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Patterning and dynamics of membrane adhesion under hydraulic stress

Author

Listed:
  • Céline Dinet

    (Durham University
    CNRS-Aix-Marseille University)

  • Alejandro Torres-Sánchez

    (Universitat Politècnica de Catalunya-BarcelonaTech
    The Barcelona Institute of Science and Technology
    European Molecular Biology Laboratory (EMBL-Barcelona))

  • Roberta Lanfranco

    (University of Cambridge)

  • Lorenzo Michele

    (University of Cambridge
    Imperial College of London)

  • Marino Arroyo

    (Universitat Politècnica de Catalunya-BarcelonaTech
    The Barcelona Institute of Science and Technology
    Centre Internacional de Mètodes Numèrics en Enginyeria (CIMNE))

  • Margarita Staykova

    (Durham University)

Abstract

Hydraulic fracturing plays a major role in cavity formation during embryonic development, when pressurized fluid opens microlumens at cell-cell contacts, which evolve to form a single large lumen. However, the fundamental physical mechanisms behind these processes remain masked by the complexity and specificity of biological systems. Here, we show that adhered lipid vesicles subjected to osmotic stress form hydraulic microlumens similar to those in cells. Combining vesicle experiments with theoretical modelling and numerical simulations, we provide a physical framework for the hydraulic reconfiguration of cell-cell adhesions. We map the conditions for microlumen formation from a pristine adhesion, the emerging dynamical patterns and their subsequent maturation. We demonstrate control of the fracturing process depending on the applied pressure gradients and the type and density of membrane bonds. Our experiments further reveal an unexpected, passive transition of microlumens to closed buds that suggests a physical route to adhesion remodeling by endocytosis.

Suggested Citation

  • Céline Dinet & Alejandro Torres-Sánchez & Roberta Lanfranco & Lorenzo Michele & Marino Arroyo & Margarita Staykova, 2023. "Patterning and dynamics of membrane adhesion under hydraulic stress," Nature Communications, Nature, vol. 14(1), pages 1-11, December.
  • Handle: RePEc:nat:natcom:v:14:y:2023:i:1:d:10.1038_s41467-023-43246-7
    DOI: 10.1038/s41467-023-43246-7
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    1. Anita Joanna Kosmalska & Laura Casares & Alberto Elosegui-Artola & Joseph Jose Thottacherry & Roberto Moreno-Vicente & Víctor González-Tarragó & Miguel Ángel del Pozo & Satyajit Mayor & Marino Arroyo , 2015. "Physical principles of membrane remodelling during cell mechanoadaptation," Nature Communications, Nature, vol. 6(1), pages 1-11, November.
    2. Ernest Latorre & Sohan Kale & Laura Casares & Manuel Gómez-González & Marina Uroz & Léo Valon & Roshna V. Nair & Elena Garreta & Nuria Montserrat & Aránzazu Campo & Benoit Ladoux & Marino Arroyo & Xav, 2018. "Active superelasticity in three-dimensional epithelia of controlled shape," Nature, Nature, vol. 563(7730), pages 203-208, November.
    3. V. Trappe & V. Prasad & Luca Cipelletti & P. N. Segre & D. A. Weitz, 2001. "Jamming phase diagram for attractive particles," Nature, Nature, vol. 411(6839), pages 772-775, June.
    4. Chii Jou Chan & Maria Costanzo & Teresa Ruiz-Herrero & Gregor Mönke & Ryan J. Petrie & Martin Bergert & Alba Diz-Muñoz & L. Mahadevan & Takashi Hiiragi, 2019. "Hydraulic control of mammalian embryo size and cell fate," Nature, Nature, vol. 571(7763), pages 112-116, July.
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