SNAP-25 regulates spine formation through postsynaptic binding to p140Cap

Nature Communications

Volumn 4, Issue , 2013, Pages 1-13

  Tomasoni, Romana ^a,b   Repetto, Daniele ^c,e   Morini, Raffaella ^a,b   Elia, Chiara ^a,d   Gardoni, Fabrizio ^a   Di Luca, Monica ^a   Turco, Emilia ^c   Defilippi, Paola ^c   Matteoli, Michela ^a,b  

^a UNIVERSITY OF MILAN   (Italy)

^b HUMANITAS CLINICAL AND RESEARCH CENTER   (Italy)

^c UNIVERSITY OF TURIN   (Italy)

^d CNR   (Italy)

^e UNIVERSITY OF MÜNSTER   (Germany)

Author keywords

[No Author keywords available]

Indexed keywords

ADAPTOR PROTEIN; ADAPTOR PROTEIN P140CAP; DLGH4 PROTEIN, RAT; MEMBRANE PROTEIN; POSTSYNAPTIC DENSITY PROTEIN 95; PROTEIN BINDING; SIGNAL PEPTIDE; SNAP25 PROTEIN, RAT; SNIP PROTEIN, RAT; SYNAPTOSOMAL ASSOCIATED PROTEIN 25; UNCLASSIFIED DRUG; VESICULAR TRANSPORT ADAPTOR PROTEIN;

BIOCHEMISTRY; BIOLOGICAL DEVELOPMENT; CHEMICAL BINDING; CYTOLOGY; CYTOPLASM; FUNCTIONAL ROLE; GENE EXPRESSION; MEMBRANE; MORPHOGENESIS; PHENOTYPE; PHYSIOLOGY; PLASMA; PROTEIN;

ACTIN FILAMENT; ANIMAL; ANIMAL CELL; ANIMAL EMBRYO; ARTICLE; CELL MEMBRANE; CONTROLLED STUDY; CYTOLOGY; DENDRITIC SPINE; DENSITY; EMBRYOLOGY; EXCITATORY POSTSYNAPTIC POTENTIAL; GENE EXPRESSION REGULATION; GENETICS; HELA CELL LINE; HIPPOCAMPUS; HUMAN; MEMBRANE BINDING; METABOLISM; MORPHOGENESIS; NERVE CELL; NONHUMAN; PHENOTYPE; PRIMARY CELL CULTURE; PROTEIN EXPRESSION; PROTEIN LOCALIZATION; PROTEIN STABILITY; RAT; SIGNAL TRANSDUCTION; ULTRASTRUCTURE; HELA CELL; PRENATAL DEVELOPMENT; PROTEIN BINDING;

ACTIN CYTOSKELETON; ADAPTOR PROTEINS, VESICULAR TRANSPORT; ANIMALS; CYTOLOGY; DENDRITIC SPINES; EMBRYO, MAMMALIAN; EMBRYOLOGY; GENE EXPRESSION REGULATION, DEVELOPMENTAL; GENETICS; HELA CELLS; HIPPOCAMPUS; HUMANS; INTRACELLULAR SIGNALING PEPTIDES AND PROTEINS; MEMBRANE PROTEINS; METABOLISM; PRIMARY CELL CULTURE; PROTEIN BINDING; PROTEIN STABILITY; RATS; SIGNAL TRANSDUCTION; SYNAPTOSOMAL-ASSOCIATED PROTEIN 25; ULTRASTRUCTURE;

EID: 84880850503     PISSN: None     EISSN: 20411723     Source Type: Journal    
DOI: 10.1038/ncomms3136     Document Type: Article

References (60)

