Home LiteratureArticle Details
PMID: 15821166 Published · ppublish English Journal Article Research Support, N.I.H., Extramural Research Support, Non-U.S. Gov't Research Support, U.S. Gov't, Non-P.H.S. Research Support, U.S. Gov't, P.H.S.

Single-molecule studies of synaptotagmin and complexin binding to the SNARE complex.

Biophysical journal ·Vol. 89 ·No. 1 ·2005-07-00 ·Pages 690-702

Bowen ME, Weninger K, Ernst J, Chu S, Brunger AT

Abstract

The assembly of multiprotein complexes at the membrane interface governs many signaling processes in cells. However, very few methods exist for obtaining biophysical information about protein complex formation at the membrane. We used single molecule fluorescence resonance energy transfer to study complexin and synaptotagmin interactions with the SNARE complex in deposited lipid bilayers. Using total internal reflectance microscopy, individual binding events at the membrane could be resolved despite an excess of unbound protein in solution. Fluorescence resonance energy transfer (FRET)-efficiency derived distances for the complexin-SNARE interaction were consistent with the crystal structure of the complexin-SNARE complex. The unstructured N-terminal region of complexin showed broad distributions of FRET efficiencies to the SNARE complex, suggesting that information on conformational variability can be obtained from FRET efficiency distributions. The low-affinity interaction of synaptotagmin with the SNARE complex changed dramatically upon addition of Ca2+ with high FRET efficiency interactions appearing between the C2B domain and linker domains of synaptotagmin and the membrane proximal portion of the SNARE complex. These results demonstrate that single molecule FRET can be used as a "spectroscopic ruler" to simultaneously gain structural and kinetic information about transient multiprotein complexes at the membrane interface.

