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Intercellular adhesion boots collective cell migration through elevated membrane tension

Author

Listed:
  • Brent M. Bijonowski

    (University of Münster)

  • Jongkwon Park

    (University of Münster)

  • Martin Bergert

    (European Molecular Biology Laboratory)

  • Christina Teubert

    (University of Münster)

  • Alba Diz-Muñoz

    (European Molecular Biology Laboratory)

  • Milos Galic

    (University of Münster)

  • Seraphine V. Wegner

    (University of Münster)

Abstract

In multicellular systems, the migration pattern of individual cells critically relies on the interactions with neighboring cells. Depending on the strength of these interactions, cells either move as a collective, as observed during morphogenesis and wound healing, or migrate individually, as it is the case for immune cells and fibroblasts. Mediators of cell-cell adhesions, such as cadherins coordinate collective dynamics by linking the cytoskeleton of neighboring cells. However, whether intercellular binding alone triggers signals that originate from within the plasma membrane itself, remains unclear. Here, we address this question through artificial photoswitchable cell-cell adhesions that selectively connect adjacent plasma membranes without linking directly to cytoskeletal elements. We find that these intercellular adhesions are sufficient to achieve collective cell migration. Linking adjacent cells increases membrane tension, which activates the enzyme phospholipase D2. The resulting increase in phosphatidic acid, in turn, stimulates the mammalian target of rapamycin, a known actuator of collective cell migration. Collectively, these findings introduce a membrane-based signaling axis as promotor of collective cell dynamics, which is independent of the direct coupling of cell-cell adhesions to the cytoskeleton.

Suggested Citation

  • Brent M. Bijonowski & Jongkwon Park & Martin Bergert & Christina Teubert & Alba Diz-Muñoz & Milos Galic & Seraphine V. Wegner, 2025. "Intercellular adhesion boots collective cell migration through elevated membrane tension," Nature Communications, Nature, vol. 16(1), pages 1-14, December.
  • Handle: RePEc:nat:natcom:v:16:y:2025:i:1:d:10.1038_s41467-025-56941-4
    DOI: 10.1038/s41467-025-56941-4
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    References listed on IDEAS

    as
    1. Brice Nzigou Mombo & Brent M. Bijonowski & Christopher A. Raab & Stephan Niland & Katrin Brockhaus & Marc Müller & Johannes A. Eble & Seraphine V. Wegner, 2023. "Reversible photoregulation of cell-cell adhesions with opto-E-cadherin," Nature Communications, Nature, vol. 14(1), pages 1-15, December.
    2. Laura Canty & Eleyine Zarour & Leily Kashkooli & Paul François & François Fagotto, 2017. "Sorting at embryonic boundaries requires high heterotypic interfacial tension," Nature Communications, Nature, vol. 8(1), pages 1-15, December.
    3. Andrew J. Price & Anna-Lena Cost & Hanna Ungewiß & Jens Waschke & Alexander R. Dunn & Carsten Grashoff, 2018. "Mechanical loading of desmosomes depends on the magnitude and orientation of external stress," Nature Communications, Nature, vol. 9(1), pages 1-11, December.
    4. Kazuya Tsujita & Reiko Satow & Shinobu Asada & Yoshikazu Nakamura & Luis Arnes & Keisuke Sako & Yasuyuki Fujita & Kiyoko Fukami & Toshiki Itoh, 2021. "Homeostatic membrane tension constrains cancer cell dissemination by counteracting BAR protein assembly," Nature Communications, Nature, vol. 12(1), pages 1-14, December.
    5. Maximilian Huber & Javier Casares-Arias & Reinhard Fässler & Daniel J. Müller & Nico Strohmeyer, 2023. "In mitosis integrins reduce adhesion to extracellular matrix and strengthen adhesion to adjacent cells," Nature Communications, Nature, vol. 14(1), pages 1-17, December.
    6. Asier Echarri & Dácil M. Pavón & Sara Sánchez & María García-García & Enrique Calvo & Carla Huerta-López & Diana Velázquez-Carreras & Christine Viaris de Lesegno & Nicholas Ariotti & Ana Lázaro-Carril, 2019. "An Abl-FBP17 mechanosensing system couples local plasma membrane curvature and stress fiber remodeling during mechanoadaptation," Nature Communications, Nature, vol. 10(1), pages 1-16, December.
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