Epidermal growth factor signalling controls Myosin II planar polarity to orchestrate convergent extension movements during Drosophila tubulogenesis
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Most epithelial tubes arise as small buds and elongate by regulated morphogenetic processes including oriented cell division, cell rearrangements, and changes in cell shape. Through live analysis of Drosophila renal tubule morphogenesis we show that tissue elongation results from polarised cell intercalations around the tubule circumference, producing convergent-extension tissue movements. Using genetic techniques, we demonstrate that the vector of cell movement is regulated by localised epidermal growth factor (EGF) signalling from the distally placed tip cell lineage, which sets up a distal-to-proximal gradient of pathway activation to planar polarise cells, without the involvement for PCP gene activity. Time-lapse imaging at subcellular resolution shows that the acquisition of planar polarity leads to asymmetric pulsatile Myosin II accumulation in the basal, proximal cortex of tubule cells, resulting in repeated, transient shortening of their circumferential length. This repeated bias in the polarity of cell contraction allows cells to move relative to each other, leading to a reduction in cell number around the lumen and an increase in tubule length. Physiological analysis demonstrates that animals whose tubules fail to elongate exhibit abnormal excretory function, defective osmoregulation, and lethality.
Saxena , A , Denholm , B , Bunt , S , Bischoff , M , VijayRaghavan , K & Skaer , H 2014 , ' Epidermal growth factor signalling controls Myosin II planar polarity to orchestrate convergent extension movements during Drosophila tubulogenesis ' , PLoS Biology , vol. 12 , no. 12 , e1002013 . https://doi.org/10.1371/journal.pbio.1002013
Copyright © 2014. Saxena et al. 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.
DescriptionAditya Saxena was funded by the Cambridge Commonwealth Trust. Barry Denholm was funded by Kidney Research UK PDF1/2010. Stephanie Bunt was funded by The Rae and Edith Bennett Travelling Scholarship and John Stanley Gardiner Trust Fund. Marcus Bischoff was supported by WG086986 and WT096645MA to Peter Lawrence. Krishnaswamy VijayRaghavan was funded by The Wellcome Trust: 079221/B/06/Z. Helen Skaer was funded by The Wellcome Trust: 079221/B/06/Z and 094879/A/10/Z.
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