In vivo collective cell migration requires an LPAR2-dependent increase in tissue fluidity

Kuriyama, Sei; Théveneau, Eric; Benedetto, Alexandre; Parsons, Maddy; Tanaka, Masamitsu; Charras, Guillaume; Kabla, Alexandre; Mayor, Roberto

doi:10.1083/jcb.201402093

Cited by 127 publications

(143 citation statements)

References 67 publications

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“…Another solution to reducing the influence of viscous drag was recently described for cranial neural crest cells, which migrate collectively as a large group. Instead of splitting into small clusters, these cells reduce the strength of cell-cell adhesions so that they can move in a more fluid-like manner (41). Note that we find that chemotactic migration in 3D mimics the kinematic behavior of objects falling under gravity or bubbles rising through a confined column of viscous medium.…”

Section: Discussionmentioning

confidence: 71%

Modeling and analysis of collective cell migration in an in vivo three-dimensional environment

Cai

Dai

Prasad

et al. 2016

Proc. Natl. Acad. Sci. U.S.A.

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A long-standing question in collective cell migration has been what might be the relative advantage of forming a cluster over migrating individually. Does an increase in the size of a collectively migrating group of cells enable them to sample the chemical gradient over a greater distance because the difference between front and rear of a cluster would be greater than for single cells? We combined theoretical modeling with experiments to study collective migration of the border cells in-between nurse cells in the Drosophila egg chamber. We discovered that cluster size is positively correlated with migration speed, up to a particular point above which speed plummets. This may be due to the effect of viscous drag from surrounding nurse cells together with confinement of all of the cells within a stiff extracellular matrix. The model predicts no relationship between cluster size and velocity for cells moving on a flat surface, in contrast to movement within a 3D environment. Our analyses also suggest that the overall chemoattractant profile in the egg chamber is likely to be exponential, with the highest concentration in the oocyte. These findings provide insights into collective chemotaxis by combining theoretical modeling with experimentation.cell migration | theoretical modeling | three-dimensional | chemotaxis

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Section: Discussionmentioning

confidence: 71%

Modeling and analysis of collective cell migration in an in vivo three-dimensional environment

Cai

Dai

Prasad

et al. 2016

Proc. Natl. Acad. Sci. U.S.A.

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“…Cell-cell adhesions after NC delamination are maintained usually by type II classical cadherins (Kuriyama et al, 2014;Theveneau et al, 2010). …”

Section: Epidermal-to-mesenchymal Transition (Emt)-basic Conceptmentioning

confidence: 99%

Controlled levels of canonical Wnt signaling are required for neural crest migration

Maj

Künneke

Loresch

et al. 2016

Developmental Biology

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“…Thus, although neural crest shows all the hallmarks of mesenchymal cells, they obviously form transient AJs (Scarpa et al 2015). The endocytosis of N-cadherin at the AJs is essential for neural crest migration in vivo, as it confers sufficient fluidity on the cell cluster for it to migrate under physical constrains (Kuriyama et al 2014). This increase in tissue fluidity allows a dynamic exchange of neighbors while retaining cell -cell interaction.…”

Section: Tissue Morphogenesis and Regenerationmentioning

confidence: 99%

Tuning Collective Cell Migration by Cell–Cell Junction Regulation

Friedl

Mayor

2017

Cold Spring Harb Perspect Biol

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281

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Collective cell migration critically depends on cell -cell interactions coupled to a dynamic actin cytoskeleton. Important cell-cell adhesion receptor systems implicated in controlling collective movements include cadherins, immunoglobulin superfamily members (L1CAM, NCAM, ALCAM), Ephrin/Eph receptors, Slit/Robo, connexins and integrins, and an adaptive array of intracellular adapter and signaling proteins. Depending on molecular composition and signaling context, cell -cell junctions adapt their shape and stability, and this gradual junction plasticity enables different types of collective cell movements such as epithelial sheet and cluster migration, branching morphogenesis and sprouting, collective network migration, as well as coordinated individual-cell migration and streaming. Thereby, plasticity of cell -cell junction composition and turnover defines the type of collective movements in epithelial, mesenchymal, neuronal, and immune cells, and defines migration coordination, anchorage, and cell dissociation. We here review cell -cell adhesion systems and their functions in different types of collective cell migration as key regulators of collective plasticity.

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In vivo collective cell migration requires an LPAR2-dependent increase in tissue fluidity

Abstract: Neural crest epithelial–mesenchymal transition (EMT) and collective cell migration rely on a solid-to-liquid-like transition triggered by internalization of N-cadherin downstream of lysophosphatidic acid receptor 2.

Cited by 127 publications

References 67 publications

Modeling and analysis of collective cell migration in an in vivo three-dimensional environment

Modeling and analysis of collective cell migration in an in vivo three-dimensional environment

Controlled levels of canonical Wnt signaling are required for neural crest migration

Tuning Collective Cell Migration by Cell–Cell Junction Regulation

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