Studying calcium-triggered vesicle fusion in a single vesicle-vesicle content and lipid-mixing system

Nature Protocols

Volumn 8, Issue 1, 2013, Pages 1-16

  Kyoung, Minjoung ^a,d   Zhang, Yunxiang ^a,b,c   Diao, Jiajie ^a   Chu, Steven ^b,c   Brunger, Axel T ^a  

^a STANFORD UNIVERSITY   (United States)

^b LAWRENCE BERKELEY NATIONAL LABORATORY   (United States)

^c UNIVERSITY OF CALIFORNIA   (United States)

^d UNIVERSITY OF MARYLAND BALTIMORE COUNTY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CALCIUM; FLUORESCENT DYE; LIPID; SYNAPTOSOMAL ASSOCIATED PROTEIN 25;

ARTICLE; CALIBRATION; CLINICAL PROTOCOL; DATA ANALYSIS; EXPERIMENTAL DESIGN; FLUORESCENCE IMAGING; FLUORESCENCE MICROSCOPY; IMAGE ANALYSIS; IMMOBILIZATION; INCUBATION TEMPERATURE; INCUBATION TIME; MATERIAL COATING; MEMBRANE FUSION; MEMBRANE VESICLE; MICROSCOPY; PRIORITY JOURNAL; PROCESS DESIGN; PROCESS MONITORING; PROTEIN EXPRESSION; PROTEIN PURIFICATION; SINGLE VESICLE VESICLE MICROSCOPY;

CALCIUM; IMAGE PROCESSING, COMPUTER-ASSISTED; LIPID METABOLISM; MEMBRANE FUSION; MICROSCOPY, FLUORESCENCE; R-SNARE PROTEINS; SYNAPTIC VESICLES; SYNAPTOSOMAL-ASSOCIATED PROTEIN 25; SYNAPTOTAGMIN I; SYNAPTOTAGMINS;

EID: 84872008490     PISSN: 17542189     EISSN: 17502799     Source Type: Journal    
DOI: 10.1038/nprot.2012.134     Document Type: Article

References (42)

