Diffusional Trapping of GluR1 AMPA Receptors by Input-Specific Synaptic Activity

Neuron

Volumn 54, Issue 3, 2007, Pages 447-460

  Ehlers, Michael D ^a   Heine, Martin ^b   Groc, Laurent ^b   Lee, Ming Chia ^a   Choquet, Daniel ^b  

^a DUKE UNIVERSITY MEDICAL CENTER   (United States)

^b University of Bordeaux   (France)

Author keywords

MOLNEURO; PROTEINS; SIGNALING

Indexed keywords

AMPA RECEPTOR; ANTIPORTER; GLUTAMATE RECEPTOR 1;

ANIMAL CELL; ANIMAL EXPERIMENT; ARTICLE; CONTROLLED STUDY; DIFFUSION; EMBRYO; NONHUMAN; POSTSYNAPTIC MEMBRANE; PRIORITY JOURNAL; RAT; SYNAPTIC MEMBRANE; SYNAPTIC TRANSMISSION;

EID: 34247464768     PISSN: 08966273     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.neuron.2007.04.010     Document Type: Article

References (71)

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. Ashby M.C., De La Rue S.A., Ralph G.S., Uney J., Collingridge G.L., and Henley J.M. Removal of AMPA receptors (AMPARs) from synapses is preceded by transient endocytosis of extrasynaptic AMPARs. J. Neurosci. 24 (2004) 5172-5176
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. Bats C., Groc L., and Choquet D. The interaction between Stargazin and PSD-95 regulates AMPA receptor surface trafficking. Neuron 53 (2007) 719-734
5. Baude A., Nusser Z., Roberts J.D., Mulvihill E., McIlhinney R.A., and Somogyi P. The metabotropic glutamate receptor (mGluR1 alpha) is concentrated at perisynaptic membrane of neuronal subpopulations as detected by immunogold reaction. Neuron 11 (1993) 771-787
6. 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
7. Boehm J., Kang M.G., Johnson R.C., Esteban J., Huganir R.L., and Malinow R. Synaptic incorporation of AMPA receptors during LTP is controlled by a PKC phosphorylation site on GluR1. Neuron 51 (2006) 213-225
8. Borgdorff A.J., and Choquet D. Regulation of AMPA receptor lateral movements. Nature 417 (2002) 649-653
9. Bredt D.S., and Nicoll R.A. AMPA receptor trafficking at excitatory synapses. Neuron 40 (2003) 361-379
10. Cheezum M.K., Walker W.F., and Guilford W.H. Quantitative comparison of algorithms for tracking single fluorescent particles. Biophys. J. 81 (2001) 2378-2388
11. 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 10.1126/stke.3272006pe13
12. 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
13. Davis G.W. Homeostatic control of neural activity: from phenomenology to molecular design. Annu. Rev. Neurosci. 29 (2006) 307-323
14. Ehlers M.D. Reinsertion or degradation of AMPA receptors determined by activity-dependent endocytic sorting. Neuron 28 (2000) 511-525
15. Ehlers M.D. Activity level controls postsynaptic composition and signaling via the ubiquitin-proteasome system. Nat. Neurosci. 6 (2003) 231-242
16. Esteban J.A., Shi S.H., Wilson C., Nuriya M., Huganir R.L., and Malinow R. PKA phosphorylation of AMPA receptor subunits controls synaptic trafficking underlying plasticity. Nat. Neurosci. 6 (2003) 136-143
17. Franks K.M., Stevens C.F., and Sejnowski T.J. Independent sources of quantal variability at single glutamatergic synapses. J. Neurosci. 23 (2003) 3186-3195
18. Friedman H.V., Bresler T., Garner C.C., and Ziv N.E. Assembly of new individual excitatory synapses: time course and temporal order of synaptic molecule recruitment. Neuron 27 (2000) 57-69
19. Gardner S.M., Takamiya K., Xia J., Suh J.G., Johnson R., Yu S., and Huganir R.L. Calcium-permeable AMPA receptor plasticity is mediated by subunit-specific interactions with PICK1 and NSF. Neuron 45 (2005) 903-915
20. Geinisman Y., de Toledo-Morrell L., Morrell F., Heller R.E., Rossi M., and Parshall R.F. Structural synaptic correlate of long-term potentiation: formation of axospinous synapses with multiple, completely partitioned transmission zones. Hippocampus 3 (1993) 435-445
21. Gerges N.Z., Backos D.S., Rupasinghe C.N., Spaller M.R., and Esteban J.A. Dual role of the exocyst in AMPA receptor targeting and insertion into the postsynaptic membrane. EMBO J. 25 (2006) 1623-1634 10.1038/sj.emboj.7601065 Published online April 6, 2006
22. 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 10.1038/nn1270 Published online June 20, 2004
23. Groc L., Heine M., Cousins S.L., Stephenson F.A., Lounis B., Cognet L., and Choquet D. NMDA receptor surface mobility depends on NR2A-2B subunits. Proc. Natl. Acad. Sci. USA 103 (2006) 18769-18774 10.1073/pnas.0605238103 Published online November 21, 2006
