Rapid surface accumulation of NMDA receptors increases glutamatergic excitation during status epilepticus

Neurobiology of Disease

Volumn 54, Issue , 2013, Pages 225-238

  Naylor, David E ^a,b,d   Liu, Hantao ^b,d   Niquet, Jerome ^b,d   Wasterlain, Claude G ^b,c,d  

^a HARBOR UCLA MEDICAL CENTER   (United States)

^b VA GREATER LOS ANGELES HEALTHCARE SYSTEM   (United States)

^c UNIVERSITY OF CALIFORNIA   (United States)

^d UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

Epilepsy; Hippocampus; NMDA receptor trafficking; Status epilepticus; Synaptic excitation

Indexed keywords

IFENPRODIL; N METHYL DEXTRO ASPARTIC ACID; N METHYL DEXTRO ASPARTIC ACID RECEPTOR; N METHYL DEXTRO ASPARTIC ACID RECEPTOR 1; N METHYL DEXTRO ASPARTIC ACID RECEPTOR 2B;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; CELL LABELING; CELL SURFACE; CONTROLLED STUDY; DENTATE GYRUS; EPILEPTIC STATE; EXCITATION; EXCITATORY POSTSYNAPTIC POTENTIAL; EXCITOTOXICITY; GLUTAMATERGIC EXCITATION; GRANULE CELL; HIPPOCAMPAL CA3 REGION; IMMUNOCYTOCHEMISTRY; MALE; MOUSE; NERVE CELL STIMULATION; NONHUMAN; PRIORITY JOURNAL; PYRAMIDAL NERVE CELL; SYNAPSE;

ANIMALS; DISEASE MODELS, ANIMAL; EXCITATORY POSTSYNAPTIC POTENTIALS; GLUTAMIC ACID; HIPPOCAMPUS; IMMUNOHISTOCHEMISTRY; MALE; PATCH-CLAMP TECHNIQUES; PROTEIN TRANSPORT; RATS; RATS, WISTAR; RECEPTORS, N-METHYL-D-ASPARTATE; STATUS EPILEPTICUS; SYNAPSES;

EID: 84876337975     PISSN: 09699961     EISSN: 1095953X     Source Type: Journal    
DOI: 10.1016/j.nbd.2012.12.015     Document Type: Article

References (119)

1. Ali D.W., Salter M.W. NMDA receptor regulation by Src kinase signalling in excitatory synaptic transmission and plasticity. Curr. Opin. Neurobiol. 2001, 11:336-342.
2. Alldredge B.K., Gelb A.M., Isaacs S.M., Corry M.D., Allen F., Ulrich S., Gottwald M.D., O'Neil N., Neuhaus J.M., Segal M.R., Lowenstein D.H. A comparison of lorazepam, diazepam, and placebo for the treatment of out-of-hospital status epilepticus. N. Engl. J. Med. 2001, 345:631-637.
3. Bekkers J.M., Stevens C.F. NMDA and non-NMDA receptors are co-localized at individual excitatory synapses in cultured rat hippocampus. Nature 1989, 341:230-233.
4. Beldhuis H.J., Everts H.G., Van der Zee E.A., Luiten P.G., Bohus B. Amygdala kindling-induced seizures selectively impair spatial memory. 2. Effects on hippocampal neuronal and glial muscarinic acetylcholine receptor. Hippocampus 1992, 2:411-419.
5. Berberich S., Punnakkal P., Jensen V., Pawlak V., Seeburg P.H., Hvalby O., Kohr G. Lack of NMDA receptor subtype selectivity for hippocampal long-term potentiation. J. Neurosci. 2005, 25:6907-6910.
6. Bertram E.H., Lothman E.W. NMDA receptor antagonists and limbic status epilepticus: a comparison with standard anticonvulsants. Epilepsy Res. 1990, 5:177-184.
