Selective reduction of GluR2 protein in adult hippocampal CA3 neurons following status epilepticus but prior to cell loss

Hippocampus

Volumn 8, Issue 5, 1998, Pages 511-525

  Friedman, Linda K ^a,b,c  

^a ALBERT EINSTEIN COLLEGE OF MEDICINE   (United States)

^b NEW JERSEY NEUROSCIENCE INSTITUTE   (United States)

^c SETON HALL UNIVERSITY   (United States)

Author keywords

AMPA; Apoptosis; Hippocampus; Immunohistochemistry; Kainate; Necrosis; Neurodegeneration; Status epilepticus

Indexed keywords

AMPA RECEPTOR; ANTIBODY; CALCIUM; GLUTAMATE RECEPTOR; KAINIC ACID; MESSENGER RNA; RECEPTOR PROTEIN;

ANIMAL TISSUE; ANTIBODY LABELING; APOPTOSIS; ARGYROPHILIA; ARTICLE; CELL DEATH; CELL LOSS; CONTROLLED STUDY; ELECTRON MICROSCOPY; EMULSION; EPILEPTIC STATE; HIPPOCAMPUS; HISTOLOGY; IMMUNOBLOTTING; IMMUNOFLUORESCENCE TEST; IMMUNOHISTOCHEMISTRY; IN SITU HYBRIDIZATION; LABORATORY; MALE; NERVE CELL; NERVE CELL DEGENERATION; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; PYRAMIDAL NERVE CELL; RAT; REDUCTION; SILVER IMPREGNATION;

ANIMALS; CELL COUNT; HIPPOCAMPUS; IMMUNOHISTOCHEMISTRY; KAINIC ACID; MALE; MICROSCOPY, ELECTRON; NERVE DEGENERATION; NEURONS; RATS; RATS, SPRAGUE-DAWLEY; RECEPTORS, AMPA; REFERENCE VALUES; RNA, MESSENGER; SILVER STAINING; STATUS EPILEPTICUS;

EID: 0031731307     PISSN: 10509631     EISSN: None     Source Type: Journal    
DOI: 10.1002/(SICI)1098-1063(1998)8:5<511::AID-HIPO9>3.0.CO;2-W     Document Type: Article

References (85)

