Subunit- and pathway-specific localization of NMD a receptors and scaffolding proteins at ganglion cell synapses in rat retina

Journal of Neuroscience

Volumn 29, Issue 13, 2009, Pages 4274-4286

  Zhang, Jun ^a   Diamond, Jeffrey S ^a  

^a NATIONAL INSTITUTE OF NEUROLOGICAL DISORDERS AND STROKE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

4 BENZYL ALPHA (4 HYDROXYPHENYL) BETA METHYL 1 PIPERIDINEPROPANOL; MEMBRANE ASSOCIATED GUANYLATE CYCLASE KINASE; N METHYL DEXTRO ASPARTIC ACID RECEPTOR 1; N METHYL DEXTRO ASPARTIC ACID RECEPTOR 2A; SCAFFOLD PROTEIN; AMINO ACID RECEPTOR AFFECTING AGENT; CALCIUM; CHOLERA TOXIN; MEMBRANE PROTEIN; N METHYL DEXTRO ASPARTIC ACID RECEPTOR; NERVE PROTEIN; NR1 NMDA RECEPTOR; NR2A NMDA RECEPTOR;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; BRAIN NERVE CELL; EMBEDDING; IMMUNOGOLD ELECTRON MICROSCOPY; IMMUNOHISTOCHEMISTRY; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; RAT; RETINA GANGLION CELL; SYNAPSE; WESTERN BLOTTING; ANIMAL; CEREBELLUM; CYTOLOGY; DRUG EFFECT; EXCITATORY POSTSYNAPTIC POTENTIAL; IMMUNOELECTRON MICROSCOPY; IN VITRO STUDY; METABOLISM; METHODOLOGY; NEWBORN; PATCH CLAMP; PHYSIOLOGY; RETINA; SPRAGUE DAWLEY RAT; ULTRASTRUCTURE;

ANIMALS; ANIMALS, NEWBORN; CALCIUM; CEREBELLUM; CHOLERA TOXIN; EXCITATORY AMINO ACID AGENTS; EXCITATORY POSTSYNAPTIC POTENTIALS; MEMBRANE PROTEINS; MICROSCOPY, IMMUNOELECTRON; NERVE TISSUE PROTEINS; PATCH-CLAMP TECHNIQUES; RATS; RATS, SPRAGUE-DAWLEY; RECEPTORS, N-METHYL-D-ASPARTATE; RETINA; RETINAL GANGLION CELLS; SYNAPSES;

EID: 65249144104     PISSN: 02706474     EISSN: 15292401     Source Type: Journal    
DOI: 10.1523/JNEUROSCI.5602-08.2009     Document Type: Article

References (84)