7. Borris D.J., Bertram E.H., Kapur J. Ketamine controls prolonged status epilepticus. Epilepsy Res. 2000, 42:117-122.
8. Brandt C., Potschka H., Loscher W., Ebert U. N-methyl-D-aspartate receptor blockade after status epilepticus protects against limbic brain damage but not against epilepsy in the kainate model of temporal lobe epilepsy. Neuroscience 2003, 118:727-740.
9. Brimecombe J.C., Boeckman F.A., Aizenman E. Functional consequences of NR2 subunit composition in single recombinant N-methyl-D-aspartate receptors. Proc. Natl. Acad. Sci. U. S. A. 1997, 94:11019-11024.
10. Carroll R.C., Zukin R.S. NMDA-receptor trafficking and targeting: implications for synaptic transmission and plasticity. Trends Neurosci. 2002, 25:571-577.
11. Chen J., Li H., Luo C., Li Z., Zheng J. Involvement of peripheral NMDA and non-NMDA receptors in development of persistent firing of spinal wide-dynamic-range neurons induced by subcutaneous bee venom injection in the cat. Brain Res. 1999, 844:98-105.
12. Chen N., Luo T., Raymond L.A. Subtype-dependence of NMDA receptor channel open probability. J. Neurosci. 1999, 19:6844-6854.
13. Chen N., Luo T., Wellington C., Metzler M., McCutcheon K., Hayden M.R., Raymond L.A. Subtype-specific enhancement of NMDA receptor currents by mutant huntingtin. J. Neurochem. 1999, 72:1890-1898.
14. Choi D.W. Calcium and excitotoxic neuronal injury. Ann. N. Y. Acad. Sci. 1994, 747:162-171.
15. Choi D.W. Glutamate receptors and the induction of excitotoxic neuronal death. Prog. Brain Res. 1994, 100:47-51.
16. Clark B.A., Farrant M., Cull-Candy S.G. A direct comparison of the single-channel properties of synaptic and extrasynaptic NMDA receptors. J. Neurosci. 1997, 17:107-116.
17. Clifford D.B., Olney J.W., Benz A.M., Fuller T.A., Zorumski C.F. Ketamine, phencyclidine, and MK-801 protect against kainic acid-induced seizure-related brain damage. Epilepsia 1990, 31:382-390.
18. DeLorenzo R.J., Hauser W.A., Towne A.R., Boggs J.G., Pellock J.M., Penberthy L., Garnett L., Fortner C.A., Ko D. A prospective, population-based epidemiologic study of status epilepticus in Richmond. Virginia. Neurology 1996, 46:1029-1035.
19. Delorenzo R.J., Sun D.A., Deshpande L.S. Cellular mechanisms underlying acquired epilepsy: the calcium hypothesis of the induction and maintainance of epilepsy. Pharmacol. Ther. 2005, 105:229-266.
20. DeRidder M.N., Simon M.J., Siman R., Auberson Y.P., Raghupathi R., Meaney D.F. Traumatic mechanical injury to the hippocampus in vitro causes regional caspase-3 and calpain activation that is influenced by NMDA receptor subunit composition. Neurobiol. Dis. 2006, 22:165-176.
21. Deshpande L.S., Lou J.K., Mian A., Blair R.E., Sombati S., Attkisson E., DeLorenzo R.J. Time course and mechanism of hippocampal neuronal death in an in vitro model of status epilepticus: role of NMDA receptor activation and NMDA dependent calcium entry. Eur. J. Pharmacol. 2008, 583:73-83.
22. Di Maio R., Mastroberardino P.G., Hu X., Montero L., Greenamyre J.T. Pilocarpine alters NMDA receptor expression and function in hippocampal neurons: NADPH oxidase and ERK 1/2 mechanisms. Neurobiol. Dis. 2011, 42:482-495.
23. Dunah A.W., Sirianni A.C., Fienberg A.A., Bastia E., Schwarzschild M.A., Standaert D.G. Dopamine D1-dependent trafficking of striatal N-methyl-D-aspartate glutamate receptors requires Fyn protein tyrosine kinase but not DARPP-32. Mol. Pharmacol. 2004, 65:121-129.
