Confinement-induced transition between wave-like 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:10.1101/495747

Cited by 5 publications

(13 citation statements)

References 28 publications

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“…Pulsations and flows in tissues are striking examples of collective motions. Although pulsations and flows have independently been studied earlier in MDCK monolayers [25,26,[33][34][35][36][37][38][39], in this paper, we generated both types of multi-cellular dynamics in the same epithelial monolayers. We controlled each of them by spatially modulating substrate friction and by introducing in and then washing-out cytoskeletal inhibitors.…”

Section: Discussionmentioning

confidence: 99%

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: Discussionmentioning

confidence: 99%

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

Thiagarajan

Bhat

Salbreux

et al. 2020

Preprint

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“…The stability and origin of the oscillatory deformation of cells is now under intensive investigation [24,20]. Although experimentalists have detected and measured delays between the concentration of motor proteins (myosin or cadherin) [7], the relation between these oscillations and eventual drastic tissue deformations remains elusive.…”

Section: Discussionmentioning

confidence: 99%

“…This corresponds to reducing the dynamics to solely mode v 3 in (20). Also, due to the equilibrium condition in (15), and when λ 0 = 0, the displacement u(t) ≡ 0.…”

Section: Solution Of Linear Dde Systemmentioning

confidence: 99%

“…These oscillations have been associated with the coupling between the chemical and mechanical signalling [19,11], or the relation between cell polarity and force transmission [18,21], with a potential dependence on the confinement [20]. More recently, it has been observed that the relocation of actomyosin components from medial to junctional areas of the cell may trigger these pulsatile response, suggesting that this biochemical delay between motor molecules is responsible of the observed oscillations [26].…”

Section: Introductionmentioning

confidence: 99%

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Effects of time delays and viscoelastic parameters in oscillatory response of cell monolayers

Borja

Moral

Romero

2021

Viscoelasticity and Collective Cell Migration

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Oscillatory response of cellular tissues has been observed in multiple embryogenetic developmental stages. The source of these oscillations has been attributed to imbalance of instabilities in the chemo-mechanical signalling and delayed cell activity. Although the relation of these oscillations with further drastic tissue deformation remains uncertain, it is apparent that intracellular remodelling events seem to drive the viscoelastic properties and the measured pulsatile deformations.We here resort to a viscoelastic model that is based on a variable restlength of the cell. We include a delay between the measured elastic strain and the evolution of the rest-length which dynamically adapts to the cell strain. This law is not only able to reproduce the relaxation phenomena observed in embryonic tissues in vitro and in vivo, but also to give rise to oscillatory cell responses. We analyse the stability of the resulting oscillations on minimal systems with two cells, and also on planar or out of plane deformation modes of monolayers. We conclude that in all cases, the stability decreases with an increasing delay or with the ability to adapt in a faster manner.

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“…Oscillatory cell deformations are ubiquitous and have been quantified in vitro (Petrolli et al 2019;Peyret et al 2019) and in vivo, for instance in the segmented clock of mice (Yoshioka-Kobayashi et al 2020), during Drosophila fly dorsal closure (Solon et al 2009), cell intercalation in morphogenesis (Tao et al 2019), or wound healing (Roldán et al 2019). During apical constriction tissue oscillations have been associated with oscillatory calcium levels (Christodoulou and Skourides 2015;Suzuki et al 2017), and in Kaouri et al (2019) a mechanism of two-way coupling between these two types of oscillations was proposed.…”

Section: Introductionmentioning

confidence: 99%

Stability bounds of a delay visco-elastic rheological model with substrate friction

Dawi

Muñoz

2021

J. Math. Biol.

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Cells and tissues exhibit sustained oscillatory deformations during remodelling, migration or embryogenesis. Although it has been shown that these oscillations correlate with intracellular biochemical signalling, the role of these oscillations is as yet unclear, and whether they may trigger drastic cell reorganisation events or instabilities remains unknown. Here, we present a rheological model that incorporates elastic, viscous and frictional components, and that is able to generate oscillatory response through a delay adaptive process of the rest-length. We analyse its stability as a function of the model parameters and deduce analytical bounds of the stable domain. While increasing values of the delay and remodelling rate render the model unstable, we also show that increasing friction with the substrate destabilises the oscillatory response. This fact was unexpected and still needs to be verified experimentally. Furthermore, we numerically verify that the extension of the model with non-linear deformation measures is able to generate sustained oscillations converging towards a limit cycle. We interpret this sustained regime in terms of non-linear time varying stiffness parameters that alternate between stable and unstable regions of the linear model. We also note that this limit cycle is not present in the linear model. We study the phase diagram and the bifurcations of the non-linear model, based on our conclusions on the linear one. Such dynamic analysis of the delay visco-elastic model in the presence of friction is absent in the literature for both linear and non-linear rheologies. Our work also shows how

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Confinement-induced transition between wave-like collective cell migration modes

Cited by 5 publications

References 28 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

Effects of time delays and viscoelastic parameters in oscillatory response of cell monolayers

Stability bounds of a delay visco-elastic rheological model with substrate friction

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