Sr2+ binding to the Ca2+ binding site of the synaptotagmin 1 C2B domain triggers fast exocytosis without stimulating SNARE interactions

Neuron

Volumn 37, Issue 1, 2003, Pages 99-108

  Shin, Ok Ho ^a   Rhee, Jeong Seop ^b   Tang, Jiong ^a   Sugita, Shuzo ^a   Rosenmund, Christian ^b   Südhof, Thomas C ^a  

^a HOWARD HUGHES MEDICAL INSTITUTE   (United States)

^b MAX PLANCK INSTITUTE FOR BIOPHYSICAL CHEMISTRY   (Germany)

Author keywords

[No Author keywords available]

Indexed keywords

CALCIUM CHANNEL STIMULATING AGENT; CALCIUM ION; CATION; PHOSPHOLIPID; SNARE PROTEIN; STRONTIUM; SYNAPTOTAGMIN; BARIUM; CALCIUM; CALCIUM BINDING PROTEIN; CHELATING AGENT; MEMBRANE PROTEIN; NERVE PROTEIN; SYNAPTOTAGMIN I; SYT1 PROTEIN, MOUSE; SYT1 PROTEIN, RAT; VESICULAR TRANSPORT PROTEIN;

ANIMAL CELL; ARTICLE; BINDING AFFINITY; BINDING SITE; CALCIUM BINDING; CONTROLLED STUDY; EXOCYTOSIS; KNOCKOUT MOUSE; MOUSE; NEUROTRANSMITTER RELEASE; NEWBORN; NONHUMAN; PRIORITY JOURNAL; PROTEIN BINDING; PROTEIN DOMAIN; PROTEIN INTERACTION; ANIMAL; CALCIUM SIGNALING; CELL STRAIN; DRUG EFFECT; EXCITATORY POSTSYNAPTIC POTENTIAL; HIPPOCAMPUS; MACROMOLECULE; METABOLISM; MOUSE MUTANT; PHYSIOLOGY; PROTEIN TERTIARY STRUCTURE; RAT; REACTION TIME; SYNAPTIC MEMBRANE; SYNAPTIC TRANSMISSION; SYNAPTOSOME;

ANIMALS; ANIMALS, NEWBORN; BARIUM; CALCIUM; CALCIUM SIGNALING; CALCIUM-BINDING PROTEINS; CHELATING AGENTS; EXCITATORY POSTSYNAPTIC POTENTIALS; EXOCYTOSIS; HIPPOCAMPUS; MACROMOLECULAR SUBSTANCES; MEMBRANE GLYCOPROTEINS; MEMBRANE PROTEINS; MICE; MICE, KNOCKOUT; NERVE TISSUE PROTEINS; PC12 CELLS; PHOSPHOLIPIDS; PRESYNAPTIC TERMINALS; PROTEIN STRUCTURE, TERTIARY; RATS; REACTION TIME; SNARE PROTEINS; STRONTIUM; SYNAPTIC MEMBRANES; SYNAPTIC TRANSMISSION; SYNAPTOTAGMIN I; SYNAPTOTAGMINS; VESICULAR TRANSPORT PROTEINS;

EID: 0037427025     PISSN: 08966273     EISSN: None     Source Type: Journal    
DOI: 10.1016/S0896-6273(02)01145-5     Document Type: Article

References (54)

