Protein sorting in the synaptic vesicle life cycle

Progress in Neurobiology

Volumn 80, Issue 4, 2006, Pages 177-217

  Bonanomi, Dario ^a   Benfenati, Fabio ^b,c   Valtorta, Flavia ^a,d  

^a VITA SALUTE SAN RAFFAELE UNIVERSITY   (Italy)

^b The Italian Institute   (Italy)

^c UNIVERSITY OF GENOA   (Italy)

^d ISTITUTO ITALIANO DI TECNOLOGIA   (Italy)

Author keywords

Adaptor protein complexes; Exo endocytosis; Membrane traffic; Neurotransmission; PC12 cells; Phosphorylation; Secretory pathway; Synaptic vesicle pools; Synaptic like microvesicles

Indexed keywords

CARRIER PROTEIN; CLATHRIDINE; GLUTAMATE DECARBOXYLASE 65; PADGEM PROTEIN; PHOSPHATIDYLINOSITIDE; SYNAPTOBREVIN 2; SYNAPTOPHYSIN; SYNAPTOTAGMIN;

CELL MEMBRANE; ENDOCYTOSIS; ENDOSOME; EXOCYTOSIS; HUMAN; LIFE CYCLE; LIFESPAN; MOLECULAR MECHANICS; NERVE CELL DIFFERENTIATION; NERVE ENDING; NERVE GROWTH; NEUROTRANSMITTER RELEASE; NONHUMAN; PRIORITY JOURNAL; PROTEIN ASSEMBLY; PROTEIN FUNCTION; PROTEIN LIPID INTERACTION; PROTEIN MODIFICATION; PROTEIN MOTIF; PROTEIN PROCESSING; PROTEIN PROTEIN INTERACTION; PROTEIN TARGETING; PROTEIN TRANSPORT; REVIEW; SYNAPSE; SYNAPSE VESICLE; SYNAPTIC TRANSMISSION;

ANIMALS; AXONAL TRANSPORT; CELL MEMBRANE; ENDOSOMES; HUMANS; NERVE ENDINGS; NERVE TISSUE PROTEINS; NEURONS; SYNAPTIC VESICLES;

EID: 33751396164     PISSN: 03010082     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.pneurobio.2006.09.002     Document Type: Review

References (419)

