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Chase-and-run between adjacent cell populations promotes directional collective migration

Nature Cell Biology volume 15, pages 763–772 (2013)Cite this article

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Abstract

Collective cell migration in morphogenesis and cancer progression often involves the coordination of multiple cell types. How reciprocal interactions between adjacent cell populations lead to new emergent behaviours remains unknown. Here we studied the interaction between neural crest (NC) cells, a highly migratory cell population, and placodal cells, an epithelial tissue that contributes to sensory organs. We found that NC cells chase placodal cells by chemotaxis, and placodal cells run when contacted by NC. Chemotaxis to Sdf1 underlies the chase, and repulsion involving PCP and N-cadherin signalling is responsible for the run. This chase-and-run requires the generation of asymmetric forces, which depend on local inhibition of focal adhesions. The cell interactions described here are essential for correct NC migration and for segregation of placodes in vivo and are likely to represent a general mechanism of coordinated migration.

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Figure 1: NC cell migration triggers directional movement of placodal cells.
Figure 2: Chase-and-run: NC and placodes undergo Sdf1-dependent coordinated collective migration.
Figure 3: NC and placodes form transient, but functional, adherens junctions.
Figure 4: NC–placodal interaction leads to asymmetric traction forces and inhibition of focal adhesions.
Figure 5: N-cadherin-dependent contacts lead to cell protrusion instability.
Figure 6: Coordinated migration of NC and placodal cells requires CIL.
Figure 7: Interaction between NC and placodes through CIL and chemotaxis is required for placode and NC migration in vivo.
Figure 8: CIL and chemotaxis between NC and placodal cells drives coordinated migration of both cell populations.

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Acknowledgements

We thank L. Marchant for the experiments shown in Supplementary Fig. S2h–i. We are grateful to N. David (Ecole Normale Superieure, Paris, France) for the zebrafish Sdf1 MO and to G. Schlosser (Martin Ryan Institute, NUI Galway, Ireland) for the Xenopus Eya1 MO. We thank G. Schlosser, C. Stern, B. Stramer, L. Cramer, B. Baum, M. Tada and all members of the laboratory of R.M. for comments on the manuscript. This study was supported by grants from the MRC MR/J000655/1 and BBSRC to R.M., from the Wellcome Trust to A.S. and R.M., from the Spanish Ministry for Economy and Competitiveness (BFU2012-38146 and BFU2009-07595), and the European Research Council (Grant Agreement 242993) to X.T. and the Wellcome Trust Value in People Award to E.T.; E.S. is the recipient of a Wellcome Trust PhD fellowship.

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Author notes

  1. Benjamin Steventon

    Present address: Present address: Institut Pasteur, 75724 Paris cedex 15, France,

Authors and Affiliations

  1. Department of Cell and Developmental Biology, University College London, London WC1E 6BT, UK

    Eric Theveneau, Benjamin Steventon, Elena Scarpa, Simon Garcia & Roberto Mayor

  2. Craniofacial Development and Stem Cell Biology, King’s College London, London SE1 9RT, UK

    Benjamin Steventon & Andrea Streit

  3. Institut de Bioenginyeria de Catalunya (IBEC), ICREA, and Facultat de Medicina—Universitat de Barcelona, 08028 Barcelona, Spain

    Simon Garcia & Xavier Trepat

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Contributions

Experiments were designed by E.T., B.S. and R.M., with the participation of X.T and A.S. All experiments were performed in the laboratory of R.M. E.T and B.S. performed most of the experiments. E.S. performed the repolarization and clustering assays. S.G., E.T. and X.T. performed the traction force experiments. E.T., B.S. and R.M. analysed and interpreted data, with the participation of X.T. and A.S. E.T., B.S., A.S. and R.M. wrote the manuscript. All authors commented on the manuscript.

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Correspondence to Roberto Mayor.

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Supplementary information

Supplementary Information

Supplementary Information (PDF 1100 kb)

In vivo cell migration of neural crest and placodal cells after a double graft.

Neural crest cells are in green and placodal cells in red. Note that a gap is generated in the placodal region where neural crest cells are migrating, as marked by red dots. Green arrow corresponds to ventral limit of the migrating neural crest. 1 picture every 5 min; ×10 lens; 5 h. (MOV 7842 kb)

In vivo cell migration of neural crest and placodal cells.

