTOR; GLUTAMATE RECEPTOR; KAINIC ACID; KAINIC ACID RECEPTOR; N METHYL DEXTRO ASPARTIC ACID; POTASSIUM;

ANIMAL CELL; APOPTOSIS; ARTICLE; CELL CULTURE; CEREBELLUM; CONTROLLED STUDY; CULTURE MEDIUM; CYTOTOXICITY; ELECTROPHYSIOLOGY; ENZYME ACTIVITY; ENZYME REGULATION; EXTRACELLULAR SPACE; GRANULE CELL; IMMUNOFLUORESCENCE; INOTROPISM; NONHUMAN; POTASSIUM CONDUCTANCE; POTASSIUM CURRENT; PRIORITY JOURNAL; PROTEIN EXPRESSION; RAT; RECEPTOR INTRINSIC ACTIVITY;

ANIMALS; CELL NUCLEUS; CELL SURVIVAL; CELLS, CULTURED; CEREBELLUM; CULTURE MEDIA, SERUM-FREE; DOSE-RESPONSE RELATIONSHIP, DRUG; EXCITATORY AMINO ACID ANTAGONISTS; EXTRACELLULAR SPACE; FLUORESCENT ANTIBODY TECHNIQUE; N-METHYLASPARTATE; NECROSIS; NEURONS; PATCH-CLAMP TECHNIQUES; POTASSIUM; RATS; RATS, LONG-EVANS; RECEPTORS, AMPA;

ANIMALIA;

EID: 0036846126     PISSN: 00223042     EISSN: None     Source Type: Journal    
DOI: 10.1046/j.1471-4159.2002.01203.x     Document Type: Article

References (76)

1. Ankarcrona M., Dypbukt J. M., Bonfoco E., Zhivotovsky B., Orrenius S., Lipton S. A. and Nicotera P. (1995) Glutamate-induced neuronal death: A succession of necrosis or apoptosis depending on mitochondrial function. Neuron 15, 961-973.
2. Balazs R., Jorgensen O. S. and Hack N. (1988) N-methyl-D-aspartate promotes the survival of cerebellar granule cells in culture. Neuroscience 27, 437-451.
3. Balazs R., Resink A., Hack N., Van der Valk J. B., Kumar K. N. and Michaelis E. (1992) NMDA treatment and K(+)-induced depolarization selectively promote the expression of an NMDA-preferring class of the ionotropic glutamate receptors in cerebellar granule neurones. Neurosci. Lett. 137, 109-113.
4. Bear M. F. and Abraham W. C. (1996) Long-term depression in hippocampus. Annu. Rev. Neurosci. 19, 437-462.
5. Beattie E. C., Carroll R. C., Yu X., Morishita W., Yasuda H., von Zastrow M. and Malenka R. C. (2000) Regulation of AMPA receptor endocytosis by a signaling mechanism shared with LTD. Nat. Neurosci. 3, 1291-1300.
6. Beattie E. C., Stellwagen D., Morishita W., Bresnahan J. C., Ha B. K., von Zastrow M., Beattie M. S. and Malenka R. C. (2002) Control of synaptic strength by glial TNFα Science 295, 2282-2285.
7. Bliss T. V. and Collingridge G. L. (1993) A synaptic model of memory: long-term potentiation in the hippocampus. Nature 361, 31-39.
8. Buchan A., Li H., Cho S. and Pulsinelli W. A. (1991) Blockade of the AMPA receptor prevents CA1 hippocampal injury following severe but transient forebrain ischemia in adult rats. Neurosci. Lett. 132, 255-258.
9. Burnashev N., Monyer H., Seeburg P. H. and Sakmann B. (1992) Divalent ion permeability of AMPA receptor channels is dominated by the edited form of a single subunit. Neuron 8, 189-198.
10. Burry R. W. and Lasher R. S. (1978) A quantitative electron microscopic study of synapse formation in dispersed cell cultures of rat cerebellum stained either by Os-UL or by E-PTA. Brain Res. 147, 1-15.
11. Carroll R. C., Beattie E. C., Xia H., Luscher C., Altschuler Y., Nicoll R. A., Malenka R. C. and von Zastrow M. (1999a) Dynamindependent endocytosis of ionotropic glutamate receptors. Proc. Natl Acad. Sci. USA 96, 14112-14117.
12. Carroll R. C., Lissin D. V., von Zastrow M., Nicoll R. A. and Malenka R. C. (1999b) Rapid redistribution of glutamate receptors contributes to long-term depression in hippocampal cultures. Nat. Neurosci. 2, 454-460.
13. Chang H., Hua L. L., Morgan A. and Lee S. C. (2001) Inhibition of astrocyte TNFα expression by extracellular potassium. Brain Res. 888, 176-179.
