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Genetically-stable engineered optogenetic gene switches modulate spatial cell morphogenesis in two- and three-dimensional tissue cultures

Author

Listed:
  • Hannes M. Beyer

    (Universitätsstrasse 1)

  • Sant Kumar

    (ETH Zürich)

  • Marius Nieke

    (Universitätsstrasse 1)

  • Carroll M. C. Diehl

    (Universitätsstrasse 1)

  • Kun Tang

    (Universitätsstrasse 1)

  • Sara Shumka

    (Universitätsstrasse 1)

  • Cha San Koh

    (Universitätsstrasse 1)

  • Christian Fleck

    (Ernst-Zermelo-Straße 1)

  • Jamie A. Davies

    (University of Edinburgh)

  • Mustafa Khammash

    (ETH Zürich)

  • Matias D. Zurbriggen

    (Universitätsstrasse 1
    Universitätsstrasse 1)

Abstract

Recent advances in tissue engineering have been remarkable, yet the precise control of cellular behavior in 2D and 3D cultures remains challenging. One approach to address this limitation is to genomically engineer optogenetic control of cellular processes into tissues using gene switches that can operate with only a few genomic copies. Here, we implement blue and red light-responsive gene switches to engineer genomically stable two- and three-dimensional mammalian tissue models. Notably, we achieve precise control of cell death and morphogen-directed patterning in 2D and 3D tissues by optogenetically regulating cell necroptosis and synthetic WNT3A signaling at high spatiotemporal resolution. This is accomplished using custom-built patterned LED systems, including digital mirrors and photomasks, as well as laser techniques. These advancements demonstrate the capability of precise spatiotemporal modulation in tissue engineering and open up new avenues for developing programmable 3D tissue and organ models, with significant implications for biomedical research and therapeutic applications.

Suggested Citation

  • Hannes M. Beyer & Sant Kumar & Marius Nieke & Carroll M. C. Diehl & Kun Tang & Sara Shumka & Cha San Koh & Christian Fleck & Jamie A. Davies & Mustafa Khammash & Matias D. Zurbriggen, 2024. "Genetically-stable engineered optogenetic gene switches modulate spatial cell morphogenesis in two- and three-dimensional tissue cultures," Nature Communications, Nature, vol. 15(1), pages 1-16, December.
    • Handle: RePEc:nat:natcom:v:15:y:2024:i:1:d:10.1038_s41467-024-54350-7
    DOI: 10.1038/s41467-024-54350-7
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    References listed on IDEAS

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    1. Andrii A. Kaberniuk & Mikhail Baloban & Mikhail V. Monakhov & Daria M. Shcherbakova & Vladislav V. Verkhusha, 2021. "Single-component near-infrared optogenetic systems for gene transcription regulation," Nature Communications, Nature, vol. 12(1), pages 1-12, December.
    2. Dominik Niopek & Dirk Benzinger & Julia Roensch & Thomas Draebing & Pierre Wehler & Roland Eils & Barbara Di Ventura, 2014. "Engineering light-inducible nuclear localization signals for precise spatiotemporal control of protein dynamics in living cells," Nature Communications, Nature, vol. 5(1), pages 1-11, December.
    3. Dominik Niopek & Pierre Wehler & Julia Roensch & Roland Eils & Barbara Di Ventura, 2016. "Optogenetic control of nuclear protein export," Nature Communications, Nature, vol. 7(1), pages 1-9, April.
    4. Anselm Levskaya & Orion D. Weiner & Wendell A. Lim & Christopher A. Voigt, 2009. "Spatiotemporal control of cell signalling using a light-switchable protein interaction," Nature, Nature, vol. 461(7266), pages 997-1001, October.
    5. J. B. Gurdon & P.-Y. Bourillot, 2001. "Morphogen gradient interpretation," Nature, Nature, vol. 413(6858), pages 797-803, October.
    6. Petra van Bergeijk & Max Adrian & Casper C. Hoogenraad & Lukas C. Kapitein, 2015. "Optogenetic control of organelle transport and positioning," Nature, Nature, vol. 518(7537), pages 111-114, February.
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    Cited by:

    1. Sant Kumar & Hannes M. Beyer & Mingzhe Chen & Matias D. Zurbriggen & Mustafa Khammash, 2024. "Image-guided optogenetic spatiotemporal tissue patterning using μPatternScope," Nature Communications, Nature, vol. 15(1), pages 1-14, December.

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