Glutamate Receptors and Their Association with Other Neurochemical Parameters in Excitotoxicity

  • Akhlaq A. Farooqui
  • Wei-Yi Ong
  • Lloyd A. Horrocks


NMDA Receptor Glutamate Receptor Metabotropic Glutamate Receptor Kainic Acid Ornithine Decarboxylase 
These keywords were added by machine and not by the authors. This process is experimental and the keywords may be updated as the learning algorithm improves.


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  1. Acarin L., Paris J., Gonzàlez B., and Castellano B. (2002). Glial expression of small heat shock proteins following an excitotoxic lesion in the immature rat brain. Glia 38:1–14.PubMedGoogle Scholar
  2. Akbar M. T., Wells D. J., Latchman D. S., and De Belleroche J. (2001). Heat shock protein 27 shows a distinctive widespread spatial and temporal pattern of induction in CNS glial and neuronal cells compared to heat shock protein 70 and caspase 3 following kainate administration. Brain Res. Mol. Brain Res. 93: 148–163.PubMedGoogle Scholar
  3. Al Noori S. and Swann J. W. (2000). A role for sodium and chloride in kainic acid-induced beading of inhibitory interneuron dendrites. Neuroscience 101:337–348.PubMedGoogle Scholar
  4. Almeida A., Heales S. J., Bolanos J. P., and Medina J. M. (1998). Glutamate neurotoxicity is associated with nitric oxide-mediated mitochondrial dysfunction and glutathione depletion. Brain Res. 790:209–216.PubMedGoogle Scholar
  5. Atlante A., Gagliardi S., Minervini G. M., Ciotti M. T., Marra E., and Calissano P. (1997). Glutamate neurotoxicity in rat cerebellar granule cells: A major role for xanthine oxidase in oxygen radical formation. J. Neurochem. 68:2038–2045.PubMedGoogle Scholar
  6. Atlante A., Calissano P., Bobba A., Azzariti A., Marra E., and Passarella S. (2000). Cytochrome c is released from mitochondria in a reactive oxygen species (ROS)-dependent fashion and can operate as a ROS scavenger and as a respiratory substrate in cerebellar neurons undergoing excitotoxic death. J. Biol. Chem. 275:37159–37166.PubMedGoogle Scholar
  7. Beckman J. S., Ischiropoulos H., Zhu L., van der Woerd M., Smith C., Chen J., Harrison J., Martin J. C., and Tsai M. (1992). Kinetics of superoxide dismutase- and iron-catalyzed nitration of phenolics by peroxynitrite. Arch. Biochem. Biophys. 298:438–445.PubMedGoogle Scholar
  8. Blanc E. M., Kelly J. F., Mark R. J., Wäg G., and Mattson M. P. (1997). 4-hydroxynonenal, an aldehydic product of lipid peroxidation, impairs signal transduction associated with muscarinic acetylcholine and metabotropic glutamate receptors: Possible action on Gαq/11. J. Neurochem. 69:570–580.PubMedGoogle Scholar
  9. Bolanos J. P., Almeida A., Stewart V., Peuchen S., Land J. M., Clark J. B., and Heales S. J. (1997). Nitric oxide-mediated mitochondrial damage in the brain: mechanisms and implications for neurodegenerative diseases. J. Neurochem. 68:2227–2240.PubMedGoogle Scholar
  10. Boonplueang R., Akopian G., Stevenson F. F., Kuhlenkamp J. F., Lu S. C., Walsh J. P., and Andersen J. K. (2005). Increased susceptibility of glutathione peroxidase-1 transgenic mice to kainic acid-related seizure activity and hippocampal neuronal cell death. Exp. Neurol. 192:203–214.PubMedGoogle Scholar
  11. Boschert U., Merlo-Pich E., Higgins G., Roses A. D., and Catsicas S. (1999). Apolipoprotein E expression by neurons surviving excitotoxic stress. Neurobiol. Dis. 6:508–514.PubMedGoogle Scholar
  12. Brorson J. R., Manzolillo P. A., and Miller R. J. (1994). Ca2+ entry via AMPA/KA receptor and excitotoxicity in cultured cerebellar Purkinje cells. J. Neurosci. 14:187–197.PubMedGoogle Scholar
  13. Burdo J. R., Martin J., Menzies S. L., Dolan K. G., Romano M. A., Fletcher R. J., Garrick M. D., Garrick L. M., and Connor J. R. (1999). Cellular distribution of iron in the brain of the Belgrade rat. Neuroscience 93:1189–1196.PubMedGoogle Scholar
  14. Camandola S., Poli G., and Mattson M. P. (2000). The lipid peroxidation product 4-hydroxy-2,3-nonenal increases AP-1-binding activity through caspase activation in neurons. J. Neurochem. 74:159–168.PubMedGoogle Scholar
  15. Castagne V., Gautschi M., Lefevre K., Posada A., and Clarke P. G. H. (1999). Relationships between neuronal death and the cellular redox status. Focus on the developing nervous system. Prog. Neurobiol. 59:397–423.PubMedGoogle Scholar
  16. Chau L. Y. and Tai H. H. (1981). Release of arachidonate from diglyceride in human platelet requires the sequential action of a diacylglycerol lipase and a monoglyceride lipase. Biochem. Biophys. Res. Commun. 100:1688–1695.PubMedGoogle Scholar
  17. Ciani E. and Contestabile A. (1993). Ornithine decarboxylase is differentially induced by kainic acid during brain development in the rat. Brain Res. Dev. Brain Res. 71:258–260.PubMedGoogle Scholar
