MAGUKs in synapse assembly and function: An emerging view

Cellular and Molecular Life Sciences

Volumn 61, Issue 7-8, 2004, Pages 911-929

  Montgomery, J M ^a   Zamorano, P L ^a   Garner, C C ^a  

^a STANFORD UNIVERSITY   (United States)

Author keywords

Cytoskeleton; Glutamate receptors; MAGUKs; PDZ domain; Synapses; Synaptic plasticity

Indexed keywords

GLUTAMATE RECEPTOR; GUANYLATE KINASE; ION CHANNEL; N METHYL DEXTRO ASPARTIC ACID RECEPTOR; PDZ PROTEIN; PROTEIN P55; PROTEIN ZO1; SIGNAL PEPTIDE; SYNAPSE RECEPTOR;

HUMAN; MORPHOGENESIS; NERVE CELL MEMBRANE; NERVE CELL PLASTICITY; NERVE CONDUCTION; NERVOUS SYSTEM DEVELOPMENT; NONHUMAN; PROTEIN DOMAIN; PROTEIN PROTEIN INTERACTION; REVIEW; SIGNAL TRANSDUCTION; SRC HOMOLOGY DOMAIN; SYNAPSE; SYNAPTOGENESIS;

ANIMALS; BIOLOGICAL TRANSPORT; CA(2+)-CALMODULIN DEPENDENT PROTEIN KINASE; CARRIER PROTEINS; CENTRAL NERVOUS SYSTEM; DROSOPHILA PROTEINS; GUANYLATE KINASE; HUMANS; ION CHANNELS; MACROMOLECULAR SUBSTANCES; MEMBRANE PROTEINS; NEURONAL PLASTICITY; NEURONS; NUCLEOSIDE-PHOSPHATE KINASE; PHOSPHOPROTEINS; PROTEIN STRUCTURE, TERTIARY; RECEPTORS, GLUTAMATE; SIGNAL TRANSDUCTION; SYNAPSES;

VERTEBRATA;

EID: 2442602096     PISSN: 1420682X     EISSN: None     Source Type: Journal    
DOI: 10.1007/s00018-003-3364-5     Document Type: Review

References (180)

1. Luscher C., Xia H., Beattie E. C. et al. (1999) Role of AMPA receptor cycling in synaptic transmission and plasticity. Neuron 24: 649-658
2. Tong G., Malenka R. C. and Nicoll R. A. (1996) Long-term potentiation in cultures of single hippocampal granule cells: a presynaptic form of plasticity. Neuron 16: 1147-1157
3. Grant S. G. and Husi H. (2001) Proteomics of multiprotein complexes: answering fundamental questions in neuroscience. Trends Biotechnol. 19: S49-54
4. Husi H., Ward M. A., Choudhary J. S. et al. (2000) Proteomic analysis of NMDA receptor-adhesion protein signaling complexes. Nat. Neurosci. 3: 661-669
5. Garner C. C. and Kindler S. (1996) Synaptic proteins and the assembly of synaptic junctions. Trends in Cell Biol. 6: 429-433
6. Budnik V., Koh Y. H., Guan B. et al. (1996) Regulation of synapse structure and function by the Drosophila tumor suppressor gene dlg. Neuron 17: 627-640
7. Anderson J. M. (1996) Cell signalling: MAGUK magic. Curr. Biol. 6: 382-384
8. Chishti A. H. (1998) Function of p55 and its nonerythroid homologues. Curr. Opin. Hematol. 5: 116-121
9. Garner C. C., Nash J. and Huganir R. L. (2000) PDZ domains in synapse assembly and signalling. Trends Cell Biol. 10: 274-280
10. Gonzalez-Mariscal L., Betanzos A. and Avila-Flores A. (2000) MAGUK proteins: structure and role in the tight junction. Semin. Cell Dev. Biol. 11: 315-324
11. Koh Y. H., Gramates L. S. and Budnik V. (2000) Drosophila larval neuromuscular junction: molecular components and mechanisms underlying synaptic plasticity. Microsc. Res. Tech. 49: 14-25
12. Caruana G. (2002) Genetic studies define MAGUK proteins as regulators of epithelial cell polarity. Int. J. Dev. Biol. 46: 511-518
13. De Lorenzo C., Mechler B. M. and Bryant P. J. (1999) What is Drosophila telling us about cancer? Cancer Metastasis Rev. 18: 295-311
14. Kistner U., Garner C. C. and Linial M. (1995) Nucleotide binding by the synapse associated protein SAP90. FEBS Lett. 359: 159-163
15. Kuhlendahl S., Spangenberg O., Konrad M. et al. (1998) Functional analysis of the guanylate kinase-like domain in the synapse-associated protein SAP97. Eur. J. Biochem. 252: 305-313
16. Hoskins R., Hajnal A. F., Harp S. A. et al. (1996) The C. elegans vulval induction gene lin-2 encodes a member of the MAGUK family of cell junction proteins. Development 122: 97-111
17. Olsen O. and Bredt D. S. (2003) Functional analysis of the nucleotide binding domain of membrane-associated guanylate kinases. J. Biol. Chem. 278: 6873-6878
18. Li Y., Spangenberg O., Paarmann I. et al. (2002) Structural basis for nucleotide-dependent regulation of membrane-associated guanylate kinase-like domains. J. Biol. Chem. 277: 4159-4165
