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Drosophila motor neuron boutons remodel through membrane blebbing coupled with muscle contraction

Author

Listed:
  • Andreia R. Fernandes

    (Universidade Nova de Lisboa)

  • João P. Martins

    (Universidade Nova de Lisboa
    Faculdade de Medicina da Universidade de Lisboa)

  • Edgar R. Gomes

    (Faculdade de Medicina da Universidade de Lisboa)

  • César S. Mendes

    (Universidade Nova de Lisboa)

  • Rita O. Teodoro

    (Universidade Nova de Lisboa)

Abstract

Wired neurons form new presynaptic boutons in response to increased synaptic activity, however the mechanism(s) by which this occurs remains uncertain. Drosophila motor neurons (MNs) have clearly discernible boutons that display robust structural plasticity, being therefore an ideal system in which to study activity-dependent bouton genesis. Here, we show that in response to depolarization and in resting conditions, MNs form new boutons by membrane blebbing, a pressure-driven mechanism that occurs in 3-D cell migration, but to our knowledge not previously described to occur in neurons. Accordingly, F-actin is decreased in boutons during outgrowth, and non-muscle myosin-II is dynamically recruited to newly formed boutons. Furthermore, muscle contraction plays a mechanical role, which we hypothesize promotes bouton addition by increasing MN confinement. Overall, we identified a mechanism by which established circuits form new boutons allowing their structural expansion and plasticity, using trans-synaptic physical forces as the main driving force.

Suggested Citation

  • Andreia R. Fernandes & João P. Martins & Edgar R. Gomes & César S. Mendes & Rita O. Teodoro, 2023. "Drosophila motor neuron boutons remodel through membrane blebbing coupled with muscle contraction," Nature Communications, Nature, vol. 14(1), pages 1-20, December.
    • Handle: RePEc:nat:natcom:v:14:y:2023:i:1:d:10.1038_s41467-023-38421-9
    DOI: 10.1038/s41467-023-38421-9
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    References listed on IDEAS

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    1. Atsuki Hiramoto & Julius Jonaitis & Sawako Niki & Hiroshi Kohsaka & Richard D. Fetter & Albert Cardona & Stefan R. Pulver & Akinao Nose, 2021. "Regulation of coordinated muscular relaxation in Drosophila larvae by a pattern-regulating intersegmental circuit," Nature Communications, Nature, vol. 12(1), pages 1-14, December.
    2. Guillaume T. Charras & Justin C. Yarrow & Mike A. Horton & L. Mahadevan & T. J. Mitchison, 2005. "Non-equilibration of hydrostatic pressure in blebbing cells," Nature, Nature, vol. 435(7040), pages 365-369, May.
    3. Hasan Ucar & Satoshi Watanabe & Jun Noguchi & Yuichi Morimoto & Yusuke Iino & Sho Yagishita & Noriko Takahashi & Haruo Kasai, 2021. "Mechanical actions of dendritic-spine enlargement on presynaptic exocytosis," Nature, Nature, vol. 600(7890), pages 686-689, December.
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