Synaptic activity regulates AMPA receptor trafficking through different recycling pathways

eLife

Volumn 4, Issue MAY, 2015, Pages

  Zheng, Ning ^a   Jeyifous, Okunola ^a,c   Munro, Charlotte ^b   Montgomery, Johanna M ^b,c   Green, William N ^a,c  

^a UNIVERSITY OF CHICAGO   (United States)

^b UNIVERSITY OF AUCKLAND   (New Zealand)

^c MARINE BIOLOGICAL LABORATORY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ADENOSINE DIPHOSPHATE RIBOSYLATION FACTOR 6; AMPA RECEPTOR; COMPLEMENTARY DNA; DYNAMIN; DYNASORE; GLUTAMATE RECEPTOR 1; GUANOSINE TRIPHOSPHATASE; N METHYL DEXTRO ASPARTIC ACID; NERVE GROWTH FACTOR; NEUROPEPTIDE Y; TRANSFERRIN RECEPTOR; ADENOSINE DIPHOSPHATE RIBOSYLATION FACTOR; ADP-RIBOSYLATION FACTOR 6; GLUTAMATE RECEPTOR IONOTROPIC, AMPA 1; PRIMER DNA; RHO GUANINE NUCLEOTIDE BINDING PROTEIN; RHOQ PROTEIN, RAT;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; CONTROLLED STUDY; CORRELATION ANALYSIS; DENDRITE; ENDOCYTOSIS; ENDOPLASMIC RETICULUM; ENDOSOME; EXCITATORY POSTSYNAPTIC POTENTIAL; GENETIC TRANSFECTION; HUMAN; IMAGE ANALYSIS; IMMUNOFLUORESCENCE TEST; IMMUNOHISTOCHEMISTRY; LENTIVIRUS INFECTION; LONG TERM DEPRESSION; LONG TERM POTENTIATION; MICROSCOPY; MOLECULAR CLONING; MUTAGENESIS; NERVE CELL CULTURE; NERVE CELL PLASTICITY; NONHUMAN; POSTSYNAPTIC DENSITY; RAT; REGULATORY MECHANISM; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; SYNAPSE; SYNAPTIC POTENTIAL; SYNAPTIC TRANSMISSION; ANALYSIS OF VARIANCE; ANIMAL; BIOSYNTHESIS; BRAIN; FLUORESCENCE MICROSCOPY; GENETICS; METABOLISM; PATCH CLAMP TECHNIQUE; PHYSIOLOGY; PROTEIN TRANSPORT;

ADP-RIBOSYLATION FACTORS; ANALYSIS OF VARIANCE; ANIMALS; BRAIN; CLONING, MOLECULAR; DNA PRIMERS; DNA, COMPLEMENTARY; ENDOSOMES; LONG-TERM POTENTIATION; MICROSCOPY, FLUORESCENCE; MUTAGENESIS; PATCH-CLAMP TECHNIQUES; PROTEIN TRANSPORT; RATS; RECEPTORS, AMPA; RHO GTP-BINDING PROTEINS; SYNAPSES; TRANSFECTION;

EID: 84930649555     PISSN: None     EISSN: 2050084X     Source Type: Journal    
DOI: 10.7554/eLife.06878     Document Type: Article

References (54)

