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      An Equatorial Contractile Mechanism Drives Cell Elongation but not Cell Division

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          There is no author summary for this article yet. Authors can add summaries to their articles on ScienceOpen to make them more accessible to a non-specialist audience.

          Abstract

          A cytokinesis-like contractile mechanism is co-opted in a different developmental scenario to achieve cell elongation instead of cell division in Ciona intestinalis.

          Abstract

          Cell shape changes and proliferation are two fundamental strategies for morphogenesis in animal development. During embryogenesis of the simple chordate Ciona intestinalis, elongation of individual notochord cells constitutes a crucial stage of notochord growth, which contributes to the establishment of the larval body plan. The mechanism of cell elongation is elusive. Here we show that although notochord cells do not divide, they use a cytokinesis-like actomyosin mechanism to drive cell elongation. The actomyosin network forming at the equator of each notochord cell includes phosphorylated myosin regulatory light chain, α-actinin, cofilin, tropomyosin, and talin. We demonstrate that cofilin and α-actinin are two crucial components for cell elongation. Cortical flow contributes to the assembly of the actomyosin ring. Similar to cytokinetic cells, membrane blebs that cause local contractions form at the basal cortex next to the equator and participate in force generation. We present a model in which the cooperation of equatorial actomyosin ring-based constriction and bleb-associated contractions at the basal cortex promotes cell elongation. Our results demonstrate that a cytokinesis-like contractile mechanism is co-opted in a completely different developmental scenario to achieve cell shape change instead of cell division. We discuss the occurrences of actomyosin rings aside from cell division, suggesting that circumferential contraction is an evolutionally conserved mechanism to drive cell or tissue elongation.

          Author Summary

          The actomyosin cytoskeleton is the primary force that drives cell shape changes. These fibers are organized in elaborate structures that form sarcomeres in the muscle and the contractile ring during cytokinesis. In cytokinesis, the establishment of an equatorial actomyosin ring is preceded and regulated by many cell cycle events, and the ring itself is a complex and dynamic structure. Here we report the presence of an equatorial circumferential actomyosin structure with remarkable similarities to the cytokinetic ring formed in postmitotic notochord cells of sea squirt Ciona intestinalis. The notochord is a transient rod-like structure found in all embryos that belong to the phylum Chordata, and in Ciona, a simple chordate, it consists of only 40 cylindrical cells arranged in a single file, which elongate individually during development. Our study shows that the activity of the equatorial actomyosin ring is required for the elongation of the notochord cells. We also find that cortical flow contributes significantly to the formation of the ring at the equator. Similar to cytokinetic cells, we observe the formation of membrane blebs outside the equatorial region. Our analyses suggest that cooperation of actomyosin ring-based circumferential constriction and bleb-associated contractions drive cell elongation in Ciona. We conclude that cells can utilize a cytokinesis-like force generation mechanism to promote cell shape change instead of cell division.

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          Most cited references 97

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          Tunicates and not cephalochordates are the closest living relatives of vertebrates.

          Tunicates or urochordates (appendicularians, salps and sea squirts), cephalochordates (lancelets) and vertebrates (including lamprey and hagfish) constitute the three extant groups of chordate animals. Traditionally, cephalochordates are considered as the closest living relatives of vertebrates, with tunicates representing the earliest chordate lineage. This view is mainly justified by overall morphological similarities and an apparently increased complexity in cephalochordates and vertebrates relative to tunicates. Despite their critical importance for understanding the origins of vertebrates, phylogenetic studies of chordate relationships have provided equivocal results. Taking advantage of the genome sequencing of the appendicularian Oikopleura dioica, we assembled a phylogenomic data set of 146 nuclear genes (33,800 unambiguously aligned amino acids) from 14 deuterostomes and 24 other slowly evolving species as an outgroup. Here we show that phylogenetic analyses of this data set provide compelling evidence that tunicates, and not cephalochordates, represent the closest living relatives of vertebrates. Chordate monophyly remains uncertain because cephalochordates, albeit with a non-significant statistical support, surprisingly grouped with echinoderms, a hypothesis that needs to be tested with additional data. This new phylogenetic scheme prompts a reappraisal of both morphological and palaeontological data and has important implications for the interpretation of developmental and genomic studies in which tunicates and cephalochordates are used as model animals.
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            Cytokinesis in animal cells.

            Cytokinesis, the final step in cell division, partitions the contents of a single cell into two. In animal cells, cytokinesis occurs through cortical remodeling orchestrated by the anaphase spindle. Cytokinesis relies on a tight interplay between signaling and cellular mechanics and has attracted the attention of both biologists and physicists for more than a century. In this review, we provide an overview of four topics in animal cell cytokinesis: (a) signaling between the anaphase spindle and cortex, (b) the mechanics of cortical remodeling, (c) abscission, and (d) regulation of cytokinesis by the cell cycle machinery. We report on recent progress in these areas and highlight some of the outstanding questions that these findings bring into focus.
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              Versatile fluorescent probes for actin filaments based on the actin-binding domain of utrophin.

              Actin filaments (F-actin) are protein polymers that undergo rapid assembly and disassembly and control an enormous variety of cellular processes ranging from force production to regulation of signal transduction. Consequently, imaging of F-actin has become an increasingly important goal for biologists seeking to understand how cells and tissues function. However, most of the available means for imaging F-actin in living cells suffer from one or more biological or experimental shortcomings. Here we describe fluorescent F-actin probes based on the calponin homology domain of utrophin (Utr-CH), which binds F-actin without stabilizing it in vitro. We show that these probes faithfully report the distribution of F-actin in living and fixed cells, distinguish between stable and dynamic F-actin, and have no obvious effects on processes that depend critically on the balance of actin assembly and disassembly. (c) 2007 Wiley-Liss, Inc.
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                Author and article information

                Contributors
                Role: Academic Editor
                Journal
                PLoS Biol
                PLoS Biol
                plos
                plosbiol
                PLoS Biology
                Public Library of Science (San Francisco, USA )
                1544-9173
                1545-7885
                February 2014
                4 February 2014
                : 12
                : 2
                Affiliations
                Sars International Centre for Marine Molecular Biology, University of Bergen, Bergen, Norway
                University of California Berkeley, United States of America
                Author notes

                The authors have declared that no competing interests exist.

                The author(s) have made the following declarations about their contributions: Conceived and designed the experiments: IS BD DJ. Performed the experiments: IS BD ED PB WD DJ. Analyzed the data: IS BD ED DJ. Contributed reagents/materials/analysis tools: IS BD ED PB WD BM DJ. Wrote the paper: IS BD DJ.

                [¤]

                Current address: RIKEN Center for Developmental Biology, Kobe, Hyogo, Japan.

                Article
                PBIOLOGY-D-13-01715
                10.1371/journal.pbio.1001781
                3913557

                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 credited.

                Page count
                Pages: 16
                Funding
                This work was supported by grants 133335/V40 and 183302/S10 from the Norwegian Research Council to D.J. The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript.
                Categories
                Research Article
                Biology
                Developmental Biology
                Morphogenesis
                Evolutionary Biology
                Evolutionary Developmental Biology
                Model Organisms
                Animal Models
                Ciona Intestinalis
                Molecular Cell Biology
                Cellular Structures
                Cytoskeleton

                Life sciences

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