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Keratins and plakin family cytolinker proteins control the length of epithelial microridge protrusions

Actin filaments and microtubules create diverse cellular protrusions, but intermediate filaments, the strongest and most stable cytoskeletal elements, are not known to directly participate in the formation of protrusions. Here we show that keratin intermediate filaments directly regulate the morphog...

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Autores principales: Inaba, Yasuko, Chauhan, Vasudha, van Loon, Aaron Paul, Choudhury, Lamia Saiyara, Sagasti, Alvaro
Formato: Online Artículo Texto
Lenguaje:English
Publicado: eLife Sciences Publications, Ltd 2020
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC7535935/
https://www.ncbi.nlm.nih.gov/pubmed/32894222
http://dx.doi.org/10.7554/eLife.58149
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author Inaba, Yasuko
Chauhan, Vasudha
van Loon, Aaron Paul
Choudhury, Lamia Saiyara
Sagasti, Alvaro
author_facet Inaba, Yasuko
Chauhan, Vasudha
van Loon, Aaron Paul
Choudhury, Lamia Saiyara
Sagasti, Alvaro
author_sort Inaba, Yasuko
collection PubMed
description Actin filaments and microtubules create diverse cellular protrusions, but intermediate filaments, the strongest and most stable cytoskeletal elements, are not known to directly participate in the formation of protrusions. Here we show that keratin intermediate filaments directly regulate the morphogenesis of microridges, elongated protrusions arranged in elaborate maze-like patterns on the surface of mucosal epithelial cells. We found that microridges on zebrafish skin cells contained both actin and keratin filaments. Keratin filaments stabilized microridges, and overexpressing keratins lengthened them. Envoplakin and periplakin, plakin family cytolinkers that bind F-actin and keratins, localized to microridges, and were required for their morphogenesis. Strikingly, plakin protein levels directly dictate microridge length. An actin-binding domain of periplakin was required to initiate microridge morphogenesis, whereas periplakin-keratin binding was required to elongate microridges. These findings separate microridge morphogenesis into distinct steps, expand our understanding of intermediate filament functions, and identify microridges as protrusions that integrate actin and intermediate filaments.
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spelling pubmed-75359352020-10-07 Keratins and plakin family cytolinker proteins control the length of epithelial microridge protrusions Inaba, Yasuko Chauhan, Vasudha van Loon, Aaron Paul Choudhury, Lamia Saiyara Sagasti, Alvaro eLife Cell Biology Actin filaments and microtubules create diverse cellular protrusions, but intermediate filaments, the strongest and most stable cytoskeletal elements, are not known to directly participate in the formation of protrusions. Here we show that keratin intermediate filaments directly regulate the morphogenesis of microridges, elongated protrusions arranged in elaborate maze-like patterns on the surface of mucosal epithelial cells. We found that microridges on zebrafish skin cells contained both actin and keratin filaments. Keratin filaments stabilized microridges, and overexpressing keratins lengthened them. Envoplakin and periplakin, plakin family cytolinkers that bind F-actin and keratins, localized to microridges, and were required for their morphogenesis. Strikingly, plakin protein levels directly dictate microridge length. An actin-binding domain of periplakin was required to initiate microridge morphogenesis, whereas periplakin-keratin binding was required to elongate microridges. These findings separate microridge morphogenesis into distinct steps, expand our understanding of intermediate filament functions, and identify microridges as protrusions that integrate actin and intermediate filaments. eLife Sciences Publications, Ltd 2020-09-07 /pmc/articles/PMC7535935/ /pubmed/32894222 http://dx.doi.org/10.7554/eLife.58149 Text en © 2020, Inaba et al http://creativecommons.org/licenses/by/4.0/ http://creativecommons.org/licenses/by/4.0/This article is distributed under the terms of the Creative Commons Attribution License (http://creativecommons.org/licenses/by/4.0/) , which permits unrestricted use and redistribution provided that the original author and source are credited.
spellingShingle Cell Biology
Inaba, Yasuko
Chauhan, Vasudha
van Loon, Aaron Paul
Choudhury, Lamia Saiyara
Sagasti, Alvaro
Keratins and plakin family cytolinker proteins control the length of epithelial microridge protrusions
title Keratins and plakin family cytolinker proteins control the length of epithelial microridge protrusions
title_full Keratins and plakin family cytolinker proteins control the length of epithelial microridge protrusions
title_fullStr Keratins and plakin family cytolinker proteins control the length of epithelial microridge protrusions
title_full_unstemmed Keratins and plakin family cytolinker proteins control the length of epithelial microridge protrusions
title_short Keratins and plakin family cytolinker proteins control the length of epithelial microridge protrusions
title_sort keratins and plakin family cytolinker proteins control the length of epithelial microridge protrusions
topic Cell Biology
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC7535935/
https://www.ncbi.nlm.nih.gov/pubmed/32894222
http://dx.doi.org/10.7554/eLife.58149
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