Synaptic vesicle recycling: Genetic and cell biological studies

Journal of Neurogenetics

Volumn 24, Issue 3, 2010, Pages 146-157

  Majumder, Riddhi ^a   Krishnan, K S ^a  

^a TATA INSTITUTE OF FUNDAMENTAL RESEARCH   (India)

Author keywords

dynamin; eps15; ND kinase; stoned; vesicle recycling

Indexed keywords

CALCIUM; DYNAMIN; ENDOPHILIN; EPIDERMAL GROWTH FACTOR RECEPTOR PATHWAY SUBSTRATE 15;

CELL MIGRATION; CYTOLOGY; DROSOPHILA; ENDOCYTOSIS; GENE LOCUS; GENE MUTATION; NONHUMAN; PRIORITY JOURNAL; PROTEIN DEPHOSPHORYLATION; PROTEIN INTERACTION; PROTEIN STRUCTURE; REVIEW; SYNAPSE VESICLE; TEMPERATURE SENSITIVE MUTANT;

ANIMALS; DROSOPHILA MELANOGASTER; ENDOCYTOSIS; MOLECULAR BIOLOGY; PRESYNAPTIC TERMINALS; SYNAPTIC TRANSMISSION; SYNAPTIC VESICLES;

EID: 77956314925     PISSN: 01677063     EISSN: 15635260     Source Type: Journal    
DOI: 10.3109/01677063.2010.506229     Document Type: Review

References (124)

