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  Dynamic heterogeneity influences the leader-follower dynamics during epithelial wound closure

Vishwakarma, M., Thurakkal, B., Spatz, J. P., & Das, T. (2020). Dynamic heterogeneity influences the leader-follower dynamics during epithelial wound closure. Philosophical Transactions of the Royal Society of London, Series B: Biological Sciences, 375(1807): 20190391, pp. 1-10. doi:10.1098/rstb.2019.0391.

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Item Permalink: http://hdl.handle.net/21.11116/0000-0006-C40A-2 Version Permalink: http://hdl.handle.net/21.11116/0000-0006-CEB3-8
Genre: Journal Article

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 Creators:
Vishwakarma, Medhavi1, Author              
Thurakkal, Basil, Author
Spatz, Joachim P.1, 2, Author              
Das, Tamal, Author
Affiliations:
1Cellular Biophysics, Max Planck Institute for Medical Research, Max Planck Society, ou_2364731              
2Biophysical Chemistry, Institute of Physical Chemistry, University of Heidelberg, 69120 Heidelberg, Germany, ou_persistent22              

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Free keywords: cell density; collective cell migration; dynamic heterogeneity; mechanobiology
 Abstract: Cells of epithelial tissue proliferate and pack together to attain an eventual density homeostasis. As the cell density increases, spatial distribution of velocity and force show striking similarity to the dynamic heterogeneity observed elsewhere in dense granular matter. While the physical nature of this heterogeneity is somewhat known in the epithelial cell monolayer, its biological relevance and precise connection to cell density remain elusive. Relevantly, we had demonstrated how large-scale dynamic heterogeneity in the monolayer stress field in the bulk could critically influence the emergence of leader cells at the wound margin during wound closure, but did not connect the observation to the corresponding cell density. In fact, numerous previous reports had essentially associated long-range force and velocity correlation with either cell density or dynamic heterogeneity, without any generalization. Here, we attempted to unify these two parameters under a single framework and explored their consequence on the dynamics of leader cells, which eventually affected the efficacy of collective migration and wound closure. To this end, we first quantified the dynamic heterogeneity by the peak height of four-point susceptibility. Remarkably, this quantity showed a linear relationship with cell density over many experimental samples. We then varied the heterogeneity, by changing cell density, and found this change altered the number of leader cells at the wound margin. At low heterogeneity, wound closure was slower, with decreased persistence, reduced coordination and disruptive leader-follower interactions. Finally, microscopic characterization of cell-substrate adhesions illustrated how heterogeneity influenced orientations of focal adhesions, affecting coordinated cell movements. Together, these results demonstrate the importance of dynamic heterogeneity in epithelial wound healing. This article is part of the theme issue 'Multi-scale analysis and modelling of collective migration in biological systems'.

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Language(s): eng - English
 Dates: 2019-11-062020-07-272020-09-14
 Publication Status: Published in print
 Pages: 10
 Publishing info: -
 Table of Contents: -
 Rev. Type: Peer
 Degree: -

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Title: Philosophical Transactions of the Royal Society of London, Series B: Biological Sciences
Source Genre: Journal
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Publ. Info: London : Royal Society
Pages: - Volume / Issue: 375 (1807) Sequence Number: 20190391 Start / End Page: 1 - 10 Identifier: ISSN: 0962-8436
CoNE: https://pure.mpg.de/cone/journals/resource/963017382021_1