19. Saras J. and Heldin C. H. (1996) PDZ domains bind carboxy-terminal sequences of target proteins. Trends Biochem. Sci. 21: 455-458
20. Sheng M. and Sala C. (2001) PDZ domains and the organization of supramolecular complexes. Annu. Rev. Neurosci. 24: 1-29
21. Harris B. Z. and Lim W. A. (2001) Mechanism and role of PDZ domains in signaling complex assembly. J. Cell Sci. 114: 3219-3231
22. Daniels D. L., Cohen A. R., Anderson J. M. et al. (1998) Crystal structure of the hCASK PDZ domain reveals the structural basis of class II PDZ domain target recognition. Nat. Struct. Biol. 5: 317-325
23. Doyle D. A., Lee A., Lewis J. et al. (1996) Crystal structures of a complexed and peptide-free membrane protein-binding domain: molecular basis of peptide recognition by PDZ. Cell 85: 1067-1076
24. Piserchio A., Pellegrini M., Mehta S. et al. (2002) The PDZ1 domain of SAP90. Characterization of structure and binding. J. Biol. Chem. 277: 6967-6973
25. Morais Cabral J. H., Petosa C., Sutcliffe M. J. et al. (1996) Crystal structure of a PDZ domain. Nature 382: 649-652
26. Cai C., Coleman S. K., Niemi K. et al. (2002) Selective binding of synapse-associated protein 97 to GluR-A alpha-amino-5-hydroxy-3-methyl-4- isoxazole propionate receptor subunit is determined by a novel sequence motif. J. Biol. Chem. 277: 31484-31490
27. Shieh B. H. and Zhu M. Y. (1996) Regulation of the TRP Ca2+ channel by INAD in Drosophila photoreceptors. Neuron 16: 991-998
28. Gee S. H., Sekely S. A., Lombardo C. et al. (1998) Cyclic peptides as non-carboxyl-terminal ligands of syntrophin PDZ domains. J. Biol. Chem. 273: 21980-21987
29. Hillier B. J., Christopherson K. S., Prehoda K. E. et al. (1999) Unexpected modes of PDZ domain scaffolding revealed by structure of nNOS-syntrophin complex. Science 284: 812-815
30. Xia H., Winokur S. T., Kuo W. L. et al. (1997) Actinin-associated LIM protein: identification of a domain interaction between PDZ and spectrin-like repeat motifs. J. Cell Biol. 139: 507-515
31. Cuppen E., Gerrits H., Pepers B. et al. (1998) PDZ motifs in PTP-BL and RIL bind to internal protein segments in the LIM domain protein RIL. Mol. Biol. Cell 9: 671-683
32. Tavares G. A., Panepucci E. H. and Brunger A. T. (2001) Structural characterization of the intramolecular interaction between the SH3 and guanylate kinase domains of PSD-95. Mol. Cell 8: 1313-1325
33. McGee A. W., Dakoji S. R., Olsen O. et al. (2001) Structure of the SH3-guanylate kinase module from PSD-95 suggests a mechanism for regulated assembly of MAGUK scaffolding proteins. Mol. Cell 8: 1291-1301
34. Mehta S., Wu H., Garner C. C. et al. (2001) Molecular mechanisms regulating the differential association of kainate receptor subunits with SAP90/PSD-95 and SAP97. J. Biol. Chem. 276: 16092-16099
35. McGee A. W. and Bredt D. S. (1999) Identification of an intramolecular interaction between the SH3 and guanylate kinase domains of PSD-95. J. Biol. Chem. 274: 17431-17436
36. Wu H., Reissner C., Kuhlendahl S. et al. (2000) Intramolecular interactions regulate SAP97 binding to GKAP. EMBO J. 19: 5740-5751
37. Nix S. L., Chishti A. H., Anderson J. M. et al. (2000) hCASK and hDlg associate in epithelia, and their src homology 3 and guanylate kinase domains participate in both intramolecular and intermolecular interactions. J. Biol. Chem. 275: 41192-41200
38. Shin H., Hsueh Y. P., Yang F. C. et al. (2000) An intramolecular interaction between Src homology 3 domain and guanylate kinase-like domain required for channel clustering by postsynaptic density-95/SAP90. J. Neurosci. 20: 3580-3587
39. Hough C. D., Woods D. F., Park S. et al. (1997) Organizing a functional junctional complex requires specific domains of the Drosophila MAGUK Discs large. Genes Dev. 11: 3242-3253
40. Masuko N., Makino K., Kuwahara H. et al. (1999) Interaction of NE-dlg/SAP102, a neuronal and endocrine tissue-specific membrane-associated guanylate kinase protein, with calmodulin and PSD-95/SAP90. A possible regulatory role in molecular clustering at synaptic sites. J. Biol. Chem. 274: 5782-5790
