Activity regulates the synaptic localization of the NMDA receptor in hippocampal neurons

Neuron

Volumn 19, Issue 4, 1997, Pages 801-812

  Rao, Anuradha ^a   Craig, Ann Marie ^a  

^a UNIVERSITY OF ILLINOIS AT URBANA CHAMPAIGN   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

2 AMINO 5 PHOSPHONOVALERIC ACID; AMPA RECEPTOR; GLUTAMATE RECEPTOR; N METHYL DEXTRO ASPARTIC ACID RECEPTOR; N METHYL DEXTRO ASPARTIC ACID RECEPTOR BLOCKING AGENT; SYNAPTOPHYSIN;

ANIMAL CELL; ARTICLE; CELLULAR DISTRIBUTION; EMBRYO; HIPPOCAMPUS; IMMUNOCYTOCHEMISTRY; NERVE CELL CULTURE; NERVE CELL PLASTICITY; NEUROMUSCULAR SYNAPSE; NONHUMAN; PRIORITY JOURNAL; PYRAMIDAL NERVE CELL; RAT; RECEPTOR BINDING;

EID: 0030819659     PISSN: 08966273     EISSN: None     Source Type: Journal    
DOI: 10.1016/S0896-6273(00)80962-9     Document Type: Article

References (67)

1. Abraham, W.C., and Bear, M.F. (1996). Metaplasticity: the plasticity of synaptic plasticity. Trends Neurosci. 19, 126-130.
2. Aoki, C., Venkatesan, C., Go, C.-G., Mong, J.A., and Dawson, T.M. (1994). Cellular and subcellular localization of NMDA-R1 subunit immunoreactivity in the visual cortex of adult and neonatal rats. J. Neurosci. 14, 5202-5222.
3. Bading, H., Ginty, D., and Greenberg, M.E. (1993). Regulation of gene expression in hippocampal neurons by distinct calcium signaling pathways. Science 260, 181-186.
4. Balice-Gordon, R.J., and Lichtman, J.W. (1994). Long term synapse loss induced by focal blockade of postsynaptic receptors. Nature 372, 519-524.
5. Basarsky, T.A., Parpura, V., and Haydon, P.G. (1994). Hippocampal synaptogenesis in cell culture: developmental time course of synapse formation, calcium influx, and synaptic protein distribution. J. Neurosci. 14, 6402-6411.
6. Bekkers, J.M., and Stevens, C.F. (1989). NMDA and non-NMDA receptors are co-localized at individual excitatory synapses in cultured rat hippocampus. Nature 341, 230-233.
7. +-induced depolarization and NMDA treatment. Neuron 12, 87-95.
8. Bliss, T.V.P., and Collingridge, G.L. (1993). A synaptic model of memory: long-term potentiation in the hippocampus. Nature 361, 31-39.
9. Carmignato, G., and Vicini, S. (1992). Activity-dependent decrease in NMDA receptor responses during development of the visual cortex. Science 258, 1007-1011.
10. Cho, K.O., Hunt, C.A., and Kennedy, M.B. (1992). The rat brain postsynaptic density fraction contains a homolog of the Drosophila discs-large tumor suppressor protein. Neuron 9, 929-942.
11. Choi, D.W. (1994). Glutamate receptors and the induction of excitotoxic neuronal death. Prog. Brain Res. 100, 47-51.
12. + channel Kir 2.3 to PSD-95 is regulated by protein kinase A phosphorylation. Neuron 17, 759-767.
13. Craig, A.M., Blackstone, C.D., Huganir, R.L., and Banker, G. (1993). The distribution of glutamate receptors in cultured rat hippocampal neurons: postsynaptic clustering of AMPA-selective subunits. Neuron 10, 1055-1068.
14. Craig, A.M., Blackstone, C.D., Huganir, R.L., and 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.
15. Debski, E.A., Cline, H.T., McDonald, J.W., and Constantine-Paton, M. (1991). Chronic application of NMDA decreases the NMDA sensitivity of the evoked tectal potential in the frog. J. Neurosci. 11, 2947-2957.
