Synaptic localization of NMDA receptor subunits in the rat retina

Journal of Comparative Neurology

Volumn 420, Issue 1, 2000, Pages 98-112

  Fletcher, Erica L ^a,b   Hack, Iris ^a   Brandstätter, Johann Helmut ^a   Wässle, Heinz ^a  

^a MAX PLANCK INSTITUTE FOR BRAIN RESEARCH   (Germany)

^b Dept of Anatomy and Cell Biology ^*  (Australia)

Author keywords

NR1; NR1C2'; NR2A; NR2B; PSD 93; PSD 95; Rod bipolar cells; SAP 102; Synaptic clustering

Indexed keywords

N METHYL DEXTRO ASPARTIC ACID RECEPTOR;

ANIMAL CELL; ANIMAL TISSUE; ARTICLE; ELECTRON MICROSCOPY; IMMUNOFLUORESCENCE; IMMUNOREACTIVITY; NERVE CELL; NEUROTRANSMISSION; NONHUMAN; POSTSYNAPTIC MEMBRANE; PRIORITY JOURNAL; PROTEIN LOCALIZATION; RAT; RETINA; RETINA AMACRINE CELL; RETINA CONE; RETINA ROD; SYNAPSE;

ANIMALS; CONES (RETINA); INTRACELLULAR SIGNALING PEPTIDES AND PROTEINS; MEMBRANE PROTEINS; NERVE TISSUE PROTEINS; RATS; RECEPTORS, N-METHYL-D-ASPARTATE; RETINA; RODS (RETINA); SYNAPSES;

EID: 0034709283     PISSN: 00219967     EISSN: None     Source Type: Journal    
DOI: 10.1002/(SICI)1096-9861(20000424)420:1<98::AID-CNE7>3.0.CO;2-U     Document Type: Article

References (87)