41. Paarmann I., Spangenberg O., Lavie A. et al. (2002) Formation of complexes between Ca2+.calmodulin and the synapse-associated protein SAP97 requires the SH3 domain-guanylate kinase domain-connecting HOOK region. J. Biol. Chem. 277: 40832-40838
42. Brenman J. E., Topinka J. R., Cooper E. C. et al. (1998) Localization of postsynaptic density-93 to dendritic microtubules and interaction with microtubule-associated protein 1A. J. Neurosci. 18: 8805-8813
43. Marfatia S. M., Leu R. A., Branton D. et al. (1995) Identification of the protein 4.1 binding interface on glycophorin C and p55, a homologue of the Drosophila discs-large tumor suppressor protein. J. Biol. Chem. 270: 715-719
44. Lin L., Peters L. L., Ciciotte S. L. et al. (1998) cDNA sequence and chromosomal localization of mouse Dlgh3 gene adjacent to the BRCA1 tumor suppressor locus. Biochim. Biophys. Acta 1443: 211-216
45. Tseng T. C., Marfatia S. M., Bryant P. J. et al. (2001) VAM-1: a new member of the MAGUK family binds to human Veli-1 through a conserved domain. Biochim. Biophys. Acta 1518: 249-259
46. Stohr H. and Weber B. H. (2001) Cloning and characterization of the human retina-specific gene MPP4, a novel member of the p55 subfamily of MAGUK proteins. Genomics 74: 377-384
47. 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
48. Lahey T., Gorczyca M., Jia X. X. et al. (1994) The Drosophila tumor suppressor gene dlg is required for normal synaptic bouton structure. Neuron 13: 823-835
49. Woods D. F., Hough C., Peel D. et al. (1996) Dlg protein is required for junction structure, cell polarity, and proliferation control in Drosophila epithelia. J. Cell Biol. 134: 1469-1482
50. Aoki C., Miko I., Oviedo H. et al. (2001) Electron microscopic immunocytochemical detection of PSD-95, PSD-93, SAP-102, and SAP-97 at postsynaptic, presynaptic and non-synaptic sites of adult and neonatal rat visual cortex. Synapse 40: 239-257
51. Conroy W. G., Liu Z., Nai Q. et al. (2003) PDZ-containing proteins provide a functional postsynaptic scaffold for nicotinic receptors in neurons. Neuron 38: 759-771
52. Huang Y. Z., Wang Q., Won S. et al. (2002) Compartmentalized NRG signaling and PDZ domain-containing proteins in synapse structure and function. Int. J. Dev. Neurosci. 20: 173-185
53. Sheng M. and Pak D. T. (2000) Ligand-gated ion channel interactions with cytoskeletal and signaling proteins. Annu. Rev. Physiol. 62: 755-778
54. Sheng M. (2001) Molecular organization of the postsynaptic specialization. Proc. Natl. Acad. Sci. USA 98: 7058-7061
55. Hata Y., Butz S. and Sudhof T. C. (1996) CASK: a novel dlg/PSD95 homolog with an N-terminal calmodulin-dependent protein kinase domain identified by interaction with neurexins. J. Neurosci. 16: 2488-2494
56. Lee S., Fan S., Makarova O. et al. (2002) A novel and conserved protein-protein interaction domain of mammalian Lin-2/CASK binds and recruits SAP97 to the lateral surface of epithelia. Mol. Cell Biol. 22: 1778-1791
57. Butz S., Okamoto M. and Sudhof T. C. (1998) A tripartite protein complex with the potential to couple synaptic vesicle exocytosis to cell adhesion in brain. Cell 94: 773-782
58. Tabuchi K., Biederer T., Butz S. et al. (2002) CASK participates in alternative tripartite complexes in which Mint 1 competes for binding with caskin 1, a novel CASK-binding protein. J. Neurosci. 22: 4264-4273
59. Kaech S. M., Whitfield C. W. and Kim S. K. (1998) The LIN-2/LIN-7/LIN-10 complex mediates basolateral membrane localization of the C. elegans EGF receptor LET-23 in vulval epithelial cells. Cell 94: 761-771
60. Leonard A. S., Davare M. A., Horne M. C. et al. (1998) SAP97 is associated with the alpha-amino-3-hydroxy-5-methylisoxazole-4-propionic acid receptor GluR1 subunit. J. Biol. Chem. 273: 19518-19524
61. Setou M., Nakagawa T., Seog D. H. et al. (2000) Kinesin superfamily motor protein KIF17 and mLin-10 in NMDA receptor-containing vesicle transport. Science 288: 1796-1802
62. Maximov A. and Bezprozvanny I. (2002) Synaptic targeting of N-type calcium channels in hippocampal neurons. J. Neurosci. 22: 6939-6952
