Role of the NR2A/2B subunits of the N-methyl-d-aspartate receptor in glutamate-induced glutamic acid decarboxylase alteration in cortical GABAergic neurons in vitro

Neuroscience

Volumn 171, Issue 4, 2010, Pages 1075-1090

  Monnerie, H ^a   Hsu, F C ^b   Coulter, D A ^a,b   Le Roux, P D ^a  

^a UNIVERSITY OF PENNSYLVANIA   (United States)

^b CHILDREN S HOSPITAL OF PHILADELPHIA   (United States)

Author keywords

Calpain; Cerebral cortex; Excitatory amino acids; Excitotoxicity; GABAergic neurons; NMDA receptors

Indexed keywords

4 AMINOBUTYRIC ACID RECEPTOR; CALPAIN; EXCITATORY AMINO ACID; GLUTAMATE DECARBOXYLASE; GLUTAMATE DECARBOXYLASE 65; GLUTAMATE DECARBOXYLASE 67; GLUTAMIC ACID; N METHYL DEXTRO ASPARTIC ACID RECEPTOR; N METHYL DEXTRO ASPARTIC ACID RECEPTOR 2A; N METHYL DEXTRO ASPARTIC ACID RECEPTOR 2B;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; BRAIN CORTEX; CELL CULTURE; CELL SURVIVAL; CELL VIABILITY; CONTROLLED STUDY; DOSE RESPONSE; EXCITATION AND STIMULATION; EXCITATORY POSTSYNAPTIC POTENTIAL; EXCITOTOXICITY; GABAERGIC SYSTEM; IN VITRO STUDY; MOUSE; NERVE CELL CULTURE; NONHUMAN; POSTSYNAPTIC MEMBRANE; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN FUNCTION; SIGNAL TRANSDUCTION; WESTERN BLOTTING;

ANALYSIS OF VARIANCE; ANIMALS; BICUCULLINE; CALPAIN; CELL SURVIVAL; CELLS, CULTURED; CEREBRAL CORTEX; DOSE-RESPONSE RELATIONSHIP, DRUG; DRUG INTERACTIONS; EMBRYO, MAMMALIAN; ENZYME INHIBITORS; EXCITATORY AMINO ACID AGENTS; GABA AGENTS; GAMMA-AMINOBUTYRIC ACID; GENE EXPRESSION REGULATION; GLUTAMATE DECARBOXYLASE; GLUTAMIC ACID; GLYCINE AGENTS; MEMBRANE POTENTIALS; MICE; MICE, INBRED BALB C; NEURONS; PATCH-CLAMP TECHNIQUES; RECEPTORS, N-METHYL-D-ASPARTATE; STRYCHNINE;

EID: 78650173475     PISSN: 03064522     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.neuroscience.2010.09.050     Document Type: Article

References (69)