1. Andrews, J., Smith, M., Merakovsky, J., Coulson, M., Hannan, F., & Kelly, L. E. (1996). The stoned locus of Drosophila melanogaster produces a dicistronic transcript and encodes two distinct polypeptides. Genetics, 143, 1699-1711.
2. Barker, L. A., Dowdall, M. J., & Whittaker, V. P. (1972). Choline metabolism in the cerebral cortex of guinea pigs. Stablebound acetylcholine. Biochem J 130, 1063-1075.
3. Benmerah, A. (2004). Endocytosis: Signaling from endocytic membranes to the nucleus. Curr Biol 14, R314-R316.
4. Benmerah, A., Begue, B., Dautry-Varsat, A., & Cerf-Bensussan, N. (1996). The ear of alpha-adaptin interacts with the COOH-terminal domain of the Eps 15 protein. J Biol Chem 271, 12111-12116.
5. 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.
6. Ceccarelli, B., Hurlbut, W. P., & Mauro, A. (1973). Turnover of transmitter and synaptic vesicles at the frog neuromuscular junction. J Cell Biol 57, 499-524.
7. Chadda, R., Howes, M. T., Plowman, S. J., Hancock, J. F., Parton, R. G., & Mayor, S. (2007). Cholesterol-sensitive Cdc42 activation regulates actin polymerization for endocytosis via the GEEC pathway. Traffi c 8, 702-717.
8. Chen, M. L., Green, D., Liu, L., Lam, Y. C., Mukai, L., Rao, S., Ramagiri, S., Krishnan, K. S., Engel, J. E., Lin, J. J., et al. (2002). Unique biochemical and behavioral alterations in Drosophila shibire(ts1) mutants imply a conformational state affecting dynamin subcellular distribution and synaptic vesicle cycling. J Neurobiol 53, 319-329.
9. Chen, M. S., Obar, R. A., Schroeder, C. C., Austin, T. W., Poodry, C. A., Wadsworth, S. C., & Vallee, R. B. (1991). Multiple forms of dynamin are encoded by shibire, a Drosophila gene involved in endocytosis. Nature 351, 583-586.
10. Cheung, G., Jupp, O. J., & Cousin, M. A. (2010). Activitydependent bulk endocytosis and clathrin-dependent endocytosis replenish specifi c synaptic vesicle pools in central nerve terminals. J Neurosci 30, 8151-8161.
11. Collins, B. M., McCoy, A. J., Kent, H. M., Evans, P. R., & Owen, D. J. (2002). Molecular architecture and functional model of the endocytic AP2 complex. Cell 109, 523-535.
12. Conner, S. D., & Schmid, S. L. (2003). Differential requirements for AP-2 in clathrin-mediated endocytosis. J Cell Biol 162, 773-779.
13. Conner, S. D., Schroter, T., & Schmid, S. L. (2003). AAK1-mediated micro2 phosphorylation is stimulated by assembled clathrin. Traffi c 4, 885-890.
14. Cremona, O., Di Paolo, G., Wenk, M. R., Luthi, A., Kim, W. T., Takei, K., Daniell, L., Nemoto, Y., Shears, S. B., Flavell, R. A. et al. (1999). Essential role of phosphoinositide metabolism in synaptic vesicle recycling. Cell 99, 179-188.
15. Cupers, P., Jadhav, A. P., & Kirchhausen, T. (1998). Assembly of clathrin coats disrupts the association between Eps15 and AP-2 adaptors. J Biol Chem 273, 1847-1850.
16. de Celis, J. F., de Celis, J., Ligoxygakis, P., Preiss, A., Delidakis, C., & Bray, S. (1996). Functional relationships between Notch, Su(H) and the bHLH genes of the E(spl) complex: The E(spl) genes mediate only a subset of Notch activities during imaginal development. Development 122, 2719-2728.
17. Diril, M. K., Wienisch, M., Jung, N., Klingauf, J., & Haucke, V. (2006). Stonin 2 is an AP-2-dependent endocytic sorting adaptor for synaptotagmin internalization and recycling. Dev Cell 10, 233-244.
18. Doherty, G. J., & McMahon, H. T. (2009). Mechanisms of endocytosis. Annu Rev Biochem 78, 857-902.
19. Estes, P. S., Jackson, T. C., Stimson, D. T., Sanyal, S., Kelly, L. E., & Ramaswami, M. (2003). Functional dissection of a eukaryotic dicistronic gene: Transgenic stonedB, but not stonedA, restores normal synaptic properties to Drosophila stoned mutants. Genetics 165, 185-196.
20. Estes, P. S., Roos, J., van der Bliek, A., Kelly, R. B., Krishnan, K. S., & Ramaswami, M. (1996). Traffi c of dynamin within individual Drosophila synaptic boutons relative to compartment-specifi c markers. J Neurosci 16, 5443-5456.
