Discrete Residues in the C2B Domain of Synaptotagmin I Independently Specify Endocytic Rate and Synaptic Vesicle Size

Neuron

Volumn 50, Issue 1, 2006, Pages 49-62

  Poskanzer, Kira E ^a   Fetter, Richard D ^a   Davis, Graeme W ^a  

^a UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

CELLBIO; MOLNEURO

Indexed keywords

SYNAPTOTAGMIN; SYNAPTOTAGMIN I; UNCLASSIFIED DRUG;

ANIMAL EXPERIMENT; ARTICLE; CALCIUM TRANSPORT; CELL ULTRASTRUCTURE; CONTROLLED STUDY; CORRELATION ANALYSIS; DROSOPHILA; ENDOCYTOSIS; EXTRACELLULAR CALCIUM; INTERNALIZATION; LARVA; MUTATION; NONHUMAN; PEPTIDE MAPPING; PRIORITY JOURNAL; PROTEIN DOMAIN; PROTEIN FUNCTION; SYNAPSE VESICLE; SYNAPTIC MEMBRANE;

ADAPTOR PROTEIN COMPLEX ALPHA SUBUNITS; ANIMALS; ANIMALS, GENETICALLY MODIFIED; ASPARTIC ACID; CALCIUM; CALCIUM-BINDING PROTEINS; DOSE-RESPONSE RELATIONSHIP, DRUG; DOSE-RESPONSE RELATIONSHIP, RADIATION; DROSOPHILA; DROSOPHILA PROTEINS; ELECTRIC STIMULATION; ENDOCYTOSIS; EXCITATORY POSTSYNAPTIC POTENTIALS; GREEN FLUORESCENT PROTEINS; IMMUNOHISTOCHEMISTRY; LARVA; LYSINE; MEMBRANE POTENTIALS; MICROSCOPY, ELECTRON, TRANSMISSION; MUTATION; PHOTIC STIMULATION; PROTEIN STRUCTURE, TERTIARY; SYNAPSES; SYNAPTIC VESICLES; SYNAPTOTAGMIN I; TIME FACTORS;

EID: 33645968966     PISSN: 08966273     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.neuron.2006.02.021     Document Type: Article

References (59)