1. Auberson Y.P., Allgeier H., Bischoff S., Lingenhoehl K., Moretti R., Schmutz M. 5-phosphonomethylquinoxalinediones as competitive NMDA receptor antagonists with a preference for the human 1A/2A, rather 1A/2B receptor composition. Bioorg Med Chem Lett 2002, 12:1099-1102.
2. Becerra G.D., Tatko L.M., Pak E.S., Murashov A.K., Hoane M.R. Transplantation of GABAergic neurons but not astrocytes induced recovery of sensorimotor function in the traumatically injured brain. Behav Brain Res 2007, 179:118-125.
3. Bengtson C.P., Dick O., Bading H. A quantitative method to assess extrasynaptic NMDA receptor function in the protective effect of synaptic activity against neurotoxicity. BMC Neurosci 2008, 9:11.
4. 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.
5. Bonislawski D.P., Schwarzbach E.P., Cohen A.S. Brain injury impairs dentate gyrus inhibitory efficacy. Neurobiol Dis 2007, 25:163-169.
6. Centonze D., Marfia G.A., Pisani A., Picconi B., Bernardi G., Calabresi P. Ionic mechanisms underlying differential vulnerability to ischemia in striatal neurons. Prog Neurobiol 2001, 63:687-696.
7. Cortez S.C., Mcintosh T.K., Noble L.J. Experimental fluid percussion brain injury: vascular disruption and neuronal and glial alterations. Brain Res 1989, 482:271-282.
8. Cull-Candy S.G., Brickley S., Farrant M. NMDA receptor subunits: diversity, development and disease. Curr Opin Neurobiol 2001, 11:327-335.
9. Cull-Candy S.G., Leszkiewick D.N. Role of distinct NMDA receptor subtypes at central synapses. Sci STKE 2004, 255:re16.
10. Dani V.S., Chang Q., Maffei A., Turrigiano G.G., Jaenisch R., Nelson S.B. Reduced cortical activity due to a shift in the balance between excitation and inhibition in a mouse model of Rett syndrome. Proc Natl Acad Sci U S A 2005, 102:12560-12565.
11. Deng Y.P., Albin R.L., Penney J.B., Young A.B., Anderson K.D., Reiner A. Differential loss of striatal projection systems in Huntington's disease: a quantitative immunohistochemical study. J Chem Neuroanat 2004, 27:143-164.
12. Dong Y.N., Waxman E.A., Lynch D.R. Interactions of postsynaptic density-95 and the NMDA receptor 2 subunit control calpain-mediated cleavage of the NMDA receptor. J Neurosci 2004, 24:11035-11045.
13. Dong Y.N., Wu H.Y., Hsu F.C., Coulter D.A., Lynch D.R. Developmental and cell-selective variations in N-methyl-d aspartate receptor degradation by calpain. J Neurochem 2006, 99:206-217.
14. Engelhardt J., Coserea I., Pawlak V., Fuchs E.C., Kohr G., Seeburg P.H., Monyer H. Excitotoxicity in vitro by NR2A- and NR2B-containing NMDA receptors. Neuropharmacology 2007, 53:10-17.
15. Fatemi S.H., Halt A.R., Stary J.M., Kanodia R., Schultz S.C., Realmuto G.R. Glutamic acid decarboxylase 65 and 67 kDa proteins are reduced in autistic parietal and cerebellar cortices. Biol Psych 2002, 52:805-810.
16. Feng B., Tse H.W., Skifter D.A., Morley R., Jane D.E., Monaghan D.T. Structure-activity analysis of a novel NR2C/NR2D-preferring NMDA receptor antagonist: 1-(phenanthrene-2-carbonyl)piperazine-2,3-dicarboxylic acid. Br J Pharmacol 2004, 141:508-516.
17. Frahm C., Haupt C., Witte O.W. GABA neurons survive focal ischemic injury. Neuroscience 2004, 127:341-346.
18. Gascon S., Sobrado M., Roda J., Rodriguez-Pena A., Diaz-Guerra M. Excitotoxicity and focal cerebral ischemia induce truncation of the NR2A and NR2B subunits of the NMDA receptor and cleavage of the scaffolding protein PSD-95. Mol Psychiatry 2008, 13:99-114.
19. Giorgi S., Rimoldi M., Rossi M., Consolo S. The parafascicular thalamic nucleus modulates messenger RNA encoding glutamate decarboxylase 67 in rat striatum. Neuroscience 1997, 80:793-801.
20. 2 deprivation in the central nervous system: on the mechanisms of neuronal response, differential sensitivity and injury. Prog Neurobiol 1993, 40:277-318.
21. 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.
22. Hatton C.J., Paoletti P. Modulation of triheteromeric NMDA receptors by N-terminal domain ligands. Neuron 2005, 46:261-274.
23. Heckers S., Stone D., Walsh J., Shick J., Koul P., Benes F.M. Differential hippocampal expression of glumatic acid decarboxylase 65 and 67 messenger RNA in bipolar disorder and schizophrenia. Arch Gen Psychiatry 2002, 59:521-529.
24. Ivanov A., Pellegrino C., Rama S., Dumalska I., Salyha Y., Ben-Ari Y., Medina I. Opposing role of synaptic and extrasynaptic NMDA receptors in regulation of the extracellular signal-regulated kinases (ERK) activity in cultured rat hippocampal neurons. J Physiol 2006, 572(3):789-798.