63. Cohen A. R., Woods D. F., Marfatia S. M. et al. (1998) Human CASK/LIN-2 binds syndecan-2 and protein 4.1 and localizes to the basolateral membrane of epithelial cells. J. Cell Biol. 142: 129-138
64. Hsueh Y. P., Yang F. C., Kharazia V. et al. (1998) Direct interaction of CASK/LIN-2 and syndecan heparan sulfate proteoglycan and their overlapping distribution in neuronal synapses. J. Cell Biol. 142: 139-151
65. Kamberov E., Makarova O., Roh M. et al. (2000) Molecular cloning and characterization of Pals, proteins associated with mLin-7. J. Biol. Chem. 275: 11425-11431
66. Roh M. H., Makarova O., Liu C. J. et al. (2002) The Maguk protein, Pals1, functions as an adapter, linking mammalian homologues of Crumbs and Discs Lost. J. Cell Biol. 157: 161-172
67. Gaide O., Favier B., Legler D. F. et al. (2002) CARMA1 is a critical lipid raft-associated regulator of TCR-induced NF-kappa B activation. Nat. Immunol. 3: 836-843
68. Pomerantz J. L., Denny E. M. and Baltimore D. (2002) CARD11 mediates factor-specific activation of NF-kappaB by the T cell receptor complex. EMBO J. 21: 5184-5194
69. Mitic L. L., Van Itallie C. M. and Anderson J. M. (2000) Molecular physiology and pathophysiology of tight junctions I. Tight junction structure and function: lessons from mutant animals and proteins. Am. J. Physiol. Gastrointest Liver Physiol. 279: G250-254
70. Fanning A. S. and Anderson J. M. (1999) Protein modules as organizers of membrane structure. Curr. Opin. Cell Biol. 11: 432-439
71. Itoh M., Nagafuchi A., Moroi S. et al. (1997) Involvement of ZO-1 in cadherin-based cell adhesion through its direct binding to alpha catenin and actin filaments. J. Cell Biol. 138: 181-192
72. Inagaki M., Irie K., Deguchi-Tawarada M. et al. (2003) Nectin-dependent localization of ZO-1 at puncta adhaerentia junctions between the mossy fiber terminals and the dendrites of the pyramidal cells in the CA3 area of adult mouse hippocampus. J. Comp. Neurol. 460: 514-524
73. Laura R. P., Ross S., Koeppen H. et al. (2002) MAGI-1: a widely expressed, alternatively spliced tight junction protein. Exp. Cell Res. 275: 155-170
74. Hirao K., Hata Y., Ide N. et al. (1998) A novel multiple PDZ domain-containing molecule interacting with N-methyl-D-aspartate receptors and neuronal cell adhesion proteins. J. Biol. Chem. 273: 21105-21110
75. Deguchi M., Hata Y., Takeuchi M. et al. (1998) BEGAIN (brain-enriched guanylate kinase-associated protein), a novel neuronal PSD-95/SAP90-binding protein. J. Biol. Chem. 273: 26269-26272
76. Yao I., Iida J., Nishimura W. et al. (2003) Synaptic localization of SAPAP1, a synaptic membrane-associated protein. Genes Cells 8: 121-129
77. Hirao K., Hata Y., Yao I. et al. (2000) Three isoforms of synaptic scaffolding molecule and their characterization. Multimerization between the isoforms and their interaction with N-methyl-D-aspartate receptors and SAP90/PSD-95-associated protein. J. Biol. Chem. 275: 2966-2972
78. Ide N., Hata Y., Nishioka H. et al. (1999) Localization of membrane-associated guanylate kinase (MAGI)-1/BAI-associated protein (BAP) 1 at tight junctions of epithelial cells. Oncogene 18: 7810-7815
79. Garner C. C., Zhai R. G., Gundelfinger E. D. et al. (2002) Molecular mechanisms of CNS synaptogenesis. Trends Neurosci. 25: 243-251
80. Ziv N. E. and Garner C. C. (2001) Principles of glutamatergic synapse formation: seeing the forest for the trees. Curr. Opin. Neurobiol. 11: 536-543
81. Dresbach T., Qualmann B., Kessels M. M. et al. (2001) The presynaptic cytomatrix of brain synapses. Cell Mol. Life Sci. 58: 94-116
82. Friedman H. V., Bresler T., Garner C. C. et al. (2000) Assembly of new individual excitatory synapses: time course and temporal order of synaptic molecule recruitment. Neuron 27: 57-69
83. Zhai R. G., Vardinon-Friedman H., Cases-Langhoff C. et al. (2001) Assembling the presynaptic active zone: a characterization of an active one precursor vesicle. Neuron 29: 131-143
84. Shapira M., Zhai R. G., Dresbach T. et al. (2003) Unitary assembly of presynaptic active zones from Piccolo-Bassoon transport vesicles. Neuron 38: 237-252
