Internalization at glutamatergic synapses during development

European Journal of Neuroscience

Volumn 18, Issue 12, 2003, Pages 3207-3217

  Petralia, Ronald S ^a   Wang, Ya Xian ^a   Wenthold, Robert J ^a  

^a NATIONAL INSTITUTE ON DEAFNESS AND OTHER COMMUNICATION DISORDERS   (United States)

Author keywords

AMPA; Caveolin; Clathrin; NMDA; Rat

Indexed keywords

ALPHA AMINO 3 HYDROXY 5 METHYL 4 ISOXAZOLEPROPIONIC ACID; CAVEOLIN; CLATHRIN; GLUTAMATE RECEPTOR; GLUTAMIC ACID; N METHYL DEXTRO ASPARTIC ACID;

ANIMAL CELL; ANIMAL TISSUE; ARTICLE; BRAIN; CELL MEMBRANE; COATED VESICLE; CONTROLLED STUDY; HIPPOCAMPUS; IMMUNOGOLD LABELING; IMMUNOLOCALIZATION; IN VITRO STUDY; IN VIVO STUDY; INTERNALIZATION; NONHUMAN; PRIORITY JOURNAL; PROTEIN LOCALIZATION; PROTEIN STABILITY; RAT; SPINE; SYNAPSE;

ANIMALS; ANIMALS, NEWBORN; CAVEOLIN 1; CAVEOLINS; CELL DIFFERENTIATION; CELLS, CULTURED; CLATHRIN-COATED VESICLES; DENDRITES; ENDOCYTOSIS; FETUS; GLUTAMIC ACID; HIPPOCAMPUS; IMMUNOHISTOCHEMISTRY; MICROSCOPY, ELECTRON; PRESYNAPTIC TERMINALS; RATS; RATS, SPRAGUE-DAWLEY; RECEPTORS, AMPA; RECEPTORS, N-METHYL-D-ASPARTATE; SYNAPSES; SYNAPTIC MEMBRANES;

EID: 0346158326     PISSN: 0953816X     EISSN: None     Source Type: Journal    
DOI: 10.1111/j.1460-9568.2003.03074.x     Document Type: Article

References (62)

