SAP90 binds and clusters kainate receptors causing incomplete desensitization

Neuron

Volumn 21, Issue 4, 1998, Pages 727-739

  Garcia, Elizabeth P ^a   Mehta, Sunil ^a   Blair, Leslie A C ^a   Wells, David G ^b   Shang, Jing ^a   Fukushima, Teruyuki ^a   Fallon, Justin R ^b   Garner, Craig C ^c   Marshall, John ^a  

^a BROWN UNIVERSITY   (United States)

^b BROWN UNIVERSITY   (United States)

^c UNIVERSITY OF ALABAMA AT BIRMINGHAM   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ALPHA AMINO 3 HYDROXY 5 METHYL 4 ISOXAZOLEPROPIONIC ACID; GLUTAMIC ACID; KAINIC ACID RECEPTOR; N METHYL DEXTRO ASPARTIC ACID RECEPTOR; NEUROTRANSMITTER;

AMINO ACID SEQUENCE; ARTICLE; CARBOXY TERMINAL SEQUENCE; DESENSITIZATION; ELECTROPHYSIOLOGY; MAMMAL; PRIORITY JOURNAL; PROTEIN BINDING; PROTEIN TARGETING; RECEPTOR BINDING;

EID: 0032191152     PISSN: 08966273     EISSN: None     Source Type: Journal    
DOI: 10.1016/S0896-6273(00)80590-5     Document Type: Article

References (71)

