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Targeted mechanical stimulation via magnetic nanoparticles guides in vitro tissue development

Author

Listed:
  • Abdel Rahman Abdel Fattah

    (KU Leuven
    CeMM Research Center for Molecular Medicine of the Austrian Academy of Sciences)

  • Niko Kolaitis

    (KU Leuven)

  • Katrien Daele

    (KU Leuven)

  • Brian Daza

    (KU Leuven)

  • Andika Gregorius Rustandi

    (KU Leuven)

  • Adrian Ranga

    (KU Leuven)

Abstract

Tissues take shape through a series of morphogenetic movements guided by local cell-scale mechanical forces. Current in vitro approaches to recapitulate tissue mechanics rely on uncontrolled self-organization or on the imposition of extrinsic and homogenous forces using matrix or instrument-driven stimulation, thereby failing to recapitulate highly localized and spatially varying forces. Here we develop a method for targeted mechanical stimulation of organoids using embedded magnetic nanoparticles. We show that magnetic clusters within organoids can be produced by sequential aggregation of magnetically labeled and non-labeled human pluripotent stem cells. These clusters impose local mechanical forces on the surrounding cells in response to applied magnetic fields. We show that precise, spatially defined actuation provides short-term mechanical tissue perturbations as well as long-term cytoskeleton remodeling in these organoids, which we term “magnetoids”. We demonstrate that targeted magnetic nanoparticle-driven actuation guides asymmetric tissue growth and proliferation, leading to enhanced patterning in human neural magnetoids. This approach, enabled by nanoparticle technology, allows for precise and locally controllable mechanical actuation in human neural tube organoids, and could be widely applicable to interrogate the role of local mechanotransduction in developmental and disease model systems.

Suggested Citation

  • Abdel Rahman Abdel Fattah & Niko Kolaitis & Katrien Daele & Brian Daza & Andika Gregorius Rustandi & Adrian Ranga, 2023. "Targeted mechanical stimulation via magnetic nanoparticles guides in vitro tissue development," Nature Communications, Nature, vol. 14(1), pages 1-14, December.
  • Handle: RePEc:nat:natcom:v:14:y:2023:i:1:d:10.1038_s41467-023-41037-8
    DOI: 10.1038/s41467-023-41037-8
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    as
    1. Abdel Rahman Abdel Fattah & Brian Daza & Gregorius Rustandi & Miguel Ángel Berrocal-Rubio & Benjamin Gorissen & Suresh Poovathingal & Kristofer Davie & Jorge Barrasa-Fano & Mar Cóndor & Xuanye Cao & D, 2021. "Actuation enhances patterning in human neural tube organoids," Nature Communications, Nature, vol. 12(1), pages 1-13, December.
    2. Sirio Dupont & Leonardo Morsut & Mariaceleste Aragona & Elena Enzo & Stefano Giulitti & Michelangelo Cordenonsi & Francesca Zanconato & Jimmy Le Digabel & Mattia Forcato & Silvio Bicciato & Nicola Elv, 2011. "Role of YAP/TAZ in mechanotransduction," Nature, Nature, vol. 474(7350), pages 179-183, June.
    3. Hye Young Kim & Timothy R. Jackson & Carsten Stuckenholz & Lance A. Davidson, 2020. "Tissue mechanics drives regeneration of a mucociliated epidermis on the surface of Xenopus embryonic aggregates," Nature Communications, Nature, vol. 11(1), pages 1-10, December.
    4. Anna Urciuolo & Giovanni Giuseppe Giobbe & Yixiao Dong & Federica Michielin & Luca Brandolino & Michael Magnussen & Onelia Gagliano & Giulia Selmin & Valentina Scattolini & Paolo Raffa & Paola Caccin , 2023. "Hydrogel-in-hydrogel live bioprinting for guidance and control of organoids and organotypic cultures," Nature Communications, Nature, vol. 14(1), pages 1-14, December.
    5. Nikolce Gjorevski & Norman Sachs & Andrea Manfrin & Sonja Giger & Maiia E. Bragina & Paloma Ordóñez-Morán & Hans Clevers & Matthias P. Lutolf, 2016. "Designer matrices for intestinal stem cell and organoid culture," Nature, Nature, vol. 539(7630), pages 560-564, November.
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