The dynamin-binding domains of Dap160/intersectin affect bulk membrane retrieval in synapses

Journal of Cell Science

Volumn 126, Issue 4, 2013, Pages 1021-1031

  Winther, Åsa M E ^a   Jiao, Wei ^a,c   Vorontsova, Olga ^a   Rees, Kathryn A ^a   Koh, Tong Wey ^b,d   Sopova, Elena ^a   Schulze, Karen L ^b   Bellen, Hugo J ^b   Shupliakov, Oleg ^a  

^a KAROLINSKA INSTITUTE   (Sweden)

^b BAYLOR COLLEGE OF MEDICINE   (United States)

^c NewYork Presbyterian Hospital   (United States)

^d YALE UNIVERSITY   (United States)

Author keywords

Drosophila; Neuromuscular junction; Protein migration; Scaffolding molecules; SH3 domain

Indexed keywords

DYNAMIN ASSOCIATED PROTEIN 160; INTERSECTIN; PROTEIN SH3; UNCLASSIFIED DRUG;

ARTICLE; DROSOPHILA; ELECTROPHYSIOLOGY; EXCITATORY JUNCTION POTENTIAL; GENE EXPRESSION; IMMUNOCYTOCHEMISTRY; NEUROMUSCULAR SYNAPSE; NONHUMAN; PRIORITY JOURNAL; SYNAPSE; SYNAPSE VESICLE;

ANIMALS; DROSOPHILA PROTEINS; ELECTROPHYSIOLOGY; IMMUNOHISTOCHEMISTRY; NEUROMUSCULAR JUNCTION; PROTEIN TRANSPORT; SYNAPSES; VESICULAR TRANSPORT PROTEINS;

EID: 84876332420     PISSN: 00219533     EISSN: 14779137     Source Type: Journal    
DOI: 10.1242/jcs.118968     Document Type: Article

References (31)

