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

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 "This ORCID iD identifies the author of this article:" 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 "This ORCID iD identifies the author of this article:" 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 "This ORCID iD identifies the author of this article:" 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 "This ORCID iD identifies the author of this article:" 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, California Institute of Technology, United States

Version 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.

Metrics

  • 3,602
    Page views
  • 451
    Downloads
  • 22
    Citations

Article citation count generated by polling the highest count across the following sources: Crossref, PubMed Central, Scopus.

Download links

A two-part list of links to download the article, or parts of the article, in various formats.

Downloads (link to download the article as PDF)

Open citations (links to open the citations from this article in various online reference manager services)

Cite this article (links to download the citations from this article in formats compatible with various reference manager tools)

  1. Agnik Dasgupta
  2. Matthias Merkel
  3. Madeline J Clark
  4. Andrew E Jacob
  5. Jonathan Edward Dawson
  6. M Lisa Manning
  7. Jeffrey D Amack
(2018)
Cell volume changes contribute to epithelial morphogenesis in zebrafish Kupffer's vesicle
eLife 7:e30963.
https://doi.org/10.7554/eLife.30963

Share this article

https://doi.org/10.7554/eLife.30963

Further reading

    1. Cell Biology
    2. Neuroscience
    Rachel L Doser, Kaz M Knight ... Frederic J Hoerndli
    Research Article

    Our understanding of mitochondrial signaling in the nervous system has been limited by the technical challenge of analyzing mitochondrial function in vivo. In the transparent genetic model Caenorhabditis elegans, we were able to manipulate and measure mitochondrial ROS (reactive oxygen species) signaling of individual mitochondria as well as neuronal activity of single neurons in vivo. Using this approach, we provide evidence supporting a novel role for mitochondrial ROS signaling in dendrites of excitatory glutamatergic C. elegans interneurons. Specifically, we show that following neuronal activity, dendritic mitochondria take up calcium (Ca2+) via the mitochondrial Ca2+ uniporter MCU-1 that results in an upregulation of mitochondrial ROS production. We also observed that mitochondria are positioned in close proximity to synaptic clusters of GLR-1, the C. elegans ortholog of the AMPA subtype of glutamate receptors that mediate neuronal excitation. We show that synaptic recruitment of GLR-1 is upregulated when MCU-1 function is pharmacologically or genetically impaired but is downregulated by mitoROS signaling. Thus, signaling from postsynaptic mitochondria may regulate excitatory synapse function to maintain neuronal homeostasis by preventing excitotoxicity and energy depletion.

    1. Cell Biology
    2. Developmental Biology
    Houyu Zhang, Yan Li ... Meng Xie
    Research Article

    Perirenal adipose tissue (PRAT) is a unique visceral depot that contains a mixture of brown and white adipocytes. The origin and plasticity of such cellular heterogeneity remains unknown. Here, we combine single-nucleus RNA sequencing with genetic lineage tracing to reveal the existence of a distinct subpopulation of Ucp1-&Cidea+ adipocytes that arises from brown-to-white conversion during postnatal life in the periureter region of mouse PRAT. Cold exposure restores Ucp1 expression and a thermogenic phenotype in this subpopulation. These cells have a transcriptome that is distinct from subcutaneous beige adipocytes and may represent a unique type of cold-recruitable adipocytes. These results pave the way for studies of PRAT physiology and mechanisms controlling the plasticity of brown/white adipocyte phenotypes.