1. Sudhof, T. C. & Rothman, J. E. Membrane fusion: grappling with SNARE and SM proteins. Science 323, 474-477 (2009).
2. Jahn, R. & Scheller, R. H. SNAREs - engines for membrane fusion. Nat. Rev. Mol. Cell Biol. 7, 631-643 (2006).
3. Washbourne, P. et al. Genetic ablation of the t-SNARE SNAP-25 distinguishes mechanisms of neuroexocytosis. Nat. Neurosci. 5, 19-26 (2002).
4. Hess, D. T., Slater, T. M., Wilson, M. C. & Skene, J. H. The 25 kDa synaptosomal-associated protein SNAP-25 is the major methionine-rich polypeptide in rapid axonal transport and a major substrate for palmitoylation in adult CNS. J. Neurosci. 12, 4634-4641 (1992).
5. Gonzalo, S., Greentree, W. K. & Linder, M. E. SNAP-25 is targeted to the plasma membrane through a novel membrane-binding domain. J. Biol. Chem. 274, 21313-21318 (1999).
6. Catterall, W. A. & Few, A. P. Calcium channel regulation and presynaptic plasticity. Neuron 59, 882-901 (2008).
7. Lau, C. G. et al. SNAP-25 is a target of protein kinase C phosphorylation critical to NMDA receptor trafficking. J. Neurosci. 30, 242-254 (2010).
8. Selak, S. et al. A role for SNAP25 in internalization of kainate receptors and synaptic plasticity. Neuron 63, 357-371 (2009).
9. Chin, L. S., Nugent, R. D., Raynor, M. C., Vavalle, J. P. & Li, L. SNIP, a novel SNAP-25-interacting protein implicated in regulated exocytosis. J. Biol. Chem. 275, 1191-1200 (2000).
10. Di Stefano, P. et al. P130Cas-associated protein (p140Cap) as a new tyrosinephosphorylated protein involved in cell spreading. Mol. Biol. Cell 15, 787-800 (2004).
11. Damiano, L. et al. p140Cap suppresses the invasive properties of highly metastatic MTLn3-EGFR cells via impaired cortactin phosphorylation. Oncogene 31, 624-633 (2012).
12. Ito, H. et al. Characterization of a multidomain adaptor protein, p140Cap, as part of a pre-synaptic complex. J. Neurochem. 107, 61-72 (2008).
13. Jaworski, J. et al. Dynamic microtubules regulate dendritic spine morphology and synaptic plasticity. Neuron 61, 85-100 (2009).
14. Ethell, I. M. & Pasquale, E. B. Molecular mechanisms of dendritic spine development and remodeling. Prog. Neurobiol. 75, 161-205 (2005).
15. Tada, T. & Sheng, M. Molecular mechanisms of dendritic spine morphogenesis. Curr. Opin. Neurobiol. 16, 95-101 (2006).
16. Cheng, A. et al. Involvement of PGC-1alpha in the formation and maintenance of neuronal dendritic spines. Nat. Commun. 3, 1250 (2012).
17. Harris, K. M. & Kater, S. B. Dendritic spines: cellular specializations imparting both stability and flexibility to synaptic function. Annu. Rev. Neurosci. 17, 341-371 (1994).
18. Hering, H. & Sheng, M. Dendritic spines: structure, dynamics and regulation. Nat. Rev. Neurosci. 2, 880-888 (2001).
19. Kasai, H., Matsuzaki, M., Noguchi, J., Yasumatsu, N. & Nakahara, H. Structure-stability-function relationships of dendritic spines. Trends Neurosci. 26, 360-368 (2003).
20. Lamprecht, R. & LeDoux, J. Structural plasticity and memory. Nat. Rev. Neurosci. 5, 45-54 (2004).
21. Yuste, R. & Bonhoeffer, T. Morphological changes in dendritic spines associated with long-term synaptic plasticity. Annu. Rev. Neurosci. 24, 1071-1089 (2001).
22. Kaufmann, W. E. & Moser, H. W. Dendritic anomalies in disorders associated with mental retardation. Cereb. Cortex 10, 981-991 (2000).
