PSD-95 is a negative regulator of the tyrosine kinase Src in the NMDA receptor complex

EMBO Journal

Volumn 25, Issue 20, 2006, Pages 4971-4982

  Kalia, Lorraine V ^a,b   Pitcher, Graham M ^a,b   Pelkey, Kenneth A ^c   Salter, Michael W ^a,b  

^a UNIVERSITY OF TORONTO   (Canada)

^b HOSPITAL FOR SICK CHILDREN   (Canada)

^c EUNICE KENNEDY SHRIVER NATIONAL INSTITUTE OF CHILD HEALTH AND HUMAN DEVELOPMENT   (United States)

Author keywords

LTP; NMDA receptor; PSD 95; SH2 domain; Src

Indexed keywords

AMINO ACID; N METHYL DEXTRO ASPARTIC ACID RECEPTOR; PEPTIDE; PHOSPHOTYROSINE; POSTSYNAPTIC DENSITY PROTEIN 95; PROTEIN TYROSINE KINASE;

AMINO ACID SEQUENCE; AMINO TERMINAL SEQUENCE; ANIMAL TISSUE; ARTICLE; CONTROLLED STUDY; EMBRYO; ENZYME ACTIVITY; HIPPOCAMPUS; HUMAN; HUMAN CELL; LONG TERM POTENTIATION; MALE; NERVE CELL; NERVE CELL CULTURE; NERVE CELL PLASTICITY; NONHUMAN; PRIORITY JOURNAL; PROTEIN ANALYSIS; PROTEIN BINDING; PROTEIN DOMAIN; PROTEIN FUNCTION; PROTEIN INTERACTION; PROTEIN PHOSPHORYLATION; PROTEIN PROTEIN INTERACTION; RAT; SYNAPTIC TRANSMISSION; UPREGULATION;

ANIMALS; CELL LINE; DOWN-REGULATION; HUMANS; INTRACELLULAR SIGNALING PEPTIDES AND PROTEINS; MEMBRANE PROTEINS; MICE; NEURONAL PLASTICITY; NEURONS; PROTEIN BINDING; RECEPTORS, N-METHYL-D-ASPARTATE; SRC HOMOLOGY DOMAINS; SRC-FAMILY KINASES; SYNAPSES; SYNAPTIC TRANSMISSION;

EID: 33750211862     PISSN: 02614189     EISSN: 14602075     Source Type: Journal    
DOI: 10.1038/sj.emboj.7601342     Document Type: Article

References (43)

