Glutamate receptors in dysplasic cortex: An in situ hybridization and immunohistochemistry study in rats with prenatal treatment with methylazoxymethanol

Brain Research

Volumn 782, Issue 1-2, 1998, Pages 142-152

  Rafiki, A ^a   Chevassus au Louis, N ^a   Ben Ari, Y ^a   Khrestchatisky, M ^a   Represa, A ^a  

^a INSERM   (France)

Author keywords

Cognitive disorder; Epilepsy; Hippocampus; Microcephaly; Neocortex

Indexed keywords

GLUTAMATE RECEPTOR; METHYLAZOXYMETHANOL; RECEPTOR SUBTYPE;

AMNESIA; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; COGNITIVE DEFECT; CONGENITAL MALFORMATION; CONTROLLED STUDY; EPILEPSY; FEMALE; GENETIC TRANSCRIPTION; HETEROTOPIA; HIPPOCAMPUS; IMMUNOHISTOCHEMISTRY; IN SITU HYBRIDIZATION; MICROCEPHALY; NEOCORTEX; NONHUMAN; PRENATAL DRUG EXPOSURE; PRIORITY JOURNAL; RAT; WHITE MATTER;

ANIMALS; BRAIN DISEASES; CEREBRAL CORTEX; CHORISTOMA; FEMALE; HIPPOCAMPUS; IMMUNOHISTOCHEMISTRY; IN SITU HYBRIDIZATION; METHYLAZOXYMETHANOL ACETATE; PREGNANCY; PRENATAL EXPOSURE DELAYED EFFECTS; RATS; RECEPTORS, GLUTAMATE; RNA, MESSENGER;

EID: 0032567734     PISSN: 00068993     EISSN: None     Source Type: Journal    
DOI: 10.1016/S0006-8993(97)01273-0     Document Type: Article

References (72)

