The Interaction between Stargazin and PSD-95 Regulates AMPA Receptor Surface Trafficking

Neuron

Volumn 53, Issue 5, 2007, Pages 719-734

  Bats, Cecile ^a   Groc, Laurent ^a   Choquet, Daniel ^a  

^a UNIVERSITÉ DE BORDEAUX   (France)

Author keywords

CELLBIO; MOLNEURO

Indexed keywords

AMPA RECEPTOR; GLUTAMATE RECEPTOR 2; MEMBRANE PROTEIN; POSTSYNAPTIC DENSITY PROTEIN 95; QUANTUM DOT; RECEPTOR PROTEIN; RECEPTOR SUBUNIT; STARGAZIN; UNCLASSIFIED DRUG;

ANIMAL CELL; ARTICLE; CARBOXY TERMINAL SEQUENCE; CELL LABELING; CONTROLLED STUDY; DIFFUSION; FLUORESCENCE RECOVERY AFTER PHOTOBLEACHING; HIPPOCAMPUS; NERVE CELL CULTURE; NONHUMAN; POSTSYNAPTIC MEMBRANE; PRIORITY JOURNAL; PROTEIN FAMILY; PROTEIN PROTEIN INTERACTION; PROTEIN TRANSPORT; REGULATORY MECHANISM; SYNAPTIC TRANSMISSION;

ANIMALS; CALCIUM CHANNELS; CELLS, CULTURED; EXCITATORY POSTSYNAPTIC POTENTIALS; FLUORESCENCE RECOVERY AFTER PHOTOBLEACHING; GENE EXPRESSION; GREEN FLUORESCENT PROTEINS; HIPPOCAMPUS; INTRACELLULAR SIGNALING PEPTIDES AND PROTEINS; MEMBRANE PROTEINS; MICE; NEURONS; PROTEIN BINDING; PROTEIN TRANSPORT; RECEPTOR AGGREGATION; RECEPTORS, AMPA; RECOMBINANT PROTEINS; SYNAPSES;

EID: 33847162742     PISSN: 08966273     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.neuron.2007.01.030     Document Type: Article

References (75)

