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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...

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Detalles Bibliográficos
Autores principales: Yanakieva, Iskra, Erzberger, Anna, Matejčić, Marija, Modes, Carl D., Norden, Caren
Formato: Online Artículo Texto
Lenguaje:English
Publicado: Rockefeller University Press 2019
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.
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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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