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.

Metrics

  • 414
    Page views
  • 55
    Downloads
  • 0
    Citations

Article citation count generated by polling the highest count across the following sources: Crossref, PubMed Central, Scopus.

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. 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

Further reading

    1. Cell Biology
    2. Microbiology and Infectious Disease
    Takehiro Kado, Zarina Akbary ... M Sloan Siegrist
    Research Article Updated

    Lateral partitioning of proteins and lipids shapes membrane function. In model membranes, partitioning can be influenced both by bilayer-intrinsic factors like molecular composition and by bilayer-extrinsic factors such as interactions with other membranes and solid supports. While cellular membranes can departition in response to bilayer-intrinsic or -extrinsic disruptions, the mechanisms by which they partition de novo are largely unknown. The plasma membrane of Mycobacterium smegmatis spatially and biochemically departitions in response to the fluidizing agent benzyl alcohol, then repartitions upon fluidizer washout. By screening for mutants that are sensitive to benzyl alcohol, we show that the bifunctional cell wall synthase PonA2 promotes membrane partitioning and cell growth during recovery from benzyl alcohol exposure. PonA2’s role in membrane repartitioning and regrowth depends solely on its conserved transglycosylase domain. Active cell wall polymerization promotes de novo membrane partitioning and the completed cell wall polymer helps to maintain membrane partitioning. Our work highlights the complexity of membrane–cell wall interactions and establishes a facile model system for departitioning and repartitioning cellular membranes.

    1. Cell Biology
    2. Computational and Systems Biology
    Breanne Sparta, Nont Kosaisawe ... John G Albeck
    Research Article Updated

    mTORC1 senses nutrients and growth factors and phosphorylates downstream targets, including the transcription factor TFEB, to coordinate metabolic supply and demand. These functions position mTORC1 as a central controller of cellular homeostasis, but the behavior of this system in individual cells has not been well characterized. Here, we provide measurements necessary to refine quantitative models for mTORC1 as a metabolic controller. We developed a series of fluorescent protein-TFEB fusions and a multiplexed immunofluorescence approach to investigate how combinations of stimuli jointly regulate mTORC1 signaling at the single-cell level. Live imaging of individual MCF10A cells confirmed that mTORC1-TFEB signaling responds continuously to individual, sequential, or simultaneous treatment with amino acids and the growth factor insulin. Under physiologically relevant concentrations of amino acids, we observe correlated fluctuations in TFEB, AMPK, and AKT signaling that indicate continuous activity adjustments to nutrient availability. Using partial least squares regression modeling, we show that these continuous gradations are connected to protein synthesis rate via a distributed network of mTORC1 effectors, providing quantitative support for the qualitative model of mTORC1 as a homeostatic controller and clarifying its functional behavior within individual cells.