Computational modelling of cell chain migration reveals mechanisms that sustain follow-the-leader behaviour

Wynn, Michelle L.; Kulesa, Paul M.; Schnell, Santiago

doi:10.1098/rsif.2011.0726

Cited by 28 publications

(40 citation statements)

References 32 publications

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“…Differences in velocity were observed between leading and trailing cells when co-attraction occurred at every 0.1 s or less (see Figure S6, Video S2b). Leading and trailing behaviour has previously been shown to occur in the chick and Xenopus NC [12], [37], [40]. We suggest that this could emerge in a population of identical cells without requiring differentiation of microscopic parameters, as it has been shown for NC migrating in vitro [12].…”

Section: Resultssupporting

confidence: 61%

Directional Collective Cell Migration Emerges as a Property of Cell Interactions

et al. 2014

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Collective cell migration is a fundamental process, occurring during embryogenesis and cancer metastasis. Neural crest cells exhibit such coordinated migration, where aberrant motion can lead to fatality or dysfunction of the embryo. Migration involves at least two complementary mechanisms: contact inhibition of locomotion (a repulsive interaction corresponding to a directional change of migration upon contact with a reciprocating cell), and co-attraction (a mutual chemoattraction mechanism). Here, we develop and employ a parameterized discrete element model of neural crest cells, to investigate how these mechanisms contribute to long-range directional migration during development. Motion is characterized using a coherence parameter and the time taken to reach, collectively, a target location. The simulated cell group is shown to switch from a diffusive to a persistent state as the response-rate to co-attraction is increased. Furthermore, the model predicts that when co-attraction is inhibited, neural crest cells can migrate into restrictive regions. Indeed, inhibition of co-attraction in vivo and in vitro leads to cell invasion into restrictive areas, confirming the prediction of the model. This suggests that the interplay between the complementary mechanisms may contribute to guidance of the neural crest. We conclude that directional migration is a system property and does not require action of external chemoattractants.

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Section: Resultssupporting

confidence: 61%

Directional Collective Cell Migration Emerges as a Property of Cell Interactions

et al. 2014

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“…Other models try to describe collective migration using agent-based models [25]. A study shown by Mi et al [26] models a healing process using an elastic continuum model.…”

Section: Introductionmentioning

confidence: 99%

Mathematical Modeling of Melanoma Cell Migration with an Elastic Continuum Model for the Evaluation of the Influence of Tumor Necrosis Factor-Alpha on Migration

Gallinaro

Marques

Azevedo

et al. 2013

Journal of Computational Medicine

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An elastic continuum mathematical model was implemented to study collective C8161 melanoma cell migration during a "scratch wound" assay, in control and under the influence of the proinflammatory cytokine tumour necrosis factor-alpha (TNF-). The model has four constants: force that results from lamellipod formation (F), adhesion constant between cells and extracellular matrix (ECM) (b), cell layer elasticity modulus (k), and growth rate ( ). A nonlinear regression routine was used to obtain the parameters of the model with data from an experiment made with C8161 melanoma cells, with and without TNF-. Coefficient of determination for both situations was 2 = 0.89 and 2 = 0.92, respectively. The parameters values obtained were similar to the ones found in the literature. However, the adhesion constant value decreased with the introduction of TNF-, which is not in accordance with expected since the presence of TNF-is associated with an increased expression of integrins that would promote an enhanced adhesion among cells. The model was used in a study relating to the adhesion constant and cell migration, and the results suggested that cell migration decreases with higher adhesion, which is also not in accordance with expected. These differences would not occur if it was considered that TNF-increases the elasticity modulus of the cell layer.

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“…In this paradigm, ‘leader’ cells of NC migratory streams interpret signals from the microenvironment and chart the course for ‘follower’ cells (Wynn et al, 2013, 2012). However, identifying these leader cells genetically has been challenging, perhaps in part due to a dynamic identity and/or shifting population.…”

Section: Migratory Mechanisms and Communicationmentioning

confidence: 99%

“…Several models have been put forward to explain the underlying mechanisms for NC migratory guidance, including leader-follower models (Wynn et al, 2013, 2012), chase-and-run (Theveneau et al, 2013), and contact inhibition of locomotion (CIL) (Carmona-Fontaine et al, 2008). While it is established that NCCs use guidance cues and the local extracellular matrix (ECM) to collectively migrate (Banerjee et al, 2013; McLennan et al, 2010), we lack a thorough mechanistic understanding of NCC collective migration and how it varies between subpopulations of NCCs destined for different locations and fates.…”

Section: Introductionmentioning

confidence: 99%

Neural crest and cancer: Divergent travelers on similar paths

Gallik

Treffy

Nacke

et al. 2017

Mechanisms of Development

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Neural crest cells are multipotent progenitors that dynamically interpret diverse microenvironments to migrate significant distances as a loosely associated collective and contribute to many tissues in the developing vertebrate embryo. Uncovering details of neural crest migration has helped to inform a general understanding of collective cell migration, including that which occurs during cancer metastasis. Here, we discuss several commonalities and differences of neural crest and cancer cell migration and behavior. First, we focus on some of the molecular pathways required for the initial specification and potency of neural crest cells and the roles of many of these pathways in cancer progression. We also describe epithelial-to-mesenchymal transition, which plays a critical role in initiating both neural crest migration and cancer metastasis. Finally, we evaluate studies that demonstrate myriad forms of cell-cell and cell-environment communication during neural crest and cancer collective migration to highlight the remarkable similarities in their molecular and cell biological regulation.

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Computational modelling of cell chain migration reveals mechanisms that sustain follow-the-leader behaviour

Cited by 28 publications

References 32 publications

Directional Collective Cell Migration Emerges as a Property of Cell Interactions

Directional Collective Cell Migration Emerges as a Property of Cell Interactions

Mathematical Modeling of Melanoma Cell Migration with an Elastic Continuum Model for the Evaluation of the Influence of Tumor Necrosis Factor-Alpha on Migration

Neural crest and cancer: Divergent travelers on similar paths

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