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...
Autores principales: | , , , , , |
---|---|
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 |