23. Newey, S. E., Velamoor, V., Govek, E. E. & Van Aelst, L. Rho GTPases, dendritic structure, and mental retardation. J. Neurobiol. 64, 58-74 (2005).
24. Barr, C. L. et al. Identification of DNA variants in the SNAP-25 gene and linkage study of these polymorphisms and attention-deficit hyperactivity disorder. Mol. Psychiatry 5, 405-409 (2000).
25. Young, C. E. et al. SNAP-25 deficit and hippocampal connectivity in schizophrenia. Cereb. Cortex 8, 261-268 (1998).
26. Corradini, I., Verderio, C., Sala, M., Wilson, M. C. & Matteoli, M. SNAP-25 in neuropsychiatric disorders. Ann. NY Acad. Sci. 1152, 93-99 (2009).
27. Etain, B. et al. A SNAP25 promoter variant is associated with early-onset bipolar disorder and a high expression level in brain. Mol. Psychiatry 15, 748-755 (2010).
28. Sharma, M., Burre, J. & Sudhof, T. C. CSPalpha promotes SNARE-complex assembly by chaperoning SNAP-25 during synaptic activity. Nat. Cell Biol. 13, 30-39 (2011).
29. Verderio, C. et al. SNAP-25 modulation of calcium dynamics underlies differences in GABAergic and glutamatergic responsiveness to depolarization. Neuron 41, 599-610 (2004).
30. Grumelli, C., Corradini, I., Matteoli, M. & Verderio, C. Intrinsic calcium dynamics control botulinum toxin A susceptibility in distinct neuronal populations. Cell Calcium 47, 419-424 (2010).
31. Huang, X. et al. Truncated SNAP-25 (1-197), like botulinum neurotoxin A, can inhibit insulin secretion from HIT-T15 insulinoma cells. Mol. Endocrinol. 12, 1060-1070 (1998).
32. O'Sullivan, G. A., Mohammed, N., Foran, P. G., Lawrence, G. W. & Oliver Dolly, J. Rescue of exocytosis in botulinum toxin A-poisoned chromaffin cells by expression of cleavage-resistant SNAP-25. Identification of the minimal essential C-terminal residues. J. Biol. Chem. 274, 36897-36904 (1999).
33. Hayashi, K. et al. Maintenance of dendritic spine morphology by partitioningdefective 1b through regulation of microtubule growth. J. Neurosci. 31, 12094-12103 (2011).
34. Garcia, E. P., McPherson, P. S., Chilcote, T. J., Takei, K. & De Camilli, P. rbSec1A and B colocalize with syntaxin 1 and SNAP-25 throughout the axon, but are not in a stable complex with syntaxin. J. Cell Biol. 129, 105-120 (1995).
35. Holderith, N. et al. Release probability of hippocampal glutamatergic terminals scales with the size of the active zone. Nat. Neurosci. 15, 988-997 (2012).
36. Ovsepian, S. V. & Dolly, J. O. Dendritic SNAREs add a new twist to the old neuron theory. Proc. Natl Acad. Sci. USA 108, 19113-19120 (2011).
37. Di Stefano, P. et al. p140Cap protein suppresses tumour cell properties, regulating Csk and Src kinase activity. EMBO J. 26, 2843-2855 (2007).
38. Torregrosa-Hetland, C. J. et al. Cortical F-actin affects the localization and dynamics of SNAP-25 membrane clusters in chromaffin cells. Int. J. Biochem. Cell. Biol. 45, 583-592 (2013).
39. Bourne, J. N. & Harris, K. M. Balancing structure and function at hippocampal dendritic spines. Annu. Rev. Neurosci. 31, 47-67 (2008).
40. Sorra, K. E. & Harris, K. M. Overview on the structure, composition, function, development, and plasticity of hippocampal dendritic spines. Hippocampus 10, 501-511 (2000).