1. Amano S, Obata T, Hazama F, Kashiro N, Shimada M. Hypoxia prevents seizures and neuronal damages of the hippocampus induced by kainic acid in rats. Brain Res 1990;523:121-126.
2. Ben-Ari Y. Limbic seizure and brain damage produced by kainic acid: Mechanisms and relevance to human temporal lobe epilepsy. Neuro-science 1985;14:375-403.
3. Ben-Ari Y, Tremblay E, Ottersen OP, Naquet R. Evidence suggesting secondary epileptogenic lesion after kainic acid Pre-treatment with diazepam reduces distant but not local brain damage. Brain Res 1979;165:362-365.
4. Blackstone CD, Moss SJ, Martin LJ, Levey, Price DL, Huganir RL. Biochemical characterization and localization of a non-NMDA glutamate receptor in rat brain. J Neurochem 1992;58:1-9.
5. Brusa R, Zimmermann F, Duk-Su Koh, Feldmeyer D, Gass, Seeburg PH, Sprengel R. Early onset epilepsy and postnatal lethality associated with an editing-deficient GluR-B allele in mice. Science 1995;270:8.
6. Burnashev N, Khodorova A, Jonas P, Helm PJ, Wisden W, Monyer H, Seeburg P, Sakmann B. Calcium-permeable AMPA-kainate receptors in fusiform cerebellar glial cells. Science 1992;256:1566-1570.
7. Charriaut-Marlangue C, Aggoun-Zouaoui D, Repressa A, Ben-Ari Y. Apoptotic features of selective neuronal death in ischemia, epilepsy and gp 120 toxicity. TINS 1996;19:109-114.
8. Condorelli DF, Bellueardo N, Mudo G, Dell P, Jiang X, Giuffrida-Stella AM. Changes in gene expession of AMPA-selective glutamate receptor subunits induced by status epilepticus in rat brain. Neurochem Int 1994;25:367-376.
9. Crain BJ, Westerkam WD, Harrison AH, Nadler JV. Selective neuronal death after transient forebrain ischemia in the Mongloilan gerbil: A silver impregnation study. Neuroscience 1988;27:387-402.
10. DeFelipe J, Huntly GW, del Rio MR, Sola RG. Microzonal decreases in the immunostaining for non-NMDA ionotropic excitatory amino acid receptor subunits GluR2/3 and GluR5/6/7 in the human epileptogenic neocortex. Brain Res 1994;657:150-158.
11. Douglass J, Grimes L, Shook J, Lee PHK, Hong JS. Systemic administration of kainic acid differentially regulates the levels of prodynorphin and proenkephalin mRNA and peptides in the rat hippocampus. Mol Brain Res 1991;9:79-86.
12. Ferhat L, Chevassus-au-Lous M, Krestchatisky M, Ben-Ari Y, Repressa A. Seizures induce tenascin-C mRNA expression in neurons. J Neurocytol 1996;25:535-546.
13. Franck JE, Roberts DL. Combined kainate and ischemia produces "mesial temporal sclerosis." Neurosci Lett 1990;118:159-163.
14. Frank L, Diemer NH, Kaiser F, Sheardown M, Rasmussen JS, Kristenstein P. Unchanged balance between levels of mRNA encoding AMPA encoding AMPA glutamate recepotr subtypes following global cerebral ischemia in the rat. Neurol Scand 1995;92:337-343.
15. Franklin JL, Johnson EM Jr. Suppression of programmed neuronal death by sustained elevation of cytoplasmic calcium. TINS 1992;15:501-508.
16. Franklin JL, Johnson EM Jr. Elevated intracellular calcium blocks programmed cell death. Ann NY Acad Sci 1994;747:195-204.
17. 2+ influx but not Trk activation. J Neurosci 1995;15:643-664.
18. A receptor gene expression in adult rat hippocampus: An in situ hybridization study. J Neurosci 1994;14:2697-2707.
19. A receptor gene expression in rat hippocampus following kainate-induced status epilepticus. Dev Neurosci 1997;19:529-542.
20. Friedman LK and Sperber EF. GluR2 receptor mRNA is increased in the dentate gyrus at times associated with synaptic reorganization. Epilepsia (Suppl 8) 1994;35:85.
21. Gall CM, Isackson PJ. Limbic seizures increase neuronal production of messenger RNA for nerve growth factor. Science 1989;245:758-761.