1. Adesnik H., Nicoll R.A., and England P.M. Photoinactivation of native AMPA receptors reveals their real-time trafficking. Neuron 48 (2005) 977-985
2. Andrasfalvy B.K., and Magee J.C. Changes in AMPA receptor currents following LTP induction on rat CA1 pyramidal neurones. J. Physiol. 559 (2004) 543-554
3. Ashby M.C., Maier S.R., Nishimune A., and Henley J.M. Lateral diffusion drives constitutive exchange of AMPA receptors at dendritic spines and is regulated by spine morphology. J. Neurosci. 26 (2006) 7046-7055
4. Barry M.F., and Ziff E.B. Receptor trafficking and the plasticity of excitatory synapses. Curr. Opin. Neurobiol. 12 (2002) 279-286
5. Baude A., Nusser Z., Molnar E., McIlhinney R.A., and Somogyi P. High-resolution immunogold localization of AMPA type glutamate receptor subunits at synaptic and non-synaptic sites in rat hippocampus. Neuroscience 69 (1995) 1031-1055
6. Beique J.C., and Andrade R. PSD-95 regulates synaptic transmission and plasticity in rat cerebral cortex. J. Physiol. 546 (2003) 859-867
7. Beique J.C., Lin D.T., Kang M.G., Aizawa H., Takamiya K., and Huganir R.L. Synapse-specific regulation of AMPA receptor function by PSD-95. Proc. Natl. Acad. Sci. USA 103 (2006) 19535-19540
8. Blanpied T.A., Scott D.B., and Ehlers M.D. Dynamics and regulation of clathrin coats at specialized endocytic zones of dendrites and spines. Neuron 36 (2002) 435-449
9. Borgdorff A.J., and Choquet D. Regulation of AMPA receptor lateral movements. Nature 417 (2002) 649-653
10. Braithwaite S.P., Meyer G., and Henley J.M. Interactions between AMPA receptors and intracellular proteins. Neuropharmacology 39 (2000) 919-930
11. Bredt D.S., and Nicoll R.A. AMPA receptor trafficking at excitatory synapses. Neuron 40 (2003) 361-379
12. Campbell R.E., Tour O., Palmer A.E., Steinbach P.A., Baird G.S., Zacharias D.A., and Tsien R.Y. A monomeric red fluorescent protein. Proc. Natl. Acad. Sci. USA 99 (2002) 7877-7882
13. Chen L., Chetkovich D.M., Petralia R.S., Sweeney N.T., Kawasaki Y., Wenthold R.J., Bredt D.S., and Nicoll R.A. Stargazin regulates synaptic targeting of AMPA receptors by two distinct mechanisms. Nature 408 (2000) 936-943
14. Chetkovich D.M., Chen L., Stocker T.J., Nicoll R.A., and Bredt D.S. Phosphorylation of the postsynaptic density-95 (PSD-95)/discs large/zona occludens-1 binding site of stargazin regulates binding to PSD-95 and synaptic targeting of AMPA receptors. J. Neurosci. 22 (2002) 5791-5796
15. Choquet D., and Triller A. The role of receptor diffusion in the organization of the postsynaptic membrane. Nat. Rev. Neurosci. 4 (2003) 251-265
16. Christopherson K.S., Sweeney N.T., Craven S.E., Kang R., El-Husseini Ael D., and Bredt D.S. Lipid- and protein-mediated multimerization of PSD-95: implications for receptor clustering and assembly of synaptic protein networks. J. Cell Sci. 116 (2003) 3213-3219
17. Chung H.J., Xia J., Scannevin R.H., Zhang X., and Huganir R.L. Phosphorylation of the AMPA receptor subunit GluR2 differentially regulates its interaction with PDZ domain-containing proteins. J. Neurosci. 20 (2000) 7258-7267
18. Cognet L., Groc L., Lounis B., and Choquet D. Multiple routes for glutamate receptor trafficking: surface diffusion and membrane traffic cooperate to bring receptors to synapses. Sci. STKE 2006 (2006) pe13
19. Collingridge G.L., Isaac J.T., and Wang Y.T. Receptor trafficking and synaptic plasticity. Nat. Rev. Neurosci. 5 (2004) 952-962
20. Cottrell J.R., Dube G.R., Egles C., and Liu G. Distribution, density, and clustering of functional glutamate receptors before and after synaptogenesis in hippocampal neurons. J. Neurophysiol. 84 (2000) 1573-1587