14. Chen Q., Harris C., Brown C. S., Howe A., Surmeier D. J. and Reiner A. (1995) Glutamate-mediated excitotoxic death of cultured striatal neurons is mediated by non-NMDA receptors. Exp. Neurol. 136, 212-224.
15. i increases and NMDA receptor mRNA levels. Brain Res. 849, 97-108.
16. Cheung N. S., Carroll F. Y., Larm J. A., Beart P. M. and Giardina S. F. (1998) Kainate-induced apoptosis correlates with c-Jun activation in cultured cerebellar granule cells. J. Neurosci. Res. 52, 69-82.
17. Chittajallu R., Braithwaite S. P., Clarke V. R. and Henley J. M. (1999) Kainate receptors: Subunits, synaptic localization and function. Trends Pharmacol. Sci. 20, 26-35.
18. Choi D. W. (1992a) Bench to bedside: The glutamate connection. Science 258, 241-243.
19. Choi D. W. (1992b) Excitotoxic cell death. J. Neurobiol. 23, 1261-1276.
20. Ciabarra A. M., Sullivan J. M., Gahn L. G., Pecht G., Heinemann S. and Sevarino K. A. (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.
21. Condorelli D. F., Dell'Albani P., Aronica E., Genazzani A. A., Casabona G., Corsaro M., Balazs R. and Nicoletti F. (1993) Growth conditions differentially regulate the expression of α-amino-3-hydroxy-5-methylisoxazole-4-propionate (AMPA) receptor sub-units in cultured neurons. J. Neurochem. 61, 2133-2139.
22. Cox J. A., Felder C. C. and Henneberry R. C. (1990) Differential expression of excitatory amino acid receptor subtypes in cultured cerebellar neurons. Neuron 4, 941-947.
23. Daniels M. and Brown D. R. (2001) Astrocytes regulate N-methyl-D-aspartate receptor subunit composition increasing neuronal sensitivity to excitotoxicity. J. Biol. Chem. 276, 22446-22452.
24. Das S., Sasaki Y. F., Rothe T., Premkumar L. S., Takasu M., Crandall J. E., Dikkes P., Conner D. A., Rayudu P. V., Cheung W., Chen H. S., Lipton S. A. and Nakanishi N. (1998) Increased NMDA current and spine density in mice lacking the NMDA receptor subunit NR3A. Nature 393, 377-381.
25. Dessi F., Charriaut-Marlangue C. and Ben-Ari Y. (1994) Glutamate-induced neuronal death in cerebellar culture is mediated by two distinct components: A sodium-chloride component and a calcium component. Brain Res. 650, 49-55.
26. Diemer N. H., Jorgensen M. B., Johansen F. F., Sheardown M. and Honore T. (1992) Protection against ischemic hippocampal CA1 damage in rat with a new non-NMDA antagonist, NBQX. Acta Neurol. Scand. 86, 45-49.
27. Dingledine R., Borges K., Bowie D. and Traynelis S. F. (1999) The glutamate receptor ion channels. Pharmacol. Rev. 51, 7-61.
28. Frandsen A., Drejer J. and Schousboe A. (1989) Direct evidence that excitotoxicity in cultured neurons is mediated via N-methyl-D- aspartate (NMDA) as well as non-NMDA receptors. J. Neurochem. 53, 297-299.
29. Fryer H. J., Knox R. J., Strittmatter S. M. and Kalb R. G. (1999) Excitotoxic death of a subset of embryonic rat motor neurons in vitro. J. Neurochem. 72, 500-513.
30. Gallo V., Kingsbury A., Balazs R. and Jorgensen O. S. (1987) The role of depolarization in the survival and differentiation of cerebellar granule cells in culture. J. Neurosci. 7, 2203-2213.
31. Garthwaite G. and Garthwaite J. (1986) In vitro neurotoxicity of excitatory acid analogues during cerebellar development. Neuroscience 17, 755-767.
32. 2+ permeability of AMPA receptors in principal neurons and intemeurons in rat CNS. Neuron 15, 193-204.
33. Hermann G. E., Rogers R. C., Bresnahan J. C. and Beattie M. S. (2001) Tumor necrosis factor-α induces cFOS and strongly potentiates glutamate-mediated cell death in the rat spinal cord. Neurobiol. Dis 8, 590-599.
34. Hoffmann H., Gremme T., Hatt H. and Gottmann K. (2000) Synaptic activity-dependent developmental regulation of NMDA receptor subunit expression in cultured neocortical neurons. J. Neurochem. 75, 1590-1599.
35. Hollmann M. and Heinemann S. (1994) Cloned glutamate receptors. Annu. Rev. Neurosci. 17, 31-108.
36. 2+ permeability of KA-AMPA-gated glutamate receptor channels depends on subunit composition. Science 252, 851-853.