1. Abraham C., Hutter H., Palfreyman M.T., Spatkowski G., Weimer R.M., Windoffer R., Jorgensen E.M., and Leube R.E. Synaptic tetraspan vesicle membrane proteins are conserved but not needed for synaptogenesis and neuronal function in Caenorhabditis elegans. Proc. Natl. Acad. Sci. U.S.A. 103 (2006) 8227-8232
2. Ahmari S.E., Buchanan J., and Smith S.J. Assembly of presynaptic active zones from cytoplasmic transport packets. Nat. Neurosci. 3 (2000) 445-451
3. Aikawa Y., and Martin T.F. ARF6 regulates a plasma membrane pool of phosphatidylinositol(4,5)bisphosphate required for regulated exocytosis. J. Cell Biol. 162 (2003) 647-659
4. Alder J., Lu B., Valtorta F., Greengard P., and Poo M.M. Calcium-dependent transmitter secretion reconstituted in Xenopus oocytes: requirement for synaptophysin. Science 257 (1992) 657-661
5. Altschuler Y., Liu S., Katz L., Tang K., Hardy S., Brodsky F., Apodaca G., and Mostov K. ADP-ribosylation factor 6 and endocytosis at the apical surface of Madin-Darby canine kidney cells. J. Cell Biol. 147 (1999) 7-12
6. Antonov I., Chang S., Zakharenko S., and Popov S.V. Distribution of neurotransmitter secretion in growing axons. Neuroscience 90 (1999) 975-984
7. Aoyagi K., Sugaya T., Umeda M., Yamamoto S., Terakawa S., and Takahashi M. The activation of exocytotic sites by the formation of phosphatidylinositol 4,5-bisphosphate microdomains at syntaxin clusters. J. Biol. Chem. 280 (2005) 17346-17352
8. Aravanis A.M., Pyle J.L., Harata N.C., and Tsien R.W. Imaging single synaptic vesicles undergoing repeated fusion events: kissing, running, and kissing again. Neuropharmacology 45 (2003) 797-813
9. Aravanis A.M., Pyle J.L., and Tsien R.W. Single synaptic vesicles fusing transiently and successively without loss of identity. Nature 423 (2003) 643-647
10. Bacci A., Coco S., Pravettoni E., Schenk U., Armano S., Frassoni C., Verderio C., De Camilli P., and Matteoli M. Chronic blockade of glutamate receptors enhances presynaptic release and downregulates the interaction between synaptophysin-synaptobrevin-vesicle-associated membrane protein 2. J. Neurosci. 21 (2001) 6588-6596
11. Baitinger C., and Willard M. Axonal transport of synapsin I-like proteins in rabbit retinal ganglion cells. J. Neurosci. 7 (1987) 3723-3735
12. Baldelli P., Fassio A., Corradi A., Cremona O., Valtorta F., and Benfenati F. Synapsins and neuroexocytosis: recent views from functional studies on synapsin null mutant mice. Arch. Ital. Biol. 143 (2005) 113-126
13. 2+-triggered exocytosis. J. Neurophysiol. 94 (2005) 1888-1903
14. Bauerfeind R., Regnier-Vigouroux A., Flatmark T., and Huttner W.B. Selective storage of acetylcholine, but not catecholamines, in neuroendocrine synaptic-like microvesicles of early endosomal origin. Neuron 11 (1993) 105-121
15. Bauerfeind R., Jelinek R., Hellwig A., and Huttner W.B. Neurosecretory vesicles can be hybrids of synaptic vesicles and secretory granules. Proc. Natl. Acad. Sci. U.S.A. 92 (1995) 7342-7346
16. Beaumont V., Llobet A., and Lagnado L. Expansion of calcium microdomains regulates fast exocytosis at a ribbon synapse. Proc. Natl. Acad. Sci. U.S.A. 102 (2005) 10700-10705
17. Belfort G.M., and Kandror K.V. Cellugyrin and synaptogyrin facilitate targeting of synaptophysin to a ubiquitous synaptic vesicle-sized compartment in PC12 cells. J. Biol. Chem. 278 (2003) 47971-47978
18. Belfort G.M., Bakirtzi K., and Kandror K.V. Cellugyrin induces biogenesis of synaptic-like microvesicles in PC12 cells. J. Biol. Chem. 280 (2005) 7262-7272
19. 2+/calmodulin-dependent protein kinase II is a binding protein for synapsin I. Nature 359 (1992) 417-420
20. Bennett M.K., Calakos N., Kreiner T., and Scheller R.H. Synaptic vesicle membrane proteins interact to form a multimeric complex. J. Cell Biol. 116 (1992) 761-775
21. Berridge M.J. Inositol trisphosphate and calcium signalling. Nature 361 (1993) 315-325
22. Betz W.J., and Henkel A.W. Okadaic acid disrupts clusters of synaptic vesicles in frog motor nerve terminals. J. Cell Biol. 124 (1994) 843-854
23. Bhattacharya S., Stewart B.A., Niemeyer B.A., Burgess R.W., McCabe B.D., Lin P., Boulianne G., O'Kane C.J., and Schwarz T.L. Members of the synaptobrevin/vesicle-associated membrane protein (VAMP) family in Drosophila are functionally interchangeable in vivo for neurotransmitter release and cell viability. Proc. Natl. Acad. Sci. U.S.A. 99 (2002) 13867-13872
24. Blagoveshchenskaya A.D., and Cutler D.F. Sorting to synaptic-like microvesicles from early and late endosomes requires overlapping but not identical targeting signals. Mol. Biol. Cell 11 (2000) 1801-1814
25. Blagoveshchenskaya A.D., Hewitt E.W., and Cutler D.F. Di-leucine signals mediate targeting of tyrosinase and synaptotagmin to synaptic-like microvesicles within PC12 cells. Mol. Biol. Cell 10 (1999) 3979-3990
26. Blagoveshchenskaya A.D., Hewitt E.W., and Cutler D.F. A complex web of signal-dependent trafficking underlies the triorganellar distribution of P-selectin in neuroendocrine PC12 cells. J. Cell Biol. 145 (1999) 1419-1433
27. Blondeau F., Ritter B., Allaire P.D., Wasiak S., Girard M., Hussain N.K., Angers A., Legendre-Guillemin V., Roy L., Boismenu D., Kearney R.E., Bell A.W., Bergeron J.J., and McPherson P.S. Tandem MS analysis of brain clathrin-coated vesicles reveals their critical involvement in synaptic vesicle recycling. Proc. Natl. Acad. Sci. U.S.A. 101 (2004) 3833-3838
28. Blumstein J., Faundez V., Nakatsu F., Saito T., Ohno H., and Kelly R.B. The neuronal form of adaptor protein-3 is required for synaptic vesicle formation from endosomes. J. Neurosci. 21 (2001) 8034-8042
29. Bollmann J.H., Sakmann B., and Borst J.G. Calcium sensitivity of glutamate release in a calyx-type terminal. Science 289 (2000) 953-957
30. Bonanomi D., Pennuto M., Rigoni M., Rossetto O., Montecucco C., and Valtorta F. Taipoxin induces synaptic vesicle exocytosis and disrupts the interaction of synaptophysin I with VAMP2. Mol. Pharmacol. 67 (2005) 1901-1908
31. Bonanomi D., Menegon A., Miccio A., Ferrari G., Corradi A., Kao H.T., Benfenati F., and Valtorta F. Phosphorylation of synapsin I by cAMP-dependent protein kinase controls synaptic vesicle dynamics in developing neurons. J. Neurosci. 25 (2005) 7299-7308
32. Bonifacino J.S., and Traub L.M. Signals for sorting of transmembrane proteins to endosomes and lysosomes. Annu. Rev. Biochem. 72 (2003) 395-447
33. Bonzelius F., Herman G.A., Cardone M.H., Mostov K.E., and Kelly R.B. The polymeric immunoglobulin receptor accumulates in specialized endosomes but not synaptic vesicles within the neurites of transfected neuroendocrine PC12 cells. J. Cell Biol. 127 (1994) 1603-1616
34. Booj S., Goldstein M., Fischer-Colbrie R., and Dahlstrom A. Calcitonin gene-related peptide and chromogranin A: presence and intra-axonal transport in lumbar motor neurons in the rat, a comparison with synaptic vesicle antigens in immunohistochemical studies. Neuroscience 30 (1989) 479-501
35. Breckenridge W.C., Morgan I.G., Zanetta J.P., and Vincendon G. Adult rat brain synaptic vesicles II. Lipid composition. Biochim. Biophys. Acta 320 (1973) 681-686
36. Brose N., Hofmann K., Hata Y., and Sudhof T.C. Mammalian homologues of Caenorhabditis elegans unc-13 gene define novel family of C2-domain proteins. J. Biol. Chem. 270 (1995) 25273-25280
37. Brown F.D., Rozelle A.L., Yin H.L., Balla T., and Donaldson J.G. Phosphatidylinositol 4,5-bisphosphate and Arf6-regulated membrane traffic. J. Cell Biol. 154 (2001) 1007-1017
38. Bucci C., Parton R.G., Mather I.H., Stunnenberg H., Simons K., Hoflack B., and Zerial M. The small GTPase rab5 functions as a regulatory factor in the early endocytic pathway. Cell 70 (1992) 715-728
39. Calakos N., and Scheller R.H. Vesicle-associated membrane protein and synaptophysin are associated on the synaptic vesicle. J. Biol. Chem. 269 (1994) 24534-24537
40. Cameron P.L., Südhof T.C., Jahn R., and De Camilli P. Colocalization of synaptophysin with transferrin receptors: implications for synaptic vesicle biogenesis. J. Cell Biol. 115 (1991) 151-164
41. Carrion-Vazquez M., Fernandez A.M., Chowen J., and Nieto-Sampedro M. Brain Ac39/physophilin: cloning, coexpression and colocalization with synaptophysin. Eur. J. Neurosci. 10 (1998) 1153-1166
42. Ceccarelli B., and Hurlbut W.P. The effects of prolonged repetitive stimulation in hemicholinium on the frog neuromuscular junction. J. Physiol. 247 (1975) 163-188
43. Ceccarelli B., Hurlbut W.P., and Mauro A. Depletion of vesicles from frog neuromuscular junctions by prolonged tetanic stimulation. J. Cell Biol. 54 (1972) 30-38
44. Ceccarelli B., Hurlbut W.P., and Mauro A. Turnover of transmitter and synaptic vesicles at the frog neuromuscular junction. J. Cell Biol. 57 (1973) 499-524
45. Chamberlain L.H., Burgoyne R.D., and Gould G.W. SNARE proteins are highly enriched in lipid rafts in PC12 cells: implications for the spatial control of exocytosis. Proc. Natl. Acad. Sci. U.S.A. 98 (2001) 5619-5624
46. Chen Y.J., Zhang P., Egelman E.H., and Hinshaw J.E. The stalk region of dynamin drives the constriction of dynamin tubes. Nat. Struct. Mol. Biol. 11 (2004) 574-575
47. Chi P., Greengard P., and Ryan T.A. Synapsin dispersion and reclustering during synaptic activity. Nat. Neurosci. 4 (2001) 1187-1193
48. Chi P., Greengard P., and Ryan T.A. Synaptic vesicle mobilization is regulated by distinct synapsin I phosphorylation pathways at different frequencies. Neuron 38 (2003) 69-78
49. Chou J.H., and Jahn R. Binding of Rab3A to synaptic vesicles. J. Biol. Chem. 275 (2000) 9433-9440
50. Chow I., and Poo M.M. Release of acetylcholine from embryonic neurons upon contact with muscle cell. J. Neurosci. 5 (1985) 1076-1082
51. Christoforidis S., McBride H.M., Burgoyne R.D., and Zerial M. The Rab5 effector EEA1 is a core component of endosome docking. Nature 397 (1999) 621-625
52. 2+-dependent manner. In vitro characteristics and possible significance. J. Biol. Chem. 273 (1998) 10240-10248
53. Clift-O'Grady L., Linstedt A.D., Lowe A.W., Grote E., and Kelly R.B. Biogenesis of synaptic vesicle-like structures in a pheochromocytoma cell line PC-12. J. Cell Biol. 110 (1990) 1693-1703
54. Coco S., Raposo G., Martinez S., Fontaine J.J., Takamori S., Zahraoui A., Jahn R., Matteoli M., Louvard D., and Galli T. Subcellular localization of tetanus neurotoxin-insensitive vesicle-associated membrane protein (VAMP)/VAMP7 in neuronal cells: evidence for a novel membrane compartment. J. Neurosci. 19 (1999) 9803-9812
55. Conner S.D., and Schmid S.L. Regulated portals of entry into the cell. Nature 422 (2003) 37-44
56. Cousin M.A., Malladi C.S., Tan T.C., Raymond C.R., Smillie K.J., and Robinson P.J. Synapsin I-associated phosphatidylinositol 3-kinase mediates synaptic vesicle delivery to the readily releasable pool. J. Biol. Chem. 278 (2003) 29065-29071
57. Cremona O., and De Camilli P. Synaptic vesicle endocytosis. Curr. Opin. Neurobiol. 7 (1997) 323-330
58. Cremona O., and De Camilli P. Phosphoinositides in membrane traffic at the synapse. J. Cell. Sci. 114 (2001) 1041-1052
59. 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., McCormick D.A., and De Camilli P. Essential role of phosphoinositide metabolism in synaptic vesicle recycling. Cell 99 (1999) 179-188
60. Croft B.G., Fortin G.D., Corera A.T., Edwards R.H., Beaudet A., Trudeau L.E., and Fon E.A. Normal biogenesis and cycling of empty synaptic vesicles in dopamine neurons of vesicular monoamine transporter 2 knockout mice. Mol. Biol. Cell 16 (2005) 306-315