16. Didier, M., Mienville, J.M., Soubrie, P., Bockaert, J., Berman, S., Bursztajn, S., and Pin, J.P. (1994). Plasticity of NMDA receptor expression during mouse cerebellar granule cell development. Eur. J. Neurosci. 6, 1536-1543.
17. Duclert, A., and Changeaux, J.-P. (1995). Acetylcholine receptor gene expression at the developing neuromuscular junction. Physiol. Rev. 75, 339-368.
18. Durand, G.M., Bennett, M.V., and Zukin, R.S. (1993). Splice variants of the N-methyl-D-aspartate receptor NR1 identify domains involved in regulation by polyamines and protein kinase. Proc. Natl. Acad. Sci. USA 90, 6731-6735.
19. Ehlers, M.D., Tingley, W.G., and Huganir, R.L. (1995). Regulated subcellular distribution of the NR1 subunit of the NMDA receptor. Science 269, 1734-1737.
20. Feldmeyer, D., and Cull-Candy, S. (1996). Functional consequences of changes in NMDA receptor subunit expression during development. J. Neurocytol. 25, 857-867.
21. Fletcher, T.L., Cameron, P., DeCamilli, P., and Banker, G. (1991). Synaptogenesis in hippocampal cultures: evidence indicating that axons and dendrites become competent to form synapses at different stages of neuronal development. J. Neurosci. 11, 1617-1628.
22. Follesa, P., and Ticku, M.N. (1996). NMDA receptor upregulation: molecular studies in cultured mouse cortical neurons after chronic antagonist exposure. J. Neurosci. 16, 2172-2178.
23. Forrest, D., Yuzaki, M., Soares, H.D., Ng, L., Luk, D.C., Sheng, M., Stewart, C.L., Morgan, J.I., Connor, G.A., and Curran, T. (1994). Targeted disruption of NMDA receptor 1 gene abolishes NMDA response and results in neonatal death. Neuron 13, 325-328.
24. Fox, K., Daw, N., Sato, H., and Czepita, D. (1991). Dark-rearing delays the loss of NMDA-receptor function in kitten visual cortex. Nature 350, 342-344.
25. Furshpan, E.J., and Potter, D.D. (1989). Seizure-like activity and cellular damage in rat hippocampal neurons in cell culture. Neuron 3, 199-207.
26. Ghosh, A., and Greenberg, M.E. (1995). Calcium signaling in neurons: molecular mechanisms and cellular consequences. Science 268, 239-247.
27. Gomperts, S.N. (1996). Clustering membrane proteins: it's all coming together with the PSD-95/SAP90 protein family. Cell 84, 659-662.
28. Goslin, K., and Banker, G. (1991). Rat hippocampal neurons in low density culture. In Culturing Nerve Cells, G. Banker and K. Goslin, eds. (Cambridge, MA: MIT Press), pp. 251-282.
29. Hall, Z.W., and Sanes, J.R. (1993). Synaptic structure and development: the neuromuscular junction. Cell 72/Neuron 10 Suppl., 99-122.
30. Hall, Z.W., and Sanes, J.R. (1993). Synaptic structure and development: the neuromuscular junction. Cell 72/Neuron 10 Suppl., 99-122.
31. Hall, R.A., and Soderling, T.R. (1997). Differential surface expression and phosphorylationof the N-methyl-D-aspartate receptor subunits NR1 and NR2 in cultured hippocampal neurons. J. Biol. Chem. 272, 4135-4140.
32. Huntley, G.W., Vickers, J.C., Brose, N., Janssen, W., Heinemann, S.H., and Morrison, J.H. (1994). Distribution and synaptic localization of immunocytochemically identified NMDA receptor subunit proteins in sensorimotor and visual cortices of monkey and human. J. Neurosci. 14, 3603-3619.
