Reactive oxygen species regulate activity-dependent neuronal plasticity in Drosophila

  1. Matthew C W Oswald  Is a corresponding author
  2. Paul S Brooks
  3. Maarten F Zwart
  4. Amrita Mukherjee
  5. Ryan J H West
  6. Carlo N G Giachello
  7. Khomgrit Morarach
  8. Richard A Baines
  9. Sean T Sweeney  Is a corresponding author
  10. Matthias Landgraf  Is a corresponding author
  1. University of Cambridge, United Kingdom
  2. Janelia Research Campus, Howard Hughes Medical Institute, United States
  3. University of Manchester, United Kingdom
  4. University of York, United Kingdom

Abstract

Reactive oxygen species (ROS) have been extensively studied as damaging agents associated with ageing and neurodegenerative conditions. Their role in the nervous system under non-pathological conditions has remained poorly understood. Working with the Drosophila larval locomotor network, we show that in neurons ROS act as obligate signals required for neuronal activity-dependent structural plasticity, of both pre- and postsynaptic terminals. ROS signaling is also necessary for maintaining evoked synaptic transmission at the neuromuscular junction, and for activity-regulated homeostatic adjustment of motor network output, as measured by larval crawling behavior. We identified the highly conserved Parkinson's disease-linked protein DJ-1ß as a redox sensor in neurons where it regulates structural plasticity, in part via modulation of the PTEN-PI3Kinase pathway. This study provides a new conceptual framework of neuronal ROS as second messengers required for neuronal plasticity and for network tuning, whose dysregulation in the ageing brain and under neurodegenerative conditions may contribute to synaptic dysfunction.

Data availability

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

Article and author information

Author details

  1. Matthew C W Oswald

    Department of Zoology, University of Cambridge, Cambridge, United Kingdom
    For correspondence
    mo364@cam.ac.uk
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0001-8586-9351
  2. Paul S Brooks

    Department of Zoology, University of Cambridge, Cambridge, United Kingdom
    Competing interests
    The authors declare that no competing interests exist.
  3. Maarten F Zwart

    Janelia Research Campus, Howard Hughes Medical Institute, Ashburn, United States
    Competing interests
    The authors declare that no competing interests exist.
  4. Amrita Mukherjee

    Department of Zoology, University of Cambridge, Cambridge, United Kingdom
    Competing interests
    The authors declare that no competing interests exist.
  5. Ryan J H West

    Faculty of Biology, Medicine and Health, University of Manchester, Manchester, United Kingdom
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0001-9873-2258
  6. Carlo N G Giachello

    Faculty of Biology, Medicine and Health, University of Manchester, Manchester, United Kingdom
    Competing interests
    The authors declare that no competing interests exist.
  7. Khomgrit Morarach

    Department of Zoology, University of Cambridge, Cambridge, United Kingdom
    Competing interests
    The authors declare that no competing interests exist.
  8. Richard A Baines

    Faculty of Biology, Medicine and Health, University of Manchester, Manchester, United Kingdom
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0001-8571-4376
  9. Sean T Sweeney

    Department of Biology, University of York, York, United Kingdom
    For correspondence
    sean.sweeney@york.ac.uk
    Competing interests
    The authors declare that no competing interests exist.
  10. Matthias Landgraf

    Department of Zoology, University of Cambridge, Cambridge, United Kingdom
    For correspondence
    ml10006@cam.ac.uk
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0001-5142-1997

Funding

Biotechnology and Biological Sciences Research Council (BB/I01179X/1)

  • Matthias Landgraf

Biotechnology and Biological Sciences Research Council (BB/M002934/1)

  • Matthias Landgraf

Biotechnology and Biological Sciences Research Council (BB/I012273/1)

  • Sean T Sweeney

Biotechnology and Biological Sciences Research Council (BB/M002322/1)

  • Sean T Sweeney

Biotechnology and Biological Sciences Research Council (BB/N/014561/1)

  • Richard A Baines

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

Reviewing Editor

  1. Graeme W Davis, University of California, San Francisco, United States

Version history

  1. Received: June 20, 2018
  2. Accepted: December 12, 2018
  3. Accepted Manuscript published: December 12, 2018 (version 1)
  4. Accepted Manuscript updated: December 17, 2018 (version 2)
  5. Version of Record published: December 27, 2018 (version 3)

Copyright

© 2018, Oswald 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. Matthew C W Oswald
  2. Paul S Brooks
  3. Maarten F Zwart
  4. Amrita Mukherjee
  5. Ryan J H West
  6. Carlo N G Giachello
  7. Khomgrit Morarach
  8. Richard A Baines
  9. Sean T Sweeney
  10. Matthias Landgraf
(2018)
Reactive oxygen species regulate activity-dependent neuronal plasticity in Drosophila
eLife 7:e39393.
https://doi.org/10.7554/eLife.39393

Share this article

https://doi.org/10.7554/eLife.39393

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