61. 2+-dependent formation of a dynamin-synaptophysin complex: potential role in synaptic vesicle endocytosis. J. Biol. Chem. 277 (2002) 9010-9015
62. Daly C., Sugimori M., Moreira J.E., Ziff E.B., and Llinas R. Synaptophysin regulates clathrin-independent endocytosis of synaptic vesicles. Proc. Natl. Acad. Sci. U.S.A. 97 (2000) 6120-6125
63. Dan Y., and Poo M.M. Quantal transmitter secretion from myocytes loaded with acetylcholine. Nature 359 (1992) 733-736
64. Danino D., Moon K.H., and Hinshaw J.E. Rapid constriction of lipid bilayers by the mechanochemical enzyme dynamin. J. Struct. Biol. 147 (2004) 259-267
65. Darcy K.J., Staras K., Collinson L.M., and Goda Y. Constitutive sharing of recycling synaptic vesicles between presynaptic boutons. Nat. Neurosci. 9 (2006) 315-321
66. De Camilli P., and Takei K. Molecular mechanisms in synaptic vesicle endocytosis and recycling. Neuron 16 (1996) 481-486
67. De Camilli P., Cameron R., and Greengard P. Synapsin I (protein I), a nerve terminal-specific phosphoprotein I. Its general distribution in synapses of the central and peripheral nervous system demonstrated by immunofluorescence in frozen and plastic sections. J. Cell Biol. 96 (1983) 1337-1354
68. de Hoop M.J., Huber L.A., Stenmark H., Williamson E., Zerial M., Parton R.G., and Dotti C.G. The involvement of the small GTP-binding protein Rab5a in neuronal endocytosis. Neuron 13 (1994) 11-22
69. de Lange R.P., de Roos A.D., and Borst J.G. Two modes of vesicle recycling in the rat calyx of Held. J. Neurosci. 23 (2003) 10164-10173
70. de Wit H., Lichtenstein Y., Geuze H.J., Kelly R.B., van der Sluijs P., and Klumperman J. Synaptic vesicles form by budding from tubular extensions of sorting endosomes in PC12 cells. Mol. Biol. Cell 10 (1999) 4163-4176
71. de Wit H., Lichtenstein Y., Kelly R.B., Geuze H.J., Klumperman J., and van der Sluijs P. Rab4 regulates formation of synaptic-like microvesicles from early endosomes in PC12 cells. Mol. Biol. Cell 12 (2001) 3703-3715
72. Deak F., Schoch S., Liu X., Südhof T.C., and Kavalali E.T. Synaptobrevin is essential for fast synaptic-vesicle endocytosis. Nat. Cell Biol. 6 (2004) 1102-1108
73. Deak F., Shin O.H., Kavalali E.T., and Sudhof T.C. Structural determinants of synaptobrevin 2 function in synaptic vesicle fusion. J. Neurosci. 26 (2006) 6668-6676
74. 2+- and SNARE-independent release of GABA and glutamate prior to synapse formation. Neuron 36 (2002) 1051-1061
75. Desnos C., Clift-O'Grady L., and Kelly R.B. Biogenesis of synaptic vesicles in vitro. J. Cell Biol. 130 (1995) 1041-1049
76. Di Paolo G., Moskowitz H.S., Gipson K., Wenk M.R., Voronov S., Obayashi M., Flavell R., Fitzsimonds R.M., Ryan T.A., and De Camilli P. Impaired PtdIns(4,5)P2 synthesis in nerve terminals produces defects in synaptic vesicle trafficking. Nature 431 (2004) 415-422
77. Dickman D.K., Horne J.A., Meinertzhagen I.A., and Schwarz T.L. A slowed classical pathway rather than kiss-and-run mediates endocytosis at synapses lacking synaptojanin and endophilin. Cell 123 (2005) 521-533
78. Diril M.K., Wienisch M., Jung N., Klingauf J., and Haucke V. Stonin 2 is an AP2-dependent endocytic sorting adaptor for synaptotagmin internalization and recycling. Dev. Cell. 10 (2006) 233-244
79. Dittman J.S., and Kaplan J.M. Factors regulating the abundance and localization of synaptobrevin in the plasma membrane. Proc. Natl. Acad. Sci. U.S.A. 103 (2006) 11399-11404
80. Dotti C.G., and Simons K. Polarized sorting of viral glycoproteins to the axon and dendrites of hippocampal neurons in culture. Cell 62 (1990) 63-72
81. Duncan R.R., Greaves J., Wiegand U.K., Matskevich I., Bodammer G., Apps D.K., Shipston M.J., and Chow R.H. Functional and spatial segregation of secretory vesicle pools according to vesicle age. Nature 422 (2003) 176-180
82. Eaton B.A., Haugwitz M., Lau D., and Moore H.P. Biogenesis of regulated exocytotic carriers in neuroendocrine cells. J. Neurosci. 20 (2000) 7334-7344
83. Eberhard D.A., Cooper C.L., Low M.G., and Holz R.W. Evidence that the inositol phospholipids are necessary for exocytosis Loss of inositol phospholipids and inhibition of secretion in permeabilized cells caused by a bacterial phospholipase C and removal of ATP. Biochem. J. 268 (1990) 15-25
84. Edeling M.A., Smith C., and Owen D. Life of a clathrin coat: insights from clathrin and AP structures. Nat. Rev. Mol. Cell Biol. 7 (2006) 32-44
85. Edelmann L., Hanson P.I., Chapman E.R., and Jahn R. Synaptobrevin binding to synaptophysin: a potential mechanism for controlling the exocytotic fusion machine. EMBO J. 14 (1995) 224-231
86. Eshkind L.G., and Leube R.E. Mice lacking synaptophysin reproduce and form typical synaptic vesicles. Cell Tissue Res. 282 (1995) 423-433
87. Esser L., Wang C.R., Hosaka M., Smagula C.S., Südhof T.C., and Deisenhofer J. Synapsin I is structurally similar to ATP-utilizing enzymes. EMBO J. 17 (1998) 977-984
88. Evers J., Laser M., Sun Y.A., Xie Z.P., and Poo M.M. Studies of nerve-muscle interactions in Xenopus cell culture: analysis of early synaptic currents. J. Neurosci. 9 (1989) 1523-1539
89. Fassio A., Merlo D., Mapelli J., Menegon A., Corradi A., Mete M., Zappettini S., Bonanno G., Valtorta F., D'Angelo E., and Benfenati F. The synapsin domain E accelerates the exo-endocytotic cycle of synaptic vesicles in cerebellar purkinje cells. J. Cell. Sci. 119 (2006) 4257-4268
90. Faundez V.V., and Kelly R.B. The AP3 complex required for endosomal synaptic vesicle biogenesis is associated with a casein kinase Ialpha-like isoform. Mol. Biol. Cell 11 (2000) 2591-2604
91. Faundez V., Horng J.T., and Kelly R.B. ADP ribosylation factor 1 is required for synaptic vesicle budding in PC12 cells. J. Cell Biol. 138 (1997) 505-515
92. Faundez V., Horng J.T., and Kelly R.B. A function for the AP3 coat complex in synaptic vesicle formation from endosomes. Cell 93 (1998) 423-432
93. Favre D., Scarfone E., Di Gioia G., De Camilli P., and Dememes D. Presence of synapsin I in afferent and efferent nerve endings of vestibular sensory epithelia. Brain Res. 384 (1986) 379-382
94. Feany M.B., Yee A.G., Delvy M.L., and Buckley K.M. The synaptic vesicle proteins SV2, synaptotagmin and synaptophysin are sorted to separate cellular compartments in CHO fibroblasts. J. Cell Biol. 123 (1993) 575-584
95. Feng J., Chi P., Blanpied T.A., Xu Y., Magarinos A.M., Ferreira A., Takahashi R.H., Kao H.T., McEwen B.S., Ryan T.A., Augustine G.J., and Greengard P. Regulation of neurotransmitter release by synapsin III. J. Neurosci. 22 (2002) 4372-4380
96. Fergestad T., and Broadie K. Interaction of stoned and synaptotagmin in synaptic vesicle endocytosis. J. Neurosci. 21 (2001) 1218-1227
97. Fernandez-Alfonso T., Kwan R., and Ryan T.A. Synaptic vesicles interchange their membrane proteins with a large surface reservoir during recycling. Neuron 51 (2006) 179-186
98. Ferreira A., Kao H.T., Feng J., Rapoport M., and Greengard P. Synapsin III: developmental expression, subcellular localization, and role in axon formation. J. Neurosci. 20 (2000) 3736-3744
99. Fesce R., and Meldolesi J. Peeping at the vesicle kiss. Nat. Cell Biol. 1 (1999) E3-E4
100. Fesce R., Grohovaz F., Valtorta F., and Meldolesi J. Neurotransmitter release: fusion or 'kiss-and-run'?. Trends Cell Biol. 4 (1994) 1-4
101. Finger T.E., Womble M., Kinnamon J.C., and Ueda T. Synapsin I-like immunoreactivity in nerve fibers associated with lingual taste buds of the rat. J. Comp. Neurol. 292 (1990) 283-290
102. Fischer von Mollard G., Südhof T.C., and Jahn R. A small GTP-binding protein dissociates from synaptic vesicles during exocytosis. Nature 349 (1991) 79-81
103. Fischer von Mollard G., Stahl B., Walch-Solimena C., Takei K., Daniels L., Khoklatchev A., De Camilli P., Südhof T.C., and Jahn R. Localization of Rab5 to synaptic vesicles identifies endosomal intermediate in synaptic vesicle recycling pathway. Eur. J. Cell Biol. 65 (1994) 319-326
104. Fiumara F., Onofri F., Benfenati F., Montarolo P.G., and Ghirardi M. Intracellular injection of synapsin I induces neurotransmitter release in C1 neurons of Helix pomatia contacting a wrong target. Neuroscience 104 (2001) 271-280
105. Fiumara F., Giovedi S., Menegon A., Milanese C., Merlo D., Montarolo P.G., Valtorta F., Benfenati F., and Ghirardi M. Phosphorylation by cAMP-dependent protein kinase is essential for synapsin-induced enhancement of neurotransmitter release in invertebrate neurons. J. Cell. Sci. 117 (2004) 5145-5154
106. Fletcher T.L., Cameron P., De Camilli P., and Banker G. The distribution of synapsin I and synaptophysin in hippocampal neurons developing in culture. J. Neurosci. 11 (1991) 1617-1626
107. Foletti D.L., Blitzer J.T., and Scheller R.H. Physiological modulation of rabphilin phosphorylation. J. Neurosci. 21 (2001) 5473-5483
108. Ford M.G., Pearse B.M., Higgins M.K., Vallis Y., Owen D.J., Gibson A., Hopkins C.R., Evans P.R., and McMahon H.T. Simultaneous binding of PtdIns(4,5)P2 and clathrin by AP180 in the nucleation of clathrin lattices on membranes. Science 291 (2001) 1051-1055
109. Fremeau Jr. R.T., Troyer M.D., Pahner I., Nygaard G.O., Tran C.H., Reimer R.J., Bellocchio E.E., Fortin D., Storm-Mathisen J., and Edwards R.H. The expression of vesicular glutamate transporters defines two classes of excitatory synapse. Neuron 31 (2001) 247-260
110. Fremeau Jr. R.T., Kam K., Qureshi T., Johnson J., Copenhagen D.R., Storm-Mathisen J., Chaudhry F.A., Nicoll R.A., and Edwards R.H. Vesicular glutamate transporters 1 and 2 target to functionally distinct synaptic release sites. Science 304 (2004) 1815-1819
111. Friedman H.V., Bresler T., Garner C.C., and Ziv N.E. Assembly of new individual excitatory synapses: time course and temporal order of synaptic molecule recruitment. Neuron 27 (2000) 57-69
112. 2+-triggered synaptic vesicle exocytosis and clathrin-mediated endocytosis at a central synapse. Neuron 21 (1998) 607-616
113. Gaidarov I., and Keen J.H. Phosphoinositide-AP2 interactions required for targeting to plasma membrane clathrin-coated pits. J. Cell Biol. 146 (1999) 755-764
114. Galli T., McPherson P.S., and De Camilli P. The V0 sector of the V-ATPase, synaptobrevin, and synaptophysin are associated on synaptic vesicles in a Triton X-100-resistant, freeze-thawing sensitive, complex. J. Biol. Chem. 271 (1996) 2193-2198
115. Gao X.B., and van den Pol A.N. GABA release from mouse axonal growth cones. J. Physiol. 523 Pt 3 (2000) 629-637
116. Gaspary H.L., Wang W., and Richerson G.B. Carrier-mediated GABA release activates GABA receptors on hippocampal neurons. J. Neurophysiol. 80 (1998) 270-281
117. Geppert M., and Südhof T.C. RAB3 and synaptotagmin: the yin and yang of synaptic membrane fusion. Annu. Rev. Neurosci. 21 (1998) 75-95
118. Geppert M., Bolshakov V.Y., Siegelbaum S.A., Takei K., De Camilli P., Hammer R.E., and Südhof T.C. The role of Rab3A in neurotransmitter release. Nature 369 (1994) 493-497
119. 2+ sensor for transmitter release at a central synapse. Cell 79 (1994) 717-727
120. Geppert M., Ullrich B., Green D.G., Takei K., Daniels L., De Camilli P., Südhof T.C., and Hammer R.E. Synaptic targeting domains of synapsin I revealed by transgenic expression in photoreceptor cells. EMBO J. 13 (1994) 3720-3727
121. Geppert M., Goda Y., Stevens C.F., and Südhof T.C. The small GTP-binding protein Rab3A regulates a late step in synaptic vesicle fusion. Nature 387 (1997) 810-814