Panel 1: Placodes from the third epibranchial domain located posterior to the third neural crest stream. Panel 2: Neural crest cells from the third neural crest stream. Panel 3: Neural crest cells from the second neural crest stream. Panel 4: Placodes from the first epibranchial domain located ventral and anterior to the second neural crest stream. Note that placodes move away from the migratory neural crest cells but that the actual direction of their movement depends on the relative position of placodes and neural crest cells. Diagrams at the top indicate which regions are monitored. Blue squares mark the NC streams whereas yellow squares indicate the placodes. 1 picture every 5 min; ×10 lens; 1 h 30 min. (MOV 4397 kb)

In vivo placodal cell migration. Placodal cells express nuclear RFP.

Time-lapse movie of the placodal region depicted in Supplementary Fig. S1i–k. Left panel: Placodal cells in a control embryo before neural crest cell migration. Middle panel: Placodal cell movements during neural crest cell migration. Right panel: Placodes in an embryo where neural crest cells were removed. Note that directionality is observed only in the control situation (middle panel) in cells that are located to a gap (second neural crest stream, green circle). 1 picture every 5 min; ×10 lens; 3 h. (MOV 6250 kb)

Chase-and-run: co-culture of neural crest cells and placodes.

First row: Control neural crest cells. Second row: Control placodal cells. Third row: Co-culture of neural crest (green) and placodes (red). Note that neural crest and placodes undergo coordinated cell migration (chase-and-run). Fourth row: Co-culture of Cxcr4MO neural crest (green) and placodes (red). Note that inhibiting Sdf1 chemotaxis impairs the coordinated migration. 1 picture every 5 min; 5 h. (MOV 8761 kb)

Attraction assay.

Control neural crest cells and control placodes (left), Cxcr4MO neural crest cells and control placodes (middle), and control neural crest cells and Sdf1MO placodes (right). Note that control placodal cells endogenously express Sdf1. Lower panels show the automated tracks for neural crest cells for each condition. 1 picture every 5 min; 5 h. (MOV 8499 kb)

Invasion assay.

Control neural crest cells are co-cultured with control non-placodal ectoderm from stage 10 Xenopus embryo (left panel) or control placodes (right panel). Both tissues endogenously express Sdf1. Note that neural crest cells invade the ectoderm and do not undergo coordinated migration. White cross marks the centre of the placode explants at the beginning of the video for reference. 1 picture every 5 min; 5 h. (MOV 4983 kb)

Cell–cell interaction at the neural-crest–placodes interface.

This video shows two examples of the dynamic interactions of neural crest and placode cells at the interface. Left panel: neural crest (green) migrates towards placodes (red) making numerous transient contacts. Note that neural crest cells are far more active and migratory than placodes in accordance with their respective mesenchymal (neural crest) and epithelial (placodes) phenotypes. 1 picture every 30 s; ×10 objective; 1 h 45 mins. Right panel: neural crest (green) and placodes (red) go through a cycle of protrusion, contact and retraction. Note that neural crest cells are more readily reforming cell protrusions than placodes. 1 picture every 10 s; ×40 objective; 35mins. Both examples show how repeated contacts between neural crest cells progressively force placodes to retreat. (MOV 9585 kb)

Transient accumulation of N-cadherin-GFP between neural crest and placodes.

Both neural crest and placodes were transfected with N-cadherin-GFP. Placodes were also injected with nuclear mCherry. Top panel shows the merged green (N-cadherin) and red (nuclear mCherry) fluorescent channels. Middle panels show the green channel only. Bottom panels show the heat maps of the green channel. Regions of cell–cell contact are highlighted with a white square. Frames are from a single confocal zplan extracted from a stack. ×63 objective, digital zoom ×2; 1 picture every 15 s; 6 mins. (MOV 6761 kb)

Placodal cells protrusion dynamics.

Spinning disk confocal microscopy. Both cell types were injected with LifeActin-mCherry. Neural crest cells were co-injected with membrane GFP. Left panel, placodal cells alone; right panel, interface between neural crest and placodes explants. Asterisks mark the collapsing protrusions. ×100 lens; 1 picture per minute; 30min. (MOV 5457 kb)

N-Cadherin affects Placodal cell protrusions.