21. Dahan M., Levi S., Luccardini C., Rostaing P., Riveau B., and Triller A. Diffusion dynamics of glycine receptors revealed by single-quantum dot tracking. Science 302 (2003) 442-445
22. Dakoji S., Tomita S., Karimzadegan S., Nicoll R.A., and Bredt D.S. Interaction of transmembrane AMPA receptor regulatory proteins with multiple membrane associated guanylate kinases. Neuropharmacology 45 (2003) 849-856
23. Daw M.I., Chittajallu R., Bortolotto Z.A., Dev K.K., Duprat F., Henley J.M., Collingridge G.L., and Isaac J.T. PDZ proteins interacting with C-terminal GluR2/3 are involved in a PKC-dependent regulation of AMPA receptors at hippocampal synapses. Neuron 28 (2000) 873-886
24. DeSouza S., Fu J., States B.A., and Ziff E.B. Differential palmitoylation directs the AMPA receptor-binding protein ABP to spines or to intracellular clusters. J. Neurosci. 22 (2002) 3493-3503
25. Dingledine R., Borges K., Bowie D., and Traynelis S.F. The glutamate receptor ion channels. Pharmacol. Rev. 51 (1999) 7-61
26. Ehrlich I., and Malinow R. Postsynaptic density 95 controls AMPA receptor incorporation during long-term potentiation and experience-driven synaptic plasticity. J. Neurosci. 24 (2004) 916-927
27. El-Husseini A.E., Schnell E., Chetkovich D.M., Nicoll R.A., and Bredt D.S. PSD-95 involvement in maturation of excitatory synapses. Science 290 (2000) 1364-1368
28. El-Husseini Ael D., Schnell E., Dakoji S., Sweeney N., Zhou Q., Prange O., Gauthier-Campbell C., Aguilera-Moreno A., Nicoll R.A., and Bredt D.S. Synaptic strength regulated by palmitate cycling on PSD-95. Cell 108 (2002) 849-863
29. Elias G.M., Funke L., Stein V., Grant S.G., Bredt D.S., and Nicoll R.A. Synapse-specific and developmentally regulated targeting of AMPA receptors by a family of MAGUK scaffolding proteins. Neuron 52 (2006) 307-320
30. Falk J., Thoumine O., Dequidt C., Choquet D., and Faivre-Sarrailh C. NrCAM coupling to the cytoskeleton depends on multiple protein domains and partitioning into lipid rafts. Mol. Biol. Cell 15 (2004) 4695-4709
31. Fukata Y., Tzingounis A.V., Trinidad J.C., Fukata M., Burlingame A.L., Nicoll R.A., and Bredt D.S. Molecular constituents of neuronal AMPA receptors. J. Cell Biol. 169 (2005) 399-404
32. Garner C.C., Nash J., and Huganir R.L. PDZ domains in synapse assembly and signalling. Trends Cell Biol. 10 (2000) 274-280
33. Garner C.C., Zhai R.G., Gundelfinger E.D., and Ziv N.E. Molecular mechanisms of CNS synaptogenesis. Trends Neurosci. 25 (2002) 243-251
34. Groc L., Heine M., Cognet L., Brickley K., Stephenson F.A., Lounis B., and Choquet D. Differential activity-dependent regulation of the lateral mobilities of AMPA and NMDA receptors. Nat. Neurosci. 7 (2004) 695-696
35. Groc L., Gustafsson B., and Hanse E. AMPA signalling in nascent glutamatergic synapses: there and not there!. Trends Neurosci. 29 (2006) 132-139
36. Hollmann M., and Heinemann S. Cloned glutamate receptors. Annu. Rev. Neurosci. 17 (1994) 31-108
37. Howarth M., Takao K., Hayashi Y., and Ting A.Y. Targeting quantum dots to surface proteins in living cells with biotin ligase. Proc. Natl. Acad. Sci. USA 102 (2005) 7583-7588
38. Keinanen K., Wisden W., Sommer B., Werner P., Herb A., Verdoorn T.A., Sakmann B., and Seeburg P.H. A family of AMPA-selective glutamate receptors. Science 249 (1990) 556-560
39. Kim E., and Sheng M. PDZ domain proteins of synapses. Nat. Rev. Neurosci. 5 (2004) 771-781
