The decoy SNARE Tomosyn sets tonic versus phasic release properties and is required for homeostatic synaptic plasticity

Abstract

Synaptic vesicle release probability (Pr) is a key presynaptic determinant of synaptic strength established by cell intrinsic properties and further refined by plasticity. To characterize mechanisms that generate Pr heterogeneity between distinct neuronal populations, we examined glutamatergic tonic (Ib) and phasic (Is) motoneurons in Drosophila with stereotyped differences in Pr and synaptic plasticity. We found the decoy SNARE Tomosyn is differentially expressed between these motoneuron subclasses and contributes to intrinsic differences in their synaptic output. Tomosyn expression enables tonic release in Ib motoneurons by reducing SNARE complex formation and suppressing Pr to generate decreased levels of synaptic vesicle fusion and enhanced resistance to synaptic fatigue. In contrast, phasic release dominates when Tomosyn expression is low, enabling high intrinsic Pr at Is terminals at the expense of sustained release and robust presynaptic potentiation. In addition, loss of Tomosyn disrupts the ability of tonic synapses to undergo presynaptic homeostatic potentiation (PHP).

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All data generated or analysed during this study are included in the manuscript and supporting figures.

Article and author information

Author details

  1. Chad W Sauvola

    Massachusetts Institute of Technology, Cambridge, United States
    Competing interests
    The authors declare that no competing interests exist.
  2. Yulia Akbergenova

    Massachusetts Institute of Technology, Cambridge, United States
    Competing interests
    The authors declare that no competing interests exist.
  3. Karen L Cunningham

    Massachusetts Institute of Technology, Cambridge, United States
    Competing interests
    The authors declare that no competing interests exist.
  4. Nicole A Aponte-Santiago

    Massachusetts Institute of Technology, Cambridge, United States
    Competing interests
    The authors declare that no competing interests exist.
  5. J Troy Littleton

    Massachusetts Institute of Technology, Cambridge, United States
    For correspondence
    troy@mit.edu
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0001-5576-2887

Funding

National Institute of Neurological Disorders and Stroke (NS040296)

  • J Troy Littleton

National Institute of Mental Health (MH104536)

  • J Troy Littleton

The funders had no role in study design, data collection and interpretation, or the decision to submit the work for publication.

Reviewing Editor

  1. Hugo J Bellen, Baylor College of Medicine, United States

Version history

  1. Preprint posted: August 5, 2021 (view preprint)
  2. Received: August 6, 2021
  3. Accepted: October 27, 2021
  4. Accepted Manuscript published: October 29, 2021 (version 1)
  5. Version of Record published: November 24, 2021 (version 2)

Copyright

© 2021, Sauvola et al.

This article is distributed under the terms of the Creative Commons Attribution License permitting unrestricted use and redistribution provided that the original author and source are credited.

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  1. Chad W Sauvola
  2. Yulia Akbergenova
  3. Karen L Cunningham
  4. Nicole A Aponte-Santiago
  5. J Troy Littleton
(2021)
The decoy SNARE Tomosyn sets tonic versus phasic release properties and is required for homeostatic synaptic plasticity
eLife 10:e72841.
https://doi.org/10.7554/eLife.72841

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https://doi.org/10.7554/eLife.72841

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