Complexin Clamps Asynchronous Release by Blocking a Secondary Ca2+ Sensor via Its Accessory α Helix

Neuron

Volumn 68, Issue 5, 2010, Pages 907-920

  Yang, Xiaofei ^a   Kaeser Woo, Yea Jin ^a   Pang, Zhiping P ^a   Xu, Wei ^a   Südhof, Thomas C ^a  

^a STANFORD UNIVERSITY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CALCIUM ION; CELL MEMBRANE PROTEIN; COMPLEXIN; SNARE PROTEIN; SYNAPTOBREVIN 2; SYNAPTOTAGMIN I; UNCLASSIFIED DRUG;

ALPHA HELIX; AMINO TERMINAL SEQUENCE; ANIMAL CELL; ARTICLE; CALCIUM BINDING; CELL ACTIVATION; CELL MEMBRANE TRANSPORT; COMPLEX FORMATION; CONTROLLED STUDY; EXOCYTOSIS; MOUSE; MUTATIONAL ANALYSIS; NEWBORN; NONHUMAN; PRIORITY JOURNAL; PROTEIN ASSEMBLY; PROTEIN FUNCTION; PROTEIN PROTEIN INTERACTION; PROTEIN TRANSPORT; RAT; SYNAPSE VESICLE;

ADAPTOR PROTEINS, VESICULAR TRANSPORT; ANIMALS; CALCIUM SIGNALING; CELLS, CULTURED; EXOCYTOSIS; INTRACELLULAR CALCIUM-SENSING PROTEINS; MICE; MICE, KNOCKOUT; NERVE TISSUE PROTEINS; PROTEIN STRUCTURE, SECONDARY; RATS; RATS, MUTANT STRAINS; SNARE PROTEINS; SYNAPTIC TRANSMISSION; SYNAPTOTAGMIN I;

EID: 78649930845     PISSN: 08966273     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.neuron.2010.11.001     Document Type: Article

References (49)

