A neuronal role for SNAP-23 in postsynaptic glutamate receptor trafficking

Nature Neuroscience

Volumn 13, Issue 3, 2010, Pages 338-343

  Suh, Young Ho ^a,b   Terashima, Akira ^a   Petralia, Ronald S ^c   Wenthold, Robert J ^c   Isaac, John T R ^a   Roche, Katherine W ^a   Roche, Paul A ^b  

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

^b Institut national du cancer du Canada   (Canada)

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

Author keywords

[No Author keywords available]

Indexed keywords

GLUTAMATE RECEPTOR; N METHYL DEXTRO ASPARTIC ACID RECEPTOR; POSTSYNAPTIC RECEPTOR; SHORT HAIRPIN RNA; SNARE PROTEIN; SYNAPTOSOMAL ASSOCIATED PROTEIN 23; SYNAPTOSOMAL ASSOCIATED PROTEIN 25;

ANIMAL CELL; ANIMAL EXPERIMENT; ARTICLE; CELLULAR DISTRIBUTION; CONTROLLED STUDY; DENDRITIC SPINE; EXCITATORY POSTSYNAPTIC POTENTIAL; MOUSE; NERVE CELL; NERVE FIBER; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN LOCALIZATION; SYNAPSE VESICLE; SYNAPTOSOME;

ANIMALS; AXONS; CELL LINE; CELL MEMBRANE; DENDRITES; DENDRITIC SPINES; HIPPOCAMPUS; HUMANS; MEMBRANE POTENTIALS; MICE; MICE, TRANSGENIC; NEURONS; QB-SNARE PROTEINS; QC-SNARE PROTEINS; RATS; RATS, SPRAGUE-DAWLEY; RECEPTORS, GLUTAMATE; RECEPTORS, N-METHYL-D-ASPARTATE; SYNAPSES; SYNAPTOSOMAL-ASSOCIATED PROTEIN 25; VESICULAR TRANSPORT PROTEINS;

EID: 77649179060     PISSN: 10976256     EISSN: None     Source Type: Journal    
DOI: 10.1038/nn.2488     Document Type: Article

References (48)