33. Isaac, J.T.R., Nicoll, R.A., and Malenka, R.C. (1995). Evidence for silent synapses: implications for the expression of LTP. Neuron 15, 427-434.
34. Ishii, T., Moriyoshi, K., Sugihara, H., Sakurada, K., Kadotani, H., Yokoi, M., Akazawa, C., Shigemoto, R., Mizuno, M., Masu, M., and Nakanishi, S. (1993). Molecular characterization of the family of the N-methyl-D-aspartate receptor subunits. J. Biol. Chem. 268, 2836-2843.
35. Jones, K., and Baughman, R.W. (1991). Both NMDA and non-NMDA subtypes of glutamate receptors are concentrated at synapses on cerebral cortical neurons in culture. Neuron 17, 103-113.
36. Johnson, R.R., Jiang, X., and Burkhalter, A. (1996). Regional and laminar differences in synaptic localization of NMDA receptor subunit NR1 splice variants in rat visula cortex and hippocampus. J. Comp. Neurol. 368, 335-355.
37. Kharazia, V.N., Phend, K.D., Rustioni, A., and Weinberg, R.J. (1996). EM colocalization of AMPA and NMDA receptor subunits at synapses in rat cerebral cortex. Neurosci. Lett. 210, 37-40.
38. + channels by interaction with a family of membrane associated guanylate kinases. Nature 378, 85-88.
39. Kim, E., Cho, K.O., Rothschild, A., and 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.
40. Kistner, U., Wenzel, B.M., Veh, R.W., Cases-Langhoff, C., Garner, A.M., Appeltauer, U., Voss, B., Gundelfinger, E.D., and Garner, C.C. (1993). SAP90, a rat presynaptic protein related to the product of the Drosophila tumor supressor gene dlg-A. J. Biol. Chem. 268, 4580-4583.
41. Kornau, H.-C., Schenker, LT., Kennedy, M.B., and Seeburg, P.H. (1995). Domain interaction between NMDA receptor subunits and the postsynaptic density protein PSD-95. Science 269, 1737-1740.
42. Kullmann, D.M., and Siegelbaum, S.A. (1995).The site of expression of NMDA receptor-dependent LTP: new fuel for an old fire. Neuron 15, 997-1002.
43. Kutsuwada, T., Kashiwabuchi, N., Mori, H., Sakimura, K., Kushiya, E., Araki, K., Meguro, H., Masaki, H., Kumanishi, T., Arakawa, M., and Mishina, M. (1992). Molecular diversity of the NMDA receptor channel. Nature 358, 36-41.
44. Laurie, D.J., and Seeburg, P.H. (1994). Regional and developmental heterogeneity in splicing of the rat brain NMDAR1 mRNA. J. Neurosci. 14, 3180-3194.
45. Li, Y., Erzurumlu, R., Chen, C., Zhaveri, S., and Tonegawa, S. (1994). Whisker-related neuronal patterns fail to develop in the trigeminal brainstem nuclei of NMDAR1 knockout mice. Cell 76, 427-437.
46. Liao, D., Hessler, N.A., and Malinow, R. (1995). Activation of postsynaptically silent synapses during pairing-induced LTP in CA1 region of hippocampal slice. Nature 375, 400-403.
47. McBain, C.J., and Mayer, M.L. (1994). N-Methyl-D-aspartic acid receptor structure and function. Physiol. Rev. 74, 723-760.
48. McDonald, J.W., Silverstein, F.S., and Johnston, M.V. (1990). MK-801 pretreatment enhances N-methyl-D-aspartate-mediated brain injury and increases brain N-methyl-D-aspartate recognition site binding in rats. Neuroscience 38, 103-113.
49. McIlhinney, R.A.J., Molnar, E., Atack, J.R., and Whiting, P.J. (1996). Cell surface expression of the human N-methyl-D-aspartate receptor subunit 1a requires the co-expression of the NR2a subunit in transfected cells. Neuroscience 70, 989-997.
