SynGAP: A synaptic RasGAP that associates with the PSD-95/SAP90 protein family

Neuron

Volumn 20, Issue 4, 1998, Pages 683-691

  Kim, Jee Hae ^a   Liao, Dezhi ^a   Lau, Lit Fui ^a   Huganir, Richard L ^a  

^a JOHNS HOPKINS UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

GUANOSINE TRIPHOSPHATASE; N METHYL DEXTRO ASPARTIC ACID; N METHYL DEXTRO ASPARTIC ACID RECEPTOR; NEUROTROPHIN; RAS PROTEIN;

AMINO ACID SEQUENCE; ARTICLE; BRAIN; IMMUNOBLOTTING; IMMUNOCYTOCHEMISTRY; NERVE CELL PLASTICITY; NORTHERN BLOTTING; POSTSYNAPTIC MEMBRANE; PRIORITY JOURNAL; PROTEIN ANALYSIS; PROTEIN EXPRESSION; PROTEIN ISOLATION; SIGNAL TRANSDUCTION; SYNAPSE; SYNAPTIC TRANSMISSION;

EID: 0032055396     PISSN: 08966273     EISSN: None     Source Type: Journal    
DOI: 10.1016/S0896-6273(00)81008-9     Document Type: Article

References (69)

1. Blackstone, C.D., Moss, S.J., Martin, L.J., Levey, A.I., Price, D.L., and Huganir, R.L. (1992). Biochemical characterization and localization of a non-N-methyl-D-aspartate glutamate receptor in rat brain. J. Neurochem. 58, 1118-1126.
2. Boguski, M.S., and McCormick, F. (1993). Proteins regulating Ras and its relatives. Nature 366, 643-654.
3. Bokoch, G.M., and Der, C.J. (1993). Emerging concepts in the Ras superfamily of GTP-binding proteins. FASEB J. 7, 750-759.
4. Brakeman, P.R., Lanahan, A.A., O'Brien, R., Roche, K., Barnes, C.A., Huganir, R.L., and Worley, P.F. (1997). Homer: a protein that selectively binds metabotropic glutamate receptors. Nature 386, 284-288.
5. Brambilla, R., Gnesutta, N., Minichiello, L., White, G., Roylance, A.J., Herron, C.E., Ramsey, M., Wolfer, D.P., Cestari, V., Rossi-Arnaud, C., et al. (1997). A role for the Ras signalling pathway in synaptic transmission and long-term memory. Nature 390, 281-286.
6. Breeden, L., and Nasmyth, K. (1985). Regulation of the yeast HO gene. Cold Spring Harbor Symp. Quant. Biol. 50, 643-650.
7. 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., et al. (1996a). Interaction of nitric oxide synthase with the postsynaptic density protein PSD-95 and α1-syntrophin mediated by PDZ domains. Cell 84, 757-767.
8. Brenman, J.E., Christopherson, K.S., Craven, S.E., McGee, A.W., and Bredt, D.S. (1996b). Cloning and characterization of postsynaptic density 93, a nitric oxide synthase interacting protein. J. Neurosci. 16, 7407-7415.
9. Carlin, R.K., Bartelt, D.C., and Siekevitz, P. (1983). Identification of fodrin as a major calmodulin-binding protein in postsynaptic density preparations. J. Cell Biol. 96, 443-448.
10. Chevray, P.M., and Nathans, D. (1992). Protein interaction cloning in yeast: identification of mammalian proteins that react with the leucine zipper of Jun. Proc. Natl. Acad. Sci. USA 89, 5789-5793.
11. 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.
12. Cullen, P.J., Hsuan, J.J., Truong, O., Letcher, A.J., Jackson, T.R., Dawson, A.P., and Irvine, R.F. (1995). Identification of a specific Ins(1,3,4,5)P4-binding protein as a member of the GAP1 family. Nature 376, 527-530.
13. Dong, H., O'Brien, R.J., Fung, E.T., Lanahan, A.A., Worley, P.F., and Huganir, R.L. (1997). GRIP: a synaptic PDZ domain-containing protein that interacts with AMPA receptors [see comments]. Nature 386, 279-284.
14. Durfee, T., Becherer, K., Chen, P.L., Yeh, S.H., Yang, Y., Kilburn, A.E., Lee, W.H., and Elledge, S.J. (1993). The retinoblastoma protein associates with the protein phosphatase type 1 catalytic subunit. Genes Dev. 7, 555-569.
15. Ehlers, M.D., Mammen, A.L., Lau, L.F., and Huganir, R.L. (1996). Synaptic targeting of glutamate receptors. Curr. Opin. Cell Biol. 8, 484-489.
16. Fields, S., and Song, O. (1989). A novel genetic system to detect protein-protein interactions. Nature 340, 245-246.
17. Figurov, A., Pozzo-Miller, L.D., Olafsson, P., Wang, T., and Lu, B. (1996). Regulation of synaptic responses to high-frequency stimulation and LTP by neurotrophins in the hippocampus. Nature 381, 706-709.
