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Active superelasticity in three-dimensional epithelia of controlled shape

Author

Listed:
  • Ernest Latorre

    (The Barcelona Institute for Science and Technology (BIST)
    LaCàN, Universitat Politècnica de Catalunya-BarcelonaTech)

  • Sohan Kale

    (LaCàN, Universitat Politècnica de Catalunya-BarcelonaTech)

  • Laura Casares

    (The Barcelona Institute for Science and Technology (BIST))

  • Manuel Gómez-González

    (The Barcelona Institute for Science and Technology (BIST))

  • Marina Uroz

    (The Barcelona Institute for Science and Technology (BIST))

  • Léo Valon

    (The Barcelona Institute for Science and Technology (BIST))

  • Roshna V. Nair

    (INM-Leibniz Institut für Neue Materialien)

  • Elena Garreta

    (The Barcelona Institute for Science and Technology (BIST))

  • Nuria Montserrat

    (The Barcelona Institute for Science and Technology (BIST)
    Biomateriales y Nanomedicina)

  • Aránzazu Campo

    (INM-Leibniz Institut für Neue Materialien
    Saarland University)

  • Benoit Ladoux

    (CNRS UMR 7592, Institut Jacques Monod (IJM), Université Paris Diderot
    Mechanobiology Institute (MBI), National University of Singapore)

  • Marino Arroyo

    (The Barcelona Institute for Science and Technology (BIST)
    LaCàN, Universitat Politècnica de Catalunya-BarcelonaTech)

  • Xavier Trepat

    (The Barcelona Institute for Science and Technology (BIST)
    Biomateriales y Nanomedicina
    Unitat de Biofísica i Bioenginyeria, Universitat de Barcelona
    Institució Catalana de Recerca i Estudis Avançats (ICREA))

Abstract

Fundamental biological processes are carried out by curved epithelial sheets that enclose a pressurized lumen. How these sheets develop and withstand three-dimensional deformations has remained unclear. Here we combine measurements of epithelial tension and shape with theoretical modelling to show that epithelial sheets are active superelastic materials. We produce arrays of epithelial domes with controlled geometry. Quantification of luminal pressure and epithelial tension reveals a tensional plateau over several-fold areal strains. These extreme strains in the tissue are accommodated by highly heterogeneous strains at a cellular level, in seeming contradiction to the measured tensional uniformity. This phenomenon is reminiscent of superelasticity, a behaviour that is generally attributed to microscopic material instabilities in metal alloys. We show that in epithelial cells this instability is triggered by a stretch-induced dilution of the actin cortex, and is rescued by the intermediate filament network. Our study reveals a type of mechanical behaviour—which we term active superelasticity—that enables epithelial sheets to sustain extreme stretching under constant tension.

Suggested Citation

  • 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.
  • Handle: RePEc:nat:nature:v:563:y:2018:i:7730:d:10.1038_s41586-018-0671-4
    DOI: 10.1038/s41586-018-0671-4
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    Citations

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    Cited by:

    1. Jorge Barbazan & Carlos Pérez-González & Manuel Gómez-González & Mathieu Dedenon & Sophie Richon & Ernest Latorre & Marco Serra & Pascale Mariani & Stéphanie Descroix & Pierre Sens & Xavier Trepat & D, 2023. "Cancer-associated fibroblasts actively compress cancer cells and modulate mechanotransduction," Nature Communications, Nature, vol. 14(1), pages 1-17, December.
    2. Ariadna Marín-Llauradó & Sohan Kale & Adam Ouzeri & Tom Golde & Raimon Sunyer & Alejandro Torres-Sánchez & Ernest Latorre & Manuel Gómez-González & Pere Roca-Cusachs & Marino Arroyo & Xavier Trepat, 2023. "Mapping mechanical stress in curved epithelia of designed size and shape," Nature Communications, Nature, vol. 14(1), pages 1-11, December.
    3. Mohammad Ikbal Choudhury & Yizeng Li & Panagiotis Mistriotis & Ana Carina N. Vasconcelos & Eryn E. Dixon & Jing Yang & Morgan Benson & Debonil Maity & Rebecca Walker & Leigha Martin & Fatima Koroma & , 2022. "Kidney epithelial cells are active mechano-biological fluid pumps," Nature Communications, Nature, vol. 13(1), pages 1-13, December.
    4. 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.
    5. Shalaka Chitale & Wenxuan Wu & Avik Mukherjee & Herbert Lannon & Pooja Suresh & Ishan Nag & Christina M. Ambrosi & Rona S. Gertner & Hendrick Melo & Brendan Powers & Hollin Wilkins & Henry Hinton & Mi, 2023. "A semiconductor 96-microplate platform for electrical-imaging based high-throughput phenotypic screening," Nature Communications, Nature, vol. 14(1), pages 1-13, December.
    6. Jiu-Tao Hang & Yu Kang & Guang-Kui Xu & Huajian Gao, 2021. "A hierarchical cellular structural model to unravel the universal power-law rheological behavior of living cells," Nature Communications, Nature, vol. 12(1), pages 1-7, December.
    7. Gawoon Shim & Isaac B. Breinyn & Alejandro Martínez-Calvo & Sameeksha Rao & Daniel J. Cohen, 2024. "Bioelectric stimulation controls tissue shape and size," Nature Communications, Nature, vol. 15(1), pages 1-17, December.

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