  18. Codazzi F., Di Cesare A., Chiulli N., Albanese A., Meyer T., Zacchetti D., and Grohovaz F. (2006). Synergistic control of protein kinase Cγ activity by ionotropic and metabotropic glutamate receptor inputs in hippocampal neurons. J. Neurosci. 26:3404–3411.PubMedGoogle Scholar
  19. Cohen M. R., Ramchand C. N., Sailer V., Fernandez M., McAmis W., Sridhara N., and Alston C. (1987). Detoxification enzymes following intrastriatal kainic acid. Neurochem. Res. 12:425–429.PubMedGoogle Scholar
  20. Coyle J. T. (1983). Neurotoxic action of kainic acid. J. Neurochem. 41:1–11.PubMedGoogle Scholar
  21. Cruise L., Ho L. K., Veitch K., Fuller G., and Morris B. J. (2000). Kainate receptors activate NF-κB via MAP kinase in striatal neurones. NeuroReport 11:395–398.PubMedGoogle Scholar
  22. Davis K. E., Straff D. J., Weinstein E. A., Bannerman P. G., Correale D. M., Rothstein J. D., and Robinson M. B. (1998). Multiple signaling pathways regulate cell surface expression and activity of the excitatory amino acid carrier 1 subtype of Glu transporter in C6 glioma. J. Neurosci. 18:2475–2485.PubMedGoogle Scholar
  23. de Vera N., Artigas F., Serratosa J., and Martìnez E. (1991). Changes in polyamine levels in rat brain after systemic kainic acid administration: relationship to convulsant activity and brain damage. J. Neurochem. 57:1–8.PubMedGoogle Scholar
  24. Dell’Acqua M. L., Smith K. E., Gorski J. A., Horne E. A., Gibson E. S., and Gomez L. L. (2006). Regulation of neuronal PKA signaling through AKAP targeting dynamics. Eur. J. Cell Biol. 85:627–633.PubMedGoogle Scholar
  25. Dietschy J. M. and Turley S. D. (2001). Cholesterol metabolism in the brain. Curr. Opin. Lipidol. 12:105–112.PubMedGoogle Scholar
  26. Djebaili M., Rondouin G., Baille V., and Bockaert J. (2000). p53 and Bax implication in NMDA induced-apoptosis in mouse hippocampus. NeuroReport 11:2973–2976.PubMedGoogle Scholar
  27. Djebaili M., De Bock F., Baille V., Bockaert J., and Rondouin G. (2002). Implication of p53 and caspase-3 in kainic acid but not in N-methyl-d-aspartic acid-induced apoptosis in organotypic hippocampal mouse cultures. Neurosci. Lett. 327:1–4.PubMedGoogle Scholar
  28. Dobrowsky R. T. and Carter B. D. (1998). Coupling of the p75 neurotrophin receptor to sphingolipid signaling. Ann. N.Y Acad. Sci. 845:32–45.PubMedGoogle Scholar
  29. Enslen H., Tokumitsu H., Stork P. J., Davis R. J., and Soderling T. R. (1996). Regulation of mitogen-activated protein kinases by a calcium/calmodulin-dependent protein kinase cascade. Proc. Natl. Acad. Sci. USA 93:10803–10808.PubMedGoogle Scholar
  30. Eriksson C., Winblad B., and Schultzberg M. (1998). Kainic acid-induced expression of interleukin-1 receptor antagonist mRNA in the rat brain. Brain Res. Mol. Brain Res. 58:195–208.PubMedGoogle Scholar
  31. Fage D., Voltz C., Scatton B., and Carter C. (1992). Selective release of spermine and spermidine from the rat striatum by N-methyl-D-aspartate receptor activation in vivo. J. Neurochem. 58:2170–2175.PubMedGoogle Scholar
  32. Faherty C. J., Xanthoudakis S., and Smeyne R. J. (1999). Caspase-3-dependent neuronal death in the hippocampus following kainic acid treatment. Brain Res. Mol. Brain Res. 70:159–163.PubMedGoogle Scholar
  33. Farooqui A. A. and Horrocks L. A. (1991). Excitatory amino acid receptors, neural membrane phospholipid metabolism and neurological disorders. Brain Res. Rev. 16:171–191.PubMedGoogle Scholar
  34. Farooqui A. A. and Horrocks L. A. (1994). Excitotoxicity and neurological disorders: involvement of membrane phospholipids. Int. Rev. Neurobiol. 36:267–323.PubMedGoogle Scholar
  35. Farooqui A. A. and Horrocks L. A. (2006). Phospholipase A2-generated lipid mediators in the brain: the good, the bad, and the ugly. Neuroscientist 12:245–260.PubMedGoogle Scholar
  36. Farooqui A. A., Anderson D. K., and Horrocks L. A. (1993). Effect of glutamate and its analogs on diacylglycerol and monoacylglycerol lipase activities of neuron-enriched cultures. Brain Res. 604:180–184.PubMedGoogle Scholar
  37. Farooqui A. A., Horrocks L. A., and Farooqui T. (2000). Deacylation and reacylation of neural membrane glycerophospholipids. J. Mol. Neurosci. 14:123–135.PubMedGoogle Scholar
  38. Farooqui A. A., Ong W. Y., and Horrocks L. A. (2004). Biochemical aspects of neurodegeneration in human brain: involvement of neural membrane phospholipids and phospholipases A2. Neurochem. Res. 29:1961–1977.PubMedGoogle Scholar
  39. Furukawa K. and Mattson M. P. (1998). The transcription factor NF-κB mediates increases in calcium currents and decreases in NMDA- and AMPA/kainate-induced currents induced by tumor necrosis factor-α in hippocampal neurons. J. Neurochem. 70:1876–1886.PubMedGoogle Scholar
