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A molecular toggle after exocytosis sequesters the presynaptic syntaxin1a molecules involved in prior vesicle fusion

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  • Deirdre M. Kavanagh

    (Institute of Biological Chemistry, Biophysics and Bioengineering, Heriot Watt University
    Edinburgh Super-Resolution Imaging Consortium, www.esric.org)

  • Annya M. Smyth

    (Institute of Biological Chemistry, Biophysics and Bioengineering, Heriot Watt University
    Edinburgh Super-Resolution Imaging Consortium, www.esric.org
    Centre for Integrative Physiology, University of Edinburgh, George Square
    Present address: Research Governance & QA Office, University of Edinburgh, The Queen’s Medical Research Institute, 47 Little France Crescent, Edinburgh EH16 4TJ, UK)

  • Kirsty J. Martin

    (Institute of Biological Chemistry, Biophysics and Bioengineering, Heriot Watt University
    Edinburgh Super-Resolution Imaging Consortium, www.esric.org
    Present address: Beatson Institute for Cancer Research, Switchback Road, Bearsden, Glasgow G61 1BD, UK)

  • Alison Dun

    (Institute of Biological Chemistry, Biophysics and Bioengineering, Heriot Watt University
    Edinburgh Super-Resolution Imaging Consortium, www.esric.org)

  • Euan R. Brown

    (Institute of Biological Chemistry, Biophysics and Bioengineering, Heriot Watt University
    Edinburgh Super-Resolution Imaging Consortium, www.esric.org)

  • Sarah Gordon

    (Centre for Integrative Physiology, University of Edinburgh, George Square)

  • Karen J. Smillie

    (Centre for Integrative Physiology, University of Edinburgh, George Square)

  • Luke H. Chamberlain

    (Strathclyde Institute of Pharmacy and Biomedical Sciences)

  • Rhodri S. Wilson

    (Institute of Biological Chemistry, Biophysics and Bioengineering, Heriot Watt University
    Edinburgh Super-Resolution Imaging Consortium, www.esric.org)

  • Lei Yang

    (Institute of Biological Chemistry, Biophysics and Bioengineering, Heriot Watt University
    Edinburgh Super-Resolution Imaging Consortium, www.esric.org)

  • Weiping Lu

    (Institute of Biological Chemistry, Biophysics and Bioengineering, Heriot Watt University
    Edinburgh Super-Resolution Imaging Consortium, www.esric.org)

  • Michael A. Cousin

    (Centre for Integrative Physiology, University of Edinburgh, George Square)

  • Colin Rickman

    (Institute of Biological Chemistry, Biophysics and Bioengineering, Heriot Watt University
    Edinburgh Super-Resolution Imaging Consortium, www.esric.org)

  • Rory R. Duncan

    (Institute of Biological Chemistry, Biophysics and Bioengineering, Heriot Watt University
    Edinburgh Super-Resolution Imaging Consortium, www.esric.org)

Abstract

Neuronal synapses are among the most scrutinized of cellular systems, serving as a model for all membrane trafficking studies. Despite this, synaptic biology has proven difficult to interrogate directly in situ due to the small size and dynamic nature of central synapses and the molecules within them. Here we determine the spatial and temporal interaction status of presynaptic proteins, imaging large cohorts of single molecules inside active synapses. Measuring rapid interaction dynamics during synaptic depolarization identified the small number of syntaxin1a and munc18-1 protein molecules required to support synaptic vesicle exocytosis. After vesicle fusion and subsequent SNARE complex disassembly, a prompt switch in syntaxin1a and munc18-1-binding mode, regulated by charge alteration on the syntaxin1a N-terminal, sequesters monomeric syntaxin1a from other disassembled fusion complex components, preventing ectopic SNARE complex formation, readying the synapse for subsequent rounds of neurotransmission.

Suggested Citation

  • Deirdre M. Kavanagh & Annya M. Smyth & Kirsty J. Martin & Alison Dun & Euan R. Brown & Sarah Gordon & Karen J. Smillie & Luke H. Chamberlain & Rhodri S. Wilson & Lei Yang & Weiping Lu & Michael A. Cou, 2014. "A molecular toggle after exocytosis sequesters the presynaptic syntaxin1a molecules involved in prior vesicle fusion," Nature Communications, Nature, vol. 5(1), pages 1-14, December.
    • Handle: RePEc:nat:natcom:v:5:y:2014:i:1:d:10.1038_ncomms6774
    DOI: 10.1038/ncomms6774
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    Cited by:

    1. Aske L. Ejdrup & Matthew D. Lycas & Niels Lorenzen & Ainoa Konomi & Freja Herborg & Kenneth L. Madsen & Ulrik Gether, 2022. "A density-based enrichment measure for assessing colocalization in single-molecule localization microscopy data," Nature Communications, Nature, vol. 13(1), pages 1-10, December.

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