24. During M.J., Symes C.W., Lawlor P.A., Lin J., Dunning J., Fitzsimons H.L., Poulsen D., Leone P., Xu R., Dicker B.L., Lipski J., Young D. An oral vaccine against NMDAR1 with efficacy in experimental stroke and epilepsy. Science 2000, 287:1453-1460.
25. Erreger K., Dravid S.M., Banke T.G., Wyllie D.J., Traynelis S.F. Subunit-specific gating controls rat NR1/NR2A and NR1/NR2B NMDA channel kinetics and synaptic signalling profiles. J. Physiol. 2005, 563:345-358.
26. Flint A.C., Maisch U.S., Weishaupt J.H., Kriegstein A.R., Monyer H. NR2A subunit expression shortens NMDA receptor synaptic currents in developing neocortex. J. Neurosci. 1997, 17:2469-2476.
27. Fong D.K., Rao A., Crump F.T., Craig A.M. Rapid synaptic remodeling by protein kinase C: reciprocal translocation of NMDA receptors and calcium/calmodulin-dependent kinase II. J. Neurosci. 2002, 22:2153-2164.
28. Frasca A., Aalbers M., Frigerio F., Fiordaliso F., Salio M., Gobbi M., Cagnotto A., Gardoni F., Battaglia G.S., Hoogland G., Di Luca M., Vezzani A. Misplaced NMDA receptors in epileptogenesis contribute to excitotoxicity. Neurobiol. Dis. 2011, 43:507-515.
29. Friedman L.M., Matsuda Y., Lazarovici P. The microbial alkaloid toxin staurosporine blocks the phorbol ester-induced increase in beta-amyloid precursor protein in PC12 cells. Nat. Toxins 1997, 5:173-179.
30. Fujikawa D.G. Neuroprotective effect of ketamine administered after status epilepticus onset. Epilepsia 1995, 36:186-195.
31. Fujikawa D.G., Vannucci R.C., Dwyer B.E., Wasterlain C.G. Generalized seizures deplete brain energy reserves in normoxemic newborn monkeys. Brain Res. 1988, 454:51-59.
32. Gee C.E., Benquet P., Raineteau O., Rietschin L., Kirbach S.W., Gerber U. NMDA receptors and the differential ischemic vulnerability of hippocampal neurons. Eur. J. Neurosci. 2006, 23:2595-2603.
33. Goodkin H.P., Kapur J. Responsiveness of Status Epilepticus to Treatment with Diazepan Decreases Rapidly as Seizure Duration Increases. Epilepsy Curr. 2003, 3:11-12.
34. Goodkin H.P., Yeh J.L., Kapur J. Status epilepticus increases the intracellular accumulation of GABAA receptors. J. Neurosci. 2005, 25:5511-5520.
35. Goodkin H.P., Joshi S., Mtchedlishvili Z., Brar J., Kapur J. Subunit-specific trafficking of GABA(A) receptors during status epilepticus. J. Neurosci. 2008, 28:2527-2538.
36. Grosshans D.R., Clayton D.A., Coultrap S.J., Browning M.D. LTP leads to rapid surface expression of NMDA but not AMPA receptors in adult rat CA1. Nat. Neurosci. 2002, 5:27-33.
37. Guerguerian A.M., Brambrink A.M., Traystman R.J., Huganir R.L., Martin L.J. Altered expression and phosphorylation of N-methyl-D-aspartate receptors in piglet striatum after hypoxia-ischemia. Brain Res. Mol. Brain Res. 2002, 104:66-80.
38. Hardingham G.E., Fukunaga Y., Bading H. Extrasynaptic NMDARs oppose synaptic NMDARs by triggering CREB shut-off and cell death pathways. Nat. Neurosci. 2002, 5:405-414.