122. Gerber S.H., Garcia J., Rizo J., and Sudhof T.C. An unusual C(2)-domain in the active-zone protein piccolo: implications for Ca(2+) regulation of neurotransmitter release. EMBO J. 20 (2001) 1605-1619
123. Giovedi S., Vaccaro P., Valtorta F., Darchen F., Greengard P., Cesareni G., and Benfenati F. Synapsin is a novel Rab3 effector protein on small synaptic vesicles. I. Identification and characterization of the synapsin I-Rab3 interactions in vitro and in intact nerve terminals. J. Biol. Chem. 279 (2004) 43760-43768
124. Giovedi S., Darchen F., Valtorta F., Greengard P., and Benfenati F. Synapsin is a novel Rab3 effector protein on small synaptic vesicles. II. Functional effects of the Rab3A-synapsin I interaction. J. Biol. Chem. 279 (2004) 43769-43779
125. Girod R., Popov S., Alder J., Zheng J.Q., Lohof A., and Poo M.M. Spontaneous quantal transmitter secretion from myocytes and fibroblasts: comparison with neuronal secretion. J. Neurosci. 15 (1995) 2826-2838
126. Gitler D., Xu Y., Kao H.T., Lin D., Lim S., Feng J., Greengard P., and Augustine G.J. Molecular determinants of synapsin targeting to presynaptic terminals. J. Neurosci. 24 (2004) 3711-3720
127. Goldstein L.S. Do disorders of movement cause movement disorders and dementia?. Neuron 40 (2003) 415-425
128. Gonzalez-Gaitan M., and Jackle H. Role of Drosophila alpha-adaptin in presynaptic vesicle recycling. Cell 88 (1997) 767-776
129. Grass I., Thiel S., Honing S., and Haucke V. Recognition of a basic AP2 binding motif within the C2B domain of synaptotagmin is dependent on multimerization. J. Biol. Chem. 279 (2004) 54872-54880
130. Greengard P., Valtorta F., Czernik A.J., and Benfenati F. Synaptic vesicle phosphoproteins and regulation of synaptic function. Science 259 (1993) 780-785
131. Grishanin R.N., Kowalchyk J.A., Klenchin V.A., Ann K., Earles C.A., Chapman E.R., Gerona R.R., and Martin T.F. CAPS acts at a prefusion step in dense-core vesicle exocytosis as a PIP2 binding protein. Neuron 43 (2004) 551-562
132. Grote E., and Kelly R.B. Endocytosis of VAMP is facilitated by a synaptic vesicle targeting signal. J. Cell Biol. 132 (1996) 537-547
133. Grote E., Hao J.C., Bennett M.K., and Kelly R.B. A targeting signal in VAMP regulating transport to synaptic vesicles. Cell 81 (1995) 581-589
134. Guo J., Wenk M.R., Pellegrini L., Onofri F., Benfenati F., and De Camilli P. Phosphatidylinositol 4-kinase type IIalpha is responsible for the phosphatidylinositol 4-kinase activity associated with synaptic vesicles. Proc. Natl. Acad. Sci. U.S.A. 100 (2003) 3995-4000
135. Han W., Rhee J.S., Maximov A., Lao Y., Mashimo T., Rosenmund C., and Südhof T.C. N-glycosylation is essential for vesicular targeting of synaptotagmin 1. Neuron 41 (2004) 85-99
136. Hannah M.J., Schmidt A.A., and Huttner W.B. Synaptic vesicle biogenesis. Annu. Rev. Cell Dev. Biol. 15 (1999) 733-798
137. Harata N., Pyle J.L., Aravanis A.M., Mozhayeva M., Kavalali E.T., and Tsien R.W. Limited numbers of recycling vesicles in small CNS nerve terminals: implications for neural signaling and vesicular cycling. Trends Neurosci. 24 (2001) 637-643
138. Harata N.C., Aravanis A.M., and Tsien R.W. Kiss-and-run and full-collapse fusion as modes of exo-endocytosis in neurosecretion. J. Neurochem. 97 (2006) 1546-1570
139. Harata N.C., Choi S., Pyle J.L., Aravanis A.M., and Tsien R.W. Frequency-dependent kinetics and prevalence of kiss-and-run and reuse at hippocampal synapses studied with novel quenching methods. Neuron 49 (2006) 243-256
140. Haucke V., and De Camilli P. AP2 recruitment to synaptotagmin stimulated by tyrosine-based endocytic motifs. Science 285 (1999) 1268-1271
141. Haucke V., Wenk M.R., Chapman E.R., Farsad K., and De Camilli P. Dual interaction of synaptotagmin with mu2- and alpha-adaptin facilitates clathrin-coated pit nucleation. EMBO J. 19 (2000) 6011-6019
142. Hay J.C., and Martin T.F. Phosphatidylinositol transfer protein required for ATP-dependent priming of Ca(2+)-activated secretion. Nature 366 (1993) 572-575
143. Hay J.C., Fisette P.L., Jenkins G.H., Fukami K., Takenawa T., Anderson R.A., and Martin T.F. ATP-dependent inositide phosphorylation required for Ca(2+)-activated secretion. Nature 374 (1995) 173-177
144. Hessler N.A., Shirke A.M., and Malinow R. The probability of transmitter release at a mammalian central synapse. Nature 366 (1993) 569-572
145. Heuser J.E., and Reese T.S. Evidence for recycling of synaptic vesicle membrane during transmitter release at the frog neuromuscular junction. J. Cell Biol. 57 (1973) 315-344
146. Hilfiker S., Schweizer F.E., Kao H.T., Czernik A.J., Greengard P., and Augustine G.J. Two sites of action for synapsin domain E in regulating neurotransmitter release. Nat. Neurosci. 1 (1998) 29-35
147. Hilfiker S., Pieribone V.A., Czernik A.J., Kao H.T., Augustine G.J., and Greengard P. Synapsins as regulators of neurotransmitter release. Philos. Trans. R. Soc. Lond. B. Biol. Sci. 354 (1999) 269-279
148. Hilfiker S., Benfenati F., Doussau F., Nairn A.C., Czernik A.J., Augustine G.J., and Greengard P. Structural domains involved in the regulation of transmitter release by synapsins. J. Neurosci. 25 (2005) 2658-2669
149. Hinshaw J.E. Dynamin and its role in membrane fission. Annu. Rev. Cell Dev. Biol. 16 (2000) 483-519
150. Holt M., Cooke A., Wu M.M., and Lagnado L. Bulk membrane retrieval in the synaptic terminal of retinal bipolar cells. J. Neurosci. 23 (2003) 1329-1339
151. Honda A., Nogami M., Yokozeki T., Yamazaki M., Nakamura H., Watanabe H., Kawamoto K., Nakayama K., Morris A.J., Frohman M.A., and Kanaho Y. Phosphatidylinositol 4-phosphate 5-kinase alpha is a downstream effector of the small G protein ARF6 in membrane ruffle formation. Cell 99 (1999) 521-532
152. Honing S., Ricotta D., Krauss M., Spate K., Spolaore B., Motley A., Robinson M., Robinson C., Haucke V., and Owen D.J. Phosphatidylinositol-(4,5)-bisphosphate regulates sorting signal recognition by the clathrin-associated adaptor complex AP2. Mol. Cell 18 (2005) 519-531
153. Horikawa H.P., Kneussel M., El Far O., and Betz H. Interaction of synaptophysin with the AP1 adaptor protein gamma-adaptin. Mol. Cell. Neurosci. 21 (2002) 454-462
154. Hosaka M., and Südhof T.C. Homo- and heterodimerization of synapsins. J. Biol. Chem. 274 (1999) 16747-16753
155. Hosaka M., Hammer R.E., and Südhof T.C. A phospho-switch controls the dynamic association of synapsins with synaptic vesicles. Neuron 24 (1999) 377-387
156. Hume R.I., Role L.W., and Fischbach G.D. Acetylcholine release from growth cones detected with patches of acetylcholine receptor-rich membranes. Nature 305 (1983) 632-634
157. Huttner W.B., and Schmidt A. Lipids, lipid modification and lipid-protein interaction in membrane budding and fission-insights from the roles of endophilin A1 and synaptophysin in synaptic vesicle endocytosis. Curr. Opin. Neurobiol. 10 (2000) 543-551
158. Huttner W.B., Schiebler W., Greengard P., and De Camilli P. Synapsin I (protein I), a nerve terminal-specific phosphoprotein III. Its association with synaptic vesicles studied in a highly purified synaptic vesicle preparation. J. Cell Biol. 96 (1983) 1374-1388
159. Ikonen E. Roles of lipid rafts in membrane transport. Curr. Opin. Cell Biol. 13 (2001) 470-477
160. Jacob R., and Naim H.Y. Apical membrane proteins are transported in distinct vesicular carriers. Curr. Biol. 11 (2001) 1444-1450
161. Jahn R., Schiebler W., Ouimet C., and Greengard P. A 38,000-dalton membrane protein (p38) present in synaptic vesicles. Proc. Natl. Acad. Sci. U.S.A. 82 (1985) 4137-4141
162. Jarousse N., and Kelly R.B. The AP2 binding site of synaptotagmin 1 is not an internalization signal but a regulator of endocytosis. J. Cell Biol. 154 (2001) 857-866
163. Jia J., Lamer S., Schuemann M., Schmidt M., Krause E., and Haucke V. Quantitative proteomic analysis of detergent-resistant membranes from chemical synapses: Evidence for cholesterol as spatial organizer of synaptic vesicle cycling. Mol. Cell. Proteom. (2006)
164. Jockusch W.J., Praefcke G.J., McMahon H.T., and Lagnado L. Clathrin-dependent and clathrin-independent retrieval of synaptic vesicles in retinal bipolar cells. Neuron 46 (2005) 869-878
165. Johnston P.A., and Südhof T.C. The multisubunit structure of synaptophysin relationship between disulfide bonding and homo-oligomerization. J. Biol. Chem. 265 (1990) 8869-8873
166. Johnston P.A., Cameron P.L., Stukenbrok H., Jahn R., De Camilli P., and Südhof T.C. Synaptophysin is targeted to similar microvesicles in CHO and PC12 cells. EMBO J. 8 (1989) 2863-2872
167. Jorgensen E.M., Hartwieg E., Schuske K., Nonet M.L., Jin Y., and Horvitz H.R. Defective recycling of synaptic vesicles in synaptotagmin mutants of Caenorhabditis elegans. Nature 378 (1995) 196-199
168. Kaether C., Skehel P., and Dotti C.G. Axonal membrane proteins are transported in distinct carriers: a two-color video microscopy study in cultured hippocampal neurons. Mol. Biol. Cell 11 (2000) 1213-1224
169. Kamal A., Stokin G.B., Yang Z., Xia C.H., and Goldstein L.S. Axonal transport of amyloid precursor protein is mediated by direct binding to the kinesin light chain subunit of kinesin-I. Neuron 28 (2000) 449-459
170. Kanaani J., el-Husseini A., Aguilera-Moreno A., Diacovo J.M., Bredt D.S., and Baekkeskov S. A combination of three distinct trafficking signals mediates axonal targeting and presynaptic clustering of GAD65. J. Cell Biol. 158 (2002) 1229-1238
171. Kanaani J., Diacovo M.J., El-Husseini A., Bredt D.S., and Baekkeskov S. Palmitoylation controls trafficking of GAD65 from Golgi membranes to axon-specific endosomes and a Rab5a-dependent pathway to presynaptic clusters. J. Cell. Sci. 117 (2004) 2001-2013
172. Kang R., Swayze R., Lise M.F., Gerrow K., Mullard A., Honer W.G., and El-Husseini A. Presynaptic trafficking of synaptotagmin I is regulated by protein palmitoylation. J. Biol. Chem. 279 (2004) 50524-50536
173. Kantheti P., Qiao X., Diaz M.E., Peden A.A., Meyer G.E., Carskadon S.L., Kapfhamer D., Sufalko D., Robinson M.S., Noebels J.L., and Burmeister M. Mutation in AP3 delta in the mocha mouse links endosomal transport to storage deficiency in platelets, melanosomes, and synaptic vesicles. Neuron 21 (1998) 111-122
174. Keller P., and Simons K. Cholesterol is required for surface transport of influenza virus hemagglutinin. J. Cell Biol. 140 (1998) 1357-1367
175. Keller P., Toomre D., Diaz E., White J., and Simons K. Multicolour imaging of post-Golgi sorting and trafficking in live cells. Nat. Cell Biol. 3 (2001) 140-149
176. Kelly R.B. Secretion. A question of endosomes. Nature 364 (1993) 487-488
177. Kielland A., Erisir A., Walaas S.I., and Heggelund P. Synapsin utilization differs among functional classes of synapses on thalamocortical cells. J. Neurosci. 26 (2006) 5786-5793
178. Kim M.H., and Hersh L.B. The vesicular acetylcholine transporter interacts with clathrin-associated adaptor complexes AP1 and AP2. J. Biol. Chem. 279 (2004) 12580-12587
179. Kim P.K., Hollerbach C., Trimble W.S., Leber B., and Andrews D.W. Identification of the endoplasmic reticulum targeting signal in vesicle-associated membrane proteins. J. Biol. Chem. 274 (1999) 36876-36882
180. Kim W.T., Chang S., Daniell L., Cremona O., Di Paolo G., and De Camilli P. Delayed reentry of recycling vesicles into the fusion-competent synaptic vesicle pool in synaptojanin 1 knockout mice. Proc. Natl. Acad. Sci. U.S.A. 99 (2002) 17143-17148