24. Harms K.J., and Craig A.M. Synapse composition and organization following chronic activity blockade in cultured hippocampal neurons. J. Comp. Neurol. 490 (2005) 72-84
25. Harms K.J., Tovar K.R., and Craig A.M. Synapse-specific regulation of AMPA receptor subunit composition by activity. J. Neurosci. 25 (2005) 6379-6388
26. Holcman D., and Triller A. Modeling synaptic dynamics driven by receptor lateral diffusion. Biophys. J. 91 (2006) 2405-2415
27. Kharazia V.N., and Weinberg R.J. Tangential synaptic distribution of NMDA and AMPA receptors in rat neocortex. Neurosci. Lett. 238 (1997) 41-44
28. Kopec C.D., Li B., Wei W., Boehm J., and Malinow R. Glutamate receptor exocytosis and spine enlargement during chemically induced long-term potentiation. J. Neurosci. 26 (2006) 2000-2009
29. 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
30. 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
31. Luscher C., Xia H., Beattie E.C., Carroll R.C., von Zastrow M., Malenka R.C., and Nicoll R.A. Role of AMPA receptor cycling in synaptic transmission and plasticity. Neuron 24 (1999) 649-658
32. Mammen A.L., Huganir R.L., and O'Brien R.J. Redistribution and stabilization of cell surface glutamate receptors during synapse formation. J. Neurosci. 17 (1997) 7351-7358
33. Matsuzaki M., Ellis-Davies G.C., Nemoto T., Miyashita Y., Iino M., and Kasai H. Dendritic spine geometry is critical for AMPA receptor expression in hippocampal CA1 pyramidal neurons. Nat. Neurosci. 4 (2001) 1086-1092
34. Matsuzaki M., Honkura N., Ellis-Davies G.C., and Kasai H. Structural basis of long-term potentiation in single dendritic spines. Nature 429 (2004) 761-766 10.1038/nature02617 Published online June 9, 2004
35. McKinney R.A., Capogna M., Durr R., Gahwiler B.H., and Thompson S.M. Miniature synaptic events maintain dendritic spines via AMPA receptor activation. Nat. Neurosci. 2 (1999) 44-49
36. Morone N., Fujiwara T., Murase K., Kasai R.S., Ike H., Yuasa S., Usukura J., and Kusumi A. Three-dimensional reconstruction of the membrane skeleton at the plasma membrane interface by electron tomography. J. Cell Biol. 174 (2006) 851-862 10.1083/jcb.200606007 Published online September 5, 2006
37. Murphy T.H., Blatter L.A., Bhat R.V., Fiore R.S., Wier W.G., and Baraban J.M. Differential regulation of calcium/calmodulin-dependent protein kinase II and p42 MAP kinase activity by synaptic transmission. J. Neurosci. 14 (1994) 1320-1331
38. 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
39. O'Brien R.J., Kamboj S., Ehlers M.D., Rosen K.R., Fischbach G.D., and Huganir R.L. Activity-dependent modulation of synaptic AMPA receptor accumulation. Neuron 21 (1998) 1067-1078
40. Oh M.C., Derkach V.A., Guire E.S., and Soderling T.R. Extrasynaptic membrane trafficking regulated by GluR1 serine 845 phosphorylation primes AMPA receptors for long-term potentiation. J. Biol. Chem. 281 (2006) 752-758 10.1074/jbc.M509677200 Published online November 4, 2005
41. Okamoto K., Nagai T., Miyawaki A., and Hayashi Y. Rapid and persistent modulation of actin dynamics regulates postsynaptic reorganization underlying bidirectional plasticity. Nat. Neurosci. 7 (2004) 1104-1112 10.1038/nn1311 Published online September 7, 2004
42. Park M., Penick E.C., Edwards J.G., Kauer J.A., and Ehlers M.D. Recycling endosomes supply AMPA receptors for LTP. Science 305 (2004) 1972-1975
43. Park M., Salgado J.M., Ostroff L., Helton T.D., Robinson C.G., Harris K.M., and Ehlers M.D. Plasticity-induced growth of dendritic spines by exocytic trafficking from recycling endosomes. Neuron 52 (2006) 817-830
44. 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
45. Petersen J.D., Chen X., Vinade L., Dosemeci A., Lisman J.E., and Reese T.S. Distribution of postsynaptic density (PSD)-95 and Ca2+/calmodulin-dependent protein kinase II at the PSD. J. Neurosci. 23 (2003) 11270-11278
46. Petralia R.S., Wang Y.X., and Wenthold R.J. Internalization at glutamatergic synapses during development. Eur. J. Neurosci. 18 (2003) 3207-3217
47. Pielage J., Fetter R.D., and Davis G.W. A postsynaptic Spectrin scaffold defines active zone size, spacing, and efficacy at the Drosophila neuromuscular junction. J. Cell Biol. 175 (2006) 491-503
48. Plant K., Pelkey K.A., Bortolotto Z.A., Morita D., Terashima A., McBain C.J., Collingridge G.L., and Isaac J.T. Transient incorporation of native GluR2-lacking AMPA receptors during hippocampal long-term potentiation. Nat. Neurosci. 9 (2006) 602-604 10.1038/nn1678 Published online April 2, 2006