1. Balduini W., Cimino M., Lombardelli G., Abbrachio M.P., Peruzzi G., Cecchini T., Gazzanelli G.C., Cattabeni F. Microencephalic rats as a model for cognitive disorders. Clin. Neuropharmacol. 9:1986;S8-S18.
2. Balduini W., Lombardelli G., Peruzzi G., Cattabeni F. Cholinergic hyperinnervation in the cerebral cortex of microencephalic rats does not result in muscarinic receptor down-regulation or in alteration of receptor-stimulated phosphoinositide metabolism. Neurochem. Res. 17:1992;761-766.
3. Baraban S.C., Schwartzkroin P.A. Flurothyl seizure susceptibility in rats following prenatal methylazoxymethanol treatment. Epilepsy Res. 23:1996;189-194.
4. Baraban S.C., Schwartzkroin P.A. Electrophysiology of CA1 pyramidal neurons in an animal model of neuronal migration disorders: prenatal methylazoxymethanol treatment. Epilepsy Res. 22:1995;145-156.
5. Bliss T.V.P., Collingridge G.L. A synaptic model of memory: long-term potentiation in the hippocampus. Nature. 361:1993;31-39.
6. Caputi A., Rurale S., Pastorino L., Cimino M., Cattabeni F.N., Di Luca M. Differential translocation of protein kinase C isozymes in rats characterized by a chronic lack of LTP induction and cognitive impairment. FEBS Lett. 393:1996;121-123.
7. Cattaneo E., Reinach B., Caputi A., Cattabeni F., Di Luca M. Selective in vitro blockade of neuroepithelial cells proliferation by methylazoxymethanol acetate, a molecule capable of inducing long lasting functional impairments. J. Neurosci. Res. 41:1995;640-647.
8. N. Chevassus-au-Louis, I. Rafiki, P. Congar, Y. Ben-Ari, J.-L. Gaïarsa, A. Represa, Neocortex in the hippocampus: a morphofunctional study of CA1 ectopiae after prenatal treatment with methylazoxymethanol in rats, Soc. Neurosci. Abstr. (1997) 836.4.
9. Collier P.A., Ashwell K.W. Distribution of neuronal heterotopiae following prenatal exposure to methylazoxymethanol. Neurotoxicol. Teratol. 15:1993;439-444.
10. Collingridge G.L., Bliss T.V.P. NMDA receptors, their role in long term potentiation. Trends Neurosci. 10:1987;288-293.
11. Conti F., Minelli A., Molnar M., Brecha N.C. Cellular localization and laminar distribution of NMDAR1 mRNA in the rat cerebral cortex. J. Comp. Neurol. 343:1994;554-565.
12. Crepel V., Represa A., Beaudoin M., Ben-Ari Y. Hippocampal damage induced by ischemia and intra-amygdaloid kainate injection: effects on N-methyl-D-aspartate, N-(1-[2-thienyl]cyclohexyl) piperidine and glycine binding sites. Neurosci. 31:1989;605-612.
13. Dambska M., Haddad R., Kozlowski P.B., Lee M.H., Shek J. Telencephalic cytoarchitectonics in the brains of rats with graded degrees of micrencephaly. Acta Neuropathol. (Berlin). 58:1982;203-209.
14. De Feo M.R., Mecarelli O., Ricci G.F. Seizure susceptibility in immature rats with micrencephaly induced by prenatal exposure to methylazoxymethanol acetate. Pharmacol. Res. 31.2:1995;109-114.
15. DeFelipe J., Huntley G.W., del Rion M.R., Sola R.G., Morrison J.H. Microzonal decreases in the immunostaining for non-NMDA ionotropic excitatory amino acid receptor subunits GluR2/3 and GluR5/6/7 in the human epileptogenic cortex. Brain Res. 657:1994;150-158.
16. Di Luca M., Caputi A., Cinquanta M., Cimino M., Marini P., Princivalle A., De Graan P.N.E., Gispen W.H., Cattabeni F. Changes in protein kinase C and its presynaptic substrate B-50/GAP 43 after intrauterine exposure to methylazoxy methanol, a treatment inducing cortical and hippocampal damage and cognitive deficits in rats. Eur. J. Neurosci. 7:1995;899-906.
17. Di Luca M., Caputti A., Cattabeni F., De Graan P.N.E., Gispen W.H., Raiteri M., Fassio A., Schmid G., Bonanno G. Increased presynaptic protein kinase C activity and glutamate release in rats with prenatally induced hippocampal lesion. Eur. J. Neurosci. 9:1997;472-479.
18. Di Luca M., Cimino M., De Graan P.N.E., Oestraeicher A.B., Gispen W.H., Cattabeni F. Microencephaly reduces the phosphorylation of the PKC substrate B-50/GAP 43 in rat cortex and hippocampus. Brain Res. 538:1991;95-101.
19. Franceschetti S., Sancini G., Battaglia G., Spreafico R., Di Luca M., Avanzini G. Aberrant firing pattern of neocortical neurons from methylazoxymethanol (MAM)-treated rats in utero. Epilepsia. 37:1996;72. Suppl. 5.
20. Friedman L.K., Pellegrini-Giampetro D.E., Sperber E.F., Bennett M.V.L., Moshe N.L., Zukin S. KA-induced status epilepticus alters glutamate and GABAA receptor gene expression in adult hippocampus: an in situ hybridization study. J. Neurosci. 14:1994;2697-2707.
21. Gall C., Sumikawa K., Lynch G. Levels of mRNA for a putative kainate receptor are affected by seizures. Proc. Natl. Acad. Sci. USA. 87:1990;7643-7647.
22. I.M. Germano, E.F. Sperber, S.L. Moshe, Molecular and experimental aspects of neuronal migration disorders, in: R. Guerrini (Ed.), Dysplasias of Cerebral Cortex and Epilepsy, Lippincott-Raven, Philadelphia, 1996, pp. 27-34.
