Kainic acid-induced apoptosis in rat striatum is associated with nuclear factor-κB activation

Journal of Neurochemistry

Volumn 74, Issue 2, 2000, Pages 647-658

  Nakai, Masami ^b   Qin, Zheng Hong ^b   Chen, Jiang Fan ^a   Wang, Yumei ^b   Chase, Thomas N ^b  

^a MASSACHUSETTS GENERAL HOSPITAL   (United States)

^b NATIONAL INSTITUTE OF NEUROLOGICAL DISORDERS AND STROKE   (United States)

Author keywords

Apoptosis; I B NF B p65 c Myc p53; Kainic acid; Neurodegeneration; Nuclear transcription factor B (NF B)

Indexed keywords

6 NITRO 7 SULFAMOYLBENZO[F]QUINOXALINE 2,3 DIONE; AMPA RECEPTOR; DIZOCILPINE; DNA FRAGMENT; GLUTAMATE DECARBOXYLASE; IMMUNOGLOBULIN ENHANCER BINDING PROTEIN; KAINIC ACID; KAINIC ACID RECEPTOR; MYC PROTEIN; N METHYL DEXTRO ASPARTIC ACID RECEPTOR; PROTEIN P53; SYNAPTOTAGMIN; TRANSCRIPTION FACTOR;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; APOPTOSIS; ARTICLE; CONTROLLED STUDY; CORPUS STRIATUM; HUNTINGTON CHOREA; IMMUNOHISTOCHEMISTRY; MALE; NERVE CELL NECROSIS; NERVE DEGENERATION; NONHUMAN; PRIORITY JOURNAL; PROTEIN BINDING; PROTEIN INDUCTION; PROTEIN LOCALIZATION; RAT; RECEPTOR BINDING;

ANIMALS; APOPTOSIS; CORPUS STRIATUM; DNA FRAGMENTATION; EXCITATORY AMINO ACID AGONISTS; GLUTAMATE DECARBOXYLASE; I-KAPPA B PROTEINS; ISOENZYMES; KAINIC ACID; MALE; NF-KAPPA B; NUCLEOSOMES; PEPTIDES; PROTO-ONCOGENE PROTEINS C-MYC; RATS; RATS, SPRAGUE-DAWLEY; RNA, MESSENGER; TRANSCRIPTION FACTORS; TUMOR SUPPRESSOR PROTEIN P53;

EID: 0033966324     PISSN: 00223042     EISSN: None     Source Type: Journal    
DOI: 10.1046/j.1471-4159.2000.740647.x     Document Type: Article

References (72)