MeSH Terms
Adaptor Proteins, Vesicular Transport Animals Antigens, Surface/chemistry Biophysics/methods Calcium/chemistry,metabolism Calcium-Binding Proteins/chemistry Cell Membrane/metabolism Crystallography, X-Ray Cytoplasm/metabolism Fluorescence Resonance Energy Transfer/methods Kinetics Lipid Bilayers/chemistry Membrane Glycoproteins/chemistry Membrane Proteins/chemistry Mutation Nerve Tissue Proteins/chemistry Protein Binding Protein Structure, Tertiary Proteins/chemistry R-SNARE Proteins Rats SNARE Proteins Spectrophotometry Synaptosomal-Associated Protein 25 Synaptotagmins Syntaxin 1 Vesicular Transport Proteins/chemistry
Chemicals
Adaptor Proteins, Vesicular Transport Antigens, Surface Calcium-Binding Proteins Lipid Bilayers Membrane Glycoproteins Membrane Proteins Nerve Tissue Proteins Proteins R-SNARE Proteins SNARE Proteins Snap25 protein, rat Synaptosomal-Associated Protein 25 Syntaxin 1 Vesicular Transport Proteins complexin I Synaptotagmins Calcium
Authors & Affiliations
5 authors, click to expand affiliations / ORCID
Bowen Mark E
The Howard Hughes Medical Institute and Department of Molecular and Cellular Physiology, Stanford University, Stanford, California, USA.
Weninger Keith
Ernst James
Chu Steven
Brunger Axel T
References (71)
71 references, click to expand
  1. Synaptotagmin I, a Ca2+ sensor for neurotransmitter release.
    Trends Neurosci. 2003 Aug;26(8):413-22 PMID: 12900172
  2. The ATP-waiting conformation of rotating F1-ATPase revealed by single-pair fluorescence resonance energy transfer.
    Proc Natl Acad Sci U S A. 2003 Aug 5;100(16):9314-8 PMID: 12876203
  3. Controversies in synaptic vesicle exocytosis.
    J Cell Sci. 2003 Sep 15;116(Pt 18):3661-6 PMID: 12917353
  4. Cell biology of the presynaptic terminal.
    Annu Rev Neurosci. 2003;26:701-28 PMID: 14527272
  5. Single-molecule studies of SNARE complex assembly reveal parallel and antiparallel configurations.
    Proc Natl Acad Sci U S A. 2003 Dec 9;100(25):14800-5 PMID: 14657376
  6. Single-molecule fluorescence resonance energy transfer reveals a dynamic equilibrium between closed and open conformations of syntaxin 1.
    Proc Natl Acad Sci U S A. 2003 Dec 23;100(26):15516-21 PMID: 14668446
  7. Modeller: generation and refinement of homology-based protein structure models.
    Methods Enzymol. 2003;374:461-91 PMID: 14696385
  8. Dynamics and folding of single two-stranded coiled-coil peptides studied by fluorescent energy transfer confocal microscopy.
    Proc Natl Acad Sci U S A. 2000 Nov 21;97(24):13021-6 PMID: 11087856
  9. Synaptotagmin I functions as a calcium regulator of release probability.
    Nature. 2001 Mar 1;410(6824):41-9 PMID: 11242035
  10. The C2B domain of synaptotagmin I is a Ca2+-binding module.
    Biochemistry. 2001 May 22;40(20):5854-60 PMID: 11352720
  11. Three-dimensional structure of the synaptotagmin 1 C2B-domain: synaptotagmin 1 as a phospholipid binding machine.
    Neuron. 2001 Dec 20;32(6):1057-69 PMID: 11754837
  12. Three-dimensional structure of the complexin/SNARE complex.
    Neuron. 2002 Jan 31;33(3):397-409 PMID: 11832227
  13. Synaptic function modulated by changes in the ratio of synaptotagmin I and IV.
    Nature. 1999 Aug 19;400(6746):757-60 PMID: 10466723
  14. Polyproline and the "spectroscopic ruler" revisited with single-molecule fluorescence.
    Proc Natl Acad Sci U S A. 2005 Feb 22;102(8):2754-9 PMID: 15699337
  15. Crystal structure of the cytosolic C2A-C2B domains of synaptotagmin III. Implications for Ca(+2)-independent snare complex interaction.
    J Cell Biol. 1999 Nov 1;147(3):589-98 PMID: 10545502
  16. Kinetics of synaptotagmin responses to Ca2+ and assembly with the core SNARE complex onto membranes.
    Neuron. 1999 Oct;24(2):363-76 PMID: 10571230
  17. The C terminus of SNAP25 is essential for Ca(2+)-dependent binding of synaptotagmin to SNARE complexes.
    J Biol Chem. 2000 Mar 3;275(9):6328-36 PMID: 10692432
  18. Single-molecule protein folding: diffusion fluorescence resonance energy transfer studies of the denaturation of chymotrypsin inhibitor 2.
    Proc Natl Acad Sci U S A. 2000 May 9;97(10):5179-84 PMID: 10792044
  19. Selective interaction of complexin with the neuronal SNARE complex. Determination of the binding regions.
    J Biol Chem. 2000 Jun 30;275(26):19808-18 PMID: 10777504