23. Germano I.M., Zhang Y.F., Sperber E.F., Moshe S.L. Neuronal migration disorders increase susceptibility to hyperthermia induced seizures in developing rats. Epilepsia. 37:1996;902-910.
24. Hollmann M., Hartley M., Heinemann S. Ca2+ permeability of KA-AMPA-gated glutamate receptor channels depends on subunit composition. Science. 252:1991;851-853.
25. Hollmann M., Heinemann S. Cloned glutamate receptors. Ann. Rev. Neurosci. 17:1994;31-108.
26. Hollmann M., O'Shea-Greenfield A., Rogers S.W., Heinemann S. Cloning by functional expression of a member of the glutamate receptor family. Nature. 342:1989;643-648.
27. Ikeda K., Nagasawa M., Mori H., Araki K., Sakimura K., Watanabe M., Inoue Y., Mishima M. Cloning and expression of the e4 subunit of the NMDA receptor channel. FEBS Lett. 313:1992;34-38.
28. Izquierdo I. Role of NMDA receptors in memory. Trends Pharmacol. Sci. 12:1991;128-129.
29. Johnson R.R., Jiang X., Burkhalter A. Regional and laminar differences in synaptic localization of NMDA receptor subunit NR1 splice variant in rat visual cortex and hippocampus. J. Comp. Neurol. 368:1996;335-355.
30. Johnston M.V., Coyle J.T. Histological and neurochemical effects of fetal treatment with metylazoxymethanol on rat neocortex in adulthood. Brain Res. 170:1979;135-155.
31. Kauer J.A., Malenka R.C., Nicoll R.A. A persistent postsynaptic modification mediates long-term potentiation in the hippocampus. Neuron. 1:1988;911-917.
32. Keinänen K., Wisden W., Sommer B., Werner P., Herb A., Verdoorn T.A., Sakmann B., Seeburg P.H. A family of AMPA-selective glutamate receptors. Science. 249:1990;556-560.
33. Kraus J.E., Yeh G.-C., Bonhaus D.W., Nadler J.V., Mc Namara J.O. Kindling induced the long-lasting expression of a novel population of NMDA receptors in hippocampal region CA3. J. Neurosci. 14:1994;4196-4205.
34. Kumar K.N., Tilakaratne N., Johnson P.S., Allen A.E., Michaelis E.K. Cloning of cDNA for the glutamate-binding subunit of an NMDA receptor complex. Nature. 354:1991;70-73.
35. Kutsuwada T.et al. Molecular diversity of the NMDA receptor channel. Nature. 358:1992;36-41.
36. Laurie D.J., Seeburg P.H. Regional and developmental heterogeneity in splicing of the rat brain NR1 mRNA. J. Neurosci. 14:1994;3180-3194.
37. Marini P., Di luca M., Caputi A., Pastorino L., Cimino M., Boanno G., Raiteri M., Perez J., Cattabeni F. Functional desensitization of NMDA receptors in an animal model of chronic up-regulation of glutamate release. Soc. Neurosci. Abstr. 586.14:1995.
38. Martin D., McNamara J.O., Nadler J.V. Kindling enhances sensitivity of CA3 hippocampal pyramidal cells to NMDA. J. Neurosci. 12:1992;1928-1935.
39. Matsutani T.M.N., Tamaru M., Tsukada Y. Elevated monoamine levels in the cerebral hemispheres of microencephalic rats treated prenatally with methylazoxymethanol or cytosine arabinoside. J. Neurochem. 34.4:1980;950-956.
40. Mayer M.L., Westbrook G.L. The physiology of excitatory amino acids in the vertebrate central nervous system. Prog. Neurobiol. 8:1987;197-276.
41. McDonald J.W., Garofalo E.A., Hood T., Sackellares J.C., Gilman S., McKeever P.E., Troncoso J.C., Johnston M.V. Altered excitatory and inhibitory amino acid receptor binding in hippocampus of patients with temporal lobe epilepsy. Ann. Neurol. 29:1991;529-541.
42. Meguro H., Mori H., Kushiya E., Kutsuwada T., Yamazaki M., Kumanishi T., Arakawa M., Sakimura K., Mishina M. Functional characterization of heterodimeric NMDA receptor channel expressed from cloned cDNAs. Nature. 357:1992;70-74.
43. Mischel P.S., Nguyen L.P., Vinters H.V. Cerebral cortical dysplasia associated with pediatric epilepsy. Review of neuropathological features and proposal for a grading system. J. Neuropathol. Exp. Neurol. 54.2:1995;137-153.
44. Mody I., Heinemann U. NMDA receptors of dentate gyrus granule cells participate in synaptic transmission following kindling. Nature. 326:1987;701-704.
45. Monyer H., Burnashev N., Laurie D.J., Sakmann B., Seeburg P.H. Developmental and regional expression in the rat brain and functional properties of four NMDA receptors. Neuron. 12:1994;529-540.
46. Monyer H., Sprengel R., Scoepfer R., Herb A., Higuchi M., Lomeli H., Burnashev N., Sakmann B., Seeburg P.H. Heterodimeric NMDA receptors: molecular and functional distinction of subtypes. Science. 256:1992;1217-1221.
47. Moryoshi K., Masu M., Ishii T., Shigemoto R., Mizuno N., Nakanishi S. Molecular cloning and characterization of the rat NMDA receptor. Nature. 354:1991;31-37.
48. Müller D., Joly M., Lynch G. Contributions of quisqualate and NMDA receptors to the induction and expression of LTP. Science. 242:1988;1694-1697.
