Brownian diffusion of AMPA receptors is sufficient to explain fast onset of LTP

BMC Systems Biology

Volumn 4, Issue , 2010, Pages

  Tolle, Dominic P ^a   Le Novère, Nicolas ^a  

^a WELLCOME TRUST SANGER INSTITUTE   (United Kingdom)

Author keywords

[No Author keywords available]

Indexed keywords

AMPA RECEPTOR;

ACTION POTENTIAL; ANIMAL; ARTICLE; BIOLOGICAL MODEL; CHEMISTRY; COMPUTER SIMULATION; DIFFUSION; HUMAN; LONG TERM POTENTIATION; METABOLISM; NERVE CELL; PHYSIOLOGY;

ACTION POTENTIALS; ANIMALS; COMPUTER SIMULATION; DIFFUSION; HUMANS; LONG-TERM POTENTIATION; MODELS, NEUROLOGICAL; NEURONS; RECEPTORS, AMPA;

EID: 77951888099     PISSN: None     EISSN: 17520509     Source Type: Journal    
DOI: 10.1186/1752-0509-4-25     Document Type: Article

References (55)

1. Nusser Z. AMPA and NMDA receptors: similarities and differences in their synaptic distribution. Curr Opin Neurobiol 2000, 10(3):337-341. 10.1016/S0959-4388(00)00086-6, 10851167.
2. Borgdorff AJ, Choquet D. Regulation of AMPA receptor lateral movements. Nature 2002, 417(6889):649-653. 10.1038/nature00780, 12050666.
3. Shi S, Hayashi Y, Esteban JA, Malinow R. Subunit-specific rules governing AMPA receptor trafficking to synapses in hippocampal pyramidal neurons. Cell 2001, 105(3):331-343. 10.1016/S0092-8674(01)00321-X, 11348590.
4. Passafaro M, Piëch V, Sheng M. Subunit-specific temporal and spatial patterns of AMPA receptor exocytosis in hippocampal neurons. Nat Neurosci 2001, 4(9):917-926. 10.1038/nn0901-917, 11528423.
5. Choquet D, Triller A. The role of receptor diffusion in the organization of the postsynaptic membrane. Nat Rev Neurosci 2003, 4:251-265. 10.1038/nrn1077, 12671642.
6. Sheng M, Kim MJ. Postsynaptic signaling and plasticity mechanisms. Science 2002, 298:776-780. 10.1126/science.1075333, 12399578.
7. Lisman J. Long-term potentiation: outstanding questions and attempted synthesis. Philos Trans R Soc Lond B Biol Sci 2003, 358(1432):829-842. 10.1098/rstb.2002.1242, 1693147, 12740130.
8. Benke TA, Lüthi A, Isaac JT, Collingridge GL. Modulation of AMPA receptor unitary conductance by synaptic activity. Nature 1998, 393(6687):793-797. 10.1038/31709, 9655394.
9. Derkach V, Barria A, Soderling TR. Ca2+/calmodulin-kinase II enhances channel conductance of alpha-amino-3-hydroxy-5-methyl-4-isoxazolepropionate type glutamate receptors. Proc Natl Acad Sci USA 1999, 96(6):3269-3274. 10.1073/pnas.96.6.3269, 15931, 10077673.
10. Shi SH, Hayashi Y, Petralia RS, Zaman SH, Wenthold RJ, Svoboda K, Malinow R. Rapid spine delivery and redistribution of AMPA receptors after synaptic NMDA receptor activation. Science 1999, 284(5421):1811-1816. 10.1126/science.284.5421.1811, 10364548.
11. Hayashi Y, Shi SH, Esteban JA, Piccini A, Poncer JC, Malinow R. Driving AMPA receptors into synapses by LTP and CaMKII: requirement for GluR1 and PDZ domain interaction. Science 2000, 287(5461):2262-2267. 10.1126/science.287.5461.2262, 10731148.
12. Pickard L, Noël J, Duckworth JK, Fitzjohn SM, Henley JM, Collingridge GL, Molnar E. Transient synaptic activation of NMDA receptors leads to the insertion of native AMPA receptors at hippocampal neuronal plasma membranes. Neuropharmacology 2001, 41(6):700-713. 10.1016/S0028-3908(01)00127-7, 11640924.
13. Petersen CC, Malenka RC, Nicoll RA, Hopfield JJ. All-or-none potentiation at CA3-CA1 synapses. Proc Natl Acad Sci USA 1998, 95(8):4732-4737. 10.1073/pnas.95.8.4732, 22559, 9539807.
14. Raghavachari S, Lisman JE. Properties of quantal transmission at CA1 synapses. J Neurophysiol 2004, 92(4):2456-2467. 10.1152/jn.00258.2004, 15115789.
15. Adesnik H, Nicoll RA, England PM. Photoinactivation of native AMPA receptors reveals their real-time trafficking. Neuron 2005, 48(6):977-985. 10.1016/j.neuron.2005.11.030, 16364901.
16. Yudowski GA, Puthenveedu MA, Leonoudakis D, Panicker S, Thorn KS, Beattie EC, von Zastrow M. Real-time imaging of discrete exocytic events mediating surface delivery of AMPA receptors. J Neurosci 2007, 27(41):11112-11121. 10.1523/JNEUROSCI.2465-07.2007, 17928453.