37. Jakowec M. W., Jackson-Lewis V., Chen X., Langston J. W. and Przedborski S. (1998) The post-natal development of AMPA receptor subunits in the basal ganglia of the rat. Dev. Neurosci. 20, 19-33.
38. 2+ permeability of AMPA-type glutamate receptor channels in neocortical neurons caused by differential GluR-B subunit expression. Neuron 12, 1281-1289.
39. Kanellopoulos G. K., Xu X. M., Hsu C. Y., Lu X., Sundt T. M. and Kouchoukos N. T. (2000) White matter injury in spinal cord ischemia: protection by AMPA/kainate glutamate receptor antagonism. Stroke 31, 1945-1952.
40. Kato K., Puttfarcken P. S., Lyons W. E. and Coyle J. T. (1991) Developmental time course and ionic dependence of kainate-mediated toxicity in rat cerebellar granule cell cultures. J. Pharmacol. Exp. Ther. 256, 402-411.
41. Kawasaki-Yatsugi S., Yatsugi S., Koshiya K. and Shimizu-Sasamata M. (1997) Neuroprotective effect of YM90K, an AMPA-receptor antagonist, against delayed neuronal death induced by transient global cerebral ischemia in gerbils and rats. Jpn J. Pharmacol. 74, 253-260.
42. Keinanen K., Wisden W., Sommer B., Werner P., Herb A., Verdoom T. A., Sakmann B. and Seeburg P. H. (1990) A family of AMPA-selective glutamate receptors. Science 249, 556-560.
43. Kleinschmidt A., Bear M. F. and Singer W. (1987) Blockade of NMDA receptors disrupts experience-dependent plasticity of kitten striate cortex. Science 238, 355-358.
44. Kutsuwada T., Kashiwabuchi N., Mori H., Sakimura K., Kushiya E., Araki K., Meguro H., Masaki H., Kumanishi T., Arakawa M. and et al. (1992) Molecular diversity of the NMDA receptor channel. Nature 358, 36-41.
45. Lasher R. S. and Zagon I. S. (1972) The effect of potassium on neuronal differentiation in cultures of dissociated newborn rat cerebellum. Brain Res. 41, 482-488.
46. Lin J. W., Ju W., Foster K., Lee S. H., Ahmadian G., Wyszynski M., Wang Y. T. and Sheng M. (2000) Distinct molecular mechanisms and divergent endocytotic pathways of AMPA receptor internalization. Nat. Neurosci. 3, 1282-1290.
47. Lipton S. A. and Rosenberg P. A. (1994) Excitatory amino acids as a final common pathway for neurologic disorders. N. Engl. J. Med. 330, 613-622.
48. Lissin D. V., Carroll R. C., Nicoll R. A., Malenka R. C. and von Zastrow M. (1999) Rapid, activation-induced redistribution of ionotropic glutamate receptors in cultured hippocampal neurons. J Neurosci. 19, 1263-1272.
49. Luscher C., Nicoll R. A., Malenka R. C. and Muller D. (2000) Synaptic plasticity and dynamic modulation of the post-synaptic membrane. Nat Neurosci. 3, 545-550.
50. Luscher C., Xia H., Beattie E. C., Carroll R. C., von Zastrow M., Malenka R. C. and Nicoll R. A. (1999) Role of AMPA receptor cycling in synaptic transmission and plasticity. Neuron 24, 649-658.
51. Lynch G. and Baudry M. (1984) The biochemistry of memory: A new and specific hypothesis. Science 224, 1057-1063.
52. Malenka R. C. and Nicoll R. A. (1999) Long-term potentiation: A decade of progress? Science 285, 1870-1874.
53. Man H. Y., Ju W., Ahmadian G. and Wang Y. T. (2000a) Intracellular trafficking of AMPA receptors in synaptic plasticity. Cell Mol. Life Sci. 57, 1526-1534.
54. Man H. Y., Lin J. W., Ju W. H., Ahmadian G., Liu L., Becker L. E., Sheng M. and Wang Y. T. (2000b) Regulation of AMPA receptor-mediated synaptic transmission by clathrin-dependent receptor internalization. Neuron 25, 649-662.
55. Mizuta I., Katayama M., Watanabe M., Mishina M. and Ishii K. (1998) Developmental expression of NMDA receptor subunits and the emergence of glutamate neurotoxicity in primary cultures of murine cerebral cortical neurons. Cell Mol. Life Sci. 54, 721-725.
56. Moldrich R. X., Beart P. M., Pascoe C. J. and Cheung N. S. (2000) Low-affinity kainate receptor agonists induce insult-dependent apoptosis and necrosis in cultured murine cortical neurons. J Neurosci. Res. 59, 788-796.
