1. Cell Biology
  2. Developmental Biology and Stem Cells
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Cell volume changes contribute to epithelial morphogenesis in zebrafish Kupffer's vesicle

  1. Agnik Dasgupta
  2. Matthias Merkel
  3. Madeline J Clark
  4. Andrew E Jacob
  5. Jonathan Edward Dawson
  6. M Lisa Manning  Is a corresponding author
  7. Jeffrey D Amack  Is a corresponding author
  1. State University of New York, Upstate Medical University, United States
  2. Syracuse University, United States
Research Article
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Cite as: eLife 2018;7:e30963 doi: 10.7554/eLife.30963

Abstract

How epithelial cell behaviors are coordinately regulated to sculpt tissue architecture is a fundamental question in biology. Kupffer's vesicle (KV), a transient organ with a fluid-filled lumen, provides a simple system to investigate the interplay between intrinsic cellular mechanisms and external forces during epithelial morphogenesis. Using 3-dimensional (3D) analyses of single cells we identify asymmetric cell volume changes along the anteroposterior axis of KV that coincide with asymmetric cell shape changes. Blocking ion flux prevents these cell volume changes and cell shape changes. Vertex simulations suggest cell shape changes do not depend on lumen expansion. Consistent with this prediction, asymmetric changes in KV cell volume and shape occur normally when KV lumen growth fails due to leaky cell adhesions. These results indicate ion flux mediates cell volume changes that contribute to asymmetric cell shape changes in KV, and that these changes in epithelial morphology are separable from lumen-generated forces.

Article and author information

Author details

  1. Agnik Dasgupta

    Department of Cell and Developmental Biology, State University of New York, Upstate Medical University, Syracuse, United States
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon 0000-0003-0860-1006
  2. Matthias Merkel

    Department of Physics, Syracuse University, Syracuse, United States
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon 0000-0001-9118-1270
  3. Madeline J Clark

    Department of Cell and Developmental Biology, State University of New York, Upstate Medical University, Syracuse, United States
    Competing interests
    The authors declare that no competing interests exist.
  4. Andrew E Jacob

    Department of Cell and Developmental Biology, State University of New York, Upstate Medical University, Syracuse, United States
    Competing interests
    The authors declare that no competing interests exist.
  5. Jonathan Edward Dawson

    Department of Physics, Syracuse University, Syracuse, United States
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon 0000-0001-9770-8475
  6. M Lisa Manning

    Department of Physics, Syracuse University, Syracuse, United States
    For correspondence
    mmanning@syr.edu
    Competing interests
    The authors declare that no competing interests exist.
  7. Jeffrey D Amack

    Department of Cell and Developmental Bilogy, State University of New York, Upstate Medical University, Syracuse, United States
    For correspondence
    amackj@upstate.edu
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon 0000-0002-5465-9754

Funding

National Institutes of Health (R01HL095690)

  • Jeffrey D Amack

National Institutes of Health (R01GM117598)

  • M Lisa Manning

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

Reviewing Editor

  1. Marianne Bronner, Reviewing Editor, California Institute of Technology, United States

Publication history

  1. Received: August 5, 2017
  2. Accepted: January 26, 2018
  3. Accepted Manuscript published: January 29, 2018 (version 1)
  4. Version of Record published: February 6, 2018 (version 2)

Copyright

© 2018, Dasgupta 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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