1. Mayer, A. Membrane fusion in eukaryotic cells. Annu. Rev. Cell Dev. Biol. 18, 289-314 (2002).
2. Jahn, R. & Sudhof, T.C. Membrane fusion and exocytosis. Annu. Rev. Biochem. 68, 863-911 (1999).
3. Jahn, R. & Scheller, R.H. SNAREs-engines for membrane fusion. Nat. Rev. Mol. Cell Biol. 7, 631-643 (2006).
4. Lin, R.C. & Scheller, R.H. Mechanisms of synaptic vesicle exocytosis. Annu. Rev. Cell Dev. Biol. 16, 19-49 (2000).
5. Duc, C. & Catsicas, S. Ultrastructural localization of SNAP-25 within the rat spinal cord and peripheral nervous system. J. Comp. Neurol. 356, 152-163 (1995).
6. Oyler, G.A. et al. The identifcation of a novel synaptosomal-associated protein, SNAP-25, differentially expressed by neuronal subpopulations. J. Cell Biol. 109, 3039-3052 (1989).
7. Tao-Cheng, J.H., Du, J. & McBain, C.J. Snap-25 is polarized to axons and abundant along the axolemma: an immunogold study of intact neurons. J. Neurocytol. 29, 67-77 (2000).
8. Washbourne, P. et al. Genetic ablation of the t-SNARE SNAP-25 distinguishes mechanisms of neuroexocytosis. Nat. Neurosci. 5, 19-26 (2002).
9. Ravichandran, V., Chawla, A. & Roche, P.A. Identifcation of a novel syntaxin-and synaptobrevin/VAMP-binding protein, SNAP-23, expressed in non-neuronal tissues. J. Biol. Chem. 271, 13300-13303 (1996).
10. Chen, D., Bernstein, A.M., Lemons, P.P. & Whiteheart, S.W. Molecular mechanisms of platelet exocytosis: role of SNAP-23 and syntaxin 2 in dense core granule release. Blood 95, 921-929 (2000). (Pubitemid 30062714)
11. Foster, L.J., Yaworsky, K., Trimble, W.S. & Klip, A. SNAP23 promotes insulin-dependent glucose uptake in 3T3-L1 adipocytes: possible interaction with cytoskeleton. Am. J. Physiol. 276, 1108-1114 (1999).
12. Guo, Z., Turner, C. & Castle, D. Relocation of the t-SNARE SNAP-23 from lamellipodia-like cell surface projections regulates compound exocytosis in mast cells. Cell 94, 537-548 (1998).
13. Vaidyanathan, V.V., Puri, N. & Roche, P.A. The last exon of SNAP-23 regulates granule exocytosis from mast cells. J. Biol. Chem. 276, 25101-25106 (2001).
14. Bragina, L. et al. Heterogeneity of glutamatergic and GABAergic release machinery in cerebral cortex. Neuroscience 146, 1829-1840 (2007).
15. Chen, D., Minger, S.L., Honer, W.G. & Whiteheart, S.W. Organization of the secretory machinery in the rodent brain: distribution of the t-SNAREs, SNAP-25 and SNAP-23. Brain Res. 831, 11-24 (1999).
16. Verderio, C. et al. SNAP-25 modulation of calcium dynamics underlies differences in GABAergic and glutamatergic responsiveness to depolarization. Neuron 41, 599-610 (2004).
17. Sadoul, K. et al. SNAP-23 is not cleaved by botulinum neurotoxin E and can replace SNAP-25 in the process of insulin secretion. J. Biol. Chem. 272, 33023-33027 (1997).
18. Lau, C.G. & Zukin, R.S. NMDA receptor traffcking in synaptic plasticity and neuropsychiatric disorders. Nat. Rev. Neurosci. 8, 413-426 (2007).
19. Wenthold, R.J., Prybylowski, K., Standley, S., Sans, N. & Petralia, R.S. Traffcking of NMDA receptors. Annu. Rev. Pharmacol. Toxicol. 43, 335-358 (2003).
20. Groc, L. & Choquet, D. AMPA and NMDA glutamate receptor traffcking: multiple roads for reaching and leaving the synapse. Cell Tissue Res. 326, 423-438 (2006).
21. Roche, K.W. et al. Molecular determinants of NMDA receptor internalization. Nat. Neurosci. 4, 794-802 (2001).
22. Lavezzari, G., McCallum, J., Dewey, C.M. & Roche, K.W. Subunit-specifc regulation of NMDA receptor endocytosis. J. Neurosci. 24, 6383-6391 (2004).
23. Sans, N. et al. NMDA receptor traffcking through an interaction between PDZ proteins and the exocyst complex. Nat. Cell Biol. 5, 520-530 (2003).
24. Washbourne, P., Liu, X.B., Jones, E.G. & McAllister, A.K. Cycling of NMDA receptors during traffcking in neurons before synapse formation. J. Neurosci. 24, 8253-8264 (2004).
