Regulation of AMPA receptor surface diffusion by PSD-95 slots

Current Opinion in Neurobiology

Volumn 22, Issue 3, 2012, Pages 453-460

  Opazo, Patricio ^a,b   Sainlos, Matthieu ^a,b   Choquet, Daniel ^a,b  

^a UNIVERSITÉ DE BORDEAUX   (France)

^b University of Bordeaux   (France)

Author keywords

[No Author keywords available]

Indexed keywords

AMPA RECEPTOR; CELL PROTEIN; POSTSYNAPTIC DENSITY PROTEIN 95; REGULATOR PROTEIN; STARGAZIN; TRANSMEMBRANE AMPA RECEPTOR REGULATORY PROTEIN; UNCLASSIFIED DRUG;

AMINO ACID SEQUENCE; CELL SURFACE; COMPLEX FORMATION; DIFFUSION; LONG TERM POTENTIATION; MEMORY; MOLECULAR STABILITY; NERVE CELL PLASTICITY; NONHUMAN; POSTSYNAPTIC DENSITY; PRIORITY JOURNAL; PROTEIN ANALYSIS; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN PROTEIN INTERACTION; RECEPTOR OCCUPANCY; RECEPTOR UPREGULATION; REVIEW; SIGNAL TRANSDUCTION; STOICHIOMETRY; SYNAPTIC TRANSMISSION;

ANIMALS; INTRACELLULAR SIGNALING PEPTIDES AND PROTEINS; LONG-TERM POTENTIATION; PROTEIN TRANSPORT; RECEPTORS, AMPA; SYNAPSES; SYNAPTIC TRANSMISSION;

EID: 84863488995     PISSN: 09594388     EISSN: 18736882     Source Type: Journal    
DOI: 10.1016/j.conb.2011.10.010     Document Type: Review

References (96)

