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Mechanical forces drive ordered patterning of hair cells in the mammalian inner ear

Periodic organization of cells is required for the function of many organs and tissues. The development of such periodic patterns is typically associated with mechanisms based on intercellular signaling such as lateral inhibition and Turing patterning. Here we show that the transition from disordere...

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Autores principales: Cohen, Roie, Amir-Zilberstein, Liat, Hersch, Micha, Woland, Shiran, Loza, Olga, Taiber, Shahar, Matsuzaki, Fumio, Bergmann, Sven, Avraham, Karen B., Sprinzak, David
Formato: Online Artículo Texto
Lenguaje:English
Publicado: Nature Publishing Group UK 2020
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC7550578/
https://www.ncbi.nlm.nih.gov/pubmed/33046691
http://dx.doi.org/10.1038/s41467-020-18894-8
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author Cohen, Roie
Amir-Zilberstein, Liat
Hersch, Micha
Woland, Shiran
Loza, Olga
Taiber, Shahar
Matsuzaki, Fumio
Bergmann, Sven
Avraham, Karen B.
Sprinzak, David
author_facet Cohen, Roie
Amir-Zilberstein, Liat
Hersch, Micha
Woland, Shiran
Loza, Olga
Taiber, Shahar
Matsuzaki, Fumio
Bergmann, Sven
Avraham, Karen B.
Sprinzak, David
author_sort Cohen, Roie
collection PubMed
description Periodic organization of cells is required for the function of many organs and tissues. The development of such periodic patterns is typically associated with mechanisms based on intercellular signaling such as lateral inhibition and Turing patterning. Here we show that the transition from disordered to ordered checkerboard-like pattern of hair cells and supporting cells in the mammalian hearing organ, the organ of Corti, is likely based on mechanical forces rather than signaling events. Using time-lapse imaging of mouse cochlear explants, we show that hair cells rearrange gradually into a checkerboard-like pattern through a tissue-wide shear motion that coordinates intercalation and delamination events. Using mechanical models of the tissue, we show that global shear and local repulsion forces on hair cells are sufficient to drive the transition from disordered to ordered cellular pattern. Our findings suggest that mechanical forces drive ordered hair cell patterning in a process strikingly analogous to the process of shear-induced crystallization in polymer and granular physics.
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spelling pubmed-75505782020-10-19 Mechanical forces drive ordered patterning of hair cells in the mammalian inner ear Cohen, Roie Amir-Zilberstein, Liat Hersch, Micha Woland, Shiran Loza, Olga Taiber, Shahar Matsuzaki, Fumio Bergmann, Sven Avraham, Karen B. Sprinzak, David Nat Commun Article Periodic organization of cells is required for the function of many organs and tissues. The development of such periodic patterns is typically associated with mechanisms based on intercellular signaling such as lateral inhibition and Turing patterning. Here we show that the transition from disordered to ordered checkerboard-like pattern of hair cells and supporting cells in the mammalian hearing organ, the organ of Corti, is likely based on mechanical forces rather than signaling events. Using time-lapse imaging of mouse cochlear explants, we show that hair cells rearrange gradually into a checkerboard-like pattern through a tissue-wide shear motion that coordinates intercalation and delamination events. Using mechanical models of the tissue, we show that global shear and local repulsion forces on hair cells are sufficient to drive the transition from disordered to ordered cellular pattern. Our findings suggest that mechanical forces drive ordered hair cell patterning in a process strikingly analogous to the process of shear-induced crystallization in polymer and granular physics. Nature Publishing Group UK 2020-10-12 /pmc/articles/PMC7550578/ /pubmed/33046691 http://dx.doi.org/10.1038/s41467-020-18894-8 Text en © The Author(s) 2020 Open Access This article is licensed under a Creative Commons Attribution 4.0 International License, which permits use, sharing, adaptation, distribution and reproduction in any medium or format, as long as you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons license, and indicate if changes were made. The images or other third party material in this article are included in the article’s Creative Commons license, unless indicated otherwise in a credit line to the material. If material is not included in the article’s Creative Commons license and your intended use is not permitted by statutory regulation or exceeds the permitted use, you will need to obtain permission directly from the copyright holder. To view a copy of this license, visit http://creativecommons.org/licenses/by/4.0/.
spellingShingle Article
Cohen, Roie
Amir-Zilberstein, Liat
Hersch, Micha
Woland, Shiran
Loza, Olga
Taiber, Shahar
Matsuzaki, Fumio
Bergmann, Sven
Avraham, Karen B.
Sprinzak, David
Mechanical forces drive ordered patterning of hair cells in the mammalian inner ear
title Mechanical forces drive ordered patterning of hair cells in the mammalian inner ear
title_full Mechanical forces drive ordered patterning of hair cells in the mammalian inner ear
title_fullStr Mechanical forces drive ordered patterning of hair cells in the mammalian inner ear
title_full_unstemmed Mechanical forces drive ordered patterning of hair cells in the mammalian inner ear
title_short Mechanical forces drive ordered patterning of hair cells in the mammalian inner ear
title_sort mechanical forces drive ordered patterning of hair cells in the mammalian inner ear
topic Article
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC7550578/
https://www.ncbi.nlm.nih.gov/pubmed/33046691
http://dx.doi.org/10.1038/s41467-020-18894-8
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