22. Gall CM, Murray K, Isackson PJ. Kainic acid-induced seizures stimulate increased expression of nerve growth factor mRNA in rat hippocampus. Mol Brain Res 1991;9:113-123.
23. Gallyas F, Wolff JR, B_ttcher WH, Zaborszky L. A reliable and sensitive method to localize terminal degeneration and lysosomes in the central nervous system. Stain Technol 1980;55:299-306.
24. 2+ permeability of AMPA receptors in principal neurons and interneurons. Neuron 1995;15:193-204.
25. Haber SN, Ryoo H, Cox C, Lu W. Subsets of midbrain dopaminergic neurons in monkeys are distinguished by different levels of mRNA for the dopamine transporter: Comparison with the mRNA for the D2 receptor, tyrosine hydroxylase and calbindin immunoreactivity. J Comp Neurol 1995;362:400-410.
26. Hartley Z, Dubinsky J. Changes in intracellular pH associated with glutamate excitotoxicity. J Neurosci 1993;13:4690-4699.
27. 2+ accumulation in cortical culture correlates with subsequent neuronal degeneration. J Neurosci 1993;13:1993-2000.
28. 2+ permeability of KA-AMPA-gated glutamate receptor channels depends on subunit composition. Science 1991;252:851-853.
29. Iino JM, Ozawa S, Tsuzuki K. Permeation of calcium through excitatory amino acid receptor channels in cultured rat hippocampal neurones. J Physiol 1990;424:151-165.
30. Jonas P, Sakmann B. Properties of AMPA subtype glutamate receptors in pyramidal cells of rat hippocampal slices. J Physiol 1991;438:321P.
31. Kaku DA, Goldberg MP, Choi DW. Antagonism of non-NMDA receptors augment the neuroprotective effect of NMDA receptor blockade in cortical cultures subjected to prolonged deprivation to oxygen and glucose. Brain Res 1991;554:344-347.
32. Koh DS, Burnashev N, Jonas P, Sakmann B. Ca(2+)-permeable AMPA and NMDA receptor channels in basket cells of rat hippocampal dentate gyrus. J Physiol 1995;485:383-402.
33. Kyrozis A, Goldstein PA, Health MJS, MacDermott AB. Calcium entry through a subpopulation of AMPA receptors desensitizing neighbouring NMDA receptors in rat dorsal horn neurons. J Physiol 1995;485: 373-381.
34. Laemmli UK. Cleavage of structural proteins during the assembly of bacteriophage T4. Nature 1970;227:680-685.
35. 2+ influx. J Neurobiol 1995;26:205-12.
36. Leranth C, Szeidemann Z, Hsu M, Buzáki G. AMPA receptors in the rat and primate hippocampus: Apossible absence of GluR2/3 subunits in most intemeurons. Neuroscience 1996;70:631-652.
37. Lassmann H, Petsche U, Kitz K, Baran H. Sperk G, Seitelberger F, Hornykiewcz O. The role of brain edema in epileptic brain damage induced by systemic kainic acid injection Neuroscience 1984;13:691-704.
38. Lee S, Miskovsky, Williamson J, Howells R, Devinsky, Lothman E, Christakos. Changes in glutamate receptor expression and proenkephalin gene expression after kindled seizures. Brain Res Mol Brain Res 1994;24:34-42.
39. Lees GJ, Leong W. NBQX prevents contralateral but not ipsilateral seizure-induced cytotoxicty of kainate but not AMPA-reversal at high doses of NBQX. NeuroReport 1994;5:2153-2156.
40. Lowry OH, Rosebrough NJ, Farr AL, Randall RJ. Protein measurement with the phenol reagent. J Biol Chem 1951;193:265-275.
41. 2+ influx underlies potent induction of injury. J Neurosci 1996;16:5457-5465.
42. McBain CJ, Dingledine R. Heterogeneity of synaptic glutamate receptors on CA3 stratum radiatum intereurons of rat hippocampus. J Physiol 1993;462:373-392.
43. Monacada C, Arvin B, Le Peillet E, Meldrum BS. Non-NMDA antagonists protect against kainate more that AMPA toxicity in the rat hippocampus. Neurosci Lett 1991;133:287-290.
44. Mosinger JL, Price MT, Bai HY, Xiao H, Wonziak DF, Olney JW. Blockade of both NMDA and non-NMDA receptors is required for optimal protection against ischemic neuronal degeneration in the in vivo adult mammalian retna. Exp Neurol 1991;113:10-17.