25. Tovar, K.R. & Westbrook, G.L. Mobile NMDA receptors at hippocampal synapses. Neuron 34, 255-264 (2002).
26. Oyler, G.A., Polli, J.W., Wilson, M.C. & Billingsley, M.L. Developmental expression of the 25-kDa synaptosomal-associated protein (SNAP-25) in rat brain. Proc. Natl. Acad. Sci. USA 88, 5247-5251 (1991).
27. Vaidyanathan, V.V. & Roche, P.A. Structure and chromosomal localization of the mouse Snap23 gene. Gene 247, 181-189 (2000).
28. Cahill, A.L., Herring, B.E. & Fox, A.P. Stable silencing of SNAP-25 in PC12 cells by RNA interference. BMC Neurosci. 7, 9 (2006).
29. Scott, D.B., Michailidis, I., Mu, Y., Logothetis, D. & Ehlers, M.D. Endocytosis and degradative sorting of NMDA receptors by conserved membrane-proximal signals. J. Neurosci. 24, 7096-7109 (2004).
30. Sutton, R.B., Fasshauer, D., Jahn, R. & Brunger, A.T. Crystal structure of a SNARE complex involved in synaptic exocytosis at 2.4 angstrom resolution. Nature 395, 347-353 (1998).
31. Leung, S.M., Chen, D., DasGupta, B.R., Whiteheart, S.W. & Apodaca, G. SNAP-23 requirement for transferrin recycling in Streptolysin-O-permeabilized Madin-Darby canine kidney cells. J. Biol. Chem. 273, 17732-17741 (1998).
32. Lledo, P.M., Zhang, X., Sudhof, T.C., Malenka, R.C. & Nicoll, R.A. Postsynaptic membrane fusion and long-term potentiation. Science 279, 399-403 (1998).
33. Nishimune, A. et al. NSF binding to GluR2 regulates synaptic transmission. Neuron 21, 87-97 (1998).
34. Osten, P. et al. The AMPA receptor GluR2 C terminus can mediate a reversible, ATP-dependent interaction with NSF and alpha-and beta-SNAPs. Neuron 21, 99-110 (1998).
35. Song, I. et al. Interaction of the N-ethylmaleimide-sensitive factor with AMPA receptors. Neuron 21, 393-400 (1998).
36. Lan, J.Y. et al. Protein kinase C modulates NMDA receptor traffcking and gating. Nat. Neurosci. 4, 382-390 (2001).
37. Lan, J.Y. et al. Activation of metabotropic glutamate receptor 1 accelerates NMDA receptor traffcking. J. Neurosci. 21, 6058-6068 (2001).
38. Lüscher, C. et al. Role of AMPA receptor cycling in synaptic transmission and plasticity. Neuron 24, 649-658 (1999).
39. Selak, S. et al. A role for SNAP25 in internalization of kainate receptors and synaptic plasticity. Neuron 63, 357-371 (2009).
40. Hayashi, T. et al. Synaptic vesicle membrane fusion complex: action of clostridial neurotoxins on assembly. EMBO J. 13, 5051-5061 (1994).
41. Petralia, R.S., Sans, N., Wang, Y.X. & Wenthold, R.J. Ontogeny of postsynaptic density proteins at glutamatergic synapses. Mol. Cell. Neurosci. 29, 436-452 (2005).
42. Petralia, R.S., Wang, Y.X. & Wenthold, R.J. Internalization at glutamatergic synapses during development. Eur. J. Neurosci. 18, 3207-3217 (2003).
43. Petralia, R.S. & Wenthold, R.J. Immunocytochemistry of NMDA receptors. Methods Mol. Biol. 128, 73-92 (1999).
44. Yi, Z. et al. The role of the PDZ protein GIPC in regulating NMDA receptor traffcking. J. Neurosci. 27, 11663-11675 (2007).
45. Carlin, R.K., Grab, D.J., Cohen, R.S. & Siekevitz, P. Isolation and characterization of postsynaptic densities from various brain regions: enrichment of different types of postsynaptic densities. J. Cell Biol. 86, 831-845 (1980).
46. Schlüter, O.M., Xu, W. & Malenka, R.C. Alternative N-terminal domains of PSD-95 and SAP97 govern activity-dependent regulation of synaptic AMPA receptor function. Neuron 51, 99-111 (2006).
47. Suh, Y.H. et al. Corequirement of PICK1 binding and PKC phosphorylation for stable surface expression of the metabotropic glutamate receptor mGluR7. Neuron 58, 736-748 (2008).
48. Terashima, A. et al. An essential role for PICK1 in NMDA receptor-dependent bidirectional synaptic plasticity. Neuron 57, 872-882 (2008).