181. Kishida S., Shirataki H., Sasaki T., Kato M., Kaibuchi K., and Takai Y. Rab3A GTPase-activating protein-inhibiting activity of Rabphilin-3A, a putative Rab3A target protein. J. Biol. Chem. 268 (1993) 22259-22261
182. Klumperman J., Hille A., Veenendaal T., Oorschot V., Stoorvogel W., von Figura K., and Geuze H.J. Differences in the endosomal distributions of the two mannose 6-phosphate receptors. J. Cell Biol. 121 (1993) 997-1010
183. Knight D., Mann D.L., Jackson V.M., Trout S.J., Cunnane T.C., and Lavidis N.A. Correlation of non-uniform protein expression with variation in transmitter release probability. Synapse 55 (2005) 110-121
184. Koenig J.H., and Ikeda K. Disappearance and reformation of synaptic vesicle membrane upon transmitter release observed under reversible blockage of membrane retrieval. J. Neurosci. 9 (1989) 3844-3860
185. Koenig J.H., and Ikeda K. Synaptic vesicles have two distinct recycling pathways. J. Cell Biol. 135 (1996) 797-808
186. Koh T.W., Verstreken P., and Bellen H.J. Dap160/intersectin acts as a stabilizing scaffold required for synaptic development and vesicle endocytosis. Neuron 43 (2004) 193-205
187. Krantz D.E., Waites C., Oorschot V., Liu Y., Wilson R.I., Tan P.K., Klumperman J., and Edwards R.H. A phosphorylation site regulates sorting of the vesicular acetylcholine transporter to dense core vesicles. J. Cell Biol. 149 (2000) 379-396
188. Kraszewski K., Mundigl O., Daniell L., Verderio C., Matteoli M., and De Camilli P. Synaptic vesicle dynamics in living cultured hippocampal neurons visualized with CY3-conjugated antibodies directed against the lumenal domain of synaptotagmin. J. Neurosci. 15 (1995) 4328-4342
189. Krauss M., Kinuta M., Wenk M.R., De Camilli P., Takei K., and Haucke V. ARF6 stimulates clathrin/AP2 recruitment to synaptic membranes by activating phosphatidylinositol phosphate kinase type Igamma. J. Cell Biol. 162 (2003) 113-124
190. Kuromi H., and Kidokoro Y. Two distinct pools of synaptic vesicles in single presynaptic boutons in a temperature-sensitive Drosophila mutant, shibire. Neuron 20 (1998) 917-925
191. 2+ at the Drosophila synapse. Neuron 35 (2002) 333-343
192. Kutay U., Hartmann E., and Rapoport T.A. A class of membrane proteins with a C-terminal anchor. Trends Cell Biol. 3 (1993) 72-75
193. Kutay U., Ahnert-Hilger G., Hartmann E., Wiedenmann B., and Rapoport T.A. Transport route for synaptobrevin via a novel pathway of insertion into the endoplasmic reticulum membrane. EMBO J. 14 (1995) 217-223
194. Lang T., Bruns D., Wenzel D., Riedel D., Holroyd P., Thiele C., and Jahn R. SNAREs are concentrated in cholesterol-dependent clusters that define docking and fusion sites for exocytosis. EMBO J. 20 (2001) 2202-2213
195. Laux T., Fukami K., Thelen M., Golub T., Frey D., and Caroni P. GAP43, MARCKS, and CAP23 modulate PI(4,5)P(2) at plasmalemmal rafts, and regulate cell cortex actin dynamics through a common mechanism. J. Cell Biol. 149 (2000) 1455-1472
196. Ledesma M.D., Simons K., and Dotti C.G. Neuronal polarity: essential role of protein-lipid complexes in axonal sorting. Proc. Natl. Acad. Sci. U.S.A. 95 (1998) 3966-3971
197. Ledesma M.D., Brugger B., Bunning C., Wieland F.T., and Dotti C.G. Maturation of the axonal plasma membrane requires upregulation of sphingomyelin synthesis and formation of protein-lipid complexes. EMBO J. 18 (1999) 1761-1771
198. Lee S.Y., Wenk M.R., Kim Y., Nairn A.C., and De Camilli P. Regulation of synaptojanin 1 by cyclin-dependent kinase 5 at synapses. Proc. Natl. Acad. Sci. U.S.A. 101 (2004) 546-551
199. Leenders A.G., Lopes da Silva F.H., Ghijsen W.E., and Verhage M. Rab3a is involved in transport of synaptic vesicles to the active zone in mouse brain nerve terminals. Mol. Biol. Cell 12 (2001) 3095-3102
200. Leenders A.G., Scholten G., de Lange R.P., Lopes da Silva F.H., and Ghijsen W.E. Sequential changes in synaptic vesicle pools and endosome-like organelles during depolarization near the active zone of central nerve terminals. Neuroscience 109 (2002) 195-206
201. Lemmon M.A. Phosphoinositide recognition domains. Traffic 4 (2003) 201-213
202. Leoni C., Menegon A., Benfenati F., Toniolo D., Pennuto M., and Valtorta F. Neurite extension occurs in the absence of regulated exocytosis in PC12 subclones. Mol. Biol. Cell 10 (1999) 2919-2931
203. Leube R.E., Wiedenmann B., and Franke W.W. Topogenesis and sorting of synaptophysin: synthesis of a synaptic vesicle protein from a gene transfected into non-neuroendocrine cells. Cell 59 (1989) 433-446
204. Leube R.E., Leimer U., Grund C., Franke W.W., Harth N., and Wiedenmann B. Sorting of synaptophysin into special vesicles in non-neuroendocrine epithelial cells. J. Cell Biol. 127 (1994) 1589-1601
205. Li J.Y., and Dahlstrom A. Axonal transport of synaptic vesicle proteins in the rat optic nerve. J. Neurobiol. 32 (1997) 237-250
206. Li Z., and Murthy V.N. Visualizing postendocytic traffic of synaptic vesicles at hippocampal synapses. Neuron 31 (2001) 593-605
207. Li C., Ullrich B., Zhang J.Z., Anderson R.G., Brose N., and Südhof T.C. Ca(2+)-dependent and -independent activities of neural and non-neural synaptotagmins. Nature 375 (1995) 594-599
208. Li J.Y., Jahn R., and Dahlstrom A. Rab3a, a small GTP-binding protein, undergoes fast anterograde transport but not retrograde transport in neurons. Eur. J. Cell Biol. 67 (1995) 297-307
209. Li L., Chin L.S., Shupliakov O., Brodin L., Sihra T.S., Hvalby O., Jensen V., Zheng D., McNamara J.O., and Greengard P. Impairment of synaptic vesicle clustering and of synaptic transmission, and increased seizure propensity, in synapsin I-deficient mice. Proc. Natl. Acad. Sci. U.S.A. 92 (1995) 9235-9239
210. Li J.Y., Jahn R., Hou X.E., Kling-Petersen A., and Dahlstrom A. Distribution of Rab3a in rat nervous system: comparison with other synaptic vesicle proteins and neuropeptides. Brain Res. 706 (1996) 103-112
211. Li Z., Burrone J., Tyler W.J., Hartman K.N., Albeanu D.F., and Murthy V.N. Synaptic vesicle recycling studied in transgenic mice expressing synaptopHluorin. Proc. Natl. Acad. Sci. U.S.A. 102 (2005) 6131-6136
212. Lichtenstein Y., Desnos C., Faundez V., Kelly R.B., and Clift-O'Grady L. Vesiculation and sorting from PC12-derived endosomes in vitro. Proc. Natl. Acad. Sci. U.S.A. 95 (1998) 11223-11228
213. Linstedt A.D., and Kelly R.B. Synaptophysin is sorted from endocytotic markers in neuroendocrine PC12 cells but not transfected fibroblasts. Neuron 7 (1991) 309-317
214. Linstedt A.D., and Kelly R.B. Endocytosis of the synaptic vesicle protein, synaptophysin, requires the COOH-terminal tail. J. Physiol. (Paris) 85 (1991) 90-96
215. Littleton J.T., Serano T.L., Rubin G.M., Ganetzky B., and Chapman E.R. Synaptic function modulated by changes in the ratio of synaptotagmin I and IV. Nature 400 (1999) 757-760
216. 2+-triggered fusion and recycling of synaptic vesicles in vivo. J. Neurosci. 21 (2001) 1421-1433
217. Liu Y., and Edwards R.H. Differential localization of vesicular acetylcholine and monoamine transporters in PC12 cells but not CHO cells. J. Cell Biol. 139 (1997) 907-916
218. Liu G., and Tsien R.W. Properties of synaptic transmission at single hippocampal synaptic boutons. Nature 375 (1995) 404-408
219. Lu B., Greengard P., and Poo M.M. Exogenous synapsin I promotes functional maturation of developing neuromuscular synapses. Neuron 8 (1992) 521-529
220. Mandell J.W., Townes-Anderson E., Czernik A.J., Cameron R., Greengard P., and De Camilli P. Synapsins in the vertebrate retina: absence from ribbon synapses and heterogeneous distribution among conventional synapses. Neuron 5 (1990) 19-33
221. Mandell J.W., Czernik A.J., De Camilli P., Greengard P., and Townes-Anderson E. Differential expression of synapsins I and II among rat retinal synapses. J. Neurosci. 12 (1992) 1736-1749
222. Marquez-Sterling N.R., Lo A.C., Sisodia S.S., and Koo E.H. Trafficking of cell-surface beta-amyloid precursor protein: evidence that a sorting intermediate participates in synaptic vesicle recycling. J. Neurosci. 17 (1997) 140-151
223. Martina J.A., Bonangelino C.J., Aguilar R.C., and Bonifacino J.S. Stonin 2: an adaptor-like protein that interacts with components of the endocytic machinery. J. Cell Biol. 153 (2001) 1111-1120
224. Martinez-Arca S., Alberts P., Zahraoui A., Louvard D., and Galli T. Role of tetanus neurotoxin insensitive vesicle-associated membrane protein (TI-VAMP) in vesicular transport mediating neurite outgrowth. J. Cell Biol. 149 (2000) 889-900
225. Martinez-Arca S., Arold S., Rudge R., Laroche F., and Galli T. A mutant impaired in SNARE complex dissociation identifies the plasma membrane as first target of synaptobrevin 2. Traffic 5 (2004) 371-382
226. Marxen M., Volknandt W., and Zimmermann H. Endocytic vacuoles formed following a short pulse of K+-stimulation contain a plethora of presynaptic membrane proteins. Neuroscience 94 (1999) 985-996
227. Matteoli M., Takei K., Cameron R., Hurlbut P., Johnston P.A., Südhof T.C., Jahn R., and De Camilli P. Association of Rab3A with synaptic vesicles at late stages of the secretory pathway. J. Cell Biol. 115 (1991) 625-633
228. Matteoli M., Takei K., Perin M.S., Südhof T.C., and De Camilli P. Exo-endocytotic recycling of synaptic vesicles in developing processes of cultured hippocampal neurons. J. Cell Biol. 117 (1992) 849-861
229. Matteoli M., Coco S., Schenk U., and Verderio C. Vesicle turnover in developing neurons: how to build a presynaptic terminal. Trends Cell Biol. 14 (2004) 133-140
230. Matus-Leibovitch N., Nevo I., and Vogel Z. Differential distribution of synapsin IIa and IIb mRNAs in various brain structures and the effect of chronic morphine administration on the regional expression of these isoforms. Brain Res. Mol. Brain Res. 45 (1997) 301-316
231. Maycox P.R., Link E., Reetz A., Morris S.A., and Jahn R. Clathrin-coated vesicles in nervous tissue are involved primarily in synaptic vesicle recycling. J. Cell Biol. 118 (1992) 1379-1388
232. McKiernan C.J., Stabila P.F., and Macara I.G. Role of the Rab3A-binding domain in targeting of rabphilin-3A to vesicle membranes of PC12 cells. Mol. Cell Biol. 16 (1996) 4985-4995
233. McMahon H.T., Bolshakov V.Y., Janz R., Hammer R.E., Siegelbaum S.A., and Südhof T.C. Synaptophysin, a major synaptic vesicle protein, is not essential for neurotransmitter release. Proc. Natl. Acad. Sci. U.S.A. 93 (1996) 4760-4764
234. McPherson P.S., Garcia E.P., Slepnev V.I., David C., Zhang X., Grabs D., Sossin W.S., Bauerfeind R., Nemoto Y., and De Camilli P. A presynaptic inositol-5-phosphatase. Nature 379 (1996) 353-357
235. Meunier F.A., Osborne S.L., Hammond G.R., Cooke F.T., Parker P.J., Domin J., and Schiavo G. Phosphatidylinositol 3-kinase C2alpha is essential for ATP-dependent priming of neurosecretory granule exocytosis. Mol. Biol. Cell 16 (2005) 4841-4851
236. Micheva K.D., Buchanan J., Holz R.W., and Smith S.J. Retrograde regulation of synaptic vesicle endocytosis and recycling. Nat. Neurosci. 6 (2003) 925-932
237. Milosevic I., Sorensen J.B., Lang T., Krauss M., Nagy G., Haucke V., Jahn R., and Neher E. Plasmalemmal phosphatidylinositol-4,5-bisphosphate level regulates the releasable vesicle pool size in chromaffin cells. J. Neurosci. 25 (2005) 2557-2565
238. Mitchell S.J., and Ryan T.A. Syntaxin-1A is excluded from recycling synaptic vesicles at nerve terminals. J. Neurosci. 24 (2004) 4884-4888