1. Martin S.J., Grimwood P.D., Morris R.G. Synaptic plasticity and memory: an evaluation of the hypothesis. Annu Rev Neurosci 2000, 23:649-711.
2. Whitlock J.R., Heynen A.J., Shuler M.G., Bear M.F. Learning induces long-term potentiation in the hippocampus. Science 2006, 313:1093-1097.
3. Gruart A., Munoz M.D., Delgado-Garcia J.M. Involvement of the CA3-CA1 synapse in the acquisition of associative learning in behaving mice. J Neurosci 2006, 26:1077-1087.
4. Shepherd J.D., Huganir R.L. The cell biology of synaptic plasticity: AMPA receptor trafficking. Annu Rev Cell Dev Biol 2007, 23:613-643.
5. Opazo P., Choquet D. A three-step model for the synaptic recruitment of AMPA receptors. Mol Cell Neurosci 2011, 46:1-8.
6. Borgdorff A.J., Choquet D. Regulation of AMPA receptor lateral movements. Nature 2002, 417:649-653.
7. Tardin C., Cognet L., Bats C., Lounis B., Choquet D. Direct imaging of lateral movements of AMPA receptors inside synapses. Embo J 2003, 22:4656-4665.
8. Bats C., Groc L., Choquet D. The interaction between Stargazin and PSD-95 regulates AMPA receptor surface trafficking. Neuron 2007, 53:719-734.
9. Heine M., Groc L., Frischknecht R., Beique J.C., Lounis B., Rumbaugh G., Huganir R.L., Cognet L., Choquet D. Surface mobility of postsynaptic AMPARs tunes synaptic transmission. Science 2008, 320:201-205.
10. Moga D.E., Shapiro M.L., Morrison J.H. Bidirectional redistribution of AMPA but not NMDA receptors after perforant path simulation in the adult rat hippocampus in vivo. Hippocampus 2006, 16:990-1003.
11. Tao-Cheng J.H., Crocker V.T., Winters C.A., Azzam R., Chludzinski J., Reese T.S. Trafficking of AMPA receptors at plasma membranes of hippocampal neurons. J Neurosci 2011, 31:4834-4843.
12. Makino H., Malinow R. AMPA receptor incorporation into synapses during LTP: the role of lateral movement and exocytosis. Neuron 2009, 64:381-390.
13. Petrini E.M., Lu J., Cognet L., Lounis B., Ehlers M.D., Choquet D. Endocytic trafficking and recycling maintain a pool of mobile surface AMPA receptors required for synaptic potentiation. Neuron 2009, 63:92-105.
14. Opazo P., Labrecque S., Tigaret C.M., Frouin A., Wiseman P.W., De Koninck P., Choquet D. CaMKII triggers the diffusional trapping of surface AMPARs through phosphorylation of Stargazin. Neuron 2010, 67:239-252.
15. Patterson M.A., Szatmari E.M., Yasuda R. AMPA receptors are exocytosed in stimulated spines and adjacent dendrites in a Ras-ERK-dependent manner during long-term potentiation. Proc Natl Acad Sci USA 2010, 107:15951-15956.
16. Malinow R., Mainen Z.F., Hayashi Y. LTP mechanisms: from silence to four-lane traffic. Curr Opin Neurobiol 2000, 10:352-357.
17. Sheng M., Kim M.J. Postsynaptic signaling and plasticity mechanisms. Science 2002, 298:776-780.
18. Bredt D.S., Nicoll R.A. AMPA receptor trafficking at excitatory synapses. Neuron 2003, 40:361-379.
19. Malinow R., Malenka R.C. AMPA receptor trafficking and synaptic plasticity. Annu Rev Neurosci 2002, 25:103-126.
20. Garner C.C., Nash J., Huganir R.L. PDZ domains in synapse assembly and signalling. Trends Cell Biol 2000, 10:274-280.
21. Scannevin R.H., Huganir R.L. Postsynaptic organization and regulation of excitatory synapses. Nat Rev Neurosci 2000, 1:133-141.
22. Sheng M., Sala C. PDZ domains and the organization of supramolecular complexes. Annu Rev Neurosci 2001, 24:1-29.
23. Henley J. Proteins involved in the synaptic organization of AMPA (alpha-amino-3-hydroxy-5-methylisoxazolepropionate) receptors. Biochem Soc Trans 2001, 29:485-488.
24. Collingridge G.L., Isaac J.T., Wang Y.T. Receptor trafficking and synaptic plasticity. Nat Rev Neurosci 2004, 5:952-962.
