Kindling induces the long-lasting expression of a novel population of NMDA receptors in hippocampal region CA3

Journal of Neuroscience

Volumn 14, Issue 7, 1994, Pages 4196-4205

  Kraus, John E ^a   Yeh, Geng Chang ^a,c   Bonhaus, Douglas W ^a,d   Nadler, J Victor ^a   McNamara, James O ^a,b  

^a DUKE UNIVERSITY MEDICAL CENTER   (United States)

^b DURHAM VA MEDICAL CENTER   (United States)

^c TAIPEI MEDICAL UNIVERSITY   (Taiwan)

^d ROCHE BIOSCIENCE   (United States)

Author keywords

epilepsy; hippocampus; in situ hybridization; kindling; NMDA receptor; plasticity

Indexed keywords

4 PHOSPHONOMETHYLPIPECOLIC ACID; BINDING PROTEIN; GLUTAMATE RECEPTOR; MESSENGER RNA; N METHYL DEXTRO ASPARTIC ACID; N METHYL DEXTRO ASPARTIC ACID RECEPTOR; N METHYL DEXTRO ASPARTIC ACID RECEPTOR BLOCKING AGENT;

ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; BINDING SITE; CELL MEMBRANE DEPOLARIZATION; CONTROLLED STUDY; DENTATE GYRUS; ELECTROSTIMULATION; EPILEPSY; GENE EXPRESSION; GRANULE CELL; HIPPOCAMPUS; IN SITU HYBRIDIZATION; KINDLING; LIGAND BINDING; MALE; NERVE CELL EXCITABILITY; NERVE CELL PLASTICITY; NONHUMAN; PRIORITY JOURNAL; PYRAMIDAL NERVE CELL; RAT; SEIZURE;

EID: 0028246080     PISSN: 02706474     EISSN: None     Source Type: Journal    
DOI: 10.1523/jneurosci.14-07-04196.1994     Document Type: Article

References (56)