49. Qu X., Wu D., Mets L., and Scherer N.F. Nanometer-localized multiple single-molecule fluorescence microscopy. Proc. Natl. Acad. Sci. USA 101 (2004) 11298-11303 10.1073/pnas.0402155101 Published online July 26, 2004
50. Racine V., Sachse M., Salamero J., Fraisier V., Trubuil A., and Sibarita J.-B. Visualization and quantification of vesicle trafficking on a three-dimensional cytoskeleton network in living cells. J. Microsc. 225 (2007) 214-228
51. 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 10.1038/nn1303 Published online Aug 22, 2004
52. Raghavachari S., and Lisman J.E. Properties of quantal transmission at CA1 synapses. J. Neurophysiol. 92 (2004) 2456-2467 10.1152/jn.00258.2004 Published online Apr 28, 2004
53. Richards D.A., De Paola V., Caroni P., Gahwiler B.H., and McKinney R.A. AMPA-receptor activation regulates the diffusion of a membrane marker in parallel with dendritic spine motility in the mouse hippocampus. J. Physiol. 558 (2004) 503-512 10.1113/jphysiol.2004.062091v1 Published online May 28, 2004
54. Shi S., Hayashi Y., Esteban J.A., and Malinow R. Subunit-specific rules governing AMPA receptor trafficking to synapses in hippocampal pyramidal neurons. Cell 105 (2001) 331-343
55. Shi S.H., Hayashi Y., Petralia R.S., Zaman S.H., Wenthold R.J., Svoboda K., and Malinow R. Rapid spine delivery and redistribution of AMPA receptors after synaptic NMDA receptor activation. Science 284 (1999) 1811-1816
56. Shouval H.Z. Clusters of interacting receptors can stabilize synaptic efficacies. Proc. Natl. Acad. Sci. USA 102 (2005) 14440-14445 10.1073/pnas.0506934102 Published online September 27, 2005
57. Smith M.A., Ellis-Davies G.C., and Magee J.C. Mechanism of the distance-dependent scaling of Schaffer collateral synapses in rat CA1 pyramidal neurons. J. Physiol. 548 (2003) 245-258 10.1113/jphysiol.2002.036376 Published online February 21, 2003
58. Sutton M.A., Ito H.T., Cressy P., Kempf C., Woo J.C., and Schuman E.M. Miniature neurotransmission stabilizes synaptic function via tonic suppression of local dendritic protein synthesis. Cell 125 (2006) 785-799
59. Tanaka J., Matsuzaki M., Tarusawa E., Momiyama A., Molnar E., Kasai H., and Shigemoto R. Number and density of AMPA receptors in single synapses in immature cerebellum. J. Neurosci. 25 (2005) 799-807
60. 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
61. Thiagarajan T.C., Lindskog M., and Tsien R.W. Adaptation to synaptic inactivity in hippocampal neurons. Neuron 47 (2005) 725-737
62. Thorne R.G., and Nicholson C. In vivo diffusion analysis with quantum dots and dextrans predicts the width of brain extracellular space. Proc. Natl. Acad. Sci. USA 103 (2006) 5567-5572 10.1073/pnas.0509425103 Published online March 27, 2006
63. Tovar K.R., and Westbrook G.L. Mobile NMDA receptors at hippocampal synapses. Neuron 34 (2002) 255-264
64. Turrigiano G.G., Leslie K.R., Desai N.S., Rutherford L.C., and Nelson S.B. Activity-dependent scaling of quantal amplitude in neocortical neurons. Nature 391 (1998) 892-896
65. Turrigiano G.G., and Nelson S.B. Homeostatic plasticity in the developing nervous system. Nat. Rev. Neurosci. 5 (2004) 97-107
66. Valtschanoff J.G., and Weinberg R.J. Laminar organization of the NMDA receptor complex within the postsynaptic density. J. Neurosci. 21 (2001) 1211-1217
67. Yu C.R., Power J., Barnea G., O'Donnell S., Brown H.E., Osborne J., Axel R., and Gogos J.A. Spontaneous neural activity is required for the establishment and maintenance of the olfactory sensory map. Neuron 42 (2004) 553-566
68. Zamanillo D., Sprengel R., Hvalby O., Jensen V., Burnashev N., Rozov A., Kaiser K.M., Koster H.J., Borchardt T., Worley P., et al. Importance of AMPA receptors for hippocampal synaptic plasticity but not for spatial learning. Science 284 (1999) 1805-1811
69. Zhou Q., Xiao M., and Nicoll R.A. Contribution of cytoskeleton to the internalization of AMPA receptors. Proc. Natl. Acad. Sci. USA 98 (2001) 1261-1266
70. Zhu J.J., Esteban J.A., Hayashi Y., and Malinow R. Postnatal synaptic potentiation: Delivery of GluR4-containing AMPA receptors by spontaneous activity. Nat. Neurosci. 3 (2000) 1098-1106
71. Zona C., Palma E., Brancati A., and Avoli M. Age-dependent appearance of synaptic currents in rat neocortical neurons in culture. Synapse 18 (1994) 1-6