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14-3-3 targets keratin intermediate filaments to mechanically sensitive cell–cell contacts

Intermediate filament (IF) cytoskeletal networks simultaneously support mechanical integrity and influence signal transduction pathways. Marked remodeling of the keratin IF network accompanies collective cellular morphogenetic movements that occur during early embryonic development in the frog Xenop...

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Autores principales: Mariani, Richard A., Paranjpe, Shalaka, Dobrowolski, Radek, Weber, Gregory F.
Formato: Online Artículo Texto
Lenguaje:English
Publicado: The American Society for Cell Biology 2020
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC7185971/
https://www.ncbi.nlm.nih.gov/pubmed/32074004
http://dx.doi.org/10.1091/mbc.E18-06-0373
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author Mariani, Richard A.
Paranjpe, Shalaka
Dobrowolski, Radek
Weber, Gregory F.
author_facet Mariani, Richard A.
Paranjpe, Shalaka
Dobrowolski, Radek
Weber, Gregory F.
author_sort Mariani, Richard A.
collection PubMed
description Intermediate filament (IF) cytoskeletal networks simultaneously support mechanical integrity and influence signal transduction pathways. Marked remodeling of the keratin IF network accompanies collective cellular morphogenetic movements that occur during early embryonic development in the frog Xenopus laevis. While this reorganization of keratin is initiated by force transduction on cell–cell contacts mediated by C-cadherin, the mechanism by which keratin filament reorganization occurs remains poorly understood. In this work, we demonstrate that 14-3-3 proteins regulate keratin reorganization dynamics in embryonic mesendoderm cells from Xenopus gastrula. 14-3-3 colocalizes with keratin filaments near cell–cell junctions in migrating mesendoderm. Coimmunoprecipitation, mass spectrometry, and bioinformatic analyses indicate 14-3-3 is associated with Keratin 19 (K19) in the whole embryo and, more specifically, mesendoderm tissue. Inhibition of 14-3-3 results in both the decreased exchange of keratin subunits into filaments and blocks keratin filament recruitment toward cell–cell contacts. Synthetically coupling 14-3-3 to K19 through a unique fusion construct conversely induces the localization of this keratin population to the region of cell–cell contacts. Taken together, these findings indicate that 14-3-3 acts on keratin IFs and is involved in their reorganization to sites of cell adhesion.
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spelling pubmed-71859712020-06-30 14-3-3 targets keratin intermediate filaments to mechanically sensitive cell–cell contacts Mariani, Richard A. Paranjpe, Shalaka Dobrowolski, Radek Weber, Gregory F. Mol Biol Cell Articles Intermediate filament (IF) cytoskeletal networks simultaneously support mechanical integrity and influence signal transduction pathways. Marked remodeling of the keratin IF network accompanies collective cellular morphogenetic movements that occur during early embryonic development in the frog Xenopus laevis. While this reorganization of keratin is initiated by force transduction on cell–cell contacts mediated by C-cadherin, the mechanism by which keratin filament reorganization occurs remains poorly understood. In this work, we demonstrate that 14-3-3 proteins regulate keratin reorganization dynamics in embryonic mesendoderm cells from Xenopus gastrula. 14-3-3 colocalizes with keratin filaments near cell–cell junctions in migrating mesendoderm. Coimmunoprecipitation, mass spectrometry, and bioinformatic analyses indicate 14-3-3 is associated with Keratin 19 (K19) in the whole embryo and, more specifically, mesendoderm tissue. Inhibition of 14-3-3 results in both the decreased exchange of keratin subunits into filaments and blocks keratin filament recruitment toward cell–cell contacts. Synthetically coupling 14-3-3 to K19 through a unique fusion construct conversely induces the localization of this keratin population to the region of cell–cell contacts. Taken together, these findings indicate that 14-3-3 acts on keratin IFs and is involved in their reorganization to sites of cell adhesion. The American Society for Cell Biology 2020-04-15 /pmc/articles/PMC7185971/ /pubmed/32074004 http://dx.doi.org/10.1091/mbc.E18-06-0373 Text en © 2020 Mariani et al. “ASCB®,” “The American Society for Cell Biology®,” and “Molecular Biology of the Cell®” are registered trademarks of The American Society for Cell Biology. http://creativecommons.org/licenses/by-nc-sa/3.0 This article is distributed by The American Society for Cell Biology under license from the author(s). Two months after publication it is available to the public under an Attribution–Noncommercial–Share Alike 3.0 Unported Creative Commons License.
spellingShingle Articles
Mariani, Richard A.
Paranjpe, Shalaka
Dobrowolski, Radek
Weber, Gregory F.
14-3-3 targets keratin intermediate filaments to mechanically sensitive cell–cell contacts
title 14-3-3 targets keratin intermediate filaments to mechanically sensitive cell–cell contacts
title_full 14-3-3 targets keratin intermediate filaments to mechanically sensitive cell–cell contacts
title_fullStr 14-3-3 targets keratin intermediate filaments to mechanically sensitive cell–cell contacts
title_full_unstemmed 14-3-3 targets keratin intermediate filaments to mechanically sensitive cell–cell contacts
title_short 14-3-3 targets keratin intermediate filaments to mechanically sensitive cell–cell contacts
title_sort 14-3-3 targets keratin intermediate filaments to mechanically sensitive cell–cell contacts
topic Articles
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC7185971/
https://www.ncbi.nlm.nih.gov/pubmed/32074004
http://dx.doi.org/10.1091/mbc.E18-06-0373
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