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Optogenetic control of apical constriction induces synthetic morphogenesis in mammalian tissues

Author

Listed:
  • Guillermo Martínez-Ara

    (European Molecular Biology Laboratory (EMBL) Barcelona)

  • Núria Taberner

    (European Molecular Biology Laboratory (EMBL) Barcelona
    RIKEN Center for Biosystems Dynamics Research (RIKEN BDR))

  • Mami Takayama

    (RIKEN Center for Biosystems Dynamics Research (RIKEN BDR))

  • Elissavet Sandaltzopoulou

    (European Molecular Biology Laboratory (EMBL) Barcelona)

  • Casandra E. Villava

    (European Molecular Biology Laboratory (EMBL) Barcelona)

  • Miquel Bosch-Padrós

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

  • Nozomu Takata

    (RIKEN Center for Biosystems Dynamics Research (RIKEN BDR))

  • Xavier Trepat

    (The Barcelona Institute for Science and Technology (BIST)
    Biomateriales y Nanomedicina (CIBER-BBN)
    Institució Catalana de Recerca i Estudis Avançats (ICREA))

  • Mototsugu Eiraku

    (RIKEN Center for Biosystems Dynamics Research (RIKEN BDR))

  • Miki Ebisuya

    (European Molecular Biology Laboratory (EMBL) Barcelona
    RIKEN Center for Biosystems Dynamics Research (RIKEN BDR))

Abstract

The emerging field of synthetic developmental biology proposes bottom-up approaches to examine the contribution of each cellular process to complex morphogenesis. However, the shortage of tools to manipulate three-dimensional (3D) shapes of mammalian tissues hinders the progress of the field. Here we report the development of OptoShroom3, an optogenetic tool that achieves fast spatiotemporal control of apical constriction in mammalian epithelia. Activation of OptoShroom3 through illumination in an epithelial Madin-Darby Canine Kidney (MDCK) cell sheet reduces the apical surface of the stimulated cells and causes displacements in the adjacent regions. Light-induced apical constriction provokes the folding of epithelial cell colonies on soft gels. Its application to murine and human neural organoids leads to thickening of neuroepithelia, apical lumen reduction in optic vesicles, and flattening in neuroectodermal tissues. These results show that spatiotemporal control of apical constriction can trigger several types of 3D deformation depending on the initial tissue context.

Suggested Citation

  • 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.
    • Handle: RePEc:nat:natcom:v:13:y:2022:i:1:d:10.1038_s41467-022-33115-0
    DOI: 10.1038/s41467-022-33115-0
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    References listed on IDEAS

    as
    1. 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.
    2. Mototsugu Eiraku & Nozomu Takata & Hiroki Ishibashi & Masako Kawada & Eriko Sakakura & Satoru Okuda & Kiyotoshi Sekiguchi & Taiji Adachi & Yoshiki Sasai, 2011. "Self-organizing optic-cup morphogenesis in three-dimensional culture," Nature, Nature, vol. 472(7341), pages 51-56, April.
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    1. 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.

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