1. Developmental Biology
  2. Stem Cells and Regenerative Medicine
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Pattern regulation in a regenerating jellyfish

  1. Chiara Sinigaglia  Is a corresponding author
  2. Sophie Peron
  3. Jeanne Eichelbrenner
  4. Sandra Chevalier
  5. Julia Steger
  6. Carine Barreau
  7. Evelyn Houliston
  8. Lucas Leclère  Is a corresponding author
  1. ENS Lyon, France
  2. Sorbonne Université, France
  3. University of Vienna, Austria
Research Article
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Cite this article as: eLife 2020;9:e54868 doi: 10.7554/eLife.54868

Abstract

Clytia hemisphaerica jellyfish, with their tetraradial symmetry, offer a novel paradigm for addressing patterning mechanisms during regeneration. Here we show that an interplay between mechanical forces, cell migration and proliferation allows jellyfish fragments to regain shape and functionality rapidly, notably by efficient restoration of the central feeding organ (manubrium). Fragmentation first triggers actomyosin-powered remodeling that restores body umbrella shape, causing radial smooth muscle fibers to converge around 'hubs' which serve as positional landmarks. Stabilization of these hubs, and associated expression of Wnt6, depends on the configuration of the adjoining muscle fiber 'spokes'. Stabilized hubs presage the site of the manubrium blastema, whose growth is Wnt/β-catenin dependent and fueled by both cell proliferation and long-range cell recruitment. Manubrium morphogenesis is modulated by its connections with the gastrovascular canal system. We conclude that body patterning in regenerating jellyfish emerges mainly from local interactions, triggered and directed by the remodeling process.

Article and author information

Author details

  1. Chiara Sinigaglia

    Institut de Genomique Fonctionelle de Lyon, ENS Lyon, Lyon, France
    For correspondence
    chi.sinigaglia@gmail.com
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0002-7195-7091
  2. Sophie Peron

    Laboratoire de Biologie du Développement de Villefranche-sur-mer (LBDV), Sorbonne Université, Villefranche-sur-mer, France
    Competing interests
    The authors declare that no competing interests exist.
  3. Jeanne Eichelbrenner

    Laboratoire de Biologie du Développement de Villefranche-sur-mer (LBDV), Sorbonne Université, Villefranche-sur-mer, France
    Competing interests
    The authors declare that no competing interests exist.
  4. Sandra Chevalier

    Laboratoire de Biologie du Développement de Villefranche-sur-mer (LBDV), Sorbonne Université, Villefranche-sur-mer, France
    Competing interests
    The authors declare that no competing interests exist.
  5. Julia Steger

    Molecular Evolution and Development, University of Vienna, Vienna, Austria
    Competing interests
    The authors declare that no competing interests exist.
  6. Carine Barreau

    Laboratoire de Biologie du Développement de Villefranche-sur-mer (LBDV), Sorbonne Université, Villefranche-sur-mer, France
    Competing interests
    The authors declare that no competing interests exist.
  7. Evelyn Houliston

    Laboratoire de Biologie du Développement de Villefranche-sur-mer (LBDV), Sorbonne Université, Villefranche-sur-mer, France
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0001-9264-2585
  8. Lucas Leclère

    Laboratoire de Biologie du Développement de Villefranche-sur-mer (LBDV), Sorbonne Université, Villefranche-sur-mer, France
    For correspondence
    lucas.leclere@obs-vlfr.fr
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0002-7440-0467

Funding

Agence Nationale de la Recherche (ANR-13-PDOC-0016)

  • Lucas Leclère

Agence Nationale de la Recherche (ANR-19-CE13-0003)

  • Lucas Leclère

Fondation pour la Recherche Médicale (FDT201805005536)

  • Sophie Peron

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

Reviewing Editor

  1. Phillip A Newmark, Morgridge Institute for Research, United States

Publication history

  1. Received: March 24, 2020
  2. Accepted: September 5, 2020
  3. Accepted Manuscript published: September 7, 2020 (version 1)
  4. Version of Record published: September 29, 2020 (version 2)

Copyright

© 2020, Sinigaglia 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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