Cargando…

Epidermal Growth Factor Signalling Controls Myosin II Planar Polarity to Orchestrate Convergent Extension Movements during Drosophila Tubulogenesis

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 inte...

Descripción completa

Detalles Bibliográficos
Autores principales: Saxena, Aditya, Denholm, Barry, Bunt, Stephanie, Bischoff, Marcus, VijayRaghavan, Krishnaswamy, Skaer, Helen
Formato: Online Artículo Texto
Lenguaje:English
Publicado: Public Library of Science 2014
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC4251826/
https://www.ncbi.nlm.nih.gov/pubmed/25460353
http://dx.doi.org/10.1371/journal.pbio.1002013
_version_ 1782347097075351552
author Saxena, Aditya
Denholm, Barry
Bunt, Stephanie
Bischoff, Marcus
VijayRaghavan, Krishnaswamy
Skaer, Helen
author_facet Saxena, Aditya
Denholm, Barry
Bunt, Stephanie
Bischoff, Marcus
VijayRaghavan, Krishnaswamy
Skaer, Helen
author_sort Saxena, Aditya
collection PubMed
description 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.
format Online
Article
Text
id pubmed-4251826
institution National Center for Biotechnology Information
language English
publishDate 2014
publisher Public Library of Science
record_format MEDLINE/PubMed
spelling pubmed-42518262014-12-05 Epidermal Growth Factor Signalling Controls Myosin II Planar Polarity to Orchestrate Convergent Extension Movements during Drosophila Tubulogenesis Saxena, Aditya Denholm, Barry Bunt, Stephanie Bischoff, Marcus VijayRaghavan, Krishnaswamy Skaer, Helen PLoS Biol Research Article 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. Public Library of Science 2014-12-02 /pmc/articles/PMC4251826/ /pubmed/25460353 http://dx.doi.org/10.1371/journal.pbio.1002013 Text en © 2014 Saxena et al http://creativecommons.org/licenses/by/4.0/ 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 properly credited.
spellingShingle Research Article
Saxena, Aditya
Denholm, Barry
Bunt, Stephanie
Bischoff, Marcus
VijayRaghavan, Krishnaswamy
Skaer, Helen
Epidermal Growth Factor Signalling Controls Myosin II Planar Polarity to Orchestrate Convergent Extension Movements during Drosophila Tubulogenesis
title Epidermal Growth Factor Signalling Controls Myosin II Planar Polarity to Orchestrate Convergent Extension Movements during Drosophila Tubulogenesis
title_full Epidermal Growth Factor Signalling Controls Myosin II Planar Polarity to Orchestrate Convergent Extension Movements during Drosophila Tubulogenesis
title_fullStr Epidermal Growth Factor Signalling Controls Myosin II Planar Polarity to Orchestrate Convergent Extension Movements during Drosophila Tubulogenesis
title_full_unstemmed Epidermal Growth Factor Signalling Controls Myosin II Planar Polarity to Orchestrate Convergent Extension Movements during Drosophila Tubulogenesis
title_short Epidermal Growth Factor Signalling Controls Myosin II Planar Polarity to Orchestrate Convergent Extension Movements during Drosophila Tubulogenesis
title_sort epidermal growth factor signalling controls myosin ii planar polarity to orchestrate convergent extension movements during drosophila tubulogenesis
topic Research Article
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC4251826/
https://www.ncbi.nlm.nih.gov/pubmed/25460353
http://dx.doi.org/10.1371/journal.pbio.1002013
work_keys_str_mv AT saxenaaditya epidermalgrowthfactorsignallingcontrolsmyosiniiplanarpolaritytoorchestrateconvergentextensionmovementsduringdrosophilatubulogenesis
AT denholmbarry epidermalgrowthfactorsignallingcontrolsmyosiniiplanarpolaritytoorchestrateconvergentextensionmovementsduringdrosophilatubulogenesis
AT buntstephanie epidermalgrowthfactorsignallingcontrolsmyosiniiplanarpolaritytoorchestrateconvergentextensionmovementsduringdrosophilatubulogenesis
AT bischoffmarcus epidermalgrowthfactorsignallingcontrolsmyosiniiplanarpolaritytoorchestrateconvergentextensionmovementsduringdrosophilatubulogenesis
AT vijayraghavankrishnaswamy epidermalgrowthfactorsignallingcontrolsmyosiniiplanarpolaritytoorchestrateconvergentextensionmovementsduringdrosophilatubulogenesis
AT skaerhelen epidermalgrowthfactorsignallingcontrolsmyosiniiplanarpolaritytoorchestrateconvergentextensionmovementsduringdrosophilatubulogenesis