  40. Gall C. (1988). Seizures induce dramatic and distinctly different changes in enkephalin, dynorphin, and CCK immunoreactivities in mouse hippocampal mossy fibers. J. Neurosci. 8:1852–1862.PubMedGoogle Scholar
  41. González M. I., Susarla B. T. S., and Robinson M. B. (2005). Evidence that protein kinase Cα interacts with and regulates the glial glutamate transporter GLT-1. J. Neurochem. 94:1180–1188.PubMedGoogle Scholar
  42. 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.PubMedGoogle Scholar
  43. Guan X. L., He X., Ong W. Y., Yeo W. K., Shui G. H., and Wenk M. R. (2006). Non-targeted profiling of lipids during kainate-induced neuronal injury. FASEB J. 20:1152–1161.PubMedGoogle Scholar
  44. Guglielmetti F., Rattray M., Baldessari S., Butelli E., Samanin R., and Bendotti C. (1997). Selective up-regulation of protein kinase C epsilon in granule cells after kainic acid-induced seizures in rat. Brain Res. Mol. Brain Res. 49:188–196.PubMedGoogle Scholar
  45. Gulbins E. and Li P. L. (2006). Physiological and pathophysiological aspects of ceramide. Am. J. Physiol. Regul. Integr. Comp. Physiol. 290:R11–R26.PubMedGoogle Scholar
  46. Gunshin H., Mackenzie B., Berger U. V., Gunshin Y., Romero M. F., Boron W. F., Nussberger S., Gollan J. L., and Hediger M. A. (1997). Cloning and characterization of a mammalian proton-coupled metal-ion transporter. Nature 388:482–488.PubMedGoogle Scholar
  47. Hanada K. (2003). Serine palmitoyltransferase, a key enzyme of sphingolipid metabolism. Biochim. Biophys. Acta 1632:16–30.PubMedGoogle Scholar
  48. Hashimoto K., Watanabe K., Nishimura T., Iyo M., Shirayama Y., and Minabe Y. (1998). Behavioral changes and expression of heat shock protein hsp-70 mRNA, brain-derived neurotrophic factor mRNA, and cyclooxygenase-2 mRNA in rat brain following seizures induced by systemic administration of kainic acid. Brain Res. 804:212–223.PubMedGoogle Scholar
  49. He X., Jenner A. M., Ong W. Y., Farooqui A. A., and Patel S. C. (2006). Lovastatin modulates increased cholesterol and oxysterol levels and has a neuroprotective effect on rat hippocampal neurons after kainate injury. J. Neuropathol. Exp. Neurol. 65:652–663.PubMedGoogle Scholar
  50. He X., Guan X. L., Ong W. Y., Farooqui A. A., and Wenk M. R. (2007). Expression, activity, and role of serine palmitoyltransferase in the rat hippocampus after kainate injury. J. Neurosci. Res. 85:423–432.PubMedGoogle Scholar
  51. Hjelle O. P., Chaudhry F. A., and Ottersen O. P. (1994). Antisera to glutathione: characterization and immunocytochemical application to the rat cerebellum. Eur. J. Neurosci. 6:793–804.PubMedGoogle Scholar
  52. Huang J. and Philbert M. A. (1995). Distribution of glutathione and glutathione-related enzyme systems in mitochondria and cytosol of cultured cerebellar astrocytes and granule cells. Brain Res. 680:16–22.PubMedGoogle Scholar
  53. Huang E., Ong W. Y., and Connor J. R. (2004). Distribution of divalent metal transporter-1 in the monkey basal ganglia. Neuroscience 128:487–496.PubMedGoogle Scholar
  54. Huang E., Ong W. Y., Go M. L., and Garey L. J. (2005). Heme oxygenase-1 activity after excitotoxic injury: immunohistochemical localization of bilirubin in neurons and astrocytes and deleterious effects of heme oxygenase inhibition on neuronal survival after kainate treatment. J. Neurosci. Res. 80:268–278.PubMedGoogle Scholar
  55. Humpel C., Lippoldt A., Chadi G., Ganten D., Olson L., and Fuxe K. (1993). Fast and widespread increase of basic fibroblast growth factor messenger RNA and protein in the forebrain after kainate-induced seizures. Neuroscience 57:913–922.PubMedGoogle Scholar
  56. Janaky R., Ogita K., Pasqualotto B. A., Bains J. S., Oja S. S., Yoneda Y., and Shaw C. A. (1999). Glutathione and signal transduction in the mammalian CNS. J. Neurochem. 73:889–902.PubMedGoogle Scholar
  57. Jenkinson A. M., Collins A. R., Duthie S. J., Wahle K. W. J., and Duthie G. G. (1999). The effect of increased intakes of polyunsaturated fatty acids and vitamin E on DNA damage in human lymphocytes. FASEB J. 13:2138–2142.PubMedGoogle Scholar
  58. Kim H., Bing G., Jhoo W., Ko K. H., Kim W. K., Suh J. H., Kim S. J., Kato K., and Hong J. S. (2000a). Changes of hippocampal Cu/Zn-superoxide dismutase after kainate treatment in the rat. Brain Res. 853:215–226.Google Scholar
  59. Kim H. C., Jhoo W. K., Kim W. K., Suh J. H., Shin E. J., Kato K., and Ho K. K. (2000b). An immunocytochemical study of mitochondrial manganese-superoxide dismutase in the rat hippocampus after kainate administration. Neurosci. Lett. 281:65–68.Google Scholar
  60. Kim H. C., Bing G., Kim S. J., Jhoo W. K., Shin E. J., Bok W. M., Ko K. H., Kim W. K., Flanders K. C., Choi S. G., and Hong J. S. (2002). Kainate treatment alters TGF-β3 gene expression in the rat hippocampus. Brain Res. Mol. Brain Res. 108:60–70.PubMedGoogle Scholar
