Localization of alternatively spliced NMDAR1 glutamate receptor isoforms in rat striatal neurons

Journal of Comparative Neurology

Volumn 415, Issue 2, 1999, Pages 204-217

  Küppenbender, Karsten D ^a   Albers, David S ^b   Iadarola, Michael J ^c   Landwehrmeyer, G Bernhard ^a   Standaert, David G ^b  

^a UNIVERSITY OF FREIBURG   (Germany)

^b MASSACHUSETTS GENERAL HOSPITAL   (United States)

^c NATIONAL INSTITUTE OF DENTAL AND CRANIOFACIAL RESEARCH   (United States)

Author keywords

Calbindin; Cholinergic; Glutamate receptors; Interneurons; Projection neurons; Striatum

Indexed keywords

ANTIBODY; CALBINDIN; CHOLINE; GLUTAMATE RECEPTOR; N METHYL DEXTRO ASPARTIC ACID RECEPTOR; NITRIC OXIDE SYNTHASE; PARVALBUMIN;

ANIMAL CELL; ANIMAL EXPERIMENT; ANTIBODY LABELING; ARTICLE; CHOLINERGIC SYSTEM; CONFOCAL MICROSCOPY; CORPUS STRIATUM; IMMUNOHISTOCHEMISTRY; IMMUNOREACTIVITY; INTERNEURON; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN LOCALIZATION; RAT; RNA SPLICING;

EID: 0345061653     PISSN: 00219967     EISSN: None     Source Type: Journal    
DOI: 10.1002/(SICI)1096-9861(19991213)415:2<204::AID-CNE5>3.3.CO;2-M     Document Type: Article

References (122)

