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Multiciliated cells use filopodia to probe tissue mechanics during epithelial integration in vivo

Author

Listed:
  • Guilherme Ventura

    (University of Copenhagen)

  • Aboutaleb Amiri

    (Max Planck Institute for the Physics of Complex Systems)

  • Raghavan Thiagarajan

    (University of Copenhagen)

  • Mari Tolonen

    (University of Copenhagen)

  • Amin Doostmohammadi

    (University of Copenhagen)

  • Jakub Sedzinski

    (University of Copenhagen)

Abstract

During embryonic development, regeneration, and homeostasis, cells have to migrate and physically integrate into the target tissues where they ultimately execute their function. While much is known about the biochemical pathways driving cell migration in vivo, we are only beginning to understand the mechanical interplay between migrating cells and their surrounding tissue. Here, we reveal that multiciliated cell precursors in the Xenopus embryo use filopodia to pull at the vertices of the overlying epithelial sheet. This pulling is effectively used to sense vertex stiffness and identify the preferred positions for cell integration into the tissue. Notably, we find that pulling forces equip multiciliated cells with the ability to remodel the epithelial junctions of the neighboring cells, enabling them to generate a permissive environment that facilitates integration. Our findings reveal the intricate physical crosstalk at the cell-tissue interface and uncover previously unknown functions for mechanical forces in orchestrating cell integration.

Suggested Citation

  • Guilherme Ventura & Aboutaleb Amiri & Raghavan Thiagarajan & Mari Tolonen & Amin Doostmohammadi & Jakub Sedzinski, 2022. "Multiciliated cells use filopodia to probe tissue mechanics during epithelial integration in vivo," Nature Communications, Nature, vol. 13(1), pages 1-15, December.
  • Handle: RePEc:nat:natcom:v:13:y:2022:i:1:d:10.1038_s41467-022-34165-0
    DOI: 10.1038/s41467-022-34165-0
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    1. Floris Bosveld & Olga Markova & Boris Guirao & Charlotte Martin & Zhimin Wang & Anaëlle Pierre & Maria Balakireva & Isabelle Gaugue & Anna Ainslie & Nicolas Christophorou & David K. Lubensky & Nicolas, 2016. "Epithelial tricellular junctions act as interphase cell shape sensors to orient mitosis," Nature, Nature, vol. 530(7591), pages 495-498, February.
    2. Adam C. Martin & Matthias Kaschube & Eric F. Wieschaus, 2009. "Pulsed contractions of an actin–myosin network drive apical constriction," Nature, Nature, vol. 457(7228), pages 495-499, January.
    3. N. O. Alieva & A. K. Efremov & S. Hu & D. Oh & Z. Chen & M. Natarajan & H. T. Ong & A. Jégou & G. Romet-Lemonne & J. T. Groves & M. P. Sheetz & J. Yan & A. D. Bershadsky, 2019. "Myosin IIA and formin dependent mechanosensitivity of filopodia adhesion," Nature Communications, Nature, vol. 10(1), pages 1-14, December.
    4. George T. Eisenhoffer & Patrick D. Loftus & Masaaki Yoshigi & Hideo Otsuna & Chi-Bin Chien & Paul A. Morcos & Jody Rosenblatt, 2012. "Crowding induces live cell extrusion to maintain homeostatic cell numbers in epithelia," Nature, Nature, vol. 484(7395), pages 546-549, April.
    5. Floris Bosveld & Olga Markova & Boris Guirao & Charlotte Martin & Zhimin Wang & Anaëlle Pierre & Maria Balakireva & Isabelle Gaugue & Anna Ainslie & Nicolas Christophorou & David K. Lubensky & Nicolas, 2016. "Erratum: Epithelial tricellular junctions act as interphase cell shape sensors to orient mitosis," Nature, Nature, vol. 534(7605), pages 138-138, June.
    6. Claire Bertet & Lawrence Sulak & Thomas Lecuit, 2004. "Myosin-dependent junction remodelling controls planar cell intercalation and axis elongation," Nature, Nature, vol. 429(6992), pages 667-671, June.
    7. Elias H. Barriga & Kristian Franze & Guillaume Charras & Roberto Mayor, 2018. "Tissue stiffening coordinates morphogenesis by triggering collective cell migration in vivo," Nature, Nature, vol. 554(7693), pages 523-527, February.
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