239. Mohrmann R., Lessmann V., and Gottmann K. Developmental maturation of synaptic vesicle cycling as a distinctive feature of central glutamatergic synapses. Neuroscience 117 (2003) 7-18
240. Morgan J.R., Zhao X., Womack M., Prasad K., Augustine G.J., and Lafer E.M. A role for the clathrin assembly domain of AP180 in synaptic vesicle endocytosis. J. Neurosci. 19 (1999) 10201-10212
241. Morgenthaler F.D., Knott G.W., Floyd Sarria J.C., Wang X., Staple J.K., Catsicas S., and Hirling H. Morphological and molecular heterogeneity in release sites of single neurons. Eur. J. Neurosci. 17 (2003) 1365-1374
242. Morimoto T., Popov S., Buckley K.M., and Poo M.M. Calcium-dependent transmitter secretion from fibroblasts: modulation by synaptotagmin I. Neuron 15 (1995) 689-696
243. Morimoto K., Sato K., Sato S., Suemaru S., Sato T., Yamada N., and Hayabara T. Increases in mRNA levels for synapsin I but not synapsin II in the hippocampus of the rat kindling model of epilepsy. Seizure 7 (1998) 229-235
244. Moulder K.L., and Mennerick S. Reluctant vesicles contribute to the total readily releasable pool in glutamatergic hippocampal neurons. J. Neurosci. 25 (2005) 3842-3850
245. Moulder K.L., and Mennerick S. Synaptic vesicles: turning reluctance into action. Neuroscientist 12 (2006) 11-15
246. Mousavi S.A., Malerod L., Berg T., and Kjeken R. Clathrin-dependent endocytosis. Biochem. J. 377 (2004) 1-16
247. Mozhayeva M.G., Sara Y., Liu X., and Kavalali E.T. Development of vesicle pools during maturation of hippocampal synapses. J. Neurosci. 22 (2002) 654-665
248. Mundigl O., Matteoli M., Daniell L., Thomas-Reetz A., Metcalf A., Jahn R., and De Camilli P. Synaptic vesicle proteins and early endosomes in cultured hippocampal neurons: differential effects of brefeldin A in axon and dendrites. J. Cell Biol. 122 (1993) 1207-1221
249. Murthy V.N., and Stevens C.F. Synaptic vesicles retain their identity through the endocytic cycle. Nature 392 (1998) 497-501
250. Murthy M., Garza D., Scheller R.H., and Schwarz T.L. Mutations in the exocyst component Sec5 disrupt neuronal membrane traffic, but neurotransmitter release persists. Neuron 37 (2003) 433-447
251. Nakata T., Terada S., and Hirokawa N. Visualization of the dynamics of synaptic vesicle and plasma membrane proteins in living axons. J. Cell Biol. 140 (1998) 659-674
252. Nakatsu F., Okada M., Mori F., et al. Defective function of GABA-containing synaptic vesicles in mice lacking the AP3B clathrin adaptor. J. Cell Biol. 167 (2004) 293-302
253. Navone F., Jahn R., Di Gioia G., Stukenbrok H., Greengard P., and De Camilli P. Protein p38: an integral membrane protein specific for small vesicles of neurons and neuroendocrine cells. J. Cell Biol. 103 (1986) 2511-2527
254. Navone F., Di Gioia G., Jahn R., Browning M., Greengard P., and De Camilli P. Microvesicles of the neurohypophysis are biochemically related to small synaptic vesicles of presynaptic nerve terminals. J. Cell Biol. 109 (1989) 3425-3433
255. Neeb A., Koch H., Schurmann A., and Brose N. Direct interaction between the ARF-specific guanine nucleotide exchange factor msec7-1 and presynaptic Munc13-1. Eur. J. Cell Biol. 78 (1999) 533-538
256. Newman L.S., McKeever M.O., Okano H.J., and Darnell R.B. Beta-NAP, a cerebellar degeneration antigen, is a neuron-specific vesicle coat protein. Cell 82 (1995) 773-783
257. Nicholson-Tomishima K., and Ryan T.A. Kinetic efficiency of endocytosis at mammalian CNS synapses requires synaptotagmin I. Proc. Natl. Acad. Sci. U.S.A. 101 (2004) 16648-16652
258. Nirenberg M.J., Liu Y., Peter D., Edwards R.H., and Pickel V.M. The vesicular monoamine transporter 2 is present in small synaptic vesicles and preferentially localizes to large dense core vesicles in rat solitary tract nuclei. Proc. Natl. Acad. Sci. U.S.A. 92 (1995) 8773-8777
259. Noebels J.L., and Sidman R.L. Persistent hypersynchronization of neocortical neurons in the mocha mutant of mouse. J. Neurogenet. 6 (1989) 53-56
260. Nonet M.L., Holgado A.M., Brewer F., Serpe C.J., Norbeck B.A., Holleran J., Wei L., Hartwieg E., Jorgensen E.M., and Alfonso A. UNC-11, a Caenorhabditis elegans AP180 homologue, regulates the size and protein composition of synaptic vesicles. Mol. Biol. Cell 10 (1999) 2343-2360
261. Norcott J.P., Solari R., and Cutler D.F. Targeting of P-selectin to two regulated secretory organelles in PC12 cells. J. Cell Biol. 134 (1996) 1229-1240
262. Okada Y., Yamazaki H., Sekine-Aizawa Y., and Hirokawa N. The neuron-specific kinesin superfamily protein KIF1A is a unique monomeric motor for anterograde axonal transport of synaptic vesicle precursors. Cell 81 (1995) 769-780
263. Okamoto M., and Sudhof T.C. Mints Munc18-interacting proteins in synaptic vesicle exocytosis. J. Biol. Chem. 272 (1997) 31459-31464
264. Onofri F., Giovedi S., Kao H.T., Valtorta F., Borbone L.B., De Camilli P., Greengard P., and Benfenati F. Specificity of the binding of synapsin I to Src homology 3 domains. J. Biol. Chem. 275 (2000) 29857-29867
265. Onofri F., Giovedi S., Vaccaro P., Czernik A.J., Valtorta F., De Camilli P., Greengard P., and Benfenati F. Synapsin I interacts with c-Src and stimulates its tyrosine kinase activity. Proc. Natl. Acad. Sci. U.S.A. 94 (1997) 12168-12173
266. Osborne S.L., Herreros J., Bastiaens P.I., and Schiavo G. Calcium-dependent oligomerization of synaptotagmins I and II synaptotagmins I and II are localized on the same synaptic vesicle and heterodimerize in the presence of calcium. J. Biol. Chem. 274 (1999) 59-66
267. Osborne S.L., Wen P.J., and Meunier F.A. Phosphoinositide regulation of neuroexocytosis: adding to the complexity. J. Neurochem. 98 (2006) 336-342
268. Paillart C., Li J., Matthews G., and Sterling P. Endocytosis and vesicle recycling at a ribbon synapse. J. Neurosci. 23 (2003) 4092-4099
269. Pal A., Severin F., Lommer B., Shevchenko A., and Zerial M. Huntingtin-HAP40 complex is a novel Rab5 effector that regulates early endosome motility and is up-regulated in Huntington's disease. J. Cell Biol. 172 (2006) 605-618
270. Paladino S., Pocard T., Catino M.A., and Zurzolo C. GPI-anchored proteins are directly targeted to the apical surface in fully polarized MDCK cells. J. Cell Biol. 172 (2006) 1023-1034
271. Partoens P., Slembrouck D., Quatacker J., Baudhuin P., Courtoy P.J., and De Potter W.P. Retrieved constituents of large dense-cored vesicles and synaptic vesicles intermix in stimulation-induced early endosomes of noradrenergic neurons. J. Cell. Sci. 111 Pt 6 (1998) 681-689
272. Parton R.G., and Dotti C.G. Cell biology of neuronal endocytosis. J. Neurosci. Res. 36 (1993) 1-9
273. Parton R.G., Simons K., and Dotti C.G. Axonal and dendritic endocytic pathways in cultured neurons. J. Cell Biol. 119 (1992) 123-137
274. Pennuto M., Dunlap D., Contestabile A., Benfenati F., and Valtorta F. Fluorescence resonance energy transfer detection of synaptophysin I and vesicle-associated membrane protein 2 interactions during exocytosis from single live synapses. Mol. Biol. Cell 13 (2002) 2706-2717
275. Pennuto M., Bonanomi D., Benfenati F., and Valtorta F. Synaptophysin I controls the targeting of VAMP2/synaptobrevin II to synaptic vesicles. Mol. Biol. Cell 14 (2003) 4909-4919
276. Pfrieger F.W. Role of cholesterol in synapse formation and function. Biochim. Biophys. Acta 1610 (2003) 271-280
277. Polo-Parada L., Bose C.M., and Landmesser L.T. Alterations in transmission, vesicle dynamics, and transmitter release machinery at NCAM-deficient neuromuscular junctions. Neuron 32 (2001) 815-828
278. Popov S.V., and Poo M.M. Synaptotagmin: a calcium-sensitive inhibitor of exocytosis?. Cell 73 (1993) 1247-1249
279. Poskanzer K.E., and Davis G.W. Mobilization and fusion of a non-recycling pool of synaptic vesicles under conditions of endocytic blockade. Neuropharmacology 47 (2004) 714-723
280. Poskanzer K.E., Marek K.W., Sweeney S.T., and Davis G.W. Synaptotagmin I is necessary for compensatory synaptic vesicle endocytosis in vivo. Nature 426 (2003) 559-563
281. Poskanzer K.E., Fetter R.D., and Davis G.W. Discrete residues in the c(2)b domain of synaptotagmin I independently specify endocytic rate and synaptic vesicle size. Neuron 50 (2006) 49-62
282. Powelka A.M., and Buckley K.M. Expression of ARF6 mutants in neuroendocrine cells suggests a role for ARF6 in synaptic vesicle biogenesis. FEBS Lett. 501 (2001) 47-50
283. 2+-dependent interaction with the synaptobrevin-synaptophysin complex. J. Cell Biol. 137 (1997) 1589-1601
284. Prekeris R., Klumperman J., Chen Y.A., and Scheller R.H. Syntaxin 13 mediates cycling of plasma membrane proteins via tubulovesicular recycling endosomes. J. Cell Biol. 143 (1998) 957-971
285. Prekeris R., Foletti D.L., and Scheller R.H. Dynamics of tubulovesicular recycling endosomes in hippocampal neurons. J. Neurosci. 19 (1999) 10324-10337
286. Provoda C.J., Waring M.T., and Buckley K.M. Evidence for a primary endocytic vesicle involved in synaptic vesicle biogenesis. J. Biol. Chem. 275 (2000) 7004-7012
287. Rapoport I., Miyazaki M., Boll W., Duckworth B., Cantley L.C., Shoelson S., and Kirchhausen T. Regulatory interactions in the recognition of endocytic sorting signals by AP2 complexes. EMBO J. 16 (1997) 2240-2250
288. Regnier-Vigouroux A., Tooze S.A., and Huttner W.B. Newly synthesized synaptophysin is transported to synaptic-like microvesicles via constitutive secretory vesicles and the plasma membrane. EMBO J. 10 (1991) 3589-3601
289. Rehm H., Wiedenmann B., and Betz H. Molecular characterization of synaptophysin, a major calcium-binding protein of the synaptic vesicle membrane. EMBO J. 5 (1986) 535-541
290. 2+-dependent neurotransmitter release. Cell 104 (2001) 71-81
291. Reisinger C., Yelamanchili S.V., Hinz B., Mitter D., Becher A., Bigalke H., and Ahnert-Hilger G. The synaptophysin/synaptobrevin complex dissociates independently of neuroexocytosis. J. Neurochem. 90 (2004) 1-8
292. Rhee J.S., Betz A., Pyott S., Reim K., Varoqueaux F., Augustin I., Hesse D., Südhof T.C., Takahashi M., Rosenmund C., and Brose N. Beta phorbol ester- and diacylglycerol-induced augmentation of transmitter release is mediated by Munc13s and not by PKCs. Cell 108 (2002) 121-133
293. Richards D.A., Guatimosim C., Rizzoli S.O., and Betz W.J. Synaptic vesicle pools at the frog neuromuscular junction. Neuron 39 (2003) 529-541
294. Richards D.A., Rizzoli S.O., and Betz W.J. Effects of wortmannin and latrunculin A on slow endocytosis at the frog neuromuscular junction. J. Physiol. 557 (2004) 77-91
295. Ringstad N., Nemoto Y., and De Camilli P. The SH3p4/Sh3p8/SH3p13 protein family: binding partners for synaptojanin and dynamin via a Grb2-like Src homology 3 domain. Proc. Natl. Acad. Sci. U.S.A. 94 (1997) 8569-8574
296. Rizzoli S.O., and Betz W.J. The structural organization of the readily releasable pool of synaptic vesicles. Science 303 (2004) 2037-2039
297. Roos J., and Kelly R.B. The endocytic machinery in nerve terminals surrounds sites of exocytosis. Curr. Biol. 9 (1999) 1411-1414
298. Roos J., and Kelly R.B. Preassembly and transport of nerve terminals: a new concept of axonal transport. Nat. Neurosci. 3 (2000) 415-417
299. Rosahl T.W., Spillane D., Missler M., Herz J., Selig D.K., Wolff J.R., Hammer R.E., Malenka R.C., and Südhof T.C. Essential functions of synapsins I and II in synaptic vesicle regulation. Nature 375 (1995) 488-493
300. Rosenmund C., Clements J.D., and Westbrook G.L. Non-uniform probability of glutamate release at a hippocampal synapse. Science 262 (1993) 754-757