85. Bresler T., Ramati Y., Zamorano P. L. et al. (2001) The dynamics of SAP90/PSD-95 recruitment to new synaptic junctions. Mol. Cell Neurosci. 18: 149-167
86. Baines A. J. (1996) Caenorhabditis elegans LIN-2A and mammalian neuronal CASK are prototypical members of a subfamily of MAGUKs (membrane-associated guanylate kinases) characterized by a common kinase-like domain and a guanylate kinase domain predicted to bind ATP. Biochem. J. 320 (Pt 2): 694-696
87. + channels in vivo. J. Neurosci. 17: 152-159
88. Thomas U., Kim E., Kuhlendahl S. et al. (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
89. Mathew D., Gramates L. S., Packard M. et al. (2002) Recruitment of scribble to the synaptic scaffolding complex requires GUK-holder, a novel DLG binding protein. Curr. Biol. 12: 531-539
90. Gramates L. S. and Budnik V. (1999) Assembly and maturation of the Drosophila larval neuromuscular junction. Int. Rev. Neurobiol. 43: 93-117
91. Boeckers T. M., Bockmann J., Kreutz M. R. et al. (2002) ProSAP/Shank proteins - a family of higher order organizing molecules of the postsynaptic density with an emerging role in human neurological disease. J Neurochem 81: 903-910
92. Zito K., Fetter R. D., Goodman C. S. et al. (1997) Synaptic clustering of Fascilin II and Shaker: essential targeting sequences and role of Dlg. Neuron 19: 1007-1016
93. Thomas U., Ebitsch S., Gorczyca M. et al. (2000) Synaptic argeting and localization of discs-large is a stepwise process controlled by different domains of the protein. Curr. Biol. 10: 1108-1117
94. +-channels in the central nervous system and retina of Drosophila. J. Neurochem. 82: 1490-1501
95. Koh Y. H., Popova E., Thomas U. et al. (1999) Regulation of DLG localization at synapses by CaMKII-dependent phosphorylation. Cell 98: 353-363
96. Mizoguchi A., Nakanishi H., Kimura K. et al. (2002) Nectin: an adhesion molecule involved in formation of synapses. J. Cell Biol. 156: 555-565
97. Maximov A., Sudhof T. C. and Bezprozvanny I. (1999) Association of neuronal calcium channels with modular adaptor proteins. J. Biol. Chem. 274: 24453-24456
98. Spafford J. D., Munno D. W., Van Nierop P. et al. (2003) Calcium channel structural determinants of synaptic transmission between identified invertebrate neurons. J. Biol. Chem. 278: 4258-4267
99. Biederer T. and Sudhof T. C. (2001) CASK and protein 4.1 support F-actin nucleation on neurexins. J. Biol. Chem. 276: 47869-47876
100. Ho A., Morishita W., Hammer R. E. et al. (2003) A role for Mints in transmitter release: Mint 1 knockout mice exhibit impaired GABAergic synaptic transmission. Proc. Natl. Acad. Sci. USA 100: 1409-1414
101. Ohtsuka T., Hata Y., Ide N. et al. (1999) nRap GEP: a novel neural GDP/GTP exchange protein for rap1 small G protein that interacts with synaptic scaffolding molecule (S-SCAM). Biochem. Biophys. Res. Commun. 265: 38-44
102. Wu X., Hepner K., Castelino-Prabhu S. et al. (2000) Evidence for regulation of the PTEN tumor suppressor by a membrane-localized multi-PDZ domain containing scaffold protein MAGI-2. Proc. Natl. Acad. Sci. USA 97: 4233-4238
103. Iida J., Nishimura W., Yao I. et al. (2002) Synaptic localization of membrane-associated guanylate kinase-interacting protein mediated by the pleckstrin homology domain. Eur. J. Neurosci. 15: 1493-1498
104. Ide N., Hata Y., Deguchi M. et al. (1999) Interaction of S-SCAM with neural plakophilin-related Armadillo-repeat protein/delta-catenin. Biochem. Biophys. Res. Commun. 256: 456-461
105. Nishimura W., Yao I., Iida J. et al. (2002) Interaction of synaptic scaffolding molecule and Beta-catenin. J. Neurosci. 22: 757-765
106. Shoji H., Tsuchida K., Kishi H. et al. (2000) Identification and characterization of a PDZ protein that interacts with activin type II receptors. J. Biol. Chem. 275: 5485-5492
107. Mok H., Shin H., Kim S. et al. (2002) Association of the kinesin superfamily motor protein KIF1Balpha with postsynaptic density-95 (PSD-95), synapse-associated protein-97, and synaptic scaffolding molecule PSD-95/discs large/zona occludens-1 proteins. J. Neurosci. 22: 5253-5258