25. Leonard A.S., Davare M.A., Horne M.C., Garner C.C., Hell J.W. SAP97 is associated with the alpha-amino-3-hydroxy-5-methylisoxazole-4-propionic acid receptor GluR1 subunit. J Biol Chem 1998, 273:19518-19524.
26. Waites C.L., Specht C.G., Hartel K., Leal-Ortiz S., Genoux D., Li D., Drisdel R.C., Jeyifous O., Cheyne J.E., Green W.N., et al. Synaptic SAP97 isoforms regulate AMPA receptor dynamics and access to presynaptic glutamate. J Neurosci 2009, 29:4332-4345.
27. Song I., Kamboj S., Xia J., Dong H., Liao D., Huganir R.L. Interaction of the N-ethylmaleimide-sensitive factor with AMPA receptors. Neuron 1998, 21:393-400.
28. Luthi A., Chittajallu R., Duprat F., Palmer M.J., Benke T.A., Kidd F.L., Henley J.M., Isaac J.T., Collingridge G.L. Hippocampal LTD expression involves a pool of AMPARs regulated by the NSF-GluR2 interaction. Neuron 1999, 24:389-399.
29. Nishimune A., Isaac J.T., Molnar E., Noel J., Nash S.R., Tagaya M., Collingridge G.L., Nakanishi S., Henley J.M. NSF binding to GluR2 regulates synaptic transmission. Neuron 1998, 21:87-97.
30. Lee S.H., Liu L., Wang Y.T., Sheng M. Clathrin adaptor AP2 and NSF interact with overlapping sites of GluR2 and play distinct roles in AMPA receptor trafficking and hippocampal LTD. Neuron 2002, 36:661-674.
31. Lin D.T., Makino Y., Sharma K., Hayashi T., Neve R., Takamiya K., Huganir R.L. Regulation of AMPA receptor extrasynaptic insertion by 4.1N, phosphorylation and palmitoylation. Nat Neurosci 2009, 12:879-887.
32. Frischknecht R., Heine M., Perrais D., Seidenbecher C.I., Choquet D., Gundelfinger E.D. Brain extracellular matrix affects AMPA receptor lateral mobility and short-term synaptic plasticity. Nat Neurosci 2009, 12:897-904.
33. Sia G.M., Beique J.C., Rumbaugh G., Cho R., Worley P.F., Huganir R.L. Interaction of the N-terminal domain of the AMPA receptor GluR4 subunit with the neuronal pentraxin NP1 mediates GluR4 synaptic recruitment. Neuron 2007, 55:87-102.
34. Saglietti L., Dequidt C., Kamieniarz K., Rousset M.C., Valnegri P., Thoumine O., Beretta F., Fagni L., Choquet D., Sala C., et al. Extracellular interactions between GluR2 and N-cadherin in spine regulation. Neuron 2007, 54:461-477.
35. Heine M., Thoumine O., Mondin M., Tessier B., Giannone G., Choquet D. Activity-independent and subunit-specific recruitment of functional AMPA receptors at neurexin/neuroligin contacts. Proc Natl Acad Sci USA 2008, 105:20947-20952.
36. Mondin M., Labrousse V., Hosy E., Heine M., Tessier B., Levet F., Poujol C., Blanchet C., Choquet D., Thoumine O Neurexin-neuroligin adhesions capture surface-diffusing AMPA receptors through PSD-95 scaffolds. J Neurosci 2011, 31:13500-13515.
37. Nicoll R.A., Tomita S., Bredt D.S. Auxiliary subunits assist AMPA-type glutamate receptors. Science 2006, 311:1253-1256.
38. Chen L., Chetkovich D.M., Petralia R.S., Sweeney N.T., Kawasaki Y., Wenthold R.J., Bredt D.S., Nicoll R.A. M-422: Stargazin regulates synaptic targeting of AMPA receptors by two distinct mechanisms. Nature 2000, 408:936-943.
39. Elias G.M., Nicoll R.A. Synaptic trafficking of glutamate receptors by MAGUK scaffolding proteins. Trends Cell Biol 2007, 17:343-352.
40. El-Husseini A.E., Schnell E., Chetkovich D.M., Nicoll R.A., Bredt D.S. PSD-95 involvement in maturation of excitatory synapses. Science 2000, 290:1364-1368.
41. Dakoji S., Tomita S., Karimzadegan S., Nicoll R.A., Bredt D.S. Interaction of transmembrane AMPA receptor regulatory proteins with multiple membrane associated guanylate kinases. Neuropharmacology 2003, 45:849-856.
42. Jackson A.C., Nicoll R.A. The expanding social network of ionotropic glutamate receptors: TARPs and other transmembrane auxiliary subunits. Neuron 2011, 70:178-199.
