Cell volume changes contribute to epithelial morphogenesis in zebrafish Kupffer's vesicle

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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.

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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.

"This ORCID iD identifies the author of this article:" 0000-0003-0860-1006
Matthias Merkel

Department of Physics, Syracuse University, Syracuse, United States

Competing interests
The authors declare that no competing interests exist.

"This ORCID iD identifies the author of this article:" 0000-0001-9118-1270
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.
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.
Jonathan Edward Dawson

Department of Physics, Syracuse University, Syracuse, United States

Competing interests
The authors declare that no competing interests exist.

"This ORCID iD identifies the author of this article:" 0000-0001-9770-8475
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.
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.

"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.

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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.