Anillin regulates epithelial cell mechanics by structuring the medial-apical actomyosin network

  1. Torey R Arnold
  2. Joseph H Shawky
  3. Rachel E Stephenson
  4. Kayla M Dinshaw
  5. Tomohito Higashi
  6. Farah Huq
  7. Lance A Davidson
  8. Ann L Miller  Is a corresponding author
  1. University of Michigan, United States
  2. University of Pittsburgh, United States

Abstract

Cellular forces sculpt organisms during development, while misregulation of cellular mechanics can promote disease. Here, we investigate how the actomyosin scaffold protein Anillin contributes to epithelial mechanics in Xenopus laevis embryos. Increased mechanosensitive recruitment of Vinculin to cell-cell junctions when Anillin is overexpressed, suggested that Anillin promotes junctional tension. However, junctional laser ablation unexpectedly showed that junctions recoil faster when Anillin is depleted and slower when Anillin is overexpressed. Unifying these findings, we demonstrate that Anillin regulates medial-apical actomyosin. Medial-apical laser ablation supports the conclusion that that tensile forces are stored across the apical surface of epithelial cells, and Anillin promotes the tensile forces stored in this network. Finally, we show that Anillin's effects on cellular mechanics impact tissue-wide mechanics. These results reveal Anillin as a key regulator of epithelial mechanics and lay the groundwork for future studies on how Anillin may contribute to mechanical events in development and disease.

Data availability

All data generated or analysed during this study are included in the manuscript and supporting files. Source data files have been provided for: Figure 1, Figure 2, Figure 3, Figure 4, Figure 6, Figure 7 and Figure 8

Article and author information

Author details

  1. Torey R Arnold

    Department of Molecular, Cellular, and Developmental Biology, University of Michigan, Ann Arbor, United States
    Competing interests
    The authors declare that no competing interests exist.
  2. Joseph H Shawky

    Department of Bioengineering, University of Pittsburgh, Pittsburgh, United States
    Competing interests
    The authors declare that no competing interests exist.
  3. Rachel E Stephenson

    Department of Molecular, Cellular, and Developmental Biology, University of Michigan, Ann Arbor, United States
    Competing interests
    The authors declare that no competing interests exist.
  4. Kayla M Dinshaw

    Department of Molecular, Cellular, and Developmental Biology, University of Michigan, Ann Arbor, United States
    Competing interests
    The authors declare that no competing interests exist.
  5. Tomohito Higashi

    Department of Molecular, Cellular, and Developmental Biology, University of Michigan, Ann Arbor, United States
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0001-5616-1477
  6. Farah Huq

    Department of Molecular, Cellular, and Developmental Biology, University of Michigan, Ann Arbor, United States
    Competing interests
    The authors declare that no competing interests exist.
  7. Lance A Davidson

    Department of Bioengineering, University of Pittsburgh, Pittsburgh, United States
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0002-2956-0437
  8. Ann L Miller

    Department of Molecular, Cellular, and Developmental Biology, University of Michigan, Ann Arbor, United States
    For correspondence
    annlm@umich.edu
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0002-7293-764X

Funding

National Institute of General Medical Sciences (R01 GM112794)

  • Ann L Miller

Eunice Kennedy Shriver National Institute of Child Health and Human Development (R01 HD04475)

  • Lance A Davidson

National Heart, Lung, and Blood Institute (R56 HL134195)

  • Lance A Davidson

The funders had no role in study design, data collection and interpretation, or the decision to submit the work for publication.

Reviewing Editor

  1. Valerie Horsley, Yale University, United States

Ethics

Animal experimentation: All studies conducted using Xenopus laevis embryos strictly adhered to the compliance standards of the US Department of Health and Human Services Guide for the Care and Use of Laboratory Animals and were approved by the University of Michigan's Institutional Animal Care and Use Committee (PRO00007339).

Version history

  1. Received: June 9, 2018
  2. Accepted: January 30, 2019
  3. Accepted Manuscript published: January 31, 2019 (version 1)
  4. Version of Record published: March 19, 2019 (version 2)

Copyright

© 2019, Arnold et al.

This article is distributed under the terms of the Creative Commons Attribution License permitting unrestricted use and redistribution provided that the original author and source are credited.

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  1. Torey R Arnold
  2. Joseph H Shawky
  3. Rachel E Stephenson
  4. Kayla M Dinshaw
  5. Tomohito Higashi
  6. Farah Huq
  7. Lance A Davidson
  8. Ann L Miller
(2019)
Anillin regulates epithelial cell mechanics by structuring the medial-apical actomyosin network
eLife 8:e39065.
https://doi.org/10.7554/eLife.39065

Share this article

https://doi.org/10.7554/eLife.39065

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