1. Altman, J. (1971) Coated vesicles and synaptogenesis. A developmental study in the cerebellar cortex of the rat. Brain Res., 30, 311-322.
2. Benke, T.A., Jones, O.T., Collingridge, G.L. & Angelides, K.J. (1993) N-methyl-D-aspartate receptors are clustered and immobilized on dendrites of living cortical neurons. Proc. Natl. Acad. Sci. USA, 90, 7819-7823.
3. Blanpied, T.A., Scott, D.B. & Ehlers, M.D. (2002) Dynamics and regulation of clathrin coats at specialized endocytic zones of dendrites and spines. Neuron, 36, 435-449.
4. Borgdorff, A.J. & Choquet, D. (2002) Regulation of AMPA receptor lateral movements. Nature, 417, 649-653.
5. Braun, J.E. & Madison, D.V. (2000) A novel SNAP25-caveolin complex correlates with the onset of persistent synaptic potentiation. J. Neurosci., 20, 5997-6006.
6. Brodin, L., Löw, P. & Shupliakov, O. (2000) Sequential steps in clathrin-mediated synaptic vesicle endocytosis. Curr. Opin. Neurobiol., 10, 312-320.
7. Bu, J., Bruckner, S.R., Sengoku, T., Geddes, J.W. & Estus, S. (2003) Glutamate regulates caveolin expression in rat hippocampal neurons. J. Neurosci. Res., 72, 185-190.
8. Burbea, M., Dreier, L., Dittman, J.S., Grunwald, M.E. & Kaplan, J.M. (2002) Ubiquitin and AP180 regulate the abundance of GLR-1 glutamate receptors at postsynaptic elements in C. elegans. Neuron, 35, 107-120.
9. Carroll, R.C., Beattie, E.G., von Zastrow, M. & Malenka, R.C. (2001) Role of AMPA receptor endocytosis in synaptic plasticity. Nat. Rev. Neurosci., 2, 315-324.
10. Collingridge, G.L. & Isaac, J.T.R. (2003) Functional roles of protein interactions with AMPA and kainate receptors. Neurosci. Res., 47, 3-15.
11. Cooney, J.R., Hurlburt, J.L., Selig, D.K., Harris, K.M. & Fiala, J.C. (2002) Endosomal compartments serve multiple hippocampal dendritic spines from a widespread rather than a local store of recycling membrane. J. Neurosci., 22, 2215-2224.
12. Eshhar, N., Petralia, R.S., Winters, C.A., Niedzielski, A.S. & Wenthold, R.J. (1993) The segregation and expression of glutamate receptor subunits in cultured hippocampal neurons. Neuroscience, 57, 943-964.
13. Felberbaum-Corti, M., Van Der Goot, F.G. & Gruenberg, J. (2003) Sliding doors: clathrin-coated pits or caveolae? Nat. Cell Biol., 5, 382-384.
14. Fiala, J.C., Feinberg, M., Popov, V. & Harris, K.M. (1998) Synaptogenesis via dendritic filopodia in developing hippocampal area CA1. J. Neurosci., 18, 8900-8911.
15. Fourgeaud, L., Bessis, A.-S., Rossignol, F., Pin, J.-P., Olivo-Marin, J.-C. & Èmar, A. (2003) The metabotropic glutamate receptor mGluR5 is endocytosed by a clathrin-independent pathway. J. Biol. Chem., 278, 12222-12230.
16. Friedman, H.V., Bresler, T., Garner, C.C. & Ziv, N.E. (2000) Assembly of new individual excitatory synapses: Time course and temporal order of synaptic molecule recruitment. Neuron, 27, 57-69.
17. Gad, H.L., W.P., Zotova, E., Brodin, L. & Shupliakov, O. (1998) Dissociation between Ca2+-triggered synaptic vesicle exocytosis and clathrin-mediated endocytosis at a central synapse. Neuron, 21, 607-616.
18. Galbiati, F., Volonté D., Gil, O., Zanazzi, G., Salzer, J.L., Sargiacomo, M., Scherer, P.E., Engelman, J.A., Schlegel, A., Parenti, M., Okamoto, T. & Lisanti, M.P. (1998) Expression of caveolin-1 and -2 in differentiating PC12 cells and dorsal root ganglion neurons: Caveolin-2 is up-regulated in response to cell injury. Proc. Natl. Acad. Sci. USA, 95, 10257-10262.
19. Garner, C.C., Zhai, R.G., Gundelfinger, E.D. & Ziv, N.E. (2002) Molecular mechanisms of CNS synaptogenesis. Trends Neurosci., 25, 243-250.
20. Grosshans, D.R., Clayton, D.A., Coultrap, S.J. & Browning, M.D. (2002) LTP leads to rapid surface expression of NMDA but not AMPA receptors in adult rat CA1. Nat. Neurosci., 5, 27-33.