39. Harney S.C., Jane D.E., Anwyl R. Extrasynaptic NR2D-containing NMDARs are recruited to the synapse during LTP of NMDAR-EPSCs. J. Neurosci. 2008, 28:11685-11694.
40. Harty T.P., Rogawski M.A. Felbamate block of recombinant N-methyl-D-aspartate receptors: selectivity for the NR2B subunit. Epilepsy Res. 2000, 39:47-55.
41. Huo J.Z., Dykstra C.M., Gurd J.W. Increase in tyrosine phosphorylation of the NMDA receptor following the induction of status epilepticus. Neurosci. Lett. 2006, 401:266-270.
42. Johnston M.V., Nakajima W., Hagberg H. Mechanisms of hypoxic neurodegeneration in the developing brain. Neuroscientist 2002, 8:212-220.
43. Jones D.M., Esmaeil N., Maren S., Macdonald R.L. Characterization of pharmacoresistance to benzodiazepines in the rat Li-pilocarpine model of status epilepticus. Epilepsy Res. 2002, 50:301-312.
44. Kapur J., Lothman E.W. NMDA receptor activation mediates the loss of GABAergic inhibition induced by recurrent seizures. Epilepsy Res. 1990, 5:103-111.
45. Kapur J., Macdonald R.L. Rapid seizure-induced reduction of benzodiazepine and Zn2+ sensitivity of hippocampal dentate granule cell GABAA receptors. J. Neurosci. 1997, 17:7532-7540.
46. Kohira I., Akiyama K., Daigen A., Otsuki S. Enduring increase in membrane-associated protein kinase C activity in the hippocampal-kindled rat. Brain Res. 1992, 593:82-88.
47. Kohr G., Jensen V., Koester H.J., Mihaljevic A.L., Utvik J.K., Kvello A., Ottersen O.P., Seeburg P.H., Sprengel R., Hvalby O. Intracellular domains of NMDA receptor subtypes are determinants for long-term potentiation induction. J. Neurosci. 2003, 23:10791-10799.
48. Kornblum H.I., Sankar R., Shin D.H., Wasterlain C.G., Gall C.M. Induction of brain derived neurotrophic factor mRNA by seizures in neonatal and juvenile rat brain. Brain Res. Mol. Brain Res. 1997, 44:219-228.
49. Krupp J.J., Vissel B., Thomas C.G., Heinemann S.F., Westbrook G.L. Calcineurin acts via the C-terminus of NR2A to modulate desensitization of NMDA receptors. Neuropharmacology 2002, 42:593-602.
50. Lagarias J.C., Reeds J.A., Wright M.H., Wright P.E. Convergence properties of the Nelder-Mead simplex method in low dimensions. SIAM J. Optim. 1998, 9:112-147.
51. Lan J.Y., Skeberdis V.A., Jover T., Grooms S.Y., Lin Y., Araneda R.C., Zheng X., Bennett M.V., Zukin R.S. Protein kinase C modulates NMDA receptor trafficking and gating. Nat. Neurosci. 2001, 4:382-390.
52. Lau C.G., Zukin R.S. NMDA receptor trafficking in synaptic plasticity and neuropsychiatric disorders. Nat. Rev. Neurosci. 2007, 8:413-426.
53. Le Meur K., Galante M., Angulo M.C., Audinat E. Tonic activation of NMDA receptors by ambient glutamate of non-synaptic origin in the rat hippocampus. J. Physiol. 2007, 580:373-383.
54. Lekishvili T., Hesketh S., Brazier M.W., Brown D.R. Mouse galectin-1 inhibits the toxicity of glutamate by modifying NR1 NMDA receptor expression. Eur. J. Neurosci. 2006, 24:3017-3025.
55. Li B.S., Sun M.K., Zhang L., Takahashi S., Ma W., Vinade L., Kulkarni A.B., Brady R.O., Pant H.C. Regulation of NMDA receptors by cyclin-dependent kinase-5. Proc. Natl. Acad. Sci. U. S. A. 2001, 98:12742-12747.