49. Nakanishi N., Axel R., Schneider N.A. Alternative splicing generates functionally distinct N-methyl-D-aspartate receptors. Proc. Natl. Acad. Sci. USA. 89:1992;8552-8556.
50. Nakanishi S. Molecular diversity of glutamate receptors and implication for brain function. Science. 258:1992;597-603.
51. Nowak L., Bregestovski P., Ascher P., Herbert A., Prochiantz A. Magnesium gates glutamate-activated channels in mouse central neurons. Nature. 307:1984;462-465.
52. Petralia R.S., Wang Y.-X., Wenthold R.J. The NMDA receptor subunits NR2A and NR2B show histological and ultrastructural localization patterns similar to those of NR1. J. Neurosci. 14.10:1994;6102-6120.
53. Petralia R.S., Yokotani N., Wenthold R.J. Light and electron microscope distribution of the NMDA receptor subunit NMDAR1 in the rat nervous system using a selective anti-peptide antibody. J. Neurosci. 14.2:1994;667-696.
54. Pollard H., Hron A., Moreau J., Ben-Ari Y., Khrestchatisky M. Alterations of the GLUR-B AMPA receptor subunit Flip/flop expression in kainate-induced epilepsy and ischemia. Neurosci. 57:1993;545-554.
55. Pollard H., Khrestchatisky M., Moreau J., Ben-Ari Y. Transient expression of the NR2C subunit receptor in the developing brain. Neuroreport. 4:1993;411-414.
56. Pratt G.D., Kokaia M., Bengzon J., Kokaia Z., Fritschy J.-M., Möhler H., Lindvall O. Differential regulation of N-methyl-D-aspartate receptor subunit messenger RNAs in kindling-induced epileptogenesis. Neuroscience. 57:1993;307-318.
57. Quesada O., Hirsch J., Ben-Ari Y., Bernard C. Redox sites of NMDA receptors can modulate epileptiform activity in hippocampal slices from kainic acid treated rats. Neurosci. Lett. 212:1996;171-174.
58. Ramakers G.M.J., Urban I.J.A., De Graan P.N.E., Cattabeni F., Di Luca M., Gispen W.H. Impaired LTD and paired pulse facilitation in the CA1 region of the hippocampus of cognitive deficient microencephalic rats. Soc. Neurosci. Abstr. 20:1994;622.14.
59. Ramakers G.M.J., Urban I.J.A., De Graan P.N.E., Di Luca M., Cattabeni F., Gispen W.H. The impaired long-term potentiation in the CA1 field of the hippocampus of cognitive deficient microencephalic rats is restored by D-serine. Neuroscience. 54.1:1993;49-60.
60. O. Robain, Introduction to the pathology of cerebral cortical dysplasia, in: R. Guerrini (Ed.), Dysplasias of the Cerebral Cortex and Epilepsy, Lippincott-Raven, Philadelphia, 1996, pp. 1-9.
61. Sheng M., Cummings J., Roldan L.A., Jan Y.N., Jan J.Y. Changing subunit composition of heterodimeric NMDA receptors during development of rat cortex. Nature. 368:1994;144-147.
62. Siegel S.J., Brose N., Janssen W.G., Gasic G.P., Jahn R., Heinemann S.F., Morrison J.H. Regional, cellular, and ultrastructural distribution of N-methyl-D-aspartate receptor subunit 1 in monkey hippocampus. Proc. Natl. Acad. Sci. USA. 91:1994;564-568.
63. Simpson L.H., Wheal H.V., Williamson R. The contribution of non-NMDA and NMDA receptors to graded bursting activity in the CA1 region of the hippocampus in a chronic model of epilepsy. Can. J. Physiol. Pharmacol. 69:1991;1091-1098.
64. Sommer B., Keinäken K., Verdoorn T.A., Wisden W., Burnashev N., Herb A., Köhler M., Tamakagi T., Sakmann B., Seebug P.H. Flip and flop: a cell-specific functional switch in glutamate-operated channels of the CNS. Science. 249:1990;1580-1585.
65. Sommer P., Seeburg P.H. Glutamate receptors channels-novel properties and new clones. Trends Pharmacol. Sci. 13:1992;291-296.
66. Tamaru M., Yoneda Y., Ogita K., Shimizu J., Matsutani T., Nagata T. Excitatory amino acid receptors in brains of rats with methylazoxymethanol-induced microencephaly. Neurosci. Res. 14:1992;13-25.
67. Verdoorn T.A., Burnashev N., Monyer H., Seeburg P.H., Sackmann B. Structural determinants of ion flow through recombinant glutamate receptor channels. Science. 252:1991;1715-1718.
68. Vezzani A., Speciale C., Della Vedova F., Tamburin M., Benatti L. Alternate splicing at the C-terminal but not at the N-terminal domain of the NMDA receptor NR1 is altered in kindling hippocampus. Eur. J. Neurosci. 7:1995;2513-2517.
69. Watanabe M., Inoue Y., Sakimura K., Mishima M. Distinct distributions of five N-methyl-D-aspartate receptor channel subunit nRNAs in the forebrain. J. Comp. Neurol. 338:1993;377-390.
70. Watanabe Y., Johnson R.S., Butler L.S., Binder D.K., Spigelman B.M., Papaioannou V.E., Mc Namara J.O. Null mutation of c-fos impairs structural and functional plasticities in the kindling model of epilepsy. J. Neurosci. 16:1996;3827-3836.
71. Yeh G.-C., Bonhaus D.W., Nadler J.V., McNamara J.O. N-methyl-D-aspartate receptor plasticity in kindling: Quantitative and qualitative alterations in the N-methyl-D-aspartate receptor-channel complex. Proc. Acad. Sci. USA. 86:1989;8157-8160.
72. Zukin R.S., Bennett M.V.L. Alternatively spliced isoforms of the NMDAR1 subunit. Trends Neurosci. 18:1995;306-313.