The Glide/Gcm fate determinant controls initiation of collective cell migration by regulating Frazzled
- Institut de Génétique et de Biologie Moléculaire et Cellulaire, France
- University of California, Riverside, United States
- Tata Institute for Fundamental Research, India
Abstract
Collective migration is a complex process that contributes to build precise tissue and organ architecture. Several molecules involved in cell interaction control collective migration, but what their precise role is and how is their expression finely tuned to orchestrate the different steps of the process is poorly understood. Here we show that the timely and threshold expression of the Netrin receptor Frazzled triggers the initiation of glia migration in the Drosophila wing. Frazzled expression is induced by the Glide/Gcm transcription factor in a dose dependent manner. Thus, the glial determinant also regulates the efficiency of collective migration. NetrinB but not NetrinA serves as a chemoattractant and Unc5 contributes as a repellant Netrin receptor for glia migration. Our model includes strict spatial localization of a ligand, a cell autonomously acting receptor and a fate determinant that act coordinately to direct glia towards their final destination.
Article and author information
Author details
Funding
CEFIPRA-4403-1 (graduate student fellowship)
- K VijayRaghavan
- Angela Giangrande
Agence Nationale de la Recherche (international award)
- Angela Giangrande
Fondation pour la Recherche Médicale (labelisation)
- Angela Giangrande
ARC Centre of Excellence for Coherent X-Ray Science (Projet grant)
- Angela Giangrande
Ligue Contre le Cancer (Grant regional)
- Angela Giangrande
USIAS
- Angela Giangrande
The funders had no role in study design, data collection and interpretation, or the decision to submit the work for publication.
Reviewing Editor
- Hugo J Bellen, Baylor College of Medicine, United States
Version history
- Received: March 11, 2016
- Accepted: October 12, 2016
- Accepted Manuscript published: October 14, 2016 (version 1)
- Version of Record published: November 8, 2016 (version 2)
Copyright
© 2016, Gupta et al.
This article is distributed under the terms of the Creative Commons Attribution License permitting unrestricted use and redistribution provided that the original author and source are credited.
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The Glide/Gcm fate determinant controls initiation of collective cell migration by regulating Frazzled
eLife 5:e15983.
https://doi.org/10.7554/eLife.15983
Further reading
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Large-scale cell flow characterizes gastrulation in animal development. In amniote gastrulation, particularly in avian gastrula, a bilateral vortex-like counter-rotating cell flow, called ‘polonaise movements’, appears along the midline. Here, through experimental manipulations, we addressed relationships between the polonaise movements and morphogenesis of the primitive streak, the earliest midline structure in amniotes. Suppression of the Wnt/planar cell polarity (PCP) signaling pathway maintains the polonaise movements along a deformed primitive streak. Mitotic arrest leads to diminished extension and development of the primitive streak and maintains the early phase of the polonaise movements. Ectopically induced Vg1, an axis-inducing morphogen, generates the polonaise movements, aligned to the induced midline, but disturbs the stereotypical cell flow pattern at the authentic midline. Despite the altered cell flow, induction and extension of the primitive streak are preserved along both authentic and induced midlines. Finally, we show that ectopic axis-inducing morphogen, Vg1, is capable of initiating the polonaise movements without concomitant PS extension under mitotic arrest conditions. These results are consistent with a model wherein primitive streak morphogenesis is required for the maintenance of the polonaise movements, but the polonaise movements are not necessarily responsible for primitive streak morphogenesis. Our data describe a previously undefined relationship between the large-scale cell flow and midline morphogenesis in gastrulation.
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Geometric criteria can be used to assess whether cell intercalation is active or passive during the convergent extension of tissue.