41. Lang, T. & Jahn, R. Core proteins of the secretory machinery. Handb. Exp. Pharmacol. 107-127 (2008).
42. Sorensen, J. B. SNARE complexes prepare for membrane fusion. Trends Neurosci. 28, 453-455 (2005).
43. Kidokoro, Y. Roles of SNARE proteins and synaptotagmin I in synaptic transmission: studies at the Drosophila neuromuscular synapse. Neurosignals 12, 13-30 (2003).
44. Peng, J. et al. Semiquantitative proteomic analysis of rat forebrain postsynaptic density fractions by mass spectrometry. J. Biol. Chem. 279, 21003-21011 (2004).
45. Condliffe, S. B., Corradini, I., Pozzi, D., Verderio, C. & Matteoli, M. Endogenous SNAP-25 regulates native voltage-gated calcium channels in glutamatergic neurons. J. Biol. Chem. 285, 24968-24976 (2010).
46. Bronk, P. et al. Differential effects of SNAP-25 deletion on Ca2+dependent and Ca2+independent neurotransmission. J. Neurophysiol. 98, 794-806 (2007).
47. Delgado-Martinez, I., Nehring, R. B. & Sorensen, J. B. Differential abilities of SNAP-25 homologs to support neuronal function. J. Neurosci. 27, 9380-9391 (2007).
48. Jurado, S. et al. LTP requires a unique postsynaptic SNARE fusion machinery. Neuron 77, 542-558 (2013).
49. Verpelli, C. et al. Importance of Shank3 protein in regulating metabotropic glutamate receptor 5 (mGluR5) expression and signaling at synapses. J. Biol. Chem. 286, 34839-34850 (2011).
50. Pfeiffer, B. E. & Huber, K. M. Fragile X mental retardation protein induces synapse loss through acute postsynaptic translational regulation. J. Neurosci. 27, 3120-3130 (2007).
51. Menna, E., Fossati, G., Scita, G. & Matteoli, M. From filopodia to synapses: the role of actin-capping and anti-capping proteins. Eur. J. Neurosci. 34, 1655-1662 (2011).
52. Penzes, P., Cahill, M., Jones, K., VanLeeuwen, J.-E. & Woolfrey, K. Dendritic spine pathology in neuropsychiatric disorders. Nat. Neurosci. 14, 285-378 (2011).
53. Brummelkamp, T. R., Bernards, R. & Agami, R. A system for stable expression of short interfering RNAs in mammalian cells. Science 296, 550-553 (2002).
54. Magarinos, A. M. et al. Effect of brain-derived neurotrophic factor haploinsufficiency on stress-induced remodeling of hippocampal neurons. Hippocampus 21, 253-264 (2011).
55. Harris, K. M. & Stevens, J. K. Dendritic spines of CA 1 pyramidal cells in the rat hippocampus: serial electron microscopy with reference to their biophysical characteristics. J. Neurosci. 9, 2982-2997 (1989).
56. Peters, A. & Kaiserman-Abramof, I. R. The small pyramidal neuron of the rat cerebral cortex. The perikaryon, dendrites and spines. Am. J. Anat. 127, 321-355 (1970).
57. Verderio, C., Coco, S., Fumagalli, G. & Matteoli, M. Spatial changes in calcium signaling during the establishment of neuronal polarity and synaptogenesis. J. Cell Biol. 126, 1527-1536 (1994).
58. Meixner, A. et al. A QUICK screen for Lrrk2 interaction partners - leucine-rich repeat kinase 2 is involved in actin cytoskeleton dynamics. Mol. Cell Proteomics 10, 001172 (2011).
59. Gardoni, F. et al. Calcium/calmodulin-dependent protein kinase II is associated with NR2A/B subunits of NMDA receptor in postsynaptic densities. J. Neurochem. 71, 1733-1741 (1998).
60. Hotulainen, P. & Hoogenraad, C. C. Actin in dendritic spines: connecting dynamics to function. J. Cell Biol. 189, 619-629 (2010).