The planar polarity pathway promotes coordinated cell migration during Drosophila oogenesis.
Cell migration is fundamental in both animal morphogenesis and disease. The migration of individual cells is relatively well-studied; however, in vivo, cells often remain joined by cell-cell junctions and migrate in cohesive groups. How such groups of cells coordinate their migration is poorly understood. The planar polarity pathway coordinates the polarity of non-migrating cells in epithelial sheets and is required for cell rearrangements during vertebrate morphogenesis. It is therefore a good candidate to play a role in the collective migration of groups of cells. Drosophila border cell migration is a well-characterised and genetically tractable model of collective cell migration, during which a group of about six to ten epithelial cells detaches from the anterior end of the developing egg chamber and migrates invasively towards the oocyte. We find that the planar polarity pathway promotes this invasive migration, acting both in the migrating cells themselves and in the non-migratory polar follicle cells that they carry along. Disruption of planar polarity signalling causes abnormalities in actin-rich processes on the cell surface and leads to less-efficient migration. This is apparently due, in part, to a loss of regulation of Rho GTPase activity by the planar polarity receptor Frizzled, which itself becomes localised to the migratory edge of the border cells. We conclude that, during collective cell migration, the planar polarity pathway can mediate communication between motile and non-motile cells, which enhances the efficiency of migration via the modulation of actin dynamics.
Bastock
Rebecca
R
Centre for Developmental and Biomedical Genetics, Department of Biomedical Science, University of Sheffield, Western Bank, Sheffield S10 2TN, UK.
Strutt
David
D
D008841:Actin Cytoskeleton / Q000378:metabolism; D000818:Animals; D030801:Animals, Genetically Modified; D019521:Body Patterning / Q000235:genetics / Q000502:physiology; D015820:Cadherins / Q000235:genetics; D002465:Cell Movement / Q000235:genetics / Q000502:physiology*; D016764:Cell Polarity / Q000235:genetics / Q000502:physiology*; D004330:Drosophila / Q000196:embryology* / Q000502:physiology; D029721:Drosophila Proteins / Q000235:genetics / Q000378:metabolism; D004625:Embryo, Nonmammalian; D005260:Female; D051157:Frizzled Receptors / Q000378:metabolism; D018507:Gene Expression Regulation, Developmental; D008565:Membrane Proteins / Q000378:metabolism; D008954:Models, Biological; D009866:Oogenesis / Q000235:genetics / Q000502:physiology*; D043562:Receptors, G-Protein-Coupled / Q000378:metabolism; D050791:STAT Transcription Factors / Q000235:genetics; D015398:Signal Transduction / Q000235:genetics; D020742:rhoA GTP-Binding Protein / Q000502:physiology
D015820:Cadherins; D029721:Drosophila Proteins; D051157:Frizzled Receptors; D008565:Membrane Proteins; D043562:Receptors, G-Protein-Coupled; D050791:STAT Transcription Factors; C105675:Stat92E protein, Drosophila; C111638:Vang protein, Drosophila; C058784:fz protein, Drosophila; C501889:shg protein, Drosophila; D020742:rhoA GTP-Binding Protein