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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...
Autores principales: | , , , , |
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Formato: | Online Artículo Texto |
Lenguaje: | English |
Publicado: |
eLife Sciences Publications, Ltd
2020
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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. |
format | Online Article Text |
id | pubmed-7535935 |
institution | National Center for Biotechnology Information |
language | English |
publishDate | 2020 |
publisher | eLife Sciences Publications, Ltd |
record_format | MEDLINE/PubMed |
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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