1. Katz, B. & Miledi, R. Spontaneous and evoked activity of motor nerve endings in calcium Ringer. J. Physiol. 203, 689-706 (1969).
2. Sudhof, T.C. The synaptic vesicle cycle. Annu. Rev. Neurosci. 27, 509-547 (2004). (Pubitemid 39050412)
3. Bean, A.J., Zhang, X. & Hokfelt, T. Peptide secretion: what do we know? FASEB J. 8, 630-638 (1994). (Pubitemid 24198680)
4. Voets, T., Neher, E. & Moser, T. Mechanisms underlying phasic and sustained secretion in chromaffin cells from mouse adrenal slices. Neuron 23, 607-615 (1999). (Pubitemid 29359930)
5. Lindau, M. & Gomperts, B.D. Techniques and concepts in exocytosis: focus on mast cells. Biochim. Biophys. Acta. 1071, 429-471 (1991). (Pubitemid 121002498)
6. Sollner, T. et al. SNAP receptors implicated in vesicle targeting and fusion. Nature 362, 318-324 (1993). (Pubitemid 23101303)
7. Sutton, R.B., Fasshauer, D., Jahn, R. & Brunger, A.T. Crystal structure of a SNARE complex involved in synaptic exocytosis at 2.4 Å resolution. Nature 395, 347-353 (1998). (Pubitemid 28450677)
8. 2+-triggered exocytosis. Ann. Rev. Biophys. Biomol. Struct. 35, 135-160 (2006). (Pubitemid 43877373)
9. Tang, J. et al. A complexin/synaptotagmin 1 switch controls fast synaptic vesicle exocytosis. Cell 126, 1175-1187 (2006). (Pubitemid 44380295)
10. Sudhof, T.C. & Rothman, J.E. Membrane fusion: grappling with SNARE and SM proteins. Science 323, 474-477 (2009).
11. Ma, C., Li, W., Xu, Y. & Rizo, J. Munc13 mediates the transition from the closed syntaxin-Munc18 complex to the SNARE complex. Nat. Struct. Mol. Biol. 18, 542-549 (2011).
12. Weber, T. et al. SNAREpins: minimal machinery for membrane fusion. Cell 92, 759-772 (1998). (Pubitemid 28155315)
13. Bowen, M.E., Weninger, K., Brunger, A.T. & Chu, S. Single molecule observation of liposome-bilayer fusion thermally induced by soluble N-ethyl maleimide sensitive-factor attachment protein receptors (SNAREs). Biophys. J. 87, 3569-3584 (2004). (Pubitemid 40468609)
14. 2+-triggered content mixing from lipid exchange for mechanistic studies of neurotransmitter release. Proc. Natl. Acad. Sci. USA 108, E304-E313 (2011).
15. Floyd, D.L., Ragains, J.R., Skehel, J.J., Harrison, S.C. & van Oijen, A.M. Single-particle kinetics of influenza virus membrane fusion. Proc. Natl. Acad. Sci. USA 105, 15382-15387 (2008).
16. Jun, Y. & Wickner, W. Assays of vacuole fusion resolve the stages of docking, lipid mixing, and content mixing. Proc. Natl. Acad. Sci. USA 104, 13010-13015 (2007). (Pubitemid 351737584)
17. Chan, Y.H.M., van Lengerich, B. & Boxer, S.G. Effects of linker sequences on vesicle fusion mediated by lipid-anchored DNA oligonucleotides. Proc. Natl. Acad. Sci. USA 106, 979-984 (2009).
18. Diao, J. et al. Synaptic proteins promote calcium-triggered fast transition from point contact to full fusion. eLife 1, e00109 (2012).
19. Cypionka, A. et al. Discrimination between docking and fusion of liposomes reconstituted with neuronal SNARE-proteins using FCS. Proc. Natl. Acad. Sci. USA 106, 18575-18580 (2009).
20. Yoon, T.Y., Okumus, B., Zhang, F., Shin, Y.K. & Ha, T. Multiple intermediates in SNARE-induced membrane fusion. Proc. Natl. Acad. Sci. USA 103, 19731-19736 (2006). (Pubitemid 46037499)
21. Karatekin, E. et al. A fast, single-vesicle fusion assay mimics physiological SNARE requirements. Proc. Natl. Acad. Sci. USA 107, 3517-3521 (2010).
22. 2+-dependent stimulation of vesicle fusion by membrane-anchored synaptotagmin 1. Science 328, 760-763 (2010).
23. Karatekin, E. & Rothman, J.E. Fusion of single proteoliposomes with planar, cushioned bilayers in microfluidic flow cells. Nat. Protoc. 7, 903-920 (2012).
24. Wang, T., Smith, E.A., Chapman, E.R. & Weisshaar, J.C. Lipid mixing and content release in single-vesicle, SNARE-driven fusion assay with 1-5 ms resolution. Biophys. J. 96, 4122-4131 (2009).
25. Diao, J. et al. A single-vesicle content mixing assay for SNARE-mediated membrane fusion. Nat. Commun. 1, 54 (2010).
26. Diao, J. et al. A single vesicle-vesicle fusion assay for in vitro studies of SNAREs and accessory proteins. Nat. Protoc. 7, 921-934 (2012).
27. Schneggenburger, R. & Neher, E. Intracellular calcium dependence of transmitter release rates at a fast central synapse. Nature 406, 889-893 (2000).
28. 2+-sensor model for neurotransmitter release in a central synapse. Nature 450, 676-U674 (2007).
29. Vennekate, W. et al. Cis- and trans-membrane interactions of synaptotagmin-1. Proc. Natl. Acad. Sci. USA 109, 11037-11042 (2012).
30. Gao, Y. et al. Single reconstituted neuronal SNARE complexes zipper in three distinct stages. Science (2012).
31. Weninger, K., Bowen, M.E., Chu, S. & Brunger, A.T. Single-molecule studies of SNARE complex assembly reveal parallel and antiparallel configurations. Proc. Natl. Acad. Sci. USA 100, 14800-14805 (2003). (Pubitemid 37517971)
32. 2+-induced structural changes in lipid monolayers: implications for synaptic vesicle exocytosis. Biophys. J. 102, 1394-1402 (2012).
33. Heidelberger, R., Heinemann, C., Neher, E. & Matthews, G. Calcium dependence of the rate of exocytosis in a synaptic terminal. Nature 371, 513-515 (1994). (Pubitemid 24306608)
34. Wang, Z., Liu, H., Gu, Y. & Chapman, E.R. Reconstituted synaptotagmin I mediates vesicle docking, priming, and fusion. J. Cell. Biol. 195, 1159-1170 (2011).
35. Hernandez, J.M. et al. Membrane fusion intermediates via directional and full assembly of the SNARE complex. Science 336, 1581-1584 (2012).
36. van den Bogaart, G. et al. Membrane protein sequestering by ionic protein-lipid interactions. Nature 479, 552-555 (2011).
37. Takamori, S. et al. Molecular anatomy of a trafficking organelle. Cell 127, 831-846 (2006). (Pubitemid 44716256)
38. Roy, R., Hohng, S. & Ha, T. A practical guide to single-molecule FRET. Nat. Methods 5, 507-516 (2008). (Pubitemid 351761757)
39. Zhang, Y., Sivasankar, S., Nelson, W.J. & Chu, S. Resolving cadherin interactions and binding cooperativity at the single-molecule level. Proc. Natl. Acad. Sci. USA 106, 109-114 (2009).
40. Pertsinidis, A., Zhang, Y. & Chu, S. Subnanometre single-molecule localization, registration and distance measurements. Nature 466, 647-651 (2010).
41. Bates, M., Dempsey, G.T., Chen, K.H. & Zhuang, X. Multicolor super-resolution fluorescence imaging via multi-parameter fluorophore detection. Chemphyschem. 13, 99-107 (2012).
42. Kiessling, V., Domanska, M.K. & Tamm, L.K. Single SNARE-mediated vesicle fusion observed in vitro by polarized TIRFM. Biophys. J. 99, 4047-4055 (2010).