Interaction of synaptotagmin with lipid bilayers, analyzed by single-molecule force spectroscopy

Biophysical Journal

Volumn 99, Issue 8, 2010, Pages 2550-2558

  Takahashi, Hirohide ^a   Shahin, Victor ^b,c   Henderson, Robert M ^b   Takeyasu, Kunio ^a   Edwardson, J Michael ^b  

^a KYOTO UNIVERSITY   (Japan)

^b UNIVERSITY OF CAMBRIDGE   (United Kingdom)

^c UNIVERSITY OF MÜNSTER   (Germany)

Author keywords

[No Author keywords available]

Indexed keywords

EID: 78049345303     PISSN: 00063495     EISSN: 15420086     Source Type: Journal    
DOI: 10.1016/j.bpj.2010.08.047     Document Type: Article

References (52)

1. Südhof, T. C. 2004. The synaptic vesicle cycle. Annu. Rev. Neurosci. 27:509-547.
2. Chapman, E. R. 2008. How does synaptotagmin trigger neurotransmitter release? Annu. Rev. Biochem. 77:615-641.
3. 2+-triggered neurotransmitter release. EMBO J. 25:2039-2050.
4. 2A polylysine motif. Genesis. 47:337-345.
5. 2+. Nat. Struct. Mol. Biol. 15:827-835.
6. 2+ ions bind to the tip of a C2-domain? EMBO J. 17:3921-3930.
7. Fernandez, I., D. Araç, ⋯, J. Rizo. 2001. Three-dimensional structure of the synaptotagmin 1 C2B-domain: Synaptotagmin 1 as a phospholipid binding machine. Neuron. 32:1057-1069.
8. Brose, N., A. G. Petrenko,., R. Jahn. 1992. Synaptotagmin: A calcium sensor on the synaptic vesicle surface. Science. 256:1021-1025.
9. 2+/phospholipid binding. J. Biol. Chem. 268:26386-26390.
10. Chapman, E. R., and R. Jahn. 1994. Calcium-dependent interaction of the cytoplasmic region of synaptotagmin with membranes. Autonomous function of a single C2-homologous domain. J. Biol. Chem. 269:5735-5741.
11. 2+-triggered simultaneous membrane penetration of the tandem C2-domains of synaptotagmin I. Biophys. J. 91:1767-1777.
12. Schiavo, G., Q.-M. Gu, ⋯, J. E. Rothman. 1996. Calcium-dependent switching of the specificity of phosphoinositide binding to synaptotagmin. Proc. Natl. Acad. Sci. USA. 93:13327-13332.
13. Bai, J., W. C. Tucker, and E. R. Chapman. 2004. PIP2 increases the speed of response of synaptotagmin and steers its membrane-penetration activity toward the plasma membrane. Nat. Struct. Mol. Biol. 11:36-44.
14. 2+ binding to synaptotagmin-1 C2 domains mediate neurotransmitter release. Proc. Natl. Acad. Sci. USA. 106:16469-16474.
15. 2+-dependent and -independent activities of neural and non-neural synaptotagmins. Nature. 375:594-599.
16. 2+ regulates the interaction between synaptotagmin and syntaxin 1. J. Biol. Chem. 270:23667-23671.
17. Schiavo, G., G. Stenbeck, ⋯, T. H. Söllner. 1997. 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. 94:997-1001.
18. Rickman, C., J. L. Jiménez, ⋯, B. Davletov. 2006. Conserved prefusion protein assembly in regulated exocytosis. Mol. Biol. Cell. 17:283-294.
19. 2+-triggered exocytosis. Neuron. 34:599-611.
20. Tucker, W. C., J. M. Edwardson, ⋯, E. R. Chapman. 2003. Identification of synaptotagmin effectors via acute inhibition of secretion from cracked PC12 cells. J. Cell Biol. 162:199-209.
21. 2+-regulated membrane fusion by synaptotagmin and SNAREs. Science. 304:435-438.
22. 2+-synaptotagmin directly regulates t-SNARE function during reconstituted membrane fusion. Nat. Struct. Mol. Biol. 13:323-330.
23. Damer, C. K., and C. E. Creutz. 1994. Synergistic membrane interactions of the two C2 domains of synaptotagmin. J. Biol. Chem. 269:31115-31123.
24. 2+binding loop of synaptotagmin with lipid bilayers. J. Biol. Chem. 273:13995-14001.
25. 2+ and assembly with the core SNARE complex onto membranes. Neuron. 24:363-376.
26. Herrick, D. Z., S. Sterbling, ⋯, D. S. Cafiso. 2006. Position of synaptotagmin I at the membrane interface: Cooperative interactions of tandem C2 domains. Biochemistry. 45:9668-9674.