1. Al-Hallaq RA, Yasuda RP, Wolfe BB (2001) Enrichment of N-methyl-D-aspartate NR1 splice variants and synaptic proteins in rat postsynaptic densities. J Neurochem 77:110-119.
2. Al-Hallaq RA, Conrads TP, Veenstra TD, Wenthold RJ (2007) NMDA di-heteromeric receptor populations and associated proteins in rat hippocampus. J Neurosci 27:8334-8343.
3. Amthor PR, Takahashi ES, Oyster CW (1989) Morphologies of rabbit retinal ganglion cells with complex receptive fields. J Comp Neurol 280:97-121.
4. Andressen C, Bliimcke I, Celio MR (1993) Calcium-binding proteins: Selective markers of nerve cells. Cell Tissue Res 271:181-208.
5. Aoki C, Miko I, Oviedo H, Mikeladze-Dvali T, Alexandre L, Sweeney N, Bredt DS (2001) Electron microscopic immunocyto chemical detection of PSD-95, PSD-93, SAP-102, and SAP-97 at postsynaptic, presynaptic, and nonsynaptic sites of adult and neonatal rat visual cortex. Synapse 40:239-257.
6. Arrigoni E, Greene RW (2004) Schaffer collateral and perforant path inputs activate different subtypes of NMDA receptors on the same CA1 pyramidal cell. Br J Pharmacol 142:317-322.
7. Blahos J 2nd, Wenthold RJ (1996) Relationship between N-methyl-D-aspartate receptor NR1 splice variants and NR2 subunits. J Biol Chem 271:15669-15674.
8. 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.
9. Chen S, Diamond JS (2002) Synaptically released glutamate activates extra-synaptic NMDA receptors on cells in the ganglion cell layer of rat retina. J Neurosci 22:2165-2173.
10. Chichilnisky EJ, Kalmar RS (2002) Functional asymmetries in ON and OFF ganglion cells of primate retina. J Neurosci 22:2737-2747.
11. Clark BA, Cull-Candy SG (2002) Activity-dependent recruitment of extra-synapotic NMDA receptor activation at an AMPA receptor-only synapse. J Neurosci 22:4428-4436.
12. Clements JD, Bekkers JM (1997) Detection of spontaneous synaptic events with an optimally scaled template. Biophys J 73:220-229.
13. Collingridge GL, Lester RA (1989) Excitatory amino acid receptors in the vertebrate central nervous system. Pharmacol Rev 41:143-210.
14. Cull-Candy SG, Leszkiewicz DN (2004) Role of distinct NMDA receptor subtypes at central synapses. Sci STKE 2004:rel6.
15. Davies C, Tingley D, Kachar B, Wenthold RJ, Petralia RS (2001) Distribution of members of the PSD-95 family of MAGUK proteins at the synaptic region of inner and outer hair cells of the guinea pig cochlea. Synapse 40:258-268.
16. Dingledine R, Borges K, Bowie D, Traynelis SF (1999) The glutamate receptor ion channels. Pharmacol Rev 51:7-61.
17. El-Husseini AE, Topinka JR, Lehrer-Graiwer JE, Firestein BL, Craven SE, Aoki C, Bredt DS (2000) Ion channel clustering by membrane-associated guanylate kinases. Differential regulation by N-terminal lipid and metal binding motifs. J Biol Chem 275:23904-23910.
18. Elias GM, Funke L, Stein V, Grant SG, Bredt DS, Nicoll RA (2006) Synapse-specific and developmentally regulated targeting of AMPA receptors by a family of MAGUK scaffolding proteins. Neuron 52:307-320.
19. Ewald RC, Van Keuren-Jensen KR, Aizenman CD, Cline HT (2008) Roles of NR2A and NR2B in the development of dendritic arbor morphology ni vivo. J Neurosci 28:850-861.
20. Fletcher EL, Hack I, Brandstätter JH, Wässle H (2000) Synaptic localization of NMDA receptor subunits in the rat retina. J Comp Neurol 420:98-112.
21. Goebel DJ, Amelia JL, Tai Q, Jojich L, Poosch MS (1998) Immunocyto Chemical localization of the NMDA-R2A receptor subunit in the cat retina. Brain Res 808:141-154.
22. Gründer T, Kohler K, Kaletta A, Guenther E (2000) The distribution and developmental regulation of NMDA receptor subunit proteins in the outer and inner retina of the rat. J Neurobiol 44:333-342.
23. Hardingham GE, Fukunaga Y, Bading H (2002) Extrasynaptic NMDARs oppose synaptic NMDARs by triggering CREB shut-off and cell death pathways. Nat Neurosci 5:405-414.
24. Harris AZ, Pettit DL (2007) Extrasynaptic and synaptic NMDA receptors form stable and uniform pools in rat hippocampal slices. J Physiol 584:509-519.
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. 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.
27. Honse Y, Nixon KM, Browning MD, Leslie SW (2003) Cell surface expression of NR1 splice variants and NR2 subunits is modified by prenatal ethanol exposure. Neuroscience 122:689-698.
28. 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 sub-units. J Biol Chem 268:2836-2843.
29. Ito I, Kawakami R, Sakimura K, Mishina M, Sugiyama H (2000) Input-specific targeting of NMDA receptor subtypes at mouse hippocampal CA3 pyramidal neuron synapses. Neuropharmacology 39:943-951.