1. Albers D, Weiss S, Iadarola M, Standaert D. 1999. Immunohistochemical localization of N-methyl-D-aspartate and alpha-amino-3-hydroxy-5-methyl-4-isoxazolepropionate receptor subunits in the substantia nigra pars compacta of the rat. Neuroscience 89:209-220.
2. Albin RL, Young AB, Penney JB. 1989. The functional anatomy of basal ganglia disorders. Trends Neurosci 12:366-375.
3. Albin RL, Reiner A, Anderson KD, Dure IV LS, Handelin B, Balfour R, Whetsell WO, Penney JB, Young AB. 1992. Preferential loss of striato-external pallidal projection neurons in presymptomatic Huntington's disease. Ann Neurol 31:425-430.
4. Anantharam V, Panchal RG, Wilson A, Kolchine W, Triestman SN, Bayley H. 1992. Combinatorial RNA splicing alters the surface charge on the NMDA receptor. FEBS Lett 305:27-30.
5. Aoki C. 1997. Postnatal changes in the laminar and subcellular distribution of NMDA-R1 subunits in the cat visual cortex as revealed by immunoelectron microscopy. Brain Res Dev Brain Res 98:41-59.
6. Aoki C, Venkatesan C, Go C-C, Mong JA, Dawson TM. 1994. Cellular and subcellular localization of NMDA-R1 subunit immunoreactivity in the visual cortex of adult and neonatal rats. J Neurosci 14:5202-5221.
7. Aoki C, Rhee J, Lubin M, Dawson TM. 1997. NMDA-R1 subunit of the cerebral cortex co-localizes with neuronal nitric oxide synthase at preand postsynaptic sites and in spines. Brain Res 750:25-40.
8. Armstrong DM, Saper CB, Levey AI, Wainer BH, Terry RD. 1983. Distribution of cholinergic neurons in the rat brain demonstrated by the immunocytochemical localization of choline acetyltransferase. J Comp Neurol 216:53-68.
9. Augood SJ, Faull RL, Love DR, Emson PC. 1996. Reduction in enkephalin and substance P messenger RNA in the striatum of early grade Huntington's disease: a detailed cellular in situ hybridization study. Neuroscience 72:1023-1036.
10. Beal MF, Kowall NW, Ellison DE, Mazurek MF, Swartz KJ, Martin JB. 1986. Replication of the neurochemical characteristics of Huntington's disease by quinolinic acid. Nature 321:168-171.
11. Beal MF, Ferrante RJ, Swartz KJ, Kowall NW. 1991. Chronic quinolinic acid lesions in rats closely resemble Huntington's disease. J Neurosci 11:1649-1659.
12. Bennett BD, Bolam JP. 1992. Characterization of calretinin-immunoreactive structures in the striatum of the rat. Brain Res 609:137-148.
13. 28k-immunoreactive neurones in the striatum of the rat. Brain Res 610:305-310.
14. Bernard V, Bolam JP. 1998. Subcellular and subsynaptic distribution of the NR1 subunit of the NMDA receptor in the neostriatum and globus pallidus of the rat: co-localization at synapses with the GluR2/3 subunit of the AMPA receptor. Eur J Neurosci 10:3721-3736.
15. Bernard V, Somogyi P, Bolam JP. 1997. Cellular, subcellular, and subsynaptic distribution of AMPA-type glutamate receptor subunits in the neostriatum of the rat. J Neurosci 17:819-833.
16. Berretta S, Parthasarathy HB, Graybiel AM. 1997. Local release of GABAergic inhibition in the motor cortex induces immediate-early gene expression in indirect pathway neurons of the striatum. J Neurosci 17:4752-4763.
17. Blahos J, Wenthold RJ. 1996. Relationship beween N-methyl-D-aspartate receptor NR1 splice variants and NR2 subunits. J Biol Chem 271:15669-15674.
18. Blank T, Nijholt I, Teichert U, Kugler H, Behrsing H, Fienberg A, Greengard P, Spiess J. 1997. The phosphoprotein DARPP-32 mediates cAMP-dependent potentiation of striatal N-methyl-D-aspartate responses. Proc Natl Acad Sci USA 94:14859-14864.
19. Bolam JP, Wainer BH, Smith AD. 1984. Characterisation of cholinergic neurons in the rat neostriatum. A combination of choline acetyltransferase immunocytochemistry, Golgi-impregnation and electron microscopy. Neuroscience 12:711-718.
