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Control of the collective migration of enteric neural crest cells by the Complement anaphylatoxin C3a and N-cadherin

Broders-Bondon, F; Paul-Gilloteaux, P; Gazquez, E; Heysch, J; Piel, M; Mayor, R; Lambris, JD; (2016) Control of the collective migration of enteric neural crest cells by the Complement anaphylatoxin C3a and N-cadherin. Developmental Biology , 414 (1) pp. 85-99. 10.1016/j.ydbio.2016.03.022. Green open access

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Abstract

We analyzed the cellular and molecular mechanisms governing the adhesive and migratory behavior of enteric neural crest cells (ENCCs) during their collective migration within the developing mouse gut. We aimed to decipher the role of the complement anaphylatoxin C3a during this process, because this well-known immune system attractant has been implicated in cephalic NCC co-attraction, a process controlling directional migration. We used the conditional Ht-PA-cre transgenic mouse model allowing a specific ablation of the N-cadherin gene and the expression of a fluorescent reporter in migratory ENCCs without affecting the central nervous system. We performed time-lapse videomicroscopy of ENCCs from control and N-cadherin mutant gut explants cultured on fibronectin (FN) and micropatterned FN-stripes with C3a or C3aR antagonist, and studied cell migration behavior with the use of triangulation analysis to quantify cell dispersion. We performed ex vivo gut cultures with or without C3aR antagonist to determine the effect on ENCC behavior. Confocal microscopy was used to analyze the cell-matrix adhesion properties. We provide the first demonstration of the localization of the complement anaphylatoxin C3a and its receptor on ENCCs during their migration in the embryonic gut. C3aR receptor inhibition alters ENCC adhesion and migration, perturbing directionality and increasing cell dispersion both in vitro and ex vivo. N-cadherin-null ENCCs do not respond to C3a co-attraction. These findings indicate that C3a regulates cell migration in a N-cadherin-dependent process. Our results shed light on the role of C3a in regulating collective and directional cell migration, and in ganglia network organization during enteric nervous system ontogenesis. The detection of an immune system chemokine in ENCCs during ENS development may also shed light on new mechanisms for gastrointestinal disorders.

Type: Article
Title: Control of the collective migration of enteric neural crest cells by the Complement anaphylatoxin C3a and N-cadherin
Open access status: An open access version is available from UCL Discovery
DOI: 10.1016/j.ydbio.2016.03.022
Publisher version: http://doi.org/10.1016/j.ydbio.2016.03.022
Language: English
Additional information: Copyright © 2016 Elsevier Inc. This manuscript version is made available under a Creative Commons Attribution Non-commercial Non-derivative 4.0 International license (CC BY-NC-ND 4.0). This license allows you to share, copy, distribute and transmit the work for personal and non-commercial use providing author and publisher attribution is clearly stated. Further details about CC BY licenses are available at http://creativecommons.org/licenses/by/4.0 Access may be initially restricted by the publisher.
Keywords: Enteric nervous system; Neural crest cells; Co-attraction; Complement anaphylatoxin C3a; N-cadherin; Migration; Adhesion
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: http://discovery.ucl.ac.uk/id/eprint/1508149
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