43. Schwenk J., Harmel N., Zolles G., Bildl W., Kulik A., Heimrich B., Chisaka O., Jonas P., Schulte U., Fakler B., et al. Functional proteomics identify cornichon proteins as auxiliary subunits of AMPA receptors. Science 2009, 323:1313-1319.
44. von Engelhardt J., Mack V., Sprengel R., Kavenstock N., Li K.W., Stern-Bach Y., Smit A.B., Seeburg P.H., Monyer H. CKAMP44: a brain-specific protein attenuating short-term synaptic plasticity in the dentate gyrus. Science 2010, 327:1518-1522.
45. Kalashnikova E., Lorca R.A., Kaur I., Barisone G.A., Li B., Ishimaru T., Trimmer J.S., Mohapatra D.P., Diaz E. SynDIG1: an activity-regulated, AMPA-receptor-interacting transmembrane protein that regulates excitatory synapse development. Neuron 2010, 65:80-93.
46. Deng F., Price M.G., Davis C.F., Mori M., Burgess D.L. Stargazin and other transmembrane AMPA receptor regulating proteins interact with synaptic scaffolding protein MAGI-2 in brain. J Neurosci 2006, 26:7875-7884.
47. Schnell E., Sizemore M., Karimzadegan S., Chen L., Bredt D.S., Nicoll R.A. Direct interactions between PSD-95 and stargazin control synaptic AMPA receptor number. Proc Natl Acad Sci USA 2002, 99:13902-13907.
48. Sobolevsky A.I., Rosconi M.P., Gouaux E. X-ray structure, symmetry and mechanism of an AMPA-subtype glutamate receptor. Nature 2009, 462:745-756.
49. Roberts M.F., Taylor D.W., Unger V.M. Two modes of interaction between the membrane-embedded TARP stargazin's C-terminal domain and the bilayer visualized by electron crystallography. J Struct Biol 2011, 174:542-551.
50. Xu W. PSD-95-like membrane associated guanylate kinases (PSD-MAGUKs) and synaptic plasticity. Curr Opin Neurobiol 2011, 21:306-312.
51. Nakagawa T., Futai K., Lashuel H.A., Lo I., Okamoto K., Walz T., Hayashi Y., Sheng M. Quaternary structure, protein dynamics, and synaptic function of SAP97 controlled by L27 domain interactions. Neuron 2004, 44:453-467.
52. Fomina S., Howard T.D., Sleator O.K., Golovanova M., O'Ryan L., Leyland M.L., Grossmann J.G., Collins R.F., Prince S.M. Self-directed assembly and clustering of the cytoplasmic domains of inwardly rectifying Kir2.1 potassium channels on association with PSD-95. Biochimt Biophys Acta 2011, 1808:2374-2389.
53. Chen X., Winters C., Azzam R., Li X., Galbraith J.A., Leapman R.D., Reese T.S. Organization of the core structure of the postsynaptic density. Proc Natl Acad Sci USA 2008, 105:4453-4458.
54. Vandenberghe W., Nicoll R.A., Bredt D.S. Stargazin is an AMPA receptor auxiliary subunit. Proc Natl Acad Sci USA 2005, 102:485-490.
55. Bedoukian M.A., Weeks A.M., Partin K.M. Different domains of the AMPA receptor direct stargazin-mediated trafficking and stargazin-mediated modulation of kinetics. J Biol Chem 2006, 281:23908-23921.
56. Kim K.S., Yan D., Tomita S. Assembly and stoichiometry of the AMPA receptor and transmembrane AMPA receptor regulatory protein complex. J Neurosci 2010, 30:1064-1072.
57. Nakagawa T., Cheng Y., Ramm E., Sheng M., Walz T. Structure and different conformational states of native AMPA receptor complexes. Nature 2005, 433:545-549.
58. Milstein A.D., Zhou W., Karimzadegan S., Bredt D.S., Nicoll R.A. TARP subtypes differentially and dose-dependently control synaptic AMPA receptor gating. Neuron 2007, 55:905-918.
59. Shi Y., Lu W., Milstein A.D., Nicoll R.A. The stoichiometry of AMPA receptors and TARPs varies by neuronal cell type. Neuron 2009, 62:633-640.
60. Cai C., Li H., Rivera C., Keinanen K. Interaction between SAP97 and PSD-95, two Maguk proteins involved in synaptic trafficking of AMPA receptors. J Biol Chem 2006, 281:4267-4273.