20. Buller AL, Larson HC, Schneider BE, Beaton JA, Morisett RA, Monaghan DT. 1994. The molecular basis of NMDA receptor subtypes: native receptor diversity is predicted by subunit compostion. J Neuroci 14:5471-5484.
21. Bustos G, Abarca J, Forray MI, Gysling K, Bradberry CW, Roth RH. 1992. Regulation of excitatory amino acid release by N-methyl-D-aspartate receptors in rat striatum: in vivo microdialysis studies. Brain Res 585:105-115.
22. Calabresi P, Pisani A, Mercuri NB, Bernardi G. 1992. Long-term potentiation in the striatum is unmasked by removing the voltage-dependent magnesium block of NMDA receptor channels. Eur J Neurosci 4:929-935.
23. Calabresi P, Centonze D, Pisani A, Sancesario G, Gubellini P, Marfia GA, Bernardi G. 1998. Striatal spiny neurons and cholinergic interneurons express differential ionotropic glutamatergic responses and vulnerability: implications for ischemia and Huntington's disease. Ann Neurol 43:586-597.
24. Cepeda C, Buchwald NA, Levine MS. 1993. Neuromodulatory actions of dopamine in the neostriatum are dependent upon the excitatory amino acid receptor subtypes activated. Proc Natl Acad Sci USA 90:9576-9580.
25. Cepeda C, Colwell CS, Itri JN, Gruen E, Levine MS. 1998. Dopaminergic modulation of early signs of excitotoxicity in visualized rat neostriatal neurons. Eur J Neurosci 10:3491-3497.
26. 2+-calmodulin and protein kinase Cs: a hypothetical synthesis of their conflicting convergences on shared substrate domains. Trends Neurosci 22:12-16.
27. Chazot PL, Stephenson FA. 1997. Biochemical evidence for the existence of a pool of unassembled C2 exon-containing NR1 subunits of the mammalian forebrain NMDA receptor. J Neurochem 68:507-516.
28. Chen Q, Veenman CL, Reiner A. 1996. Cellular expression of ionotropic glutamate receptor subunits on specific striatal neuron types and its implications for striatal vulnerability in glutamate receptor-mediated excitotoxicity. Neuroscience 73:715-731.
29. Cowan RL, Wilson CJ, Emson PC, Heizmann CW. 1990. Parvalbumin-containing interneurons in the rat neostriatum. J Comp Neurol 302:197-205.
30. Damsma G, Robertson GS, Tham CS, Fibiger HC. 1991. Dopaminergic regulation of striatal acetylcholine release: importance of D1 and N-methyl-D-aspartate receptors. J Pharmacol Exp Ther 259:1064-1072.
31. Dawson TM, Bredt DS, Fotuhi M, Hwang PM, Snyder SH. 1991. Nitric oxide synthase and neuronal NADPH diaphorase are identical in brain and peripheral tissues. Proc Natl Acad Sci USA 88:7797-7801.
32. DiFiglia M. 1990. Excitotoxic injury of the neostriatum: a model for Huntington's disease. Trends Neurosci 13:286-289.
33. DiFiglia M, Christakos S, Aronin N. 1989. Ultrastructural localization of immunoreactive calbindin-D28K in the rat and monkey basal ganglia, including subcellular distribution with colloidal gold labeling. J Comp Neurol 279:653-665.
34. Dingledine R, Borges K, Bowie D, Traynelis SF. 1999. The glutamate receptor ion channels. Pharm Rev 51:7-61.
35. Divac I, Fonnum F, Storm-Mathison J. 1977. High affinity uptake of glutamate in terminals of corticostriatal axons. Nature 266:377-378.
36. Dubé L, Smith AD, Bolam JP. 1988. Identification of synaptic terminals of thalamic or cortical origin in contact with distinct medium size spiny neurons in rat neostriatum. J Comp Neurol 267:455-471.
37. Durand GM, Gregor P, Zheng X, Bennett MVL, Uhl GR, Zukin RS. 1992. Cloning of an apparent splice variant of the rat N-methyl-D-aspartate receptor NMDAR1 with altered sensitivity to polyamines and activators of protein kinase C. Proc Natl Acad Sci USA 89:9359-9363.
38. Ehlers MD, Tingley WG, Huganir RL. 1995. Regulated subcellular distribution of the NR1 subunit of the NMDA receptor. Science 269:1734-1737.
39. Ehlers MD, Zhang S, Bernhardt JP, Huganir RL. 1996. Inactivation of NMDA receptors by direct interaction of calmodulin with the NR1 subunit. Cell 84:745-755.