  61. Kim D., Kim E. H., Kim C., Sun W., Kim H. J., Uhm C. S., Park S. H., and Kim H. (2003). Differential regulation of metallothionein-I, II, and III mRNA expression in the rat brain following kainic acid treatment. NeuroReport 14:679–682.PubMedGoogle Scholar
  62. Kim S. Y., Min D. S., Choi J. S., Choi Y. S., Park H. J., Sung K. W., Kim J., and Lee M. Y. (2004). Differential expression of phospholipase D isozymes in the hippocampus following kainic acid-induced seizures. J. Neuropathol. Exp. Neurol. 63:812–820.PubMedGoogle Scholar
  63. Kim W. H., Choi C. H., Kang S. K., Kwon C. H., and Kim Y. K. (2005). Ceramide induces non-apoptotic cell death in human glioma cells. Neurochem. Res. 30:969–979.PubMedGoogle Scholar
  64. Ko H. W., Park K. Y., Kim H., Han P. L., Kim Y. U., Gwag B. J., and Choi E. J. (1998). Ca2+ -mediated activation of c-Jun N-terminal kinase and nuclear factor κB by NMDA in cortical cell cultures. J. Neurochem. 71:1390–1395.PubMedGoogle Scholar
  65. Kondo T., Kakegawa W., and Yuzaki M. (2005). Induction of long-term depression and phosphorylation of the δ2 glutamate receptor by protein kinase C in cerebellar slices. Eur. J. Neurosci. 22:1817–1820.PubMedGoogle Scholar
  66. Kordas K. and Stoltzfus R. J. (2004). New evidence of iron and zinc interplay at the enterocyte and neural tissues. J. Nutr. 134:1295–1298.PubMedGoogle Scholar
  67. Kotecha S. A. and MacDonald J. F. (2003). Signaling molecules and receptor transduction cascades that regulate NMDA receptor-mediated synaptic transmission. In: Bradley R. J., Harris R. A., and Jenner P. (eds.), International Review of Neurobiology, Vol 54. International Review of Neurobiology Academic Press Inc, San Diego, pp. 53–108.Google Scholar
  68. Lauderback C. M., Hackett J. M., Huang F. F., Keller J. N., Szweda L. I., Markesbery W. R., and Butterfield D. A. (2001). The glial glutamate transporter, GLT-1, is oxidatively modified by 4-hydroxy-2-nonenal in the Alzheimer’s disease brain: the role of Aβ1-42. J. Neurochem. 78:413–416.PubMedGoogle Scholar
  69. Lee M. C., Ban S. S., Woo Y. J., and Kim S. U. (2001a). Calcium/calmodulin kinase II activity of hippocampus in kainate-induced epilepsy. J. Korean Med. Sci. 16:643–648.Google Scholar
  70. Lee M. C., Rho J. L., Kim M. K., Woo Y. J., Kim J. H., Nam S. C., Suh J. J., Chung W. K., Moon J. D., and Kim H. I. (2001b). c-JUN expression and apoptotic cell death in kainate-induced temporal lobe epilepsy. J. Korean Med. Sci. 16:649–656.Google Scholar
  71. Lerea L. S., Carlson N. G., and McNamara J. O. (1995). N-methyl-D-aspartate receptors activate transcription of c-fos and NGFI-A by distinct phospholipase A2-requiring intracellular signaling pathways. Molec. Pharmacol. 47:1119–1125.Google Scholar
  72. Leslie S. W., Brown L. M., Trent R. D., Lee Y. H., Morris J. L., Jones T. W., Randall P. K., Lau S. S., and Monks T. J. (1992). Stimulation of N-methyl-D-aspartate receptor-mediated calcium entry into dissociated neurons by reduced and oxidized glutathione. Mol. Pharmacol. 41:308–314.PubMedGoogle Scholar
  73. Liang L. P., Ho Y. S., and Patel M. (2000). Mitochondrial superoxide production in kainate-induced hippocampal damage. Neuroscience 101:563–570.PubMedGoogle Scholar
  74. Liu H. N., Larocca J. N., and Almazan G. (1999). Molecular pathways mediating activation by kainate of mitogen-activated protein kinase in oligodendrocyte progenitors. Brain Res. Mol. Brain Res. 66:50–61.PubMedGoogle Scholar
  75. Liu W., Liu R., Schreiber S. S., and Baudry M. (2001). Role of polyamine metabolism in kainic acid excitotoxicity in organotypic hippocampal slice cultures. J. Neurochem. 79:976–984.PubMedGoogle Scholar
  76. Lombardi G., Szekely A. M., Bristol L. A., Guidotti A., and Manev H. (1993). Induction of ornithine decarboxylase by N-methyl-D-aspartate receptor activation is unrelated to potentiation of glutamate excitotoxicity by polyamines in cerebellar granule neurons. J. Neurochem. 60:1317–1324.PubMedGoogle Scholar
  77. Lu C., Chan S. L., Haughey N., Lee W. T., and Mattson M. P. (2001a). Selective and biphasic effect of the membrane lipid peroxidation product 4-hydroxy-2,3-nonenal on N-methyl-D-aspartate channels. J. Neurochem. 78:577–589.Google Scholar
  78. Lu X. R., Ong W. Y., Halliwell B., Horrocks L. A., and Farooqui A. A. (2001b). Differential effects of calcium-dependent and calcium-independent phospholipase A2 inhibitors on kainate-induced neuronal injury in rat hippocampal slices. Free Radical Biol. Med. 30:1263–1273.Google Scholar
  79. Mahley R. W. (1988). Apoprotein E: cholesterol transport protein with expanding role in cell biology. Science 240:622–630.PubMedGoogle Scholar
  80. Manev H., Uz T., and Qu T. Y. (2000). 5-Lipoxygenase and cyclooxygenase mRNA expression in rat hippocampus: early response to glutamate receptor activation by kainate. Exp. Gerontol. 35:1201–1209.PubMedGoogle Scholar