25. Kang T.C., Park S.K., Hwang I.K., An J.J., Choi S.Y., Cho S.W., Won M.H. Spatial and temporal alterations in the GABA shunt in the gerbil hippocampus following transient ischemia. Brain Res 2002, 944:10-18.
26. Katayama Y., Becker D.P., Tamura T., Hovda D.A. Massive increases in extracellular potassium and indiscriminate release of glutamate following concussive brain injury. J Neurosurg 1990, 73:889-900.
27. Kinney J.W., Davis C.N., Tabarean I., Conti B., Bartfai T., Behrens M.M. A specific role for NR2A-containing NMDA receptors in the maintenance of parvalbumin and GAD67 immunoreactivity in cultured interneurons. J Neurosci 2006, 26:1604-1615.
28. Klein R.C., Prorok M., Castellino F.J. Direct binding properties of conantokins to native N-methyl d-aspartate receptors. J Peptide Res 2003, 61:307-317.
29. Klein R.C., Prorok M., Galdzicki Z., Castellino F.J. The amino acid residue at sequence position 5 in the conantokin peptides partially governs subunit-selective antagonism of recombinant N-methyl-d-aspartate receptors. J Biol Chem 2001, 276:26860-26867.
30. Lee J.M., Grabb M.C., Zipfel G., Choi W. Brain tissue response to ischemia. J Clin Invest 2000, 106:723-731.
31. Leveille F., El gaamouch T., Gouix E., Lecocq M., Lobner D., Nicole O., Buisson A. Neuronal viability is controlled by a functional relation between synaptic and extrasynaptic NMDA receptors. FASEB J 2008, 22:4258-4271.
32. Lewis D.A., Hashimoto T., Volk D.W. Cortical inhibitory neurons and schizophrenia. Nat Rev Neurosci 2005, 6:312-324.
33. Liu Y., Wong T.P., Aarts M., Rooyakkers A., Liu L., Lai T.W., Wu D.C., Lu J., Tymianski M., Craig A.M., Wang Y.T. NMDA receptor subunits have differential roles in mediating excitotoxic neuronal death both in vitro and in vivo. J Neurosci 2007, 27:2846-2857.
34. Lowenstein D.H., Thomas M.J., Smith D.H., Mcintosh T.K. Selective vulnerability of dentate hilar neurons following traumatic brain injury: a potential mechanistic link between head trauma and disorders of the hippocampus. J Neurosci 1992, 12:4846-4853.
35. Monnerie H., Le Roux P. Reduced dendrite growth and altered glutamic acid decarboxylase (GAD) 65- and 67-kDa isoform protein expression from mouse cortical GABAergic neurons following excitotoxic injury in vitro. Exp Neurol 2007, 205:367-382.
36. Monnerie H., Le Roux P.D. Glutamate alteration of glutamic acid decarboxylase (GAD) in GABAergic neurons: the role of cystein proteases. Exp Neurol 2008, 213:145-153.
37. Morrison B., Meaney D.F., Margulies S.S., McIntosh T.K. Dynamic mechanical stretch of organotypic brain slice cultures induces differential genomic expression: relationship to mechanical parameters. J Biomech Eng 2000, 122:224-230.
38. Najlerahim A., Pearson R.C.A. Changes in glutamic acid decarboxylase mRNA in the pallidum of the rat following unilateral damage of the striatum and overlying cortex. Exp Neurol 1992, 118:352-356.
39. Najlerahim A., Showell D.G., Pearson R.C. Transient increase in glutamic acid decarboxylase mRNA in the cerebral cortex following focal cortical lesion in the rat. Exp Brain Res 1991, 87:113-118.
40. Najlerahim A., Williams S.F., Pearson R.C.A., Jefferys J.G.R. Increased expression of GAD mRNA during the chronic epileptic syndrome due to intrahippocampal tetanus toxin. Exp Brain Res 1992, 90:332-342.
41. Neder L., Valente V., Carlotti C.G. Glutamate NMDA receptor subunit R1 and GAD mRNA expression in human temporal lobe epilepsy. Cell Mol Neurobiol 2002, 22:689-698.
42. Neyton J., Paoletti P. Relating NMDA receptor function to receptor subunit composition: limitations of the pharmacological approach. J Neurosci 2006, 26:1331-1333.
43. Obenaus A., Esclapez M., Hauser C.R. Loss of glutamate decarboxylase mRNA-containing neurons in the rat dentate gyrus following pilocarpine-induced seizures. J Neurosci 1993, 13:4470-4485.
44. O'Donnell L.A., Agrawal A., Jordan-Sciutto K.L., Dichter M.A., Lynch D.R., Kolson D.L. Human immunodeficiency virus (HIV)-induced neurotoxicity: roles for the NMDA receptor subtypes 2A and 2B and the calcium-activated protease calpain by a CSF-derived HIV-1 strain. J Neurosci 2006, 26:981-990.
45. Olney J.W., Collins R.C., Sloviter R.S. Excitotoxic mechanisms of epileptic brain damage. Adv Neurol 1986, 44:857-877.
