The emergence of spontaneous coordinated epithelial rotation on cylindrical curved surfaces

Glentis, Alexandros; Blanch-Mercader, Carles; Balasubramaniam, Lakshmi; Saw, Thuan Beng; D’Alessandro, Joseph; Janel, Sébastien; Douanier, Audrey; Delaval, Benedicte; Lafont, Frank; Lim, Chwee Teck; Delacour, Delphine; Prost, Jacques; Xi, Wang; Ladoux, Benoît

doi:10.1126/sciadv.abn5406

Cited by 21 publications

(10 citation statements)

References 90 publications

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“…Our findings and the generic minimal model of single-cell curvotaxis could also provide insights into the orientation and migration of cells in aggregates such as confluent cell monolayers on curved surfaces [44][45][46][47] . The competitions among cell-cell junction, cortical actin bending, and cell contractility could result in even richer emergent collective behaviors 44 .…”

Section: Implications To Curvotaxis On More Complex Curved Surfacesmentioning

confidence: 70%

Biphasic curvature-dependence of cell migration inside microcylinders: persistent randomness versus directionality

Wang

et al. 2022

Preprint

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Cell-scale curvature plays important roles in controlling cell and tissue behaviors. However, these roles have not been well quantified, and the underlying mechanisms remain elusive. We combine experiments with theory to study systematically the curvature-dependence of cell migration inside PDMS microcylinders. We find that persistence is positively correlated with speed, following the universal speed-persistence coupling relation, i.e., faster cells turn less. Cell migration inside microcylinders is anisotropic and depends on curvature in a biphasic manner. At small curvatures, as curvature increases, the average speed and anisotropy both increase, but surprisingly, the average persistence decreases. Whereas as the curvature increases over some threshold, cells detach from the surface, the average speed and anisotropy both decrease sharply but the average persistence increases. Moreover, interestingly, cells are found to leave paxillins along their trajectories (on curved but not planar surfaces), facilitating the assembly of focal adhesions of following cells. We propose a minimal model for the biphasic curvotaxis based on three mechanisms: the persistent random noise, the bending penalty of stress fibers, and the cell-surface adhesion. The findings provide a novel and general perspective on directed cell migration in the widely existing curved microenvironment of cells in vivo.

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Section: Implications To Curvotaxis On More Complex Curved Surfacesmentioning

confidence: 70%

Biphasic curvature-dependence of cell migration inside microcylinders: persistent randomness versus directionality

Wang

et al. 2022

Preprint

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“…Thus, it is likely that this cell line retains the partial function of AJs. This function may be achieved by another subclass of cadherin (cadherin-6) that is expressed in both the wild-type and the E-cadherin KO cells (T. Otani, personal communication), as shown in other MDCK cell lines (Glentis et al, 2022;Stewart et al, 2000). E-cadherin and cadherin-6 are thought to form different complexes with αand β-catenins and accumulate at cell-cell contacts through independent regulatory mechanisms in MDCK II cells (Stewart et al, 2000).…”

Section: Discussionmentioning

confidence: 99%

“…The Snail 1 overexpressing cells or the αΕ‐catenin KD cells show less coordinated movements (Doxzen et al, 2013; Jain et al, 2020; Seddiki et al, 2018). More recently, the knockout (KO) of E‐cadherin in MDCK cells led to a reduction in the percentage of collective epithelial rotation events, accompanied by a decreased rotation speed in a 3D cylindrical substrate (Glentis et al, 2022). However, how E‐cadherin contributes to the emergence of coordinated cell rotation on a confined 2D matrix remains to be addressed directly.…”

Section: Introductionmentioning

confidence: 99%

E‐cadherin‐dependent coordinated epithelial rotation on a two‐dimensional discoidal pattern

et al. 2022

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In vivo, cells collectively migrate in a variety of developmental and pathological contexts. Coordinated epithelial rotation represents a unique type of collective cell migrations, which has been modeled in vitro under spatially confined conditions. Although it is known that the coordinated rotation depends on intercellular interactions, the contribution of E‐cadherin, a major cell–cell adhesion molecule, has not been directly addressed on two‐dimensional (2D) confined substrates. Here, using well‐controlled fibronectin‐coated surfaces, we tracked and compared the migratory behaviors of MDCK cells expressing or lacking E‐cadherin. We observed that wild‐type MDCK II cells exhibited persistent and coordinated rotations on discoidal patterns, while E‐cadherin knockout cells migrated in a less coordinated manner without large‐scale rotation. Our comparison of the collective dynamics between these two cell types revealed a series of changes in migratory behavior caused by the loss of E‐cadherin, including a decreased global migration speed, less regularity in quantified coordination, and increased average density of topological defects. Taken together, these data demonstrate that spontaneous initiation of collective epithelial rotations depends on E‐cadherin under 2D discoidal confinements.

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“…In many adherent cells, the alignment is found to be determined by the competition between the bending energy of the stress fibers, of the nucleus and the contractile forces [16][17][18]. At the level of cell collectives, both alignment and cell migration within the confluent tissue, is found to be affected by the substrate curvature, experimentally [19][20][21][22][23][24] and in theoretical analysis [25].…”

Section: Introductionmentioning

confidence: 99%

A minimal physical model for curvotaxis driven by curved protein complexes at the cell’s leading edge

Sadhu

Luciano

Wang

et al. 2023

Preprint

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Cells often migrate on curved surfaces inside the body, such as curved tissues, blood vessels or highly curved protrusions of other cells. Recent in-vitro experiments provide clear evidence that motile cells are affected by the curvature of the substrate on which they migrate, preferring certain curvatures to others, termed "curvotaxis". The origin and underlying mechanism that gives rise to this curvature sensitivity are not well understood. Here, we employ a "minimal cell" model which is composed of a vesicle that contains curved membrane protein complexes, that exert protrusive forces on the membrane (representing the pressure due to actin polymerization). This minimal-cell model gives rise to spontaneous emergence of a motile phenotype, driven by a lamellipodia-like leading edge. By systematically screening the behaviour of this model on different types of curved substrates (sinusoidal, cylinder and tube), we show that minimal ingredients and energy terms capture the experimental data. The model recovers the observed migration on the sinusoidal substrate, where cells move along the grooves (minima), while avoiding motion along the ridges. In addition, the model predicts the tendency of cells to migrate circumferentially on convex substrates and axially on concave ones. Both of these predictions are verified experimentally, on several cell types. Altogether, our results identify the minimization of membrane-substrate adhesion energy and binding energy between the membrane protein complexes as key players of curvotaxis in cell migration.

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The emergence of spontaneous coordinated epithelial rotation on cylindrical curved surfaces

Cited by 21 publications

References 90 publications

Biphasic curvature-dependence of cell migration inside microcylinders: persistent randomness versus directionality

Biphasic curvature-dependence of cell migration inside microcylinders: persistent randomness versus directionality

E‐cadherin‐dependent coordinated epithelial rotation on a two‐dimensional discoidal pattern

A minimal physical model for curvotaxis driven by curved protein complexes at the cell’s leading edge

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