50. Monyer, H., Sprengel, R., Schoepfer, R., Herb, A., Higuchi, M., Lomeli, H., Burnashev, N., Sakmann, B., and Seeburg, P.H. (1992). Heteromeric NMDA receptors: molecular and functional distinction of subtypes. Science 256, 1217-1221.
51. Monyer, H., Burnashev, N., Laurie, D.J., Sakmann, B., and Seeburg, P.M. (1994). Developmental and regional expression in the rat brain and functional properties of four NMDA receptors. Neuron 12, 529-540.
52. Moriyoshi, K., Masu, M., Ishii, T., Shigemoto, R., Mizuno, N., and Nakanishi, S. (1991). Molecular cloning and characterization of the rat NMDA receptor. Nature 354, 31-37.
53. Nguyen, Q.T., and Lichtman, J.W. (1996). Mechanism of synapse disassembly at the developing neuromuscular junction. Curr. Opin. Neurobiol. 6, 104-112.
54. Niethammer, M., Kim, E., and Sheng, M. (1996). Interaction between the C terminus of NMDA receptor subunits and multiple members of the PSD-95 family of membrane-associated guanylate kinases. J. Neurosci. 16, 2157-2163.
55. Obrietan, K., and van den Pol, A.N. (1995). Calcium hyperexcitability in neurons cultured with glutamate receptor blockade. J. Neurophysiol. 73, 1524-1536.
56. Petralia, R.S., Yokotani, N., and Wenthold, R.J. (1994a). 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.
57. Petralia, R.S., Wang, Y.-X., and Wenthold, R.J. (1994b). The NMDA receptor subunits NR2A and NR2B showhistological and ultrastructural localization patterns similar to those of NR1. J. Neurosci. 14, 6102-6120.
58. +-induced depolarization and NMDA exposure. J. Neurochem. 64, 558-565.
59. Scheetz, A.J., and Constantine-Paton, M. (1994). Modulation of NMDA receptor function: implications for vertebrate neural development. FASEB J. 8, 744-752.
60. Segal, M. (1995). Imaging of calcium variations in living dendritic spines of cultured rat hippocampal neurons. J. Physiol. 486, 283-295.
61. Sheng, M., Cummings, J., Roldan, L.A., Jan, Y.N., and Jan, L.Y. (1994). Changing composition of heteromeric NMDA receptors during development of rat cortex. Nature 368, 144-147.
62. Siegel, S.J., Brose, N., Janssen, W.G., Gasic, G.P., Jahn, R., and Heinemann, S.F. (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.
63. Siegel, S.J., Janssen, W.G., Tullai, J.W., Rogers, S.W., Moran, T., Heinemann, S.F., and Morrison, J.H. (1995). Distribution of the excitatory amino acid receptor subunits GluR2(4) in monkey hippocampus and colocalization with subunits GluR5-7 and NMDAR1. J. Neurosci. 15, 2707-2719.
64. Tsien, J.Z., Huerta, P.T., and Tonegawa, S. (1996).The essential role of hippocampal CA1 NMDA receptor-dependant synaptic plasticity in spatial memory. Cell 87, 1317-1326.
65. Vallano, M.L., Lambolez, B., Audinat, E., and Rossier, J. (1996). Neuronal activity differentially regulates NMDA receptor subunit expression in cerebellar granule cells. J. Neurosci. 16, 631-639.
66. Williams, K., Dichter, M.A., and Molinoff, P.B. (1992). Up-regulation of N-methyl-D-aspartate receptors on cultured cortical neurons after exposure to antagonists. Mol. Pharmacol. 42, 147-151.
67. Wyszynski, M., Lin, J., Rao, A., Nigh, E., Beggs, A.H., Craig, A.M., and Sheng, M. (1997). Competitive binding of α-actinin and calmodulin to the NMDA receptor. Nature 385, 439-442.