30. Kalbaugh TL, Zhang J, Diamond JS (2009) Coagonist release modulates NMDA receptor subtype contributions at synaptic inputs to retinal ganglion cells. J Neurosci 29:1469-1479.
31. Kalloniatis M, Sun D, Foster L, Haverkamp S, Wässle H (2004) Localization of NMDA receptor subunits and mapping NMDA drive within the mammalian retina. Vis Neurosci 21:587-597.
32. Kawakami R, Shinohara Y, Kato Y, Sugiyama H, Shigemoto R, Ito I (2003) Asymmetrical allocation of NMDA receptor epsilon2 subunits in hip-pocampal circuitry. Science 300:990-994.
33. Kennedy MB (1995) Origin of PDZ (DHR, GLGF) domains. Trends Bio-chem Sci 20:350.
34. Kim E, Sheng M (1996) Differential K+ channel clustering activity of PSD-95 and SAP97, two related membrane-associated putative guanylate kinases. Neuropharmacology 35:993-1000.
35. Kim E, Sheng M (2004) PDZ domain proteins of synapses. Nat Rev Neuro-sci 5:771-781.
36. Kim E, Niethammer M, Rothschild A, Jan YN, Sheng M (1995) Clustering of Shaker-type K+ channels by interaction with a family of membrane-associated guanylate kinases. Nature 378:85-88.
37. 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.
38. Koulen P (1999) Localization of synapse-associated proteins during postnatal development of the rat retina. Eur J Neurosci 11:2007-2018.
39. Koulen P, Fletcher EL, Craven SE, Bredt DS, Wässle H (1998a) Immunocy-tochemical localization of postsynaptic density protein PSD-95 in the mammalian retina. J Neurosci 18:10136-10149.
40. Koulen P, Garner CC, Wässle H (1998b) Immunocyto Chemical localization of the synapse-associated protein SAP 102 in the rat retina. J Comp Neurol 397:326-336.
41. Kumar SS, Huguenard JR (2003) Pathway-specific differences in subunit composition of synaptic NMDA receptors on pyramidal neurons in neo-cortex. J Neurosci 23:10074-10083.
42. 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.
43. Liu L, Wong TP, Pozza MF, Lingenhoehl K, Wang Y, Sheng M, Auberson YP, Wang YT (2004) Role of NMDA receptor subtypes in governing the direction of hippocampal synaptic plasticity. Science 304:1021-1024.
44. Losi G, Prybylowski K, Fu Z, Luo J, Wenthold RJ, Vicini S (2003) PSD-95 regulates NMDA receptors in developing cerebellar granule neurons of the rat. J Physiol 548:21-29.
45. Massey PV, Johnson BE, Moult PR, Auberson YP, Brown MW, Molnar E, Collingridge GL, Bashir ZI (2004) Differential roles of NR2A and NR2B-containing NMDA receptors in cortical long-term potentiation and long-term depression. J Neurosci 24:7821-7828.
46. Matsui K, Hosoi N, Tachibana M (1998) Excitatory synaptic transmission in the inner retina: Paired recordings of bipolar cells and neurons of the ganglion cell layer. J Neurosci 18:4500-4510.
47. McIlhinney RA, Le Bourdellès B, Molnár E, Tricaud N, Streit P, Whiting PJ (1998) Assembly intracellular targeting and cell surface expression of the human N-methyl-D-aspartate receptor subunits NRla and NR2A in transfected cells. Neuropharmacology 37:1355-1367.
48. Mcllhinney RA, Philipps E, Le Bourdelles B, Grimwood S, Watford K, Sandhu S, Whiting P (2003) Assembly of N-methyl-D-aspartate (NMDA) receptors. Biochem Soc Trans 31:865-868.
49. Migaud M, Charlesworfh P, Dempster M, Webster LC, Watabe AM, Makhin-son M, He Y, Ramsay MF, Morris RG, Morrison JH, O'Dell TJ, Grant SG (1998) Enhanced long-term potentiation and impaired learning in mice with mutant postsynaptic density-95 protein. Nature 396:433-439.
50. Mittman S, Taylor WR, Copenhagen DR (1990) Concomitant activation of two types of glutamate receptor mediates excitation of salamander retinal ganglion cells. J Physiol 428:175-197.
51. Momiyama A (2000) Distinct synaptic and extrasynaptic NMDA receptors identified in dorsal horn neurones of the adult rat spinal cord. J Physiol 523:621-628.
52. 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.
53. Morishita W, Lu W, Smith GB, Nicoll RA, Bear MF, Malenka RC (2007) Activation of NR2B-containing NMDA receptors is not required for NMDA receptor-dependent long-term depression. Neuropharmacology 52:71-76.
54. 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.
55. Müller BM, Kistner U, Kindler S, Chung WJ, Kuhlendahl S, Fenster SD, Lau LF, Veh RW, Huganir RL, Gundelfinger ED, Garner CC (1996) SAP102, a novel postsynaptic protein that interacts with NMDA receptor complexes in vivo. Neuron 17:255-265.
56. Nelson R, Famiglietti EV Jr, Kolb H (1978) Intracellular staining reveals different levels of stratification for on- and off-center ganglion cells in cat retina. J Neurophysiol 41:472-483.
57. A receptors on cerebellar granule cells as determined by a quantitative immunogold method. J Neurosci 15:2948-2960.
58. Peichl L, Wässle H (1981) Morphological identification of on- and off-centre brisk transient (Y) cells in the cat retina. Proc R Soc Lond B Biol Sci 212:139-153.
