Lateral diffusion drives constitutive exchange of AMPA receptors at dendritic spines and is regulated by spine morphology

Journal of Neuroscience

Volumn 26, Issue 26, 2006, Pages 7046-7055

  Ashby, Michael C ^a,b   Maier, Susie R ^a   Nishimune, Atsushi ^a   Henley, Jeremy M ^a  

^a UNIVERSITY OF BRISTOL   (United Kingdom)

^b NATIONAL INSTITUTE OF NEUROLOGICAL DISORDERS AND STROKE   (United States)

Author keywords

AMPA receptor; Lateral diffusion; pHluorin; Photobleaching; Synapse specificity; Trafficking

Indexed keywords

AMPA RECEPTOR; MEMBRANE PROTEIN; GLUTAMATE RECEPTOR IONOTROPIC, AMPA 2; GREEN FLUORESCENT PROTEIN; PHLUORIN;

ANIMAL CELL; ANIMAL TISSUE; ARTICLE; CELL SPECIFICITY; DENDRITIC SPINE; DIFFUSION; HIPPOCAMPUS; MORPHOLOGY; NERVE CELL PLASTICITY; NONHUMAN; POSTSYNAPTIC MEMBRANE; PRIORITY JOURNAL; PROTEIN DETERMINATION; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN LOCALIZATION; PROTEIN TRANSPORT; RAT; SIGNAL TRANSDUCTION; SYNAPSE; ANIMAL; BLEACHING; CELL CULTURE; CELL MEMBRANE; METABOLISM; NERVE CELL; TISSUE DISTRIBUTION; TRANSPORT AT THE CELLULAR LEVEL; ULTRASTRUCTURE;

ANIMALS; BIOLOGICAL TRANSPORT; CELL MEMBRANE; CELLS, CULTURED; DENDRITIC SPINES; DIFFUSION; GREEN FLUORESCENT PROTEINS; NEURONS; PHOTOBLEACHING; PROTEIN TRANSPORT; RATS; RECEPTORS, AMPA; TISSUE DISTRIBUTION;

EID: 33745965151     PISSN: 02706474     EISSN: 02706474     Source Type: Journal    
DOI: 10.1523/JNEUROSCI.1235-06.2006     Document Type: Article

References (48)