40. Ehlers MD, Fung ET, O'Brien RJ, Huganir RL. 1998. Splice variant-specific interaction of the NMDA receptor subunit NR1 with neuronal intermediate filaments. J Neurosci 18:720-730.
41. Farb CR, Aoki C, Ledoux JE. 1995. Differential localization of NMDA and AMPA receptor subunits in the lateral and basal nuclei of the amygdala: a light and electron microscopic study. J Comp Neurol 362:86-108.
42. Ferrante FJ, Kowall NW, Beal MF, Richardson EP, Martin JB. 1987a. Selective sparing of a class of neurons in Huntington's disease. Science 230:561-563.
43. Ferrante RJ, Beal MF, Kowall NW, Richardson EP, Martin JB. 1987b. Sparing of acetylcholinesterase-containing striatal neurons in Huntington's disease. Brain Res 411:162-166.
44. Fienberg AA, Hiroi N, Mermelstein PG, Song W, Snyder GL, Nishi A, Cheramy A, O'Callaghan JP, Miller DB, Cole DG, Corbett R, Haile CN, Cooper DC, Onn SP, Grace AA, Ouimet CC, White FJ, Hyman SE, Surmeier DJ, Girault J, Nestler EJ, Greengard P. 1998. DARPP-32: regulator of the efficacy of dopaminergic neurotransmission. Science 281:838-842.
45. Figueredo-Cardenas G, Anderson KD, Chen Q, Veenman CL, Reiner A. 1994. Relative survival of striatal projection neurons and interneurons after intrastriatal injection of QA in rats. Exp Neurol 129:37-56.
46. Gallagher MJ, Huang H, Grant ER, Lynch DR. 1997. The NR2B-specific interactions of polyamines and protons with the N-methyl-D-aspartate receptor. J Biol Chem 272:24971-24979.
47. Galli T, Desce JM, Artaud F, Kernel ML, Cheramy A, Glowinski J. 1992. Modulation of GABA release by alpha-amino-3-hydroxy-5-methylisoxazole-4-propionate and N-methyl-D-aspartate receptors in matrix-enriched areas of the rat striatum. Neuroscience 50:769-780.
48. Garcia-Munoz M, Patino P, Masliah E, Young SJ, Groves PM. 1996. Glutamate-dependent long-term presynaptic changes in corticostriatal excitability. Neuroscience 73:109-119.
49. Gerfen CR. 1992. The neostriatal mosaic: multiple levels of compartmental organization. Trends Neurosci 15:133-139.
50. Gerfen CR, Baimbridge KG, Miller JJ. 1985. The neostriatal mosaic: compartimental distribution of calcium-binding protein and parvalbumin in the basal ganglia of the rat and monkey. Proc Natl Acad Sci USA 82:8780-8784.
51. Götz T, Kraushaar U, Geiger J, Lübke J, Berger T, Jonas P. 1997. Functional properties of AMPA and NMDA recpetors expressed in identified types of basal ganglia neurons. J Neurosci 17:204-215.
52. Gracy KN, Pickel VM. 1995. Comparative ultrastructural localization of the NMDAR1 glutamate receptor in the rat basolateral amygdala and bed nucleus of the stria terminalis. J Comp Neurol 362:71-85.
53. Grant ER, Bacskai BJ, Anegawa NJ, Pleasure DE, Lynch DR. 1998. Opposing contributions of NR1 and NR2 to protein kinase C modulation of NMDA receptors. J Neurochem 71:1471-1481.
54. Graybiel AM. 1990. Neurotransmitters and neuromodulators in the basal ganglia. Trends Neurosci 13:244-254.
55. Halpain S, Girault JA, Greengard P. 1990. Activation of NMDA receptors induces dephosphorylation of DARPP-32 in rat striatal slices. Nature 343:369-372.
56. Harrington KM, Kowall NW. 1991. Parvalbumin immunoreactive neurons resist degeneration in Huntington's disease striatum. J Neuropathol Exp Neurol 50:309.
57. Hisatsune C, Umemori H, Inoue T, Michikawa T, Kohda K, Mikoshiba K, Yamamoto T. 1997. Phosphorylation-dependent regulation of N-methyl-D-aspartate receptors by calmodulin. J Biol Chem 272:20805-20810.
58. Hollmann M, Boulter J, Maron C, Beasley L, Sullivan J, Pecht G, Heinemann S. 1993. Zinc potentiates agonist induced currents at certain splice variants of the NMDA receptor. Neuron 10:943-954.
59. Huang PL, Dawson TM, Bredt DS, Synder SH, Fishman MC. 1993. Targeted disruption of the neuronal nitric oxide synthase gene. Cell 75:1273-1286.