1. Akiyama K, Yoneda Y, Ogita K, Itoh T, Daigen A, Sora I, Kohira I, Ujike H, Otsuki S (1992) Brain Res 587:73-82.
2. Bonhaus DW, McNamara JO (1988) N-methyl-D-aspartate receptor regulation of uncompetitive antagonist binding in rat brain membranes: kinetic analysis. Mol Pharmacol 34:250-255.
3. Bonhaus DW, McNamara JO (1989) TCP binding: a tool for studying NMDA receptor-mediated neurotransmission in kindling. Neurosci Biobehav Rev 13:261-267.
4. Bonhaus DW, Yeh G-C, Skaryak L, McNamara JO (1989) Glycine regulation of N-methyl-D-aspartate receptor-gated ion channel in hippocampal membranes. Mol Pharmacol 36:273-279.
5. Cain DP, Desborough KA, McKitrick DJ (1988) Retardation of amygdala kindling by antagonism of N-methyl-D-aspartate and muscarinic cholinergic receptors: evidence for summation of excitatory mechanisms in kindling. Exp Neurol 100:179-187.
6. Callaghan DA, Schwark WS (1980) Pharmacological modification of amygdaloid-kindled seizures. Neuropharmacology 19:1131-1136.
7. Deuchars J, Thomson AM (1993) Synapses and receptors: a molecular perspective in honour of Professor E. A. Barnard. Trends Neurosci 16:43-45.
8. Dingledine R, Hynes MA, King GL (1986) Involvement of N-methyl-D-aspartate receptors in epileptiform bursting in the rat hippocampal slice. J Physiol (Lond) 380:175-189.
9. Froehner SC, Luetje CW, Scotland PB, Patrick J (1990) The postsynaptic 43K protein clusters muscle nicotinic acetylcholine receptors in Xenopus oocytes. Neuron 5:403-410.
10. Goddard GV, McIntyre EC, Leech CK (1969) A permanent change in brain function resulting from daily electrical stimulation. Exp Neurol 25:295-330.
11. Green JD (1964) The hippocampus. Physiol Rev 44:561-608.
12. Holmes KH, Goddard GV (1986) A role for the N-methyl-D-asparate in kindling. Proc Univ Otago Med Sch 64:37-39.
13. Holmes KH, Bilkey DK, Laverty R, Goddard GV (1990) The N-methyl-D-aspartate antagonists aminophosphonovalerate and carboxypiperazinephosphonate retard the development and expression of kindled seizures. Brain Res 506:227-235.
14. Ikeda K, Nagasawa M, Mori H, Araki K, Sakimura K, Watanabe M, Inoue Y, Mishina M (1992) Cloning and expression of the ε4 subunit of the NMDA receptor channel. FEBS Lett 313:34-38.
15. Ishii T, Moriyoshi K, Sugihara H, Sakurada K, Kadotani H, Yokoi M, Akazawa C, Shigemoto R, Mizuno N, Masu M, Nakanishi S (1993) Molecular characterization of the family of the N-methyl-D-aspartate receptor subunits. J Biol Chem 268:2836-2843.
16. King GL, Dingledine R, Giacchino JL, McNamara JO (1985) Abnormal neuronal excitability in hippocampal slices from kindled rats. J Neurophysiol 54:1295-1304.
17. Köhr G, De Koninck Y, Mody I (1993) Properties of NMDA receptor channels in neurons acutely isolated from epileptic (kindled) rats. J Neurosci 13:3612-3627.
18. Kraus JE, Yeh G-C, Bonhaus DW, Watanabe Y, Nadler JV, McNamara JO (1993) Induction of a novel NMDA receptor by kindling in CA3 is not related to alterations in NMDAR transcript levels. Soc Neurosci Abstr 19:925.
19. Kumar KN, Tilakaratne N, Johnson PS, Allen AE, Michaelis EK (1991) Cloning of cDNA for the glutamate-binding subunit of an NMDA receptor complex. Nature 354:70-73.
20. Kutsuwada T, Kashiwabuchi N, Mori H, Sakimura K, Kushiya E, Araki K, Meguro H, Masaki H, Kumanishi T, Arakawa M, Mishina M (1992) Molecular diversity of the NMDA receptor channel. Nature 358:36-41.
21. Löscher W, Hönack D (1991) Anticonvulsant and behavioral effects of two novel competitive N-methyl-D-aspartic acid receptor antagonists, CGP 37849 and CGP 39551, in the kindling model of epilepsy: comparison with MK-801 and carbamazepine. J Pharmacol Exp Ther 256:432-440.
22. Lowry OH, Rosebrough NJ, Farr AL, Randall RJ (1951) Protein measurement with the folin phenol reagent. J Biol Chem 193:265-275.
23. Martin D, McNamara JO, Nadler JV (1992) Kindling enhances sensitivity of CA3 hippocampal pyramidal cells to NMDA. J Neurosci 12:1928-1935.
24. McNamara JO, Russel RD, Rigsbee L, Bonhaus DW (1988a) Anticonvulsant and anti-epileptogenic actions of MK-801 in the kindling and electroshock models. Neuropharmacology 27:563-568.
25. McNamara JO, Bonhaus DW, Shin C (1988b) Mechanisms of kindling: a speculative hypothesis. In: Mechanisms of epileptogenesis (Dichter MA, ed), pp 85-99. New York: Plenum.
26. McNamara JO, Morrisett R, Nadler JV (1992) Recent advances in understanding mechanisms of the kindling model. Adv Neurol 57: 555-560.
27. McPherson GA (1985) A collection of radioligand binding analysis programs. Amsterdam: Elsevier.
28. Meguro H, Mori H, Araki K, Kushiya E, Kutsuwada T, Yamazaki M, Kumanishi T, Arakawa M, Sakimura K, Mishina M (1992) Functional characterization of a heteromeric NMDA receptor channel expressed from cloned cDNAs. Nature 357:70-74.
29. Mody I, Stanton PK, Heinneman U (1988) Activation of N-methyl-D-aspartate receptors parallels changes in cellular and synaptic properties of dentate granule cells after kindling. J Neurophysiol 59:1033-1054.
