Neurexin and Neuroligin-based adhesion complexes drive axonal arborisation growth independent of synaptic activity

  1. William D Constance
  2. Amrita Mukherjee
  3. Yvette E Fisher
  4. Sinziana Pop
  5. Eric Blanc
  6. Yusuke Toyama
  7. Darren W Williams  Is a corresponding author
  1. King's College London, United Kingdom
  2. Harvard Medical School, United States
  3. Berlin Institute of Health, Germany
  4. National University of Singapore, Singapore

Abstract

Building arborisations of the right size and shape is fundamental for neural network function. Live imaging in vertebrate brains strongly suggests that nascent synapses are critical for branch growth during development. The molecular mechanisms underlying this are largely unknown. Here we present a novel system in Drosophila for studying the development of complex arborisations live, in vivo during metamorphosis. In growing arborisations we see branch dynamics and localisations of presynaptic proteins very similar to the 'synaptotropic growth' described in fish/frogs. These accumulations of presynaptic proteins do not appear to be presynaptic release sites and are not paired with neurotransmitter receptors. Knockdowns of either evoked or spontaneous neurotransmission do not impact arbor growth. Instead, we find that axonal branch growth is regulated by dynamic, focal localisations of Neurexin and Neuroligin. These adhesion complexes provide stability for filopodia by a 'stick-and-grow' based mechanism wholly independent of synaptic activity.

Article and author information

Author details

  1. William D Constance

    Centre for Developmental Neurobiology, King's College London, London, United Kingdom
    Competing interests
    The authors declare that no competing interests exist.
  2. Amrita Mukherjee

    Centre for Developmental Neurobiology, King's College London, London, United Kingdom
    Competing interests
    The authors declare that no competing interests exist.
  3. Yvette E Fisher

    Department of Neurobiology, Harvard Medical School, Boston, United States
    Competing interests
    The authors declare that no competing interests exist.
  4. Sinziana Pop

    Centre for Developmental Neurobiology, King's College London, London, United Kingdom
    Competing interests
    The authors declare that no competing interests exist.
  5. Eric Blanc

    Berlin Institute of Health, Berlin, Germany
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0002-4369-0254
  6. Yusuke Toyama

    Department of Biological Sciences, National University of Singapore, Singapore, Singapore
    Competing interests
    The authors declare that no competing interests exist.
  7. Darren W Williams

    Centre for Developmental Neurobiology, King's College London, London, United Kingdom
    For correspondence
    darren.williams@kcl.ac.uk
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0001-5917-4935

Funding

Biotechnology and Biological Sciences Research Council (BB/L022672/1)

  • William D Constance
  • Amrita Mukherjee
  • Yvette E Fisher
  • Sinziana Pop
  • Eric Blanc

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

Reviewing Editor

  1. K VijayRaghavan, National Centre for Biological Sciences, Tata Institute of Fundamental Research, India

Publication history

  1. Received: August 31, 2017
  2. Accepted: March 4, 2018
  3. Accepted Manuscript published: March 5, 2018 (version 1)
  4. Version of Record published: March 26, 2018 (version 2)

Copyright

© 2018, Constance 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. William D Constance
  2. Amrita Mukherjee
  3. Yvette E Fisher
  4. Sinziana Pop
  5. Eric Blanc
  6. Yusuke Toyama
  7. Darren W Williams
(2018)
Neurexin and Neuroligin-based adhesion complexes drive axonal arborisation growth independent of synaptic activity
eLife 7:e31659.
https://doi.org/10.7554/eLife.31659
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