21. Hashimoto, M., Takenouchi, T., Rockenstein, E. & Masliah, E. (2003) α-synuclein up-regulates expression of caveolin-1 and down-regulates extracellular signal-regulated kinase activity in B103 neuroblastoma cells: role in the pathogenesis of Parkinson's disease. J. Neurochem., 85, 1468-1479.
22. Henley, J.M. (2003) Proteins interactions implicated in AMPA receptor trafficking: a clear destination and an improving route map. Neurosci. Res., 45, 243-254.
23. Hering, H., Lin, C.-C. & Sheng, M. (2003) Lipid rafts in the maintenance of synapses, dendritic spines, and surface AMPA receptor stability. J. Neurosci., 23, 3262-3271.
24. Ikezu, T., Ueda, H., Trapp, B.D., Nishiyama, K., Sha, J.F., Volonte, D., Galbiati, F., Byrd, A.L., Bassell, G., Serizawa, H., Lane, W.S., Lisanti, M.P. & Okamoto, T. (1998) Affinity-purification and characterization of caveolins from the brain: Differential expression of caveolin-1-2, and -3 in brain endothelial and astroglial cell types. Brain Res., 804, 177-192.
25. Jarousse, N. & Kelly, R.B. (2001) Endocytotic mechanisms in synapses. Curr. Opin. Cell Biol., 13, 461-469.
26. Kanaseki, T. & Kadota, K. (1969) The "vesicle in a basket". A morphological study of the coated vesicle isolated from the nerve endings of the guinea pig brain, with special reference to the mechanism of membrane movements. J. Cell Biol., 42, 202-220.
27. Lavezzari, G., McCallum, J., Lee, R. & Roche, K.W. (2003) Differential binding of the AP-2 adaptor complex and PSD-95 to the C-terminus of the NMDA receptor subunit NR2B regulates surface expression. Neuropharmacology, 45, 729-737.
28. Lee, S.H., Liu, L., Wang, Y.T. & 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.
29. Lee, S.H. & Sheng, M. (2000) Development of neuron-neuron synapses. Curr. Opin. Neurobiol., 10, 125-131.
30. Malinow, R. & Malenka, R.C. (2002) AMPA receptor trafficking and synaptic plasticity. Annu. Rev. Neurosci., 25, 103-126.
31. Man, H.-Y., Lin, J.W., Ju, W.H., Ahmadian, G., Liu, L., Becker, L.E., Sheng, M. & Wang, Y.T. (2000) Regulation of AMPA receptor-mediated synaptic transmission by clathrin-dependent receptor internalization. Neuron, 25, 649-662.
32. Nong, Y., Huang, Y.-Q., Ju, W., Kalia, L.V., Ahmadian, G., Wang, Y.T. & Salter, M.W. (2003) Glycine binding primes NMDA receptor internalization. Nature, 422, 302-307.
33. Passafaro, M., Pitch, V. & Sheng, M. (2001) Subunit-specific temporal and spatial patterns of AMPA receptor exocytosis in hippocampal neurons. Nat. Neurosci., 4, 917-926.
34. Perez, A.S. & Bredt, D.S. (1998) The N-terminal PDZ-containing region of postsynaptic density-95 mediates association with caveolar-like lipid domains. Neurosci. Lett., 258, 121-123.
35. Petralia, R.S., Esteban, J.A., Wang, Y.-X., Partridge, J.G., Zhao, H.-M., Wenthold, R.J. & Malinow, R. (1999) Selective acquisition of AMPA receptors over postnatal development suggests a molecular basis for silent synapses. Nat. Neurosci., 2, 31-36.
36. Petralia, R.S., Wang, Y.-X., Sans, N., Worley, P.F., Hammer, J.A. III & Wenthold, R.J. (2001) Glutamate receptor targeting in the postsynaptic spine involves mechanisms that are independent of myosin Va. Eur. J. Neurosci., 13, 1722-1732.
37. Petralia, R.S., Wang, Y.-X. & Wenthold, R.J. (1994b) The NMDA receptor subunits NR2A and NR2B show histological and ultrastructural localization patterns similar to those of NR1. J. Neurosci., 14, 6102-6120.
38. Petralia, R.S., Wang, Y.-X. & Wenthold, R.J. (2002) NMDA receptors and PSD-95 are found in attachment plaques in cerebellar granular layer glomeruli. Eur. J. Neurosci., 15, 583-587.
39. Petralia, R.S. & Wenthold, R.J. (1992) Light and electron immunocyto-chemical localization of AMPA-selective glutamate receptors in the rat brain. J. Comp. Neurol., 318, 329-354.
40. Petralia, R.S. & Wenthold, R.J. (1999) Immunocytochemistry of NMDA receptors. In: Li, M. (ed.) Methods in Molecular Biology: NMDA Receptor Protocols. Humana Press, Totowa, NJ, pp. 73-92.