301. Roux A., Uyhazi K., Frost A., and De Camilli P. GTP-dependent twisting of dynamin implicates constriction and tension in membrane fission. Nature 441 (2006) 528-531
302. Ryan T.A., Reuter H., Wendland B., Schweizer F.E., Tsien R.W., and Smith S.J. The kinetics of synaptic vesicle recycling measured at single presynaptic boutons. Neuron 11 (1993) 713-724
303. Ryan T.A., Li L., Chin L.S., Greengard P., and Smith S.J. Synaptic vesicle recycling in synapsin I knock-out mice. J. Cell Biol. 134 (1996) 1219-1227
304. Sabo S.L., and McAllister A.K. Mobility and cycling of synaptic protein-containing vesicles in axonal growth cone filopodia. Nat. Neurosci. 6 (2003) 1264-1269
305. Sakane A., Manabe S., Ishizaki H., Tanaka-Okamoto M., Kiyokage E., Toida K., Yoshida T., Miyoshi J., Kamiya H., Takai Y., and Sasaki T. Rab3 GTPase-activating protein regulates synaptic transmission and plasticity through the inactivation of Rab3. Proc. Natl. Acad. Sci. U.S.A. 103 (2006) 10029-10034
306. Salaun C., Gould G.W., and Chamberlain L.H. Lipid raft association of SNARE proteins regulates exocytosis in PC12 cells. J. Biol. Chem. 280 (2005) 19449-19453
307. Salazar G., Love R., Styers M.L., Werner E., Peden A., Rodriguez S., Gearing M., Wainer B.H., and Faundez V. AP3-dependent mechanisms control the targeting of a chloride channel (ClC-3) in neuronal and non-neuronal cells. J. Biol. Chem. 279 (2004) 25430-25439
308. Salazar G., Love R., Werner E., Doucette M.M., Cheng S., Levey A., and Faundez V. The zinc transporter ZnT3 interacts with AP3 and it is preferentially targeted to a distinct synaptic vesicle subpopulation. Mol. Biol. Cell 15 (2004) 575-587
309. Salazar G., Craige B., Love R., Kalman D., and Faundez V. Vglut1 and ZnT3 co-targeting mechanisms regulate vesicular zinc stores in PC12 cells. J. Cell Sci. 118 (2005) 1911-1921
310. Salazar G., Craige B., Wainer B.H., Guo J., De Camilli P., and Faundez V. Phosphatidylinositol-4-kinase type II alpha is a component of adaptor protein-3-derived vesicles. Mol. Biol. Cell 16 (2005) 3692-3704
311. Salem N., Faundez V., Horng J.T., and Kelly R.B. A v-SNARE participates in synaptic vesicle formation mediated by the AP3 adaptor complex. Nat. Neurosci. 1 (1998) 551-556
312. Sampo B., Kaech S., Kunz S., and Banker G. Two distinct mechanisms target membrane proteins to the axonal surface. Neuron 37 (2003) 611-624
313. Sankaranarayanan S., and Ryan T.A. Calcium accelerates endocytosis of vSNAREs at hippocampal synapses. Nat. Neurosci. 4 (2001) 129-136
314. Santos M.S., Barbosa Jr. J., Veloso G.S., Ribeiro F., Kushmerick C., Gomez M.V., Ferguson S.S., Prado V.F., and Prado M.A. Trafficking of green fluorescent protein tagged-vesicular acetylcholine transporter to varicosities in a cholinergic cell line. J. Neurochem. 78 (2001) 1104-1113
315. Sara Y., Mozhayeva M.G., Liu X., and Kavalali E.T. Fast vesicle recycling supports neurotransmission during sustained stimulation at hippocampal synapses. J. Neurosci. 22 (2002) 1608-1617
316. Sara Y., Virmani T., Deak F., Liu X., and Kavalali E.T. An isolated pool of vesicles recycles at rest and drives spontaneous neurotransmission. Neuron 45 (2005) 563-573
317. Schenk U., Menna E., Kim T., Passafaro M., Chang S., De Camilli P., and Matteoli M. A novel pathway for presynaptic mitogen-activated kinase activation via AMPA receptors. J. Neurosci. 25 (2005) 1654-1663
318. Schiavo G., Benfenati F., Poulain B., Rossetto O., Polverino de Laureto P., DasGupta B.R., and Montecucco C. Tetanus and botulinum-B neurotoxins block neurotransmitter release by proteolytic cleavage of synaptobrevin. Nature 359 (1992) 832-835
319. Schiavo G., Gu Q.M., Prestwich G.D., Sollner T.H., and Rothman J.E. Calcium-dependent switching of the specificity of phosphoinositide binding to synaptotagmin. Proc. Natl. Acad. Sci. U.S.A. 93 (1996) 13327-13332
320. Schikorski T., and Stevens C.F. Morphological correlates of functionally defined synaptic vesicle populations. Nat. Neurosci. 4 (2001) 391-395
321. Schluter O.M., Schnell E., Verhage M., Tzonopoulos T., Nicoll R.A., Janz R., Malenka R.C., Geppert M., and Südhof T.C. Rabphilin knock-out mice reveal that rabphilin is not required for rab3 function in regulating neurotransmitter release. J. Neurosci. 19 (1999) 5834-5846
322. Schluter O.M., Khvotchev M., Jahn R., and Südhof T.C. Localization versus function of Rab3 proteins Evidence for a common regulatory role in controlling fusion. J. Biol. Chem. 277 (2002) 40919-40929
323. Schluter O.M., Schmitz F., Jahn R., Rosenmund C., and Südhof T.C. A complete genetic analysis of neuronal Rab3 function. J. Neurosci. 24 (2004) 6629-6637
324. Schluter O.M., Basu J., Südhof T.C., and Rosenmund C. Rab3 superprimes synaptic vesicles for release: implications for short-term synaptic plasticity. J. Neurosci. 26 (2006) 1239-1246
325. Schmid S.L., McNiven M.A., and De Camilli P. Dynamin and its partners: a progress report. Curr. Opin. Cell Biol. 10 (1998) 504-512
326. Schmidt A., Hannah M.J., and Huttner W.B. Synaptic-like microvesicles of neuroendocrine cells originate from a novel compartment that is continuous with the plasma membrane and devoid of transferrin receptor. J. Cell Biol. 137 (1997) 445-458
327. Schneggenburger R., and Neher E. Intracellular calcium dependence of transmitter release rates at a fast central synapse. Nature 406 (2000) 889-893
328. Schoch S., Deak F., Konigstorfer A., Mozhayeva M., Sara Y., Südhof T.C., and Kavalali E.T. SNARE function analyzed in synaptobrevin/VAMP knockout mice. Science 294 (2001) 1117-1122
329. Senbonmatsu T., Shirataki H., Jin-no Y., Yamamoto T., and Takai Y. Interaction of Rabphilin3 with synaptic vesicles through multiple regions. Biochem. Biophys. Res. Commun. 228 (1996) 567-572
330. Shi G., Faundez V., Roos J., Dell'Angelica E.C., and Kelly R.B. Neuroendocrine synaptic vesicles are formed in vitro by both clathrin-dependent and clathrin-independent pathways. J. Cell Biol. 143 (1998) 947-955
331. Shimizu H., Kawamura S., and Ozaki K. An essential role of Rab5 in uniformity of synaptic vesicle size. J. Cell. Sci. 116 (2003) 3583-3590
332. Shupliakov O., Low P., Grabs D., Gad H., Chen H., David C., Takei K., De Camilli P., and Brodin L. Synaptic vesicle endocytosis impaired by disruption of dynamin-SH3 domain interactions. Science 276 (1997) 259-263
333. Simons K., and Ikonen E. Functional rafts in cell membranes. Nature 387 (1997) 569-572
334. Simons K., and van Meer G. Lipid sorting in epithelial cells. Biochemistry 27 (1988) 6197-6202
335. Slepnev V.I., and De Camilli P. Accessory factors in clathrin-dependent synaptic vesicle endocytosis. Nat. Rev. Neurosci. 1 (2000) 161-172
336. Song H., Ming G., Fon E., Bellocchio E., Edwards R.H., and Poo M. Expression of a putative vesicular acetylcholine transporter facilitates quantal transmitter packaging. Neuron 18 (1997) 815-826
337. Spiwoks-Becker I., Vollrath L., Seeliger M.W., Jaissle G., Eshkind L.G., and Leube R.E. Synaptic vesicle alterations in rod photoreceptors of synaptophysin-deficient mice. Neuroscience 107 (2001) 127-142
338. Stahl B., Chou J.H., Li C., Südhof T.C., and Jahn R. Rab3 reversibly recruits rabphilin to synaptic vesicles by a mechanism analogous to raf recruitment by ras. EMBO J. 15 (1996) 1799-1809
339. Staple J.K., Osen-Sand A., Benfenati F., Pich E.M., and Catsicas S. Molecular and functional diversity at synapses of individual neurons in vitro. Eur. J. Neurosci. 9 (1997) 721-731
340. Star E.N., Newton A.J., and Murthy V.N. Real-time imaging of Rab3a and Rab5a reveals differential roles in presynaptic function. J. Physiol. 569 (2005) 103-117
341. Stettler O., Moya K.L., Zahraoui A., and Tavitian B. Developmental changes in the localization of the synaptic vesicle protein rab3A in rat brain. Neuroscience 62 (1994) 587-600
342. Stone L.M., Browning M.D., and Finger T.E. Differential distribution of the synapsins in the rat olfactory bulb. J. Neurosci. 14 (1994) 301-309
343. Strasser J.E., Arribas M., Blagoveshchenskaya A.D., and Cutler D.F. Secretagogue-triggered transfer of membrane proteins from neuroendocrine secretory granules to synaptic-like microvesicles. Mol. Biol. Cell 10 (1999) 2619-2630
344. Subtil A., Gaidarov I., Kobylarz K., Lampson M.A., Keen J.H., and McGraw T.E. Acute cholesterol depletion inhibits clathrin-coated pit budding. Proc. Natl. Acad. Sci. U.S.A. 96 (1999) 6775-6780
345. Südhof T.C. The synaptic vesicle cycle revisited. Neuron 28 (2000) 317-320
346. Südhof T.C. The synaptic vesicle cycle. Annu. Rev. Neurosci. 27 (2004) 509-547
347. Südhof T.C., Czernik A.J., Kao H.T., Takei K., Johnston P.A., Horiuchi A., Kanazir S.D., Wagner M.A., Perin M.S., and De Camilli P. Synapsins: mosaics of shared and individual domains in a family of synaptic vesicle phosphoproteins. Science 245 (1989) 1474-1480
348. Südhof T.C., De Camilli P., Niemann H., and Jahn R. Membrane fusion machinery: insights from synaptic proteins. Cell 75 (1993) 1-4
349. Sun Y.A., and Poo M.M. Evoked release of acetylcholine from the growing embryonic neuron. Proc. Natl. Acad. Sci. U.S.A. 84 (1987) 2540-2544
350. Takamori S., Riedel D., and Jahn R. Immunoisolation of GABA-specific synaptic vesicles defines a functionally distinct subset of synaptic vesicles. J. Neurosci. 20 (2000) 4904-4911
351. Takamori S., Rhee J.S., Rosenmund C., and Jahn R. Identification of differentiation-associated brain-specific phosphate transporter as a second vesicular glutamate transporter (VGLUT2). J. Neurosci. 21 (2001) 1-6
352. Takei K., McPherson P.S., Schmid S.L., and De Camilli P. Tubular membrane invaginations coated by dynamin rings are induced by GTP-gamma S in nerve terminals. Nature 374 (1995) 186-190
353. Takei K., Mundigl O., Daniell L., and De Camilli P. The synaptic vesicle cycle: a single vesicle budding step involving clathrin and dynamin. J. Cell Biol. 133 (1996) 1237-1250
354. Tan P.K., Waites C., Liu Y., Krantz D.E., and Edwards R.H. A leucine-based motif mediates the endocytosis of vesicular monoamine and acetylcholine transporters. J. Biol. Chem. 273 (1998) 17351-17360
355. Tanaka C., and Nishizuka Y. The protein kinase C family for neuronal signaling. Annu. Rev. Neurosci. 17 (1994) 551-567
356. Tao-Cheng J.H., and Eiden L.E. The vesicular monoamine transporter VMAT2 and vesicular acetylcholine transporter VAChT are sorted to separate vesicle populations in PC12 cells. Adv. Pharmacol. 42 (1998) 250-253
357. Teng H., and Wilkinson R.S. Clathrin-mediated endocytosis near active zones in snake motor boutons. J. Neurosci. 20 (2000) 7986-7993
358. Thiele C., Hannah M.J., Fahrenholz F., and Huttner W.B. Cholesterol binds to synaptophysin and is required for biogenesis of synaptic vesicles. Nat. Cell Biol. 2 (2000) 42-49
359. Thoidis G., Chen P., Pushkin A.V., Vallega G., Leeman S.E., Fine R.E., and Kandror K.V. Two distinct populations of synaptic-like vesicles from rat brain. Proc. Natl. Acad. Sci. U.S.A. 95 (1998) 183-188
360. Thomas L., and Betz H. Synaptophysin binds to physophilin, a putative synaptic plasma membrane protein. J. Cell Biol. 111 (1990) 2041-2052
361. Thomas L., Hartung K., Langosch D., Rehm H., Bamberg E., Franke W.W., and Betz H. Identification of synaptophysin as a hexameric channel protein of the synaptic vesicle membrane. Science 242 (1988) 1050-1053
362. 2+-sensitive pool of vesicles contributes to linearity at the rod photoreceptor ribbon synapse. Neuron 42 (2004) 595-605