1. Bartlett, W.P., and Banker, G.A. (1984). An electron microscopic study of the development of axons and dendrites of hippocampal neurons in culture: II. synaptic relationships. J. Neurosci. 4, 1954-1965.
2. Bettler, B., Boulter, J., Hermans-Borgmeyer, I., O'Shea-Greenfield, A., Deneris, E.S., Moll, C., Borgmeyer, U., Hollmann, M., and Heinemann, S.F. (1990). Cloning of a novel glutamate receptor subunit, GluR5: expression in the nervous system during development. Neuron 5, 583-595.
3. Brenman, J.E., Chao, D.S., Gee, S.H., McGee, A.W., Craven, S.E., Santillano, D.R., Wu, Z., Huang, F., Xia, H., Peters, M.F., Froehner, S.C., and Bredt, D.S. (1996). Interaction of nitric oxide synthase with the postsynaptic density protein PSD-95 and α1-syntrophin mediated by PDZ domains. Cell 84, 757-767.
4. Bunnel, S.C., Henry, P.A., Kolluri, R., Kirchhausen, T., Rickles, R.J., and Berg, L.J. (1997). Identification of Itk/Tsk Src homology 3 domain ligands. J. Biol. Chem. 271, 25646-25656.
5. Castillo, P.E., Malenka, R.C., and Nicoll, R.A. (1997). Kainate receptors mediate a slow postsynaptic current in hippocampal CA3 neurons. Nature 388, 182-186.
6. Chen, C., and Okayama, H. (1987). High efficiency transformation of mammalian cells by plasmid DNA. Mol. Cell. Biol. 7, 2745-2752.
7. Cho, K.O., Hunt, C.A., and Kennedy, M.B. (1992). The rat brain post-synaptic density fraction contains a homolog of the Drosophila discs-large tumor suppressor protein. Neuron 9, 929-942.
8. Clarke, V.R.J., Ballyk, B.A., Hoo, K.H., Mandelzys, A., Pellizzari, A., Bath, C.P., Thomas, J., Sharpe, E.F., Davies, C.H., Ornstein, P.L., et al. (1997). A hippocampal GluR5 kainate receptor regulating inhibitory synaptic transmission. Nature 389, 599-603.
9. + channel Kir 2.3 to PSD-95 is regulated by protein kinase A phosphorylation. Neuron 17, 759-767.
10. 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.
11. Dawson, T.M., Dawson, V.L., and Snyder, S.H. (1992). A novel neuronal mesenger molecule in brain: free radical, nitric oxide. Ann. Neurol. 32, 297-311.
12. Doyle, D.A., Lee, A., Lewis, J., Kim, E., Sheng, M., and MacKinnon, R. (1996). Crystal structures of a complexed and peptide-free membrane protein-binding domain: molecular basis of peptide recognition by PDZ. Cell 85, 1067-1076.
13. Egebjerg, J., Bettler, B., Hermans-Borgmeyer, I., and Heinemann, S.F. (1991). Cloning of a cDNA for a glutamate receptor subunit activated by kainate but not AMPA. Nature 351, 745-748.
14. Ehlers, M.D., Mammen, A.L., Lau, L.F., and Huganir, R.L. (1996a). Synaptic targeting of glutamate receptors. Curr. Opin. Cell. Biol. 8, 484-489.
15. Ehlers, M.D., Shang, S., Bernhardt, J.P., and Huganir, R.L. (1996b). Inactivation of NMDA receptors by direct interaction of calmodulin with the NR1 subunit. Cell 84, 745-755.
16. Erpel, T., Superti-Furga, G., and Courtneidge, S.A. (1995). Mutational analysis of the Src SH3 domain: the same residues of the ligand binding surface are important for intra- and intermolecular interactions. EMBO. J. 14, 963-975.
17. Feng, S., Kasahara, C., Rickles, R.J., and Schreiber, S.L. (1995). Specific interactions outside the proline-rich core of two classes of Src homology 3 ligands. Proc. Natl. Acad. Sci. USA 92, 12408-12415.
18. Garcia, E.P., McPherson, P.S., Chilcote, T.J., Takei, K., and De Camilli, P. (1996). rb Sec 1A and B colocalize with syntaxin 1 and SNAP-25 throughout the axon, but are not in a stable complex with syntaxin. J. Cell. Biol. 129, 105-120.
19. Goslin, K., and Banker, G. (1991). Rat hippocampal neurons in low density. In Culturing Nerve Cells, G. Banker and K. Goslin, eds. (Cambridge, MA: MIT Press), pp. 251-282.
20. Harris, E.W., and Cotman, C.W. (1986). Long-term potentiation of guinea-pig mossy fibre responses is not blocked by N-methyl-D-aspartate antagonists. Neurosci. Lett. 70, 132-137.
21. Herb, A., Burnashev, N., Werner, P., Sakmann, B., Wisden, W., and Seeburg, P.H. (1992). The KA-2 subunit of excitatory amino acid receptors shows widespread expression in brain and forms ion channels with distantly related subunits. Neuron 8, 775-785.
22. Hollmann, M., and Heinemann, S.F. (1994). Cloned glutamate receptors. Annu. Rev. Neurosci. 17, 31-108.
23. Huettner, J.E. (1990). Glutamate receptor channels in rat DRG neurons: activation by kainate and quisqualate and blockade of desensitization by Con A. Neuron 5, 255-266.
