IDEAS home Printed from https://ideas.repec.org/a/nat/natcom/v14y2023i1d10.1038_s41467-023-38421-9.html
   My bibliography  Save this article

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
    as

    Download full text from publisher

    File URL: https://www.nature.com/articles/s41467-023-38421-9
    File Function: Abstract
    Download Restriction: no
    File URL: https://libkey.io/10.1038/s41467-023-38421-9?utm_source=ideas
    LibKey link: if access is restricted and if your library uses this service, LibKey will redirect you to where you can use your library subscription to access this item
    ---><---

    References listed on IDEAS

    as
    1. 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.
    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. 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.
    Full references (including those not matched with items on IDEAS)

    Most related items

    These are the items that most often cite the same works as this one and are cited by the same works as this one.
    1. Shilong Yang & Xinwen Miao & Steven Arnold & Boxuan Li & Alan T. Ly & Huan Wang & Matthew Wang & Xiangfu Guo & Medha M. Pathak & Wenting Zhao & Charles D. Cox & Zheng Shi, 2022. "Membrane curvature governs the distribution of Piezo1 in live cells," Nature Communications, Nature, vol. 13(1), pages 1-14, December.
    2. Jiu-Tao Hang & Yu Kang & Guang-Kui Xu & Huajian Gao, 2021. "A hierarchical cellular structural model to unravel the universal power-law rheological behavior of living cells," Nature Communications, Nature, vol. 12(1), pages 1-7, December.
    3. Kazuya Tsujita & Reiko Satow & Shinobu Asada & Yoshikazu Nakamura & Luis Arnes & Keisuke Sako & Yasuyuki Fujita & Kiyoko Fukami & Toshiki Itoh, 2021. "Homeostatic membrane tension constrains cancer cell dissemination by counteracting BAR protein assembly," Nature Communications, Nature, vol. 12(1), pages 1-14, December.

    More about this item

    Statistics

    Access and download statistics

    Corrections

    All material on this site has been provided by the respective publishers and authors. You can help correct errors and omissions. When requesting a correction, please mention this item's handle: RePEc:nat:natcom:v:14:y:2023:i:1:d:10.1038_s41467-023-38421-9. See general information about how to correct material in RePEc.

    If you have authored this item and are not yet registered with RePEc, we encourage you to do it here. This allows to link your profile to this item. It also allows you to accept potential citations to this item that we are uncertain about.

    If CitEc recognized a bibliographic reference but did not link an item in RePEc to it, you can help with this form .

    If you know of missing items citing this one, you can help us creating those links by adding the relevant references in the same way as above, for each refering item. If you are a registered author of this item, you may also want to check the "citations" tab in your RePEc Author Service profile, as there may be some citations waiting for confirmation.

    For technical questions regarding this item, or to correct its authors, title, abstract, bibliographic or download information, contact: Sonal Shukla or Springer Nature Abstracting and Indexing (email available below). General contact details of provider: http://www.nature.com .

    Please note that corrections may take a couple of weeks to filter through the various RePEc services.

    IDEAS is a RePEc service. RePEc uses bibliographic data supplied by the respective publishers.