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Microtubule deacetylation reduces cell stiffness to allow the onset of collective cell migration in vivo

CL Marchant, View ORCID ProfileAN Malmi-Kakkada, View ORCID ProfileJA Espina, View ORCID ProfileEH Barriga
doi: https://doi.org/10.1101/2021.08.12.456059
CL Marchant
1Mechanisms of Morphogenesis Lab, Gulbenkian Institute of Science (IGC), 2780-156 Oeiras, Portugal
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AN Malmi-Kakkada
2Computational Biological Physics Lab, Dept. of Chemistry and Physics, Augusta University, Augusta, GA 30912, USA
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JA Espina
1Mechanisms of Morphogenesis Lab, Gulbenkian Institute of Science (IGC), 2780-156 Oeiras, Portugal
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EH Barriga
1Mechanisms of Morphogenesis Lab, Gulbenkian Institute of Science (IGC), 2780-156 Oeiras, Portugal
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  • For correspondence: ebarriga@igc.gulbenkian.pt
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Abstract

Embryogenesis, tissue repair and cancer metastasis rely on collective cell migration (CCM). In vitro studies propose that migrating cells are stiffer when exposed to stiff substrates, known to allow CCM, but softer when plated in compliant non-permissive surfaces. Here, by combining in vivo atomic force microscopy (iAFM) and modelling we reveal that to collectively migrate in vivo, cells require to dynamically decrease their stiffness in response to the temporal stiffening of their native substrate. Moreover, molecular and mechanical perturbations of embryonic tissues uncover that this unexpected cell mechanical response is achieved by a new mechanosensitive pathway involving Piezo1-mediated microtubule deacetylation. Finally, lowering microtubule acetylation and consequently cell stiffness was sufficient to allow CCM in soft non-permissive substrates, suggesting that a fixed value of substrate stiffness is not as essential for CCM as it is reaching an optimal cell-to-substrate stiffness value. These in vivo insights on cell-to-substrate mechanical interplay have major implications to our re-interpretation of physiological and pathological contexts.

Competing Interest Statement

The authors have declared no competing interest.

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The copyright holder for this preprint is the author/funder, who has granted bioRxiv a license to display the preprint in perpetuity. It is made available under a CC-BY-NC-ND 4.0 International license.
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Posted August 12, 2021.
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Microtubule deacetylation reduces cell stiffness to allow the onset of collective cell migration in vivo
CL Marchant, AN Malmi-Kakkada, JA Espina, EH Barriga
bioRxiv 2021.08.12.456059; doi: https://doi.org/10.1101/2021.08.12.456059
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Microtubule deacetylation reduces cell stiffness to allow the onset of collective cell migration in vivo
CL Marchant, AN Malmi-Kakkada, JA Espina, EH Barriga
bioRxiv 2021.08.12.456059; doi: https://doi.org/10.1101/2021.08.12.456059

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