1. Adolfsen B., Littleton J.T. Genetic and molecular analysis of the synaptotagmin family. Cell. Mol. Life Sci. 58:2001;393-402.
2. Atluri P.P., Regehr W.G. Delayed release of neurotransmitter from cerebellar granule cells. J. Neurosci. 18:1998;8214-8227.
3. Barrett E.F., Stevens C.F. The kinetics of transmitter release at the frog neuromuscular junction. J. Physiol. 227:1972;691-708.
4. Bennett M.K., Calakos N., Scheller R.H. Syntaxin. a synaptic protein implicated in docking of synaptic vesicles at presynaptic active zones Science. 257:1992;255-259.
5. 2+ partially rescues synaptic transmission in hippocampal cultures treated with botulinum toxin A and C, but not tetanus toxin. J. Neurosci. 17:1997;7190-7202.
6. 2+ regulates the interaction between synaptotagmin and syntaxin 1. J. Biol. Chem. 270:1995;23667-23671.
7. Chen X., Tomchick D.R., Kovrigin E., Arac D., Machius M., Südhof T.C., Rizo J. Three-dimensional structure of the complexin/SNARE complex. Neuron. 33:2002;397-409.
8. Dodge F.A. Jr., Miledi R., Rahamimoff R. Strontium and quantal release of transmitter at the neuromuscular junction. J. Physiol. 200:1969;267-283.
9. 2+-binding sites that cooperate to engage t-SNAREs and trigger exocytosis. J. Cell Biol. 154:2001;1117-1123.
10. 2B-domain. synaptotagmin 1 as a phospholipid-binding machine Neuron. 32:2001;1057-1069.
11. 2+-regulator of release probability. Nature. 410:2001;41-49.
12. 2+-binding to the C2A-domain of synaptotagmin 1. J. Neurosci. 22:2002;8438-8446.
13. 2+-dependent secretion in PC12 cells. J. Biol. Chem. 277:2002;4601-4604.
14. Geppert M., Archer B.T. III, Südhof T.C. Synaptotagmin II. a novel differentially distributed form of synaptotagmin J. Biol. Chem. 266:1991;13548-13552.
15. 2+ sensor for transmitter release at a central synapse Cell. 79:1994;717-727.
16. Geppert M., Goda Y., Stevens C.F., Südhof T.C. Rab3A regulates a late step in synaptic vesicle fusion. Nature. 387:1997;810-814.
17. 2+-dependent binding of synaptotagmin to SNARE complexes. J. Biol. Chem. 275:2000;6328-6336.
18. Goda Y., Stevens C.F. Two components of transmitter release at a central synapse. Proc. Natl. Acad. Sci. USA. 91:1994;12942-12946.
19. Guan K.L., Dixon J.E. Eukaryotic proteins expressed in Escherichia coli. an improved thrombin cleavage and purification procedure of fusion proteins with glutathione S-transferase Anal. Biochem. 192:1991;262-267.
20. Hagler D.J. Jr., Goda Y. Properties of synchronous and asynchronous release during pulse train depression in cultured hippocampal neurons. J. Neurophysiol. 85:2001;2324-2334.
21. Johnston P.A., Jahn R., Südhof T.C. Transmembrane topography and evolutionary conservation of synaptophysin. J. Biol. Chem. 264:1989;1268-1273.
22. Katz B. The Release of Neural Transmitter Substances. 1969;Liverpool University Press, Liverpool, UK.
23. Kee Y., Scheller R.H. Localization of synaptotagmin-binding domains on syntaxin. J. Neurosci. 16:1996;1975-1981.
24. 2+ sensors for exocytosis in rat phaeochromocytoma cells. J. Physiol. 533:2001;627-637.
25. Laemmli U.K. Cleavage of structural proteins during the assembly of the head of bacteriophage T4. Nature. 227:1970;680-685.
26. 2+-binding properties of synaptotagmins. definition of candidate Ca2+ sensors for the fast and slow components of neurotransmitter release J. Biol. Chem. 270:1995;24898-24902. a.
27. 2+- independent activities of neural and nonneural synaptotagmins. Nature. 375:1995;594-599. b.
28. 2+-binding motif of synaptotagmin is required for synaptic transmission in vivo. Nature. 418:2002;340-344.
