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Cellular locomotion using environmental topography

Author

Listed:
  • Anne Reversat

    (Institute of Science and Technology Austria (IST Austria)
    University of Liverpool)

  • Florian Gaertner

    (Institute of Science and Technology Austria (IST Austria))

  • Jack Merrin

    (Institute of Science and Technology Austria (IST Austria))

  • Julian Stopp

    (Institute of Science and Technology Austria (IST Austria))

  • Saren Tasciyan

    (Institute of Science and Technology Austria (IST Austria))

  • Juan Aguilera

    (Institute of Science and Technology Austria (IST Austria))

  • Ingrid Vries

    (Institute of Science and Technology Austria (IST Austria))

  • Robert Hauschild

    (Institute of Science and Technology Austria (IST Austria))

  • Miroslav Hons

    (Institute of Science and Technology Austria (IST Austria)
    Institute of Scientific Instruments of the Czech Academy of Sciences
    Charles University)

  • Matthieu Piel

    (Institut Curie, PSL Research University, CNRS, UMR 144
    Institut Pierre-Gilles de Gennes, PSL Research University)

  • Andrew Callan-Jones

    (Laboratoire Matière et Systèmes Complexes, UMR 7057 CNRS, Université Paris Diderot)

  • Raphael Voituriez

    (Laboratoire de Physique Theorique de la Matière Condensée et Laboratoire Jean Perrin, CNRS/Université Pierre-et-Marie Curie)

  • Michael Sixt

    (Institute of Science and Technology Austria (IST Austria))

Abstract

Eukaryotic cells migrate by coupling the intracellular force of the actin cytoskeleton to the environment. While force coupling is usually mediated by transmembrane adhesion receptors, especially those of the integrin family, amoeboid cells such as leukocytes can migrate extremely fast despite very low adhesive forces1. Here we show that leukocytes cannot only migrate under low adhesion but can also transmit forces in the complete absence of transmembrane force coupling. When confined within three-dimensional environments, they use the topographical features of the substrate to propel themselves. Here the retrograde flow of the actin cytoskeleton follows the texture of the substrate, creating retrograde shear forces that are sufficient to drive the cell body forwards. Notably, adhesion-dependent and adhesion-independent migration are not mutually exclusive, but rather are variants of the same principle of coupling retrograde actin flow to the environment and thus can potentially operate interchangeably and simultaneously. As adhesion-free migration is independent of the chemical composition of the environment, it renders cells completely autonomous in their locomotive behaviour.

Suggested Citation

  • Anne Reversat & Florian Gaertner & Jack Merrin & Julian Stopp & Saren Tasciyan & Juan Aguilera & Ingrid Vries & Robert Hauschild & Miroslav Hons & Matthieu Piel & Andrew Callan-Jones & Raphael Voituri, 2020. "Cellular locomotion using environmental topography," Nature, Nature, vol. 582(7813), pages 582-585, June.
  • Handle: RePEc:nat:nature:v:582:y:2020:i:7813:d:10.1038_s41586-020-2283-z
    DOI: 10.1038/s41586-020-2283-z
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    Cited by:

    1. Tianchi Chen & Cecilia H. Fernández-Espartero & Abigail Illand & Ching-Ting Tsai & Yang Yang & Benjamin Klapholz & Pierre Jouchet & Mélanie Fabre & Olivier Rossier & Bianxiao Cui & Sandrine Lévêque-Fo, 2024. "Actin-driven nanotopography promotes stable integrin adhesion formation in developing tissue," Nature Communications, Nature, vol. 15(1), pages 1-16, December.
    2. Haoqing Jerry Wang & Yao Wang & Seyed Sajad Mirjavadi & Tomas Andersen & Laura Moldovan & Parham Vatankhah & Blake Russell & Jasmine Jin & Zijing Zhou & Qing Li & Charles D. Cox & Qian Peter Su & Lini, 2024. "Microscale geometrical modulation of PIEZO1 mediated mechanosensing through cytoskeletal redistribution," Nature Communications, Nature, vol. 15(1), pages 1-17, December.
    3. Chao Jiang & Hong-Yu Luo & Xinpeng Xu & Shuo-Xing Dou & Wei Li & Dongshi Guan & Fangfu Ye & Xiaosong Chen & Ming Guo & Peng-Ye Wang & Hui Li, 2023. "Switch of cell migration modes orchestrated by changes of three-dimensional lamellipodium structure and intracellular diffusion," Nature Communications, Nature, vol. 14(1), pages 1-13, December.
    4. Zülal Cibir & Jacqueline Hassel & Justin Sonneck & Lennart Kowitz & Alexander Beer & Andreas Kraus & Gabriel Hallekamp & Martin Rosenkranz & Pascal Raffelberg & Sven Olfen & Kamil Smilowski & Roman Bu, 2023. "ComplexEye: a multi-lens array microscope for high-throughput embedded immune cell migration analysis," Nature Communications, Nature, vol. 14(1), pages 1-13, December.

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