Differential interaction of NMDA receptor subtypes with the post-synaptic density-95 family of membrane associated guanylate kinase proteins

Journal of Neurochemistry

Volumn 104, Issue 4, 2008, Pages 903-913

  Cousins, Sarah L ^a   Papadakis, Michalis ^a,b   Rutter, A Richard ^a   Stephenson, F Anne ^a  

^a UNIVERSITY OF LONDON   (United Kingdom)

^b UNIVERSITY OF OXFORD   (United Kingdom)

Author keywords

And zo 1 protein scaffolding proteins; Chapsyn 110; Drosophila disc large tumour suppressor (DlgA); NMDA receptors; Post synaptic density protein (PSD95); Post synaptic density 95; Synapse associated protein 102; Synapse associated protein 97

Indexed keywords

CHAPSYN 110 PROTEIN; MEMBRANE ASSOCIATED GUANYLATE CYCLASE KINASE; N METHYL DEXTRO ASPARTIC ACID RECEPTOR; N METHYL DEXTRO ASPARTIC ACID RECEPTOR 1; N METHYL DEXTRO ASPARTIC ACID RECEPTOR 2A; N METHYL DEXTRO ASPARTIC ACID RECEPTOR 2B; N METHYL DEXTRO ASPARTIC ACID RECEPTOR 2C; N METHYL DEXTRO ASPARTIC ACID RECEPTOR 2D; POSTSYNAPTIC DENSITY PROTEIN 95; SYNAPSE ASSOCIATED PROTEIN 102; SYNAPSE ASSOCIATED PROTEIN 97; UNCLASSIFIED DRUG;

ARTICLE; BRAIN; CONTROLLED STUDY; DEVELOPMENT; EMBRYO; HUMAN; HUMAN CELL; IMMUNOPRECIPITATION; NERVE CELL; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN FAMILY; PROTEIN PROTEIN INTERACTION;

CELL LINE; GUANYLATE KINASE; HUMANS; INTRACELLULAR SIGNALING PEPTIDES AND PROTEINS; MEMBRANE PROTEINS; PROTEIN SUBUNITS; RECEPTORS, N-METHYL-D-ASPARTATE;

EID: 38449093908     PISSN: 00223042     EISSN: 14714159     Source Type: Journal    
DOI: 10.1111/j.1471-4159.2007.05067.x     Document Type: Article

References (44)