1. Malinow R, Malenka RC (2002) AMPA RECEPTOR TRAFFICKING AND SYNAPTIC PLASTICITY. pp. 103-126.
2. Pérez-Otaño I, Ehlers MD (2005) Homeostatic plasticity and NMDA receptor trafficking. Trends ends Neurosci 28: 229-238.
3. Ehlers MD (2000) Reinsertion or degradation of AMPA receptors determined by activity-dependent endocytic sorting. Neuron 28: 511-525.
4. Lin JW, Ju W, Foster K, Lee SH, Ahmadian G, et al. (2000) Distinct molecular mechanisms and divergent endocytotic pathways of AMPA receptor internalization. Nat Neurosci 3: 1282-1290.
5. Petrini EM, Lu J, Cognet L, Lounis B, Ehlers MD, et al. (2009) Endocytic Trafficking and Recycling Maintain a Pool of Mobile Surface AMPA Receptors Required for Synaptic Potentiation. Neuron 63: 92-105.
6. Ehlers MD, Heine M, Groc L, Lee MC, Choquet D (2007) Diffusional trapping of GluR1 AMPA receptors by input-specific synaptic activity. Neuron 54: 447-460.
7. Opazo P, Sainlos M, Choquet D (2012) Regulation of AMPA receptor surface diffusion by PSD-95 slots. Curr Opin Neurobiol 22: 453-460.
8. Carroll RC, Beattie EC, Xia H, Luscher C, Altschuler Y, et al. (1999) Dynamin-dependent endocytosis of ionotropic glutamate receptors. Proc Natl Acad Sci U S A 96: 14112-14117.
9. Luscher C, Xia H, Beattie EC, Carroll RC, von Zastrow M, et al. (1999) Role of AMPA receptor cycling in synaptic transmission and plasticity. Neuron 24: 649-658.
10. Park M, Penick EC, Edwards JG, Kauer JA, Ehlers MD (2004) Recycling endosomes supply AMPA receptors for LTP. Science 305: 1972-1975.
11. Park M, Salgado JM, Ostroff L, Helton TD, Robinson CG, et al. (2006) Plasticity-Induced Growth of Dendritic Spines by Exocytic Trafficking from Recycling Endosomes. Neuron 52: 817-830.
12. Ashby MC, Maier SR, Nishimune A, Henley JM (2006) Lateral Diffusion Drives Constitutive Exchange of AMPA Receptors at Dendritic Spines and Is Regulated by Spine Morphology. J Neurosci 26: 7046-7055.
13. Yudowski GA, Puthenveedu MA, Leonoudakis D, Panicker S, Thorn KS, et al. (2007) Real-Time Imaging of Discrete Exocytic Events Mediating Surface Delivery of AMPA Receptors. J Neurosci 27: 11112-11121.
14. Tao-Cheng JH, Crocker VT, Winters CA, Azzam R, Chludzinski J, et al. (2011) Trafficking of AMPA receptors at plasma membranes of hippocampal neurons. J Neurosci 31: 4834-4843.
15. Malinow R, Malenka RC (2002) AMPA receptor trafficking and synaptic plasticity. Annu Rev Neurosci 25: 103-126.
16. Mohanasundaram P, Shanmugam MM (2010) Role of syntaxin 4 in activity-dependent exocytosis and synaptic plasticity in hippocampal neurons. Sci Signal 3: jc7.
17. 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.
18. Fernandez-Monreal M, Brown TC, Royo M, Esteban JA (2012) The balance between receptor recycling and trafficking toward lysosomes determines synaptic strength during long-term depression. The Journal of neuroscience: the official journal of the Society for Neuroscience 32: 13200-13205.
19. Park M, Salgado JM, Ostroff L, Helton TD, Robinson CG, et al. (2006) Plasticity-induced growth of dendritic spines by exocytic trafficking from recycling endosomes. Neuron 52: 817-830.
20. Laurent G, Daniel C (2006) AMPA and NMDA glutamate receptor trafficking: multiple roads for reaching and leaving the synapse. Cell and Tissue Research V326: 423-438.
21. 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.
22. Scholz R, Berberich S, Rathgeber L, Kolleker A, Kohr G, et al. (2010) AMPA receptor signaling through BRAG2 and Arf6 critical for long-term synaptic depression. Neuron 66: 768-780.
23. Arendt KL, Royo M, Fernandez-Monreal M, Knafo S, Petrok CN, et al. (2010) PIP3 controls synaptic function by maintaining AMPA receptor clustering at the postsynaptic membrane. Nature neuroscience 13: 36-44.
24. Tomita S, Fukata M, Nicoll RA, Bredt DS (2004) Dynamic interaction of stargazin-like TARPs with cycling AMPA receptors at synapses. Science 303: 1508-1511.
25. Neudauer CL, Joberty G, Tatsis N, Macara IG (1998) Distinct cellular effects and interactions of the Rho-family GTPase TC10. Current biology: CB 8: 1151-1160.
26. Cuadra AE, Kuo SH, Kawasaki Y, Bredt DS, Chetkovich DM (2004) AMPA receptor synaptic targeting regulated by stargazin interactions with the Golgi-resident PDZ protein nPIST. J Neurosci 24: 7491-7502.
27. Kawase K, Nakamura T, Takaya A, Aoki K, Namikawa K, et al. (2006) GTP hydrolysis by the Rho family GTPase TC10 promotes exocytic vesicle fusion. Dev Cell 11: 411-421.