  20. Rapid and selective binding to the synaptic SNARE complex suggests a modulatory role of complexins in neuroexocytosis.
    J Biol Chem. 2002 Mar 8;277(10):7838-48 PMID: 11751907
  21. Fluorescence resonance energy transfer (FRET) and competing processes in donor-acceptor substituted DNA strands: a comparative study of ensemble and single-molecule data.
    J Biotechnol. 2002 Jan;82(3):211-31 PMID: 11999691
  22. Correlating structural dynamics and function in single ribozyme molecules.
    Science. 2002 May 24;296(5572):1473-6 PMID: 12029135
  23. X-ray structure of a neuronal complexin-SNARE complex from squid.
    J Biol Chem. 2002 Jul 19;277(29):26517-23 PMID: 12004067
  24. Sealed with a twist: complexin and the synaptic SNARE complex.
    Trends Neurosci. 2002 Aug;25(8):381-3 PMID: 12127744
  25. PIP2 increases the speed of response of synaptotagmin and steers its membrane-penetration activity toward the plasma membrane.
    Nat Struct Mol Biol. 2004 Jan;11(1):36-44 PMID: 14718921
  26. The C2 domains of synaptotagmin--partners in exocytosis.
    Trends Biochem Sci. 2004 Mar;29(3):143-51 PMID: 15003272
  27. Fusion pore dynamics are regulated by synaptotagmin*t-SNARE interactions.
    Neuron. 2004 Mar 25;41(6):929-42 PMID: 15046725
  28. Reconstitution of Ca2+-regulated membrane fusion by synaptotagmin and SNAREs.
    Science. 2004 Apr 16;304(5669):435-8 PMID: 15044754
  29. Placing single-molecule T4 lysozyme enzymes on a bacterial cell surface: toward probing single-molecule enzymatic reaction in living cells.
    Biophys J. 2004 Jul;87(1):656-61 PMID: 15240499
  30. tRNA selection and kinetic proofreading in translation.
    Nat Struct Mol Biol. 2004 Oct;11(10):1008-14 PMID: 15448679
  31. Single molecule observation of liposome-bilayer fusion thermally induced by soluble N-ethyl maleimide sensitive-factor attachment protein receptors (SNAREs).
    Biophys J. 2004 Nov;87(5):3569-84 PMID: 15347585
  32. The timing of calcium action during neuromuscular transmission.
    J Physiol. 1967 Apr;189(3):535-44 PMID: 6040160
  33. Energy transfer: a spectroscopic ruler.
    Proc Natl Acad Sci U S A. 1967 Aug;58(2):719-26 PMID: 5233469
  34. Relationship between presynaptic calcium current and postsynaptic potential in squid giant synapse.
    Biophys J. 1981 Mar;33(3):323-51 PMID: 6261850
  35. Phenomenological theory of gel electrophoresis of protein-nucleic acid complexes.
    J Biol Chem. 1989 Oct 15;264(29):17032-40 PMID: 2793842
  36. Phospholipid binding by a synaptic vesicle protein homologous to the regulatory region of protein kinase C.
    Nature. 1990 May 17;345(6272):260-3 PMID: 2333096
  37. Domain structure of synaptotagmin (p65)
    J Biol Chem. 1991 Jan 5;266(1):623-9 PMID: 1985919
  38. Synaptotagmin: a calcium sensor on the synaptic vesicle surface.
    Science. 1992 May 15;256(5059):1021-5 PMID: 1589771
  39. Syntaxin: a synaptic protein implicated in docking of synaptic vesicles at presynaptic active zones.
    Science. 1992 Jul 10;257(5067):255-9 PMID: 1321498
  40. HPC-1 is associated with synaptotagmin and omega-conotoxin receptor.
    J Biol Chem. 1992 Dec 15;267(35):24925-8 PMID: 1334074
  41. Synaptic vesicle traffic: rush hour in the nerve terminal.
    J Neurochem. 1993 Jul;61(1):12-21 PMID: 8515256
  42. A protein assembly-disassembly pathway in vitro that may correspond to sequential steps of synaptic vesicle docking, activation, and fusion.
    Cell. 1993 Nov 5;75(3):409-18 PMID: 8221884
  43. A single C2 domain from synaptotagmin I is sufficient for high affinity Ca2+/phospholipid binding.
    J Biol Chem. 1993 Dec 15;268(35):26386-90 PMID: 8253763
  44. Calcium-dependent interaction of the cytoplasmic region of synaptotagmin with membranes. Autonomous function of a single C2-homologous domain.
    J Biol Chem. 1994 Feb 25;269(8):5735-41 PMID: 8119912
  45. Structure of the first C2 domain of synaptotagmin I: a novel Ca2+/phospholipid-binding fold.
    Cell. 1995 Mar 24;80(6):929-38 PMID: 7697723
  46. Ca(2+)-dependent and -independent activities of neural and non-neural synaptotagmins.
    Nature. 1995 Jun 15;375(6532):594-9 PMID: 7791877
  47. Complexins: cytosolic proteins that regulate SNAP receptor function.
    Cell. 1995 Oct 6;83(1):111-9 PMID: 7553862