108. Craven S. E., El-Husseini A. E. and Bredt D. S. (1999) Synaptic targeting of the postsynaptic density protein PSD-95 mediated by lipid and protein motifs. Neuron 22: 497-509
109. El-Husseini A. E., Topinka J. R., Lehrer-Graiwer J. E. et al. (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
110. Christopherson K. S., Sweeney N. T., Craven S. E. et al. (2003) Lipid- and protein-mediated multimerization of PSD-95: implications for receptor clustering and assembly of synaptic protein networks. J. Cell Sci. 116: 3213-3219
111. El-Husseini Ael D., Schnell E., Dakoji S. et al. (2002) Synaptic strength regulated by palmitate cycling on PSD-95. Cell 108: 849-863
112. Firestein B. L., Craven S. E. and Bredt D. S. (2000) Postsynaptic targeting of MAGUKs mediated by distinct N-terminal domains. Neuroreport 11: 3479-3484
113. Garner C. C., Kindler S. and Gundelfinger E. D. (2000) Molecular determinants of presynaptic active zones. Curr. Opin. Neurobiol. 10: 321-327
114. Muller B. M., Kistner U., Veh R. W. et al. (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
115. Wu H., Reuver S. M., Kuhlendahl S. et al. (1998) Subcellular targeting and cytoskeletal attachment of SAP97 to the epithelial lateral membrane. J. Cell Sci. 111 (Pt 16): 2365-2376
116. Marfatia S. M., Byron O., Campbell G. et al. (2000) Human homologue of the Drosophila discs large tumor suppressor protein forms an oligomer in solution. Identification of the self-association site. J. Biol. Chem. 275: 13759-13770
117. McLaughlin M., Hale R., Ellston D. et al. (2002) The distribution and function of alternatively spliced insertions in hDlg. J. Biol. Chem. 277: 6406-6412
118. Hanada T., Lin L., Chandy K. G. et al. (1997) Human homologue of the Drosophila discs large tumor suppressor binds to p56lck tyrosine kinase and Shaker type Kv1.3 potassium channel in T lymphocytes. J. Biol. Chem. 272: 26899-26904
119. Tiffany A. M., Manganas L. N., Kim E. et al. (2000) PSD-95 and SAP97 exhibit distinct mechanisms for regulating K(+) channel surface expression and clustering. J. Cell Biol. 148: 147-158
120. Chetkovich D. M., Bunn R. C., Kuo S. H. et al. (2002) Postsynaptic targeting of alternative postsynaptic density-95 isoforms by distinct mechanisms. J. Neurosci. 22: 6415-6425
121. Hanada T., Takeuchi A., Sondarva G. et al. (2003) Protein 4.1-mediated membrane targeting of human discs large in epithelial cells. J. Biol. Chem. 278: 34445-34450
122. Karnak D., Lee S. and Margolis B. (2002) Identification of multiple binding partners for the amino-terminal domain of synapse-associated protein 97. J. Biol. Chem. 277: 46730-46735
123. Wu H., Nash J. E., Zamorano P. et al. (2002) Interaction of SAP97 with minus-end-directed actin motor myosin VI. Implications for AMPA receptor trafficking. J. Biol. Chem. 277: 30928-30934
124. Mendoza C., Olguin P., Lafferte G. et al. (2003) Novel isoforms of Dlg are fundamental for neuronal development in Drosophila. J. Neurosci. 23: 2093-2101
125. Lue R. A., Marfatia S. M., Branton D. et al. (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
126. Rumbaugh G., Sia G. M., Garner C. C. et al. (2003) Synapse-associated protein-97 isoform-specific regulation of surface AMPA receptors and synaptic function in cultured neurons. J. Neurosci. 23: 4567-4576
127. + channels by interaction with a family of membrane-associated guanylate kinases. Nature 378: 85-88
128. Kornau H. C., Schenker L. T., Kennedy M. B. et al. (1995) Domain interaction between NMDA receptor subunits and the postsynaptic density protein PSD-95. Science 269: 1737-1740
129. Muller B. M., Kistner U., Kindler S. et al. (1996) SAP102, a novel postsynaptic protein that interacts with NMDA receptor complexes in vivo. Neuron 17: 255-265
130. Garcia E. P., Mehta S., Blair L. A. et al. (1998) SAP90 binds and clusters kainate receptors causing incomplete desensitization. Neuron 21: 727-739
131. Irie M., Hata Y., Takeuchi M. et al. (1997) Binding of neuroligins to PSD-95. Science 277: 1511-1515