1. Alkalay I., Yaron A., Hatzubai A., Orian A., Ciechanover A., and Ben-Neriah Y. (1995) Stimulation-dependent IκB phosphorylation marks the NF-κB inhibitor for degradation via the ubiquitin-proteasome pathway. Proc. Natl. Acad. Sci. USA 92, 10599-10603.
2. Baeuerle P. A. (1991) The inducible transcription activator NF-κB: regulation by distinct protein subunits. Biochim. Biophys. Acta 1072, 63-80.
3. Banasiak K. J. and Haddad G. G. (1998) Hypoxia-induced apoptosis: effect of hypoxic severity and role of p53 in neuronal cell death. Brain Res. 797, 295-304.
4. Barger S. W. and Mattson M. P. (1996a) Induction of neuroprotective κB-dependent transcription by secreted forms of the Alzheimer's β-amyloid precursor. Mol. Brain Res. 40, 116-126.
5. Barger S. W. and Mattson M. P. (1996b) Participation of gene expression in the protection against amyloid 8-peptide toxicity by the β-amyloid precursor protein. Ann. NY Acad. Sci. 777, 303-309.
6. Bazzett T. J., Becker J. B., Kaatz K. W., and Albin R. Z. (1993) Chronic intrastriatal dialytic administration of quinolinic acid produces selective neural degeneration. Exp. Neural. 120, 177-185.
7. Bonfoco E., Krainc D., Ankarcrona M., Nicotera P., and Lipton S. A. (1995) Apoptosis and necrosis: two distinct events induced, respectively, by mild and intense insults with N-methyl-D-aspartate or nitric oxide/superoxide in cortical cell cultures. Proc. Natl. Acad. Sci. USA 92, 7162-7166.
8. Castillo R. E., Malenka R. C., and Nicoll R. A. (1997) Kainate receptors mediate a slow postsynaptic current in hippocampal CA3 neurons. Nature 388, 182-186.
9. Cheng B., Christakos S., and Mattson M. P. (1994) Tumor necrosis factors protect neurons against metabolic-excitotoxic insults and promote maintenance of calcium homeostasis. Neuron 12, 139-153.
10. Choi D. W. (1988) Glutamate neurotoxicity and disease of the nervous system. Neuron 1, 623-634.
11. Choi D. W. (1992) Excitotoxic cell death. J. Neurobiol. 23, 1261-1276.
12. Chopp M., Li Y., Zhang Z. G., and Freytag S. O. (1992) p53 expression in brain after middle cerebral artery occlusion in the rat. Biochem. Biophys. Res. Commun. 182, 1201-1207.
13. Clemens J. A., Stephenson D. T., Smalstig E. B., Dixon E. P., and Little S. P. (1997) Global ischemia activates nuclear factor-κB in fore-brain neurons of rats. Stroke 28, 1073-1081.
14. Clemens J. A., Stephenson D. T., Smalstig E. B., Panetta J. A., and Little S. P. (1998) Drug-induced neuroprotection from global ischemia is associated with prevention of persistent but not transient activation of nuclear factor-κB in rats. Stroke 29, 177-182.
15. Coyle J. T. and Puttfarcken P. (1993) Oxidative stress, glutamate, and neurodegenerative disorders. Science 262, 689-695.
16. Coyle J. T. and Schwarcz R. (1976) Lesion of striatal neurons with kainic acid provides a model for Huntington's chorea. Nature 263, 244-246.
17. DiFiglia M. (1990) Excitotoxic injury of the neostriatum: a model for Huntington's disease. Trends Neurosci. 13, 286-289.
18. Du Y., Bales K. R., Dodel R. C., Hamilton-Byrd E., Horn J. W., Czilli D. L., Simmons L. K., Ni B., and Paul S. M. (1997) Activation of a caspase 3-related cysteine protease is required for glutamate-mediated apoptosis of cultured cerebellar granule neurons. Proc. Natl. Acad. Sci. USA 94, 11657-11662.
19. Duyao M. P., Buckler A. J., and Sonenshein G. E. (1990) Interaction of an NF-κB-like site upstream of the c-Myc promoter. Proc. Natl. Acad. Sci. USA 87, 4727-4731.
20. Ferrante R. J., Kowall N. W., Cipolloni P. B., Storey E., and Beal M. F. (1993) Excitotoxin lesions in primates as a model for Huntington's disease: histopathologic and neurochemical characterization. Exp. Neurol. 119, 46-71.
21. Filipkowski P. K., Hetman M., Kaminska B., and Kaczmarek L. (1994) DNA fragmentation in rat brain after intraperitoneal administration of kainate. Neuroreport 5, 1538-1540.
22. Gillardon F., Wicken H., and Zimmermann M. (1995) Up-regulation of bax and down-regulation of bcl-2 is associated with kainate-induced apoptosis in mouse brain. Neurosci. Lett. 192, 85-88.
23. Goodman Y. and Mattson M. P. (1996) Ceramide protects hippocampal neurons against excitotoxic and oxidative insults, and amyloid β-peptide toxicity. J. Neurochem. 66, 869-872.
24. Grilli M., Pizzi M., Memo M., and Spano P. (1996) Neuroprotection by aspirin and sodium salicylate through blockade of NF-κB activation. Science 274, 1383-1385.
25. Hollmann M. and Heinemann S. (1994) Cloned glutamate receptors. Annu. Rev. Neurosci. 17, 31-108.
