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...
Main Authors: | , , , |
---|---|
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 |
id |
doaj-d7a922a2570a4b289f82f40b47538ed1 |
---|---|
record_format |
Article |
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 |
work_keys_str_mv |
AT rolandaufschnaiter apicalandbasalepitheliomuscularfactindynamicsduringhydrabudevagination AT rolandwedlichsoldner apicalandbasalepitheliomuscularfactindynamicsduringhydrabudevagination AT xiaomingzhang apicalandbasalepitheliomuscularfactindynamicsduringhydrabudevagination AT berthobmayer apicalandbasalepitheliomuscularfactindynamicsduringhydrabudevagination |
_version_ |
1721406069043888128 |