1. 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
2. Chapman E.R., An S., Edwardson J.M., and Jahn R. A novel function for the second C2 domain of synaptotagmin. Ca2+-triggered dimerization. J. Biol. Chem. 271 (1996) 5844-5849
3. Chapman E.R., Desai R.C., Davis A.F., and Tornehl C.K. Delineation of the oligomerization, AP-2 binding, and synprint binding region of the C2B domain of synaptotagmin. J. Biol. Chem. 273 (1998) 32966-32972
4. David C., McPherson P.S., Mundigl O., and de Camilli P. A role of amphiphysin in synaptic vesicle endocytosis suggested by its binding to dynamin in nerve terminals. Proc. Natl. Acad. Sci. USA 93 (1996) 331-335
5. 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
6. DiAntonio A., and Schwarz T.L. The effect on synaptic physiology of synaptotagmin mutations in Drosophila. Neuron 12 (1994) 909-920
7. Fernandez I., Arac D., Ubach J., Gerber S.H., Shin O., Gao Y., Anderson R.G., Sudhof T.C., and Rizo J. Three-dimensional structure of the synaptotagmin 1 C2B-domain: synaptotagmin 1 as a phospholipid binding machine. Neuron 32 (2001) 1057-1069
8. Fernandez-Alfonso T., and Ryan T.A. The kinetics of synaptic vesicle pool depletion at CNS synaptic terminals. Neuron 41 (2004) 943-953
9. Fernandez-Chacon R., Konigstorfer A., Gerber S.H., Garcia J., Matos M.F., Stevens C.F., Brose N., Rizo J., Rosenmund C., and Sudhof T.C. Synaptotagmin I functions as a calcium regulator of release probability. Nature 410 (2001) 41-49
10. Fukuda M., Kojima T., Aruga J., Niinobe M., and Mikoshiba K. Functional diversity of C2 domains of synaptotagmin family. Mutational analysis of inositol high polyphosphate binding domain. J. Biol. Chem. 270 (1995) 26523-26527
11. Fukuda M., Kabayama H., and Mikoshiba K. Drosophila AD3 mutation of synaptotagmin impairs calcium-dependent self-oligomerization activity. FEBS Lett. 482 (2000) 269-272
12. Gad H., Low P., Zotova E., Brodin L., and Shupliakov O. Dissociation between Ca2+-triggered synaptic vesicle exocytosis and clathrin-mediated endocytosis at a central synapse. Neuron 21 (1998) 607-616
13. Gaietta G., Deerinck T.J., Adams S.R., Bouwer J., Tour O., Laird D.W., Sosinsky G.E., Tsien R.Y., and Ellisman M.H. Multicolor and electron microscopic imaging of connexin trafficking. Science 296 (2002) 503-507
14. Geppert M., Goda Y., Hammer R.E., Li C., Rosahl T.W., Stevens C.F., and Sudhof T.C. Synaptotagmin I: a major Ca2+ sensor for transmitter release at a central synapse. Cell 79 (1994) 717-727
15. Guichet A., Wucherpfennig T., Dudu V., Etter S., Wilsch-Brauniger M., Hellwig A., Gonzalez-Gaitan M., Huttner W.B., and Schmidt A.A. Essential role of endophilin A in synaptic vesicle budding at the Drosophila neuromuscular junction. EMBO J. 21 (2002) 1661-1672
16. Haucke V., and De Camilli P. AP-2 recruitment to synaptotagmin stimulated by tyrosine-based endocytic motifs. Science 285 (1999) 1268-1271
17. 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
18. 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
19. 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
20. Kee Y., and Scheller R.H. Localization of synaptotagmin-binding domains on syntaxin. J. Neurosci. 16 (1996) 1975-1981
21. Klingauf J., Kavalali E.T., and Tsien R.W. Kinetics and regulation of fast endocytosis at hippocampal synapses. Nature 394 (1998) 581-585
22. 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
23. Koenig J.H., Saito K., and Ikeda K. Reversible control of synaptic transmission in a single gene mutant of Drosophila melanogaster. J. Cell Biol. 96 (1983) 1517-1522
24. 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
25. Kosaka T., and Ikeda K. Possible temperature-dependent blockage of synaptic vesicle recycling induced by a single gene mutation in Drosophila. J. Neurobiol. 14 (1983) 207-225
26. 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. USA 102 (2005) 6131-6136
27. Littleton J.T., Stern M., Schulze K., Perin M., and Bellen H.J. Mutational analysis of Drosophila synaptotagmin demonstrates its essential role in Ca(2+)-activated neurotransmitter release. Cell 74 (1993) 1125-1134
28. Littleton J.T., Stern M., Perin M., and Bellen H.J. Calcium dependence of neurotransmitter release and rate of spontaneous vesicle fusions are altered in Drosophila synaptotagmin mutants. Proc. Natl. Acad. Sci. USA 91 (1994) 10888-10892
29. Littleton J.T., Bai J., Vyas B., Desai R., Baltus A.E., Garment M.B., Carlson S.D., Ganetzky B., and Chapman E.R. synaptotagmin mutants reveal essential functions for the C2B domain in Ca2+-triggered fusion and recycling of synaptic vesicles in vivo. J. Neurosci. 21 (2001) 1421-1433
