An antibody to synaptotagmin I facilitates synaptic transmission

European Journal of Neuroscience

Volumn 25, Issue 11, 2007, Pages 3217-3225

  Hua, Shao Ying ^a   Teylan, Merilee A ^a,c   Cimenser, Aylin ^b  

^a Program on US Russia Relations at Columbia s Harriman Institute   (United States)

^b Och Spine at New York Presbyterian Hospitals   (United States)

^c ROCKEFELLER UNIVERSITY   (United States)

Author keywords

EPSP rise time; Neurotransmitter release; Synaptic delay; Synaptotagmin

Indexed keywords

ANTIBODY; SYNAPTOTAGMIN I; SYNAPTOTAGMIN I ANTIBODY; UNCLASSIFIED DRUG;

ANIMAL TISSUE; ARTICLE; CONTROLLED STUDY; CRAYFISH; EVOKED RESPONSE; MOLECULAR MECHANICS; MOTOR NERVE; NEUROMUSCULAR SYNAPSE; NEUROTRANSMITTER RELEASE; NONHUMAN; PRIORITY JOURNAL; SYNAPTIC POTENTIAL; SYNAPTIC TRANSMISSION;

ANIMALS; ANTIBODIES; BLOTTING, WESTERN; CALCIUM; CATFISHES; DOSE-RESPONSE RELATIONSHIP, DRUG; DRUG INTERACTIONS; EXCITATORY POSTSYNAPTIC POTENTIALS; MICROINJECTIONS; NEUROMUSCULAR JUNCTION; PATCH-CLAMP TECHNIQUES; RATS; SYNAPTIC TRANSMISSION; SYNAPTOTAGMIN I;

EID: 34249910332     PISSN: 0953816X     EISSN: 14609568     Source Type: Journal    
DOI: 10.1111/j.1460-9568.2007.05602.x     Document Type: Article

References (42)