21. Evergren, E., Gad, H., Walther, K., Sundborger, A., Tomilin, N., & 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.
22. Farsad, K., Ringstad, N., Takei, K., Floyd, S. R., Rose, K., & De Camilli, P. (2001). Generation of high curvature membranes mediated by direct endophilin bilayer interactions. J Cell Biol 155, 193-200.
23. Fazioli, F., Minichiello, L., Matoskova, B., Wong, W. T., & Di Fiore, P. P. (1993). eps15, a novel tyrosine kinase substrate, exhibits transforming activity. Mol Cell Biol 13, 5814-5828.
24. Fergestad, T., & Broadie, K. (2001). Interaction of stoned and synaptotagmin in synaptic vesicle endocytosis. J Neurosci 21, 1218-1227.
25. Ford, M. G., Mills, I. G., Peter, B. J., Vallis, Y., Praefcke, G. J., Evans, P. R., & McMahon, H. T. (2002). Curvature of clathrin-coated pits driven by epsin. Nature 419, 361-366.
26. Gallop, J. L., Jao, C. C., Kent, H. M., Butler, P. J., Evans, P. R., Langen, R., & McMahon, H. T. (2006). Mechanism of endophilin N-BAR domain-mediated membrane curvature. EMBO J 25, 2898-2910.
27. Gonzalez-Gaitan, M., & Jackle, H. (1997). Role of Drosophila alpha-adaptin in presynaptic vesicle recycling. Cell 88, 767-776.
28. Grant, B. D., & Donaldson, J. G. (2009). Pathways and mechanisms of endocytic recycling. Nat Rev Mol Cell Biol 10, 597-608.
29. Grant, D., Unadkat, S., Katzen, A., Krishnan, K. S., & Ramaswami, M. (1998). Probable mechanisms underlying interallelic complementation and temperature-sensitivity of mutations at the shibire locus of Drosophila melanogaster . Genetics 149, 1019-1030.
30. Grigliatti, T. A., Hall, L., Rosenbluth, R., & Suzuki, D. T. (1973). Temperature-sensitive mutations in Drosophila melanogaster . XIV. A selection of immobile adults. Mol Gen Genet 120, 107-114.
31. Guha, A., Sriram, V., Krishnan, K. S., & Mayor, S. (2003). Shibire mutations reveal distinct dynamin-independent and -dependent endocytic pathways in primary cultures of Drosophila hemocytes. J Cell Sci 116, 3373-3386.
32. Guichet, A., Wucherpfennig, T., Dudu, V., Etter, S., Wilsch-Brauniger, M., Hellwig, A., Gonzalez-Gaitan, M., Huttner, W. B., & Schmidt, A. A. (2002). Essential role of endophilin A in synaptic vesicle budding at the Drosophila neuromuscular junction. EMBO J 21, 1661-1672.
33. Hamanaka, Y., & Meinertzhagen, I. A. (2010). Immunocytochemical localization of synaptic proteins to photoreceptor synapses of Drosophila melanogaster . J Comp Neurol 518, 1133-1155.
34. Harlow, M. L., Ress, D., Stoschek, A., Marshall, R. M., & McMahan, U. J. (2001). The architecture of active zone material at the frog ' s neuromuscular junction. Nature 409, 479-484.
35. Haucke, V., & De Camilli, P. (1999). AP-2 recruitment to synaptotagmin stimulated by tyrosine-based endocytic motifs. Science 285, 1268-1271.
36. Heerssen, H., Fetter, R. D., & Davis, G. W. (2008). Clathrin dependence of synaptic-vesicle formation at the Drosophila neuromuscular junction. Curr Biol 18, 401-409.
37. Heuser, J. (1989). The role of coated vesicles in recycling of synaptic vesicle membrane. Cell Biol Int Rep 13, 1063-1076.
38. Heuser, J., Katz, B., & Miledi, R. (1971). Structural and functional changes of frog neuromuscular junctions in high calcium solutions. Proc R Soc Lond B Biol Sci 178, 407-415.
39. Heuser, J. E., & Reese, T. S. (1973). Evidence for recycling of synaptic vesicle membrane during transmitter release at the frog neuromuscular junction. J Cell Biol 57, 315-344.
40. Jung, N., & Haucke, V. (2007). Clathrin-mediated endocytosis at synapses. Traffi c 8, 1129-1136.
41. Katz, B., & Miledi, R. (1965). Release of acetylcholine from a nerve terminal by electric pulses of variable strength and duration. Nature 207, 1097-1098.
42. Katz, B., & Miledi, R. (1969). Spontaneous and evoked activity of motor nerve endings in calcium Ringer. J Physiol 203, 689-706.