18. 2+-dependent routes to Ras: mechanisms for neuronal survival, differentiation, and plasticity? Neuron 16, 233-236.
19. Gomperts, S.N. (1996). Clustering membrane proteins: it's all coming together with the PSD-95/SAP90 protein family. Cell 84, 659-662.
20. Goslin, K., and Banker, G. (1991). Culturing Nerve Cells, K.G.A.G. Banker, ed. (Cambridge: Massachusetts Institute of Technology Press).
21. Gwag, B.J., and Springer, J.E. (1993). Activation of NMDA receptors increases brain-derived neurotrophic factor (BDNF) mRNA expression in the hippocampal formation. Neuroreport 5, 125-128.
22. 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.
23. Isackson, P.J., Huntsman, M.M., Murray, K.D., and Gall, C.M. (1991). BDNF mRNA expression is increased in adult rat forebrain after limbic seizures: temporal patterns of induction distinct from NGF. Neuron 6, 937-948.
24. Kang, H., and Schuman, E.M. (1995). Long-lasting neurotrophin-induced enhancement of synaptic transmission in the adult hippocampus. Science 267, 1658-1662.
25. Kang, H., and Schuman, E.M. (1996). A requirement for local protein synthesis in neurotrophin-induced hippocampal synaptic plasticity. Science 273, 1402-1406.
26. Kelly, P.T., and Cotman, C.W. (1978). Synaptic proteins. Characterization of tubulin and actin and identification of a distinct postsynaptic density polypeptide. J. Cell Biol. 79, 173-183.
27. 2+/calmodulin-dependent protein kinase. Proc. Natl. Acad. Sci. USA 81, 945-949.
28. Kennedy, M.B. (1995). Origin of PDZ (DHR, GLGF) domains. Trends Biochem. Sci. 20, 350.
29. Kennedy, M.B. (1997). The postsynaptic density at glutamatergic synapses. Trends Neurosci. 20, 264-268.
30. Kennedy, M.B., Bennett, M.K., and Erondu, N.E. (1983). Biochemical and immunochemical evidence that the "major postsynaptic density protein" is a subunit of a calmodulin-dependent protein kinase. Proc. Natl. Acad. Sci. USA 80, 7357-7361.
31. 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.
32. 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.
33. + channels by interaction with a family of membrane-associated guanylate kinases. Nature 378, 85-88.
34. 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 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. Korte, M., Carroll, P., Wolf, E., Brem, G., Thoenen, H., and Bonhoeffer, T. (1995). Hippocampal long-term potentiation is impaired in mice lacking brain-derived neurotrophic factor. Proc. Natl. Acad. Sci. USA 92, 8856-8860.
37. Korte, M., Griesbeck, O., Gravel, C., Carroll, P., Staiger, V., Thoenen, H., and Bonhoeffer, T. (1996). Virus-mediated gene transfer into hippocampal CA1 region restores long-term potentiation in brain-derived neurotrophic factor mutant mice. Proc. Natl. Acad. Sci. USA 93, 12547-12552.
38. Laemmli, U.K. (1970). Cleavage of structural proteins during the assembly of the head of bacteriophage T4. Nature 227, 680-685.
39. Lau, L.F., and Huganir, R.L. (1995). Differential tyrosine phosphorylation of N-methyl-D-aspartate receptor subunits. J. Biol. Chem. 270, 20036-20041.
40. Lau, L.F., Mammen, A., Ehlers, M.D., Kindler, S., Chung, W.J., Garner, C.C., and Huganir, R.L. (1996). Interaction of the N-methyl-D-aspartate receptor complex with a novel synapse-associated protein, SAP102. J. Biol. Chem. 271, 21622-21628.
41. Lue, R.A., Marfatia, S.M., Branton, D., and Chishti, A.H. (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.
42. Luo, J., Wang, Y., Yasuda, R.P., Dunah, A.W., and Wolfe, B.W. (1997). The majority of N-methyl-D-aspartate receptor complexes in adult rat cerebral cortex contain at least three different subunits (NR1/ NR2A/NR2B). Mol. Pharmacol. 51, 79-86.
43. Luo, J.H., and Weinstein, I.B. (1993). Calcium-dependent activation of protein kinase C. The role of the C2 domain in divalent cation selectivity. J. Biol. Chem. 268, 23580-23584.
44. Marshall, C.J. (1996). Ras effectors. Curr. Opin. Cell Biol. 8, 197-204.