56. Li B., Chen N., Luo T., Otsu Y., Murphy T.H., Raymond L.A. Differential regulation of synaptic and extra-synaptic NMDA receptors. Nat. Neurosci. 2002, 5:833-834.
57. Li B., Otsu Y., Murphy T.H., Raymond L.A. Developmental decrease in NMDA receptor desensitization associated with shift to synapse and interaction with postsynaptic density-95. J. Neurosci. 2003, 23:11244-11254.
58. Lieberman D.N., Mody I. Casein kinase-II regulates NMDA channel function in hippocampal neurons. Nat. Neurosci. 1999, 2:125-132.
59. Lieberman D.N., Mody I. Properties of single NMDA receptor channels in human dentate gyrus granule cells. J. Physiol. 1999, 518(Pt 1):55-70.
60. Lin Y., Skeberdis V.A., Francesconi A., Bennett M.V., Zukin R.S. Postsynaptic density protein-95 regulates NMDA channel gating and surface expression. J. Neurosci. 2004, 24:10138-10148.
61. Lin Y., Jover-Mengual T., Wong J., Bennett M.V., Zukin R.S. PSD-95 and PKC converge in regulating NMDA receptor trafficking and gating. Proc. Natl. Acad. Sci. U. S. A. 2006, 103:19902-19907.
62. Liu H., Mazarati A.M., Katsumori H., Sankar R., Wasterlain C.G. Substance P is expressed in hippocampal principal neurons during status epilepticus and plays a critical role in the maintenance of status epilepticus. Proc. Natl. Acad. Sci. U. S. A. 1999, 96:5286-5291.
63. Liu L., Wong T.P., Pozza M.F., Lingenhoehl K., Wang Y., Sheng M., Auberson Y.P., Wang Y.T. Role of NMDA receptor subtypes in governing the direction of hippocampal synaptic plasticity. Science 2004, 304:1021-1024.
64. Lothman E.W., Bertram E.H., Kapur J., Stringer J.L. Recurrent spontaneous hippocampal seizures in the rat as a chronic sequela to limbic status epilepticus. Epilepsy Res. 1990, 6:110-118.
65. Lu W.Y., Jackson M.F., Bai D., Orser B.A., MacDonald J.F. In CA1 pyramidal neurons of the hippocampus protein kinase C regulates calcium-dependent inactivation of NMDA receptors. J. Neurosci. 2000, 20:4452-4461.
66. Lu W., Man H., Ju W., Trimble W.S., MacDonald J.F., Wang Y.T. Activation of synaptic NMDA receptors induces membrane insertion of new AMPA receptors and LTP in cultured hippocampal neurons. Neuron 2001, 29:243-254.
67. Manzerra P., Behrens M.M., Canzoniero L.M., Wang X.Q., Heidinger V., Ichinose T., Yu S.P., Choi D.W. Zinc induces a Src family kinase-mediated up-regulation of NMDA receptor activity and excitotoxicity. Proc. Natl. Acad. Sci. U. S. A. 2001, 98:11055-11061.
68. Massey P.V., Johnson B.E., Moult P.R., Auberson Y.P., Brown M.W., Molnar E., Collingridge G.L., Bashir Z.I. Differential roles of NR2A and NR2B-containing NMDA receptors in cortical long-term potentiation and long-term depression. J. Neurosci. 2004, 24:7821-7828.
69. Mazarati A.M., Wasterlain C.G. N-methyl-D-asparate receptor antagonists abolish the maintenance phase of self-sustaining status epilepticus in rat. Neurosci. Lett. 1999, 265:187-190.
70. Mazarati A.M., Baldwin R.A., Sankar R., Wasterlain C.G. Time-dependent decrease in the effectiveness of antiepileptic drugs during the course of self-sustaining status epilepticus. Brain Res. 1998, 814:179-185.
71. Mazarati A.M., Wasterlain C.G., Sankar R., Shin D. Self-sustaining status epilepticus after brief electrical stimulation of the perforant path. Brain Res. 1998, 801:251-253.
