Achieving functional neuronal dendrite structure through sequential stochastic growth and retraction

  1. André Ferreira Castro  Is a corresponding author
  2. Lothar Baltruschat
  3. Tomke Stürner
  4. Amirhoushang Bahrami
  5. Peter Jedlicka
  6. Gaia Tavosanis  Is a corresponding author
  7. Hermann Cuntz  Is a corresponding author
  1. Ernst Strüngmann Institut (ESI) for Neuroscience in Cooperation with Max Planck Society, Germany
  2. Center for Neurodegenerative Diseases (DZNE), Germany
  3. University of Cambridge, United Kingdom
  4. Max Planck Institute for Dynamics and Self Organization, Germany
  5. JLU Giessen, Germany

Abstract

Class I ventral posterior dendritic arborisation (c1vpda) proprioceptive sensory neurons respond to contractions in the Drosophila larval body wall during crawling. Their dendritic branches run along the direction of contraction, possibly a functional requirement to maximise membrane curvature during crawling contractions. Although the molecular machinery of dendritic patterning in c1vpda has been extensively studied, the process leading to the precise elaboration of their comb-like shapes remains elusive. Here, to link dendrite shape with its proprioceptive role, we performed long-term, non-invasive, in vivo time-lapse imaging of c1vpda embryonic and larval morphogenesis to reveal a sequence of differentiation stages. We combined computer models and dendritic branch dynamics tracking to propose that distinct sequential phases of stochastic growth and retraction achieve efficient dendritic trees both in terms of wire and function. Our study shows how dendrite growth balances structure–function requirements, shedding new light on general principles of self-organisation in functionally specialised dendrites.

Data availability

All data and all code is available on Zenodo https://doi.org/10.5281/zenodo.4290200

The following data sets were generated

Article and author information

Author details

  1. André Ferreira Castro

    Ernst Strüngmann Institut (ESI) for Neuroscience in Cooperation with Max Planck Society, Frankfurt am Main, Germany
    For correspondence
    acastro@mrc-lmb.cam.ac.uk
    Competing interests
    The authors declare that no competing interests exist.
  2. Lothar Baltruschat

    Center for Neurodegenerative Diseases (DZNE), Bonn, Germany
    Competing interests
    The authors declare that no competing interests exist.
  3. Tomke Stürner

    Department of Zoology, University of Cambridge, Cambridge, United Kingdom
    Competing interests
    The authors declare that no competing interests exist.
  4. Amirhoushang Bahrami

    Max Planck Institute for Dynamics and Self Organization, Göttingen, Germany
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0001-5841-2516
  5. Peter Jedlicka

    Institute of Clinical Neuroanatomy, JLU Giessen, Giessen, Germany
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0001-6571-5742
  6. Gaia Tavosanis

    Center for Neurodegenerative Diseases (DZNE), Bonn, Germany
    For correspondence
    Gaia.Tavosanis@dzne.de
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0002-8679-5515
  7. Hermann Cuntz

    Ernst Strüngmann Institut (ESI) for Neuroscience in Cooperation with Max Planck Society, Frankfurt am Main, Germany
    For correspondence
    cuntz@fias.uni-frankfurt.de
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0001-5445-0507

Funding

Bundesministerium für Bildung und Forschung (01GQ1406)

  • Hermann Cuntz

Deutsche Forschungsgemeinschaft (SPP 1464)

  • Gaia Tavosanis

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

Copyright

© 2020, Ferreira Castro 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.

Metrics

  • 2,344
    views
  • 308
    downloads
  • 36
    citations

Views, downloads and citations are aggregated across all versions of this paper published by eLife.

Download links

A two-part list of links to download the article, or parts of the article, in various formats.

Downloads (link to download the article as PDF)

Open citations (links to open the citations from this article in various online reference manager services)

Cite this article (links to download the citations from this article in formats compatible with various reference manager tools)

  1. André Ferreira Castro
  2. Lothar Baltruschat
  3. Tomke Stürner
  4. Amirhoushang Bahrami
  5. Peter Jedlicka
  6. Gaia Tavosanis
  7. Hermann Cuntz
(2020)
Achieving functional neuronal dendrite structure through sequential stochastic growth and retraction
eLife 9:e60920.
https://doi.org/10.7554/eLife.60920

Share this article

https://doi.org/10.7554/eLife.60920

Further reading

    1. Developmental Biology
    Eric R Brooks, Andrew R Moorman ... Jennifer A Zallen
    Tools and Resources

    The formation of the mammalian brain requires regionalization and morphogenesis of the cranial neural plate, which transforms from an epithelial sheet into a closed tube that provides the structural foundation for neural patterning and circuit formation. Sonic hedgehog (SHH) signaling is important for cranial neural plate patterning and closure, but the transcriptional changes that give rise to the spatially regulated cell fates and behaviors that build the cranial neural tube have not been systematically analyzed. Here, we used single-cell RNA sequencing to generate an atlas of gene expression at six consecutive stages of cranial neural tube closure in the mouse embryo. Ordering transcriptional profiles relative to the major axes of gene expression predicted spatially regulated expression of 870 genes along the anterior-posterior and mediolateral axes of the cranial neural plate and reproduced known expression patterns with over 85% accuracy. Single-cell RNA sequencing of embryos with activated SHH signaling revealed distinct SHH-regulated transcriptional programs in the developing forebrain, midbrain, and hindbrain, suggesting a complex interplay between anterior-posterior and mediolateral patterning systems. These results define a spatiotemporally resolved map of gene expression during cranial neural tube closure and provide a resource for investigating the transcriptional events that drive early mammalian brain development.

    1. Developmental Biology
    Mehmet Mahsum Kaplan, Erika Hudacova ... Ondrej Machon
    Research Article

    Hair follicle development is initiated by reciprocal molecular interactions between the placode-forming epithelium and the underlying mesenchyme. Cell fate transformation in dermal fibroblasts generates a cell niche for placode induction by activation of signaling pathways WNT, EDA, and FGF in the epithelium. These successive paracrine epithelial signals initiate dermal condensation in the underlying mesenchyme. Although epithelial signaling from the placode to mesenchyme is better described, little is known about primary mesenchymal signals resulting in placode induction. Using genetic approach in mice, we show that Meis2 expression in cells derived from the neural crest is critical for whisker formation and also for branching of trigeminal nerves. While whisker formation is independent of the trigeminal sensory innervation, MEIS2 in mesenchymal dermal cells orchestrates the initial steps of epithelial placode formation and subsequent dermal condensation. MEIS2 regulates the expression of transcription factor Foxd1, which is typical of pre-dermal condensation. However, deletion of Foxd1 does not affect whisker development. Overall, our data suggest an early role of mesenchymal MEIS2 during whisker formation and provide evidence that whiskers can normally develop in the absence of sensory innervation or Foxd1 expression.