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Mapping mechanical stress in curved epithelia of designed size and shape

Author

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  • Ariadna Marín-Llauradó

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

  • Sohan Kale

    (Virginia Polytechnic Institute and State University
    Virginia Polytechnic Institute and State University)

  • Adam Ouzeri

    (Universitat Politècnica de Catalunya-BarcelonaTech)

  • Tom Golde

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

  • Raimon Sunyer

    (The Barcelona Institute for Science and Technology (BIST)
    Universitat de Barcelona
    Universitat de Barcelona
    Centro de Investigación Biomédica en Red en Bioingeniería, Biomateriales y Nanomedicina (CIBER-BBN))

  • Alejandro Torres-Sánchez

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

  • Ernest Latorre

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

  • Manuel Gómez-González

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

  • Pere Roca-Cusachs

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

  • Marino Arroyo

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

  • Xavier Trepat

    (The Barcelona Institute for Science and Technology (BIST)
    Universitat de Barcelona
    Centro de Investigación Biomédica en Red en Bioingeniería, Biomateriales y Nanomedicina (CIBER-BBN)
    Institució Catalana de Recerca i Estudis Avançats (ICREA))

Abstract

The function of organs such as lungs, kidneys and mammary glands relies on the three-dimensional geometry of their epithelium. To adopt shapes such as spheres, tubes and ellipsoids, epithelia generate mechanical stresses that are generally unknown. Here we engineer curved epithelial monolayers of controlled size and shape and map their state of stress. We design pressurized epithelia with circular, rectangular and ellipsoidal footprints. We develop a computational method, called curved monolayer stress microscopy, to map the stress tensor in these epithelia. This method establishes a correspondence between epithelial shape and mechanical stress without assumptions of material properties. In epithelia with spherical geometry we show that stress weakly increases with areal strain in a size-independent manner. In epithelia with rectangular and ellipsoidal cross-section we find pronounced stress anisotropies that impact cell alignment. Our approach enables a systematic study of how geometry and stress influence epithelial fate and function in three-dimensions.

Suggested Citation

  • 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.
  • Handle: RePEc:nat:natcom:v:14:y:2023:i:1:d:10.1038_s41467-023-38879-7
    DOI: 10.1038/s41467-023-38879-7
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    as
    1. Werner Risau, 1997. "Mechanisms of angiogenesis," Nature, Nature, vol. 386(6626), pages 671-674, April.
    2. S. A. Gudipaty & J. Lindblom & P. D. Loftus & M. J. Redd & K. Edes & C. F. Davey & V. Krishnegowda & J. Rosenblatt, 2017. "Mechanical stretch triggers rapid epithelial cell division through Piezo1," Nature, Nature, vol. 543(7643), pages 118-121, March.
    3. Guillermo Martínez-Ara & Núria Taberner & Mami Takayama & Elissavet Sandaltzopoulou & Casandra E. Villava & Miquel Bosch-Padrós & Nozomu Takata & Xavier Trepat & Mototsugu Eiraku & Miki Ebisuya, 2022. "Optogenetic control of apical constriction induces synthetic morphogenesis in mammalian tissues," Nature Communications, Nature, vol. 13(1), pages 1-13, December.
    4. Emiliano Izquierdo & Theresa Quinkler & Stefano De Renzis, 2018. "Guided morphogenesis through optogenetic activation of Rho signalling during early Drosophila embryogenesis," Nature Communications, Nature, vol. 9(1), pages 1-13, December.
    5. Andreas Bauer & Magdalena Prechová & Lena Fischer & Ingo Thievessen & Martin Gregor & Ben Fabry, 2021. "pyTFM: A tool for traction force and monolayer stress microscopy," PLOS Computational Biology, Public Library of Science, vol. 17(6), pages 1-17, June.
    6. Robert W. Style & Callen Hyland & Rostislav Boltyanskiy & John S. Wettlaufer & Eric R. Dufresne, 2013. "Surface tension and contact with soft elastic solids," Nature Communications, Nature, vol. 4(1), pages 1-6, December.
    7. Laurent Pieuchot & Julie Marteau & Alain Guignandon & Thomas Dos Santos & Isabelle Brigaud & Pierre-François Chauvy & Thomas Cloatre & Arnaud Ponche & Tatiana Petithory & Pablo Rougerie & Maxime Vassa, 2018. "Curvotaxis directs cell migration through cell-scale curvature landscapes," Nature Communications, Nature, vol. 9(1), pages 1-13, December.
    8. Thuan Beng Saw & Amin Doostmohammadi & Vincent Nier & Leyla Kocgozlu & Sumesh Thampi & Yusuke Toyama & Philippe Marcq & Chwee Teck Lim & Julia M. Yeomans & Benoit Ladoux, 2017. "Topological defects in epithelia govern cell death and extrusion," Nature, Nature, vol. 544(7649), pages 212-216, April.
    9. Aleksandr Vasilyev & Yan Liu & Sudha Mudumana & Steve Mangos & Pui-Ying Lam & Arindam Majumdar & Jinhua Zhao & Kar-Lai Poon & Igor Kondrychyn & Vladimir Korzh & Iain A Drummond, 2009. "Collective Cell Migration Drives Morphogenesis of the Kidney Nephron," PLOS Biology, Public Library of Science, vol. 7(1), pages 1-14, January.
    10. 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.
    11. Léo Valon & Ariadna Marín-Llauradó & Thomas Wyatt & Guillaume Charras & Xavier Trepat, 2017. "Optogenetic control of cellular forces and mechanotransduction," Nature Communications, Nature, vol. 8(1), pages 1-10, April.
    12. 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.
    13. 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.
    14. Claudia G. Vasquez & Vipul T. Vachharajani & Carlos Garzon-Coral & Alexander R. Dunn, 2021. "Physical basis for the determination of lumen shape in a simple epithelium," Nature Communications, Nature, vol. 12(1), pages 1-12, December.
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