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Articles, Cellular/Molecular

Dance of the SNAREs: Assembly and Rearrangements Detected with FRET at Neuronal Synapses

Vadim Degtyar, Ismail M. Hafez, Christopher Bray and Robert S. Zucker
Journal of Neuroscience 27 March 2013, 33 (13) 5507-5523; DOI: https://doi.org/10.1523/JNEUROSCI.2337-12.2013
Vadim Degtyar
Department of Molecular and Cell Biology, University of California, Berkeley, Berkeley, California 94720
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Ismail M. Hafez
Department of Molecular and Cell Biology, University of California, Berkeley, Berkeley, California 94720
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Christopher Bray
Department of Molecular and Cell Biology, University of California, Berkeley, Berkeley, California 94720
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Robert S. Zucker
Department of Molecular and Cell Biology, University of California, Berkeley, Berkeley, California 94720
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Abstract

Soluble N-ethylmaleimide-sensitive fusion protein attachment protein receptors (SNAREs) mediate vesicle fusion with the plasma membrane on activation by calcium binding to synaptotagmin. In the present study, we used fluorescence resonance energy transfer (FRET) and fluorescence lifetime imaging microscopy between fluorescently labeled SNARE proteins expressed in cultured rat hippocampal neurons to detect resting SNARE complexes, their conformational rearrangement on exocytosis, their disassembly before endocytosis of vesicular proteins, and SNARE assembly at newly docked vesicles. Assembled SNAREs are not only present in docked vesicles; unexpected residual “orphan SNARE complexes” also reside in para-active zone regions. Real-time changes in FRET between N-terminally labeled SNAP-25 and VAMP reported a reorientation of the SNARE motif upon exocytosis, SNARE disassembly in the active zone periphery, and SNARE reassembly in newly docked vesicles. With VAMP labeled C-terminally, decreased fluorescence in C-terminally labeled syntaxin (extracellular) reported trans-cis-conformational changes in SNAREs on vesicle fusion. After fusion SNAP-25 and syntaxin disperse along with VAMP, as well as the FRET signal itself, indicating diffusion of intact SNAREs after vesicle fusion but before their peripheral disassembly. Our measurements of spatiotemporal dynamics of SNARE conformational changes and movements refine models of SNARE function. Technical advances required to detect tiny changes in fluorescence in small fractions of labeled proteins in presynaptic boutons on a time scale of seconds permit the detection of rapid intermolecular interactions between small proportions of protein partners in cellular subcompartments.

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The Journal of Neuroscience: 33 (13)
Journal of Neuroscience
Vol. 33, Issue 13
27 Mar 2013
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Dance of the SNAREs: Assembly and Rearrangements Detected with FRET at Neuronal Synapses
Vadim Degtyar, Ismail M. Hafez, Christopher Bray, Robert S. Zucker
Journal of Neuroscience 27 March 2013, 33 (13) 5507-5523; DOI: 10.1523/JNEUROSCI.2337-12.2013

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Dance of the SNAREs: Assembly and Rearrangements Detected with FRET at Neuronal Synapses
Vadim Degtyar, Ismail M. Hafez, Christopher Bray, Robert S. Zucker
Journal of Neuroscience 27 March 2013, 33 (13) 5507-5523; DOI: 10.1523/JNEUROSCI.2337-12.2013
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