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Vertical uniformity of cells and nuclei in epithelial monolayers

Morphological variability in cytoskeletal organization, organelle position and cell boundaries is a common feature of cultured cells. Remarkable uniformity and reproducibility in structure can be accomplished by providing cells with defined geometric cues. Cells in tissues can also self-organize in...

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Autores principales: Neelam, Srujana, Hayes, Peter Robert, Zhang, Qiao, Dickinson, Richard B., Lele, Tanmay P.
Formato: Online Artículo Texto
Lenguaje:English
Publicado: Nature Publishing Group 2016
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC4726213/
https://www.ncbi.nlm.nih.gov/pubmed/26795751
http://dx.doi.org/10.1038/srep19689
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author Neelam, Srujana
Hayes, Peter Robert
Zhang, Qiao
Dickinson, Richard B.
Lele, Tanmay P.
author_facet Neelam, Srujana
Hayes, Peter Robert
Zhang, Qiao
Dickinson, Richard B.
Lele, Tanmay P.
author_sort Neelam, Srujana
collection PubMed
description Morphological variability in cytoskeletal organization, organelle position and cell boundaries is a common feature of cultured cells. Remarkable uniformity and reproducibility in structure can be accomplished by providing cells with defined geometric cues. Cells in tissues can also self-organize in the absence of directing extracellular cues; however the mechanical principles for such self-organization are not understood. We report that unlike horizontal shapes, the vertical shapes of the cell and nucleus in the z-dimension are uniform in cells in cultured monolayers compared to isolated cells. Apical surfaces of cells and their nuclei in monolayers were flat and heights were uniform. In contrast, isolated cells, or cells with disrupted cell-cell adhesions had nuclei with curved apical surfaces and variable heights. Isolated cells cultured within micron-sized square wells displayed flat cell and nuclear shapes similar to cells in monolayers. Local disruption of nuclear-cytoskeletal linkages resulted in spatial variation in vertical uniformity. These results suggest that competition between cell-cell pulling forces that expand and shorten the vertical cell cross-section, thereby widening and flattening the nucleus, and the resistance of the nucleus to further flattening results in uniform cell and nuclear cross-sections. Our results reveal the mechanical principles of self-organized vertical uniformity in cell monolayers.
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spelling pubmed-47262132016-01-27 Vertical uniformity of cells and nuclei in epithelial monolayers Neelam, Srujana Hayes, Peter Robert Zhang, Qiao Dickinson, Richard B. Lele, Tanmay P. Sci Rep Article Morphological variability in cytoskeletal organization, organelle position and cell boundaries is a common feature of cultured cells. Remarkable uniformity and reproducibility in structure can be accomplished by providing cells with defined geometric cues. Cells in tissues can also self-organize in the absence of directing extracellular cues; however the mechanical principles for such self-organization are not understood. We report that unlike horizontal shapes, the vertical shapes of the cell and nucleus in the z-dimension are uniform in cells in cultured monolayers compared to isolated cells. Apical surfaces of cells and their nuclei in monolayers were flat and heights were uniform. In contrast, isolated cells, or cells with disrupted cell-cell adhesions had nuclei with curved apical surfaces and variable heights. Isolated cells cultured within micron-sized square wells displayed flat cell and nuclear shapes similar to cells in monolayers. Local disruption of nuclear-cytoskeletal linkages resulted in spatial variation in vertical uniformity. These results suggest that competition between cell-cell pulling forces that expand and shorten the vertical cell cross-section, thereby widening and flattening the nucleus, and the resistance of the nucleus to further flattening results in uniform cell and nuclear cross-sections. Our results reveal the mechanical principles of self-organized vertical uniformity in cell monolayers. Nature Publishing Group 2016-01-22 /pmc/articles/PMC4726213/ /pubmed/26795751 http://dx.doi.org/10.1038/srep19689 Text en Copyright © 2016, Macmillan Publishers Limited http://creativecommons.org/licenses/by/4.0/ This work is licensed under a Creative Commons Attribution 4.0 International License. The images or other third party material in this article are included in the article’s Creative Commons license, unless indicated otherwise in the credit line; if the material is not included under the Creative Commons license, users will need to obtain permission from the license holder to reproduce the material. To view a copy of this license, visit http://creativecommons.org/licenses/by/4.0/
spellingShingle Article
Neelam, Srujana
Hayes, Peter Robert
Zhang, Qiao
Dickinson, Richard B.
Lele, Tanmay P.
Vertical uniformity of cells and nuclei in epithelial monolayers
title Vertical uniformity of cells and nuclei in epithelial monolayers
title_full Vertical uniformity of cells and nuclei in epithelial monolayers
title_fullStr Vertical uniformity of cells and nuclei in epithelial monolayers
title_full_unstemmed Vertical uniformity of cells and nuclei in epithelial monolayers
title_short Vertical uniformity of cells and nuclei in epithelial monolayers
title_sort vertical uniformity of cells and nuclei in epithelial monolayers
topic Article
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC4726213/
https://www.ncbi.nlm.nih.gov/pubmed/26795751
http://dx.doi.org/10.1038/srep19689
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