1. Aizenman E, Frosch MP, Lipton SA. 1988. Responses mediated by excitatory amino acid receptors in solitary retinal ganglon cells from rat. J Physiol Lond 396:75-91.
2. Bassand P, Bernard A, Rafiki A, Gayet D, Khrestchatisky M. 1999. Differential interaction of the tSXV motifs of the NR1 and NR2A NMDA receptor subunits with PSD-95 and SAP97. Eur J Neurosci 11:2031-2043.
3. Baude A, Nusser Z, Molnár E, McIlhinney RAJ, Somogyi P. 1995. High-resolution immunogold localization of AMPA type glutamate receptor subunits at synaptic and non-synaptic sites in rat hippocampus. Neuroscience 69:1031-1055.
4. 3Cv mouse retinae. Eur J Neurosci 11:2121-2133.
5. Boos R, Schneider H, Wässle H. 1993. Voltage- and transmitter-gated currents of AII-amacrine cells in a slice preparation of the rat retina. J Neurosci 13:2874-2888.
6. Brandstätter JH, Harveit E, Sassoè-Pognetto M, Wässle H. 1994. Expression of NMDA and high affinity kainate receptor subunit mRNAs in the adult rat retina. Eur J Neurosci 6:1100-1112.
7. Brandstätter JH, Koulen P, Wässle H. 1997. Selective synaptic distribution of kainate receptor subunits in the two plexiform layers of the rat retina. J Neurosci 17:9298-9307.
8. Brandstätter JH, Koulen P, Wässle H. 1998. Diversity of glutamate receptors in the mammalian retina. Vision Res 38:1385-1397.
9. Brenman JE, Christopherson KS, Craven SE, McGee AW, Bredt DS. 1996. Cloning and characterization of postsynaptic density 93, a nitric oxide synthase interacting protein. J Neurosci 16:7407-7415.
10. Brose N, Gasic GP, Vetter DE, Sullivan JM, Heinemann SF. 1993. Protein chemical characterization and immunocytochemical localization of the NMDA receptor subunit NMDA R1. J Biol Chem 268:22663-22671.
11. Chen N, Luo T, Raymond LA. 1999. Subtype-dependence of NMDA receptor channel open probability. J Neurosci 19:6844-6854.
12. Cho K-O, Hunt CA, Kennedy MB. 1992. The rat brain postsynaptic density fraction contains a homolog of the Drosophila discs-large tumor suppressor protein. Neuron 9:929-942.
13. Chun M-H, Han S-H, Chung J-W, Wässle H. 1993. Electron microscopic analysis of the rod pathway of the rat retina. J Comp Neurol 332:421-432.
14. Ciabarra AM, Sullivan JM, Gahn LG, Pecht G, Heinemann S, Sevarino KA. 1995. Cloning and characterization of x-1: a developmentally regulated member of a novel class of ionotropic glutamate receptor family. J Neurosci 15:6498-6508.
15. Cohen ED, Zhou ZJ, Fain GL. 1994. Ligand-gated currents of alpha and beta ganglion cells in the cat retinal slice. J Neurophysiol 72:1260-1269.
16. Craig AM, Blackstone CD, Huganir RL, Banker G. 1993. The distribution of glutamate receptors in cultured rat hippocampal neurons: postsynaptic clustering of AMPA-selective subunits. Neuron 10:1055-1068.
17. Craig AM, Blackstone CD, Huganir RL, Banker G. 1994. Selective clustering of glutamate and γ-aminobutyric acid receptors opposite terminals releasing the corresponding neurotransmitters. Proc Natl Acad Sci USA 91:12373-12377.
18. 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.
19. Flint AC, Maisch US, Weishaupt JH, Kriegstein AR, Monyer H. 1997. NR2A subunit expression shortens NMDA receptor synaptic currents in developing neocortex. J Neurosci 17:2469-2476.
20. Fritschy J-M, Weinmann O, Wenzel A, Benke D. 1998. Synapse-specific localization of NMDA and GABAA receptor subunits revealed by antigen-retrieval immunohistochemistry. J Comp Neurol 390:194-210.
21. Gomperts SN. 1996. Clustering membrane proteins: it's all coming together with the PSD-95/SAP90 protein family. Cell 84:659-662.
22. Greferath U, Grünert U, Wässle H. 1990. Rod bipolar cells in the mammalian retina show protein kinase C-like immunoreactivity. J Comp Neurol 301:433-442.
23. Hartveit E. 1996. Membrane currents evoked by ionotropic glutamate receptor agonists in rod bipolar cells in the rat retinal slice preparation. J Neurophysiol 76:401-422.
24. Hartveit E, Veruki ML. 1997. All amacrine cells express functional NMDA receptors. NeuroReport 8:1219-1223.
25. Hartveit E, Brandstätter JH, Sassoè-Pognetto M, Laurie DJ, Seeburg PH, Wässle H. 1994. Localization and developmental expression of the NMDA receptor subunit NR2A in the mammalian retina. J Comp Neurol 348:570-582.
26. Hof PR, Vissavajjhala P, Rosenthal RE, Fiskum G, Morrison JH. 1996. Distribution of glutamate receptor subunit proteins GluR2(4), GluR5/ 6/7, and NMDAR1 in the canine and primate cerebral cortex - a comparative immunohistochemical analysis. Brain Res 723:77-89.
27. Hollmann M, Heinemann S. 1994. Cloned glutamate receptors. Annu Rev Neurosci 17:31-108.
28. 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.
29. 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 sensorymotor and visual cortices of monkey and man. J Neurosci 14:3603-3619.
30. Johnson RR, Jiang XP, 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.