1. Bassand P., Bernard A., Rafiki A., Gaynet D. Krestchatisky M. (1999) Differential interaction of the tSXV motifs of the NR1 and NR2A NMDA receptor subunits with PSD-95 and SAP97. Eur. J. Neurosci. 11, 2031 2043.
2. Bence M., Arbuckle M. I., Dickson K. S. Grant S. G. N. (2005) Analyses of murine postsynaptic density-95 identify novel isoforms and potential translational control elements. Mol. Brain Res. 133, 143 152.
3. Brickley S. G., Misra C., Mok M. H. C., Mishina M. Cull-Candy S. G. (2003) NR2B and NR2D subunits coassemble in cerebellar Golgi cells to form a distinct NMDA receptor subtype restricted to extrasynaptic sites. J. Neurosci. 23, 4958 4966.
4. Chazot P. L. Stephenson F. A. (1997a) Molecular dissection of native mammalian forebrain NMDA receptors containing the NR1 C2 exon: direct demonstration of NMDA receptors comprising NR1, NR2A, and NR2B subunits within the same complex. J. Neurochem. 69, 2138 2144.
5. Chazot P. L. Stephenson F. A. (1997b) Biochemical evidence for the existence of a pool of unassembled C2 exon-containing NR1 subunits of the mammalian forebrain NMDA receptor. J. Neurochem. 68, 507 516.
6. Chazot P. L., Coleman S. K., Cik M. Stephenson F. A. (1994) Molecular characterisation of N-methyl-D-aspartate receptor expressed in mammalian cells yields evidence for the coexistence of three subunit types within a discrete receptor molecule. J. Biol. Chem. 39, 24403 24409.
7. Chen B.-S., Braud S., Badger J. D. II., Isaac J. T. R. Roche K. W. (2006) Regulation of NR1/NR2C N-methyl-D-aspartate (NMDA) receptors by phosphorylation. J. Biol. Chem. 281, 16583 16590.
8. Chetkovich D. M., Bunn R. C., Kuo S.-H., Kawasaki Y., Kohwi M. Bredt D. S. (2002) Postsynaptic targeting of alternative postsynaptic density-95 isoforms by distinct mechanisms. J. Neurosci. 22, 6415 6425.
9. Chopra B., Chazot P. L. Stephenson F. A. (2000) Characterisation of the binding of two novel glycine site antagonists to cloned NMDA receptors: evidence for two pharmacological classes of antagonists. Br. J. Pharmacol. 130, 65 72.
10. Cik M., Chazot P. L. Stephenson F. A. (1993) Optimal expression of cloned NMDAR1/NMDAR2A heteromeric glutamate receptors: a biochemical characterisation. Biochem. J. 296, 877 883.
11. Cull-Candy S., Brickley S. Farrant M. (2001) NMDA receptor subunits: diversity, development and disease. Curr. Opin. Neurobiol. 11, 327 335.
12. Dong Y. N., Waxman E. A. Lynch D. R. (2004) Interactions of postsynaptic density-95 and the NMDA receptor 2 subunit control calpain-mediated cleavage of the NMDA receptor. J. Neuroscience 24, 11035 11045.
13. El-Husseini A. E., Topinka J. R., Lehrer-Graiwer J. E., Firestein B. L., Craven S. E., Aoki C. Bredt D. S. (2000) Ion channel clustering by membrane-associated guanylate kinases. J. Biol. Chem. 275, 23904 23910.
14. Firestein B., Craven S. E. Bredt D. S. (2000) Postsynaptic targeting of MAGUKs mediated by distinct N-terminal domains. Neuroreport 11, 3479 3484.
15. Gardoni F., Mauceri D., Fiorentini C., Bellone C., Missale C., Cattabeni F. Di Luca M. (2003) CaMKII-dependent phosphorylation regulates SAP97/NR2A interaction. J. Biol. Chem. 278, 44745 44752.
16. Groc L., Heine M., Cousins S. L., Stephenson F. A., Lounis B., Cognet L. Choquet D. (2006) NMDA receptor surface trafficking depends on NR2A/NR2B subunits. Proc. Natl Acad. Sci. USA 103, 18769 18774.
17. Hawkins L. M., Chazot P. L. Stephenson F. A. (1999) Biochemical evidence for the co-association of three NR2 subunits in recombinant N-methyl-D-aspartate receptors. J. Biol. Chem. 274, 27211 27218.
18. Hsueh Y.-P., Kim E. Sheng M. (1997) Disulfide-linked head-to-head multimerization in the mechanism of ion channel clustering by PSD-95. Neuron 18, 803 814.
19. Kim E. Sheng M. (2004) PDZ domain proteins of synapses. Nat. Rev. Neurosci. 5, 771 781.
20. Kim E., Cho K. O., 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 H. C., Schenker L. T., Kennedy M. B. Seeburg P. H. (1995) Domain interaction between NMDA receptor subunits and the postsynaptic density protein PSD-95. Science 269, 1737 1740.
22. Lin Y., Skeberdis A., Francesconi A., Bennett M. V. L. Zukin R. Z. (2004) Postsynaptic density protein-95 regulates NMDA channel gating and surface expression. J. Neurosci. 24, 10138 10148.
