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      Dynein-Mediated Regional Cell Division Reorientation Shapes a Tailbud Embryo

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      1 , 2 , , 1
      iScience
      Elsevier
      Organizational Aspects of Cell Biology, Developmental Biology, Embryology

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          Summary

          Regulation of cell division orientation controls the spatial distribution of cells during development and is essential for one-directional tissue transformation, such as elongation. However, little is known about whether it plays a role in other types of tissue morphogenesis. Using an ascidian Halocynthia roretzi, we found that differently oriented cell divisions in the epidermis of the future trunk (anterior) and tail (posterior) regions create an hourglass-like epithelial bending between the two regions to shape the tailbud embryo. Our results show that posterior epidermal cells are polarized with dynein protein anteriorly localized, undergo dynein-dependent spindle rotation, and divide along the anteroposterior axis. This cell division facilitates constriction around the embryo's circumference only in the posterior region and epithelial bending formation. Our findings, therefore, provide an important insight into the role of oriented cell division in tissue morphogenesis.

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          Highlights

          • Differently oriented cell division creates epithelial bending to shape the tail bud

          • Epidermal cells divide in different orientations in two different adjacent regions

          • Posterior cells undergo dynein-dependent spindle rotation and divide along A-P axis

          • Dynein is enriched in the anterior surface of the posterior cells

          Abstract

          Organizational Aspects of Cell Biology; Developmental Biology; Embryology

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          Most cited references64

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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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            Small-molecule inhibitors of the AAA+ ATPase motor cytoplasmic dynein

            The conversion of chemical energy into mechanical force by AAA+ (ATPases associated with diverse cellular activities) ATPases is integral to cellular processes, including DNA replication, protein unfolding, cargo transport, and membrane fusion 1 . The AAA+ ATPase motor cytoplasmic dynein regulates ciliary trafficking 2 , mitotic spindle formation 3 , and organelle transport 4 , and dissecting its precise functions has been challenging due to its rapid timescale of action and the lack of cell-permeable, chemical modulators. Here we describe the discovery of ciliobrevins, the first specific small-molecule antagonists of cytoplasmic dynein. Ciliobrevins perturb protein trafficking within the primary cilium, leading to their malformation and Hedgehog signaling blockade. Ciliobrevins also prevent spindle pole focusing, kinetochore-microtubule attachment, melanosome aggregation, and peroxisome motility in cultured cells. We further demonstrate the ability of ciliobrevins to block dynein-dependent microtubule gliding and ATPase activity in vitro. Ciliobrevins therefore will be useful reagents for studying cellular processes that require this microtubule motor and may guide the development of additional AAA+ ATPase superfamily inhibitors.
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              Apical constriction: a cell shape change that can drive morphogenesis.

              Biologists have long recognized that dramatic bending of a cell sheet may be driven by even modest shrinking of the apical sides of cells. Cell shape changes and tissue movements like these are at the core of many of the morphogenetic movements that shape animal form during development, driving processes such as gastrulation, tube formation, and neurulation. The mechanisms of such cell shape changes must integrate developmental patterning information in order to spatially and temporally control force production-issues that touch on fundamental aspects of both cell and developmental biology and on birth defects research. How does developmental patterning regulate force-producing mechanisms, and what roles do such mechanisms play in development? Work on apical constriction from multiple systems including Drosophila, Caenorhabditis elegans, sea urchin, Xenopus, chick, and mouse has begun to illuminate these issues. Here, we review this effort to explore the diversity of mechanisms of apical constriction, the diversity of roles that apical constriction plays in development, and the common themes that emerge from comparing systems. Copyright 2009 Elsevier Inc. All rights reserved.
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                Author and article information

                Contributors
                Journal
                iScience
                iScience
                iScience
                Elsevier
                2589-0042
                2589-0042
                07 March 2020
                27 March 2020
                07 March 2020
                : 23
                : 3
                : 100964
                Affiliations
                [1 ]Asamushi Research Center for Marine Biology, Graduate School of Life Sciences, Tohoku University, 9 Sakamoto, Asamushi, Aomori 039-3501, Japan
                Author notes
                []Corresponding author ayaki.nakamoto.a4@ 123456tohoku.ac.jp
                [2]

                Lead Contact

                Article
                S2589-0042(20)30148-6 100964
                10.1016/j.isci.2020.100964
                7082557
                32199290
                d6a7017f-c246-42fe-9bd9-96d526261cfc
                © 2020 The Authors

                This is an open access article under the CC BY-NC-ND license (http://creativecommons.org/licenses/by-nc-nd/4.0/).

                History
                : 14 August 2019
                : 17 January 2020
                : 3 March 2020
                Categories
                Article

                organizational aspects of cell biology,developmental biology,embryology

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