40. Kim C.H., Chung H.J., Lee H.K., and Huganir R.L. Interaction of the AMPA receptor subunit GluR2/3 with PDZ domains regulates hippocampal long-term depression. Proc. Natl. Acad. Sci. USA 98 (2001) 11725-11730
41. Kusumi A., Sako Y., and Yamamoto M. Confined lateral diffusion of membrane receptors as studied by single particle tracking (nanovid microscopy). Effects of calcium-induced differentiation in cultured epithelial cells. Biophys. J. 65 (1993) 2021-2040
42. Kusumi A., Nakada C., Ritchie K., Murase K., Suzuki K., Murakoshi H., Kasai R.S., Kondo J., and Fujiwara T. Paradigm shift of the plasma membrane concept from the two-dimensional continuum fluid to the partitioned fluid: high-speed single-molecule tracking of membrane molecules. Annu. Rev. Biophys. Biomol. Struct. 34 (2005) 351-378
43. Malinow R., and Malenka R.C. AMPA receptor trafficking and synaptic plasticity. Annu. Rev. Neurosci. 25 (2002) 103-126
44. Meier J., Vannier C., Serge A., Triller A., and Choquet D. Fast and reversible trapping of surface glycine receptors by gephyrin. Nat. Neurosci. 4 (2001) 253-260
45. Migaud M., Charlesworth P., Dempster M., Webster L.C., Watabe A.M., Makhinson M., He Y., Ramsay M.F., Morris R.G., Morrison J.H., et al. Enhanced long-term potentiation and impaired learning in mice with mutant postsynaptic density-95 protein. Nature 396 (1998) 433-439
46. Nicoll R.A., Tomita S., and Bredt D.S. Auxiliary subunits assist AMPA-type glutamate receptors. Science 311 (2006) 1253-1256
47. Nusser Z., Lujan R., Laube G., Roberts J.D., Molnar E., and Somogyi P. Cell type and pathway dependence of synaptic AMPA receptor number and variability in the hippocampus. Neuron 21 (1998) 545-559
48. O'Brien R.J., Lau L.F., and Huganir R.L. Molecular mechanisms of glutamate receptor clustering at excitatory synapses. Curr. Opin. Neurobiol. 8 (1998) 364-369
49. O'Brien R.J., Xu D., Petralia R.S., Steward O., Huganir R.L., and Worley P. Synaptic clustering of AMPA receptors by the extracellular immediate-early gene product Narp. Neuron 23 (1999) 309-323
50. O'Brien R., Xu D., Mi R., Tang X., Hopf C., and Worley P. Synaptically targeted narp plays an essential role in the aggregation of AMPA receptors at excitatory synapses in cultured spinal neurons. J. Neurosci. 22 (2002) 4487-4498
51. Okabe S., Urushido T., Konno D., Okado H., and Sobue K. Rapid redistribution of the postsynaptic density protein PSD-Zip45 (Homer 1c) and its differential regulation by NMDA receptors and calcium channels. J. Neurosci. 21 (2001) 9561-9571
52. Osten P., Khatri L., Perez J.L., Kohr G., Giese G., Daly C., Schulz T.W., Wensky A., Lee L.M., and Ziff E.B. Mutagenesis reveals a role for ABP/GRIP binding to GluR2 in synaptic surface accumulation of the AMPA receptor. Neuron 27 (2000) 313-325
53. Passafaro M., Piech V., and Sheng M. Subunit-specific temporal and spatial patterns of AMPA receptor exocytosis in hippocampal neurons. Nat. Neurosci. 4 (2001) 917-926
54. Perez J.L., Khatri L., Chang C., Srivastava S., Osten P., and Ziff E.B. PICK1 targets activated protein kinase Calpha to AMPA receptor clusters in spines of hippocampal neurons and reduces surface levels of the AMPA-type glutamate receptor subunit 2. J. Neurosci. 21 (2001) 5417-5428
55. Racz B., Blanpied T.A., Ehlers M.D., and Weinberg R.J. Lateral organization of endocytic machinery in dendritic spines. Nat. Neurosci. 7 (2004) 917-918
56. Rao A., Kim E., Sheng M., and Craig A.M. Heterogeneity in the molecular composition of excitatory postsynaptic sites during development of hippocampal neurons in culture. J. Neurosci. 18 (1998) 1217-1229
