Stick-slip dynamics of cell adhesion triggers spontaneous symmetry breaking and directional migration of mesenchymal cells on one-dimensional lines

Hennig, K.; Wang, I.; Moreau, Philippe; Valon, Léo; Beco, Simon de; Coppey, Mathieu; Miroshnikova, Yekaterina A.; Albiges-Rizo, Corinne; Favard, Cyril; Voituriez, Raphaël; Balland, Martial

doi:10.1126/sciadv.aau5670

Cited by 66 publications

(90 citation statements)

References 51 publications

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“…Since the maintenance of front–rear asymmetry is essential for the directional persistence, we conclude that a fibrillar FN in the positive control could favor the spontaneous cell symmetry breaking and cytoskeletal polarization, thus initiating the persistent migration in the polarity direction [ 41 ]. In the absence of any preferential direction, a randomly migrating cell moves alternating fast translocation with slow rotation [ 42 , 43 ], which causes changes in orientation, as seen for the nanopatterns.…”

Section: Discussionmentioning

confidence: 99%

The Janus Role of Adhesion in Chondrogenesis

Casanellas

Lagunas

Vida

et al. 2020

IJMS

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Tackling the first stages of the chondrogenic commitment is essential to drive chondrogenic differentiation to healthy hyaline cartilage and minimize hypertrophy. During chondrogenesis, the extracellular matrix continuously evolves, adapting to the tissue adhesive requirements at each stage. Here, we take advantage of previously developed nanopatterns, in which local surface adhesiveness can be precisely tuned, to investigate its effects on prechondrogenic condensation. Fluorescence live cell imaging, immunostaining, confocal microscopy and PCR analysis are used to follow the condensation process on the nanopatterns. Cell tracking parameters, condensate morphology, cell–cell interactions, mechanotransduction and chondrogenic commitment are evaluated in response to local surface adhesiveness. Results show that only condensates on the nanopatterns of high local surface adhesiveness are stable in culture and able to enter the chondrogenic pathway, thus highlighting the importance of controlling cell–substrate adhesion in the tissue engineering strategies for cartilage repair.

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Section: Discussionmentioning

confidence: 99%

The Janus Role of Adhesion in Chondrogenesis

Casanellas

Lagunas

Vida

et al. 2020

IJMS

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“…To simplify the study of the complex process of cell motility, cells can be confined to move along one-dimensional tracks, either on flat adhesive stripes [9,10], linear grooves [11] and channels [12,13], or thin fiber [14,15]. In addition to being a simple geometry for the study and analysis of the cell motion in general, such confined motion appears also in-vivo [16], for example when cells move along axonal fibers [17,18], or cancer invades in confined spaces between tissues [19].…”

Section: Introductionmentioning

confidence: 99%

“…The experiments listed above have shown that isolated cells on one-dimensional tracks exhibit the following stereotypical behaviors [9,10]: (i) nonmigrating and unpolarized, by remaining quiescent or elongating symmetrically, (ii) undergoing spontaneous symmetry breaking, polarization and migrating smoothly, and (iii) as in (ii) but exhibiting stick-slip migration. The stick-slip motility mode is characterized by protrusive motion at the cell front, coupled with an overall elongation of the cell and followed by rapid retraction of the cell back.…”

Section: Introductionmentioning

confidence: 99%

One-dimensional cell motility patterns

Ron

Monzo

Gauthier

et al. 2020

Phys. Rev. Research

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During migration, cells exhibit a rich variety of seemingly random migration patterns, which makes unraveling the underlying mechanisms that control cell migration a difficult challenge. For efficient migration, cells require a mechanism for polarization, so that traction forces are produced in the direction of motion, while adhesion is released to allow forward migration. To simplify the study of this process, cells have been studied when placed along one-dimensional tracks, where single cells exhibit both smooth and stick-slip migration modes. The stick-slip motility mode is characterized by protrusive motion at the cell front, coupled with a slow elongation of the cell, which is followed by a rapid retraction of the cell rear. In this study, we explore a minimal physical model that couples the force applied on the adhesion bonds to the length variations of the cell and to the traction forces applied by the polarized actin retrograde flow. We show that the rich spectrum of cell migration patterns emerges from this model as different deterministic dynamical phases. This result suggests a source for the large cell-tocell variability (CCV) in cell migration patterns observed in single cells over time and within cell populations: fluctuations in the cellular components, such as adhesion strength or polymerization activity, can shift the cells from one migration mode to another, due to crossing the dynamical phase transition lines. Temporal noise is shown to drive random changes in the cellular polarization direction, which is enhanced during the stick-slip migration mode. The model contains an emergent critical length for cell polarization, whereby cells that retract below this length loose polarity, and are prone to making direction changes in migration. These results offer a new framework to explain experimental observations of migrating cells, resulting from noisy switching between underlying deterministic migration modes.

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“…On the other hand, the symmetrical distribution of adhesive contacts can keep cells in the non-polarized state [ 40 , 41 ]. Local inhibition of adhesive contacts on one side of non-polarized cells then leads to the formation of the cell rear at this region and induces migration in the opposite direction [ 41 , 42 ]. Since the reorganization of the actin cytoskeleton is linked to focal adhesions, focal adhesions thus may be a key factor in cell spontaneous polarization.…”

Section: Introductionmentioning

confidence: 99%

Quantitative Phase Imaging of Spreading Fibroblasts Identifies the Role of Focal Adhesion Kinase in the Stabilization of the Cell Rear

et al. 2020

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Cells attaching to the extracellular matrix spontaneously acquire front–rear polarity. This self-organization process comprises spatial activation of polarity signaling networks and the establishment of a protruding cell front and a non-protruding cell rear. Cell polarization also involves the reorganization of cell mass, notably the nucleus that is positioned at the cell rear. It remains unclear, however, how these processes are regulated. Here, using coherence-controlled holographic microscopy (CCHM) for non-invasive live-cell quantitative phase imaging (QPI), we examined the role of the focal adhesion kinase (FAK) and its interacting partner Rack1 in dry mass distribution in spreading Rat2 fibroblasts. We found that FAK-depleted cells adopt an elongated, bipolar phenotype with a high central body mass that gradually decreases toward the ends of the elongated processes. Further characterization of spreading cells showed that FAK-depleted cells are incapable of forming a stable rear; rather, they form two distally positioned protruding regions. Continuous protrusions at opposite sides results in an elongated cell shape. In contrast, Rack1-depleted cells are round and large with the cell mass sharply dropping from the nuclear area towards the basal side. We propose that FAK and Rack1 act differently yet coordinately to establish front–rear polarity in spreading cells.

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Stick-slip dynamics of cell adhesion triggers spontaneous symmetry breaking and directional migration of mesenchymal cells on one-dimensional lines

Abstract: Cell motility can be initiated without prior cytoskeleton polarity by the stochastic stick-slip dynamics of cell adhesions.

Cited by 66 publications

References 51 publications

The Janus Role of Adhesion in Chondrogenesis

The Janus Role of Adhesion in Chondrogenesis

One-dimensional cell motility patterns

Quantitative Phase Imaging of Spreading Fibroblasts Identifies the Role of Focal Adhesion Kinase in the Stabilization of the Cell Rear

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