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Tissue size controls patterns of cell proliferation and migration in freely-expanding epithelia

Matthew A. Heinrich, Julienne M. LaChance, View ORCID ProfileTom J. Zajdel, Ricard Alert, Andrej Košmrlj, View ORCID ProfileDaniel J. Cohen
doi: https://doi.org/10.1101/2020.02.28.970418
Matthew A. Heinrich
aDepartment of Mechanical and Aerospace Engineering, Princeton University, Princeton, NJ 08544
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Julienne M. LaChance
aDepartment of Mechanical and Aerospace Engineering, Princeton University, Princeton, NJ 08544
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Tom J. Zajdel
aDepartment of Mechanical and Aerospace Engineering, Princeton University, Princeton, NJ 08544
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Ricard Alert
bLewis-Sigler Institute for Integrative Genomics, Princeton University, Princeton, New Jersey 08544, USA
cPrinceton Center for Theoretical Science, Princeton University, Princeton, New Jersey 08544, USA
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Andrej Košmrlj
aDepartment of Mechanical and Aerospace Engineering, Princeton University, Princeton, NJ 08544
dPrinceton Institute for the Science and Technology of Materials (PRISM), Princeton University, Princeton, New Jersey 08544, USA
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Daniel J. Cohen
aDepartment of Mechanical and Aerospace Engineering, Princeton University, Princeton, NJ 08544
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  • For correspondence: danielcohen@princeton.edu
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Abstract

In the last decade, key advances in our understanding of collective cell migration and tissue growth have been made by studying the expansion of epithelial monolayers in vitro. However, most studies have focused on monolayers of sub-millimetric sizes, and how cell proliferation and migration are coordinated on larger scales remains poorly known. To fill this gap, we measured cell velocity, cell density, and cell-cycle state over 2 days in millimeter-scale freely-expanding monolayers. We find that tissues of different initial sizes exhibit very different spatiotemporal patterns of cell proliferation and collective cell migration in their internal regions. Specifically, within several cell cycles, the core of large tissues becomes very dense, almost quiescent, and ceases cell-cycle progression. In contrast, the core of smaller tissues develops a local minimum of cell density as well as a tissue-spanning vortex. These different dynamics are determined not by the current but by the initial tissue size, indicating that the state of the tissue depends on its history. Despite these marked differences at the internal regions, the edge zone of both large and small tissues displays rapid cell-cycle progression and radially-oriented migration with a steady velocity independent of tissue size. As a result, the overall area expansion rate is dictated by the perimeter-to-area ratio of the tissue. Our findings suggest that cell proliferation and migration are regulated in a collective manner that decouples the internal and edge regions of the tissue, which leads to size- and history-dependent internal patterns in expanding epithelia.

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Posted February 28, 2020.
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Tissue size controls patterns of cell proliferation and migration in freely-expanding epithelia
Matthew A. Heinrich, Julienne M. LaChance, Tom J. Zajdel, Ricard Alert, Andrej Košmrlj, Daniel J. Cohen
bioRxiv 2020.02.28.970418; doi: https://doi.org/10.1101/2020.02.28.970418
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Tissue size controls patterns of cell proliferation and migration in freely-expanding epithelia
Matthew A. Heinrich, Julienne M. LaChance, Tom J. Zajdel, Ricard Alert, Andrej Košmrlj, Daniel J. Cohen
bioRxiv 2020.02.28.970418; doi: https://doi.org/10.1101/2020.02.28.970418

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