The Glide/Gcm fate determinant controls initiation of collective cell migration by regulating Frazzled

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Abstract

Collective migration is a complex process that contributes to build precise tissue and organ architecture. Several molecules implicated in cell interactions also control collective migration, but their precise role and the finely tuned expression that orchestrates this complex developmental process are poorly understood. Here, we show that the timely and threshold expression of the Netrin receptor Frazzled triggers the initiation of glia migration in the developing Drosophila wing. Frazzled expression is induced by the transcription factor Glide/Gcm 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 toward their final destination.

DOI: http://dx.doi.org/10.7554/eLife.15983.001

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Most cited references 78

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Netrins are secreted proteins that were first identified as guidance cues, directing cell and axon migration during neural development. Subsequent findings have demonstrated that netrins can influence the formation of multiple tissues, including the vasculature, lung, pancreas, muscle and mammary gland, by mediating cell migration, cell-cell interactions and cell-extracellular matrix adhesion. Recent evidence also implicates the ongoing expression of netrins and netrin receptors in the maintenance of cell-cell organisation in mature tissues. Here, we review the mechanisms involved in netrin signalling in vertebrate and invertebrate systems and discuss the functions of netrin signalling during the development of neural and non-neural tissues.

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Author and article information

Contributors

Hugo J Bellen: Role: Reviewing editor

Journal

Journal ID (nlm-ta): eLife

Journal ID (iso-abbrev): Elife

Journal ID (hwp): eLife

Journal ID (publisher-id): eLife

Title: eLife

Publisher: eLife Sciences Publications, Ltd

ISSN (Electronic): 2050-084X

Publication date (Electronic, pub): 14 October 2016

Publication date Collection: 2016

Volume: 5

Electronic Location Identifier: e15983

Affiliations

[1 ]deptDepartment of Functional Genomics and Cancer , Institut de Génétique et de Biologie Moléculaire et Cellulaire , Illkirch, France

[2 ]Centre National de la Recherche Scientifique, UMR7104 , Illkirch, France

[3 ]Institut National de la Santé et de la Recherche Médicale, U964 , Illkirch, France

[4 ]Université de Strasbourg , Illkirch, France

[5 ]deptDepartment of Developmental Biology and Genetics , Tata Institute for Fundamental Research , Bangalore, India

[6 ]deptNational Centre for Biological Sciences , Tata Institute for Fundamental Research , Bangalore, India

[7]Baylor College of Medicine , United States

[8]Baylor College of Medicine , United States

Author notes

angela@ 123456igbmc.fr

[†]

Department of Entomology, University of California, Riverside, United States.

Author information

K VijayRaghavan http://orcid.org/0000-0002-4705-5629

Angela Giangrande http://orcid.org/0000-0001-6278-5120

Article

Publisher ID: 15983

DOI: 10.7554/eLife.15983

PMC ID: 5114015

PubMed ID: 27740455

SO-VID: f96b40de-2498-4573-8bd7-f5cbd977986a

License:

This article is distributed under the terms of the Creative Commons Attribution License, which permits unrestricted use and redistribution provided that the original author and source are credited.

History

Date received : 11 March 2016

Date accepted : 12 October 2016

Funding

Funded by: CEFIPRA-4403-1;

Award ID: graduate student fellowship

Award Recipient : K VijayRaghavan Angela Giangrande

Funded by: FundRef http://dx.doi.org/10.13039/501100001665, Agence Nationale de la Recherche;

Award ID: international award