Buckling of epithelium growing under spherical confinement

Trushko, Anastasiya; Meglio, Ilaria Di; Merzouki, Aziza; Blanch-Mercader, Carles; Guck, Jochen; Alessandri, Kévin; Nassoy, Pierre; Kruse, Karsten; Chopard, Bastien; Roux, Aurélien

doi:10.1101/513119

Cited by 25 publications

(41 citation statements)

References 38 publications

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“…Thus, the work transferred to the tissue via the cantilever displacement is equal to the sum of the variation of bending energy of the curl and stretching energy of the bulk (see details in Appendix 1). This allowed us to estimate a bending modulus of the tissue: B = (3.7 ± 0.4).10 −13 N.m, close to that predicted by the classical Kirchhoff-Love model of thin plate: B K L = (2.1 ± 0.2).10 −13 N.m and consistent with a recent estimate extracted from buckling of MDCK monolayers due to tissue-growth in long time-scale experiments (28).…”

Section: Characterisation Of Active Torques and The Bending Modulussupporting

confidence: 88%

Curling of epithelial monolayers reveals coupling between active bending and tissue tension

Fouchard

Wyatt

Proag

et al. 2019

Preprint

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Epithelial monolayers are two-dimensional cell sheets which compartmentalise the body and organs of multi-cellular organisms. Their morphogenesis during development or pathology results from patterned endogenous and exogenous forces and their interplay with tissue mechanical properties. In particular, bending of epithelia is thought to results from active torques generated by the polarization of myosin motors along their apico-basal axis. However, the contribution of these out-of-plane forces to morphogenesis remains challenging to evaluate because of the lack of direct mechanical measurement. Here, we use epithelial curling to characterize the out-of-plane mechan ics of epithelial monolayers. We find that curls of high curvature form spontaneously at the free edge of epithelial monolayers devoid of substrate in vivo and in vitro. Curling originates from an enrichment of myosin in the basal domain that generates an active spontaneous curvature. By measuring the force necessary to flatten curls, we can then estimate the active torques and the bending modulus of the tissue. Finally, we show that the extent of curling is controlled by the interplay between in-plane and out-of-plane stresses in the monolayer. Such mechanical coupling implies an unexpected role for in-plane stresses in shaping epithelia during morphogenesis.

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Section: Characterisation Of Active Torques and The Bending Modulussupporting

confidence: 88%

Curling of epithelial monolayers reveals coupling between active bending and tissue tension

Fouchard

Wyatt

Proag

et al. 2019

Preprint

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“…S1 that ≈ and the equilibrium configuration of a single cell is ≈ √ 0 + , ℎ = 0 / . The stress-free state of the bud is one where the ECM volume exactly matches the equilibrium configuration of the monolayer, so that = √2 0 , so that for larger 0 , the epithelium will be in a tensile configuration, while being compressed for lower 0 , which can trigger monolayer buckling ( Figure S5A) (Trushko et al, 2019). Numerical simulations of the equilibrium configurations of the bud for different 0 and/or different confirmed this.…”

Section: Theoretical Modelingmentioning

confidence: 77%

Extracellular hyaluronate pressure shaped by cellular tethers drives tissue morphogenesis

Munjal

Hannezo

Mitchison

et al. 2020

Preprint

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SummaryHow tissues acquire complex shapes is a fundamental question in biology and regenerative medicine. Zebrafish semicircular canals form from invaginations in the otic epithelium (buds) that extend and fuse to form the hubs of each canal. We find that conventional actomyosin-driven behaviors are not required. Instead, local secretion of hyaluronan, made by the enzymes ugdh and has3, drives canal morphogenesis. Charged hyaluronate polymers osmotically swell with water and generate isotropic extracellular pressure to deform the overlying epithelium into buds. The mechanical anisotropy needed to shape buds into tubes is conferred by a polarized distribution of cellular protrusions, linked between cells, that we term cytocinches. Most work on tissue morphogenesis ascribes actomyosin contractility as the driving force, while the extracellular matrix shapes tissues through differential stiffness. Our work inverts this expectation. Hyaluronate-pressure shaped by anisotropic tissue stiffness may be a widespread mechanism for powering morphological change in organogenesis and tissue engineering.

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“…Folding can also occur through compressive forces within epithelia 9 , forming buckled shapes predicted by mechanical models 10 and produced by several processes: proliferation under externally imposed confinement 11 , differences of proliferation between domains of the same tissue 12,13 , or active contractility of muscles around a growing intestinal epithelium 14 . Thus, mechanical stresses emerging in reaction to external constraints are determinant of epithelium folding.…”

Section: Figurementioning

confidence: 99%

Transient active osmotic swelling of epithelium upon curvature induction

Tomba

Luchnikov

Barberi

et al. 2020

Preprint

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Generation of tissue curvature is essential to morphogenesis. However, how cells adapt to changing curvature is still unknown because tools to dynamically control curvature in vitro are lacking. Here we developed self-rolling substrates to study how flat epithelial cell monolayers adapt to a rapid, anisotropic change of curvature. We show that the primary response is an active and transient osmotic swelling of cells. This cell volume increase is not observed on inducible wrinkled substrates, where concave and convex regions alternate each other over short distances, identifying swelling as a collective response to changes of curvature with persistent sign over large distances. It is triggered by a drop in membrane tension and actin depolymerization, perceived by cells as a hypertonic shock. Osmotic swelling restores tension while actin reorganizes, probably to comply with curvature. Epithelia are thus unique materials that transiently, actively swell while adapting to large curvature induction.

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Buckling of epithelium growing under spherical confinement

Cited by 25 publications

References 38 publications

Curling of epithelial monolayers reveals coupling between active bending and tissue tension

Curling of epithelial monolayers reveals coupling between active bending and tissue tension

Extracellular hyaluronate pressure shaped by cellular tethers drives tissue morphogenesis

Transient active osmotic swelling of epithelium upon curvature induction

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