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

  • 2,307
    views
  • 304
    downloads
  • 31
    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
    2. Evolutionary Biology
    Hope M Healey, Hayden B Penn ... William A Cresko
    Research Article

    Seahorses, pipefishes, and seadragons are fishes from the family Syngnathidae that have evolved extraordinary traits including male pregnancy, elongated snouts, loss of teeth, and dermal bony armor. The developmental genetic and cellular changes that led to the evolution of these traits are largely unknown. Recent syngnathid genome assemblies revealed suggestive gene content differences and provided the opportunity for detailed genetic analyses. We created a single-cell RNA sequencing atlas of Gulf pipefish embryos to understand the developmental basis of four traits: derived head shape, toothlessness, dermal armor, and male pregnancy. We completed marker gene analyses, built genetic networks, and examined the spatial expression of select genes. We identified osteochondrogenic mesenchymal cells in the elongating face that express regulatory genes bmp4, sfrp1a, and prdm16. We found no evidence for tooth primordia cells, and we observed re-deployment of osteoblast genetic networks in developing dermal armor. Finally, we found that epidermal cells expressed nutrient processing and environmental sensing genes, potentially relevant for the brooding environment. The examined pipefish evolutionary innovations are composed of recognizable cell types, suggesting that derived features originate from changes within existing gene networks. Future work addressing syngnathid gene networks across multiple stages and species is essential for understanding how the novelties of these fish evolved.

    1. Developmental Biology
    2. Genetics and Genomics
    Mehul Vora, Jonathan Dietz ... Cathy Savage-Dunn
    Research Article

    Smads and their transcription factor partners mediate the transcriptional responses of target cells to secreted ligands of the transforming growth factor-β (TGF-β) family, including those of the conserved bone morphogenetic protein (BMP) family, yet only a small number of direct target genes have been well characterized. In C. elegans, the BMP2/4 ortholog DBL-1 regulates multiple biological functions, including body size, via a canonical receptor-Smad signaling cascade. Here, we identify functional binding sites for SMA-3/Smad and its transcriptional partner SMA-9/Schnurri based on ChIP-seq peaks (identified by modEncode) and expression differences of nearby genes identified from RNA-seq analysis of corresponding mutants. We found that SMA-3 and SMA-9 have both overlapping and unique target genes. At a genome-wide scale, SMA-3/Smad acts as a transcriptional activator, whereas SMA-9/Schnurri direct targets include both activated and repressed genes. Mutations in sma-9 partially suppress the small body size phenotype of sma-3, suggesting some level of antagonism between these factors and challenging the prevailing model for Schnurri function. Functional analysis of target genes revealed a novel role in body size for genes involved in one-carbon metabolism and in the endoplasmic reticulum (ER) secretory pathway, including the disulfide reductase dpy-11. Our findings indicate that Smads and SMA-9/Schnurri have previously unappreciated complex genetic and genomic regulatory interactions that in turn regulate the secretion of extracellular components like collagen into the cuticle to mediate body size regulation.