Rapid mechanosensitive migration and dispersal of newly divided mesenchymal cells aid their recruitment into dermal condensates

Jon Riddell; Shahzeb Raja Noureen; Luigi  Sedda; James D. Glover; William K. W. Ho; Connor A. Bain; Arianna Berbeglia; Helen Brown; Calum Anderson; Yuhang Chen; Michael L. Crichton; Kit Yates; Richard L Mort; Denis J. Headon

doi:10.1371/journal.pbio.3002316

Rapid mechanosensitive migration and dispersal of newly divided mesenchymal cells aid their recruitment into dermal condensates

Jon Riddell, Shahzeb Raja Noureen, Luigi Sedda, James D. Glover, William K. W. Ho, Connor A. Bain, Arianna Berbeglia, Helen Brown, Calum Anderson, Yuhang Chen, Michael L. Crichton, Kit Yates, Richard L Mort, Denis J. Headon

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3 Citations (SciVal)

Abstract

Embryonic mesenchymal cells are dispersed within an extracellular matrix but can coalesce to form condensates with key developmental roles. Cells within condensates undergo fate and morphological changes and induce cell fate changes in nearby epithelia to produce structures including hair follicles, feathers, or intestinal villi. Here, by imaging mouse and chicken embryonic skin, we find that mesenchymal cells undergo much of their dispersal in early interphase, in a stereotyped process of displacement driven by 3 h of rapid and persistent migration followed by a long period of low motility. The cell division plane and the elevated migration speed and persistence of newly born mesenchymal cells are mechanosensitive, aligning with tissue tension, and are reliant on active WNT secretion. This behaviour disperses mesenchymal cells and allows daughters of recent divisions to travel long distances to enter dermal condensates, demonstrating an unanticipated effect of cell cycle subphase on core mesenchymal behaviour.

Original language	English
Article number	e3002316
Number of pages	21
Journal	PLOS Biology
Volume	21
Issue number	9
Early online date	25 Sept 2023
DOIs	https://doi.org/10.1371/journal.pbio.3002316
Publication status	Published - 30 Sept 2023

Bibliographical note

Funding: This work was supported by BBSRC awards BB/T007788/1 and BBS/E/D/10002071 received by DJH, and by North West Cancer Research Fund award CR1132, Royal Society award RGS\R2\212427 and Dr. Philip Welch STEM
research project funding received by RLM. SRN is supported by a scholarship from the EPSRC Centre for Doctoral Training in Statistical Applied Mathematics at Bath (SAMBa), under the project EP/S022945/1. This research made use of the Balena High Performance Computing (HPC) Service at the University of Bath. CAB is supported by a Carnegie Trust for Scotland PhD studentship. The funder had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript.

Data Availability Statement: The authors confirm that all data underlying the findings are fully available without restriction. All relevant data are within the paper and its Supporting Information files. Source code has been deposited in Zenodo repositories https://doi.org/10.5281/zenodo. 8229691 and https://doi.org/10.5281/zenodo.8229341

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10.1371/journal.pbio.3002316Licence: CC BY

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Riddell, J., Raja Noureen, S., Sedda, L., Glover, J. D., Ho, W. K. W., Bain, C. A., Berbeglia, A., Brown, H., Anderson, C., Chen, Y., Crichton, M. L., Yates, K., Mort, R. L., & Headon, D. J. (2023). Rapid mechanosensitive migration and dispersal of newly divided mesenchymal cells aid their recruitment into dermal condensates. PLOS Biology , 21(9), Article e3002316. https://doi.org/10.1371/journal.pbio.3002316

Riddell, J, Raja Noureen, S, Sedda, L, Glover, JD, Ho, WKW, Bain, CA, Berbeglia, A, Brown, H, Anderson, C, Chen, Y, Crichton, ML, Yates, K, Mort, RL & Headon, DJ 2023, 'Rapid mechanosensitive migration and dispersal of newly divided mesenchymal cells aid their recruitment into dermal condensates', PLOS Biology , vol. 21, no. 9, e3002316. https://doi.org/10.1371/journal.pbio.3002316

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abstract = "Embryonic mesenchymal cells are dispersed within an extracellular matrix but can coalesce to form condensates with key developmental roles. Cells within condensates undergo fate and morphological changes and induce cell fate changes in nearby epithelia to produce structures including hair follicles, feathers, or intestinal villi. Here, by imaging mouse and chicken embryonic skin, we find that mesenchymal cells undergo much of their dispersal in early interphase, in a stereotyped process of displacement driven by 3 h of rapid and persistent migration followed by a long period of low motility. The cell division plane and the elevated migration speed and persistence of newly born mesenchymal cells are mechanosensitive, aligning with tissue tension, and are reliant on active WNT secretion. This behaviour disperses mesenchymal cells and allows daughters of recent divisions to travel long distances to enter dermal condensates, demonstrating an unanticipated effect of cell cycle subphase on core mesenchymal behaviour.",

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Rapid mechanosensitive migration and dispersal of newly divided mesenchymal cells aid their recruitment into dermal condensates

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