43. Kawasaki, F., Mattiuz, A. M., & Ordway, R. W. (1998). Synaptic physiology and ultrastructure in comatose mutants defi ne an in vivo role for NSF in neurotransmitter release. J Neurosci 18, 10241-10249.
44. Kelly, L. E., & Phillips, A. M. (2005). Molecular and genetic characterization of the interactions between the Drosophila stoned-B protein and DAP-160 (intersectin). Biochem J 388, 195-204.
45. Kidokoro, Y. (2003). Roles of SNARE proteins and synaptotagmin I in synaptic transmission: Studies at the Drosophila neuromuscular synapse. Neurosignals 12, 13-30.
46. Kidokoro, Y. (2006). Vesicle traffi cking and recycling at the neuromuscular junction: Two pathways for endocytosis. Int Rev Neurobiol 75, 145-164.
47. Kitamoto, T. (2001). Conditional modifi cation of behavior in Drosophila by targeted expression of a temperature-sensitive shibire allele in defi ned neurons. J Neurobiol 47, 81-92.
48. Koenig, J. H., & Ikeda, K. (1990). Transformational process of the endosomal compartment in nephrocytes of Drosophila melanogaster . Cell Tissue Res 262, 233-244.
49. 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.
50. Koh, T. W., Verstreken, P., & Bellen, H. J. (2004). Dap160/ intersectin acts as a stabilizing scaffold required for synaptic development and vesicle endocytosis. Neuron 43, 193-205.
51. Kosaka, T., & Ikeda, K. (1983). Possible temperature-dependent blockage of synaptic vesicle recycling induced by a single gene mutation in Drosophila . J Neurobiol 14, 207-225.
52. Krishnan, K. S., Rikhy, R., Rao, S., Shivalkar, M., Mosko, M., Narayanan, R., Etter, P., Estes, P. S., & Ramaswami, M. (2001). Nucleoside diphosphate kinase, a source of GTP, is required for dynamin-dependent synaptic vesicle recycling. Neuron 30, 197-210.
53. Leventis, P. A., Chow, B. M., Stewart, B. A., Iyengar, B., Campos, A. R., & Boulianne, G. L. (2001). Drosophila Amphiphysin is a post-synaptic protein required for normal locomotion but not endocytosis. Traffi c 2, 839-850.
54. 2+- triggered fusion and recycling of synaptic vesicles in vivo. J Neurosci 21, 1421-1433.
55. Littleton, J. T., Stern, M., Schulze, K., Perin, M., & Bellen, H. J. (1993). Mutational analysis of Drosophila synaptotagmin demonstrates its essential role in Ca(2+ )-activated neurotransmitter release. Cell 74, 1125-1134.
56. Loughney, K., Kreber, R., & Ganetzky, B. (1989). Molecular analysis of the para locus, a sodium channel gene in Drosophila . Cell 58, 1143-1154.
57. Majumder, R. (2009). Mechanism of endocytosis: Genetic and molecular studies. In DBS , vol. Ph.D. ed., pp. 76-91. Mumbai: Tata Institute of Fundamental Research.
58. Majumdar, A., Ramagiri, S., & Rikhy, R. (2006). Drosophila homologue of Eps15 is essential for synaptic vesicle recycling. Exp Cell Res 312, 2288-2298.
59. Marie, B., Sweeney, S. T., Poskanzer, K. E., Roos, J., Kelly, R. B., & Davis, G. W. (2004). Dap160/intersectin scaffolds the periactive zone to achieve high-fi delity endocytosis and normal synaptic growth. Neuron 43, 207-219.
60. Marks, B., Stowell, M. H., Vallis, Y., Mills, I. G., Gibson, A., Hopkins, C. R., & McMahon, H. T. (2001). GTPase activity of dynamin and resulting conformation change are essential for endocytosis. Nature 410, 231-235.
61. Martina, J. A., Bonangelino, C. J., Aguilar, R. C., & Bonifacino, J. S. (2001). Stonin 2: An adaptor-like protein that interacts with components of the endocytic machinery. J Cell Biol 153, 1111-1120.
62. Massol, R. H., Boll, W., Griffin, A. M., & Kirchhausen, T. (2006). A burst of auxilin recruitment determines the onset of clathrin-coated vesicle uncoating. Proc Natl Acad Sci U S A 103, 10265-10270.
63. Mayor, S., & Pagano, R. E. (2007). Pathways of clathrinindependent endocytosis. Nat Rev Mol Cell Biol 8, 603-612.
64. Merrifield, C. J., Feldman, M. E., Wan, L., & Almers, W. (2002). Imaging actin and dynamin recruitment during invagination of single clathrin-coated pits. Nat Cell Biol 4, 691-698.