41. Petralia, R.S., Yokotani, N. & Wenthold, R.J. (1994a) Light and electron microscope distribution of the NMDA receptor subunit NMDAR1 in the rat nervous system using a selective anti-peptide antibody. J. Neurosci., 14, 667-696.
42. Petralia, R.S., Zhao, H.-M., Wang, Y.-X. & Wenthold, R.J. (1998) Variations in the tangential distribution of postsynaptic glutamate receptors in Purkinje cell parallel and climbing fiber synapses during development. Neuropharmacology, 37, 1321-1334.
43. Rees, R.P., Bunge, M.B. & Bunge, R.P. (1976) Morphological changes in the neuritic growth cone and target neuron during synaptic junction development in culture. J. Cell Biol., 68, 240-263.
44. Roche, K.W., Standley, S., McCallum, J., Ly. C.D., Ehlers, M.D. & Wenthold, R.J. (2001) Molecular determinants of NMDA receptor internalization. Nat. Neurosci., 4, 794-802.
45. Rumbaugh, G. & Vicini, S. (1999) Distinct synaptic and extrasynaptic NMDA receptors in developing cerebellar granule neurons. J. Neurosci., 19, 10603-10610.
46. Sans, N., Petralia, R.S., Wang, Y.-X., Blahos, J., II, Hell, J.W. & Wenthold, R.J. (2000) A developmental change in NMDA receptor-associated proteins at hippocampal synapses. J. Neurosci., 20, 1260-1271.
47. Sheng, M. & Lee, S.H. (2003) AMPA receptor trafficking and synaptic plasticity: major unanswered questions. Neurosci. Res., 46, 127-134.
48. Shi, S.-H., Hayashi, Y., Petralia, R.S., Zaman, S.H., Wenthold, R.J., Svoboda, K. & Malinow, R. (1999) Rapid spine delivery and redistribution of AMPA receptors after synaptic NMDA receptor activation. Science, 284, 1811-1816.
49. Slepnev, V.I. & De Camilli, P. (2000) Accessory factors in clathrin-dependent synaptic vesicle endocytosis. Nat. Rev. Neurosci., 1, 161-172.
50. Smith, C.J., Grigorieff, N. & Pearse, B.M.F. (1998) Clathrin coats at 21 Å resolution: a cellular assembly designed to recycle multiple membrane receptors. EMBO J., 17, 4943-4953.
51. Sorkin, A. & von Zastrow, M. (2002) Signal transduction and endocytosis: Close encounters of many kinds. Nat. Rev. Mol. Cell Biol., 3, 600-614.
52. Spacek, J. & Harris, K.M. (1997) Three-dimensional organization of smooth endoplasmic reticulum in hippocampal CA1 dendrites and dendritic spines of the immature and mature rat. J. Neurosci., 17, 190-203.
53. Suzuki, T. (2002) Lipid rafts at postsynaptic sites: distribution, function and linkage to postsynaptic density. Neurosci. Res., 44, 1-9.
54. Tardin, C., Cognet, L., Bats, C., Lounis, B. & Choquet, D. (2003) Direct imaging of lateral movements of AMPA receptors insided synapses. EMBO J., 22, 4656-4665.
55. Tomita, S., Chen, L., Kawasaki, Y., Petralia, R.S., Wenthold, R.J., Nicoll, R.A. & Bredt, D.S. (2003) Functional studies and distribution define a family of transmembrane AMPA receptor regulatory proteins. J. Cell Biol., 161, 805-816.
56. Toni, N., Buchs, P.-A., Nikonenko, I., Povilaitite, P., Parisi, L. & Muller, D. (2001) Remodeling of synaptic membranes after induction of long-term potentiation. J. Neurosci., 21, 6245-6251.
57. Tovar, K.R. & Westbrook, G.L. (2002) Mobile NMDA receptors at hippocampal synapses. Neuron, 34, 255-264.
58. Vaughn, J.E. (1989) Review: Fine structure of synaptogenesis in the vertebrate central nervous system. Synapse, 3, 255-285.
59. Vigers, G.P.A., Crowther, R.A. & Pearse, B.M.F. (1986) Location of the 100 kd-50 kd accessory proteins in clathrin coats. EMBO J., 5, 2079-2085.
60. Vissel, B., Krupp, J.J., Heinemann, S.F. & Westbrook, G.L. (2001) A use-dependent tyrosine dephosphorylation of NMDA receptors is independent of ion flux. Nat. Neurosci., 4, 587-596.
61. Wang, Y.T. & Linden, D.J. (2000) Expression of cerebellar long-term depression requires postsynaptic clathrin-mediated endocytosis. Neuron, 25, 635-647.
62. Wenthold, R.J., Yokotani, N., Doi, K. & Wada, K. (1992) Immunochemical characterization of the non-NMDA glutamate receptor using subunit-specific antibodies. J. Biol. Chem., 267, 501-507.