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Cell and tissue morphology determine actin-dependent nuclear migration mechanisms in neuroepithelia
Correct nuclear position is crucial for cellular function and tissue development. Depending on cell context, however, the cytoskeletal elements responsible for nuclear positioning vary. While these cytoskeletal mechanisms have been intensely studied in single cells, how nuclear positioning is linked...
Autores principales: | , , , , |
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Formato: | Online Artículo Texto |
Lenguaje: | English |
Publicado: |
Rockefeller University Press
2019
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Materias: | |
Acceso en línea: | https://www.ncbi.nlm.nih.gov/pmc/articles/PMC6781452/ https://www.ncbi.nlm.nih.gov/pubmed/31420451 http://dx.doi.org/10.1083/jcb.201901077 |
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author | Yanakieva, Iskra Erzberger, Anna Matejčić, Marija Modes, Carl D. Norden, Caren |
author_facet | Yanakieva, Iskra Erzberger, Anna Matejčić, Marija Modes, Carl D. Norden, Caren |
author_sort | Yanakieva, Iskra |
collection | PubMed |
description | Correct nuclear position is crucial for cellular function and tissue development. Depending on cell context, however, the cytoskeletal elements responsible for nuclear positioning vary. While these cytoskeletal mechanisms have been intensely studied in single cells, how nuclear positioning is linked to tissue morphology is less clear. Here, we compare apical nuclear positioning in zebrafish neuroepithelia. We find that kinetics and actin-dependent mechanisms of nuclear positioning vary in tissues of different morphology. In straight neuroepithelia, nuclear positioning is controlled by Rho-ROCK–dependent myosin contractility. In contrast, in basally constricted neuroepithelia, a novel formin-dependent pushing mechanism is found for which we propose a proof-of-principle force generation theory. Overall, our data suggest that correct nuclear positioning is ensured by the adaptability of the cytoskeleton to cell and tissue shape. This in turn leads to robust epithelial maturation across geometries. The conclusion that different nuclear positioning mechanisms are favored in tissues of different morphology highlights the importance of developmental context for the execution of intracellular processes. |
format | Online Article Text |
id | pubmed-6781452 |
institution | National Center for Biotechnology Information |
language | English |
publishDate | 2019 |
publisher | Rockefeller University Press |
record_format | MEDLINE/PubMed |
spelling | pubmed-67814522020-04-07 Cell and tissue morphology determine actin-dependent nuclear migration mechanisms in neuroepithelia Yanakieva, Iskra Erzberger, Anna Matejčić, Marija Modes, Carl D. Norden, Caren J Cell Biol Research Articles Correct nuclear position is crucial for cellular function and tissue development. Depending on cell context, however, the cytoskeletal elements responsible for nuclear positioning vary. While these cytoskeletal mechanisms have been intensely studied in single cells, how nuclear positioning is linked to tissue morphology is less clear. Here, we compare apical nuclear positioning in zebrafish neuroepithelia. We find that kinetics and actin-dependent mechanisms of nuclear positioning vary in tissues of different morphology. In straight neuroepithelia, nuclear positioning is controlled by Rho-ROCK–dependent myosin contractility. In contrast, in basally constricted neuroepithelia, a novel formin-dependent pushing mechanism is found for which we propose a proof-of-principle force generation theory. Overall, our data suggest that correct nuclear positioning is ensured by the adaptability of the cytoskeleton to cell and tissue shape. This in turn leads to robust epithelial maturation across geometries. The conclusion that different nuclear positioning mechanisms are favored in tissues of different morphology highlights the importance of developmental context for the execution of intracellular processes. Rockefeller University Press 2019-10-07 2019-08-16 /pmc/articles/PMC6781452/ /pubmed/31420451 http://dx.doi.org/10.1083/jcb.201901077 Text en © 2019 Yanakieva et al. http://www.rupress.org/terms/https://creativecommons.org/licenses/by-nc-sa/4.0/This article is distributed under the terms of an Attribution–Noncommercial–Share Alike–No Mirror Sites license for the first six months after the publication date (see http://www.rupress.org/terms/). After six months it is available under a Creative Commons License (Attribution–Noncommercial–Share Alike 4.0 International license, as described at https://creativecommons.org/licenses/by-nc-sa/4.0/). |
spellingShingle | Research Articles Yanakieva, Iskra Erzberger, Anna Matejčić, Marija Modes, Carl D. Norden, Caren Cell and tissue morphology determine actin-dependent nuclear migration mechanisms in neuroepithelia |
title | Cell and tissue morphology determine actin-dependent nuclear migration mechanisms in neuroepithelia |
title_full | Cell and tissue morphology determine actin-dependent nuclear migration mechanisms in neuroepithelia |
title_fullStr | Cell and tissue morphology determine actin-dependent nuclear migration mechanisms in neuroepithelia |
title_full_unstemmed | Cell and tissue morphology determine actin-dependent nuclear migration mechanisms in neuroepithelia |
title_short | Cell and tissue morphology determine actin-dependent nuclear migration mechanisms in neuroepithelia |
title_sort | cell and tissue morphology determine actin-dependent nuclear migration mechanisms in neuroepithelia |
topic | Research Articles |
url | https://www.ncbi.nlm.nih.gov/pmc/articles/PMC6781452/ https://www.ncbi.nlm.nih.gov/pubmed/31420451 http://dx.doi.org/10.1083/jcb.201901077 |
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