65. Mishra, S. K., Hawryluk, M. J., Brett, T. J., Keyel, P. A., Dupin, A. L., Jha, A., Heuser, J. E., Fremont, D. H., & Traub, L. M. (2004). Dual engagement regulation of protein interactions with the AP-2 adaptor alpha appendage. J Biol Chem 279, 46191-46203.
66. Mizuno, N., Jao, C. C., Langen, R., & Steven, A. C. (2010). Multiple modes of endophilin-mediated conversion of lipid vesicles into coated tubes: Implications for synaptic endocytosis. J Biol Chem 285(30), 23351-23358.
67. Mohrmann, R., Matthies, H. J., Woodruff, E., 3rd, & Broadie, K. (2008). Stoned B mediates sorting of integral synaptic vesicle proteins. Neuroscience 153, 1048-1063.
68. Morgan, J. R., Prasad, K., Jin, S., Augustine, G. J., & Lafer, E. M. (2003). Eps15 homology domain-NPF motif interactions regulate clathrin coat assembly during synaptic vesicle recycling. J Biol Chem 278, 33583-33592.
69. Motley, A., Bright, N. A., Seaman, M. N., & Robinson, M. S. (2003). Clathrin-mediated endocytosis in AP-2-depleted cells. J Cell Biol 162, 909-918.
70. Obar, R. A., Collins, C. A., Hammarback, J. A., Shpetner, H. S., & Vallee, R. B. (1990). Molecular cloning of the microtubuleassociated mechanochemical enzyme dynamin reveals homology with a new family of GTP-binding proteins. Nature 347, 256-261.
71. Pallanck, L., Ordway, R. W., Ramaswami, M., Chi, W. Y., Krishnan, K. S., & Ganetzky, B. (1995). Distinct roles for N -ethylmaleimide-sensitive fusion protein (NSF) suggested by the identifi cation of a second Drosophila NSF homolog. J Biol Chem 270, 18742-18744.
72. Paumet, F., Rahimian, V., & Rothman, J. E. (2004). The specifi city of SNARE-dependent fusion is encoded in the SNARE motif. Proc Natl Acad Sci U S A 101, 3376-3380.
73. Peter, B. J., Kent, H. M., Mills, I. G., Vallis, Y., Butler, P. J., Evans, P. R., & McMahon, H. T. (2004). BAR domains as sensors of membrane curvature: The amphiphysin BAR structure. Science 303, 495-499.
74. Phillips, A. M., Smith, M., Ramaswami, M., & Kelly, L. E. (2000). The products of the Drosophila stoned locus interact with synaptic vesicles via synaptotagmin. J Neurosci 20, 8254-8261.
75. Poodry, C. A., & Edgar, L. (1979). Reversible alteration in the neuromuscular junctions of Drosophila melanogaster bearing a temperature-sensitive mutation, shibire. J Cell Biol 81, 520-527.
76. Poodry, C. A., Hall, L., & Suzuki, D. T. (1973). Developmental properties of Shibire: A pleiotropic mutation affecting larval and adult locomotion and development. Dev Biol 32, 373-386.
77. Ramaswami, M., Krishnan, K. S., & Kelly, R. B. (1994). Intermediates in synaptic vesicle recycling revealed by optical imaging of Drosophila neuromuscular junctions. Neuron 13, 363-375.
78. Ramaswami, M., Rao, S., van der Bliek, A., Kelly, R. B., & Krishnan, K. S. (1993). Genetic studies on dynamin function in Drosophila . J Neurogenet 9, 73-87.
79. Rao, S. (1997). Mutations affecting synaptic transmission in Drosophila melanogaster . In Department of Biological Sciences, Tata Institute of Fundamental Research , vol. MSc ed., pp. 74-85. Mumbai: The University of Bombay.
80. Rikhy, R. (2003). Genetic and Cell Biological Studies of Synaptic Vesicle Recycling in Drosophila melanogaster. In Department of Biological Sciences, Tata Institute of Fundamental Research, vol. Ph.D.ed., pp.82-96. Mumbai:The University of Bombay.
81. Rikhy, R., Kumar, V., Mittal, R., & Krishnan, K. S. (2002). Endophilin is critically required for synapse formation and function in Drosophila melanogaster . J Neurosci 22, 7478-7484.
82. Rikhy, R., Kamat, S., Ramagiri, S., Sriram, V., & Krishnan, K. S. (2007). Mutations in dynamin-related protein result in gross changes in mitochondrial morphology and affect synaptic vesicle recycling at the Drosophila neuromuscular junction. Genes Brain Behav 6, 42-53.
83. Rikhy, R., Ramaswami, M., & Krishnan, K. S. (2003). A temperature-sensitive allele of Drosophila sesB reveals acute functions for the mitochondrial adenine nucleotide translocase in synaptic transmission and dynamin regulation. Genetics 165, 1243-1253.