45. Moon, I.S., Apperson, M.L., and Kennedy, M.B. (1994). The major tyrosine-phosphorylated protein in the postsynaptic density fraction is N-methyl-D-aspartate receptor subunit 2B. Proc. Natl. Acad. Sci. USA 91, 3954-3958.
46. Muller, 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. Muller, 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. Nicoll, R.A., and Malenka, R.C. (1995). Contrasting properties of two forms of long-term potentiation in the hippocampus. Nature 377, 115-118.
49. Nishizuka, Y. (1988). The molecular heterogeneity of protein kinase C and its implications for cellular regulation. Nature 334, 661-665.
50. O'Brien, R.J., Mammen, A.L., Blackshaw, S., Ehlers, M.D., Rothstein, J.D., and Huganir, R.L. (1997). The development of excitatory synapses in cultured spinal neurons. J. Neurosci. 17, 7339-7350.
51. Patterson, S.L., Grover, L.M., Schwartzkroin, P.A., and Bothwell, M. (1992). Neurotrophin expression in rat hippocampal slices: a stimulus paradigm inducing LTP in CA1 evokes increases in BDNF and NT-3 mRNAs. Neuron 9, 1081-1088.
52. Patterson, S.L., Abel, T., Deuel, T.A., Martin, K.C., Rose, J.C., and Kandel, E.R. (1996). Recombinant BDNF rescues deficits in basal synaptic transmission and hippocampal LTP in BDNF knockout mice. Neuron 16, 1137-1145.
53. Perin, M.S., Brose, N., Jahn, R., and Sudhof, T.C. (1991). Domain structure of synaptotagmin (p65). J. Biol. Chem. 266, 623-629.
54. Rao, A., and Craig, M. (1997). Activity regulates the synaptic localization of the NMDA receptor in hippocampal neurons. Neuron 19, 801-812.
55. Rosen, L.B., Ginty, D.D., Weber, M.J., and Greenberg, M.E. (1994). Membrane depolarization and calcium influx stimulate MEK and MAP kinase via activation of Ras. Neuron 12, 1207-1221.
56. Saras, J., and Heldin, C.H. (1996). PDZ domains bind carboxy-terminal sequences of target proteins. Trends Biochem. Sci. 21, 455-458.
57. Scheffzek, K., Ahmadian, M.R., Kabsch, W., Wiesmuller, L., Lautwein, A., Schmitz, F., and Wittinghofer, A. (1997). The Ras-RasGAP complex: structural basis for GTPase activation and its loss in oncogenic Ras mutants. Science 277, 333-338.
58. Seger, R., and Krebs, E.G. (1995). The MAPK signaling cascade. FASEB J. 9, 726-735.
59. Shaw, G. (1996). The pleckstrin homology domain: an intriguing multifunctional protein module. Bioessays 18, 35-46.
60. Sheng, M. (1996). PDZs and receptor/channel clustering: rounding up the latest suspects. Neuron 17, 575-578.
61. Staudinger, J., Zhou, J., Burgess, R., Elledge, S.J., and Olson, E.N. (1995). PICK1: a perinuclear binding protein and substrate for protein kinase C isolated by the yeast two-hybrid system. J. Cell Biol. 128, 263-271.
62. Takeuchi, M., Hata, Y., Hirao, K., Toyoda, A., Irie, M., and Takai, Y. (1997). SAPAPs. A family of PSD-95/SAP90-associated proteins localized at postsynaptic density. J. Biol. Chem. 272, 11943-11951.
63. + channels in vivo. J. Neurosci. 17, 152-159.
64. Thomas, U., Kim, E., Kuhlendahl, S., Koh, Y.H., Gundelfinger, E.D., Sheng, M., Garner, C.C., and Budnik, V. (1997). Synaptic clustering of the cell adhesion molecule Fasciclin II by Discs-Large and its role in the regulation of presynaptic structure. Neuron 19, 787-799.
65. Tingley, W.G., Roche, K.W., Thompson, A.K., and Huganir, R.L. (1993). Regulation of NMDA receptor phosphorylation by alternative splicing of the C-terminal domain. Nature 364, 70-73.
66. 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.
67. 2+-binding domains. J. Biol. Chem. 260, 27164-27170.
68. Zafra, F., Hengerer, B., Leibrock, J., Thoenen, H., and Lindholm, D. (1990). Activity-dependent regulation of BDNF and NGF mRNAs in the rat hippocampus is mediated by non-NMDA glutamate receptors. EMBO J. 9, 3545-3550.
69. Zito, K., Fetter, R.D., Goodman, C.S., and Isacoff, E.Y. (1997). Synaptic clustering of Fascilin II and Shaker: essential targeting sequences and role of Dlg. Neuron 19, 1007-1016.