  81. Marchesini N. and Hannun Y. A. (2004). Acid and neutral sphingomyelinases: roles and mechanisms of regulation. Biochem. Cell Biol. 82:27–44.PubMedGoogle Scholar
  82. Mark R. J., Lovell M. A., Markesbery W. R., Uchida K., and Mattson M. P. (1997). A role for 4-hydroxynonenal, an aldehydic product of lipid peroxidation, in disruption of ion homeostasis and neuronal death induced by amyloid β-peptide. J. Neurochem. 68:255–264.PubMedGoogle Scholar
  83. Martins R. A., Silveira M. S., Curado M. R., Police A. I., and Linden R. (2005). NMDA receptor activation modulates programmed cell death during early post-natal retinal development: a BDNF-dependent mechanism. J. Neurochem. 95:244–253.PubMedGoogle Scholar
  84. Matute C., Domercq M., and Sánchez-Gómez M. V. (2006). Glutamate-mediated glial injury: Mechanisms and clinical importance. Glia 53:212–224.PubMedGoogle Scholar
  85. Maybodi L., Pow D. V., Kharazia V. N., and Weinberg R. J. (1999). Immunocytochemical demonstration of reduced glutathione in neurons of rat forebrain. Brain Res. 817:199–205.PubMedGoogle Scholar
  86. McCusker R. H., McCrea K., Zunich S., Dantzer R., Broussard S. R., Johnson R. W., and Kelley K. W. (2006). Insulin-like growth factor-I enhances the biological activity of brain-derived neurotrophic factor on cerebrocortical neurons. J. Neuroimmunol. 179:186–190.PubMedGoogle Scholar
  87. McInnis J., Wang C., Anastasio N., Hultman M., Ye Y., Salvemini D., and Johnson K. M. (2002). The role of superoxide and nuclear factor-κB signaling in N-methyl-D-aspartate-induced necrosis and apoptosis. J. Pharmacol. Exp. Ther. 301:478–487.PubMedGoogle Scholar
  88. McNamara R. K. and Lenox R. H. (2000). Differential regulation of primary protein kinase C substrate (MARCKS, MLP, GAP-43, RC3) mRNAs in the hippocampus during kainic acid-induced seizures and synaptic reorganization. J. Neurosci. Res. 62:416–426.PubMedGoogle Scholar
  89. McNamara R. K., Wees E. A., and Lenox R. H. (1999). Differential subcellular redistribution of protein kinase C isozymes in the rat hippocampus induced by kainic acid. J. Neurochem. 72:1735–1743.PubMedGoogle Scholar
  90. Milatovic D., Gupta R. C., and Dettbarn W. D. (2002). Involvement of nitric oxide in kainic acid-induced excitotoxicity in rat brain. Brain Res. 957:330–337.PubMedGoogle Scholar
  91. Minami M., Kuraishi Y., and Satoh M. (1991). Effects of kainic acid on messenger RNA levels of IL-1β, IL-6, TNF-α and LIF in the rat brain. Biochem. Biophys. Res. Commun. 176:593–598.PubMedGoogle Scholar
  92. Morais Cabral J. H., Atkins G. L., Sánchez L. M., López-Baodo Y. S., López-Oton C., and Sawyer L. (1995). Arachidonic acid binds to apolipoprotein D: Implications for the protein’s function. FEBS Lett. 366:53–56.PubMedGoogle Scholar
  93. Moreno J. J. and Pryor W. A. (1992). Inactivation of alpha 1-proteinase inhibitor by peroxynitrite. Chem. Res. Toxicol. 5:425–431.PubMedGoogle Scholar
  94. Moriguchi S., Han F., Nakagawasai O., Tadano T., and Fukunaga K. (2006). Decreased calcium/calmodulin-dependent protein kinase II and protein kinase C activities mediate impairment of hippocampal long-term potentiation in the olfactory bulbectomized mice. J. Neurochem. 97:22–29.PubMedGoogle Scholar
  95. Morrison R. S., Wenzel H. J., Kinoshita Y., Robbins C. A., Donehower L. A., and Schwartzkroin P. A. (1996). Loss of the p53 tumor suppressor gene protects neurons from kainate-induced cell death. J. Neurosci. 16:1337–1345.PubMedGoogle Scholar
  96. Nadkarni D. V. and Sayre L. M. (1995). Structural definition of early lysine and histidine adduction chemistry of 4-hydroxynonenal. Chem. Res. Toxicol. 8:284–291.PubMedGoogle Scholar
  97. Najm I., el-Skaf G., Massicotte G., Vanderklish P., Lynch G., and Baudry M. (1992). Changes in polyamine levels and spectrin degradation following kainate-induced seizure activity: effect of difluoromethylornithine. Exp. Neurol. 116:345–354.PubMedGoogle Scholar
  98. Nakamura H., Hirabayashi T., Shimizu M., and Murayama T. (2006). Ceramide-1-phosphate activates cytosolic phospholipase A2α directly and by PKC pathway. Biochem. Pharmacol. 71:850–857.PubMedGoogle Scholar
  99. Ong W. Y., Hu C. Y., Hjelle O. P., Ottersen O. P., and Halliwell B. (2000a). Changes in glutathione in the hippocampus of rats injected with kainate: depletion in neurons and upregulation in glia. Exp. Brain Res. 132:510–516.Google Scholar
  100. Ong W. Y., Lu X. R., Hu C. Y., and Halliwell B. (2000b). Distribution of hydroxynonenal-modified proteins in the kainate-lesioned rat hippocampus: evidence that hydroxynonenal formation precedes neuronal cell death. Free Radic. Biol. Med. 28:1214–1221.Google Scholar