45. Murphy SN, Miller RJ. Regulation of Ca++ influx into striatal neurons by kainic acid. J Pharmacol Exp Therp 1989;249:184-193.
46. Nadler JV. Kainic acid as a tool for the study of temporal lobe epilepsy. Life Sci 1981;29:31-42.
47. Nadler JV, Perry BW, Cotman CW. Intraventricular kainic acid preferentially destroys hippocampal pyramidal cells. Nature 1978;271:676-677.
48. Nakanishi N, Schneider NA. Alternative splicing generates functionally distinct N-methyl-D-aspartate receptors. Proc Natl Acad Sci USA 1992;89:8552-8556.
49. Namba T, Morimoto K, Sato K, Yamada N, Shigetoshi K. Antiepileptogenic and anticonvulsant effects of NBQX, a selective AMPA receptor antagonist, in the rat kindling model of epilepsy. Brain Res 1996;638: 36-44.
50. Nishiyama K, Kwak S, Takekoshi S, Watanabe K, Kanazwa I. In situ nick end labeling detects necrosis of hippocampal pyramidal cells induced by kainic acid. Neurosci Lett 1996;212:139-42.
51. Olney JW, Fuller T, de Gubareff T. Widespread changes in the hippocampus of kainate treated rats. Brain Res 1979;176:91-100.
52. Oppenheim RW, Schartz LM, Shatz CJ. Neuronal death, a tradition of dying. J Neurobiol 1992;23:1111-1115.
53. 2+ permeability mediate synaptic transmission in the avian auditory pathway. J Physiol 1995;482:309-315.
54. Paxinos G, Watson C. The rat brain in stereotaxic coordinates, 2nd ed. Sydney: Academic Press, 1986.
55. Petralia RS, Wenthold RJ. Light and electron immunocytochemical localization of AMPA-selective glutamate receptors in the rat brain. J Comp Neurol 1992;318:329-354.
56. Petralia RS, Yokotani N, Wenthold RJ. Light and electron microscope distribution of the NMDA receptor subunit NMDAR1 in the rat nervous system using a selective anti-peptide antibody. J Neurosci 1994;14:667-696.
57. Pinard E, Ben-Ari Y, Tremblay E, Seylaz J. Is intratissular hypoxia responsible for lesions during seizures induced by kainic acid? In: Baldy-Moulinier M, ed. Cerebral blood flow, metabolism, and epilepsy. London: J. Libby, 1983:252-257.
58. Pollard H, Moreau HJ, Ben-Ari Y, Khrestchatisky. Alterations of the GluR-B AMPA receptor subunit flip/flop expression in kainateinduced epilepsy and ischemia. Neuroscience 1993;57:545-554.
59. Pollard H, Charriaut-Marlangue C, Cantagrel S, Repressa A, Robain O, Moreau J, Ben-Ari Y. Kainate-induced apoptotic cell death in hippocampal neurons. Neuroscience 1994;63:7-18.
60. Prince HK, Conn PJ, Blackstone CD, Huganir RL, Levey AI. Down-regulation of AMPA receptor subunit GluR2 in amygdaloid kindling. J Neurochem 1995;64:462-465.
61. Randall RD, Thayer SA. Glutamate-calcium transient triggers delayed calcium overload and neurotoxicity in rat hippocampal neurons. J Neurosci 1992;12:1882-1895.
62. Rogers SW, Hughes TE, Hollmann M, Gasic GP, Deneris ES, Heinemann S. The characterization and localization of the glutamte receptor subunit GluR1 in the rat brain. J Neurosci 1991;11:2713-2724.
63. Schreiber SS, Baudry M. Selective neuronal vulnerability in the hippocampus - a role for gene expression? TINS 1995;18:446-450.
64. Schneggenburger R, Zhou Z, Konnerth A, Neher E. Excitatory and inhibitory synaptic currents and receptors in rat medial septal neurones. Neuron 1993;11:133-143.
65. Schwob JE, Fuller T, Price JL, Olney JW. Widespread patterns of neuronal damage following systemic or intracerebral injections of kainic acid Ahistological study. Neuroscience 1980;5:991-1014.
66. Sheardown MJ, Nielsen E, Hansen AJ. 2,3-Dihydroxy-6-nitro-7-sulfamonyl-benzo(F) quinoxaline: A neuroprotectant for cerebral ishemia. Science 1990;247:571-574.
