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Synapsin 2a tetramerisation selectively controls the presynaptic nanoscale organisation of reserve synaptic vesicles

Author

Listed:
  • Shanley F. Longfield

    (The University of Queensland)

  • Rachel S. Gormal

    (The University of Queensland)

  • Matis Feller

    (IBENS, Ecole Normale Superieure)

  • Pierre Parutto

    (IBENS, Ecole Normale Superieure)

  • Jürgen Reingruber

    (IBENS, Ecole Normale Superieure)

  • Tristan P. Wallis

    (The University of Queensland)

  • Merja Joensuu

    (The University of Queensland
    The University of Queensland)

  • George J. Augustine

    (Temasek Lifesciences Laboratory)

  • Ramón Martínez-Mármol

    (The University of Queensland)

  • David Holcman

    (IBENS, Ecole Normale Superieure
    University of Cambridge, and Churchill College)

  • Frédéric A. Meunier

    (The University of Queensland
    The University of Queensland)

Abstract

Neurotransmitter release relies on the regulated fusion of synaptic vesicles (SVs) that are tightly packed within the presynaptic bouton of neurons. The mechanism by which SVs are clustered at the presynapse, while preserving their ability to dynamically recycle to support neuronal communication, remains unknown. Synapsin 2a (Syn2a) tetramerization has been suggested as a potential clustering mechanism. Here, we used Dual-pulse sub-diffractional Tracking of Internalised Molecules (DsdTIM) to simultaneously track single SVs from the recycling and the reserve pools, in live hippocampal neurons. The reserve pool displays a lower presynaptic mobility compared to the recycling pool and is also present in the axons. Triple knockout of Synapsin 1-3 genes (SynTKO) increased the mobility of reserve pool SVs. Re-expression of wild-type Syn2a (Syn2aWT), but not the tetramerization-deficient mutant K337Q (Syn2aK337Q), fully rescued these effects. Single-particle tracking revealed that Syn2aK337QmEos3.1 exhibited altered activity-dependent presynaptic translocation and nanoclustering. Therefore, Syn2a tetramerization controls its own presynaptic nanoclustering and thereby contributes to the dynamic immobilisation of the SV reserve pool.

Suggested Citation

  • Shanley F. Longfield & Rachel S. Gormal & Matis Feller & Pierre Parutto & Jürgen Reingruber & Tristan P. Wallis & Merja Joensuu & George J. Augustine & Ramón Martínez-Mármol & David Holcman & Frédéric, 2024. "Synapsin 2a tetramerisation selectively controls the presynaptic nanoscale organisation of reserve synaptic vesicles," Nature Communications, Nature, vol. 15(1), pages 1-18, December.
    • Handle: RePEc:nat:natcom:v:15:y:2024:i:1:d:10.1038_s41467-024-46256-1
    DOI: 10.1038/s41467-024-46256-1
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    References listed on IDEAS

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    1. 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, 2017. "Erratum: In vivo single-molecule imaging of syntaxin1A reveals polyphosphoinositide- and activity-dependent trapping in presynaptic nanoclusters," Nature Communications, Nature, vol. 8(1), pages 1-1, April.
    2. Christian Hoffmann & Jakob Rentsch & Taka A. Tsunoyama & Akshita Chhabra & Gerard Aguilar Perez & Rajdeep Chowdhury & Franziska Trnka & Aleksandr A. Korobeinikov & Ali H. Shaib & Marcelo Ganzella & Gr, 2023. "Synapsin condensation controls synaptic vesicle sequestering and dynamics," Nature Communications, Nature, vol. 14(1), pages 1-13, December.
    3. Sunil P. Gandhi & Charles F. Stevens, 2003. "Three modes of synaptic vesicular recycling revealed by single-vesicle imaging," Nature, Nature, vol. 423(6940), pages 607-613, June.
    4. Lucian Medrihan & Fabrizia Cesca & Andrea Raimondi & Gabriele Lignani & Pietro Baldelli & Fabio Benfenati, 2013. "Synapsin II desynchronizes neurotransmitter release at inhibitory synapses by interacting with presynaptic calcium channels," Nature Communications, Nature, vol. 4(1), pages 1-13, June.
    5. Tristan P. Wallis & Anmin Jiang & Kyle Young & Huiyi Hou & Kye Kudo & Alex J. McCann & Nela Durisic & Merja Joensuu & Dietmar Oelz & Hien Nguyen & Rachel S. Gormal & Frédéric A. Meunier, 2023. "Super-resolved trajectory-derived nanoclustering analysis using spatiotemporal indexing," Nature Communications, Nature, vol. 14(1), pages 1-16, December.
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