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Wnt-Ror-Dvl signalling and the dystrophin complex organize planar-polarized membrane compartments in C. elegans muscles

Author

Listed:
  • Alice Peysson

    (MeLiS)

  • Noura Zariohi

    (MeLiS)

  • Marie Gendrel

    (Université Paris Sciences et Lettres Research University)

  • Amandine Chambert-Loir

    (MeLiS)

  • Noémie Frébault

    (MeLiS)

  • Elise Cheynet

    (MeLiS)

  • Olga Andrini

    (MeLiS)

  • Thomas Boulin

    (MeLiS)

Abstract

Cell polarity mechanisms allow the formation of specialized membrane domains with unique protein compositions, signalling properties, and functional characteristics. By analyzing the localization of potassium channels and proteins belonging to the dystrophin-associated protein complex, we reveal the existence of distinct planar-polarized membrane compartments at the surface of C. elegans muscle cells. We find that muscle polarity is controlled by a non-canonical Wnt signalling cascade involving the ligand EGL-20/Wnt, the receptor CAM-1/Ror, and the intracellular effector DSH-1/Dishevelled. Interestingly, classical planar cell polarity proteins are not required for this process. Using time-resolved protein degradation, we demonstrate that –while it is essentially in place by the end of embryogenesis– muscle polarity is a dynamic state, requiring continued presence of DSH-1 throughout post-embryonic life. Our results reveal the unsuspected complexity of the C. elegans muscle membrane and establish a genetically tractable model system to study cellular polarity and membrane compartmentalization in vivo.

Suggested Citation

  • Alice Peysson & Noura Zariohi & Marie Gendrel & Amandine Chambert-Loir & Noémie Frébault & Elise Cheynet & Olga Andrini & Thomas Boulin, 2024. "Wnt-Ror-Dvl signalling and the dystrophin complex organize planar-polarized membrane compartments in C. elegans muscles," Nature Communications, Nature, vol. 15(1), pages 1-15, December.
    • Handle: RePEc:nat:natcom:v:15:y:2024:i:1:d:10.1038_s41467-024-49154-8
    DOI: 10.1038/s41467-024-49154-8
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    References listed on IDEAS

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    1. Mireille Montcouquiol & Rivka A. Rachel & Pamela J. Lanford & Neal G. Copeland & Nancy A. Jenkins & Matthew W. Kelley, 2003. "Identification of Vangl2 and Scrb1 as planar polarity genes in mammals," Nature, Nature, vol. 423(6936), pages 173-177, May.
    2. Marten Postma & Joachim Goedhart, 2019. "PlotsOfData—A web app for visualizing data together with their summaries," PLOS Biology, Public Library of Science, vol. 17(3), pages 1-8, March.
    3. Raj N. Sewduth & Béatrice Jaspard-Vinassa & Claire Peghaire & Aude Guillabert & Nathalie Franzl & Frederic Larrieu-Lahargue & Catherine Moreau & Marcus Fruttiger & Pascale Dufourcq & Thierry Couffinha, 2014. "The ubiquitin ligase PDZRN3 is required for vascular morphogenesis through Wnt/planar cell polarity signalling," Nature Communications, Nature, vol. 5(1), pages 1-13, December.
    4. Ismail Soussia & Sonia El Mouridi & Dawon Kang & Alice Leclercq-Blondel & Lamyaa Khoubza & Philippe Tardy & Nora Zariohi & Marie Gendrel & Florian Lesage & Eun-Jin Kim & Delphine Bichet & Olga Andrini, 2019. "Mutation of a single residue promotes gating of vertebrate and invertebrate two-pore domain potassium channels," Nature Communications, Nature, vol. 10(1), pages 1-13, December.
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