26. Hughes P. E., Alexi T., Yoshida T., Schreiber S. S., and Knusel B. (1996) Excitotoxic lesion of rat brain with quinolinic acid induces expression of p53 messenger RNA and protein and p53-inducible genes Bax and Gadd-45 in brain areas showing DNA fragmentation. Neuroscience 74, 1143-1160.
27. Ikonomidou C., Bosch F., Miksa M., Bittigau P., Vockler J., Dikranian K., Tenkova T. I., Stefovska V., Turski L., and Olney J. W. (1999) Blockade of NMDA receptors and apoptotic neurodegeneration in the developing brain. Science 283, 70-74.
28. Johnson M. D., Kinoshita Y., Xiang H., Ghatan S., and Morrison R. S. (1999) Contribution of p53-dependent caspase activation to neuronal cell death declines with neuronal maturation. J. Neurosci. 19, 2996-3006.
29. Jordan J., Galino M. F., Prehn J. H. M., Weichselbaum R. R., Beckett M., Ghadge G. D., Roos R. P., Leiden J. M., and Miller R. J. (1997) p53 expression induces apoptosis in hippocampal pyramidal neuron cultures. J. Neurosci. 17, 1397-1405.
30. Kaku D. A., Goldberg M. P., and Choi D. W. (1991) Antagonism of non-NMDA receptors augments the neuroprotective effect of NMDA receptor blockade in cortical cultures subjected to prolonged deprivation of oxygen and glucose. Brain Res. 554, 344-347.
31. Kessler D. J., Duyao M. P., Spicer D. B., and Sonenshein G. E. (1992) NF-κB-like factors mediate interleukin 1 induction of c-myc gene transcription in fibroblasts. J. Exp. Med. 176, 787-792.
32. Kiedrowski L. (1998) The difference between mechanisms of kainate and glutamate excitotoxicity in vitro: osmotic lesions versus mitochondrial depolarization. Restor. Neurol. Neurosci. 12, 71-79.
33. 2+-mediated activation of c-Jun N-terminal kinase and nuclear factor κB by NMDA in cortical cell cultures. J. Neurochem. 71, 1390-1395.
34. Lee H., Arsura M., Wu M., Duyao M., Buckler A. J., and Sonenshein G. E. (1995) Role of Rel-related factors in control of c-myc gene transcription in receptor-mediated apoptosis of murine B cell WEHI 231 line. J. Exp. Med. 181, 1169-1177.
35. Lerma J. (1997) Kainate reveals its targets. Neuron 19, 1155-1158.
36. Li Y., Chopp M., Zhang Z. G., Zaloga C., Niewenhuis L., and Gautam S. (1994) p53-immunoreactive protein and p53 mRNA expression after transient middle cerebral artery occlusion in rats. Stroke 25, 849-856.
37. Lin K.-I., Lee S.-W., Narayanan R., Baraban J. M., and Hardwick J. M. (1995) Thiol agents and Bcl-2 identify an alphavirus-induced apoptosis pathway that requires activation of the transcription factor NF-κB. J. Cell Biol. 131, 1149-1161.
38. Marinovich M., Viviani B., Corsini E., Ghilardi F., and Galli C. L. (1996) NF-κB activation by triphenyltin triggers apoptosis in HL-60 cells. Exp. Cell Res. 226, 98-104.
39. Matsuoka Y., Kitamura Y., Okazaki M., Terai K., and Taniguchi T. (1999) Kainic acid-induced activation of nuclear factor-κB in rat hippocampus. Exp. Brain Res. 124, 215-222.
40. Mercurio F., Zhu H., Murray B. W., Shevchenko A., Bennett B. L., Li J. W., Young D. B., Barbosa M., Mann M., Manning A., and Rao A. (1997) IKK-1 and IKK-2: cytokine-activated IκB kinases essential for NF-κB activation. Science 278, 860-866.
41. Montpied P., Weller M., and Paul S. M. (1993) N-Methyl-D-aspartate receptor agonists decrease protooncogene Bcl-2 mRNA expression in cultured rat cerebellar granule neurons. Biochem. Biophys. Res. Commun. 195, 623-629.
42. Nakagomi T., Asai A., Kanemitsu H., Narita K., Kuchino Y., Tamura A., and Kirino T. (1996) Up-regulation of c-myc gene expression following focal ischemia in the rat brain. Neurol. Res. 18, 559-563.
43. Nakai M., Qin Z.-H., Wang Y., and Chase T. N. (1999) Free radical scavenger OPC-14117 attenuates quinolinic acid-induced NF-κB activation and apoptosis in rat striatum. Mol. Brain Res. 64, 59-68.
44. Olney J. W. (1989) Excitotoxicity and N-methyl-D-aspartate receptors. Drug Dev. Res. 17, 299-319.
45. Packham G. and Cleveland J. L. (1995) c-Myc and apoptosis. Biochim. Biophys. Acta 1242, 11-28.
46. Packham G., Porter C. W., and Cleveland J. L. (1996) c-Myc induces apoptosis and cell cycle progression by separable, yet overlapping, pathways. Oncogene 13, 461-469.
47. Pérez-Otaño I., McMillian M. K., Chen J., Bing G., Hong J. S., and Pennypacker K. R. (1996) Induction of NF-κB-like transcription factors in brain areas susceptible to kainate toxicity. Glia 16, 306-315.