60. Huntley GW, Vickers JC, Janssen W, Brose N, Heinemann SF, Morrison JH. 1994. Distribution and synaptic localization of immunocytochemically identified NMDA receptor subunit proteins in sensory-motor cortex and visual cortices of monkey and human. J Neurosci 14:3603-3619.
61. Iadarola MJ, Kim DJ, Caudle RM. 1996. Analysis of C-terminal splice variants of the NMDA NR1 subunit in spinal cord using sequence specific antisera. Soc Neurosci Abstr 22:1996.
62. Jacobowitz DM, Winsky L. 1991. Immunocytochemical localization of calretinin in the forebrain of the rat. J Comp Neurol 304:198-218.
63. Johnson RR, Jiang X, Burkhalter A. 1996. Regional and laminar differences in synaptic localization of NMDA receptor subunit NR1 splice variants in rat visual cortex and hippocampus. J Comp Neurol 368:335-355.
64. Kawaguchi Y, Wilson CJ, Augood SA, Emson PC. 1995. Striatal interneurons: chemical, physiological, and morphological characterization. Trends Neurosci 18:527-535.
65. Kim JS, Hassler R, Haug P, Paik KS. 1977. Effect of frontal cortex ablation on striatal glutamic acid level in the rat. Brain Res 132:370-374.
66. Kita H, Kitai ST. 1987. Efferent projections of the substhalamic nucleus in the rat: light and electron microscopic analysis with the PHA-L method. J Comp Neurol 260:435-452.
67. Kita H, Kosaka T, Heizmann CW. 1990. Parvalbumin-immunoreactive neurons in the rat neostriatum: a light and electron microscopic study. Brain Res 536:1-15.
68. Kiyama H, Seto-Ohshima A, Emson PC. 1990. Calbindin D28k as a marker for the degeneration of the striatonigral pathway in Huntington's disease. Brain Res 525:209-214.
69. Kornau HC, Schenker LT, Kennedy MB, Seeburg PH. 1995. Domain interaction between NMDA receptor subunits and the postsynaptic density protein PSD-95. Science 269:1737-1740.
70. Kosinski CM, Cha JH, Young AB, Persichetti F, MacDonald M, Gusella JF, Penney JB, Standaert DG. 1997. Huntingtin immunoreactivity in the rat neostriatum: differential accumulation in projection and interneurons. Exp Neurol 144:239-247.
71. Kosinski CM, Standaert DG, Counihan TJ, Scherzer CR, Kerner JA, Daggett LP, Velicelebi G, Penney JB, Young AB, Landwehrmeyer GB. 1998. Expression of N-methyl-D-aspartate receptor subunit mRNAs in the human brain: striatum and globus pallidus. J Comp Neurol 390:63-74.
72. Krupp JJ, Vissel B, Heinemann SF, Westbrook GL. 1998. N-terminal domains in the NR2 subunit control desensitization of NMDA receptors. Neuron 20:317-327.
73. Kubota Y, Mikawa S, Kawaguchi Y. 1993. Neostriatal GABAergic interneurones contain NOS, calretinin or parvalbumin. NeuroReport 5:205-208.
74. Küppenbender KD, Ziefer PA, Feuerstein TJ, Standaert DG, Penney JB, Young AB, Landwehrmeyer GB. 1997. NMDA receptor subunit mRNA expression in identified human striatal neurons. Soc Neurosci Abstr 23:929.
75. Landwehrmeyer GB, Standaert DG, Testa CM, Penney JB, Young AB. 1995. NMDA receptor subunit mRNA expression by projection neurons and interneurons in rat striatum. J Neurosci 15:5297-5307.
76. Laurie DJ, Seeburg PH. 1994a. Ligand affinities at recombinant N-methyl-D-aspartate receptors depend on subunit composition. Eur J Pharmacol 268:335-345.
77. Laurie DJ, Seeburg PH. 1994b. Regional and developmental heterogenity in splicing of the rat brain NMDAR1 mRNA. J Neurosci 14:3180-3194.
78. Laurie DJ, Putzke J, Zieglgänsberger W, Seeburg PH, Tölle TR. 1995. The distribution of splice variants of the NMDAR1 subunit mRNA in adult rat brain. Mol Brain Res 32:94-108.
79. Lenz S, Perney TM, Qin Y, Robbins E, Chesselet MF. 1994. GABA-ergic interneurons of the striatum express the Shaw-like potassium channel KvS.1. Synapse 18:55-66.
80. Leonard AS, Hell JW. 1997. Cyclic AMP-dependent protein kinase and protein kinase C phosphorylate N-methyl-D-aspartate receptors at different sites. J Biol Chem 272:12107-12115.
