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Neural crest streaming as an emergent property of tissue interactions during morphogenesis

Szabó, A; Theveneau, E; Turan, M; Mayor, R; (2019) Neural crest streaming as an emergent property of tissue interactions during morphogenesis. PLoS Computational Biology , 15 (4) , Article e1007002. 10.1371/journal.pcbi.1007002. Green open access

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Abstract

A fundamental question in embryo morphogenesis is how a complex pattern is established in seemingly uniform tissues. During vertebrate development, neural crest cells differentiate as a continuous mass of tissue along the neural tube and subsequently split into spatially distinct migratory streams to invade the rest of the embryo. How these streams are established is not well understood. Inhibitory signals surrounding the migratory streams led to the idea that position and size of streams are determined by a pre-pattern of such signals. While clear evidence for a pre-pattern in the cranial region is still lacking, all computational models of neural crest migration published so far have assumed a pre-pattern of negative signals that channel the neural crest into streams. Here we test the hypothesis that instead of following a pre-existing pattern, the cranial neural crest creates their own migratory pathway by interacting with the surrounding tissue. By combining theoretical modeling with experimentation, we show that streams emerge from the interaction of the hindbrain neural crest and the neighboring epibranchial placodal tissues, without the need for a pre-existing guidance cue. Our model suggests that the initial collective neural crest invasion is based on shortrange repulsion and asymmetric attraction between neighboring tissues. The model provides a coherent explanation for the formation of cranial neural crest streams in concert with previously reported findings and our new in vivo observations. Our results point to a general mechanism of inducing collective invasion patterns.

Type: Article
Title: Neural crest streaming as an emergent property of tissue interactions during morphogenesis
Location: United States
Open access status: An open access version is available from UCL Discovery
DOI: 10.1371/journal.pcbi.1007002
Publisher version: https://doi.org/10.1371/journal.pcbi.1007002
Language: English
Additional information: This is an open access article distributed under the terms of the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited. https://creativecommons.org/licenses/by/4.0/
UCL classification: UCL > Provost and Vice Provost Offices
UCL > Provost and Vice Provost Offices > School of Life and Medical Sciences
UCL > Provost and Vice Provost Offices > School of Life and Medical Sciences > Faculty of Life Sciences
UCL > Provost and Vice Provost Offices > School of Life and Medical Sciences > Faculty of Life Sciences > Div of Biosciences
UCL > Provost and Vice Provost Offices > School of Life and Medical Sciences > Faculty of Life Sciences > Div of Biosciences > Cell and Developmental Biology
URI: https://discovery.ucl.ac.uk/id/eprint/10073778
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