48. Pittman R. N., Wang S., DiBenedetto A. J., and Mills J. C. (1993) A system for characterizing cellular and molecular events in programmed neuronal cell death. J. Neurosci. 13, 3669-3680.
49. Portera-Cailliau C., Hedreen J. C., Price D. L., and Koliatsos V. E. (1995) Evidence for apoptotic cell death in Huntington disease and excitotoxic animal models. J. Neurosci. 15, 3775-3787.
50. Portera-Cailliau C., Price D. L., and Martin L. J. (1997) Non-NMDA and NMDA receptor-mediated excitotoxic neuronal deaths in adult brain are morphologically distinct: further evidence for an apoptosis-necrosis continuum. J. Comp. Neurol. 378, 88-104.
51. Qin Z.-H., Zhang S.-P., and Weiss B. (1994) Dopaminergic and glutamatergic blocking drugs differentially regulate gene expression of glutamic acid decarboxylase in mouse brain. Mol. Brain Res. 21, 293-302.
52. Qin Z.-H., Wang Y., and Chase T. N. (1996) Stimulation of N-methyl-D-asparate receptors induces apoptosis in rat brain. Brain Res. 725, 166-177.
53. Qin Z.-H., Wang Y., Nakai M., and Chase T. N. (1998) Nuclear factor-κB contributes to excitotoxin-induced apoptosis in rat striatum. Mol. Pharmacol. 53, 33-42.
54. Qin Z.-H., Wang Y., Chen R.-W., Nakai M., Chuang D.-M., and Chase T. N. (1999) NF-κB nuclear translocation upregulates c-Myc and p53 expression during NMDA-mediated apoptosis in rat striatum. J. Neurosci. 19, 4023-4033.
55. Rothstein J. D., Jin L., Dykes-Hoberg M., and Kuncl R. W. (1993) Chronic inhibition of glutamate uptake produces a model of slow neurotoxicity. Proc. Natl. Acad. Sci. USA 90, 6591-6595.
56. Sakhi S., Bruce A., Sun N., Tocco G., and Baudry M. (1994) p53 induction is associated with neuronal damage in the central nervous system. Proc. Natl. Acad. Sci. USA 91, 7525-7529.
57. Sakhi S., Bruce A., Sun N., Tocco G., Baudry M., and Schreiber S. S. (1997) Induction of tumor suppressor p53 and DNA fragmentation in organotypic hippocampal cultures following excitotoxin treatment. Exp. Neurol. 145, 81-88.
58. Seeburg P. (1993) The molecular biology of mammalian glutamate receptor channels. Trends Pharmacol. Sci. 14, 297-303.
59. Sheardown M. J., Nielsen E. O., Hansen A. J., Jacobsen P., and Honore T. (1990) 2,3-Dihydroxy-6-nitro-7-sulfamoyl-benzo(F)quinoxaline: a neuroprotectant for cerebral ischemia. Science 247, 571-574.
60. 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.
61. Slack R. S., Belliveau D. J., Rosenberg M., Atwal J., Lochmuller H., Aloyz R., Haghighi A., Lach B., Seth P., Cooper E., and Miller F. D. (1996) Adenovirus-mediated gene transfer of the tumor suppressor, p53, induces apoptosis in postmitotic neurons. J. Cell Biol. 135, 1085-1096.
62. Spencer P. S., Nunn P. B., Hugon J., Ludolph A. C., Ross S. M., Roy D. N., and Robertson R. C. (1987) Guam amyotrophic lateral sclerosis-parkinsonism-dementia linked to a plant excitant neurotoxin. Science 237, 517-522.
63. 2+-dependent cleavage of DNA into kilobase pair fragments is responsible for the initial degradation of DNA in apoptosis. J. Biol. Chem. 269, 14857-14860.
64. Susel Z., Engber T. M., Kuo S., and Chase T. N. (1991) Prolonged infusion of quinolinic acid into rat striatum as an excitotoxic model of neurodegenerative disease. Neurosci. Lett. 121, 234-238.
65. Thanos D. and Maniatis T. (1995) NF-κB: a lesson in family values. Cell 80, 529-532.
66. Tomasevic G., Kamme F., Stubberod P., Wieloch M., and Wieloch T. (1999) The tumor suppressor p53 and its response gene p21WAF1/Cip1 are not markers of neuronal death following transient global cerebral ischemia. Neuroscience 90, 781-792.
67. Uberti D., Belloni M., Grilli M., Spano P., and Memo M. (1998) Induction of tumor-suppressor phosphoprotein p53 in the apoptosis of cultured rat cerebellar neurones triggered by excitatory amino acids. Eur. J. Neurosci. 10, 246-254.
68. Vignes M. and Collingridge G. L. (1997) The synaptic activation of kainate receptors. Nature 388, 179-182.
69. Wang Y., Qin Z.-H., Nakai M., Chen R.-W., Chuang D.-M., and Chase T. N. (1999) Co-stimulation of cyclic AMP-linked metabotropic receptors in rat striatum attenuates excitotoxin-induced NF-κB activation and apoptosis. Neuroscience 94, 1153-1162.
70. Weil R., Laurent-Winter C., and Israel A. (1997) Regulation of IκBβ degradation: similarities to and differences from IκBα. J. Biol. Chem. 272, 9942-9949.
71. 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.
72. Wu H. and Lozano G. (1994) NF-κB activation of p53, a potential mechanism for suppressing cell growth in response to stress. J. Biol. Chem. 269, 20067-20074.