28. Fujita A, Koinuma S, Yasuda S, Nagai H, Kamiguchi H, et al. (2013) GTP hydrolysis of TC10 promotes neurite outgrowth through exocytic fusion of Rab11- and L1-containing vesicles by releasing exocyst component Exo70. PLoS One 8: e79689.
29. Jeyifous O, Waites CL, Specht CG, Fujisawa S, Schubert M, et al. (2009) SAP97 and CASK mediate sorting of NMDA receptors through a previously unknown secretory pathway. Nat Neurosci 12: 1011-1019.
30. Greger IH, Khatri L, Ziff EB (2002) RNA Editing at Arg607 Controls AMPA Receptor Exit from the Endoplasmic Reticulum. Neuron 34: 759-772.
31. Newpher TM, Ehlers MD (2008) Glutamate Receptor Dynamics in Dendritic Microdomains. Neuron 58: 472-497.
32. Doherty GJ, McMahon HT (2009) Mechanisms of endocytosis. Annual review of biochemistry 78: 857-902.
33. Lavezzari G, Roche KW (2007) Constitutive endocytosis of the metabotropic glutamate receptor mGluR7 is clathrin-independent. Neuropharmacology 52: 100-107.
34. Gong Q, Weide M, Huntsman C, Xu Z, Jan LY, et al. (2007) Identification and characterization of a new class of trafficking motifs for controlling clathrin-independent internalization and recycling. J Biol Chem 282: 13087-13097.
35. Donaldson JG, Porat-Shliom N, Cohen LA (2009) Clathrin-independent endocytosis: a unique platform for cell signaling and PM remodeling. Cell Signal 21: 1-6.
36. Montgomery JM, Madison DV (2002) State-dependent heterogeneity in synaptic depression between pyramidal cell pairs. Neuron 33: 765-777.
37. Montgomery JM, Selcher JC, Hanson JE, Madison DV (2005) Dynamin-dependent NMDAR endocytosis during LTD and its dependence on synaptic state. BMC neuroscience 6: 48.
38. Shi SH, Hayashi Y, Petralia RS, Zaman SH, Wenthold RJ, et al. (1999) Rapid spine delivery and redistribution of AMPA receptors after synaptic NMDA receptor activation. Science 284: 1811-1816.
39. Li D, Specht CG, Waites CL, Butler-Munro C, Leal-Ortiz S, et al. (2011) SAP97 directs NMDA receptor spine targeting and synaptic plasticity. The Journal of physiology 589: 4491-4510.
40. Fourgeaud L, Bessis AS, Rossignol F, Pin JP, Olivo-Marin JC, et al. (2003) The metabotropic glutamate receptor mGluR5 is endocytosed by a clathrin-independent pathway. J Biol Chem 278: 12222-12230.
41. Glodowski DR, Chen CC-H, Schaefer H, Grant BD, Rongo C (2007) RAB-10 Regulates Glutamate Receptor Recycling in a Cholesterol-dependent Endocytosis Pathway. Mol Biol Cell 18: 4387-4396.
42. Petralia RS, Wang YX, Wenthold RJ (2003) Internalization at glutamatergic synapses during development. Eur J Neurosci 18: 3207-3217.
43. Racz B, Blanpied TA, Ehlers MD, Weinberg RJ (2004) Lateral organization of endocytic machinery in dendritic spines. Nature neuroscience 7: 917-918.
44. Lu J, Helton TD, Blanpied TA, Racz B, Newpher TM, et al. (2007) Postsynaptic positioning of endocytic zones and AMPA receptor cycling by physical coupling of dynamin-3 to Homer. Neuron 55: 874-889.
45. Kennedy MJ, Davison IG, Robinson CG, Ehlers MD (2010) Syntaxin-4 defines a domain for activity-dependent exocytosis in dendritic spines. Cell 141: 524-535.
46. Chen A, Gossling EK, Witkowski L, Bhindi A, Bauch C, et al. (2012) Regional and subcellular distribution of the receptor-targeting protein PIST in the rat central nervous system. The Journal of comparative neurology 520: 889-913.
47. Ahmad M, Polepalli JS, Goswami D, Yang X, Kaeser-Woo YJ, et al. (2012) Postsynaptic complexin controls AMPA receptor exocytosis during LTP. Neuron 73: 260-267.
48. Scarselli M, Donaldson JG (2009) Constitutive internalization of G protein-coupled receptors and G proteins via clathrin-independent endocytosis. J Biol Chem 284: 3577-3585.
49. Arjonen A, Alanko J, Veltel S, Ivaska J (2012) Distinct recycling of active and inactive beta1 integrins. Traffic 13: 610-625.
50. Bredt DS, Nicoll RA (2003) AMPA receptor trafficking at excitatory synapses. Neuron 40: 361-379.
51. Collingridge GL, Isaac JT, Wang YT (2004) Receptor trafficking and synaptic plasticity. Nature reviews Neuroscience 5: 952-962.
52. Shepherd JD, Huganir RL (2007) The cell biology of synaptic plasticity: AMPA receptor trafficking. Annual review of cell and developmental biology 23: 613-643.
53. Yap CC, Winckler B (2012) Harnessing the power of the endosome to regulate neural development. Neuron 74: 440-451.
54. Cooney JR, Hurlburt JL, Selig DK, Harris KM, Fiala JC (2002) Endosomal compartments serve multiple hippocampal dendritic spines from a widespread rather than a local store of recycling membrane. The Journal of neuroscience: the official journal of the Society for Neuroscience 22: 2215-2224.