57. Rouach N., Byrd K., Petralia R.S., Elias G.M., Adesnik H., Tomita S., Karimzadegan S., Kealey C., Bredt D.S., and Nicoll R.A. TARP gamma-8 controls hippocampal AMPA receptor number, distribution and synaptic plasticity. Nat. Neurosci. 8 (2005) 1525-1533
58. Sans N., Petralia R.S., Wang Y.X., Blahos II J., Hell J.W., and Wenthold R.J. A developmental change in NMDA receptor-associated proteins at hippocampal synapses. J. Neurosci. 20 (2000) 1260-1271
59. Scannevin R.H., and Huganir R.L. Postsynaptic organization and regulation of excitatory synapses. Nat. Rev. Neurosci. 1 (2000) 133-141
60. Schnell E., Sizemore M., Karimzadegan S., Chen L., Bredt D.S., and Nicoll R.A. Direct interactions between PSD-95 and stargazin control synaptic AMPA receptor number. Proc. Natl. Acad. Sci. USA 99 (2002) 13902-13907
61. Seidenman K.J., Steinberg J.P., Huganir R., and Malinow R. Glutamate receptor subunit 2 Serine 880 phosphorylation modulates synaptic transmission and mediates plasticity in CA1 pyramidal cells. J. Neurosci. 23 (2003) 9220-9228
62. Serge A., Fourgeaud L., Hemar A., and Choquet D. Receptor activation and homer differentially control the lateral mobility of metabotropic glutamate receptor 5 in the neuronal membrane. J. Neurosci. 22 (2002) 3910-3920
63. Sharma K., Fong D.K., and Craig A.M. Postsynaptic protein mobility in dendritic spines: long-term regulation by synaptic NMDA receptor activation. Mol. Cell. Neurosci. 31 (2006) 702-712
64. Sheng M. Molecular organization of the postsynaptic specialization. Proc. Natl. Acad. Sci. USA 98 (2001) 7058-7061
65. Song I., and Huganir R.L. Regulation of AMPA receptors during synaptic plasticity. Trends Neurosci. 25 (2002) 578-588
66. Stein V., House D.R., Bredt D.S., and Nicoll R.A. Postsynaptic density-95 mimics and occludes hippocampal long-term potentiation and enhances long-term depression. J. Neurosci. 23 (2003) 5503-5506
67. Tardin C., Cognet L., Bats C., Lounis B., and Choquet D. Direct imaging of lateral movements of AMPA receptors inside synapses. EMBO J. 22 (2003) 4656-4665
68. Terashima A., Cotton L., Dev K.K., Meyer G., Zaman S., Duprat F., Henley J.M., Collingridge G.L., and Isaac J.T. Regulation of synaptic strength and AMPA receptor subunit composition by PICK1. J. Neurosci. 24 (2004) 5381-5390
69. Tomita S., Chen L., Kawasaki Y., Petralia R.S., Wenthold R.J., Nicoll R.A., and Bredt D.S. Functional studies and distribution define a family of transmembrane AMPA receptor regulatory proteins. J. Cell Biol. 161 (2003) 805-816
70. Tomita S., Fukata M., Nicoll R.A., and Bredt D.S. Dynamic interaction of stargazin-like TARPs with cycling AMPA receptors at synapses. Science 303 (2004) 1508-1511
71. Tomita S., Stein V., Stocker T.J., Nicoll R.A., and Bredt D.S. Bidirectional synaptic plasticity regulated by phosphorylation of stargazin-like TARPs. Neuron 45 (2005) 269-277
72. Triller A., and Choquet D. Synaptic structure and diffusion dynamics of synaptic receptors. Biol. Cell. 95 (2003) 465-476
73. Vandenberghe W., Nicoll R.A., and Bredt D.S. Interaction with the unfolded protein response reveals a role for stargazin in biosynthetic AMPA receptor transport. J. Neurosci. 25 (2005) 1095-1102
74. Vandenberghe W., Nicoll R.A., and Bredt D.S. Stargazin is an AMPA receptor auxiliary subunit. Proc. Natl. Acad. Sci. USA 102 (2005) 485-490
75. Xu D., Hopf C., Reddy R., Cho R.W., Guo L., Lanahan A., Petralia R.S., Wenthold R.J., O'Brien R.J., and Worley P. Narp and NP1 form heterocomplexes that function in developmental and activity-dependent synaptic plasticity. Neuron 39 (2003) 513-528