132. Kim J. H., Liao D., Lau L. F. et al. (1998) SynGAP: a synaptic RasGAP that associates with the PSD-95/SAP90 protein family. Neuron 20: 683-691
133. Chen H. J., Rojas-Soto M., Oguni A. et al. (1998) A synaptic Ras-GTPase activating protein (p135 SynGAP) inhibited by CaM kinase II. Neuron 20: 895-904
134. Kim E., Naisbitt S., Hsueh Y. P. et al. (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
135. Takeuchi M., Hata Y., Hirao K. et al. (1997) SAPAPs. A family of PSD-95/SAP90-associated proteins localized at postsynaptic density. J. Biol. Chem. 272: 11943-11951
136. Boeckers T. M., Winter C., Smalla K. H. et al. (1999) Proline-rich synapse-associated proteins ProSAP and ProSAP2 interact with synaptic proteins of the SAPAP/GKAP family. Biochem. Biophys. Res. Commun. 264: 247-252
137. Naisbitt S., Kim E., Tu J. C. et al. (1999) Shank, a novel family of postsynaptic density proteins that binds to the NMDA receptor/PSD-95/GKAP complex and cortactin. Neuron 23: 569-582
138. Sala C., Futai K., Yamamoto K. et al. (2003) Inhibition of dendritic spine morphogenesis and synaptic transmission by activity-inducible protein Homerla. J. Neurosci. 23: 6327-6337
139. Pak D. T., Yang S., Rudolph-Correia S. et al. (2001) Regulation of dendritic spine morphology by SPAR, a PSD-95-associated RapGAP. Neuron 31: 289-303
140. Colledge M., Dean R. A., Scott G. K. et al. (2000) Targeting of PKA to glutamate receptors through a MAGUK-AKAP complex. Neuron 27: 107-119
141. 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
142. Huang Y. Z., Wang Q., Won S. et al. (2001) Compartmentalized NRG signaling and PdZ domain-containing proteins in synapse structure and function. Int. J. Dev. Neurosci. 20: 173-185
143. Migaud M., Charlesworth P., Dempster M. et al. (1998) Enhanced long-term potentiation and impaired learning in mice with mutant postsynaptic density-95 protein. Nature 396: 433-439
144. Sans N., Racca C., Petralia R. S. et al. (2001) Synapse-associated protein 97 selectively associates with a subset of AMPA receptors early in their biosynthetic pathway. J. Neurosci. 21: 7506-7516
145. Sans N., Prybylowski K., Petralia R. S. et al. (2003) NMDA receptor trafficking through an interaction between PDZ proteins and the exocyst complex. Nat. Cell Biol. 5: 520-530
146. Asaba N., Hanada T., Takeuchi A. et al. (2003) Direct interaction with a kinesin-related motor mediates transport of mammalian discs large tumor suppressor homologue in epithelial cells. J. Biol. Chem. 278: 8395-8400
147. Hanada T., Lin L., Tibaldi E. V. et al. (2000) GAKIN, a novel kinesin-like protein associates with the human homologue of the Drosophila discs large tumor suppressor in T lymphocytes. J. Biol. Chem. 275: 28774-28784
148. Naisbitt S., Valtschanoff J., Allison D. W. et al. (2000) Interaction of the postsynaptic density-95/guanylate kinase domain-associated protein complex with a light chain of myosin-V and dynein. J. Neurosci. 20: 4524-4534
149. Malenka R. C. and Nicoll R. A. (1999) Long-term potentiation - a decade of progress? Science 285: 1870-1874
150. Carroll R. C., Beattie E. C., von Zastrow M. et al. (2001) Role of AMPA receptor endocytosis in synaptic plasticity. Nat. Rev. Neurosci. 2: 315-324
151. Passafaro M., Piech V. and Sheng M. (2001) Subunit-specific temporal and spatial patterns of AMPA receptor exocytosis in hippocampal neurons. Nat. Neurosci. 4: 917-926
152. Schnell E., Sizemore M., Karimzadegan S. et al. (2002) Direct interactions between PSD-95 and stargazin control synaptic AMPA receptor number. Proc. Natl. Acad. Sci. USA 99: 13902-13907
153. Borgdorff A. J. and Choquet D. (2002) Regulation of AMPA receptor lateral movements. Nature 417: 649-653
154. Nishimune A., Isaac J. T., Molnar E. et al. (1998) NSF binding to GluR2 regulates synaptic transmission. Neuron 21: 87-97
155. Osten P., Srivastava S., Inman G. J. et al. (1998) The AMPA receptor GluR2 C terminus can mediate a reversible, ATP-dependent interaction with NSF and alpha- and beta-SNAPs. Neuron 21: 99-110