1. Adesnik H, Nicoll RA, England PM (2005) Photoinactivation of native AMPA receptors reveals their real-time trafficking. Neuron 48:977-985.
2. Ashby MC, Ibaraki K, Henley JM (2004a) It's green outside: tracking cell surface proteins with pH-sensitive GFP. Trends Neurosci 27:257-261.
3. Ashby MC, De La Rue SA, Ralph GS, Uney J, Collingridge GL, Henley JM (2004b) Removal of AMPA receptors (AMPARs) from synapses is preceded by transient endocytosis of extrasynaptic AMPARs. J Neurosci 24:5172-5176.
4. Axelrod D, Koppel DE, Schlessinger J, Elson E, Webb WW (1976) Mobility measurement by analysis of fluorescence photobleaching recovery kinetics. Biophys J 16:1055-1069.
5. Blanpied TA, Scott DB, Ehlers MD (2002) Dynamics and regulation of clathrin coats at specialized endocytic zones of dendrites and spines. Neuron 36:435-449.
6. Bloodgood BL, Sabatini BL (2005) Neuronal activity regulates diffusion across the neck of dendritic spines. Science 310:866-869.
7. Borgdorff AJ, Choquet D (2002) Regulation of AMPA receptor lateral movements. Nature 417:649-653.
8. Choquet D, Triller A (2003) The role of receptor diffusion in the organization of the postsynaptic membrane. Nat Rev Neurosci 4:251-265.
9. Collingridge GL, Isaac JT, Wang YT (2004) Receptor trafficking and synaptic plasticity. Nat Rev Neurosci 5:952-962.
10. Ehlers MD (2000) Reinsertion or degradation of AMPA receptors determined by activity-dependent endocytic sorting. Neuron 28:511-525.
11. Feder TJ, Brust-Mascher I, Slattery JP, Baird B, Webb WW (1996) Constrained diffusion or immobile fraction on cell surfaces: a new interpretation. Biophys J 70:2767-2773.
12. Gardner SM, Takamiya K, Xia J, Suh JG, Johnson R, Yu S, Huganir RL (2005) Calcium-permeable AMPA receptor plasticity is mediated by subunit-specific interactions with PICK1 and NSF. Neuron 45:903-915.
13. Gray EG (1959) Electron microscopy of synaptic contacts on dendrite spines of the cerebral cortex. Nature 183:1592-1593.
14. Groc L, Heine M, Cognet L, Brickley K, Stephenson FA, Lounis B, Choquet D (2004) Differential activity-dependent regulation of the lateral mobilities of AMPA and NMDA receptors. Nat Neurosci 7:695-696.
15. Hering H, Lin CC, Sheng M (2003) Lipid rafts in the maintenance of synapses, dendritic spines, and surface AMPA receptor stability. J Neurosci 23:3262-3271.
16. Kopec CD, Li B, Wei W, Boehm J, Malinow R (2006) Glutamate receptor exocytosis and spine enlargement during chemically induced long-term potentiation. J Neurosci 26:2000-2009.
17. Lee HK, Barbarosie M, Kameyama K, Bear MF, Huganir RL (2000) Regulation of distinct AMPA receptor phosphorylation sites during bidirectional synaptic plasticity. Nature 405:955-959.
18. Lee SH, Liu L, Wang YT, Sheng M (2002) Clathrin adaptor AP2 and NSF interact with overlapping sites of GluR2 and play distinct roles in AMPA receptor trafficking and hippocampal LTD. Neuron 36:661-674.
19. Lledo PM, Zhang X, Sudhof TC, Malenka RC, Nicoll RA (1998) Postsynaptic membrane fusion and long-term potentiation. Science 279:399-403.
20. Luscher C, Xia H, Beattie EC, Carroll RC, von Zastrow M, Malenka RC, Nicoll RA (1999) Role of AMPA receptor cycling in synaptic transmission and plasticity. Neuron 24:649-658.
21. Malinow R, Malenka RC (2002) AMPA receptor trafficking and synaptic plasticity. Annu Rev Neurosci 25:103-126.
22. Mammen AL, Huganir RL, O'Brien RJ (1997) Redistribution and stabilization of cell surface glutamate receptors during synapse formation. J Neurosci 17:7351-7358.
23. Martin S, Henley JM (2004) Activity-dependent endocytic sorting of kainate receptors to recycling or degradation pathways. EMBO J 23:4749-4759.
24. Matsuzaki M, Honkura N, Ellis-Davies GC, Kasai H (2004) Structural basis of long-term potentiation in single dendritic spines. Nature 429:761-766.
25. Mitchell SJ, Ryan TA (2004) Syntaxin-1A is excluded from recycling synaptic vesicles at nerve terminals. J Neurosci 24:4884-4888.
26. Moriyoshi K, Richards LJ, Akazawa C, O'Leary DD, Nakanishi S (1996) Labeling neural cells using adenoviral gene transfer of membrane-targeted GFP. Neuron 16:255-260.
27. Nagerl UV, Eberhorn N, Cambridge SB, Bonhoeffer T (2004) Bidirectional activity-dependent morphological plasticity in hippocampal neurons. Neuron 44:759-767.
28. Nimchinsky EA, Sabatini BL, Svoboda K (2002) Structure and function of dendritic spines. Annu Rev Physiol 64:313-353.
29. Nishimune A, Isaac JT, Molnar E, Noel J, Nash SR, Tagaya M, Collingridge GL, Nakanishi S, Henley JM (1998) NSF binding to GluR2 regulates synaptic transmission. Neuron 21:87-97.
30. Noel J, Ralph GS, Pickard L, Williams J, Molnar E, Uney JB, Collingridge GL, Henley JM (1999) Surface expression of AMPA receptors in hippocampal neurons is regulated by an NSF-dependent mechanism. Neuron 23:365-376.
31. Park M, Penick EC, Edwards JG, Kauer JA, Ehlers MD (2004) Recycling endosomes supply AMPA receptors for LTP. Science 305:1972-1975.
32. Passafaro M, Piech V, Sheng M (2001) Subunit-specific temporal and spatial patterns of AMPA receptor exocytosis in hippocampal neurons. Nat Neurosci 4:917-926.
33. Petralia RS, Wang YX, Wenthold RJ (2003) Internalization at glutamatergic synapses during development. Eur J Neurosci 18:3207-3217.
34. Pickard L, Noel J, Duckworth JK, Fitzjohn SM, Henley JM, Collingridge GL, Molnar E (2001) Transient synaptic activation of NMDA receptors leads to the insertion of native AMPA receptors at hippocampal neuronal plasma membranes. Neuropharmacology 41:700-713.
35. Racz B, Blanpied TA, Ehlers MD, Weinberg RJ (2004) Lateral organization of endocytic machinery in dendritic spines. Nat Neurosci 7:917-918.
36. Reits EA, Neefjes JJ (2001) From fixed to FRAP: measuring protein mobility and activity in living cells. Nat Cell Biol 3:E145-E147.
37. Richards DA, De Paola V, Caroni P, Gahwiler BH, McKinney RA (2004) AMPA-receptor activation regulates the diffusion of a membrane marker in parallel with dendritic spine motility in the mouse hippocampus. J Physiol (Lond) 558:503-512.
38. Sankaranarayanan S, De Angelis D, Rothman JE, Ryan TA (2000) The use of pHluorins for optical measurements of presynaptic activity. Biophys J 79:2199-2208.
39. Sheng M (2001) Molecular organization of the postsynaptic specialization. Proc Natl Acad Sci USA 98:7058-7061.
40. Shi S, Hayashi Y, Esteban JA, Malinow R (2001) Subunit-specific rules governing AMPA receptor trafficking to synapses in hippocampal pyramidal neurons. Cell 105:331-343.
41. Svoboda K, Tank DW, Denk W (1996) Direct measurement of coupling between dendritic spines and shafts. Science 272:716-719.
42. Tardin C, Cognet L, Bats C, Lounis B, Choquet D (2003) Direct imaging of lateral movements of AMPA receptors inside synapses. EMBO J 22:4656-4665.
43. Tashiro A, Yuste R (2003) Structure and molecular organization of dendritic spines. Histol Histopathol 18:617-634.
44. Triller A, Choquet D (2005) Surface trafficking of receptors between synaptic and extrasynaptic membranes: and yet they do move! Trends Neurosci 28:133-139.
45. Washbourne P, Bennett JE, McAllister AK (2002) Rapid recruitment of NMDA receptor transport packets to nascent synapses. Nat Neurosci 5:751-759.
46. Wenthold RJ, Petralia RS, Blahos J, II, Niedzielski AS (1996) Evidence for multiple AMPA receptor complexes in hippocampal CA1/CA2 neurons. J Neurosci 16:1982-1989.
47. Yuste R, Majewska A, Holthoff K (2000) From form to function: calcium compartmentalization in dendritic spines. Nat Neurosci 3:653-659.
48. Zhou Q, Homma KJ, Poo MM (2004) Shrinkage of dendritic spines associated with long-term depression of hippocampal synapses. Neuron 44: 749-757.