81. Lin JW, Wyszynski M, Madhavan R, Sealock R, Kim JU, Sheng M. 1998. Yotiao, a novel protein of neuromuscular junction and brain that interacts with specific splice variants of NMDA receptor subunit NR1. J Neurosci 18:2017-2027.
82. Liu H, Wang H, Sheng M, Jan LY, Basbaum AI. 1994. Evidence for presynaptic N-methyl-D-aspartate autoreceptors in the spinal cord dorsal horn. Proc Natl Acad Sci USA 91:8383-8387.
83. Logan SM, Rivera FE, Leonard JP. 1999. Protein kinase C modulation of recombinant NMDA receptor currents: roles for the C-terminal C1 exon and calcium ions. J Neurosci 19:974-986.
84. Loopuijt LD, van der Kooy D. 1985. Organization of the striatum: collateralization of its efferent axons. Brain Res 348:86-99.
85. McGeer PL, McGeer EG, Scherer U, Singh K. 1977. A glutamatergic corticostriatal path? Brain Res 128:369-373.
86. Monyer H, Sprengel R, Schoepfer R, Herb A, Higuchi M, Lomeli H, Burnashev N, Sakmann B, Seeburg P. 1992. Heteromeric NMDA receptors: molecular and functional distinction of subtypes. Science 256:1217-1221.
87. Monyer H, Burnashev N, Laurie DJ, Sakmann B, Seeburg PH. 1994. Developmental and regional expression in the rat brain and functional properties of four NMDA receptors. Neuron 12:529-540.
88. Morari M, O'Connor WT, Ungerstedt U, Fuxe K. 1993. N-methyl-D-aspartic acid differentially regulates extracellular dopamine, GABA, and glutamate levels in the dorsolateral neostriatum of the halothane-anesthetized rat: an in vivo microdialysis study. J Neurochem 60:1884-1893.
89. 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.
90. Nash NR, Heilman CJ, Rees HD, Levey AI. 1997. Cloning and localization of Exon 5-containing isoforms of the NMDAR1 subunit in human and rat brains. J Neurochem 69:485-493.
91. Parent A, Hazrati L-N. 1995. Functional anatomy of the basal ganglia. I. The cortico-basal ganglia-thalamo-cortical loop. Brain Res Rev 20:91-127.
92. Paxinos G, Watson C. 1986. The rat brain in stereotaxic coordinates. New York: Academic Press.
93. Petralia RS, Yokotani N, Wenthold RJ. 1994. Light and electron microscope distributions of the NMDA receptor subunit NMDAR1 in the rat nervous system using a selective anti-peptide antibody. J Neurosci 14:667-696.
94. Rajakumar N, Elisevich K, Flumerfeldt BA. 1993. Biotinylated dextran: a versatile anterograde and retrograde neuronal tracer. Brain Res 607:47-53.
95. Reiner A, Albin RL, Andersen KD, D'Amato CJ, Penney JB, Young AB. 1988. Differential loss of striatal projection neurons in Huntington disease. Proc Natl Acad Sci USA 85:5733-5737.
96. Roberts RC, Ahn A, Swartz KJ, Beal MF, DiFiglia M. 1993. Intrastriatal injections of quinolinic acid or kainic acid: differential patterns of cell survival and the effects of data analysis on outcome. Exp Neurol 124:274-282.
97. Rushlow W, Flumerfelt BA, Naus CC. 1995. Colocalization of somatostatin, neuropeptide Y, and NADPH-diaphorase in the caudate-putamen of the rat. J Comp Neurol 351:499-508.
98. Ruzicka BB, Jhamandas K. 1991. Met-enkephalin release from slices of the rat striatum and globus pallidus: stimulation by excitatory amino acids. J Pharmacol Exp Ther 257:1025-1033.
99. Seto-Ohshima A, Emson PC, Lawson E, Mountjoy CQ, Carrasco LH. 1988. Loss of matrix calcium-binding protein-containing neurons in Huntington's disease. Lancet 1(8597):1252-1254.
100. Sheng M, Cummings J, Roldan LA, Jan YN, Jan LY. 1994. Changing subunit composition of heteromeric NMDA receptors during development of rat cortex. Nature 368:144-147.
101. Siegel SJ, Brose N, Janssen WG, Gasic GP, Jahn R, Heinemann SF, Morrison JH. 1994. Regional, cellular, and ultrastructural distribution of N-methyl-D-aspartate receptor subunit 1 in monkey hippocampus. Proc Natl Acad Sci USA 91:564-568.
102. Snyder GL, Fienberg AA, Huganir RL, Greengard P. 1998. A dopamine/D1 receptor/protein kinase A/dopamine- and cAMP-regulated phosphoprotein (Mr 32 kDa)/protein phosphatase-1 pathway regulates dephosphorylation of the NMDA receptor. J Neurosci 18:10297-10303.