24. Hunt, C.A., Schenker, L.J., and Kennedy, M.B. (1996). PSD-95 is associated with the postsynaptic density and not with the presynaptic membrane at forebrain synapses. J. Neurosci. 16, 1380-1388.
25. Huntley, G.W., Rogers, S.W., Moran, T., Janssen, W., Archin, N., Vickers, J.C., Cauley, K., Heinemann, S.F., and Morrison, J.H. (1993). Selective distribution of kainate receptors subunits immunoreactivity in monkey neocortex revealed by a monoclonal antibody that recognizes glutamate receptor subunits GluR5/6/7. J. Neurosci. 13, 2965-2981.
26. Jones, M.V., and Westbrook, G.L. (1996). The impact of receptor desensitization on fast synaptic transmission. Trends Neurosci. 19, 96-101.
27. Kennedy, M.B. (1997). The postsynaptic density at glutamatergic synapses. Trends Neurosci. 20, 264-268.
28. + channel clustering activity of PSD-95 and SAP97, two related membrane-associated putative guanylate kinases. Neuropharmacol. 35, 993-1000.
29. + channels by interaction with a family of membrane-associated guanylate kinases. Nature 378, 85-86.
30. 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.
31. Kim, E., Naisbitt, S., Hsueh, Y.P., Rao, A., Rothschild, A., Craig, A.M., and Sheng, M. (1997). GKAP, a novel synaptic protein that interacts with the guanylate kinase-like domain of the PSD-95/SAP90 family of channel clustering molecules. J. Cell. Biol. 136, 669-678.
32. Kim, J.H., Liao, D., Lau, L.-F., and Huganir, R.L. (1998). SynGAP: a synaptic RasGAP that associates with the PSD-95/SAP90 protein family. Neuron 20, 683-691.
33. Kirsch, J., and Betz, H. (1998). Glycine-receptor activation is required for receptor clustering in spinal neurons. Nature 392, 717-720.
34. Kistner, U., Wenzel, B.M., Veh, R.W., Cases-Langhoff, C., Garner, A., 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 suppressor gene dlg-A. J. Biol. Chem. 268, 4580-4583.
35. Kornau, H.C., Schenker, L.T., 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.
36. Kuhlendahl, S., Spangenberg, O., Konrad, M., Kim, E., and Garner, C.C. (1998). Functional analysis of the guanylate kinase-like domain in the synapse-associated protein SAP97. Eur. J. Biochem., in press.
37. Lahey, T., Gorczyca, M., Jia, X.X., and Budnik, V. (1994). The Drosophila tumor suppressor gene dlg is required for normal synaptic bouton structure. Neuron 13, 823-835.
38. Lee, C.H., Leung, B., Lemmon, M.A., Zheng, J., Cowburn, D., Kuriyan, J., and Saksela, K. (1995). A single amino acid in the SH3 domain of Hck determines its high affinity and specificity in binding to HIV-1 Nef protein. EMBO J. 14, 5006-5015.
39. Lerma, J. (1997). Kainate reveals its targets. Neuron 19, 1155-1158.
40. Lerma, J., Paternain, A.V., Naranjo, J.R., and Mellstrom, B. (1993). Functional kainate-selective glutamate receptor in cultured hippocampal neurons. Proc. Natl. Acad. Sci. USA 90, 11688-11692.
41. Marshall, J., Molloy, R., Moss, G.W.J., Howe, J.R., and Hughes, T.E. (1995). The jellyfish green fluorescent protein: a new tool for studying ion channel expression and function. Neuron 14, 211-215.
42. Matoskova, B., Wong, W.T., Nomura, N., Robbins, K.C., and Di Fiore, P.P. (1996). RN-tre specifically binds to the SH3 domain of eps8 with high affinity and confers growth advantage to NIH3T3 upon carboxy-terminal truncation. Oncogene 12, 2679-2688.
43. Mayer, B.J., and Eck, M.J. (1995). SH3 domains: minding your p's and q's. Curr. Biol. 5, 364-367.
44. McPherson, P., Garcia, E.P., David, C., Takei, K., and DeCamilli, P. (1996). A presynaptic inositol-5-phosphatase. Nature 379, 353-357.
45. Mulle, C., Sailer, A., Pèrez-Otaño, I., Dickinson-Anson, H., Castillo, P.E., Bureau, I., Maron, C., Gage, F.H., Mann, J.R., Bettler, B., and Heinemann, S.F. (1998). Altered synaptic physiology and reduced susceptibility to kainate-induced seizures in GluR6-deficient mice. Nature 392, 601-605.
46. Müller, B.M., Kistner, U., Veh, R. W., Cases-Langhoff, C., Becker, B., Gundelfinger, E.D., and Garner, C.C. (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.
47. Müller, B.M., Kistner, U., Kindler, S., Chung, W.J., Kuhlendahl, S., Fenster, S.D., Lau, L.F., Veh, R.W., Huganir, R.L., Gundelfinger, E.D., and Garner, C.C. (1996). SAP102, a novel postsynaptic protein that interacts with NMDA receptor complexes in vivo. Neuron 17, 255-265.