Panel 1: Placodal cells cultured on fibronectin. Panel 2: Placodal cells on FN+1 μg ml−1 of N-cadherin. Panel 3: Placodal cells on FN+3 μg ml−1 of N-cadherin. Panel 4: Placodal cells on FN+3 μg ml−1 of N-cadherin in low calcium/magnesium conditions. Panel 5: Placodal cells on FN+3 μg ml−1 of N-cadherin with placodal cells pre-incubated in blocking antibody against N-cadherin (NCD2). ×10 lens, digital zoom ×2; 1 picture every 3 min; 1h. (MOV 7023 kb)

Heterotypic collisions between control neural crest cells and control placodal cells.

Left panel: Single neural crest cell versus a placode explant. Middle panel: Single placodal cell versus a neural crest explant. Right panel: Single placodal cells colliding. Note that collisions between neural crest and placodal cells lead to contact-inhibition of locomotion with cells moving away from each other, whereas collisions between placodal cells lead to cell clustering. 1 picture every 3 min; ×10 lens; 30mins. (MOV 7141 kb)

Homotypic collisions between neural crest or placodes.

Top panel: Collisions between neural crest cells. Bottom panel: Collisions between placodes. Consecutive frames were subtracted and colour-coded such that protrusions and retraction appear red and blue respectively. Cell bodies are green. Note that cells collapse protrusions and repolarize following contact with one another, making new protrusions opposite to the region cell–cell contact. Neural crest cells subsequently move away from each other, whereas placodes cluster. 1 picture every 3 min; ×10 lens; 36min. (MOV 3834 kb)

Heterotypic collisions between neural crest and placodal cells following inhibition of N-cadherin, Dishevelled and dnWnt11.

Panel 1: Control cells. Panel 2: Both cell types injected with N-cadherin morpholino. Panel 3: Both cell types expressing Dishevelled dominant-negative (DshDep+). Panel 4: Control placodes (red) and neural crest cells expressing dominant-negative Wnt11 (dnWnt11, green). Note that control NC and placodal cells move away from each other. When N-cadherin, Dsh or dnWnt11 are inhibited, neural crest and placodal cells remain in contact after collision. 1 picture every 5 min; ×10 lens; 30min. (MOV 2686 kb)

Invasion assay with neural crest and placodal cells.

Panel 1: Control cells. Panel 2: Both cell types injected with DshDep+. Panel 3: Placodal explants treated with N-cadherin antibody (NCD2). Panel 4: Placodal explants treated with E-cadherin antibody. Note that control conditions and E-cadherin-treated explants show a clear chase-and-run behaviour, whereas Dsh and N-cadherin inhibition lead to overlapping of both explants and no directional movement of the placodal cells. 1 picture every 5 min; ×10 lens; 5h. (MOV 4854 kb)

Co-culture of neural crest explants.

Left panel: Control neural crest cells alone. Middle panel: Two control neural crest explants. Right panel: A control neural crest explant (red, nuclear mCherry) is co-cultured next to a neural crest explant injected with Sdf1 (green, cytoplasmic fluorescein dextran). Note that overexpressing Sdf1 in one neural crest explant is sufficient to drive a coordinated migration of the two explants. 1 picture every 3 min; ×10 lens; 4h. (MOV 2213 kb)

In vivo placodal cell migration.

Left panel: Control conditions Middle and right panels: Placodal cells expressing Dishevelled dominant negative (DshDep+). Note that coordinated movements can be seen in DshDep+ conditions compared with the control placodes (left). 1 picture every 5 min; ×10 lens; 3 h. (MOV 1944 kb)

3D reconstruction of Sox3 in situ hybridization in zebrafish injected with a control MO or Sdf1 MO.

Note that after blocking neural crest cell migration with Sdf1 MO (right panel), placodal cells remain organized as one domain instead of splitting into subgroups (control embryo, left panel). (MOV 2969 kb)

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Theveneau, E., Steventon, B., Scarpa, E. et al. Chase-and-run between adjacent cell populations promotes directional collective migration. Nat Cell Biol 15, 763–772 (2013). https://doi.org/10.1038/ncb2772

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