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      Crosslinking activity of non-muscle myosin II is not sufficient for embryonic cytokinesis in C. elegans

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          ABSTRACT

          Cytokinesis in animal cells requires the assembly and constriction of a contractile actomyosin ring. Non-muscle myosin II is essential for cytokinesis, but the role of its motor activity remains unclear. Here, we examine cytokinesis in C. elegans embryos expressing non-muscle myosin motor mutants generated by genome editing. Two non-muscle motor-dead myosins capable of binding F-actin do not support cytokinesis in the one-cell embryo, and two partially motor-impaired myosins delay cytokinesis and render rings more sensitive to reduced myosin levels. Further analysis of myosin mutants suggests that it is myosin motor activity, and not the ability of myosin to crosslink F-actin, that drives the alignment and compaction of F-actin bundles during contractile ring assembly, and that myosin motor activity sets the pace of contractile ring constriction. We conclude that myosin motor activity is required at all stages of cytokinesis. Finally, characterization of the corresponding motor mutations in C. elegans major muscle myosin shows that motor activity is required for muscle contraction but is dispensable for F-actin organization in adult muscles.

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          [Related article:] Highlighted Article: The motor activity of non-muscle myosin II is essential for cytokinesis and contributes to all stages of the process in C. elegans embryos.

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          Most cited references81

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          Non-muscle myosin II takes centre stage in cell adhesion and migration.

          Non-muscle myosin II (NM II) is an actin-binding protein that has actin cross-linking and contractile properties and is regulated by the phosphorylation of its light and heavy chains. The three mammalian NM II isoforms have both overlapping and unique properties. Owing to its position downstream of convergent signalling pathways, NM II is central in the control of cell adhesion, cell migration and tissue architecture. Recent insight into the role of NM II in these processes has been gained from loss-of-function and mutant approaches, methods that quantitatively measure actin and adhesion dynamics and the discovery of NM II mutations that cause monogenic diseases.
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            Single-copy insertion of transgenes in Caenorhabditis elegans.

            At present, transgenes in Caenorhabditis elegans are generated by injecting DNA into the germline. The DNA assembles into a semistable extrachromosomal array composed of many copies of injected DNA. These transgenes are typically overexpressed in somatic cells and silenced in the germline. We have developed a method that inserts a single copy of a transgene into a defined site. Mobilization of a Mos1 transposon generates a double-strand break in noncoding DNA. The break is repaired by copying DNA from an extrachromosomal template into the chromosomal site. Homozygous single-copy insertions can be obtained in less than 2 weeks by injecting approximately 20 worms. We have successfully inserted transgenes as long as 9 kb and verified that single copies are inserted at the targeted site. Single-copy transgenes are expressed at endogenous levels and can be expressed in the female and male germlines.
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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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                Author and article information

                Journal
                Development
                Development
                DEV
                develop
                Development (Cambridge, England)
                The Company of Biologists Ltd
                0950-1991
                1477-9129
                1 November 2019
                12 November 2019
                12 November 2019
                : 146
                : 21
                : dev179150
                Affiliations
                [1 ]Instituto de Investigação e Inovação em Saúde (i3S), Universidade do Porto , 4200-135 Porto, Portugal
                [2 ]Instituto de Biologia Molecular e Celular, Universidade do Porto , 4200-135 Porto, Portugal
                Author notes
                [*]

                These authors contributed equally to this work

                Author information
                http://orcid.org/0000-0003-4144-8189
                http://orcid.org/0000-0002-4770-9768
                http://orcid.org/0000-0002-8190-2617
                http://orcid.org/0000-0001-5970-1870
                http://orcid.org/0000-0002-1840-1473
                http://orcid.org/0000-0003-3674-3116
                http://orcid.org/0000-0002-0360-2977
                http://orcid.org/0000-0002-2256-7134
                Article
                DEV179150
                10.1242/dev.179150
                6857588
                31582415
                d8065d8a-6a58-43ad-8421-c51582f87065
                © 2019. Published by The Company of Biologists Ltd

                This is an Open Access article distributed under the terms of the Creative Commons Attribution License ( https://creativecommons.org/licenses/by/4.0), which permits unrestricted use, distribution and reproduction in any medium provided that the original work is properly attributed.

                History
                : 8 April 2019
                : 23 September 2019
                Funding
                Funded by: European Research Council, http://dx.doi.org/10.13039/100010663;
                Award ID: 640553 - ACTOMYO
                Funded by: Fundação para a Ciência e Tecnologia, http://dx.doi.org/10.13039/100008382;
                Award ID: PTDC/BEX-BCM/0654/2012
                Award ID: SFRH/BD/121874/2016
                Award ID: DL 57/2016/CP1355/CT0013
                Award ID: DL 57/2016/CP1355/CT0017
                Award ID: CEECIND/01967/2017
                Award ID: CEECIND/00333/2017
                Funded by: Fundo Europeu de Desenvolvimento Regional, http://dx.doi.org/10.13039/501100008530;
                Award ID: NORTE-07-0124-FEDER-000003
                Award ID: Norte-01-0145-FEDER-000029
                Award ID: FCOMP-01-0124-FEDER-028255
                Award ID: LISBOA-01-0145-FEDER-022125
                Categories
                Research Article

                Developmental biology
                c. elegans,actomyosin contractility,contractile ring,cytokinesis,non-muscle myosin ii mutants,muscle myosin ii mutants

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