72. Mazarati A.M., Baldwin R.A., Sofia R.D., Wasterain C.G. Felbamate in experimental model of status epilepticus. Epilepsia 2000, 41:123-127.
73. Mazarati A., Bragin A., Baldwin R., Shin D., Wilson C., Sankar R., Naylor D., Engel J., Wasterlain C.G. Epileptogenesis after self-sustaining status epilepticus. Epilepsia 2002, 43(Suppl. 5):74-80.
74. Mazarati A.M., Sofia R.D., Wasterlain C.G. Anticonvulsant and antiepileptogenic effects of fluorofelbamate in experimental status epilepticus. Seizure 2002, 11:423-430.
75. McDonald J.W., Silverstein F.S., Cardona D., Hudson C., Chen R., Johnston M.V. Systemic administration of MK-801 protects against N-methyl-D-aspartate- and quisqualate-mediated neurotoxicity in perinatal rats. Neuroscience 1990, 36:589-599.
76. McDonald J.W., Silverstein F.S., Johnston M.V. Magnesium reduces N-methyl-D-aspartate (NMDA)-mediated brain injury in perinatal rats. Neurosci. Lett. 1990, 109:234-238.
77. McNamara J.O., Russell R.D., Rigsbee L., Bonhaus D.W. Anticonvulsant and antiepileptogenic actions of MK-801 in the kindling and electroshock models. Neuropharmacology 1988, 27:563-568.
78. Mewasingh L.D., Sekhara T., Aeby A., Christiaens F.J., Dan B. Oral ketamine in paediatric non-convulsive status epilepticus. Seizure 2003, 12:483-489.
79. Milnerwood A.J., Gladding C.M., Pouladi M.A., Kaufman A.M., Hines R.M., Boyd J.D., Ko R.W., Vasuta O.C., Graham R.K., Hayden M.R., Murphy T.H., Raymond L.A. Early increase in extrasynaptic NMDA receptor signaling and expression contributes to phenotype onset in Huntington's disease mice. Neuron 2010, 65:178-190.
80. Moga D.E., Shapiro M.L., Morrison J.H. Bidirectional redistribution of AMPA but not NMDA receptors after perforant path simulation in the adult rat hippocampus in vivo. Hippocampus 2006, 16:990-1003.
81. Monyer H., Sprengel R., Schoepfer R., Herb A., Higuchi M., Lomeli H., Burnashev N., Sakmann B., Seeburg P.H. Heteromeric NMDA receptors: molecular and functional distinction of subtypes. Science 1992, 256:1217-1221.
82. Morrisett R.A., Jope R.S., Snead O.C. Effects of drugs on the initiation and maintenance of status epilepticus induced by administration of pilocarpine to lithium-pretreated rats. Exp. Neurol. 1987, 97:193-200.
83. Moussa R.C., Ikeda-Douglas C.J., Thakur V., Milgram N.W., Gurd J.W. Seizure activity results in increased tyrosine phosphorylation of the N-methyl-D-aspartate receptor in the hippocampus. Brain Res. Mol. Brain Res. 2001, 95:36-47.
84. Naylor D.E., Liu H., Wasterlain C.G. Trafficking of GABA(A) receptors, loss of inhibition, and a mechanism for pharmacoresistance in status epilepticus. J. Neurosci. 2005, 25:7724-7733.
85. Niimura M., Moussa R., Bissoon N., Ikeda-Douglas C., Milgram N.W., Gurd J.W. Changes in phosphorylation of the NMDA receptor in the rat hippocampus induced by status epilepticus. J. Neurochem. 2005, 92:1377-1385.
86. Nimchinsky E.A., Yasuda R., Oertner T.G., Svoboda K. The number of glutamate receptors opened by synaptic stimulation in single hippocampal spines. J. Neurosci. 2004, 24:2054-2064.
