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Actomyosin controls planarity and folding of epithelia in response to compression.

Accepted version
Peer-reviewed

Type

Article

Change log

Authors

Wyatt, Tom PJ 
Fouchard, Jonathan 
Lisica, Ana 
Khalilgharibi, Nargess 

Abstract

Throughout embryonic development and adult life, epithelia are subjected to compressive deformations. While these have been shown to trigger mechanosensitive responses such as cell extrusion and differentiation, which span tens of minutes, little is known about how epithelia adapt to compression over shorter timescales. Here, using suspended epithelia, we uncover the immediate response of epithelial tissues to the application of in-plane compressive strains (5-80%). We show that fast compression induces tissue buckling followed by actomyosin-dependent tissue flattening that erases the buckle within tens of seconds, in both mono- and multi-layered epithelia. Strikingly, we identify a well-defined limit to this response, so that stable folds form in the tissue when compressive strains exceed a 'buckling threshold' of ~35%. A combination of experiment and modelling shows that this behaviour is orchestrated by adaptation of the actomyosin cytoskeleton as it re-establishes tissue tension following compression. Thus, tissue pre-tension allows epithelia to both buffer against deformation and sets their ability to form and retain folds during morphogenesis.

Description

Keywords

Actomyosin, Animals, Cadherins, Compressive Strength, Cytoskeleton, Dogs, Elasticity, Epithelial Cells, Epithelium, Green Fluorescent Proteins, Madin Darby Canine Kidney Cells, Microscopy, Confocal, Models, Biological, Morphogenesis, Stress, Mechanical, Viscosity

Journal Title

Nat Mater

Conference Name

Journal ISSN

1476-1122
1476-4660

Volume Title

19

Publisher

Springer Science and Business Media LLC

Rights

All rights reserved
Sponsorship
Biotechnology and Biological Sciences Research Council (BB/M002578/1)
Biotechnology and Biological Sciences Research Council (BB/K013696/1)
T.P.J.W. and N.K. were part of the EPSRC funded doctoral training programme CoMPLEX. J.F. and P.R. were funded by BBSRC grants (nos. BB/M003280 and BB/M002578) to G.T.C. and A.J.K. N.K. was funded by the Rosetrees Trust and the UCL Graduate School through a UCL Overseas Research Scholarship. A.L. was supported by an EMBO long-term post-doctoral fellowship. B.B. was supported by UCL, a BBSRC project grant (no. BB/K009001/1) and a CRUK programme grant (no. 17343). T.P.J.W., J.F., N.K., A.L. and G.T.C. were supported by a consolidator grant from the European Research Council to G.T.C. (MolCellTissMech, agreement no. 647186).
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