  101. Ong W. Y., Goh E. W. S., Lu X. R., Farooqui A. A., Patel S. C., and Halliwell B. (2003). Increase in cholesterol and cholesterol oxidation products, and role of cholesterol oxidation products in kainate-induced neuronal injury. Brain Path. 13:250–262.Google Scholar
  102. Ong W. Y., He X., Chua L. H., and Ong C. N. (2006). Increased uptake of divalent metals lead and cadmium into the brain after kainite-induced neuronal injury. Exp. Brain Res. 173:468–474.PubMedGoogle Scholar
  103. Oyama Y., Sadakata C., Chikahisa L., Nagano T., and Okazaki E. (1997). Flow-cytometric analysis on kainate-induced decrease in the cellular content of non-protein thiols in dissociated rat brain neurons. Brain Res. 760:277–280.PubMedGoogle Scholar
  104. Paradis É., Clavel S., Julien P., Murthy M. R. V., de Bilbao F., Arsenijevic D., Giannakopoulos P., Vallet P., and Richard D. (2004). Lipoprotein lipase and endothelial lipase expression in mouse brain: regional distribution and selective induction following kainic acid-induced lesion and focal cerebral ischemia. Neurobiol. Dis. 15:312–325.PubMedGoogle Scholar
  105. Parihar M. S. and Hemnani T. (2003). Phenolic antioxidants attenuate hippocampal neuronal cell damage against kainic acid induced excitotoxicity. J. Biosci. 28:121–128.PubMedGoogle Scholar
  106. Parihar M. S. and Hemnani T. (2004). Experimental excitotoxicity provokes oxidative damage in mice brain and attenuation by extract of Asparagus racemosus. J. Neural Transm. 111:1–12.PubMedGoogle Scholar
  107. Park D. S., Obeidat A., Giovanni A., and Greene L. A. (2000). Cell cycle regulators in neuronal death evoked by excitotoxic stress: implications for neurodegeneration and its treatment. Neurobiol. Aging 21:771–781.PubMedGoogle Scholar
  108. Patel S. C., Asotra K., Patel Y. C., McConathy W. J., Patel R. C., and Suresh S. (1995). Astrocytes synthesize and secrete the lipophilic ligand carrier apolipoprotein D. NeuroReport 6:653–657.PubMedGoogle Scholar
  109. Pepicelli O., Fedele E., Bonanno G., Raiteri M., Ajmone-Cat M. A., Greco A., Levi G., and Minghetti L. (2002). In vivo activation of N-methyl-D-aspartate receptors in the rat hippocampus increases prostaglandin E2 extracellular levels and triggers lipid peroxidation through cyclooxygenase-mediated mechanisms. J. Neurochem. 81:1028–1034.PubMedGoogle Scholar
  110. Perez Y., Morin F., Beaulieu C., and Lacaille J. C. (1996). Axonal sprouting of CA1 pyramidal cells in hyperexcitable hippocampal slices of kainate-treated rats. Eur. J. Neurosci. 8:736–748.PubMedGoogle Scholar
  111. Pfrieger F. W. (2003). Outsourcing in the brain: do neurons depend on cholesterol delivery by astrocytes? BioEssays 25:72–78.PubMedGoogle Scholar
  112. Phillis J. W., Horrocks L. A., and Farooqui A. A. (2006). Cyclooxygenases, lipoxygenases, and epoxygenases in CNS: Their role and involvement in neurological disorders. Brain Res. Rev. 52:201–243.PubMedGoogle Scholar
  113. Popovici T., Represa A., Crepel V., Barbin G., Beaudoin M., and Ben Ari Y. (1990). Effects of kainic acid-induced seizures and ischemia on c-fos-like proteins in rat brain. Brain Res. 536:183–194.PubMedGoogle Scholar
  114. Pryor W. A. and Squadrito G. L. (1995). The chemistry of peroxynitrite: a product from the reaction of nitric oxide with superoxide. Am. J. Physiol 268:L699–L722.PubMedGoogle Scholar
  115. Qi W., Reiter R. J., Tan D. X., Manchester L. C., Siu A. W., and Garcia J. J. (2000). Increased levels of oxidatively damaged DNA induced by chromium(III) and H2O2: protection by melatonin and related molecules. J. Pineal Res. 29:54–61.PubMedGoogle Scholar
  116. Qin Z. H., Chen R. W., Wang Y., Nakai M., Chuang D. M., and Chase T. N. (1999). Nuclear factor kB nuclear translocation upregulates c-Myc and p53 expression during NMDA receptor-mediated apoptosis in rat striatum. J. Neurosci. 19:4023–4033.PubMedGoogle Scholar
  117. Radi R., Beckman J. S., Bush K. M., and Freeman B. A. (1991a). Peroxynitrite oxidation of sulfhydryls. The cytotoxic potential of superoxide and nitric oxide. J. Biol. Chem. 266:4244–4250.Google Scholar
  118. Radi R., Beckman J. S., Bush K. M., and Freeman B. A. (1991b). Peroxynitrite-induced membrane lipid peroxidation: the cytotoxic potential of superoxide and nitric oxide. Arch. Biochem. Biophys. 288:481–487.Google Scholar
  119. Reed L. J. and De Belleroche J. (1990). Induction of ornithine decarboxylase in cerebral cortex by excitotoxin lesion of nucleus basalis: association with postsynaptic responsiveness and N-methyl-D-aspartate receptor activation. J. Neurochem. 55:780–787.PubMedGoogle Scholar
  120. Retz K. C. and Coyle J. T. (1982). Effects of kainic acid on high-energy metabolites in the mouse striatum. J. Neurochem. 38:196–203.PubMedGoogle Scholar