46. Papadia S., Soriano F.X., Leveille F., Martel M.A., Dakin K.A., Hansen H., Kaindl A., Sifringer M., Fowler J., Mckenzie G., Craigon M., Corriveau R., Ghazal P., Horsburgh K., Yankner B., Wyllie D., Ikonomidou C., Hardingham G.E. Synaptic NMDA receptor activity boosts intrinsic antioxidant defenses. Nat Neurosci 2008, 11:476-487.
47. Pulsinelli W.A. Selective neuronal vulnerability: morphological and molecular characteristics. Prog Brain Res 1985, 63:29-37.
48. Ribak C.E., Harris A.B., Vaughn J.E., Roberts E. Inhibitory, GABAergic nerve terminals decrease at sites of focal epilepsy. Science 1979, 205:211-214.
49. Ross S.T., Soltesz I. Selective depolarization of interneurons in the early posttraumatic dentate gyrus: involvement of the Na+/K+-ATPase. J Neurophysiol 2000, 83:2916-2930.
50. Saji M., Cohen M., Blau A.D., Wessel T.C., Volpe B.T. Transient forebrain ischemia induces delayed injury in the substantia nigra reticulata: degeneration of GABA neurons, compensatory expression of GAD mRNA. Brain Res 1994, 643:234-244.
51. Salin P., Chesselet M.F. Expression of GAD67 and its messenger RNA in basal ganglia and cerebral cortex after ischemic cortical lesions in rats. Exp Neurol 1993, 119:291-301.
52. Schwartz-Bloom R.D., Sah R. γ-Aminobutyric acid neurotransmission and cerebral ischemia. J Neurochem 2001, 77:353-371.
53. Shetty A.K., Turner D.A. Glutamic acid decarboxylase-67-positive hippocampal interneurons undergo a permanent reduction in number following kainic acid-induced degeneration of CA3 pyramidal neurons. Exp Neurol 2001, 169:276-297.
54. Simon R.P., Griffiths T., Evans M.C., Swan J.H., Meldrum B.S. Calcium overload in selectively vulnerable neurons in the hippocampus during and after ischemia: an electron microscopy study in the rat. J Cereb Blood Flow Metab 1984, 4:350-361.
55. Simpkins K.L., Guttmann R.P., Dong Y., Chen Z., Sokol S., Neumar R.W., Lynch D.R. Selective activation induced cleavage of the NR2B subunit by calpain. J Neurosci 2003, 23:11322-11331.
56. Soghomonian J., Laprade N. Glutamate decarboxylase (GAD67 and GAD65) gene expression is increased subpopulation of neurons in the putamen of parkinsonian monkeys. Synapse 1997, 27:122-132.
57. Soghomonian J.J., Martin D.L. Two isoforms of glutamate decarboxylase: why?. TIPS 1998, 19:500-505.
58. Tecoma E.S., Choi D.W. GABAergic neocortical neurons are resistant to NMDA receptor-mediated injury. Neurology 1989, 39:676-682.
59. Thomas C.G., Miller A.J., Westbrook G.L. Synaptic and extrasynaptic NMDA receptor NR2 subunits in cultured hippocampal neurons. J Neurophysiol 2006, 95:1727-1734.
60. Torrey E.F., Barci B.M., Webster M.J., Bartko J.J., Meador-Woodruff J.H., Knable M.B. Neurochemical markers for schizophrenia, bipolar disorder, and major depression in portmortem brains. Biol Psychiatry 2005, 57:252-260.
61. Toth Z., Hollrigel G.S., Gorcs T., Soltesz I. Instantaneous perturbation of dentate interneuronal networks by a pressure wave-transient delivered to the neocortex. J Neurosci 1997, 17:8106-8117.
62. Waxman E.A., Lynch D.R. N-methyl-d-aspartate receptor subtypes: multiple roles in excitotoxicity and neurological disease. Neuroscientist 2005, 11:37-49.
63. Witgen B.M., Lifshitz J., Smith M.L., Schwartzbach E., Liang S.L., Grady M.S., Cohen A.S. Regional hippocampal alteration associated with cognitive deficit following experimental brain injury: a systems, network and cellular evaluation. Neuroscience 2005, 133:1-15.
64. Wu H.Y., Hsu F.C., Gleichman A.J., Baconguis I., Coulter D.A., Lynch D.R. Fyn-mediated phosphorylation of NR2B Tyr-1336 controls calpain-mediated NR2B cleavage in neurons and heterologous systems. J Biol Chem 2007, 282:20075-20087.
65. Wu H.Y., Lynch D.R. Calpain and synaptic function. Mol Neurobiol 2006, 33:215-236.
66. Wu H.Y., Yuen E.Y., Lu Y.F., Matsushita M., Matsui H., Yan Z., Tomizawa K. Regulation of NMDA receptors by calpain in cortical neurons. J Biol Chem 2005, 280:21588-21593.
67. Yang L., Benardo L.S., Valsamis H., Ling D.S.F. Acute injury to superficial cortex leads to a decrease in synaptic inhibitio and increase in excitation in neocortical layer V pyramidal cells. J Neurophysiol 2007, 97:178-187.
68. Zhang S., Steijaert M.N., Lau D., Schutz G., Delucinge-Vivier C., Descombes P., Bading H. Decoding NMDAreceptor signaling: identification of genomic programs specifying neuronal survival and death. Neuron 2007, 53:549-562.
69. Zhou M., Baudry M. Developmental changes in NMDA neurotoxicity developmental changes in subunit composition of NMDA receptors. J Neurosci 2006, 26:2956-2963.