17. Makino H, Malinov R. AMPA receptor incorporation into synapses during LTP: the role of lateral movement and exocytosis. Neuron 2009, 64:381-390. 10.1016/j.neuron.2009.08.035, 19914186.
18. Triller A, Choquet D. Surface trafficking of receptors between synaptic and extrasynaptic membranes: and yet they do move!. Trends Neurosci 2005, 28(3):133-139. 10.1016/j.tins.2005.01.001, 15749166.
19. Tanaka J, Matsuzaki M, Tarusawa E, Momiyama A, Molnar E, Kasai H, Shigemoto R. Number and density of AMPA receptors in single synapses in immature cerebellum. J Neurosci 2005, 25(4):799-807. 10.1523/JNEUROSCI.4256-04.2005, 15673659.
20. Ehlers MD, Heine M, Groc L, Lee MC, Choquet D. Diffusional trapping of GluR1 AMPA receptors by input-specific synaptic activity. Neuron 2007, 54(3):447-460. 10.1016/j.neuron.2007.04.010, 1993808, 17481397.
21. Earnshaw BA, Bressloff PC. Biophysical model of AMPA receptor trafficking and its regulation during long-term potentiation/long-term depression. J Neurosci 2006, 26(47):12362-12373. 10.1523/JNEUROSCI.3601-06.2006, 17122061.
22. Bressloff PC, Earnshaw BA. Diffusion-trapping model of receptor trafficking in dendrites. Phys Rev E Stat Nonlin Soft Matter Phys 2007, 75(4 Pt 1):041915.
23. Holcman D, Triller A. Modeling synaptic dynamics driven by receptor lateral diffusion. Biophys J 2006, 91(7):2405-2415. 10.1529/biophysj.106.081935, 1562376, 16844759.
24. Renner ML, Cognet L, Lounis B, Triller A, Choquet D. The excitatory postsynaptic density is a size exclusion diffusion environment. Neuropharmacology 2008, 56(1):30-6. 10.1016/j.neuropharm.2008.07.022, 18694768.
25. Goldman J, Andrews S, Bray D. Size and composition of membrane protein clusters predicted by Monte Carlo analysis. Eur Biophys J 2004, 33(6):506-512. 10.1007/s00249-004-0391-6, 14997356.
26. English TJ, Hammer DA. The Effect of Cellular Receptor Diffusion on Receptor-Mediated Viral Binding Using Brownian Adhesive Dynamics (BRAD) Simulations. Biophys J 2005, 88:1666-1675. 10.1529/biophysj.104.047043, 1305223, 15556985.
27. Goddard NH, Hucka M, Howell F, Cornelis H, Shankar K, Beeman D. Towards NeuroML: model description methods for collaborative modelling in neuroscience. Philos Trans R Soc Lond B Biol Sci 2001, 356(1412):1209-1228. 10.1098/rstb.2001.0910, 1088511, 11545699.
28. Tardin C, Cognet L, Bats C, Lounis B, Choquet D. Direct imaging of lateral movements of AMPA receptors inside synapses. EMBO J 2003, 22(18):4656-4665. 10.1093/emboj/cdg463, 212729, 12970178.
29. Andrews SS, Bray D. Stochastic simulation of chemical reactions with spatial resolution and single molecule detail. Phys Biol 2004, 1(3-4):137-151. 10.1088/1478-3967/1/3/001, 16204833.
30. Saffman PG, Delbrück M. Brownian motion in biological membranes. Proc Natl Acad Sci USA 1975, 72(8):3111-3113. 10.1073/pnas.72.8.3111, 432930, 1059096.
31. Barry MF, Ziff EB. Receptor trafficking and the plasticity of excitatory synapses. Curr Opin Neurobiol 2002, 12(3):279-286. 10.1016/S0959-4388(02)00329-X, 12049934.
32. Collingridge GL, Isaac JT, Wang YT. Receptor trafficking and synaptic plasticity. Nat Rev Neurosci 2004, 5:952-962. 10.1038/nrn1556, 15550950.
33. Sheng M, Hoogenraad CC. The postsynaptic architecture of excitatory synapses: a more quantitative view. Annu Rev Biochem 2007, 76:823-847. 10.1146/annurev.biochem.76.060805.160029, 17243894.
34. Nusser Z, Mulvihill E, Streit P, Somogyi P. Subsynaptic segregation of metabotropic and ionotropic glutamate receptors as revealed by immunogold localization. Neuroscience 1994, 61(3):421-427. 10.1016/0306-4522(94)90421-9, 7969918.
35. Kharazia VN, Weinberg RJ. Tangential synaptic distribution of NMDA and AMPA receptors in rat neocortex. Neurosci Lett 1997, 238(1-2):41-44. 10.1016/S0304-3940(97)00846-X, 9464650.