87. Osonoe K., Ogata S., Iwata Y., Mori N. Kindled amygdaloid seizures in rats cause immediate and transient increase in protein kinase C activity followed by transient suppression of the activity. Epilepsia 1994, 35:850-854.
88. Prasad A., Williamson J.M., Bertram E.H. Phenobarbital and MK-801, but not phenytoin, improve the long-term outcome of status epilepticus. Ann. Neurol. 2002, 51:175-181.
89. Prybylowski K., Fu Z., Losi G., Hawkins L.M., Luo J., Chang K., Wenthold R.J., Vicini S. Relationship between availability of NMDA receptor subunits and their expression at the synapse. J. Neurosci. 2002, 22:8902-8910.
90. Prybylowski K., Chang K., Sans N., Kan L., Vicini S., Wenthold R.J. The synaptic localization of NR2B-containing NMDA receptors is controlled by interactions with PDZ proteins and AP-2. Neuron 2005, 47:845-857.
91. Quinlan E.M., Olstein D.H., Bear M.F. Bidirectional, experience-dependent regulation of N-methyl-D-aspartate receptor subunit composition in the rat visual cortex during postnatal development. Proc. Natl. Acad. Sci. U. S. A. 1999, 96:12876-12880.
92. Quinlan E.M., Philpot B.D., Huganir R.L., Bear M.F. Rapid, experience-dependent expression of synaptic NMDA receptors in visual cortex in vivo. Nat. Neurosci. 1999, 2:352-357.
93. Racine R.J. Modification of seizure activity by electrical stimulation. II. Motor seizure. Electroencephalogr. Clin. Neurophysiol. 1972, 32:281-294.
94. Rho J.M., Donevan S.D., Rogawski M.A. Mechanism of action of the anticonvulsant felbamate: opposing effects on N-methyl-D-aspartate and gamma-aminobutyric acidA receptors. Ann. Neurol. 1994, 35:229-234.
95. Rice A.C., DeLorenzo R.J. NMDA receptor activation during status epilepticus is required for the development of epilepsy. Brain Res. 1998, 782:240-247.
96. Rice A.C., DeLorenzo R.J. N-methyl-D-aspartate receptor activation regulates refractoriness of status epilepticus to diazepam. Neuroscience 1999, 93:117-123.
97. Rycroft B.K., Gibb A.J. Regulation of single NMDA receptor channel activity by alpha-actinin and calmodulin in rat hippocampal granule cells. J. Physiol. 2004, 557:795-808.
98. Scott D.B., Blanpied T.A., Ehlers M.D. Coordinated PKA and PKC phosphorylation suppresses RXR-mediated ER retention and regulates the surface delivery of NMDA receptors. Neuropharmacology 2003, 45:755-767.
99. Seo D.W., Lopez-Meraz M.L., Allen S., Wasterlain C.G., Niquet J. Contribution of a mitochondrial pathway to excitotoxic neuronal necrosis. J. Neurosci. Res. 2009, 87:2087-2094.
100. Shi S.H., Hayashi Y., Petralia R.S., Zaman S.H., Wenthold R.J., Svoboda K., Malinow R. Rapid spine delivery and redistribution of AMPA receptors after synaptic NMDA receptor activation. Science 1999, 284:1811-1816.
101. Silbergleit R., Durkalski V., Lowenstein D., Conwit R., Pancioli A., Palesch Y., Barsan W. Intramuscular versus intravenous therapy for prehospital status epilepticus. N. Engl. J. Med. 2012, 366:591-600.
102. Snyder E.M., Nong Y., Almeida C.G., Paul S., Moran T., Choi E.Y., Nairn A.C., Salter M.W., Lombroso P.J., Gouras G.K., Greengard P. Regulation of NMDA receptor trafficking by amyloid-beta. Nat. Neurosci. 2005, 8:1051-1058.
103. Starr M.S., Starr B.S. The new competitive NMDA receptor antagonist CGP 40116 inhibits pilocarpine-induced limbic motor seizures and unconditioned motor behaviour in the mouse. Pharmacol. Biochem. Behav. 1994, 47:127-131.