29. Marqueze B., Boudier J.A., Mizuta M., Inagaki N., Seino S., Seagar M. Cellular localization of synaptotagmin I, II, and III mRNAs in the central nervous system and pituitary and adrenal glands of the rat. J. Neurosci. 15:1995;4906-4917.
30. Matthew W.D., Tsavaler L., Reichardt L.F. Identification of a synaptic vesicle-specific membrane protein with a wide distribution in neuronal and neurosecretory tissue. J. Cell Biol. 91:1981;257-269.
31. McMahon H.T., Missler M., Li C., Südhof T.C. Complexins. cytosolic proteins that regulate SNAP-receptor function Cell. 83:1995;111-119.
32. Miledi R. Strontium as a substitute for calcium in the process of transmitter release at the neuromuscular junction. Nature. 212:1966;1233-1234.
33. Perin M.S., Fried V.A., Mignery G.A., Jahn R., Südhof T.C. Phospholipid binding by a synaptic vesicle protein homologous to the regulatory region of protein kinase C. Nature. 345:1990;260-263.
34. Pyott S.J., Rosenmund C. The effects of temperature on vesicular supply and release in autaptic cultures of rat and mouse hippocampal neurons. J. Physiol. 539:2002;523-535.
35. 2+-binding domain. J. Biol. Chem. 273:1998;15879-15882.
36. 2A domain. Nature. 418:2002;336-340.
37. Rosenmund C., Sigler A., Augustin I., Reim K., Brose N., Rhee J.S. Differential control of vesicle priming and short-term plasticity by Munc13 isoforms. Neuron. 33:2002;411-424.
38. 2+-dependent asynchronous evoked transmission at rat striatal inhibitory synapses in vitro. J. Physiol. 514:1999;447-458.
39. Sabatini B.L., Regehr W.G. Timing of neurotransmission at fast synapses in the mammalian brain. Nature. 384:1996;170-172.
40. Sabatini B.L., Regehr W.G. Timing of synaptic transmission. Annu. Rev. Physiol. 61:1999;521-542.
41. Schiavo G., Stenbeck G., Rothman J.E., Sollner T.H. Binding of the synaptic vesicle v-SNARE, synaptotagmin, to the plasma membrane t-SNARE, SNAP-25, can explain docked vesicles at neurotoxin-treated synapses. Proc. Natl. Acad. Sci. USA. 94:1997;997-1001.
42. Shin O.-H., Rizo J., Südhof T.C. Synaptotagmin function in dense core vesicle exocytosis studied in cracked PC12 cells. Nat. Neurosci. 5:2002;649-656.
43. Shoji-Kasai Y., Yoshida A., Sato K., Hoshino T., Ogura A., Kondo S., Fujimoto Y., Kuwahara R., Kato R., Takahashi M. Neurotransmitter release from synaptotagmin-deficient clonal variants of PC12 cells. Science. 256:1992;1821-1823.
44. Silinsky E.M. On the role of barium in supporting the asynchronous release of acetylcholine quanta by motor nerve impulses. J. Physiol. 274:1978;157-171.
45. Südhof T.C. The synaptic vesicle cycle. a cascade of protein-protein interactions Nature. 375:1995;645-653.
46. Südhof T.C. Synaptotagmins. why so many? J. Biol. Chem. 277:2002;7629-7632.
47. 2+ sensor in exocytosis. Neuron. 30:2001;459-473.
48. 2+-affinities. EMBO J. 21:2002;270-280.
49. 2+-binding module. Biochemistry. 40:2001;5854-5860.
50. Ullrich B., Li C., Zhang J.Z., McMahon H., Anderson R.G.W., Geppert M., Südhof T.C. Functional properties of multiple synaptotagmins in brain. Neuron. 13:1994;1281-1291.
51. Voets T., Moser T., Lund P.E., Chow R.H., Geppert M., Südhof T.C., Neher E. Intracellular calcium dependence of large dense-core vesicle exocytosis in the absence of synaptotagmin 1. Proc. Natl. Acad. Sci. USA. 98:2001;11680-11685.
52. Xu-Friedman M.A., Regehr W.G. Presynaptic strontium dynamics and synaptic transmission. Biophys. J. 76:1999;2029-2042.
53. Xu-Friedman M.A., Regehr W.G. Probing fundamental aspects of synaptic transmission with strontium. J. Neurosci. 20:2000;4414-4422.
54. 2+-triggered exocytosis. Neuron. 34:2002;599-611.