Desmosomal connectomics of all somatic muscles in an annelid larva

Abstract

Cells form networks in animal tissues through synaptic, chemical and adhesive links. Invertebrate muscle cells often connect to other cells through desmosomes, adhesive junctions anchored by intermediate filaments. To study desmosomal networks, we skeletonised 853 muscle cells and their desmosomal partners in volume electron microscopy data covering an entire larva of the annelid Platynereis. Muscle cells adhere to each other, to epithelial, glial, ciliated, and bristle-producing cells and to the basal lamina, forming a desmosomal connectome of over 2,000 cells. The aciculae - chitin rods that form an endoskeleton in the segmental appendages - are highly connected hubs in this network. This agrees with the many degrees of freedom of their movement, as revealed by video microscopy. Mapping motoneuron synapses to the desmosomal connectome allowed us to infer the extent of tissue influenced by motoneurons. Our work shows how cellular-level maps of synaptic and adherent force networks can elucidate body mechanics.

Data availability

All EM, tracing and annotation data are available at https://catmaid.jekelylab.ex.ac.ukAll code is available at https://github.com/JekelyLab/Jasek_et_al

The following data sets were generated

Article and author information

Author details

  1. Sanja Jasek

    Living Systems Institute, University of Exeter, Exeter, United Kingdom
    Competing interests
    No competing interests declared.
  2. Csaba Verasztó

    Living Systems Institute, University of Exeter, Exeter, United Kingdom
    Competing interests
    No competing interests declared.
  3. Emelie Brodrick

    Living Systems Institute, University of Exeter, Exeter, United Kingdom
    Competing interests
    No competing interests declared.
  4. Réza Shahidi

    Living Systems Institute, University of Exeter, Exeter, United Kingdom
    Competing interests
    No competing interests declared.
  5. Tom Kazimiers

    kazmos GmbH, Dresden, Germany
    Competing interests
    Tom Kazimiers, Tom Kazimiers is the founder of kazmos GmbH, a company that continues the development of the open-source package CATMAID..
  6. Alexandra Kerbl

    Living Systems Institute, University of Exeter, Exeter, United Kingdom
    Competing interests
    No competing interests declared.
  7. Gáspár Jékely

    Living Systems Institute, University of Exeter, Exeter, United Kingdom
    For correspondence
    g.jekely@exeter.ac.uk
    Competing interests
    Gáspár Jékely, Reviewing editor, eLife.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0001-8496-9836

Funding

European Commission (FP7-PEOPLE-2012-ITN grant no. 317172)

  • Sanja Jasek
  • Gáspár Jékely

Wellcome Trust (Investigator Award 214337/Z/18/Z)

  • Sanja Jasek
  • Csaba Verasztó
  • Réza Shahidi
  • Gáspár Jékely

European Research Council (grant agreement No 101020792)

  • Alexandra Kerbl
  • Gáspár Jékely

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

Reviewing Editor

  1. Kristin Tessmar-Raible, University of Vienna, Austria

Version history

  1. Preprint posted: June 10, 2021 (view preprint)
  2. Received: June 12, 2021
  3. Accepted: December 7, 2022
  4. Accepted Manuscript published: December 20, 2022 (version 1)
  5. Version of Record published: January 25, 2023 (version 2)

Copyright

© 2022, Jasek 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. Sanja Jasek
  2. Csaba Verasztó
  3. Emelie Brodrick
  4. Réza Shahidi
  5. Tom Kazimiers
  6. Alexandra Kerbl
  7. Gáspár Jékely
(2022)
Desmosomal connectomics of all somatic muscles in an annelid larva
eLife 11:e71231.
https://doi.org/10.7554/eLife.71231

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https://doi.org/10.7554/eLife.71231

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