84. Ringstad, N., Gad, H., Low, P., Di Paolo, G., Brodin, L., Shupliakov, O., & De Camilli, P. (1999). Endophilin/SH3p4 is required for the transition from early to late stages in clathrin-mediated synaptic vesicle endocytosis. Neuron 24, 143-154.
85. Robinson, M. S., & Bonifacino, J. S. (2001). Adaptor-related proteins. Curr Opin Cell Biol 13, 444-453.
86. Robinson, P. J., Sontag, J. M., Liu, J. P., Fykse, E. M., Slaughter, C., McMahon, H., & Sudhof, T. C. (1993). Dynamin GTPase regulated by protein kinase C phosphorylation in nerve terminals. Nature 365, 163-166.
87. Roth, T. F., & Porter, K. R. (1964). Yolk protein uptake in the oocyte of the mosquito Aedes aegypti L. J Cell Biol 20, 313-332.
88. Rothman, J. E., & Warren, G. (1994). Implications of the SNARE hypothesis for intracellular membrane topology and dynamics. Curr Biol 4, 220-233.
89. Roux, A., Uyhazi, K., Frost, A., & De Camilli, P. (2006). GTPdependent twisting of dynamin implicates constriction and tension in membrane fi ssion. Nature 441, 528-531.
90. Rumpf, J., Simon, B., Jung, N., Maritzen, T., Haucke, V., Sattler, M., & Groemping, Y. (2008). Structure of the Eps15-stonin2 complex provides a molecular explanation for EH-domain ligand specifi city. EMBO J 27, 558-569.
91. Ryan, T. A. (2006). A pre-synaptic to-do list for coupling exocytosis to endocytosis. Curr Opin Cell Biol 18, 416-421.
92. Salcini, A. E., Chen, H., Iannolo, G., De Camilli, P., & Di Fiore, P. P. (1999). Epidermal growth factor pathway substrate 15, Eps15. Int J Biochem Cell Biol 31, 805-809.
93. Salcini, A. E., Hilliard, M. A., Croce, A., Arbucci, S., Luzzi, P., Tacchetti, C., Daniell, L., De Camilli, P., Pelicci, P. G., Di Fiore, P. P., et al. (2001). The Eps15 C. elegans homologue EHS-1 is implicated in synaptic vesicle recycling. Nat Cell Biol 3, 755-760.
94. Sanyal, S., Basole, A., & Krishnan, K. S. (1999). Phenotypic interaction between temperature-sensitive paralytic mutants comatose and paralytic suggests a role for N -ethylmaleimidesensitive fusion factor in synaptic vesicle cycling in Drosophila . J Neurosci 19, RC47, 1-5.
95. Sanyal, S., Tolar, L. A., Pallanck, L., & Krishnan, K. S. (2001). Genetic interaction between shibire and comatose mutations in Drosophila suggest a role for snap-receptor complex assembly and disassembly for maintenance of synaptic vesicle cycling. Neurosci Lett 311, 21-24.
96. Schmid, E. M., Ford, M. G., Burtey, A., Praefcke, G. J., Peak-Chew, S. Y., Mills, I. G., Benmerah, A., & McMahon, H. T. (2006). Role of the AP2 beta-appendage hub in recruiting partners for clathrin-coated vesicle assembly. PLoS Biol 4, e262.
97. Schmid, S. L. (1997). Clathrin-coated vesicle formation and protein sorting: An integrated process. Annu Rev Biochem 66, 511-548.
98. Schmidt, A., Wolde, M., Thiele, C., Fest, W., Kratzin, H., Podtelejnikov, A. V., Witke, W., Huttner, W. B., & Soling, H. D. (1999). Endophilin I mediates synaptic vesicle formation by transfer of arachidonate to lysophosphatidic acid. Nature 401, 133-141.
99. Sengar, A. S., Wang, W., Bishay, J., Cohen, S., & Egan, S. E. (1999). The EH and SH3 domain Ese proteins regulate endocytosis by linking to dynamin and Eps15. EMBO J 18, 1159-1171.
100. Sever, S., Muhlberg, A. B., & Schmid, S. L. (1999). Impairment of dynamin ' s GAP domain stimulates receptor-mediated endocytosis. Nature 398, 481-486.
101. Shpetner, H. S., & Vallee, R. B. (1989). Identifi cation of dynamin, a novel mechanochemical enzyme that mediates interactions between microtubules. Cell 59, 421-432.
102. Siddiqi, O., & Benzer, S. (1976). Neurophysiological defects in temperature-sensitive paralytic mutants of Drosophila melanogaster . Proc Natl Acad Sci U S A 73, 3253-3257.
103. Sollner, T., Bennett, M. K., Whiteheart, S. W., Scheller, R. H., & Rothman, J. E. (1993). A protein assembly-disassembly pathway in vitro that may correspond to sequential steps of synaptic vesicle docking, activation, and fusion. Cell 75, 409-418.