30. Monaghan DT, Olverman HJ, Nguyen L, Watkins JC, Cotman CW (1988) Two classes of N-methyl-D-aspartate recognition sites: differential distribution and differential regulation by glycine. Proc Natl Acad Sci USA 85:9836-9840.
31. Monyer H, Sprengel R, Schoepfer R, Herb A, Higuchi M, Lomeli H, Burnashev N, Sakmann B, Seeburg PH (1992) Heteromeric NMDA receptors: molecular and functional distinction of subtypes. Science 256:1217-1221.
32. Monyer H, Laurie DJ, Seeburg PH (1993) Ontogeny of NMDA receptors in the rat brain. Soc Neurosci Abstr 19:648.
33. Moriyoshi K, Masu M, Ishii T, Shigemoto R, Mizuno N, Nakanishi S (1991) Molecular cloning and characterization of the rat NMDA receptor. Nature 354:31-37.
34. Morrisett RA, Chow C, Nadler JV, McNamara JO (1989) Biochemical evidence for enhanced sensitivity to N-methyl-D-aspartate in the hippocampal formation of kindled rats. Brain Res 496:25-28.
35. Morrisett RA, Chow C, Sakaguchi T, Shin C, McNamara JO (1990) Inhibition of muscarinic-coupled phosphoinositide hydrolysis by N-methyl-D-aspartate is dependent upon depolarization via channel activation. J Neurochem 54:1517-1525.
36. Nadler JV, Thompson MA, McNamara JO (1994) Kindling reduces sensitivity of CA3 hippocampal pyramidal cells to competitive NMDA receptor antagonists. Neuropharmacology, in press.
37. Nakanishi N, Axel A, Schneider NA (1992) Alternative splicing generates functionally distinct N-methyl-D-aspartate receptors. Proc Natl Acad Sci USA 89:8552-8556.
38. Nakanishi S (1992) Molecular diversity of glutamate receptors and implications for brain function. Science 258:597-603.
39. Okazaki MM, McNamara JO, Nadler JV (1989) N-methyl-D-aspartate receptor autoradiography in rat brain after angular bundle kindling. Brain Res 482:359-364.
40. Okazaki MM, McNamara JO, Nadler JV (1990) Kainate and quisqualate receptor autoradiography in rat brain after angular bundle kindling. Neuroscience 37:135-142.
41. Otis TS, Mody I (1993) Three mechanisms for increased GABAergic inhibition after kindling-induced epilepsy. Soc Neurosci Abstr 19: 1267.
42. Paré D, deCurtis M, Llinás R (1992) Role of the hippocampal-entorhinal loop in temporal lobe epilepsy: extra- and intracellular study in the isolated guinea pig brain in vitro. J Neurosci 12:1867-1881.
43. Paxinos G, Watson C (1986) The rat brain in stereotactic coordinates, 2d ed. New York: Academic.
44. Peterson DW, Collins JF, Bradford HF (1983) The kindled amygdala model of epilepsy: anticonvulsant action of amino acid antagonism. Brain Res 275:169-172.
45. Peterson DW, Collins JF, Bradford HF (1984) Anticonvulsant action of amino acid antagonists against kindled hippocampal seizures. Brain Res 311:176-180.
46. Racine RJ (1972) Modulation of seizure activity by electrical stimulation. II. Motor seizure. Electroencephalogr Clin Neurophysiol 32: 281-294.
47. Raymond LA, Blackstone CD, Huganir RL (1993) Phosphorylation and modulation of recombinant GluR6 receptors by cAMP-dependent protein kinase. Nature 361:637-641.
48. Rogers SW, Hughs TE, Hollmann M, Gasic GP, Deneris ES, Heinemann S (1991) The characterization and localization of the glutamate receptor subunit GluR1 in the rat brain. J Neurosci 11:2713-2724.
49. Savage DD, Werling LL, Nadler JV, McNamara JO (1984a) Selective and reversible increase in the number of quisqualate-sensitive glutamate binding sites on hippocampal synaptic membranes after angular bundle kindling. Brain Res 307:332-335.
50. Savage DD, Nadler JV, McNamara JO (1984b) Reduced kainate acid binding in rat hippocampal formation after limbic kindling. Brain Res 323:128-131.
51. Shin C, Pedersen HB, McNamara JO (1985) γ-Aminobutyric acid and benzodiazepine receptors in the kindling model of epilepsy: a quantitative radiohistochemical study. J Neurosci 5:2696-2701.
52. Sugihara H, Moriyoshi K, Ishii T, Masu M, Nakanishi S (1992) Structures and properties of seven genes of the NMDA receptor generated by alternative splicing. Biochem Biophys Res Commun 185:826-836.
53. Tingley WG, Roche KW, Thompson AK, Huganir RL (1993) Regulation of NMDA receptor phosphorylation by alternative splicing of the C-terminal domain. Nature 364:70-73.
54. Traub RD, Miles R, Jefferys JGR (1993) Synaptic and intrinsic conductances shape picrotoxin-induced synchronized after-discharges in the guinea-pig hippocampal slice. J Physiol (Lond) 461:525-547.
55. Wisden W, Morris BJ, Hunt SP (1991) In situ hybridization with synthetic DNA probes. In: Molecular neurobiology: a practical approach (Chad J, Wheal H, eds), pp 205-225. New York: IRL Press at Oxford UP.
56. Yeh G-C, Bonhaus DW, Nadler JV, McNamara JO (1989) N-methyl-D-aspartate receptor plasticity in kindling: quantitative and qualitative alterations in the N-methyl-D-aspartate receptor-channel complex. Proc Natl Acad Sci USA 86:8157-8160.