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...
| Main Authors: | , , , , |
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| Format: | Article |
| Language: | English |
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eLife Sciences Publications Ltd
2020-09-01
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| Series: | eLife |
| Subjects: | |
| Online Access: | https://elifesciences.org/articles/58149 |
| _version_ | 1811200867370532864 |
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| author | Yasuko Inaba Vasudha Chauhan Aaron Paul van Loon Lamia Saiyara Choudhury Alvaro Sagasti |
| author_facet | Yasuko Inaba Vasudha Chauhan Aaron Paul van Loon Lamia Saiyara Choudhury Alvaro Sagasti |
| author_sort | Yasuko Inaba |
| collection | DOAJ |
| 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. |
| first_indexed | 2024-04-12T02:10:53Z |
| format | Article |
| id | doaj.art-29b0840fd46346ff9c29d04f791f0492 |
| institution | Directory Open Access Journal |
| issn | 2050-084X |
| language | English |
| last_indexed | 2024-04-12T02:10:53Z |
| publishDate | 2020-09-01 |
| publisher | eLife Sciences Publications Ltd |
| record_format | Article |
| series | eLife |
| spelling | doaj.art-29b0840fd46346ff9c29d04f791f04922022-12-22T03:52:23ZengeLife Sciences Publications LtdeLife2050-084X2020-09-01910.7554/eLife.58149Keratins and plakin family cytolinker proteins control the length of epithelial microridge protrusionsYasuko Inaba0https://orcid.org/0000-0002-3239-2075Vasudha Chauhan1Aaron Paul van Loon2Lamia Saiyara Choudhury3Alvaro Sagasti4https://orcid.org/0000-0002-6823-0692Molecular, Cell and Developmental Biology Department and Molecular Biology Institute, University of California, Los Angeles, Los Angeles, United StatesMolecular, Cell and Developmental Biology Department and Molecular Biology Institute, University of California, Los Angeles, Los Angeles, United StatesMolecular, Cell and Developmental Biology Department and Molecular Biology Institute, University of California, Los Angeles, Los Angeles, United StatesMolecular, Cell and Developmental Biology Department and Molecular Biology Institute, University of California, Los Angeles, Los Angeles, United StatesMolecular, Cell and Developmental Biology Department and Molecular Biology Institute, University of California, Los Angeles, Los Angeles, United StatesActin 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.https://elifesciences.org/articles/58149keratinactinPlakinmorphogenesisprotrusionmicroridge |
| spellingShingle | Yasuko Inaba Vasudha Chauhan Aaron Paul van Loon Lamia Saiyara Choudhury Alvaro Sagasti Keratins and plakin family cytolinker proteins control the length of epithelial microridge protrusions eLife keratin actin Plakin morphogenesis protrusion microridge |
| 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 | keratin actin Plakin morphogenesis protrusion microridge |
| url | https://elifesciences.org/articles/58149 |
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