104. Suchomelova L., Baldwin R.A., Kubova H., Thompson K.W., Sankar R., Wasterlain C.G. Treatment of experimental status epilepticus in immature rats: dissociation between anticonvulsant and antiepileptogenic effects. Pediatr. Res. 2006, 59:237-243.
105. Tovar K.R., Westbrook G.L. Mobile NMDA receptors at hippocampal synapses. Neuron 2002, 34:255-264.
106. Treiman D.M., Meyers P.D., Walton N.Y., Collins J.F., Colling C., Rowan A.J., Handforth A., Faught E., Calabrese V.P., Uthman B.M., Ramsay R.E., Mamdani M.B. A comparison of four treatments for generalized convulsive status epilepticus. Veterans Affairs Status Epilepticus Cooperative Study Group. N. Engl. J. Med. 1998, 339:792-798.
107. Triller A., Choquet D. Synaptic structure and diffusion dynamics of synaptic receptors. Biol. Cell 2003, 95:465-476.
108. van Zundert B., Yoshii A., Constantine-Paton M. Receptor compartmentalization and trafficking at glutamate synapses: a developmental proposal. Trends Neurosci. 2004, 27:428-437.
109. Vissel B., Krupp J.J., Heinemann S.F., Westbrook G.L. A use-dependent tyrosine dephosphorylation of NMDA receptors is independent of ion flux. Nat. Neurosci. 2001, 4:587-596.
110. Walton N.Y., Treiman D.M. Response of status epilepticus induced by lithium and pilocarpine to treatment with diazepam. Exp. Neurol. 1988, 101:267-275.
111. Wasterlain C.G. Inhibition of cerebral protein synthesis by epileptic seizures without motor manifestations. Neurology 1974, 24:175-180.
112. Wasterlain C.G., Liu H., Mazarati A.M., Baldwin R.A., Shirasaka Y., Katsumori H., Thompson K.W., Sankar R., Pereira de Vasconselos A., Nehlig A. Self-sustaining status epilepticus: a condition maintained by potentiation of glutamate receptors and by plastic changes in substance P and other peptide neuromodulators. Epilepsia 2000, 41(Suppl. 6):S134-S143.
113. Wasterlain C.G., Baldwin R., Naylor D.E., Thompson K.W., Suchomelova L., Niquet J. Rational polytherapy in the treatment of acute seizures and status epilepticus. Epilepsia 2011, 52(Suppl. 8):70-71.
114. Watt A.J., Sjostrom P.J., Hausser M., Nelson S.B., Turrigiano G.G. A proportional but slower NMDA potentiation follows AMPA potentiation in LTP. Nat. Neurosci. 2004, 7:518-524.
115. Wenthold R.J., Prybylowski K., Standley S., Sans N., Petralia R.S. Trafficking of NMDA receptors. Annu. Rev. Pharmacol. Toxicol. 2003, 43:335-358.
116. Wenthold R.J., Sans N., Standley S., Prybylowski K., Petralia R.S. Early events in the trafficking of N-methyl-D-aspartate (NMDA) receptors. Biochem. Soc. Trans. 2003, 31:885-888.
117. Wyneken U., Marengo J.J., Villanueva S., Soto D., Sandoval R., Gundelfinger E.D., Orrego F. Epilepsy-induced changes in signaling systems of human and rat postsynaptic densities. Epilepsia 2003, 44:243-246.
118. Yaka R., Thornton C., Vagts A.J., Phamluong K., Bonci A., Ron D. NMDA receptor function is regulated by the inhibitory scaffolding protein, RACK1. Proc. Natl. Acad. Sci. U. S. A. 2002, 99:5710-5715.
119. Yen W., Williamson J., Bertram E.H., Kapur J. A comparison of three NMDA receptor antagonists in the treatment of prolonged status epilepticus. Epilepsy Res. 2004, 59:43-50.