59. Peters A, Palay S, Webster H (1991) The fine structure of the nervous system: Neurons and their supporting cells, Ed 3. New York: Oxford UP.
60. Petralia RS, Wang YX, Wenthold RJ (1994) The NMDA receptor subunits NR2A and NR2B show histological and ultra structural location patterns similar to those of NR1. J Neurosci 10:6102-6120.
61. Prybylowski K, Chang K, Sans N, Kan L, Vicini S, Wenthold RJ (2005) The synaptic localization of NR2B-containing NMDA receptors is controlled by interactions with PDZ proteins and AP-2. Neuron 47:845-857.
62. Rivera N, Lugo N (1998) Four retinal ganglion cell types that project to the superior colliculus in the thirteen-lined ground squirrel (Spermophilus tridecemlineatus). J Comp Neurol 396:105-120.
63. Roche KW, Ly CD, Petralia RS, Wang YX, McGee AW, Bredt DS, Wenthold RJ (1999) Postsynaptic density-93 interacts with the 62 glutamate receptor subunit at parallel fiber synapses. J Neurosci 19:3926-3934.
64. Rumbaugh G, Vicini S (1999) Distinct synaptic and extrasynaptic NMDA receptors in developing cerebellar granule neurons. J Neurosci 19:10603-10610.
65. Sagdullaev BT, McCall MA, Lukasiewicz PD (2006) Presynaptic inhibition modulates spillover, creating distinct dynamic response ranges of sensory output. Neuron 50:923-935.
66. Sans N, Petralia RS, Wang YX, Blahos J 2nd, Hell JW, Wenthold RJ (2000) A developmental change in NMDA receptor-associated proteins at hippocampal synapses. J Neurosci 20:1260-1271.
67. Sassoé-Pognetto M, Ottersen OP (2000) Organization of ionotropic glutamate receptors at dendrodendritic synapses in the rat olfactory bulb. J Neurosci 20:2192-2201.
68. Schneggenburger R, Zhou Z, Konnerth A, Neher E (1993) Fractional contribution of calcium to the cation current through glutamate receptor channels. Neuron 11:133-143.
69. Scimemi A, Fine A, Kullmann DM, Rusakov DA (2004) NR2B-containing receptors mediate cross talk among hippocampal synapses. J Neurosci 24:4767-4777.
70. Sheng M, Cummings J, Roldan LA, Jan YN, Jan LY (1994) Changing sub-unit composition of heteromeric NMDA receptors during development of rat cortex. Nature 368:144-147.
71. Steigerwald F, Schulz TW, Schenker LT, Kennedy MB, Seeburg PH, Köhr G (2000) C-terminal truncation of NR2A subunits impairs synaptic but not extrasynaptic localization of NMDA receptors. J Neurosci 20:4573-4581.
72. Stocca G, Vicini S (1998) Increased contribution of NR2A subunit to synaptic NMDA receptors in developing rat cortical neurons. J Physiol 507:13-24.
73. Thomas CG, Miller AJ, Westbrook GL (2006) Synaptic and extrasynaptic NMDA receptor NR2 subunits in cultured hippocampal neurons. J Neurophysiol 95:1727-1734.
74. Thompson CL, Drewery DL, Atkins HD, Stephenson FA, Chazot PL (2000) Immunohisto chemical localization of JV-methyl-D-aspartate receptor NR1, NR2A, NR2B and NR2C/D subunits in the adult mammalian cerebellum. Neurosci Lett 283:85-88.
75. Tovar KR, Westbrook GL (1999) The incorpation of NMDA receptors with a distinct subunit composition at nascent hippocampal synapses in vitro. J Neurosci 19:4180-4188.
76. Townsend M, Yoshii A, Mishina M, Constantine-Paton M (2003) Developmental loss of miniature N-methyl-D-aspartate receptor currents in NR2A knockout mice. Proc Natl Acad Sci U S A 100:1340-1345.
77. 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.
78. Weitlauf C, Honse Y, Auberson YP, Mishina M, Lovinger DM, Winder DG (2005) Activation of NR2A-containing NMDA receptors is not obligatory for NMDA receptor-dependent long-term potentiation. J Neurosci 25:8386-8390.
79. Werblin FS, Dowling JE (1969) Organization of the retina of the mudp-uppy, Necturus maculosus. II. Intracellular recording. J Neurophysiol 32:339-355.
80. Wu Y, Kawakami R, Shinohara Y, Fukaya M, Sakimura K, Mishina M, Wa-tanabe M, Ito I, Shigemoto R (2005) Target-cell-specific left-right asymmetry of NMDA receptor content in Schaffer collateral synapses in ε 1/NR2A knock-out mice. J Neurosci 25:9213-9226.
81. Yazulla S, Studholme KM (1998) Differential distribution of Shaker-like and Shab-like K+-channel subunits in goldfish retina and retinal bipolar cells. J Comp Neurol 396:131-140.
82. Zaghloul KA, Boahen K, Demb JB (2003) Different circuits for ON and OFF retinal ganglion cells cause different contrast sensitivities. J Neurosci 23:2645-2654.
83. Zhang J, Diamond JS (2006) Distinct perisynaptic and synaptic localization of NMDA and AMPA receptors on ganglion cells in rat retina. J Comp Neurol 498:810-820.
84. Zukin RS, Bennett MV (1995) Alternatively spliced isoforms of the NMDARI receptor subunit. Trends Neurosci 18:306-313.