1. Bibbins KB, Boeuf H, Varmus HE (1993) Binding of the Src SH2 domain to phosphopeptides is determined by residues in both the SH2 domain and the phosphopeptides. Mol Cell Biol 13: 7278-7287
2. Bliss TV, Collingridge GL (1993) A synaptic model of memory: long-term potentiation in the hippocampus. Nature 361: 31-39
3. Brown MT, Cooper JA (1996) Regulation, substrates and functions of src. Biochim Biophys Acta 1287: 121-149
4. Chang BY, Conroy KB, Machleder EM, Cartwright CA (1998) RACK1, a receptor for activated C kinase and a homolog of the beta subunit of G proteins, inhibits activity of src tyrosine kinases and growth of NIH 3T3 cells. Mol Cell Biol 18: 3245-3256
5. Chen Y, Beffert U, Ertunc M, Tang TS, Kavalali ET, Bezprozvanny I, Herz J (2005) Reelin modulates NMDA receptor activity in cortical neurons. J Neurosci 25: 8209-8216
6. Cheng HC, Nishio H, Hatase O, Ralph S, Wang JH (1992) A synthetic peptide derived from p34cdc2 is a specific and efficient substrate of src-family tyrosine kinases. J Biol Chem 267: 9248-9256
7. Cheung HH, Gurd JW (2001) Tyrosine phosphorylation of the N-methyl-D-aspartate receptor by exogenous and postsynaptic density-associated Src-family kinases. J Neurochem 78: 524-534
8. Cho KO, Hunt CA, Kennedy MB (1992) The rat brain postsynaptic density fraction contains a homolog of the Drosophila discs-large tumor suppressor protein. Neuron 9: 929-942
9. Dingledine R, Borges K, Bowie D, Traynelis SF (1999) The glutamate receptor ion channels. Pharmacol Rev 51: 7-61
10. Donaldson LW, Gish G, Pawson T, Kay LE, Forman-Kay JD (2002) Structure of a regulatory complex involving the Abl SH3 domain, the Crk SH2 domain, and a Crk-derived phosphopeptide. Proc Natl Acad Sci USA 99: 14053-14058
11. El Husseini AE, Craven SE, Chetkovich DM, Firestein BL, Schnell E, Aoki C, Bredt DS (2000) Dual palmitoylation of PSD-95 mediates its vesiculotubular sorting, postsynaptic targeting, and ion channel clustering. J Cell Biol 148: 159-172
12. Gilmer T, Rodriguez M, Jordan S, Crosby R, Alligood K, Green M, Kimery M, Wagner C, Kinder D, Charifson P (1994) Peptide inhibitors of src SH3-SH2-phosphoprotein interactions. J Biol Chem 269: 31711-31719
13. Gingrich JR, Pelkey KA, Fam SR, Huang Y, Petralia RS, Wenthold RJ, Salter MW (2004) Unique domain anchoring of Src to synaptic NMDA receptors via the mitochondrial protein NADH dehydrogenase subunit 2. Proc Natl Acad Sci USA 101: 6237-6242
14. Huang Y, Lu W, Ali DW, Pelkey KA, Pitcher GM, Lu YM, Aoto H, Roder JC, Sasaki T, Salter MW, MacDonald JF (2001) CAKbeta/Pyk2 kinase is a signaling link for induction of long-term potentiation in CA1 hippocampus. Neuron 29: 485-496
15. Husi H, Ward MA, Choudhary JS, Blackstock WP, Grant SG (2000) Proteomic analysis of NMDA receptor-adhesion protein signaling complexes. Nat Neurosci 3: 661-669
16. Jones ML, Leonard JP (2005) PKC site mutations reveal differential modulation by insulin of NMDA receptors containing NR2A or NR2B subunits. J Neurochem 92: 1431-1438
17. Kalia LV, Salter MW (2003) Interactions between Src family protein tyrosine kinases and PSD-95. Neuropharmacology 45: 720-728
18. Kamps MP, Sefton BM (1986) Neither arginine nor histidine can carry out the function of lysine-295 in the ATP-binding site of p60src. Mol Cell Biol 6: 751-757
19. Kim E, Sheng M (2004) PDZ domain proteins of synapses. Nat Rev Neurosci 5: 771-781
20. Kim E, Cho KO, Rothschild A, 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
21. 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
22. Li SC, Gish G, Yang D, Coffey AJ, Forman-Kay JD, Ernberg I, Kay LE, Pawson T (1999) Novel mode of ligand binding by the SH2 domain of the human XLP disease gene product SAP/SH2D1A. Curr Biol 9: 1355-1362
23. Lim IA, Hall DD, Hell JW (2002) Selectivity and promiscuity of the first and second PDZ domains of PSD-95 and synapse-associated protein 102. J Biol Chem 277: 21697-21711