  48. Ca2+ regulates the interaction between synaptotagmin and syntaxin 1.
    J Biol Chem. 1995 Oct 6;270(40):23667-71 PMID: 7559535
  49. Localization of synaptotagmin-binding domains on syntaxin.
    J Neurosci. 1996 Mar 15;16(6):1975-81 PMID: 8604041
  50. Synaptotagmins: C2-domain proteins that regulate membrane traffic.
    Neuron. 1996 Sep;17(3):379-88 PMID: 8816702
  51. Timing of neurotransmission at fast synapses in the mammalian brain.
    Nature. 1996 Nov 14;384(6605):170-2 PMID: 8906792
  52. Synaptotagmin-syntaxin interaction: the C2 domain as a Ca2+-dependent electrostatic switch.
    Neuron. 1997 Jan;18(1):133-42 PMID: 9010211
  53. 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 U S A. 1997 Feb 4;94(3):997-1001 PMID: 9023371
  54. SNAREpins: minimal machinery for membrane fusion.
    Cell. 1998 Mar 20;92(6):759-72 PMID: 9529252
  55. Identification of a minimal core of the synaptic SNARE complex sufficient for reversible assembly and disassembly.
    Biochemistry. 1998 Jul 21;37(29):10354-62 PMID: 9671503
  56. Crystal structure of a SNARE complex involved in synaptic exocytosis at 2.4 A resolution.
    Nature. 1998 Sep 24;395(6700):347-53 PMID: 9759724
  57. Solution structures of the Ca2+-free and Ca2+-bound C2A domain of synaptotagmin I: does Ca2+ induce a conformational change?
    Biochemistry. 1998 Nov 17;37(46):16106-15 PMID: 9819203
  58. Single-molecule fluorescence spectroscopy of enzyme conformational dynamics and cleavage mechanism.
    Proc Natl Acad Sci U S A. 1999 Feb 2;96(3):893-8 PMID: 9927664
  59. Single-pair fluorescence resonance energy transfer on freely diffusing molecules: observation of Förster distance dependence and subpopulations.
    Proc Natl Acad Sci U S A. 1999 Mar 30;96(7):3670-5 PMID: 10097095
  60. Ligand-induced conformational changes observed in single RNA molecules.
    Proc Natl Acad Sci U S A. 1999 Aug 3;96(16):9077-82 PMID: 10430898
  61. The C2B domain of synaptotagmin is a Ca(2+)-sensing module essential for exocytosis.
    J Cell Biol. 2000 Sep 4;150(5):1125-36 PMID: 10974000
  62. Vesicle-associated membrane protein-2/synaptobrevin binding to synaptotagmin I promotes O-glycosylation of synaptotagmin I.
    J Biol Chem. 2002 Aug 16;277(33):30351-8 PMID: 12048209
  63. Efficiencies of fluorescence resonance energy transfer and contact-mediated quenching in oligonucleotide probes.
    Nucleic Acids Res. 2002 Nov 1;30(21):e122 PMID: 12409481
  64. Mutational analysis of synaptobrevin transmembrane domain oligomerization.
    Biochemistry. 2002 Dec 31;41(52):15861-6 PMID: 12501216
  65. Sr2+ binding to the Ca2+ binding site of the synaptotagmin 1 C2B domain triggers fast exocytosis without stimulating SNARE interactions.
    Neuron. 2003 Jan 9;37(1):99-108 PMID: 12526776
  66. Mechanism of calcium-independent synaptotagmin binding to target SNAREs.
    J Biol Chem. 2003 Feb 21;278(8):5501-4 PMID: 12496268
  67. Membrane fusion.
    Cell. 2003 Feb 21;112(4):519-33 PMID: 12600315
  68. High resolution structure, stability, and synaptotagmin binding of a truncated neuronal SNARE complex.
    J Biol Chem. 2003 Mar 7;278(10):8630-6 PMID: 12496247
  69. Facile detection of protein-protein interactions by one-dimensional NMR spectroscopy.
    Biochemistry. 2003 Mar 18;42(10):2774-80 PMID: 12627942
  70. Investigations of bivalent antibody binding on fluid-supported phospholipid membranes: the effect of hapten density.
    J Am Chem Soc. 2003 Apr 23;125(16):4779-84 PMID: 12696896
  71. Fusion of cells by flipped SNAREs.
    Science. 2003 Jun 13;300(5626):1745-9 PMID: 12805548
Article Info
Journal
Biophysical journal
Abbr.
Biophys J
ISSN
0006-3495
Published
2005-07-00
Epub
2005-00-08
Pages
690-702
Language
English
Region
United States
NLM ID
0370626
PMCID
PMC1366567
Subset
IM
Grants
NIMH NIH HHS · R01 MH063105 · United States
NIMH NIH HHS · R01-MH63105-01 · United States
Analysis Services
Analysis Services

Contact

No. 2 Wenbo Road, Zhangqiu District, Jinan, Shandong

Qilu Normal University · Genelibs Bioinformatics Lab

750 Shunhua Rd, Jinan

2F, Bldg F, University Science Park

Tel: 0531-88819269

WeChat Official Account

Follow our WeChat subscription account for real-time updates and the latest in medical and biological research.


Business Email

E-mail: product@genelibs.com