27. Shahin, V., D. Datta, ⋯, J. M. Edwardson. 2008. Synaptotagmin perturbs the structure of phospholipid bilayers. Biochemistry. 47:2143-2152.
28. 2+-dependent multivalent binding of synaptotagmin- 1 to phospholipids. Nat. Struct. Mol. Biol. 13:209-217.
29. Mackler, J. M., and N. E. Reist. 2001. Mutations in the second C2 domain of synaptotagmin disrupt synaptic transmission at Drosophila neuromuscular junctions. J. Comp. Neurol. 436:4-16.
30. 2+-independent stage of synaptic vesicle priming in vivo. Mol. Biol. Cell. 17:5211-5226.
31. 2+-driven molecular hammer. Biophys. J. 92:1409-1418.
32. Wu, Y., Y. He, ⋯, S. F. Sui. 2003. Visualization of synaptotagmin I oligomers assembled onto lipid monolayers. Proc. Natl. Acad. Sci. USA. 100:2082-2087.
33. Yoshimura, S. H., H. Takahashi, ⋯, K. Takeyasu. 2006. Development of glutathione-coupled cantilever for the single-molecule force measurement by scanning force microscopy. FEBS Lett. 580:3961-3965.
34. Kienberger, F., V. P. Pastushenko, ⋯, P. Hinterdorfer. 2000. Static and dynamic properties of single poly(ethylene glycol) molecules investigated by force spectroscopy. Single Mol. 1:123-128.
35. Otsuka, S., S. Iwasaka, ⋯, S. H. Yoshimura. 2008. Individual binding pockets of importin-b for FG-nucleoporins have different binding properties and different sensitivities to RanGTP. Proc. Natl. Acad. Sci. USA. 105:16101-16106.
36. Lawrence, J. C., D. E. Saslowsky, ⋯, R. M. Henderson. 2003. Realtime analysis of the effects of cholesterol on lipid raft behavior using atomic force microscopy. Biophys. J. 84:1827-1832.
37. Sprong, H., P. van der Sluijs, and G. van Meer. 2001. How proteins move lipids and lipids move proteins. Nat. Rev. Mol. Cell Biol. 2:504-513.
38. Tamm, L. K., and H. M. McConnell. 1985. Supported phospholipid bilayers. Biophys. J. 47:105-113.
39. Kienberger, F., G. Kada, ⋯, P. Hinterdorfer. 2005. Single molecule studies of antibody-antigen interaction strength versus intra-molecular antigen stability. J. Mol. Biol. 347:597-606.
40. Stevens, C. F., and J. M. Sullivan. 2003. The synaptotagmin C2A domain is part of the calcium sensor controlling fast synaptic transmission. Neuron. 39:299-308.
41. 2+ binding in the C2A domain. Nature. 418:336-340.
42. Fernández-Chacón, R., A. Königstorfer,., T.C. Südhof. 2001. Synaptotagmin I functions as a calcium regulator of release probability. Nature. 410:41-49.
43. 2+ affinity of synaptotagmin 1. Proc. Natl. Acad. Sci. USA. 102:18664-18669.
44. 2+binding motif of synaptotagmin is required for synaptic transmission in vivo. Nature. 418:340-344.
45. 2+-dependent neurotransmitter release. J. Neurosci. 24:8542-8550.
46. 2+-dependent trans interaction with phospholipids. Nat. Struct. Mol. Biol. 14:904-911.
47. 2+-triggered fusion in vitro: Critical residues revealed by scanning alanine mutagenesis. J. Biol. Chem. 283:31763-31775.
48. Frazier, A. A., C. R. Roller, ⋯, D. S. Cafiso. 2003. Membrane-bound orientation and position of the synaptotagmin I C2A domain by sitedirected spin labeling. Biochemistry. 42:96-105.
49. Rufener, E., A. A. Frazier, ⋯, D. S. Cafiso. 2005. Membrane-bound orientation and position of the synaptotagmin C2B domain determined by site-directed spin labeling. Biochemistry. 44:18-28.
50. Kuo,W., D. Z. Herrick,., D. S. Cafiso. 2009. The calcium-dependent and calcium-independent membrane binding of synaptotagmin 1: Two modes of C2B binding. J. Mol. Biol. 387:284-294.
51. 2+ binding to C2 domains of synaptotagmin 1. J. Biol. Chem. 281:15845-15852.
52. 2+-sensing module essential for exocytosis. J. Cell Biol. 150:1125-1136.