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

Biophys J. 2005 Jul;89(1):690-702. doi: 10.1529/biophysj.104.054064. Epub 2005 Apr 8.

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.

Publication types

  • 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.

MeSH terms

  • Adaptor Proteins, Vesicular Transport
  • Animals
  • Antigens, Surface / chemistry
  • Biophysics / methods*
  • Calcium / chemistry
  • Calcium / 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*

Substances

  • 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