23. Lin Y., Jover-Mengual T., Wong J., Bennett M. V. L. Zukin R. S. (2006) PSD-95 and PKC converge in regulating NMDA receptor trafficking and gating. Proc. Natl Acad. Sci. USA 103, 19902 19907.
24. Losi G., Prybylowski K., Fu Z., Lou J., Wenthold R. J. Vicini S. (2003) PSD-95 regulates NMDA receptors in developing cerebellar granule neurones of the rat. J. Physiol. 548, 21 29.
25. McIlhinney R. A. J., le Bourdelles B., Tricuad N., Molnar E., Streit P. Whiting P. J. (1998) Assembly intracellular targeting and cell surface expression of the human N-methyl-D-aspartate receptor subunits NR1a and NR2A in transfected cells. Neuropharmacology 37, 1355 1367.
26. Mi R., Sia G.-K., Rosen K., Tang X., Moghekar A., Black J. L., McEnery M., Huganir R. L. O'Brien R. J. (2004) AMPA receptor-dependent clustering of synaptic NMDA receptors is mediated by stargazin and NR2A/B in spinal neurons and hippocampal interneurons. Neuron 44, 335 349.
27. 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 GluRε2 (NR2B) subunit of the N-methyl-D-aspartate receptor. J. Biol. Chem. 276, 693 699.
28. Niethammer M., Kim E. 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.
29. Papadakis M., Hawkins L. M. Stephenson F. A. (2004) Appropriate NR1-NR1 disulfide-linked homodimer formation is requisite for efficient expression of functional, cell surface N-methyl-D-aspartate NR1/NR2 receptors. J. Biol. Chem. 279, 14703 14712.
30. Roche K. W., Standley S., McCallum J., Dune Ly C., Ehlers M. D. Wenthold R. J. (2001) Molecular determinants of NMDA receptor internalization. Nat. Neurosci. 4, 794 802.
31. Rutter A. R. Stephenson F. A. (2000) Co-expression of PSD-95 with NMDA receptors results in enhanced receptor expression together with a decreased sensitivity to L-glutamate. J. Neurochem. 75, 2501 2510.
32. Rutter A. R., Freeman F. M. Stephenson F. A. (2002) Further characterization of the molecular interaction between PSD-95 and NMDA receptors: the effect of the NR1 splice variant and evidence for modulation of channel gating. J. Neurochem. 81, 1298 1307.
33. Salter M. W. Kalia L. V. (2004) Src kinases: a hub for NMDA receptor regulation. Nat. Rev. Neurosci. 5, 317 328.
34. Sans N., Petralia R. S., wang Y.-X., Blahos J. II., Hell J. W. Wenthold R. J. (2000) A developmental change in NMDA receptor-associated proteins at hippocampal synapses. J. Neurosci. 20, 1260 1271.
35. Sans N., Prybylowski K., Petralia R. S., Chang K., Wang Y.-X., Racca C., Vicini S. Wenthold R. J. (2003) NMDA receptor trafficking through an interaction between PDZ proteins and the exocyst complex. Nat. Cell Biol. 5, 520 530.
36. Sans N., Wang P. Y., Du Q., Petralia R. S., Wang Y.-X., Nakka S., Blumer J. B., Macara I. Wenthold R. J. (2005) mPins modulates PSD-95 and SAP102 trafficking and influences NMDA receptor surface expression. Nat. Cell Biol. 7, 1179 1190.
37. Seabold G. K., Burette A., Lim I. A., Weinberg R. J. Hell J. W. (2003) Interaction of the tyrosine kinase Pyk2 with the N-methyl-D-asparate receptor complex via the src homology 3 domains of PSD-95 and SAP102. J. Biol. Chem. 278, 15040 15048.
38. Standley S., Roche K. R., McCallum J., Sans N. Wenthold R. J. (2000) PDZ domain suppression of an ER retention signal in NMDA receptor NR1 splice variants. Neuron 28, 887 898.
39. Thompson C. L., Drewery D. L., Atkins H. D., Stephenson F. A. Chazot P. L. (2000) Immunohistochemical localization of N-methyl-D-aspartate receptor NR1, NR2A, NR2B and NR2C/D subunits in the adult mammalian cerebellum. Neurosci. Lett. 283, 85 88.
40. + channel Kv1.4. Neuron 20, 125 134.
41. Van Zundert B., Yoshi A. Constantine-Paton M. (2004) Receptor compartmentalisation and trafficking at glutamate synapses: a developmental proposal. Trends Neurosci. 27, 428 436.
42. Wang L., Piserchio A. Mierke A.F. (2005) Structural characterization of the intermolecular interactions of synapse-associated protein-97 with the NR2B subunit of N-methyl-D-aspartate receptors. J. Biol. Chem. 280, 26992 26996.
43. Yamada Y., Chochi Y., Takamiya K., Sobue K. Inui M. (1999) Modulation of the channel activity of the ε2/ζ1-subtype N-methyl-D-aspartate receptor by PSD-95. J. Biol. Chem. 274, 6647 6652.
44. Yamada Y., Iwamoto T., Watanabe Y., Sobue K. Inui M. (2002) PSD-95 eliminates Src-induced potentiation of NR1/NR2A-subtype NMDA receptor channels and reduces high affinity zinc inhibition. J. Neurochem. 81, 758 764.