104. Stimson, D. T., Estes, P. S., Rao, S., Krishnan, K. S., Kelly, L. E., & Ramaswami, M. (2001). Drosophila stoned proteins regulate the rate and fidelity of synaptic vesicle internalization. J Neurosci 21, 3034-3044.
105. Stimson, D. T., Estes, P. S., Smith, M., Kelly, L. E., & Ramaswami, M. (1998). A product of the Drosophila stoned locus regulates neurotransmitter release. J Neurosci 18, 9638-9649.
106. Stowell, M. H., Marks, B., Wigge, P., & McMahon, H. T. (1999). Nucleotide-dependent conformational changes in dynamin: Evidence for a mechanochemical molecular spring. Nat Cell Biol 1, 27-32.
107. Sudhof, T. C. (2004). The synaptic vesicle cycle. Annu Rev Neurosci 27, 509-547.
108. Sudhof, T. C., & Rothman, J. E. (2009). Membrane fusion: Grappling with SNARE and SM proteins. Science 323, 474-477.
109. Suzuki, D. T., Grigliatti, T., & Williamson, R. (1971). Temperaturesensitive mutations in Drosophila melanogaster . VII. A mutation (para-ts) causing reversible adult paralysis. Proc Natl Acad Sci U S A 68, 890-893.
110. Sweitzer, S. M., & Hinshaw, J. E. (1998). Dynamin undergoes a GTP-dependent conformational change causing vesiculation. Cell 93, 1021-1029.
111. Takei, K., McPherson, P. S., Schmid, S. L., & De Camilli, P. (1995). Tubular membrane invaginations coated by dynamin rings are induced by GTP-gamma S in nerve terminals. Nature 374, 186-190.
112. Takei, K., Yoshida, Y., & Yamada, H. (2005). Regulatory mechanisms of dynamin-dependent endocytosis. J Biochem 137, 243-247.
113. Tsuboi, T., Terakawa, S., Scalettar, B. A., Fantus, C., Roder, J., & Jeromin, A. (2002). Sweeping model of dynamin activity. Visualization of coupling between exocytosis and endocytosis under an evanescent wave microscope with green fl uorescent proteins. J Biol Chem 277, 15957-15961.
114. van der Bliek, A. M., & Meyerowitz, E. M. (1991). Dynamin-like protein encoded by the Drosophila shibire gene associated with vesicular traffi c. Nature 351, 411-414.
115. Verstreken, P., Kjaerulff, O., Lloyd, T. E., Atkinson, R., Zhou, Y., Meinertzhagen, I. A., & Bellen, H. J. (2002). Endophilin mutations block clathrin-mediated endocytosis but not neurotransmitter release. Cell 109, 101-112.
116. VijayRaghavan, K. (1995). Synaptic vesicle recycling intermediates revealed. Bioessays 17, 195-198.
117. von Gersdorff, H., & Matthews, G. (1994). Dynamics of synaptic vesicle fusion and membrane retrieval in synaptic terminals. Nature 367, 735-739.
118. Wang, Z. W., Saifee, O., Nonet, M. L., & Salkoff, L. (2001). SLO-1 potassium channels control quantal content of neurotransmitter release at the C. elegans neuromuscular junction. Neuron 32, 867-881.
119. Woolworth, J. A., Nallamothu, G., & Hsu, T. (2009). The Drosophila metastasis suppressor gene Nm23 homolog, awd, regulates epithelial integrity during oogenesis. Mol Cell Biol 29, 4679-4690.
120. Wu, L. G., Ryan, T. A., & Lagnado, L. (2007). Modes of vesicle retrieval at ribbon synapses, calyx-type synapses, and small central synapses. J Neurosci 27, 11793-11802.
121. Yoshida, Y., Kinuta, M., Abe, T., Liang, S., Araki, K., Cremona, O., Di Paolo, G., Moriyama, Y., Yasuda, T., De Camilli, P., et al. (2004). The stimulatory action of amphiphysin on dynamin function is dependent on lipid bilayer curvature. EMBO J 23, 3483-3491.
122. Zenisek, D., Steyer, J. A., & Almers, W. (2000). Transport, capture and exocytosis of single synaptic vesicles at active zones. Nature 406, 849-854.
123. Zhang, B., Koh, Y. H., Beckstead, R. B., Budnik, V., Ganetzky, B., & Bellen, H. J. (1998). Synaptic vesicle size and number are regulated by a clathrin adaptor protein required for endocytosis. Neuron 21, 1465-1475.
124. Zhang, B., & Zelhof, A. C. (2002). Amphiphysins: Raising the BAR for synaptic vesicle recycling and membrane dynamics. Bin-Amphiphysin-Rvsp. Traffi c 3, 452-460.