61. Christopherson K.S., Sweeney N.T., Craven S.E., Kang R., El-Husseini Ael D., Bredt D.S. Lipid- and protein-mediated multimerization of PSD-95: implications for receptor clustering and assembly of synaptic protein networks. J Cell Sci 2003, 116:3213-3219.
62. Craven S.E., El-Husseini A.E., Bredt D.S. Synaptic targeting of the postsynaptic density protein PSD-95 mediated by lipid and protein motifs. Neuron 1999, 22:497-509.
63. El-Husseini Ael D., Schnell E., Dakoji S., Sweeney N., Zhou Q., Prange O., Gauthier-Campbell C., Aguilera-Moreno A., Nicoll R.A., Bredt D.S. Synaptic strength regulated by palmitate cycling on PSD-95. Cell 2002, 108:849-863.
64. Hsueh Y.P., Sheng M. Requirement of N-terminal cysteines of PSD-95 for PSD-95 multimerization and ternary complex formation, but not for binding to potassium channel Kv1.4. J Biol Chem 1999, 274:532-536.
65. Xu W., Schluter O.M., Steiner P., Czervionke B.L., Sabatini B., Malenka R.C. Molecular dissociation of the role of PSD-95 in regulating synaptic strength and LTD. Neuron 2008, 57:248-262.
66. Masuko N., Makino K., Kuwahara H., Fukunaga K., Sudo T., Araki N., Yamamoto H., Yamada Y., Miyamoto E., Saya H. 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 1999, 274:5782-5790.
67. McGee A.W., Bredt D.S. Identification of an intramolecular interaction between the SH3 and guanylate kinase domains of PSD-95. J Biol Chem 1999, 274:17431-17436.
68. McGee A.W., Dakoji S.R., Olsen O., Bredt D.S., Lim W.A., Prehoda K.E. Structure of the SH3-guanylate kinase module from PSD-95 suggests a mechanism for regulated assembly of MAGUK scaffolding proteins. Mol Cell 2001, 8:1291-1301.
69. Shin H., Hsueh Y.P., Yang F.C., Kim E., Sheng M. An intramolecular interaction between Src homology 3 domain and guanylate kinase-like domain required for channel clustering by postsynaptic density-95/SAP90. J Neurosci 2000, 20:3580-3587.
70. Long J.F., Tochio H., Wang P., Fan J.S., Sala C., Niethammer M., Sheng M., Zhang M.J. Supramodular structure and synergistic target binding of the N-terminal tandem PDZ domains of PSD-95. J Mol Biol 2003, 327:203-214.
71. Wang W., Weng J., Zhang X., Liu M., Zhang M. Creating conformational entropy by increasing interdomain mobility in ligand binding regulation: a revisit to N-terminal tandem PDZ domains of PSD-95. J Am Chem Soc 2009, 131:787-796.
72. Sainlos M., Tigaret C., Poujol C., Olivier N.B., Bard L., Breillat C., Thiolon K., Choquet D., Imperiali B. Biomimetic divalent ligands for the acute disruption of synaptic AMPARs stabilization. Nat Chem Biol 2011, 7:81-91.
73. McCann J.J., Zheng L., Chiantia S., Bowen M.E. Domain orientation in the N-Terminal PDZ tandem from PSD-95 is maintained in the full-length protein. Structure 2011, 19:810-820.
74. Pegan S., Tan J., Huang A., Slesinger P.A., Riek R., Choe S. NMR studies of interactions between C-terminal tail of Kir2.1 channel and PDZ1,2 domains of PSD95. Biochemistry 2007, 46:5315-5322.
75. Bard L., Sainlos M., Bouchet D., Cousins S., Mikasova L., Breillat C., Stephenson F.A., Imperiali B., Choquet D., Groc L. Dynamic and specific interaction between synaptic NR2-NMDA receptor and PDZ proteins. Proc Natl Acad Sci USA 2010, 107:19561-19566.
76. Ehrlich I., Malinow R. Postsynaptic density 95 controls AMPA receptor incorporation during long-term potentiation and experience-driven synaptic plasticity. J Neurosci 2004, 24:916-927.
77. Elias G.M., Funke L., Stein V., Grant S.G., Bredt D.S., Nicoll R.A. Synapse-specific and developmentally regulated targeting of AMPA receptors by a family of MAGUK scaffolding proteins. Neuron 2006, 52:307-320.