48. Naisbitt, S., Kim, E., Weinberg, R.J., Rao, A., Yang, F.C., Craig, A.M., and Sheng, M. (1997). Characterization of guanylate kinase-associated protein, a postsynaptic density protein at excitatory synapses that interacts directly with postsynaptic density-95/synapse-associated protein 90. J. Neurosci. 17, 5687-5696.
49. 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.
50. Niethammer, M., Valtschanoff, J.G., Kapoor, T.M., Allison, D.W., Weinberg, R.J., Craig, A.M., and Sheng, M. (1998). CRIPT, a novel postsynaptic protein that binds to the third PDZ domain of PSD-95/SAP90. Neuron 20, 693-707.
51. Otis, T., Zhang, S., and Trussell, L.O. (1996). Direct measurement of AMPA receptor desensitization induced by glutamatergic synaptic transmission. J. Neurosci. 16, 7496-7504.
52. Paternain, A.V., Morales, M., and Lerma, J. (1995). Selective antagonism of AMPA receptors unmasks kainate receptor-mediated responses in hippocampal neurons. Neuron 14, 185-189.
53. Pawson, T., and Scott, J.D. (1997). Signaling through scaffold, anchoring, and adaptor proteins. Science 278, 2975-2080.
54. Rae, J., Cooper, K., Gates, P., and Watsky, M. (1991). Low access resistance perforated patch recordings using amphotericin B. J. Neurosci. Meth. 37, 15-26.
55. Rao, A., Kim, E., Sheng, M., and Craig, A.M. (1998). Heterogeneity in the molecular composition of excitatory postsynaptic sites during development of hippocampal neurons in culture. J. Neurosci. 18, 1217-1229.
56. Raymond, L.A., Blackstone, C.D., and Huganir, R.L. (1993). Phosphorylation and modulation of recombinant GluR6 glutamate receptors by cAMP-dependent protein kinase. Nature 361, 637-641.
57. Sastry, L., Lin, W., Wong, W.T., Di Fiore, P.P., Scoppa, C.A., and King, C.R. (1995). Quantitative analysis of Grb2-Sos1 interaction: the N terminal SH3 domain of Grb2 mediates affinity. Oncogene 11, 1107-1112.
58. Schiffer, H.H., Swanson, G.T., and Heinemann, S.F. (1997). Rat GluR7 and a carboxy-terminal splice variant, GluR7b, are functional kainate receptor subunits with a low sensitivity to glutamate. Neuron 19, 1141-1146.
59. Seeburg, P.H. (1993). The molecular biology of mammalian glutamate receptor channels. Trends Neurosci. 16, 359-648.
60. Sheng, M. (1996). PDZs and receptor/channel clustering: rounding up the latest suspects. Neuron 17, 575-578.
61. 2+ channel by InaD in Drosophila photoreceptors. Neuron 16, 991-998.
62. Swanson, G.T., Gereau, R.W., Green, T., and Heinemann, S.F. (1997). Identification of amino acid residues that control functional behavior in GluR5 and GluR6 kainate receptors. Neuron 19, 913-926.
63. Tsunoda, S., Sierralta, J., Sun, Y., Bodner, R., Suzuki, E., Becker, A., Socolich, M., and Zucker, C.S. (1997). A multivalent PDZ-domain protein assembles signaling complexes in a G-protein-coupled cascade. Nature 288, 243-249.
64. Vignes, M., and Collingridge, G.L. (1997). The synaptic activation of kainate receptors. Nature 388, 179-182.
65. Wang, L.-Y., Taverna, F.A., Huang, X.-P., MacDonald, J.F., and Hampson, D.R. (1993). Phosphorylation and modulation of a kainate receptor (GluRB) by cAMP-dependent protein kinase. Science 259, 1173-1175.
66. Weng, Z., Rickles, R.J., Feng, S., Richard, S., Shaw, A.S., Schreiber, S.L., and Brugge, J.S. (1995). Structure-function analysis of SH3 domains: SH3 binding specificity altered by single amino acid substitutions. Mol. Cell. Biol. 15, 5627-5634.
67. Wenthold, R.J., Trunpy, V.A., Zhu, W.-S., and Petralia, R.S. (1994). Biochemical and assembly properties of GluR6 and KA2, two members of the kainate receptor family, determined with subunit-specific antibodies. J. Biol. Chem. 269, 1332-1339.
68. Wilding, T.J., and Huettner, J.E. (1997). Activation and desentization of hippocampal kainate receptors. J. Neurosci. 17, 2713-2721.
69. Woods, D.F., and Bryant, P.J. (1991). The discs-large tumor suppressor gene of Drosophila encodes a guanylate kinase homolog localized at septate junctions. Cell 66, 451-464.
70. Wyszynski, M., Lin, J., Rao, A., Nigh, E., Beggs, A.M., Craig, A.M., and Sheng, M. (1997). Competitive binding of alpha-actinin and calmodulin to the NMDA receptor. Nature 385, 439-442.
71. Zorumski, C.F., Mennerick, S., and Que, J. (1996). Modulation of excitatory synaptic transmission by low concentrations of glutamate in cultured rat hippocampal neurons. J. Physiol. 494, 465-477.