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In vivo single-molecule imaging of syntaxin1A reveals polyphosphoinositide- and activity-dependent trapping in presynaptic nanoclusters

Author

Listed:
  • Adekunle T. Bademosi

    (Clem Jones Centre for Ageing Dementia Research, Queensland Brain Institute, The University of Queensland)

  • Elsa Lauwers

    (VIB Center for the Biology of Disease
    Leuven Institute for Neurodegenerative Disease (LIND))

  • Pranesh Padmanabhan

    (Queensland Brain Institute, The University of Queensland)

  • Lorenzo Odierna

    (School of Biomedical Sciences, The University of Queensland)

  • Ye Jin Chai

    (Clem Jones Centre for Ageing Dementia Research, Queensland Brain Institute, The University of Queensland)

  • Andreas Papadopulos

    (Clem Jones Centre for Ageing Dementia Research, Queensland Brain Institute, The University of Queensland)

  • Geoffrey J. Goodhill

    (Queensland Brain Institute, The University of Queensland
    School of Mathematics and Physics, The University of Queensland)

  • Patrik Verstreken

    (VIB Center for the Biology of Disease
    Leuven Institute for Neurodegenerative Disease (LIND))

  • Bruno van Swinderen

    (Queensland Brain Institute, The University of Queensland)

  • Frédéric A. Meunier

    (Clem Jones Centre for Ageing Dementia Research, Queensland Brain Institute, The University of Queensland)

Abstract

Syntaxin1A is organized in nanoclusters that are critical for the docking and priming of secretory vesicles from neurosecretory cells. Whether and how these nanoclusters are affected by neurotransmitter release in nerve terminals from a living organism is unknown. Here we imaged photoconvertible syntaxin1A-mEos2 in the motor nerve terminal of Drosophila larvae by single-particle tracking photoactivation localization microscopy. Opto- and thermo-genetic neuronal stimulation increased syntaxin1A-mEos2 mobility, and reduced the size and molecular density of nanoclusters, suggesting an activity-dependent release of syntaxin1A from the confinement of nanoclusters. Syntaxin1A mobility was increased by mutating its polyphosphoinositide-binding site or preventing SNARE complex assembly via co-expression of tetanus toxin light chain. In contrast, syntaxin1A mobility was reduced by preventing SNARE complex disassembly. Our data demonstrate that polyphosphoinositide favours syntaxin1A trapping, and show that SNARE complex disassembly leads to syntaxin1A dissociation from nanoclusters. Lateral diffusion and trapping of syntaxin1A in nanoclusters therefore dynamically regulate neurotransmitter release.

Suggested Citation

  • Adekunle T. Bademosi & Elsa Lauwers & Pranesh Padmanabhan & Lorenzo Odierna & Ye Jin Chai & Andreas Papadopulos & Geoffrey J. Goodhill & Patrik Verstreken & Bruno van Swinderen & Frédéric A. Meunier, 2016. "In vivo single-molecule imaging of syntaxin1A reveals polyphosphoinositide- and activity-dependent trapping in presynaptic nanoclusters," Nature Communications, Nature, vol. 7(1), pages 1-17, December.
    • Handle: RePEc:nat:natcom:v:7:y:2016:i:1:d:10.1038_ncomms13660
    DOI: 10.1038/ncomms13660
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    Cited by:

    1. Anmin Jiang & Kye Kudo & Rachel S. Gormal & Sevannah Ellis & Sikao Guo & Tristan P. Wallis & Shanley F. Longfield & Phillip J. Robinson & Margaret E. Johnson & Merja Joensuu & Frédéric A. Meunier, 2024. "Dynamin1 long- and short-tail isoforms exploit distinct recruitment and spatial patterns to form endocytic nanoclusters," Nature Communications, Nature, vol. 15(1), pages 1-21, December.

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