30. Llinas R.R., Sugimori M., Moran K.A., Moreira J.E., and Fukuda M. Vesicular reuptake inhibition by a synaptotagmin I C2B domain antibody at the squid giant synapse. Proc. Natl. Acad. Sci. USA 101 (2004) 17855-17860
31. Mackler J.M., and Reist N.E. Mutations in the second C2 domain of synaptotagmin disrupt synaptic transmission at Drosophila neuromuscular junctions. J. Comp. Neurol. 436 (2001) 4-16
32. Mackler J.M., Drummond J.A., Loewen C.A., Robinson I.M., and Reist N.E. The C(2)B Ca(2+)-binding motif of synaptotagmin is required for synaptic transmission in vivo. Nature 418 (2002) 340-344
33. Marek K.W., and Davis G.W. Transgenically encoded protein photoinactivation (FlAsH-FALI): acute inactivation of synaptotagmin I. Neuron 36 (2002) 805-813
34. Marie B., Sweeney S.T., Poskanzer K.E., Roos J., Kelly R.B., and Davis G.W. Dap160/intersectin scaffolds the periactive zone to achieve high-fidelity endocytosis and normal synaptic growth. Neuron 43 (2004) 207-219
35. 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
36. Miesenbock G., De Angelis D.A., and Rothman J.E. Visualizing secretion and synaptic transmission with pH-sensitive green fluorescent proteins. Nature 394 (1998) 192-195
37. Neves G., and Lagnado L. The kinetics of exocytosis and endocytosis in the synaptic terminal of goldfish retinal bipolar cells. J. Physiol. 515 (1999) 181-202
38. Nicholson-Tomishima K., and Ryan T.A. Kinetic efficiency of endocytosis at mammalian CNS synapses requires synaptotagmin I. Proc. Natl. Acad. Sci. USA 101 (2004) 16648-16652
39. Perin M.S., Brose N., Jahn R., and Sudhof T.C. Domain structure of synaptotagmin (p65). J. Biol. Chem. 266 (1991) 623-629
40. Phillips A.M., Smith M., Ramaswami M., and Kelly L.E. The products of the Drosophila stoned locus interact with synaptic vesicles via synaptotagmin. J. Neurosci. 20 (2000) 8254-8261
41. Pielage J., Fetter R.D., and Davis G.W. Presynaptic spectrin is essential for synapse stabilization. Curr. Biol. 15 (2005) 918-928
42. 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
43. 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
44. Reist N.E., Buchanan J., Li J., DiAntonio A., Buxton E.M., and Schwarz T.L. Morphologically docked synaptic vesicles are reduced in synaptotagmin mutants of Drosophila. J. Neurosci. 18 (1998) 7662-7673
45. Ringstad N., Gad H., Low P., Di Paolo G., Brodin L., Shupliakov O., and De Camilli P. Endophilin/SH3p4 is required for the transition from early to late stages in clathrin-mediated synaptic vesicle endocytosis. Neuron 24 (1999) 143-154
46. Robinson I.M., Ranjan R., and Schwarz T.L. Synaptotagmins I and IV promote transmitter release independently of Ca(2+) binding in the C(2)A domain. Nature 418 (2002) 336-340
47. Ryan T.A., Smith S.J., and Reuter H. The timing of synaptic vesicle endocytosis. Proc. Natl. Acad. Sci. USA 93 (1996) 5567-5571
48. Sankaranarayanan S., and Ryan T.A. Real-time measurements of vesicle-SNARE recycling in synapses of the central nervous system. Nat. Cell Biol. 2 (2000) 197-204
49. 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. USA 93 (1996) 13327-13332
50. Sheng Z.H., Yokoyama C.T., and Catterall W.A. Interaction of the synprint site of N-type Ca2+ channels with the C2B domain of synaptotagmin I. Proc. Natl. Acad. Sci. USA 94 (1997) 5405-5410
51. Stevens C.F., and Sullivan J.M. The synaptotagmin C2A domain is part of the calcium sensor controlling fast synaptic transmission. Neuron 39 (2003) 299-308
52. Stoorvogel W., Oorschot V., and Geuze H.J. A novel class of clathrin-coated vesicles budding from endosomes. J. Cell Biol. 132 (1996) 21-33
53. Sugita S., Hata Y., and Sudhof T.C. Distinct Ca(2+)-dependent properties of the first and second C2-domains of synaptotagmin I. J. Biol. Chem. 271 (1996) 1262-1265
54. Ubach J., Zhang X., Shao X., Sudhof T.C., and Rizo J. Ca2+ binding to synaptotagmin: how many Ca2+ ions bind to the tip of a C2-domain?. EMBO J. 17 (1998) 3921-3930
55. 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
56. von Gersdorff H., and Matthews G. Dynamics of synaptic vesicle fusion and membrane retrieval in synaptic terminals. Nature 367 (1994) 735-739
57. Whitney J.A., Gomez M., Sheff D., Kreis T.E., and Mellman I. Cytoplasmic coat proteins involved in endosome function. Cell 83 (1995) 703-713
58. Zhang J.Z., Davletov B.A., Sudhof T.C., and Anderson R.G. Synaptotagmin I is a high affinity receptor for clathrin AP-2: implications for membrane recycling. Cell 78 (1994) 751-760
59. 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