24. Lu YM, Roder JC, Davidow J, Salter MW (1998) Src activation in the induction of long-term potentiation in CA1 hippocampal neurons. Science 279: 1363-1367
25. Macdonald DS, Weerapura M, Beazely MA, Martin L, Czerwinski W, Roder JC, Orser BA, MacDonald JF (2005) Modulation of NMDA receptors by pituitary adenylate cyclase activating peptide in CA1 neurons requires G alpha q, protein kinase C, and activation of Src. J Neurosci 25: 11374-11384
26. Masuko N, Makino K, Kuwahara H, Fukunaga K, Sudo T, Araki N, Yamamoto H, Yamada Y, Miyamoto E, Saya H (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
27. Mehta S, Wu H, Garner CC, Marshall J (2001) Molecular mechanisms regulating the differential association of kainate receptor subunits with SAP90/PSD-95 and SAP97. J Biol Chem 276: 16092-16099
28. Migaud M, Charlesworth P, Dempster M, Webster LC, Watabe AM, Makhinson 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
29. Moon IS, Apperson ML, Kennedy MB (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
30. Nada S, Shima T, Yanai H, Husi H, Grant SG, Okada M, Akiyama T (2003) Identification of PSD-93 as a substrate for the Src family tyrosine kinase Fyn. J Biol Chem 278: 47610-47621
31. Nakazawa T, Komai S, Tezuka T, Hisatsune C, Umemori H, Semba K, Mishina M, Manabe T, Yamamoto T (2001) Characterization of Fyn-mediated tyrosine phosphorylation sites on GluR epsilon 2 (NR2B) subunit of the N-methyl-D-aspartate receptor. J Biol Chem 276: 693-699
32. Pelkey KA, Askalan R, Paul S, Kalia LV, Nguyen TH, Pitcher GM, Salter MW, Lombroso PJ (2002) Tyrosine phosphatase STEP is a tonic brake on induction of long-term potentiation. Neuron 34: 127-138
33. Poy F, Yaffe MB, Sayos J, Saxena K, Morra M, Sumegi J, Cantley LC, Terhorst C, Eck MJ (1999) Crystal structures of the XLP protein SAP reveal a class of SH2 domains with extended, phosphotyrosine-independent sequence recognition. Mol Cell 4: 555-561
34. Rostas JA, Brent VA, Voss K, Errington ML, Bliss TV, Gurd JW (1996) Enhanced tyrosine phosphorylation of the 2B subunit of the N-methyl-D-aspartate receptor in long-term potentiation. Proc Natl Acad Sci USA 93: 10452-10456
35. Salter MW, Kalia LV (2004) Src kinases: a hub for NMDA receptor regulation. Nat Rev Neurosci 5: 317-328
36. Shakespeare W, Yang M, Bohacek R, Cerasoli F, Stebbins K, Sundaramoorthi R, Azimioara M, Vu C, Pradeepan S, Metcalf III C, Haraldson C, Merry T, Dalgarno D, Narula S, Hatada M, Lu X, van Schravendijk MR, Adams S, Violette S, Smith J, Guan W, Bartlett C, Herson J, Iuliucci J, Weigele M, Sawyer T (2000) Structure-based design of an osteoclast-selective, nonpeptide src homology 2 inhibitor with in vivo antiresorptive activity. Proc Natl Acad Sci USA 97: 9373-9378
37. Songyang Z, Shoelson SE, Chaudhuri M, Gish G, Pawson T, Haser WG, King F, Roberts T, Ratnofsky S, Lechleider RJ (1993) SH2 domains recognize specific phosphopeptide sequences. Cell 72: 767-778
38. Tavares GA, Panepucci EH, Brunger AT (2001) Structural characterization of the intramolecular interaction between the SH3 and guanylate kinase domains of PSD-95. Mol Cell 8: 1313-1325
39. Tezuka T, Umemori H, Akiyama T, Nakanishi S, Yamamoto T (1999) PSD-95 promotes Fyn-mediated tyrosine phosphorylation of the N-methyl-D-aspartate receptor subunit NR2A. Proc Natl Acad Sci USA 96: 435-440
40. Thomas SM, Brugge JS (1997) Cellular functions regulated by Src family kinases. Annu Rev Cell Dev Biol 13: 513-609
41. Waksman G, Shoelson SE, Pant N, Cowburn D, Kuriyan J (1993) Binding of a high affinity phosphotyrosyl peptide to the Src SH2 domain: crystal structures of the complexed and peptide-free forms. Cell 72: 779-790
42. Yaffe MB, Leparc GG, Lai J, Obata T, Volinia S, Cantley LC (2001) A motif-based profile scanning approach for genome-wide prediction of signaling pathways. Nat Biotechnol 19: 348-353
43. Yu XM, Askalan R, Keil GJ, Salter MW (1997) NMDA channel regulation by channel-associated protein tyrosine kinase Src. Science 275: 674-678