67. Siegal SJ, Jansen WG, Tullai JW, Rogers SW, Moran T, Heinemann SF, Morrison JH. Distribution of the excitatory amino acid receptor subunits GluR2(4) in monkey hippocampus and colocalization with subunits GluR5-7 and NMDAR1. J Neurosci 1995;15:2707-2719.
68. Sonnenberg JL, Macgregor-Leon, Curran T, Morgan JI. Dynamic alterations occur in the levels and composition of transcription factor AP-I complexes after seizure. Neuron 1989a;3:359-365.
69. Sonnenberg JL, Mitchelmore C, Macgregor-Leon PF, Hempstead J, Morgan JI, Curran T. Glutamate receptor agonists increase the expression Fos, Fra, and AP-1 DNA binding activity in the mammalian brain. J Neurosci Res 1989b;24:72-80.
70. Sperk G. Kainic acid seizures in the rat. Prog Neurobiol 1994;42:1-32.
71. Takazawa A, Yamazaki O, Kanai H, Ishida N, Nobumasa K, Yamauchi. Potent and long lasting-anticonvulsant effects of 1-napthylacetyl spermine an analogue of Joro spider toxin, against amygdaloid kindled seizures. Brain Res 1996;706:173-176.
72. Tanaka T, Kondo S, Tanaka S, Sako K, Yonemasu Y. Long term observations of rats after unilateral intra-amygdaloid injection of kainic acid. Brain Res 1988;463:163-167.
73. Tanaka T, Tanaka S, Fujita T, Takano K, Fukuda H, Sako K, Yonemasu Y. Experimental complex partial seizures induced by microinjection of kainic acid into limbic structures. Prog Neurobiol 1992;38:317-334.
74. Tempia F, Masanobu K, Schneggenburger R, Schirra C, Garaschuk O, Plant T, Konnerth A. Fractional calcium current through neuronal AMPA-receptor channels with a low calcium permeability. J Neurosci 1996;16:456-466.
75. Teitelbaum JS, Zatorre RJ, Carpenter S, Gendron D, Evans AC, Gjedde A, Cashman NR. Neurologic sequelae of domoic acid intoxication due to injestion of contaminated muscles. New Eng J Med 1990;322: 1781-1787.
76. Toth Z, Hollrigel GS, Gorcs T, Soltesz I. Instantaneous perturbation of dentate interneuronal networks by pressure wave-transient delivered to the neocortex. J Neurosci 1997;17:8106-8117.
77. Towbin H, Staehelin T, Gordon J. Electrophoretic transfer of proteins from polyacrylamide gels to nitrocellulose sheets: Procedure and some applications. Proc Natl Acad Sci USA 1979;76:4350-4354.
78. 2+ overload indicates early neuronal injury which precedes staining with viability indicators. Brain Res 1993a;607:319-323.
79. 2+ chelators reduce early excitotoxic and ischemic neuronal injury in vitro and in vivo. Neuron 1993b;11: 221-235.
80. Verdoorn TA, Burnashev N, Monyer H, Seeburg PH, Sakmann B. Structural determinants of ion flow through recombinant glutamate receptor channels. Science 1991;252:1715-1718.
81. Vickers JC, Huntly GW, Edwards AM, Moran T, Rogers SW, Heinemann SF, Morrison JH. Quantitative localization of AMPA/kainate and kainate glutamate receptor subunit immunoreactivity in neurochemically identified subpopulations of neurons in the prefrontal cortex of the macaque monkey. J Neurosci 1993;13:2982-2992.
82. Vissavajjhala P, Janssen WGM, Hu Y, Gazzaley AH, Moran T, Hof PR, Morrison JH. Synaptic distribution of the AMPA[00d0]GluR2 subunit and its colocalization with calcium-binding proteins in rat and cerebral cortex: An immunohistochemical study using a GluR2-specific monoclonal antibody. Exp Neurol 1996;142:295-311.
83. Wenthold RJ, Petralia RA, Blahos J II, Niedzielski AS. Evidence for multiple AMPA receptor complexes in hippocampal CA1/CA2 neurons. J Neurosci 1996;16:1982-1989.
84. White JD, Gall CM, McKelvy JF. Enkephalin biosynthesis and enkephalin gene expression are increased in hippocampal mossy fibers following a unilateral lesion of the hilus. J Neurosci 1987;7:753-759.
85. Xia Z, Dudek H, Miranti CK, Greenberg ME. Calcium influx via the NMDA receptor induces immediate early gene transcription by a MAP kinase/ERK-dependent mechanism. J Neurosci 1996;16:5425-5436.