1. Arac, D., Chen, X., Khant, H.A., Ubach, J., Ludtke, S.J., Kikkawa, M., Johnson, A.E., Chiu, W., Südhof, T.C. Rizo, J. (2006) Close membrane-membrane proximity induced by Ca(2+)-dependent multivalent binding of synaptotagmin-1 to phospholipids. Nat. Struct. Mol. Biol., 13, 209 217.
2. Bai, J., Wang, P. Chapman, E.R. (2002) C2A activates a cryptic Ca(2+)-triggered membrane penetration activity within the C2B domain of synaptotagmin I. Proc. Natl Acad. Sci. USA, 99, 1665 1670.
3. Bhalla, A., Chicka, M.C., Tucker, W.C. Chapman, E.R. (2006) Ca(2+)-synaptotagmin directly regulates t-SNARE function during reconstituted membrane fusion. Nat. Struct. Mol. Biol., 13, 323 330.
4. Bommert, K., Charlton, M.P., DeBello, W.M., Chin, G.J., Betz, H. Augustine, G.J. (1993) Inhibition of neurotransmitter release by C2-domain peptides implicates synaptotagmin in exocytosis. Nature, 363, 163 165.
5. Broadie, K., Bellen, H.J., DiAntonio, A., Littleton, J.T. Schwarz, T.L. (1994) Absence of synaptotagmin disrupts excitation-secretion coupling during synaptic transmission. Proc. Natl Acad. Sci. USA, 91, 10727 10731.
6. Chapman, E.R. (2002) Synaptotagmin: a Ca2+ sensor that triggers exocytosis? Nat. Rev. Mol. Cell. Biol., 3, 498 508.
7. Cooper, R.L., Hampson, D.R. Atwood, H.L. (1995) Synaptotagmin-like expression in the motor nerve terminals of crayfish. Brain Res., 703, 214 216.
8. Davis, A.F., Bai, J., Fasshauer, D., Wolowick, M.J., Lewis, J.L. Chapman, E.R. (1999) Kinetics of synaptotagmin responses to Ca2+ and assembly with the core SNARE complex onto membranes. Neuron, 24, 363 376.
9. DiAntonio, A., Parfitt, K.D. Schwarz, T.L. (1993) Synaptic transmission persists in synaptotagmin mutants of Drosophila. Cell, 73, 1281 1290.
10. DiAntonio, A. Schwarz, T.L. (1994) The effect on synaptic physiology of synaptotagmin mutations in Drosophila. Neuron, 12, 909 920.
11. Fernández-Chacón, R., Königstorfer, A., Gerber, S.H., Garcia, J., Matos, M.F., Stevens, C.F., Brose, N., Rizo, J., Rosenmund, C. Südhof, T.C. (2001) Synaptotagmin I functions as a calcium regulator of release probability. Nature, 410, 41 49.
12. Geppert, M., Goda, Y., Hammer, R.E., Li, C., Rosahl, T.W., Stevens, C.F. Südhof, T.C. (1994) Synaptotagmin I: a major Ca2+ sensor for transmitter release at a central synapse. Cell, 79, 717 727.
13. Giraudo, C.G., Eng, W.S., Melia, T.J. Rothman, J.E. (2006) A clamping mechanism involved in SNARE-dependent exocytosis. Science, 313, 676 680.
14. He, P., Southard, R.C., Chen, D., Whiteheart, S.W. Cooper, R.L. (1999) Role of alpha-SNAP in promoting efficient neurotransmission at the crayfish neuromuscular junction. J. Neurophysiol., 82, 3406 3416.
15. Hilfiker, S., Pieribone, V.A., Nordstedt, C., Greengard, P. Czernik, A.J. (1999) Regulation of synaptotagmin I phosphorylation by multiple protein kinases. J. Neurochem., 73, 921 932.
16. Hoyle, G. Wiersma, C.A. (1958) Excitation at neuromuscular junctions in Crustacea. J. Physiol., 143, 403 425.
17. Hua, S.Y. Charlton, M.P. (1999) Activity-dependent changes in partial VAMP complexes during neurotransmitter release. Nat. Neurosci., 2, 1078 1083.
18. Hua, S.Y., Raciborska, D.A., Trimble, W.S. Charlton, M.P. (1998) Different VAMP/synaptobrevin complexes for spontaneous and evoked transmitter release at the crayfish neuromuscular junction. J. Neurophysiol., 80, 3233 3246.
19. Katz, B. Miledi, R. (1965) The measurement of synaptic delay and the time course of acetylcholine release at the neuromuscular junction. Proc. R. Soc. Lond. B Biol. Sci., 161, 483 895.
20. Littleton, J.T., Stern, M., Perin, M. Bellen, H.J. (1994) Calcium dependence of neurotransmitter release and rate of spontaneous vesicle fusions are altered in Drosophila synaptotagmin mutants. Proc. Natl Acad. Sci. USA, 91, 10888 10892.
21. Littleton, J.T., Stern, M., Schulze, K., Perin, M. Bellen, H.J. (1993) Mutational analysis of Drosophila synaptotagmin demonstrates its essential role in Ca(2+)-activated neurotransmitter release. Cell, 74, 1125 1134.