363. Tooze S.A., and Stinchcombe J.C. Biogenesis of secretory granules. Semin. Cell Biol. 3 (1992) 357-366
364. Torri-Tarelli F., Villa A., Valtorta F., De Camilli P., Greengard P., and Ceccarelli B. Redistribution of synaptophysin and synapsin I during alpha-latrotoxin-induced release of neurotransmitter at the neuromuscular junction. J. Cell Biol. 110 (1990) 449-459
365. Torri-Tarelli F., Bossi M., Fesce R., Greengard P., and Valtorta F. Synapsin I partially dissociates from synaptic vesicles during exocytosis induced by electrical stimulation. Neuron 9 (1992) 1143-1153
366. Tosoni D., Puri C., Confalonieri S., Salcini A.E., De Camilli P., Tacchetti C., and Di Fiore P.P. TTP specifically regulates the internalization of the transferrin receptor. Cell 123 (2005) 875-888
367. Traub L.M. Sorting it out: AP2 and alternate clathrin adaptors in endocytic cargo selection. J. Cell Biol. 163 (2003) 203-208
368. Tsukita S., and Ishikawa H. The movement of membranous organelles in axons Electron microscopic identification of anterogradely and retrogradely transported organelles. J. Cell Biol. 84 (1980) 513-530
369. Tucker W.C., Edwardson J.M., Bai J., Kim H.J., Martin T.F., and Chapman E.R. Identification of synaptotagmin effectors via acute inhibition of secretion from cracked PC12 cells. J. Cell Biol. 162 (2003) 199-209
370. 2+-regulated membrane fusion by synaptotagmin and SNAREs. Science 304 (2004) 435-438
371. Valtorta F., Jahn R., Fesce R., Greengard P., and Ceccarelli B. Synaptophysin (p38) at the frog neuromuscular junction: its incorporation into the axolemma and recycling after intense quantal secretion. J. Cell Biol. 107 (1988) 2717-2727
372. Valtorta F., Fesce R., Grohovaz F., Haimann C., Hurlbut W.P., Iezzi N., Torri Tarelli F., Villa A., and Ceccarelli B. Neurotransmitter release and synaptic vesicle recycling. Neuroscience 35 (1990) 477-489
373. Valtorta F., Iezzi N., Benfenati F., Lu B., Poo M.M., and Greengard P. Accelerated structural maturation induced by synapsin I at developing neuromuscular synapses of Xenopus laevis. Eur. J. Neurosci. 7 (1995) 261-270
374. Valtorta F., Meldolesi J., and Fesce R. Synaptic vesicles: is kissing a matter of competence?. Trends Cell Biol. 11 (2001) 324-328
375. Valtorta F., Pennuto M., Bonanomi D., and Benfenati F. Synaptophysin: leading actor or walk-on role in synaptic vesicle exocytosis?. Bioessays 26 (2004) 445-453
376. van der Sluijs P., Hull M., Huber L.A., Male P., Goud B., and Mellman I. Reversible phosphorylation-dephosphorylation determines the localization of rab4 during the cell cycle. EMBO J. 11 (1992) 4379-4389
377. Varoqueaux F., Sigler A., Rhee J.S., Brose N., Enk C., Reim K., and Rosenmund C. Total arrest of spontaneous and evoked synaptic transmission but normal synaptogenesis in the absence of Munc13-mediated vesicle priming. Proc. Natl. Acad. Sci. U.S.A. 99 (2002) 9037-9042
378. Varoqui H., and Erickson J.D. The cytoplasmic tail of the vesicular acetylcholine transporter contains a synaptic vesicle targeting signal. J. Biol. Chem. 273 (1998) 9094-9098
379. +/PI transporter as a novel vesicular glutamate transporter expressed in a distinct set of glutamatergic synapses. J. Neurosci. 22 (2002) 142-155
380. Verderio C., Coco S., Pravettoni E., Bacci A., and Matteoli M. Synaptogenesis in hippocampal cultures. Cell Mol. Life Sci. 55 (1999) 1448-1462
381. Verhage M., Maia A.S., Plomp J.J., Brussaard A.B., Heeroma J.H., Vermeer H., Toonen R.F., Hammer R.E., van den Berg T.K., Missler M., Geuze H.J., and Südhof T.C. Synaptic assembly of the brain in the absence of neurotransmitter secretion. Science 287 (2000) 864-869
382. Verstreken P., Kjaerulff O., Lloyd T.E., Atkinson R., Zhou Y., Meinertzhagen I.A., and Bellen H.J. Endophilin mutations block clathrin-mediated endocytosis but not neurotransmitter release. Cell 109 (2002) 101-112
383. Verstreken P., Koh T.W., Schulze K.L., Zhai R.G., Hiesinger P.R., Zhou Y., Mehta S.Q., Cao Y., Roos J., and Bellen H.J. Synaptojanin is recruited by endophilin to promote synaptic vesicle uncoating. Neuron 40 (2003) 733-748
384. Vincendon G., Morgan I.G., Gombos G., and Breckenridge W.C. Comparative study of the composition of the synaptic vesicles and synaptosomal plasma membranes of the rat brain. J. Physiol. (Paris) 65 Suppl 1 (1972) 173A
385. Virmani T., Ertunc M., Sara Y., Mozhayeva M., and Kavalali E.T. Phorbol esters target the activity-dependent recycling pool and spare spontaneous vesicle recycling. J. Neurosci. 25 (2005) 10922-10929
386. Virmani T., Atasoy D., and Kavalali E.T. Synaptic vesicle recycling adapts to chronic changes in activity. J. Neurosci. 26 (2006) 2197-2206
387. Voglmaier S.M., Kam K., Yang H., Fortin D.L., Hua Z., Nicoll R.A., and Edwards R.H. Distinct endocytic pathways control the rate and extent of synaptic vesicle protein recycling. Neuron 51 (2006) 71-84
388. Von Kriegstein K., Schmitz F., Link E., and Südhof T.C. Distribution of synaptic vesicle proteins in the mammalian retina identifies obligatory and facultative components of ribbon synapses. Eur. J. Neurosci. 11 (1999) 1335-1348
389. von Poser C., Zhang J.Z., Mineo C., Ding W., Ying Y., Südhof T.C., and Anderson R.G. Synaptotagmin regulation of coated pit assembly. J. Biol. Chem. 275 (2000) 30916-30924
390. Walther K., Diril M.K., Jung N., and Haucke V. Functional dissection of the interactions of stonin 2 with the adaptor complex AP2 and synaptotagmin. Proc. Natl. Acad. Sci. U.S.A. 101 (2004) 964-969
391. Wang Y., Okamoto M., Schmitz F., Hofmann K., and Sudhof T.C. Rim is a putative Rab3 effector in regulating synaptic-vesicle fusion. Nature 388 (1997) 593-598
392. Wang Y., Thiele C., and Huttner W.B. Cholesterol is required for the formation of regulated and constitutive secretory vesicles from the trans-Golgi network. Traffic 1 (2000) 952-962
393. Warr O., Takahashi M., and Attwell D. Modulation of extracellular glutamate concentration in rat brain slices by cystine-glutamate exchange. J. Physiol. 514 Pt 3 (1999) 783-793
394. Washbourne P., Schiavo G., and Montecucco C. Vesicle-associated membrane protein-2 (synaptobrevin-2) forms a complex with synaptophysin. Biochem. J. 305 Pt 3 (1995) 721-724
395. Weihe E., Tao-Cheng J.H., Schafer M.K., Erickson J.D., and Eiden L.E. Visualization of the vesicular acetylcholine transporter in cholinergic nerve terminals and its targeting to a specific population of small synaptic vesicles. Proc. Natl. Acad. Sci. U.S.A. 93 (1996) 3547-3552
396. Wenk M.R., and De Camilli P. Protein-lipid interactions and phosphoinositide metabolism in membrane traffic: insights from vesicle recycling in nerve terminals. Proc. Natl. Acad. Sci. U.S.A. 101 (2004) 8262-8269
397. Wenk M.R., Pellegrini L., Klenchin V.A., Di Paolo G., Chang S., Daniell L., Arioka M., Martin T.F., and De Camilli P. PIP kinase Igamma is the major PI(4,5)P(2) synthesizing enzyme at the synapse. Neuron 32 (2001) 79-88
398. West A.E., Neve R.L., and Buckley K.M. Targeting of the synaptic vesicle protein synaptobrevin in the axon of cultured hippocampal neurons: evidence for two distinct sorting steps. J. Cell Biol. 139 (1997) 917-927
399. Wiedenmann B., and Franke W.W. Identification and localization of synaptophysin, an integral membrane glycoprotein of Mr 38,000 characteristic of presynaptic vesicles. Cell 41 (1985) 1017-1028
400. Wienisch M., and Klingauf J. Vesicular proteins exocytosed and subsequently retrieved by compensatory endocytosis are non-identical. Nat. Neurosci. 9 (2006) 1019-1027
401. Wilson J.M., de Hoop M., Zorzi N., Toh B.H., Dotti C.G., and Parton R.G. EEA1, a tethering protein of the early sorting endosome, shows a polarized distribution in hippocampal neurons, epithelial cells, and fibroblasts. Mol. Biol. Cell 11 (2000) 2657-2671
402. Wojcik S.M., Rhee J.S., Herzog E., Sigler A., Jahn R., Takamori S., Brose N., and Rosenmund C. An essential role for vesicular glutamate transporter 1 (VGLUT1) in postnatal development and control of quantal size. Proc. Natl. Acad. Sci. U.S.A. 101 (2004) 7158-7163
403. Wucherpfennig T., Wilsch-Brauninger M., and Gonzalez-Gaitan M. Role of Drosophila Rab5 during endosomal trafficking at the synapse and evoked neurotransmitter release. J. Cell Biol. 161 (2003) 609-624
404. Xie Z.P., and Poo M.M. Initial events in the formation of neuromuscular synapse: rapid induction of acetylcholine release from embryonic neuron. Proc. Natl. Acad. Sci. U.S.A. 83 (1986) 7069-7073
405. Yamada K.M., Spooner B.S., and Wessells N.K. Ultrastructure and function of growth cones and axons of cultured nerve cells. J. Cell Biol. 49 (1971) 614-635
406. 2+-sensitive pool of vesicles is regulated by protein kinase C in adrenal chromaffin cells. Proc. Natl. Acad. Sci. U.S.A. 99 (2002) 17060-17065
407. Yao W.D., Rusch J., Poo M., and Wu C.F. Spontaneous acetylcholine secretion from developing growth cones of Drosophila central neurons in culture: effects of cAMP-pathway mutations. J. Neurosci. 20 (2000) 2626-2637
408. Yao J., Erickson J.D., and Hersh L.B. Protein kinase A affects trafficking of the vesicular monoamine transporters in PC12 cells. Traffic 5 (2004) 1006-1016
409. Ye W., Ali N., Bembenek M.E., Shears S.B., and Lafer E.M. Inhibition of clathrin assembly by high affinity binding of specific inositol polyphosphates to the synapse-specific clathrin assembly protein AP3. J. Biol. Chem. 270 (1995) 1564-1568
410. Yelamanchili S.V., Pendyala G., Brunk I., Darna M., Albrecht U., and Ahnert-Hilger G. Differential sorting of the vesicular glutamate transporter 1 into a defined vesicular pool is regulated by light signaling involving the clock gene period2. J. Biol. Chem. 281 (2006) 15671-15679
411. Yonekawa Y., Harada A., Okada Y., Funakoshi T., Kanai Y., Takei Y., Terada S., Noda T., and Hirokawa N. Defect in synaptic vesicle precursor transport and neuronal cell death in KIF1A motor protein-deficient mice. J. Cell Biol. 141 (1998) 431-441
412. Young S.H., and Poo M.M. Spontaneous release of transmitter from growth cones of embryonic neurones. Nature 305 (1983) 634-637
413. Zakharenko S., Chang S., O'Donoghue M., and Popov S.V. Neurotransmitter secretion along growing nerve processes: comparison with synaptic vesicle exocytosis. J. Cell Biol. 144 (1999) 507-518
414. Zhai R.G., Vardinon-Friedman H., Cases-Langhoff C., Becker B., Gundelfinger E.D., Ziv N.E., and Garner C.C. Assembling the presynaptic active zone: a characterization of an active one precursor vesicle. Neuron 29 (2001) 131-143
415. Zhang J.Z., Davletov B.A., Südhof T.C., and Anderson R.G. Synaptotagmin I is a high affinity receptor for clathrin AP2: implications for membrane recycling. Cell 78 (1994) 751-760
416. Zhang B., Koh Y.H., Beckstead R.B., Budnik V., Ganetzky B., and Bellen H.J. Synaptic vesicle size and number are regulated by a clathrin adaptor protein required for endocytosis. Neuron 21 (1998) 1465-1475
417. Zhao H., and Nonet M.L. A conserved mechanism of synaptogyrin localization. Mol. Biol. Cell 12 (2001) 2275-2289
418. Zhao C., Takita J., Tanaka Y., Setou M., Nakagawa T., Takeda S., Yang H.W., Terada S., Nakata T., Takei Y., Saito M., Tsuji S., Hayashi Y., and Hirokawa N. Charcot-Marie-tooth disease type 2A caused by mutation in a microtubule motor KIF1Bbeta. Cell 105 (2001) 587-597
419. Zimmermann H., Volknandt W., Wittich B., and Hausinger A. Synaptic vesicle life cycle and synaptic turnover. J. Physiol. (Paris) 87 (1993) 159-170