31. Karschin A, Aizenman E, Lipton S. 1988. The interaction of agonists and noncompetitive antagonists at the excitatory amino acid receptors in rat retinal ganglion cells. J Neurosci 8:2895-2906.
32. Kennedy MB. 1997. The postsynaptic density at glutamatergic synapses. Trends Neurosci 20:264-268.
33. Kharazia VN, Phend KD, Rustioni A, Weinberg RJ. 1996. EM colocalization of AMPA and NMDA receptor subunits at synapses in rat cerebral cortex. Neurosci Lett 210:37-40.
34. Kim E, Cho KO, Rothschild A, Sheng M. 1996. Heteromultimerization and NMDA receptor-clustering activity of chapsyn-110, a member of the PSD-95 family of proteins. Neuron 17:103-113.
35. Kim JH, Huganir RL. 1999. Organization and regulation of proteins at synapses. Curr Opin Cell Biol 11:248-254.
36. Kistner U, Wenzel BM, Veh RW, Cases-Langhoff C, Garner AM, Appeltauer U, Voss B, Gundelfinger ED, Garner CC. 1993. SAP90, a rat presynaptic protein related to the product of the Drosophila tumor suppressoe gene dlg-A. J Biol Chem 268:4580-4583.
37. Kolb H, Famiglietti EV. 1974. Rod and cone pathways in the inner plexiform layer of cat retina. Science 186:47-49.
38. Kornau HC, Schenker LT, Kennedy MB, Seeburg PH. 1995. Domain interaction between NMDA receptor subunits and the post-synaptic density protein PSD-95. Science 269:1737-1740.
39. Koulen P, Fletcher EL, Craven SE, Bredt DS, Wässle H. 1998. Immunocytochemical localization of the postsynaptic density protein PSD-95 in the mammalian retina. J Neurosci 18:10136-10149.
40. Kreutz MR, Böckers TM, Bockmann J, Seidenbecher CI, Kracht B, Vorwerk CK, Weise J, Sabel BA. 1998. Axonal injury alters alternative splicing of the retinal NR1 receptor: the preferential expression of the NR1b isoforms is crucial for retinal ganglion cell survival. J Neurosci 15:8278-8291.
41. Laube B, Kuhse J, Betz H. 1998. Evidence for tetrameric structure of recombinant NMDA receptors. J Neurosci 18:2954-2961.
42. Laurie DJ, Bartke I, Schoepfer R, Naujoks K, Seeburg PH. 1997. Regional, developmental and interspecies expression of the four NMDAR2 subunits, examined using monoclonal antibodies. Mol Brain Res 51:23-32.
43. Lo W, Molloy R, Hughes TE. 1998. Ionotropic glutamate receptors in the retina: moving from molecules to circuits. Vision Res 38:1399-1410.
44. Lue RA, Marfatia SM, Branton D, Chishti AH. 1994. Cloning and characterization of hdlg: the human homologue of the Drosophila discs-large tumor suppressor binds to protein 4.1. Proc Natl Acad Sci USA 91: 9818-9822.
45. Marc R. 1999. Mapping glutamatergic drive in the vertebrate retina with a channel-permeant organic cation. J Comp Neurol 407:47-64.
46. Massey SC. 1990. Cell types using glutamate as a neurotransmitter in the vertebrate retina. In: Osborne N, Chader J, editors. Progress in retinal research. Oxford: Pergamon Press. p 399-425.
47. Massey SC, Miller RF. 1990. N-methyl-D-aspartate receptors of ganglion cells in the rabbit retina. J Neurophysiol 63:16-30.
48. Migaud M, Charlesworth P, Dempster M, Webster LC, Watabe AM, Makhinson M, He Y, Ramsay MF, Morris RGM, Morrison JH, O'Dell TJ, Grant SGN. 1998. Enhanced long-term potentiation and impaired learning in mice with mutant postsynaptic density-95 protein. Nature 396:433-439.
49. Mittman S, Taylor WR, Copenhgen DR. 1990. Concomitant activation of two types of glutamate receptor mediates excitation of salamander retinal ganglion cells. J Physiol 428:175-197.
50. Moffett JR, Palkovits M, Namboodiri A, Neale JH. 1994. Comparative distribution of N-acetylaspartylglutamate and GAD67 in the cerebellum and precerebellar nuclei of the rat utilizing enhanced carbodiimide fixation and immunohistochemistry. J Comp Neurol 347:598-618.
51. Monyer H, Sprengel R, Schoepfer R, Hebb 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.
52. Müller BM, Kistner U, Veh RW, Cases-Langhoff C, Becker B, Gundelfinger ED, Garner CC. 1995. Molecular characterization and spatial distribution of SAP97, a novel presynaptic protein homologous to SAP90 and the Drosophila discs-large tumor suppressor protein. J Neurosci 15: 2354-2366.
53. Müller BM, Kistner U, Kindler S, Chung WJ, Kuhlendahl S, Lau L-F, Veh RW, Huganir RI, Gundelfinger ED, Garner CC. 1996. SAP 102, a novel postsynaptic protein that interacts with the cytoplasmic tail of the NMDA receptor subunit NR2B. Neuron 17:255-265.
54. Nakanishi S, Masu M. 1994. Molecular diversity and functions of glutamate receptors. Annu Rev Biophys Biomol Struct 23:319-348.
55. Negishi K, Kato S, Teranishi T. 1988. Dopamine cells and rod bipolar cells contain protein kinase C-like immunoreactivity in some vertebrate retinas. Neurosci Lett 94:247-252.
56. Nissinen MJ, Panula P. 1993. Histamine-storing cells in the oxyntic mucosa of the rat stomach: a transmission electron microscopic study employing fixation with carbodiimide. J Histochem Cytochem 41:1405-1412.
57. Nusser Z, Mulvihill E, Streit P, Somogyi P. 1994. Subsynaptic segregation of metabotropic and ionotropic glutamate receptors as revealed by immunogold localization. Neuroscience 61:421-427.
