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Building the cytokinetic contractile ring in an early embryo: initiation as clusters of myosin II, anillin and septin, and visualization of a septin filament network

Chelsea Garno, Zoe H. Irons, Courtney M. Gamache, Xufeng Wu, Charles B. Shuster, View ORCID ProfileJohn H. Henson
doi: https://doi.org/10.1101/2021.05.25.445582
Chelsea Garno
1Department of Biology, New Mexico State University, Las Cruces, New Mexico, United States of America
2Friday Harbor Laboratories, University of Washington, Friday Harbor, Washington, United States of America
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Zoe H. Irons
2Friday Harbor Laboratories, University of Washington, Friday Harbor, Washington, United States of America
3Department of Biology, Dickinson College, Carlisle, Pennsylvania, United States of America
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Courtney M. Gamache
2Friday Harbor Laboratories, University of Washington, Friday Harbor, Washington, United States of America
3Department of Biology, Dickinson College, Carlisle, Pennsylvania, United States of America
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Xufeng Wu
4National Heart, Lung, and Blood Institute, National Institutes of Health, Bethesda, Maryland, United States of America
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Charles B. Shuster
1Department of Biology, New Mexico State University, Las Cruces, New Mexico, United States of America
2Friday Harbor Laboratories, University of Washington, Friday Harbor, Washington, United States of America
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John H. Henson
2Friday Harbor Laboratories, University of Washington, Friday Harbor, Washington, United States of America
3Department of Biology, Dickinson College, Carlisle, Pennsylvania, United States of America
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  • ORCID record for John H. Henson
  • For correspondence: henson@dickinson.edu
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Abstract

The cytokinetic contractile ring (CR) was first described some 50 years ago, however our understanding of the assembly and structure of the animal cell CR remains incomplete. We recently reported that mature CRs in sea urchin embryos contain myosin II mini-filaments organized into aligned concatenated arrays, and that in early CRs myosin II formed discrete clusters that transformed into the linearized structure over time. The present study extends our previous work by addressing the hypothesis that these myosin II clusters also contain the crucial scaffolding proteins anillin and septin, known to help link actin, myosin II, RhoA, and the membrane during cytokinesis. Super-resolution imaging of cortices from dividing embryos indicates that within each cluster, anillin and septin2 occupy a centralized position relative to the myosin II mini-filaments. As CR formation progresses, the myosin II, septin and anillin containing clusters enlarge and coalesce into patchy and faintly linear patterns. Our super-resolution images provide the initial visualization of anillin and septin nanostructure within an animal cell CR, including evidence of a septin filament network. Furthermore, Latrunculin-treated embryos indicated that the localization of septin or anillin to the myosin II clusters in the early CR was not dependent on actin filaments. These results highlight the structural progression of the CR in sea urchin embryos from an array of clusters to a linearized purse string, the association of anillin and septin with this process, and provide, for the first time, the visualization of septin filament higher order structure in an animal cell CR.

Competing Interest Statement

The authors have declared no competing interest.

Copyright 
The copyright holder for this preprint is the author/funder, who has granted bioRxiv a license to display the preprint in perpetuity. This article is a US Government work. It is not subject to copyright under 17 USC 105 and is also made available for use under a CC0 license.
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Posted May 25, 2021.
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Building the cytokinetic contractile ring in an early embryo: initiation as clusters of myosin II, anillin and septin, and visualization of a septin filament network
Chelsea Garno, Zoe H. Irons, Courtney M. Gamache, Xufeng Wu, Charles B. Shuster, John H. Henson
bioRxiv 2021.05.25.445582; doi: https://doi.org/10.1101/2021.05.25.445582
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Building the cytokinetic contractile ring in an early embryo: initiation as clusters of myosin II, anillin and septin, and visualization of a septin filament network
Chelsea Garno, Zoe H. Irons, Courtney M. Gamache, Xufeng Wu, Charles B. Shuster, John H. Henson
bioRxiv 2021.05.25.445582; doi: https://doi.org/10.1101/2021.05.25.445582

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