156. Song I., Kamboj S., Xia J. et al. (1998) Interaction of the N-ethylmaleimide-sensitive factor with AMPA receptors. Neuron 21: 393-400
157. Valtschanoff J. G., Burette A., Davare M. A. et al. (2000) SAP97 concentrates at the postsynaptic density in cerebral cortex. Eur. J. Neurosci. 12: 3605-3614
158. Klocker N., Bunn R. C., Schnell E. et al. (2002) Synaptic glutamate receptor clustering in mice lacking the SH3 and GK domains of SAP97. Eur. J. Neurosci. 16: 1517-1522
159. Shi S., Hayashi Y., Esteban J. A. et al. (2001) Subunit-specific rules governing AMPA receptor trafficking to synapses in hippocampal pyramidal neurons. Cell 105: 331-343
160. Ehlers M. D. (2000) Reinsertion or degradation of AMPA receptors determined by activity-dependent endocytic sorting. Neuron 28: 511-525
161. Rao A. and Craig A. M. (1997) Activity regulates the synaptic localization of the NMDA receptor in hippocampal neurons. Neuron 19: 801-812
162. Crump F. T., Dillman K. S. and Craig A. M. (2001) cAMP-dependent protein kinase mediates activity-regulated synaptic targeting of NMDA receptors. J. Neurosci. 21: 5079-5088
163. Montgomery J. M., Pavlidis P. and Madison D. V. (2001) Pair recordings reveal all-silent synaptic connections and the postsynaptic expression of long-term potentiation. Neuron 29: 691-701
164. Montgomery J. M. and Madison D. V. (2002) State-dependent heterogeneity in synaptic depression between pyramidal cell pairs. Neuron 33: 765-777
165. Washbourne P., Bennett J. E. and McAllister A. K. (2002) Rapid recruitment of NMDA receptor transport packets to nascent synapses. Nat. Neurosci. 5: 751-759
166. Malinow R. and Malenka R. C. (2002) AMPA receptor trafficking and synaptic plasticity. Annu. Rev. Neurosci. 25: 103-126
167. Okabe S., Urushido T., Konno D. et al. (2001) Rapid redistribution of the postsynaptic density protein PSD-Zip45 (Homer 1c) and its differential regulation by NMDA receptors and calcium channels. J. Neurosci. 21: 9561-9571
168. Marrs G. S., Green S. H. and Dailey M. E. (2001) Rapid formation and remodeling of postsynaptic densities in developing dendrites. Nat. Neurosci. 4: 1006-1013
169. Lau L. F., Mammen A., Ehlers M. D. et al. (1996) Interaction of the N-methyl-D-aspartate receptor complex with a novel synapse-associated protein, SAP102. J. Biol. Chem. 271: 21622-21628
170. Gardoni F., Mauceri D., Fiorentini C. et al. (2003) CaMKII dependent phosphorylation regulates SAP97/NR2A interaction. J. Biol. Chem. 278: 44745-44752
171. Nong Y., Huang Y. Q., Ju W. et al. (2003) Glycine binding primes NMDA receptor internalization. Nature 422: 302-307
172. Vissel B., Krupp J. J., Heinemann S. F. et al. (2001) A use-dependent tyrosine dephosphorylation of NMDA receptors is independent of ion flux. Nat. Neurosci. 4: 587-596
173. Tovar K. R. and Westbrook G. L. (2002) Mobile NMDA receptors at hippocampal synapses. Neuron 34: 255-264
174. Roche K. W., Standley S., McCallum J. et al. (2001) Molecular determinants of NMDA receptor internalization. Nat. Neurosci. 4: 794-802
175. McGee A. W., Topinka J. R., Hashimoto K. et al. (2001) PSD-93 knock-out mice reveal that neuronal MAGUKs are not required for development or function of parallel fiber synapses in cerebellum. J. Neurosci. 21: 3085-3091
176. Caruana G. and Bernstein A. (2001) Craniofacial dysmorphogenesis including cleft palate in mice with an insertional mutation in the discs large gene. Mol. Cell Biol. 21: 1475-1483
177. Beique J. C. and Andrade R. (2003) PSD-95 regulates synaptic transmission and plasticity in rat cerebral cortex. J. Physiol. 546: 859-867
178. Tao Y. X., Rumbaugh G., Wang G. D. et al. (2003) Impaired NMDA receptor-mediated postsynaptic function and blunted NMDA receptor-dependent persistent pain in mice lacking postsynaptic density-93 protein. J. Neurosci. 23: 6703-6712
179. Ehlers M. D. (2003) Activity level controls postsynaptic composition and signaling via the ubiquitin-proteasome system. Nat. Neurosci. 6: 231-242
180. Okabe S., Kim H. D., Miwa A. et al. (1999) Continual remodeling of postsynaptic density and its regulation by synaptic activity. Nat. Neurosci. 2: 804-811