58. A receptor in relation to specific GABAergic synapses in the dentate gyrus. Eur J Neurosci 7:630-646.
59. A receptors on cerebellar granule cells as determined by a quantitative immunogold method. J Neurosci 15:2948-2960.
60. Nusser Z, Sieghart W, Benke D, Fritschy J-M, Somogyi P. 1996. Differential synaptic localization of two major γ-aminobutyric acid type A receptor alpha subunits on hippocampal pyramidal neurons. Proc Natl Acad Sci USA 93:11939-11944.
61. Ottersen OP, Landsend AS. 1997. Organization of glutamate receptors at the synapse. Eur J Neurosci 9:2219-2224.
62. Ozawa S, Kamiya H, Tsuzuki K. 1998. Glutamate reeptors in the mammalian central nervous system. Prog Neurobiol 54:581-618.
63. Petralia RS, Wang YX, Wenthold RJ. 1994a. The NMDA receptor subunits NR2A and NR2B show histological and ultrastructural localization patterns similar to those of NR1. J Neurosci 14:6102-6120.
64. Petralia RS, Yokotani N, Wenthold RJ. 1994b. Light and electron microscope distribution of the NMDA-receptor subunit NMDAR1 in the rat nervous system using a selective anti-peptide antibody. J Neurosci 14:667-696.
65. Pin JP, Duvoisin R. 1995. Neurotransmitter receptors I. The metabotropic glutamate receptors: structure and functions. Neuropharmacology 34: 1-26.
66. Qin P, Pourcho RG. 1999. Localization of AMPA-selective glutamate receptor subunits in the cat retina: a light- and electron-microscopic study. Visual Neurosci 16:169-177.
67. Rao A, Craig AM. 1997. Activity regulates the synaptic localization of the NMDA receptor in hippocampal neurons. Neuron 19:801-812.
68. Rema V, Ebner FF. 1996. Postnatal changes in NMDAR1 subunit expression in the rat trigeminal pathway to barrel field cortex. J Comp Neurol 368:165-184.
69. Sassoè-Pognetto M, Wässle H, Grünert U. 1994. Glycinergic synapses in the rod pathway of the rat retina: cone bipolar cells express the a1 subunit of the glycine receptor. J Neurosci 14:5131-5146.
70. Sheng M. 1996. PDZs and receptor/channel clustering: rounding up the latest suspects. Neuron 17:575-578.
71. Strettoi E, Dacheux RF, Raviola E. 1990. Synaptic connections of rod bipolar cells in the inner plexiform layer of the rabbit retina. J Comp Neurol 295:449-466.
72. Sucher NJ, Akbararian S, Chi CL, Leclerc CL, Awobuluyi M, Deitcher DL, Wu MK, Auan JP, Jones EG, Lipton SA. 1995. Developmental and regional expression pattern of a novel NMDA receptor-like subunit (NMDAR-L) in rodent brain. J Neurosci 15:6509-6520.
73. Tachibana M, Okada T. 1991. Release of endogenous excitatory amino acids from ON-type bipolar cells isolated from the goldfish retina. J Neurosci 11:2199-2208.
74. Takumi Y, Bergersen L, Landsend AS, Rinvik E, Ottersen OP. 1998. Synaptic arrangement of glutamate receptors. In: Ottersen OP, Langmoen IA, Gjerstad L, editors. Progress in brain research. Amsterdam: Elsevier Science p 105-121.
75. Takumi Y, Ramirez-León V, Laake P, Rinvik E, Ottersen OP. 1999. Different modes of expression of AMPA and NMDA receptors in hippocampal synapses. Nature Neurosci 2:618-624.
76. Taylor WR, Chen E, Copenhagen DR. 1995. Characterization of spontaneous excitatory synaptic currents in salamander retinal ganglion cells. J Physiol 486:207-221.
77. Tovar KR, Westbrook GL. 1999. The incorporation of NMDA receptors with a distinct subunit composition at nascent hippocampal synapses in vitro. J Neurosci 19:4180-4188.
78. Valtschanoff JG, Burette A, Wenthold RJ, Weinberg RJ. 1999. Expression of NR2 receptor subunit in rat somatic sensory cortex: synaptic distribution and colocalization with NR1 and PSD-95. J Comp Neurol 410: 599-611.
79. von Kriegstein K, Schmitz F, Link E, Südhof TC. 1999. Distribution of synaptic vesicle proteins in the mammalian retina identifies obligatory and facultative components of ribbon synapses. Eur J Neurosci 11: 1335-1348.
80. Wassle H, Koulen P, Brandstätter JH, Fletcher EL, Becker C-M. 1998. Glycine and GABA receptors in the mammalian retina. Vision Res 38:1411-1430.
81. Watanabe M, Mishina M, Inoue Y. 1994. Differential distributions of NMDA receptor channel subunit mRNAs in mouse retina. Brain Res 34:328-332.
82. Watanabe M, Fukaya M, Sakimura K, Manabe T, Mishina M, Inoue Y. 1998. Selective scarcity of NMDA receptor channel subunits in the stratum lucidum (mossy fibre-recipient layer) of the mouse hippocampal CA3 subfield. Eur J Neurosci 10:478-487.
83. 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.
84. Wenzel A, Benke D, Möhler H, Fritschy J-M. 1997. N-methyl-D-aspartate receptors containing the NR2D subunit in the retina are selectively expressed in rod bipolar cells. Neuroscience 78:1105-1112.
85. + ATPase and NMDA receptor subunit 1. Vision Res 38:1455-1477.
86. Ziff EB. 1997. Enlightening the postsynaptic density. Neuron 19:1163-1174.
87. Zukin RS, Bennett MVL. 1995. Alternatively spliced isoforms of the NMDAR1 receptor subunit. Trends Neurosci 18:306-313.