36. Masugi-Tokita M, Tarusawa E, Watanabe M, Molnár E, Fujimoto K, Shigemoto R. Number and density of AMPA receptors in individual synapses in the rat cerebellum as revealed by SDS-digested freeze-fracture replica labeling. J Neurosci 2007, 27(8):2135-2144. 10.1523/JNEUROSCI.2861-06.2007, 17314308.
37. Jonas P, Major G, Sakmann B. Quantal components of unitary EPSCs at the mossy fibre synapse on CA3 pyramidal cells of rat hippocampus. J Physiol 1993, 472:615-663. 1160505, 7908327.
38. Wahl LM, Pouzat C, Stratford KJ. Monte Carlo simulation of fast excitatory synaptic transmission at a hippocampal synapse. J Neurophysiol 1996, 75(2):597-608.
39. Riveros N, Fiedler J, Lagos N, Muñoz C, Orrego F. Glutamate in rat brain cortex synaptic vesicles: influence of the vesicle isolation procedure. Brain Res 1986, 386(1-2):405-408. 10.1016/0006-8993(86)90181-2, 2877717.
40. Magee JC, Cook EP. Somatic EPSP amplitude is independent of synapse location in hippocampal pyramidal neurons. Nat Neurosci 2000, 3(9):895-903. 10.1038/78800, 10966620.
41. Riley M, Buettner H, Muzzio F, Reyes S. Monte Carlo simulation of diffusion and reaction in two-dimensional cell structures. Biophys J 1995, 68(5):1716-26. 10.1016/S0006-3495(95)80349-8, 1282075, 7612815.
42. Malinow R, Malenka RC. AMPA receptor trafficking and synaptic plasticity. Annu Rev Neurosci 2002, 25:103-126. 10.1146/annurev.neuro.25.112701.142758, 12052905.
43. Elias GM, Nicoll RA. Synaptic trafficking of glutamate receptors by MAGUK scaffolding proteins. Trends Cell Biol 2007, 17(7):343-352. 10.1016/j.tcb.2007.07.005, 17644382.
44. Bats C, Groc L, Choquet D. The interaction between Stargazin and PSD-95 regulates AMPA receptor surface trafficking. Neuron 2007, 53(5):719-734. 10.1016/j.neuron.2007.01.030, 17329211.
45. Smoluchowski M. Versuch einer mathematischen Theorie der Koagulationskinetik kolloider Lösungen. Zeitschrift für physikalische Chemie 1916, XCII:129-168.
46. Hering H, Lin CC, Sheng M. Lipid rafts in the maintenance of synapses, dendritic spines, and surface AMPA receptor stability. J Neurosci 2003, 23(8):3262-3271.
47. Franks KM, Stevens CF, Sejnowski TJ. Independent sources of quantal variability at single glutamatergic synapses. J Neurosci 2003, 23(8):3186-3195.
48. Kusumi A, Sako Y, 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 1993, 65(5):2021-2040. 10.1016/S0006-3495(93)81253-0, 1225938, 8298032.
49. Lledo PM, Zhang X, Südhof TC, Malenka RC, Nicoll RA. Postsynaptic membrane fusion and long-term potentiation. Science 1998, 279(5349):399-403. 10.1126/science.279.5349.399, 9430593.
50. Ashby MC, Maier SR, Nishimune A, Henley JM. Lateral diffusion drives constitutive exchange of AMPA receptors at dendritic spines and is regulated by spine morphology. J Neurosci 2006, 26(26):7046-7055. 10.1523/JNEUROSCI.1235-06.2006, 16807334.
51. Correia SS, Bassani S, Brown TC, Lisé MF, Backos DS, El-Husseini A, Passafaro M, Esteban JA. Motor protein-dependent transport of AMPA receptors into spines during long-term potentiation. Nat Neurosci 2008, 11(4):457-466. 10.1038/nn2063, 18311135.
52. Harris KM, Kater SB. Dendritic spines: cellular specializations imparting both stability and flexibility to synaptic function. Annu Rev Neurosci 1994, 17:341-371. 10.1146/annurev.ne.17.030194.002013, 8210179.
53. Nusser Z, Lujan R, Laube G, Roberts JD, Molnar E, Somogyi P. Cell type and pathway dependence of synaptic AMPA receptor number and variability in the hippocampus. Neuron 1998, 21(3):545-559. 10.1016/S0896-6273(00)80565-6, 9768841.
54. Franks KM, Bartol TM, Sejnowski TJ. A Monte Carlo model reveals independent signaling at central glutamatergic synapses. Biophys J 2002, 83(5):2333-2348. 10.1016/S0006-3495(02)75248-X, 1302323, 12414671.
55. Chicurel ME, Harris KM. Three-dimensional analysis of the structure and composition of CA3 branched dendritic spines and their synaptic relationships with mossy fiber boutons in the rat hippocampus. J Comp Neurol 1992, 325(2):169-182. 10.1002/cne.903250204, 1460112.