103. Somers DL, Beckstead RM. 1992. N-methyl-D-aspartate receptor antagonism alters substance P and met5-enkephalin biosynthesis in neurons of the rat striatum. J Pharmacol Exp Ther 262:823-833.
104. Standaert DG, Watson SJ, Houghten RA, Saper CB. 1986. Opioid peptide immunoreactivity in spinal and trigeminal dorsal horn neurons projecting to the parabrachial nucleus. J Neurosci 6:1220-1226.
105. Standaert DG, Testa CM, Penney JB, Young AB. 1994. Organization of N-methyl-D-aspartate glutamate receptor gene expression in the basal ganglia of the rat. J Comp Neurol 343:1-16.
106. Standaert DG, Landwehrmeyer GB, Kerner JA, Penney JB, Young AB. 1996. Expression of NMDAR2D glutamate receptor subunit mRNA in neurochemically identified interneurons in the rat neostriatum, neocortex and hippocampus. Mol Brain Res 42:89-102.
107. Standaert DG, Friberg IK, Landwehrmeyer GB, Young AB, Penney JB, Jr. 1999. Expression of NMDA glutamate receptor subunit mRNAs in neurochemically identified projection and interneurons in the striatum of the rat. Brain Res Mol Brain Res 64:11-23.
108. Sugihara H, Moriyoshi K, Ishii T, Masu M, Nakanishi S. 1992. Structures and properties of seven isoforms of the NMDA receptor generated by alternative splicing. Biochem Biophys Res Commun 185:826-832.
109. Tallaksen-Greene SJ, Albin RL. 1994. Localization of AMPA-selective excitatory amino acid receptor subunits in identified populations of striatal neurons. Neuroscience 61:509-519.
110. Testa CM, Friberg IK, Weiss SW, Standaert DG. 1998. Immunohistochemical localization of metabotropic glutamate receptors niGluR1a and mGluR2/3 in the rat basal ganglia. J Comp Neurol 390:5-19.
111. 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.
112. Tingley WG, Ehlers MD, Kameyama K, Doherty C, Ptak JB, Riley CT, Huganir RL. 1997. Characterization of protein kinase A and protein kinase C phosphorylation of the N-methyl-D-aspartate receptor NR1 subunit using phosphorylation site-specific antibodies. J Biol Chem 272:5157-5166.
113. Traynelis SF, Hartley M, Heinemann SF. 1995. Control of proton sensitivity of the NMDA receptor by RNA splicing and polyamines. Science 268:873-876.
114. Traynelis SF, Burgess MF, Zheng F, Lyuboslavsky P, Powers JL. 1998. Control of voltage-independent zinc inhibition of NMDA receptors by the NR1 subunit. J Neurosci 18:6163-6175.
115. Vincent SR, Johansson O. 1983. Striatal neurons containing both somatostatin- and avian pancreatic polypeptide (APP)-like immunoreactivities and NADPH-diaphorase activity: a light and electron microscopic study. J Comp Neurol 217:264-270.
116. Walsh JP, Dunia R. 1993. Synaptic activation of N-methyl-D-aspartate receptors induces short-term potentiation at excitatory synapses in the striatum of the rat. Neuroscience 57:241-248.
117. Weiss SW, Albers DS, Iadarola MJ, Dawson TM, Dawson VL, Standaert DG. 1998. NMDAR1 glutamate receptor subunit isoforms in neostriatal, neocortical, and hippocampal nitric oxide synthase neurons. J Neurosci 18:1725-1734.
118. Williams K. 1997. Interactions of polyamines with ion channels. Biochem J 325:289-297.
119. Xia Z, Dudek H, Miranti CK, Greenberg ME. 1996. Calcium influx via the NMDA receptor induces immediate early gene transcription by a MAP kinase/ERK-dependent mechanism. J Neurosci 16:5425-5436.
120. Young AM, Bradford HF. 1991. N-methyl-D-aspartate releases excitatory amino acids in rat corpus striatum in vivo. J Neurochem 56:1677-1683.
121. Young AM, Bradford HF. 1993. N-methyl-D-aspartate releases gamma-aminobutyric acid from rat striatum in vivo: a microdialysis study using a novel preloading method. J Neurochem 60:487-492.
122. Zukin RS, Bennett MVL. 1995. Alternatively spliced isoforms of the NMDAR1 receptor subunit. Trends Neurosci 18:306-313.