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

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          ABSTRACT

          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.

          Abstract

          Summary: Transgenic Lifeact-GFP Hydra polyps provide a powerful system for live imaging of actin dynamics during morphogenesis and development of a simple and ancestral animal model.

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          Most cited references53

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          Fluorogenic probes for live-cell imaging of the cytoskeleton.

          We introduce far-red, fluorogenic probes that combine minimal cytotoxicity with excellent brightness and photostability for fluorescence imaging of actin and tubulin in living cells. Applied in stimulated emission depletion (STED) microscopy, they reveal the ninefold symmetry of the centrosome and the spatial organization of actin in the axon of cultured rat neurons with a resolution unprecedented for imaging cytoskeletal structures in living cells.
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            Integration of actin dynamics and cell adhesion by a three-dimensional, mechanosensitive molecular clutch.

            During cell migration, the forces generated in the actin cytoskeleton are transmitted across transmembrane receptors to the extracellular matrix or other cells through a series of mechanosensitive, regulable protein-protein interactions termed the molecular clutch. In integrin-based focal adhesions, the proteins forming this linkage are organized into a conserved three-dimensional nano-architecture. Here we discuss how the physical interactions between the actin cytoskeleton and focal-adhesion-associated molecules mediate force transmission from the molecular clutch to the extracellular matrix.
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              Apical constriction: themes and variations on a cellular mechanism driving morphogenesis.

              Apical constriction is a cell shape change that promotes tissue remodeling in a variety of homeostatic and developmental contexts, including gastrulation in many organisms and neural tube formation in vertebrates. In recent years, progress has been made towards understanding how the distinct cell biological processes that together drive apical constriction are coordinated. These processes include the contraction of actin-myosin networks, which generates force, and the attachment of actin networks to cell-cell junctions, which allows forces to be transmitted between cells. Different cell types regulate contractility and adhesion in unique ways, resulting in apical constriction with varying dynamics and subcellular organizations, as well as a variety of resulting tissue shape changes. Understanding both the common themes and the variations in apical constriction mechanisms promises to provide insight into the mechanics that underlie tissue morphogenesis.
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                Author and article information

                Journal
                Biol Open
                Biol Open
                bio
                biolopen
                Biology Open
                The Company of Biologists Ltd
                2046-6390
                15 August 2017
                19 June 2017
                19 June 2017
                : 6
                : 8
                : 1137-1148
                Affiliations
                [1 ]Department for Evolutionary Developmental Biology, Institute of Zoology and Centre for Molecular Biosciences, University of Innsbruck , Technikerstr. 25, A-6020 Innsbruck, Austria
                [2 ]Max-Planck-Institute of Biochemistry , Research Group Cellular Dynamics and Cell Patterning, Am Klopferspitz 18, D-82152 Planegg, Martinsried, Germany
                [3 ]Department of Anatomy and Cell Biology, University of Kansas Medical Centre , Kansas City, KS 66160, USA
                Author notes
                [*]

                Present address: Institute of Cell Dynamics and Imaging and Cells-In-Motion Cluster of Excellence (EXC1003 – CiM), University of Münster, Münster, Germany.

                [‡]

                Present address: Department of Molecular and Cellular Biology, Baylor College of Medicine, Houston, TX 77030, USA.

                [§ ]Author for correspondence ( bert.hobmayer@ 123456uibk.ac.at )
                Author information
                http://orcid.org/0000-0002-3401-3294
                Article
                BIO022723
                10.1242/bio.022723
                5576072
                28630355
                16e64a0f-ee20-444b-a494-da05c6a6b636
                © 2017. Published by The Company of Biologists Ltd

                This is an Open Access article distributed under the terms of the Creative Commons Attribution License ( http://creativecommons.org/licenses/by/3.0), which permits unrestricted use, distribution and reproduction in any medium provided that the original work is properly attributed.

                History
                : 22 November 2016
                : 13 June 2017
                Funding
                Funded by: Austrian Science Fund, http://dx.doi.org/10.13039/501100002428;
                Award ID: P16685
                Award ID: P19232
                Award ID: P20734
                Funded by: Tirol Science Fund;
                Award ID: UNI-0404/185
                Categories
                Research Article

                Life sciences
                lifeact,epithelial cell,morphogenesis,cnidarian,tissue evagination,evolution
                Life sciences
                lifeact, epithelial cell, morphogenesis, cnidarian, tissue evagination, evolution

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