1. Abbott L.F., Regehr W.G. Synaptic computation. Nature 2004, 431:796-803.
2. 2+-dependent multivalent binding of Syt1 to phospholipids. Nat. Struct. Mol. Biol. 2006, 13:209-217.
3. Bennett M.K., Calakos N., Scheller R.H. Syntaxin: a synaptic protein implicated in docking of synaptic vesicles at presynaptic active zones. Science 1992, 257:255-259.
4. 2+-triggered exocytosis by facilitating vesicle priming. Proc. Natl. Acad. Sci. USA 2008, 105:19538-19543.
5. 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 2002, 33:397-409.
6. Chicka M.C., Chapman E.R. Concurrent binding of complexin and synaptotagmin to liposome-embedded SNARE complexes. Biochemistry 2009, 48:657-659.
7. Fernandez-Chacon R., Konigstorfer A., Gerber S.H., Garcia J., Matos M.F., Stevens C.F., Brose N., Rizo J., Rosenmund C., Südhof T.C. Synaptotagmin I functions as a calcium regulator of release probability. Nature 2001, 410:41-49.
8. 2+ sensor for transmitter release at a central synapse. Cell 1994, 79:717-727.
9. Giraudo C.G., Eng W.S., Melia T.J., Rothman J.E. A clamping mechanism involved in SNARE-dependent exocytosis. Science 2006, 313:676-680.
10. Giraudo C.G., Garcia-Diaz A., Eng W.S., Chen Y., Hendrickson W.A., Melia T.J., Rothman J.E. Alternative zippering as an on-off switch for SNARE-mediated fusion. Science 2009, 323:512-516.
11. Giraudo C.G., Garcia-Diaz A., Eng W.S., Yamamoto A., Melia T.J., Rothman J.E. Distinct domains of complexins bind SNARE complexes and clamp fusion in vitro. J. Biol. Chem. 2008, 283:21211-21219.
12. 2+-sensor for spontaneous neurotransmitter release. Science 2010, 327:1614-1618.
13. 2+-regulated fusion. Cell 2009, 138:709-721.
14. Huntwork S., Littleton J.T. A complexin fusion clamp regulates spontaneous neurotransmitter release and synaptic growth. Nat. Neurosci. 2007, 10:1235-1237.
15. 2+ sensors for the fast and slow components of neurotransmitter release. J. Biol. Chem. 1995, 270:24898-24902.
16. Lu B., Song S., Shin Y.K. Accessory α-helix of complexin I can displace VAMP2 locally in the complexin-SNARE quaternary complex. J. Mol. Biol. 2010, 396:602-609.
17. Malsam J., Seiler F., Schollmeier Y., Rusu P., Krause J.M., Sollner T.H. The carboxy-terminal domain of complexin I stimulates liposome fusion. Proc. Natl. Acad. Sci. USA 2009, 106:2001-2006.
18. Martens S., Kozlov M.M., McMahon H.T. How synaptotagmin promotes membrane fusion. Science 2007, 316:1205-1208.
19. Martens S., McMahon H.T. Mechanisms of membrane fusion: disparate players and common principles. Nat. Rev. Mol. Cell Biol. 2008, 9:543-556.
20. Matteoli M., Takei K., Perin M.S., Südhof T.C., De Camilli P. Exo-endocytotic recycling of synaptic vesicles in developing processes of cultured hippocampal neurons. J. Cell Biol. 1992, 117:849-861.
21. Maximov A., Südhof T.C. Autonomous function of synaptotagmin 1 in triggering synchronous release independent of asynchronous release. Neuron 2005, 48:547-554.
22. Maximov A., Tang J., Yang X., Pang Z.P., Südhof T.C. Complexin controls the force transfer from SNARE complexes to membranes in fusion. Science 2009, 323:516-521.
23. McMahon H.T., Missler M., Li C., Südhof T.C. Complexins: cytosolic proteins that regulate SNAP receptor function. Cell 1995, 83:111-119.
24. ++ signals. Cell Calcium 1998, 24:345-357.
25. Neher E., Sakaba T. Multiple roles of calcium ions in the regulation of neurotransmitter release. Neuron 2008, 59:861-872.
26. Okamoto M., Südhof T.C. Mints, Munc18-interacting proteins in synaptic vesicle exocytosis. J. Biol. Chem. 1997, 272:31459-31464.
27. Pan B., Zucker R.S. A general model of synaptic transmission and short-term plasticity. Neuron 2009, 62:539-554.
28. 2+-dependent soluble N-ethylmaleimide-sensitive factor attachment protein receptor complex binding in synaptic exocytosis. J. Neurosci. 2006, 26:12556-12565.
29. 2+-triggered neurotransmitter release. EMBO J. 2006, 25:2039-2050.
30. Perin M.S., Brose N., Jahn R., Südhof T.C. Domain structure of synaptotagmin (p65). J. Biol. Chem. 1991, 266:623-629.
31. 2+-dependent neurotransmitter release. Cell 2001, 104:71-81.
32. Rizo J., Rosenmund C. Synaptic vesicle fusion. Nat. Struct. Mol. Biol. 2008, 15:665-674.
33. Rosenmund C., Stevens C.F. Definition of the readily releasable pool of vesicles at hippocampal synapses. Neuron 1996, 16:1197-1207.
34. Sara Y., Virmani T., Deák F., Liu X., Kavalali E.T. An isolated pool of vesicles recycles at rest and drives spontaneous neurotransmission. Neuron 2005, 45:563-573.
35. 2+-synaptotagmin I. Nat. Struct. Mol. Biol. 2006, 13:748-750.
36. Seiler F., Malsam J., Krause J.M., Sollner T.H. A role of complexin-lipid interactions in membrane fusion. FEBS Lett. 2009, 583:2343-2348.
37. 2+-dependent trans interaction with phospholipids. Nat. Struct. Mol. Biol. 2007, 14:904-911.
38. Stein A., Weber G., Wahl M.C., Jahn R. Helical extension of the neuronal SNARE complex into the membrane. Nature 2009, 460:525-528.
39. Strenzke N., Chanda S., Kopp-Scheinpflug C., Khimich D., Reim K., Bulankina A.V., Neef A., Wolf F., Brose N., Xu-Friedman M.A., Moser T. Complexin-I is required for high-fidelity transmission at the endbulb of held auditory synapse. J. Neurosci. 2009, 29:7991-8004.
40. Südhof T.C. The synaptic vesicle cycle. Annu. Rev. Neurosci. 2004, 27:509-547.
41. Südhof T.C., Rothman J.E. Membrane fusion: grappling with SNARE and SM proteins. Science 2009, 323:474-477.
42. 2+-sensor model for neurotransmitter release in a central synapse. Nature 2007, 450:676-682.
43. Tang J., Maximov A., Shin O.H., Dai H., Rizo J., Südhof T.C. A complexin/synaptotagmin 1 switch controls fast synaptic vesicle exocytosis. Cell 2006, 126:1175-1187.
44. Tokumaru H., Shimizu-Okabe C., Abe T. Direct interaction of SNARE complex binding protein synaphin/complexin with calcium sensor synaptotagmin 1. Brain Cell Biol. 2008, 36:173-189.
45. 2+ sensor for spontaneous release. Nat. Neurosci. 2009, 12:759-766.
46. Xue M., Reim K., Chen X., Chao H.T., Deng H., Rizo J., Brose N., Rosenmund C. Distinct domains of complexin I differentially regulate neurotransmitter release. Nat. Struct. Mol. Biol. 2007, 14:949-958.
47. Xue M., Lin Y.Q., Pan H., Reim K., Deng H., Bellen H.J., Rosenmund C. Tilting the balance between facilitatory and inhibitory functions of mammalian and Drosophila Complexins orchestrates synaptic vesicle exocytosis. Neuron 2009, 64:367-380.
48. Xue M., Craig T.K., Xu J., Chao H.T., Rizo J., Rosenmund C. Binding of the complexin N terminus to the SNARE complex potentiates synaptic-vesicle fusogenicity. Nat. Struct. Mol. Biol. 2010, 17:568-575.
49. 2+ stimulate SNARE-mediated membrane fusion. Nat. Struct. Mol. Biol. 2008, 15:707-713.