A Toll-receptor map underlies structural brain plasticity

  1. Guiyi Li
  2. Manuel G Forero
  3. Jill S Wentzell
  4. Ilgim Durmus
  5. Reinhard Wolf
  6. Niki C Anthoney
  7. Mieczyslaw Parker
  8. Ruiying Jiang
  9. Jacob Hasenauer
  10. Nicholas James Strausfeld
  11. Martin Heisenberg
  12. Alicia Hidalgo  Is a corresponding author
  1. University of Birmingham, United Kingdom
  2. Universidad de Ibagué, Colombia
  3. University of Würzburg, Germany
  4. University of Arizona, United States

Abstract

Experience alters brain structure, but the underlying mechanism remained unknown. Structural plasticity reveals that brain function is encoded in generative changes to cells that compete with destructive processes driving neurodegeneration. At an adult critical period, experience increases fiber number and brain size in Drosophila. Here, we asked if Toll receptors are involved. Tolls demarcate a map of brain anatomical domains. Focusing on Toll-2, loss of function caused apoptosis, neurite atrophy and impaired behaviour. Toll-2 gain of function and neuronal activity at the critical period increased cell number. Toll-2 induced cycling of adult progenitor cells via a novel pathway, that antagonized MyD88-dependent quiescence, and engaged Weckle and Yorkie downstream. Constant knock-down of multiple Tolls synergistically reduced brain size. Conditional over-expression of Toll-2 and wek at the adult critical period increased brain size. Through their topographic distribution, Toll receptors regulate neuronal number and brain size, modulating structural plasticity in the adult brain.

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. Guiyi Li

    School of Biosciences, University of Birmingham, Birmingham, United Kingdom
    Competing interests
    The authors declare that no competing interests exist.
  2. Manuel G Forero

    Facultad de Ingeniería, Universidad de Ibagué, Ibagué, Colombia
    Competing interests
    The authors declare that no competing interests exist.
  3. Jill S Wentzell

    School of Biosciences, University of Birmingham, Birmingham, United Kingdom
    Competing interests
    The authors declare that no competing interests exist.
  4. Ilgim Durmus

    School of Biosciences, University of Birmingham, Birmingham, United Kingdom
    Competing interests
    The authors declare that no competing interests exist.
  5. Reinhard Wolf

    Rudolf-Virchow-Center for Experimental Biomedicine, University of Würzburg, Würzburg, Germany
    Competing interests
    The authors declare that no competing interests exist.
  6. Niki C Anthoney

    Institute of Cancer and Genomic Sciences, University of Birmingham, Birmingham, United Kingdom
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0003-3311-6328
  7. Mieczyslaw Parker

    School of Biosciences, University of Birmingham, Birmingham, United Kingdom
    Competing interests
    The authors declare that no competing interests exist.
  8. Ruiying Jiang

    School of Biosciences, University of Birmingham, Birmingham, United Kingdom
    Competing interests
    The authors declare that no competing interests exist.
  9. Jacob Hasenauer

    School of Biosciences, University of Birmingham, Birmingham, United Kingdom
    Competing interests
    The authors declare that no competing interests exist.
  10. Nicholas James Strausfeld

    Department of Neuroscience, University of Arizona, Tucson, United States
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0002-1115-1774
  11. Martin Heisenberg

    Rudolf-Virchow-Center for Experimental Biomedicine, University of Würzburg, Würzburg, Germany
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0002-4462-8655
  12. Alicia Hidalgo

    School of Biosciences, University of Birmingham, Birmingham, United Kingdom
    For correspondence
    a.hidalgo@bham.ac.uk
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0001-8041-5764

Funding

Biotechnology and Biological Sciences Research Council (BB/P004997/1)

  • Alicia Hidalgo

Biotechnology and Biological Sciences Research Council (BB/R017034/1)

  • Alicia Hidalgo

EU Marie Curie-Sklodowska Fellowship (NPN)

  • Jill S Wentzell

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. Received: October 14, 2019
  2. Accepted: February 12, 2020
  3. Accepted Manuscript published: February 18, 2020 (version 1)
  4. Version of Record published: March 17, 2020 (version 2)

Copyright

© 2020, Li 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. Guiyi Li
  2. Manuel G Forero
  3. Jill S Wentzell
  4. Ilgim Durmus
  5. Reinhard Wolf
  6. Niki C Anthoney
  7. Mieczyslaw Parker
  8. Ruiying Jiang
  9. Jacob Hasenauer
  10. Nicholas James Strausfeld
  11. Martin Heisenberg
  12. Alicia Hidalgo
(2020)
A Toll-receptor map underlies structural brain plasticity
eLife 9:e52743.
https://doi.org/10.7554/eLife.52743

Share this article

https://doi.org/10.7554/eLife.52743

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