  121. Rodríguez-Moreno A. and Lerma J. (1998). Kainate receptor modulation of GABA release involves a metabotropic function. Neuron 20:1211–1218.PubMedGoogle Scholar
  122. Rossler O. G., Bauer I., Chung H. Y., and Thiel G. (2004). Glutamate-induced cell death of immortalized murine hippocampal neurons: neuroprotective activity of heme oxygenase-1, heat shock protein 70, and sodium selenite. Neurosci. Lett. 362:253–257.PubMedGoogle Scholar
  123. Rothstein J. D. and Kuncl R. W. (1995). Neuroprotective strategies in a model of chronic glutamate-mediated motor neuron toxicity. J. Neurochem. 65:643–651.PubMedGoogle Scholar
  124. Rusanescu G., Qi H., Thomas S. M., Brugge J. S., and Halegoua S. (1995). Calcium influx induces neurite growth through a Src-Ras signaling cassette. Neuron 15:1415–1425.PubMedGoogle Scholar
  125. Sakhi S., Bruce A., Sun N., Tocco G., Baudry M., and Schreiber S. S. (1994). p53 induction is associated with neuronal damage in the central nervous system. Proc. Natl. Acad. Sci. USA 91:7525–7529.PubMedGoogle Scholar
  126. Sandhya T. L., Ong W. Y., Horrocks L. A., and Farooqui A. A. (1998). A light and electron microscopic study of cytoplasmic phospholipase A2 and cyclooxygenase-2 in the hippocampus after kainate lesions. Brain Res. 788:223–231.PubMedGoogle Scholar
  127. Sato K. and Matsuki N. (2002). A 72 kDa heat shock protein is protective against the selective vulnerability of CA1 neurons and is essential for the tolerance exhibited by CA3 neurons in the hippocampus. Neuroscience 109:745–756.PubMedGoogle Scholar
  128. Shoham S. and Ebstein R. P. (1997). The distribution of β-amyloid precursor protein in rat cortex after systemic kainate-induced seizures. Exp. Neurol. 147:361–376.PubMedGoogle Scholar
  129. Siskind L. J. (2005). Mitochondrial ceramide and the induction of apoptosis. J. Bioenerg. Biomembr. 37:143–153.PubMedGoogle Scholar
  130. Sohl G., Guldenagel M., Beck H., Teubner B., Traub O., Gutierrez R., Heinemann U., and Willecke K. (2000). Expression of connexin genes in hippocampus of kainate-treated and kindled rats under conditions of experimental epilepsy. Brain Res. Mol. Brain Res. 83:44–51.PubMedGoogle Scholar
  131. Sola C., Tusell J. M., and Serratosa J. (1997). Calmodulin is expressed by reactive microglia in the hippocampus of kainic acid-treated mice. Neuroscience 81:699–705.PubMedGoogle Scholar
  132. Sorger P. K. (1991). Heat shock factor and the heat shock response. Cell 65:363–366.PubMedGoogle Scholar
  133. Soule J., Messaoudi E., and Bramham C. R. (2006). Brain-derived neurotrophic factor and control of synaptic consolidation in the adult brain. Biochem. Soc. Trans. 34:600–604.PubMedGoogle Scholar
  134. Sperk G. (1994). Kainic acid seizures in the rat. Prog. Neurobiol. 42:1–32.PubMedGoogle Scholar
  135. Stein-Behrens B. A., Elliott E. M., Miller C. A., Schilling J. W., Newcombe R., and Sapolsky R. M. (1992). Glucocorticoids exacerbate kainic acid-induced extracellular accumulation of excitatory amino acids in the rat hippocampus. J. Neurochem. 58: 1730–1735.PubMedGoogle Scholar
  136. Stoica B. A., Movsesyan V. A., Knoblach S. M., and Faden A. I. (2005). Ceramide induces neuronal apoptosis through mitogen-activated protein kinases and causes release of multiple mitochondrial proteins. Mol. Cell Neurosci. 29:355–371.PubMedGoogle Scholar
  137. Sun A. Y., Cheng Y., Bu Q., and Oldfield F. (1992). The biochemical mechanisms of the excitotoxicity of kainic acid. Free radical formation. Mol. Chem. Neuropathol. 17:51–63.PubMedGoogle Scholar
  138. Tamagno E., Robino G., Obbili A., Bardini P., Aragno M., Parola M., and Danni O. (2003). H2O2 and 4-hydroxynonenal mediate amyloid beta-induced neuronal apoptosis by activating JNKs and p38MAPK. Exp. Neurol. 180:144–155.PubMedGoogle Scholar
  139. Tatsukawa T., Chimura T., Miyakawa H., and Yamaguchi K. (2006). Involvement of basal protein kinase C and extracellular signal-regulated kinase 1/2 activities in constitutive internalization of AMPA receptors in cerebellar Purkinje cells. J. Neurosci. 26:4820–4825.PubMedGoogle Scholar
  140. Thorburne S. K. and Juurlink B. H. (1996). Low glutathione and high iron govern the susceptibility of oligodendroglial precursors to oxidative stress. J. Neurochem. 67:1014–1022.PubMedGoogle Scholar
  141. van der Brug M. P., Goodenough S., and Wilce P. (2002). Kainic acid induces 14-3-3 ζ expression in distinct regions of rat brain. Brain Res. 956:110–115.PubMedGoogle Scholar
  142. Vance J. E., Pan D., Campenot R. B., Bussière M., and Vance D. E. (1994). Evidence that the major membrane lipids, except cholesterol, are made in axons of cultured rat sympathetic neurons. J. Neurochem. 62:329–337.PubMedGoogle Scholar
  143. Varga V., Jenei Z., Janaky R., Saransaari P., and Oja S. S. (1997). Glutathione is an endogenous ligand of rat brain N-methyl-D-aspartate (NMDA) and 2-amino-3-hydroxy-5-methyl-4-isoxazolepropionate (AMPA) receptors. Neurochem. Res. 22:1165–1171.PubMedGoogle Scholar