1. Broadie, K. (2004). Synapse scaffolding: intersection of endocytosis and growth. Curr. Biol. 14, R853-R855.
2. Cheung, G. and Cousin, M. A. (2012). Adaptor protein complexes 1 and 3 are essential for generation of synaptic vesicles from activity-dependent bulk endosomes. J. Neurosci. 32, 6014-6023.
3. Cho, K. O., Chern, J., Izaddoost, S. and Choi, K. W. (2000). Novel signaling from the peripodial membrane is essential for eye disc patterning in Drosophila. Cell 103, 331- 342.
4. Coyle, I. P., Koh, Y. H., Lee, W. C., Slind, J., Fergestad, T., Littleton, J. T. and Ganetzky, B. (2004). Nervous wreck, an SH3 adaptor protein that interacts with Wsp, regulates synaptic growth in Drosophila. Neuron 41, 521-534.
5. Dittman, J. and Ryan, T. A. (2009). Molecular circuitry of endocytosis at nerve terminals. Annu. Rev. Cell Dev. Biol. 25, 133-160.
6. Estes, P. S., Roos, J., van der Bliek, A., Kelly, R. B., Krishnan, K. S. and Ramaswami, M. (1996). Traffic of dynamin within individual Drosophila synaptic boutons relative to compartment-specific markers. J. Neurosci. 16, 5443-5456.
7. Evergren, E., Gad, H., Walther, K., Sundborger, A., Tomilin, N. and Shupliakov, O. (2007). Intersectin is a negative regulator of dynamin recruitment to the synaptic endocytic zone in the central synapse. J. Neurosci. 27, 379-390.
8. Ferguson, S. M. and De Camilli, P. (2012). Dynamin, a membrane-remodelling GTPase. Nat. Rev. Mol. Cell Biol. 13, 75-88.
9. González-Gaitán, M. and Jäckle, H. (1997). Role of Drosophila alpha-adaptin in presynaptic vesicle recycling. Cell 88, 767-776.
10. Hallermann, S., Heckmann, M. and Kittel, R. J. (2010). Mechanisms of short-term plasticity at neuromuscular active zones of Drosophila. HFSP J. 4, 72-84.
11. Hayashi, M., Raimondi, A., O'Toole, E., Paradise, S., Collesi, C., Cremona, O., Ferguson, S. M. and De Camilli, P. (2008). Cell- and stimulus-dependent heterogeneity of synaptic vesicle endocytic recycling mechanisms revealed by studies of dynamin 1-null neurons. Proc. Natl. Acad. Sci. USA 105, 2175-2180.
12. Henne, W. M., Boucrot, E., Meinecke, M., Evergren, E., Vallis, Y., Mittal, R. and McMahon, H. T. (2010). FCHo proteins are nucleators of clathrin-mediated endocytosis. Science 328, 1281-1284.
13. Jiao, W., Masich, S., Franzén, O. and Shupliakov, O. (2010a). Two pools of vesicles associated with the presynaptic cytosolic projection in Drosophila neuromuscular junctions. J. Struct. Biol. 172, 389-394.
14. Jiao, W., Shupliakov, A. and Shupliakov, O. (2010b). A semi-correlative technique for the subcellular localization of proteins in Drosophila synapses. J. Neurosci. Methods 185, 273-279.
15. Kasprowicz, J., Kuenen, S., Miskiewicz, K., Habets, R. L., Smitz, L. and Verstreken, P. (2008). Inactivation of clathrin heavy chain inhibits synaptic recycling but allows bulk membrane uptake. J. Cell Biol. 182, 1007-1016.
16. Koenig, J. H. and Ikeda, K. (1989). Disappearance and reformation of synaptic vesicle membrane upon transmitter release observed under reversible blockage of membrane retrieval. J. Neurosci. 9, 3844-3860.
17. Koh, T. W., Verstreken, P. and Bellen, H. J. (2004). Dap160/intersectin acts as a stabilizing scaffold required for synaptic development and vesicle endocytosis. Neuron 43, 193-205.
18. Koh, T. W., Korolchuk, V. I., Wairkar, Y. P., Jiao, W., Evergren, E., Pan, H., Zhou, Y., Venken, K. J., Shupliakov, O., Robinson, I. M. et al. (2007). Eps15 and Dap160 control synaptic vesicle membrane retrieval and synapse development. J. Cell Biol. 178, 309-322.
19. Littleton, J. T., Bellen, H. J. and Perin, M. S. (1993). Expression of synaptotagmin in Drosophila reveals transport and localization of synaptic vesicles to the synapse. Development 118, 1077-1088.
20. Marie, B., Sweeney, S. T., Poskanzer, K. E., Roos, J., Kelly, R. B. and Davis, G. W. (2004). Dap160/intersectin scaffolds the periactive zone to achieve high-fidelity endocytosis and normal synaptic growth. Neuron 43, 207-219.
21. O'Connor-Giles, K. M., Ho, L. L. and Ganetzky, B. (2008). Nervous wreck interacts with thickveins and the endocytic machinery to attenuate retrograde BMP signaling during synaptic growth. Neuron 58, 507-518.
22. Pechstein, A., Shupliakov, O. and Haucke, V. (2010). Intersectin 1: a versatile actor in the synaptic vesicle cycle. Biochem. Soc. Trans. 38, 181-186.
23. Rodal, A. A., Motola-Barnes, R. N. and Littleton, J. T. (2008). Nervous wreck and Cdc42 cooperate to regulate endocytic actin assembly during synaptic growth. J. Neurosci. 28, 8316-8325.
24. Roos, J. and Kelly, R. B. (1998). Dap160, a neural-specific Eps15 homology and multiple SH3 domain-containing protein that interacts with Drosophila dynamin. J. Biol. Chem. 273, 19108-19119.
25. Roos, J. and Kelly, R. B. (1999). The endocytic machinery in nerve terminals surrounds sites of exocytosis. Curr. Biol. 9, 1411-1414.
26. Saheki, Y. and De Camilli, P. (2012). Synaptic vesicle endocytosis. Cold Spring Harb. Perspect. Biol. 4, a005645.
27. Takei, K., McPherson, P. S., Schmid, S. L. and De Camilli, P. (1995). Tubular membrane invaginations coated by dynamin rings are induced by GTP-gamma S in nerve terminals. Nature 374, 186-190.
28. Verstreken, P., Ohyama, T. and Bellen, H. J. (2008). FM 1-43 labeling of synaptic vesicle pools at the Drosophila neuromuscular junction. Methods Mol. Biol. 440, 349- 369.
29. Wagh, D. A., Rasse, T. M., Asan, E., Hofbauer, A., Schwenkert, I., Dürrbeck, H., Buchner, S., Dabauvalle, M. C., Schmidt, M., Qin, G. et al. (2006). Bruchpilot, a protein with homology to ELKS/CAST, is required for structural integrity and function of synaptic active zones in Drosophila. Neuron 49, 833-844.
30. Yang, P., Shaver, S. A., Hilliker, A. J. and Sokolowski, M. B. (2000). Abnormal turning behaviour in Drosophila larvae: Identification and molecular analysis of scribbler (sbb). Genetics 155, 1161-1174.
31. Zinsmaier, K. E., Eberle, K. K., Buchner, E., Walter, N. and Benzer, S. (1994). Paralysis and early death in cysteine string protein mutants of Drosophila. Science 263, 977-980