Confinement-Induced Transition between Wavelike Collective Cell Migration Modes

Petrolli, Vanni; Goff, Magali Le; Tadrous, Monika; Martens, Kirsten; Allier, Cédric; Mandula, Ondřej; Hervé, Lionel; Henkes, Silke; Sknepnek, Rastko; Boudou, Thomas; Cappello, Giovanni; Balland, Martial

doi:10.1103/physrevlett.122.168101

Cited by 58 publications

(83 citation statements)

References 27 publications

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“…These results go along other studies performed on MDCK epithelial monolayers with a variety of theoretical approaches [8]. For example, various studies reported oscillations in vitro and they characterized them with various metrics yielding about the same length and time scales as ours [14][15][16][17][18][19][20]. Their theoretical approaches were based on Langevin harmonic oscillator, continuum active elastic tissue, phase field active Brownian particles, and Voronoi active Brownian model.…”

Section: Discussionsupporting

confidence: 83%

Pulsations and flows in tissues: two collective dynamics with simple cellular rules

Thiagarajan

Bhat

Salbreux

et al. 2020

Preprint

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Epithelial cells flows are observed both in vivo and in vitro and are essential for morphogenesis. Here, we show that pulsatile flows involving local contraction and expansion of a tissue can arise in vitro in an epithelial monolayer of Madine Darby Canine Kidney (MDCK) cells. The strength of pulsation can be modulated through friction heterogeneity by observing the monolayer dynamics on micro-contact printed fibronectin grids with dimensions matching the length-scale of spontaneous oscillations. We also report pulsations by inducing wound closure in domains of similar size with micro-fabricated pillars. In contrast, strongly coherent flows can be induced by adding and washing out acto-myosin cytoskeleton inhibitors. To gain insight into the associated cellular mechanisms, we fluorescently label actin and myosin. We find that lamellipodia align with the direction of the flow, and tissue-scale myosin gradients arise during pulsations in wound-healing experiments. Pulsations and flows are recapitulated in silico by a vertex model with cell motility and polarisation dynamics. The nature of collective movements depends on the interplay between velocity alignment and random diffusion of cell polarisation. When they are comparable, a significant pulsatile flow emerges, whereas the tissue undergoes long-range flows when alignment dominates. We conjecture that the interplay between lamellipodial motile activity and cell polarization, with a possible additional role for tissue-scale myosin gradients, is at the origin of the pulsatile nature of the collective flow. Altogether, our study reveals that monolayer dynamics is dictated by simple rules of interaction at cellular levels which could be involved in morphogenesis.

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Section: Discussionsupporting

confidence: 83%

Pulsations and flows in tissues: two collective dynamics with simple cellular rules

Thiagarajan

Bhat

Salbreux

et al. 2020

Preprint

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“…There exist numerous physics-based theoretical models that relate force and motion in a cell layer 7,[9][10][11][12][13][14][15][16][17][18][19][20][21][22] . The formulation of those models may differ-for example, models have treated the cell layer as a continuum, a set of points on a lattice, a collection of polygons, or a group of self-propelled particles-but the models often have similar components, namely forces within the cell layer and at the cell-substrate interface balance with a viscous friction caused by cell motion.…”

Section: Background and Summarymentioning

confidence: 99%

“…These confined islands are one of multiple possible geometrical constraints, and the forces and motion may differ from other geometries such as larger cell layers and cell monolayers that are free to migrate outward, as in a wound healing assay. However, confinement has been considered in some theoretical models 7,10,21,22 , making this geometry a reasonable starting point. The data we provide include simultaneous measurements of cell velocities, cell-substrate tractions, and monolayer stresses.…”

Section: Background and Summarymentioning

confidence: 99%

Spatiotemporal force and motion in collective cell migration

2020

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Cells move in collective groups in biological processes such as wound healing, morphogenesis, and cancer metastasis. How active cell forces produce the motion in collective cell migration is still unclear. Many theoretical models have been introduced to elucidate the relationship between the cell's active forces and different observations about the collective motion such as collective swirls, oscillations, and rearrangements. though many models share the common feature of balancing forces in the cell layer, the specific relationships between force and motion vary among the different models, which can lead to different conclusions. Simultaneous experimental measurements of force and motion can aid in testing assumptions and predictions of the theoretical models. Here, we provide time-lapse images of cells in 1 mm circular islands, which are used to compute cell velocities, cell-substrate tractions, and monolayer stresses. Additional data are included from experiments that perturbed cell number density and actomyosin contractility. We expect this data set to be useful to researchers interested in force and motion in collective cell migration.

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“…Due to the complexity of collective behaviors, much effort has gone towards reductionist assays that restrict degrees of freedom and ensemble size to simplify analysis and interpretation. One powerful approach is to confine a tissue within predefined boundaries using micropatterning to create adhesive and non-adhesive regions (6)(7)(8)(9)(10)(11). Such confinement mimics certain in vivo contexts such as constrained tumors as well as aspects of compartmentalization during morphogenesis (12).…”

Section: Introductionmentioning

confidence: 99%

Size-dependent patterns of cell proliferation and migration in freely-expanding epithelia

Heinrich

Alert

LaChance

et al. 2020

Preprint

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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. tissue growth | cell cycle | collective migration | epithelia

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Confinement-Induced Transition between Wavelike Collective Cell Migration Modes

Cited by 58 publications

References 27 publications

Pulsations and flows in tissues: two collective dynamics with simple cellular rules

Pulsations and flows in tissues: two collective dynamics with simple cellular rules

Spatiotemporal force and motion in collective cell migration

Size-dependent patterns of cell proliferation and migration in freely-expanding epithelia

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