دورية أكاديمية
Keratins and the plakin family cytolinker proteins control the length of epithelial microridge protrusions.
العنوان: | Keratins and the plakin family cytolinker proteins control the length of epithelial microridge protrusions. |
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المؤلفون: | Inaba Y; Molecular, Cell and Developmental Biology Department and Molecular Biology Institute, University of California, Los Angeles, Los Angeles, United States., Chauhan V; Molecular, Cell and Developmental Biology Department and Molecular Biology Institute, University of California, Los Angeles, Los Angeles, United States., van Loon AP; Molecular, Cell and Developmental Biology Department and Molecular Biology Institute, University of California, Los Angeles, Los Angeles, United States., Choudhury LS; Molecular, Cell and Developmental Biology Department and Molecular Biology Institute, University of California, Los Angeles, Los Angeles, United States., Sagasti A; Molecular, Cell and Developmental Biology Department and Molecular Biology Institute, University of California, Los Angeles, Los Angeles, United States. |
المصدر: | ELife [Elife] 2020 Sep 07; Vol. 9. Date of Electronic Publication: 2020 Sep 07. |
نوع المنشور: | Journal Article; Research Support, N.I.H., Extramural |
اللغة: | English |
بيانات الدورية: | Publisher: eLife Sciences Publications, Ltd Country of Publication: England NLM ID: 101579614 Publication Model: Electronic Cited Medium: Internet ISSN: 2050-084X (Electronic) Linking ISSN: 2050084X NLM ISO Abbreviation: Elife Subsets: MEDLINE |
أسماء مطبوعة: | Original Publication: Cambridge, UK : eLife Sciences Publications, Ltd., 2012- |
مواضيع طبية MeSH: | Cell Surface Extensions*/chemistry , Cell Surface Extensions*/metabolism , Keratins*/chemistry , Keratins*/metabolism , Plakins*/chemistry , Plakins*/metabolism, Animals ; Epithelial Cells/chemistry ; Epithelial Cells/cytology ; Epithelial Cells/metabolism ; Intermediate Filaments/chemistry ; Intermediate Filaments/metabolism ; Membrane Proteins/chemistry ; Membrane Proteins/metabolism ; Protein Precursors/chemistry ; Protein Precursors/metabolism ; Skin/cytology ; Zebrafish ; Zebrafish Proteins/chemistry ; Zebrafish Proteins/metabolism |
مستخلص: | 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. Competing Interests: YI, VC, Av, LC, AS No competing interests declared (© 2020, Inaba et al.) |
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معلومات مُعتمدة: | R01 GM122901 United States GM NIGMS NIH HHS; R21 EY024400 United States EY NEI NIH HHS; T32 GM007185 United States GM NIGMS NIH HHS; GM007185 United States GM NIGMS NIH HHS |
فهرسة مساهمة: | Keywords: Plakin; actin; cell biology; developmental biology; keratin; microridge; morphogenesis; protrusion; zebrafish Local Abstract: [plain-language-summary] Cells adopt a wide array of irregular and bumpy shapes, which are scaffolded by an internal structure called the cytoskeleton. This network of filaments can deform the cell membrane the way tent poles frame a canvas. Cells contain three types of cytoskeleton elements (actin filaments, intermediate filaments, and microtubules), each with unique chemical and mechanical properties. One of the main roles of the cytoskeleton is to create protrusions, a range of structures that ‘stick out’ of a cell to allow movement and interactions with the environment. Both actin filaments and microtubules help form protrusions, but the role of intermediate filaments remains unclear. Microridges are a type of protrusion found on cells covered by mucus, for instance on the surface of the eye, inside the mouth, or on fish skin. These small bumps are organised on the membrane of a cell in fingerprint-like arrangements. Scientists know that actin networks are necessary for microridges to form; yet, many structures supported by actin filaments are not stable over time, suggesting that another component of the cytoskeleton might be lending support. Intermediate filaments are the strongest, most stable type of cytoskeleton element, and they can connect to actin filaments via linker proteins. However, research has yet to show that this kind of cooperation happens in any membrane protrusion. Here, Inaba et al. used high-resolution microscopy to monitor microridge development in the skin of live fish. In particular, they focused on a type of intermediate filaments known as keratin filaments. This revealed that, inside microridges, the keratin and actin networks form alongside each other, with linker proteins called Envoplakin and Periplakin connecting the two structures together. Genetic experiments revealed that Envoplakin and Periplakin must attach to actin for microridges to start forming. However, the two proteins bind to keratin for protrusions to grow. This work therefore highlights how intermediate filaments and linker proteins contribute to the formation of these structures. Many tissues must be covered in mucus to remain moist and healthy. As microridges likely contribute to mucus retention, the findings by Inaba et al. may help to better understand how disorders linked to problems in mucus emerge. |
المشرفين على المادة: | 0 (Membrane Proteins) 0 (Plakins) 0 (Protein Precursors) 0 (Zebrafish Proteins) 0 (envoplakin) 68238-35-7 (Keratins) |
تواريخ الأحداث: | Date Created: 20200907 Date Completed: 20210317 Latest Revision: 20210317 |
رمز التحديث: | 20221213 |
مُعرف محوري في PubMed: | PMC7535935 |
DOI: | 10.7554/eLife.58149 |
PMID: | 32894222 |
قاعدة البيانات: | MEDLINE |
تدمد: | 2050-084X |
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DOI: | 10.7554/eLife.58149 |