  144. Verdaguer E., García-Jordà E., Canudas A. M., Domìnguez E., Jiménez A., Pubill D., Escubedo E., Camarasa Pallàs Mercè J., and Camins A. (2002). Kainic acid-induced apoptosis in cerebellar granule neurons: an attempt at cell cycle re-entry. NeuroReport 13:413–416.PubMedGoogle Scholar
  145. Vezzani A., Civenni G., Rizzi M., Monno A., Messali S., and Samanin R. (1994). Enhanced neuropeptide Y release in the hippocampus is associated with chronic seizure susceptibility in kainic acid treated rats. Brain Res. 660:138–143.PubMedGoogle Scholar
  146. Wang X. S., Ong W. Y., and Connor J. R. (2001). A light and electron microscopic study of the iron transporter protein DMT-1 in the monkey cerebral neocortex and hippocampus. J. Neurocytol. 30:353–360.PubMedGoogle Scholar
  147. Wang X. S., Ong W. Y., and Connor J. R. (2002). A light and electron microscopic study of divalent metal transporter-1 distribution in the rat hippocampus, after kainate-induced neuronal injury. Exp. Neurol. 177:193–201.PubMedGoogle Scholar
  148. Wang J. Q., Arora A., Yang L., Parelkar N. K., Zhang G., Liu X., Choe E. S., and Mao L. (2005a). Phosphorylation of AMPA receptors: mechanisms and synaptic plasticity. Mol. Neurobiol. 32:237–249.Google Scholar
  149. Wang Q., Yu S., Simonyi A., Sun G. Y., and Sun A. Y. (2005b). Kainic acid-mediated excitotoxicity as a model for neurodegeneration. Mol. Neurobiol. 31:3–16.Google Scholar
  150. Wang J. Q., Liu X., Zhang G., Parelkar N. K., Arora A., Haines M., Fibuch E. E., and Mao L. (2006). Phosphorylation of glutamate receptors: a potential mechanism for the regulation of receptor function and psychostimulant action. J. Neurosci. Res. 84:1621–1629.PubMedGoogle Scholar
  151. Wang J. Q., Fibuch E. E., and Mao L. (2007). Regulation of mitogen-activated protein kinases by glutamate receptors. J. Neurochem. 100:1–11.PubMedGoogle Scholar
  152. Weber G. F. (1999). Final common pathways in neurodegenerative diseases: regulatory role of the glutathione cycle. Neurosci. Biobehav. Rev. 23:1079–1086.PubMedGoogle Scholar
  153. Wilson C. J., Finch C. E., and Cohen H. J. (2002). Cytokines and cognition—the case for a head-to-toe inflammatory paradigm. J. Am. Geriatr. Soc. 50:2041–2056.PubMedGoogle Scholar
  154. Xia J., Chung H. J., Wihler C., Huganir R. L., and Linden D. J. (2000). Cerebellar long-term depression requires PKC-regulated interactions between GluR2/3 and PDZ domain-containing proteins. Neuron 28:499–510.PubMedGoogle Scholar
  155. Yabuuchi K., Minami M., Katsumata S., and Satoh M. (1993). In situ hybridization study of interleukin-1β mRNA induced by kainic acid in the rat brain. Brain Res. Mol. Brain Res. 20:153–161.PubMedGoogle Scholar
  156. Yoshikawa K., Kita Y., Kishimoto K., and Shimizu T. (2006). Profiling of eicosanoid production in the rat hippocampus during kainic acid-induced seizure - Dual phase regulation and differential involvement of COX-1 and COX-2. J. Biol. Chem. 281:14663–14669.PubMedGoogle Scholar
  157. Zafra F., Castrén E., Thoenen H., and Lindholm D. (1991). Interplay between glutamate and γ-aminobutyric acid transmitter systems in the physiological regulation of brain-derived neurotrophic factor and nerve growth factor synthesis in hippocampal neurons. Proc. Natl. Acad. Sci. USA 88:10037–10041.Google Scholar
  158. Zaleska M. M. and Wilson D. F. (1989). Lipid hydroperoxides inhibit reacylation of phospholipids in neuronal membranes. J. Neurochem. 52:255–260.PubMedGoogle Scholar
  159. Zheng W. H. and Quirion R. (2004). Comparative signaling pathways of insulin-like growth factor-1 and brain-derived neurotrophic factor in hippocampal neurons and the role of the PI3 kinase pathway in cell survival. J. Neurochem. 89:844–852.PubMedGoogle Scholar
  160. Zhu X. M. and Ong W. Y. (2004). Changes in GABA transporters in the rat hippocampus after kainate-induced neuronal injury: decrease in GAT-1 and GAT-3 but upregulation of betaine/GABA transporter BGT-1. J. Neurosci. Res. 77:402–409.PubMedGoogle Scholar
  161. Ziegra C. J., Willard J. M., and Oswald R. E. (1992). Coupling of a purified goldfish brain kainate receptor with a pertussis toxin-sensitive G protein. Proc. Natl. Acad. Sci. USA 89:4134–4138.Google Scholar

Copyright information

© Springer Science+Business Media, LLC 2008

Authors and Affiliations

  • Akhlaq A. Farooqui
    • 1
  • Wei-Yi Ong
    • 2
  • Lloyd A. Horrocks
    • 3
  1. 1.Department of Molecular and Cellular BiochemistryThe Ohio State UniversityColumbusUSA
  2. 2.Department of Anatomy, Faculty of MedicineNational University of SingaporeSingapore
  3. 3.The Ohio State UniversityColumbus

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