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Deconstructing body axis morphogenesis in zebrafish embryos using robot-assisted tissue micromanipulation

Author

Listed:
  • Ece Özelçi

    (Institute of Mechanical Engineering, Ecole Polytechnique Fédérale de Lausanne (EPFL)
    Institute of Bioengineering, EPFL)

  • Erik Mailand

    (Institute of Mechanical Engineering, Ecole Polytechnique Fédérale de Lausanne (EPFL))

  • Matthias Rüegg

    (Institute of Mechanical Engineering, Ecole Polytechnique Fédérale de Lausanne (EPFL))

  • Andrew C. Oates

    (Institute of Bioengineering, EPFL)

  • Mahmut Selman Sakar

    (Institute of Mechanical Engineering, Ecole Polytechnique Fédérale de Lausanne (EPFL)
    Institute of Bioengineering, EPFL)

Abstract

Classic microsurgical techniques, such as those used in the early 1900s by Mangold and Spemann, have been instrumental in advancing our understanding of embryonic development. However, these techniques are highly specialized, leading to issues of inter-operator variability. Here we introduce a user-friendly robotic microsurgery platform that allows precise mechanical manipulation of soft tissues in zebrafish embryos. Using our platform, we reproducibly targeted precise regions of tail explants, and quantified the response in real-time by following notochord and presomitic mesoderm (PSM) morphogenesis and segmentation clock dynamics during vertebrate anteroposterior axis elongation. We find an extension force generated through the posterior notochord that is strong enough to buckle the structure. Our data suggest that this force generates a unidirectional notochord extension towards the tailbud because PSM tissue around the posterior notochord does not let it slide anteriorly. These results complement existing biomechanical models of axis elongation, revealing a critical coupling between the posterior notochord, the tailbud, and the PSM, and show that somite patterning is robust against structural perturbations.

Suggested Citation

  • Ece Özelçi & Erik Mailand & Matthias Rüegg & Andrew C. Oates & Mahmut Selman Sakar, 2022. "Deconstructing body axis morphogenesis in zebrafish embryos using robot-assisted tissue micromanipulation," Nature Communications, Nature, vol. 13(1), pages 1-12, December.
  • Handle: RePEc:nat:natcom:v:13:y:2022:i:1:d:10.1038_s41467-022-35632-4
    DOI: 10.1038/s41467-022-35632-4
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    References listed on IDEAS

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    1. Andrea J. Liu & Sidney R. Nagel, 1998. "Jamming is not just cool any more," Nature, Nature, vol. 396(6706), pages 21-22, November.
    2. Alessandro Mongera & Payam Rowghanian & Hannah J. Gustafson & Elijah Shelton & David A. Kealhofer & Emmet K. Carn & Friedhelm Serwane & Adam A. Lucio & James Giammona & Otger Campàs, 2018. "A fluid-to-solid jamming transition underlies vertebrate body axis elongation," Nature, Nature, vol. 561(7723), pages 401-405, September.
    3. Margarete Diaz-Cuadros & Daniel E. Wagner & Christoph Budjan & Alexis Hubaud & Oscar A. Tarazona & Sophia Donelly & Arthur Michaut & Ziad Al Tanoury & Kumiko Yoshioka-Kobayashi & Yusuke Niino & Ryoich, 2020. "In vitro characterization of the human segmentation clock," Nature, Nature, vol. 580(7801), pages 113-118, April.
    4. Mitsuhiro Matsuda & Yoshihiro Yamanaka & Maya Uemura & Mitsujiro Osawa & Megumu K. Saito & Ayako Nagahashi & Megumi Nishio & Long Guo & Shiro Ikegawa & Satoko Sakurai & Shunsuke Kihara & Thomas L. Mau, 2020. "Recapitulating the human segmentation clock with pluripotent stem cells," Nature, Nature, vol. 580(7801), pages 124-129, April.
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