78. Stein V., House D.R., Bredt D.S., Nicoll R.A. Postsynaptic density-95 mimics and occludes hippocampal long-term potentiation and enhances long-term depression. J Neurosci 2003, 23:5503-5506.
79. Arendt K.L., Royo M., Fernandez-Monreal M., Knafo S., Petrok C.N., Martens J.R., Esteban J.A. PIP3 controls synaptic function by maintaining AMPA receptor clustering at the postsynaptic membrane. Nat Neurosci 2010, 13:36-44.
80. Sheng M., Hoogenraad C.C. The postsynaptic architecture of excitatory synapses: a more quantitative view. Annu Rev Biochem 2007, 76:823-847.
81. Steiner P., Higley M.J., Xu W., Czervionke B.L., Malenka R.C., Sabatini B.L. Destabilization of the postsynaptic density by PSD-95 serine 73 phosphorylation inhibits spine growth and synaptic plasticity. Neuron 2008, 60:788-802.
82. Zhu Y., Pak D., Qin Y., McCormack S.G., Kim M.J., Baumgart J.P., Velamoor V., Auberson Y.P., Osten P., van Aelst L., et al. Rap2-JNK removes synaptic AMPA receptors during depotentiation. Neuron 2005, 46:905-916.
83. Grant S.G., O'Dell T.J., Karl K.A., Stein P.L., Soriano P., Kandel E.R. Impaired long-term potentiation, spatial learning, and hippocampal development in fyn mutant mice. Science 1992, 258:1903-1910.
84. de Arce K.P., Varela-Nallar L., Farias O., Cifuentes A., Bull P., Couch B.A., Koleske A.J., Inestrosa N.C., Alvarez A.R. Synaptic clustering of PSD-95 is regulated by c-Abl through tyrosine phosphorylation. J Neurosci 2010, 30:3728-3738.
85. Kim M.J., Futai K., Jo J., Hayashi Y., Cho K., Sheng M. Synaptic accumulation of PSD-95 and synaptic function regulated by phosphorylation of serine-295 of PSD-95. Neuron 2007, 56:488-502.
86. Tomita S., Stein V., Stocker T.J., Nicoll R.A., Bredt D.S. M-447: Bidirectional synaptic plasticity regulated by phosphorylation of stargazin-like TARPs. Neuron 2005, 45:269-277.
87. Sumioka A., Yan D., Tomita S. TARP phosphorylation regulates synaptic AMPA receptors through lipid bilayers. Neuron 2010, 66:755-767.
88. Kessels H.W., Kopec C.D., Klein M.E., Malinow R. Roles of stargazin and phosphorylation in the control of AMPA receptor subcellular distribution. Nat Neurosci 2009, 12:888-896.
89. 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 1998, 396:433-439.
90. Hashimoto K., Fukaya M., Qiao X., Sakimura K., Watanabe M., Kano M. Impairment of AMPA receptor function in cerebellar granule cells of ataxic mutant mouse stargazer. J Neurosci 1999, 19:6027-6036.
91. Kropf M., Rey G., Glauser L., Kulangara K., Johnsson K., Hirling H. Subunit-specific surface mobility of differentially labeled AMPA receptor subunits. Eur J Cell Biol 2008, 87:763-778.
92. Rust M.B., Gurniak C.B., Renner M., Vara H., Morando L., Gorlich A., Sassoe-Pognetto M., Banchaabouchi M.A., Giustetto M., Triller A., et al. Learning, AMPA receptor mobility and synaptic plasticity depend on n-cofilin-mediated actin dynamics. Embo J 2010, 29:1889-1902.
93. Jaskolski F., Mayo-Martin B., Jane D., Henley J.M. Dynamin-dependent membrane drift recruits AMPA receptors to dendritic spines. J Biol Chem 2009, 284:12491-12503.
94. Ehlers M.D., Heine M., Groc L., Lee M.C., Choquet D. Diffusional trapping of GluR1 AMPA receptors by input-specific synaptic activity. Neuron 2007, 54:447-460.
95. Groc L., Heine M., Cognet L., Brickley K., Stephenson F.A., Lounis B., Choquet D. Differential activity-dependent regulation of the lateral mobilities of AMPA and NMDA receptors. Nat Neurosci 2004, 7:695-696.
96. Groc L., Choquet D., Chaouloff F. The stress hormone corticosterone conditions AMPARs surface trafficking and synaptic potentiation. Nat Neurosci 2008, 11:868-870.