57. Murase K., Ryu P. D. and Randic M. (1989) Excitatory and inhibitory amino acids and peptide-induced responses in acutely isolated rat spinal dorsal horn neurons. Neurosci. Lett. 103, 56-63.
58. Nakai M., Qin Z. H., Chen J. F., Wang Y. and Chase T. N. (2000) Kainic acid-induced apoptosis in rat striatum is associated with nuclear factor-κB activation. J. Neurochem. 74, 647-658.
59. O'Neill M. J., Bond A., Ornstein P. L., Ward M. A., Hicks C. A., Hoo K., Bleakman D. and Lodge D. (1998) Decahydroisoquinolines: Novel competitive AMPA/kainate antagonists with neuroprotective effects in global cerebral ischemia. Neuropharmacology 37, 1211-1222.
60. Pickard L., Noel J., Henley J. M., Collingridge G. L. and Molnar E. (2000) Developmental changes in synaptic AMPA and NMDA receptor distribution and AMPA receptor subunit composition in living hippocampal neurons. J Neurosci. 20, 7922-7931.
61. Porciuncula L. O., Rocha J. B., Boeck C. R., Vendite D. and Souza D. O. (2001) Ebselen prevents excitotoxicity provoked by glutamate in rat cerebellar granule neurons. Neurosci. Lett. 299, 217-220.
62. Resink A., Hack N., Boer G. J. and Balazs R. (1994) Growth conditions differentially modulate the vulnerability of developing cerebellar granule cells to excitatory amino acids. Brain Res. 655, 222-232.
63. Ritter L. M., Unis A. S. and Meador-Woodruff J. H. (2001) Ontogeny of ionotropic glutamate receptor expression in human fetal brain. Brain Res. Dev. Brain Res. 127, 123-133.
64. Rubio M. E. and Wenthold R. J. (1997) Glutamate receptors are selectively targeted to postsynaptic sites in neurons. Neuron 18, 939-950.
65. Sans N. A., Montcouquiol M. E. and Raymond J. (2000) Postnatal developmental changes in AMPA and NMDA receptors in the rat vestibular nuclei. Brain Res. Dev. Brain Res. 123, 41-52.
66. Shaw P. J. (1994) Excitotoxicity and motor neurone disease: A review of the evidence. J. Neurol. Sci. 124, 6-13.
67. Sheardown M. J., Suzdak P. D. and Nordholm L. (1993) AMPA, but not NMDA, receptor antagonism is neuroprotective in gerbil global ischaemia, even when delayed 24 h. Eur. J. Pharmacol. 236, 347-353.
68. Sheng M., Cummings J., Roldan L. A., Jan Y. N. and Jan L. Y. (1994) Changing subunit composition of heteromeric NMDA receptors during development of rat cortex. Nature 368, 144-147.
69. Shi S. H., Hayashi Y., Petralia R. S., Zaman S. H., Wenthold R. J., Svoboda K. and Malinow R. (1999) Rapid spine delivery and redistribution of AMPA receptors after synaptic NMDA receptor activation. Science 284, 1811-1816.
70. Simonian N. A., Getz R. L., Leveque J. C., Konradi C. and Coyle J. T. (1996) Kainic acid induces apoptosis in neurons. Neuroscience 75, 1047-1055.
71. Turski L., Huth A., Sheardown M., McDonald F., Neuhaus R., Schneider H. H., Dimagl U., Wiegand F., Jacobsen P. and Ottow E. (1998) ZK200775: A phosphonate quinoxalinedione AMPA antagonist for neuroprotection in stroke and trauma. Proc. Natl Acad. Sci. USA 95, 10960-10965.
72. Weiss J. H., Yin H. Z. and Choi D. W. (1994) Basal forebrain cholinergic neurons are selectively vulnerable to AMPA/kainate receptor-mediated neurotoxicity. Neuroscience 60, 659-664.
73. Wood A. M., Tiwari P. and Bristow D. R. (1997) Media composition modulates excitatory amino acid-induced death of rat cerebellar granule cells. Hum. Exp. Toxicol. 16, 350-355.
74. Wrathall J. R., Choiniere D. and Teng Y. D. (1994) Dose-dependent reduction of tissue loss and functional impairment after spinal cord trauma with the AMPA/kainate antagonist NBQX. J. Neurosci. 14, 6598-6607.
75. Wrathall J. R., Teng Y. D. and Choiniere D. (1996) Amelioration of functional deficits from spinal cord trauma with systemically administered NBQX, an antagonist of non-N-methyl-D-aspartate receptors. Exp. Neurol. 137, 119-126.
76. 2+ permeability in single rat retinal ganglion cells. Neuroscience 67, 177-188.