22. Liu, Y., Fallon, L., Lashuel, H.A., Liu, Z. Lansbury, P.T. Jr. (2002) The UCH-L1 gene encodes two opposing enzymatic activities that affect α-synuclein aegradation and Parkinson's disease susceptibility. Cell, 111, 209 218.
23. Llinás, R., Steinberg, I.Z. Walton, K. (1981) Relationship between presynaptic calcium current and postsynaptic potential in squid giant synapse. Biophys. J., 33, 323 351.
24. Martin, K.C., Hu, Y., Armitage, B.A., Siegelbaum, S.A., Kandel, E.R. Kaang, B.K. (1995) Evidence for synaptotagmin as an inhibitory clamp on synaptic vesicle release in Aplysia neurons. Proc. Natl Acad. Sci. USA, 92, 11307 11311.
25. Mikoshiba, K., Fukuda, M., Moreira, J.E., Lewis, F.M., Sugimori, M., Niinobe, M. Llinás, R. (1995) Role of the C2A domain of synaptotagmin in transmitter release as determined by specific antibody injection into the squid giant synapse preterminal. Proc. Natl Acad. Sci. USA, 92, 10703 10707.
26. Msghina, M., Govind, C.K. Atwood, H.L. (1998) Synaptic structure and transmitter release in crustacean phasic and tonic motor neurons. J. Neurosci., 18, 1374 1382.
27. Nagy, G., Kim, J.H., Pang, Z.P., Matti, U., Rettig, J., Südhof, T.C. Sorensen, J.B. (2006) Different effects on fast exocytosis induced by synaptotagmin 1 and 2 isoforms and abundance but not by phosphorylation. J. Neurosci., 26, 632 643.
28. Pang, Z.P., Sun, J., Rizo, J., Maximov, A. Südhof, T.C. (2006) Genetic analysis of synaptotagmin 2 in spontaneous and Ca2+-triggered neurotransmitter release. EMBO J., 25, 2039 2050.
29. Popov, S.V. Poo, M.M. (1993) Synaptotagmin: a calcium-sensitive inhibitor of exocytosis? Cell, 73, 1247 1249.
30. Sabatini, B.L. Regehr, W.G. (1996) Timing of neurotransmission at fast synapses in the mammalian brain. Nature, 384, 170 172.
31. Schweizer, F.E., Dresbach, T., DeBello, W.M., O'Connor, V., Augustine, G.J. Betz, H. (1998) Regulation of neurotransmitter release kinetics by NSF. Science, 279, 1203 1206.
32. Shoji-Kasai, Y., Yoshida, A., Sato, K., Hoshino, T., Ogura, A., Kondo, S., Fujimoto, Y., Kuwahara, R., Kato, R. Takahashi, M. (1992) Neurotransmitter release from synaptotagmin-deficient clonal variants of PC12 cells. Science, 256, 1821 1823.
33. Silverman-Gavrila, L.B., Orth, P.M. Charlton, M.P. (2005) Phosphorylation-dependent low-frequency depression at phasic synapses of a crayfish motoneuron. J. Neurosci., 25, 3168 3180.
34. Sollner, T., Whiteheart, S.W., Brunner, M., Erdjument-Bromage, H., Geromanos, S., Tempst, P. Rothman, J.E. (1993) SNAP receptors implicated in vesicle targeting and fusion. Nature, 362, 318 324.
35. Südhof, T.C. Rizo, J. (1996) Synaptotagmins: C2-domain proteins that regulate membrane traffic. Neuron, 17, 379 388.
36. Tang, J., Maximov, A., Shin, O.H., Dai, H., Rizo, J. Südhof, T.C. (2006) A complexin/synaptotagmin 1 switch controls fast synaptic vesicle exocytosis. Cell, 126, 1175 1187.
37. Tucker, W.C. Chapman, E.R. (2002) Role of synaptotagmin in Ca2+-triggered exocytosis. Biochem. J., 366, 1 13.
38. Tucker, W.C., Weber, T. Chapman, E.R. (2004) Reconstitution of Ca2+ regulated membrane fusion by synaptotagmin and SNAREs. Science, 304, 435 438.
39. Ubach, J., Zhang, X., Shao, X., Südhof, T.C. Rizo, J. (1998) Ca2+ binding to synaptotagmin: how many Ca2+ ions bind to the tip of a C2-domain? EMBO J., 17, 3921 3930.
40. Vyshedskiy, A., Allana, T. Lin, J.W. (2000) Analysis of presynaptic Ca2+ influx and transmitter release kinetics during facilitation at the inhibitor of the crayfish neuromuscular junction. J. Neurosci., 20, 6326 6332.
41. Wiser, O., Tobi, D., Trus, M. Atlas, D. (1997) Synaptotagmin restores kinetic properties of a syntaxin-associated N-type voltage sensitive calcium channel. FEBS Lett., 404, 203 207.
42. Yu, M., Kasai, K., Nagashima, K., Torii, S., Yokota-Hashimoto, H., Okamoto, K., Takeuchi, T., Gomi, H. Izumi, T. (2007) Exophilin4/Slp2-a targets glucagon granules to the plasma membrane through unique Ca2+-inhibitory phospholipid-binding activity of the C2A domain. Mol. Biol. Cell., 18, 688 696.