Apical and basal epitheliomuscular F-actin dynamics during Hydra bud evagination

Bending of 2D cell sheets is a fundamental morphogenetic mechanism during animal development and reproduction. A critical player driving cell shape during tissue bending is the actin cytoskeleton. Much of our current knowledge about actin dynamics in whole organisms stems from studies of embryonic d...

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Main Authors: Roland Aufschnaiter, Roland Wedlich-Söldner, Xiaoming Zhang, Bert Hobmayer
Format: Article
Language:English
Published: The Company of Biologists 2017-08-01
Series:Biology Open
Subjects:
Online Access:http://bio.biologists.org/content/6/8/1137
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spelling doaj-d7a922a2570a4b289f82f40b47538ed12021-06-02T09:07:23ZengThe Company of BiologistsBiology Open2046-63902017-08-01681137114810.1242/bio.022723022723Apical and basal epitheliomuscular F-actin dynamics during Hydra bud evaginationRoland Aufschnaiter0Roland Wedlich-Söldner1Xiaoming Zhang2Bert Hobmayer3 Department for Evolutionary Developmental Biology, Institute of Zoology and Centre for Molecular Biosciences, University of Innsbruck, Technikerstr. 25, A-6020 Innsbruck, Austria Max-Planck-Institute of Biochemistry, Research Group Cellular Dynamics and Cell Patterning, Am Klopferspitz 18, D-82152 Planegg, Martinsried, Germany Department of Anatomy and Cell Biology, University of Kansas Medical Centre, Kansas City, KS 66160, USA Department for Evolutionary Developmental Biology, Institute of Zoology and Centre for Molecular Biosciences, University of Innsbruck, Technikerstr. 25, A-6020 Innsbruck, Austria Bending of 2D cell sheets is a fundamental morphogenetic mechanism during animal development and reproduction. A critical player driving cell shape during tissue bending is the actin cytoskeleton. Much of our current knowledge about actin dynamics in whole organisms stems from studies of embryonic development in bilaterian model organisms. Here, we have analyzed actin-based processes during asexual bud evagination in the simple metazoan Hydra. We created transgenic Hydra strains stably expressing the actin marker Lifeact-GFP in either ectodermal or endodermal epitheliomuscular cells. We then combined live imaging with conventional phalloidin staining to directly follow actin reorganization. Bending of the Hydra epithelial double layer is initiated by a group of epitheliomuscular cells in the endodermal layer. These cells shorten their apical-basal axis and arrange their basal muscle processes in a circular configuration. We propose that this rearrangement generates the initial forces to bend the endoderm towards the ectoderm. Convergent tissue movement in both epithelial layers towards the centre of evagination then leads to elongation and extension of the bud along its new body axis. Tissue movement into the bud is associated with lateral intercalation of epithelial cells, remodelling of apical septate junctions, and rearrangement of basal muscle processes. The work presented here extends the analysis of morphogenetic mechanisms beyond embryonic tissues of model bilaterians.http://bio.biologists.org/content/6/8/1137LifeactEpithelial cellMorphogenesisCnidarianTissue evaginationEvolution
collection DOAJ
language English
format Article
sources DOAJ
author Roland Aufschnaiter
Roland Wedlich-Söldner
Xiaoming Zhang
Bert Hobmayer
spellingShingle Roland Aufschnaiter
Roland Wedlich-Söldner
Xiaoming Zhang
Bert Hobmayer
Apical and basal epitheliomuscular F-actin dynamics during Hydra bud evagination
Biology Open
Lifeact
Epithelial cell
Morphogenesis
Cnidarian
Tissue evagination
Evolution
author_facet Roland Aufschnaiter
Roland Wedlich-Söldner
Xiaoming Zhang
Bert Hobmayer
author_sort Roland Aufschnaiter
title Apical and basal epitheliomuscular F-actin dynamics during Hydra bud evagination
title_short Apical and basal epitheliomuscular F-actin dynamics during Hydra bud evagination
title_full Apical and basal epitheliomuscular F-actin dynamics during Hydra bud evagination
title_fullStr Apical and basal epitheliomuscular F-actin dynamics during Hydra bud evagination
title_full_unstemmed Apical and basal epitheliomuscular F-actin dynamics during Hydra bud evagination
title_sort apical and basal epitheliomuscular f-actin dynamics during hydra bud evagination
publisher The Company of Biologists
series Biology Open
issn 2046-6390
publishDate 2017-08-01
description Bending of 2D cell sheets is a fundamental morphogenetic mechanism during animal development and reproduction. A critical player driving cell shape during tissue bending is the actin cytoskeleton. Much of our current knowledge about actin dynamics in whole organisms stems from studies of embryonic development in bilaterian model organisms. Here, we have analyzed actin-based processes during asexual bud evagination in the simple metazoan Hydra. We created transgenic Hydra strains stably expressing the actin marker Lifeact-GFP in either ectodermal or endodermal epitheliomuscular cells. We then combined live imaging with conventional phalloidin staining to directly follow actin reorganization. Bending of the Hydra epithelial double layer is initiated by a group of epitheliomuscular cells in the endodermal layer. These cells shorten their apical-basal axis and arrange their basal muscle processes in a circular configuration. We propose that this rearrangement generates the initial forces to bend the endoderm towards the ectoderm. Convergent tissue movement in both epithelial layers towards the centre of evagination then leads to elongation and extension of the bud along its new body axis. Tissue movement into the bud is associated with lateral intercalation of epithelial cells, remodelling of apical septate junctions, and rearrangement of basal muscle processes. The work presented here extends the analysis of morphogenetic mechanisms beyond embryonic tissues of model bilaterians.
topic Lifeact
Epithelial cell
Morphogenesis
Cnidarian
Tissue evagination
Evolution
url http://bio.biologists.org/content/6/8/1137
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AT rolandwedlichsoldner apicalandbasalepitheliomuscularfactindynamicsduringhydrabudevagination
AT xiaomingzhang apicalandbasalepitheliomuscularfactindynamicsduringhydrabudevagination
AT berthobmayer apicalandbasalepitheliomuscularfactindynamicsduringhydrabudevagination
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