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Sensory axons induce epithelial lipid microdomain remodeling and determine the distribution of junctions in the epidermis
Epithelial cell properties are determined by the polarized distribution of membrane lipids, the cytoskeleton, and adhesive junctions. Epithelia are often profusely innervated, but little work has addressed how neurites affect epithelial organization. We previously found that basal keratinocytes in t...
Autores principales: | , , |
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Formato: | Online Artículo Texto |
Lenguaje: | English |
Publicado: |
The American Society for Cell Biology
2022
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Materias: | |
Acceso en línea: | https://www.ncbi.nlm.nih.gov/pmc/articles/PMC9816649/ https://www.ncbi.nlm.nih.gov/pubmed/36322392 http://dx.doi.org/10.1091/mbc.E22-09-0396 |
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author | Rosa, Jeffrey B. Nassman, Khaled Y. Sagasti, Alvaro |
author_facet | Rosa, Jeffrey B. Nassman, Khaled Y. Sagasti, Alvaro |
author_sort | Rosa, Jeffrey B. |
collection | PubMed |
description | Epithelial cell properties are determined by the polarized distribution of membrane lipids, the cytoskeleton, and adhesive junctions. Epithelia are often profusely innervated, but little work has addressed how neurites affect epithelial organization. We previously found that basal keratinocytes in the zebrafish epidermis enclose axons in ensheathment channels sealed by autotypic junctions. Here we characterized how axons remodel cell membranes, the cytoskeleton, and junctions in basal keratinocytes. At the apical surface of basal keratinocytes, axons organized lipid microdomains quantitatively enriched in reporters for PI(4,5)P2 and liquid-ordered (Lo) membranes. Lipid microdomains supported the formation of cadherin-enriched, F-actin protrusions, which wrapped around axons, likely initiating ensheathment. In the absence of axons, cadherin-enriched microdomains formed on basal cells but did not organize into contiguous domains. Instead, these isolated domains formed heterotypic junctions with periderm cells, a distinct epithelial cell type. Thus, axon endings dramatically remodel polarized epithelial components and regulate epidermal adhesion. |
format | Online Article Text |
id | pubmed-9816649 |
institution | National Center for Biotechnology Information |
language | English |
publishDate | 2022 |
publisher | The American Society for Cell Biology |
record_format | MEDLINE/PubMed |
spelling | pubmed-98166492023-03-02 Sensory axons induce epithelial lipid microdomain remodeling and determine the distribution of junctions in the epidermis Rosa, Jeffrey B. Nassman, Khaled Y. Sagasti, Alvaro Mol Biol Cell Articles Epithelial cell properties are determined by the polarized distribution of membrane lipids, the cytoskeleton, and adhesive junctions. Epithelia are often profusely innervated, but little work has addressed how neurites affect epithelial organization. We previously found that basal keratinocytes in the zebrafish epidermis enclose axons in ensheathment channels sealed by autotypic junctions. Here we characterized how axons remodel cell membranes, the cytoskeleton, and junctions in basal keratinocytes. At the apical surface of basal keratinocytes, axons organized lipid microdomains quantitatively enriched in reporters for PI(4,5)P2 and liquid-ordered (Lo) membranes. Lipid microdomains supported the formation of cadherin-enriched, F-actin protrusions, which wrapped around axons, likely initiating ensheathment. In the absence of axons, cadherin-enriched microdomains formed on basal cells but did not organize into contiguous domains. Instead, these isolated domains formed heterotypic junctions with periderm cells, a distinct epithelial cell type. Thus, axon endings dramatically remodel polarized epithelial components and regulate epidermal adhesion. The American Society for Cell Biology 2022-12-15 /pmc/articles/PMC9816649/ /pubmed/36322392 http://dx.doi.org/10.1091/mbc.E22-09-0396 Text en © 2023 Rosa 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. https://creativecommons.org/licenses/by-nc-sa/4.0/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 4.0 International Creative Commons License. |
spellingShingle | Articles Rosa, Jeffrey B. Nassman, Khaled Y. Sagasti, Alvaro Sensory axons induce epithelial lipid microdomain remodeling and determine the distribution of junctions in the epidermis |
title | Sensory axons induce epithelial lipid microdomain remodeling and determine the distribution of junctions in the epidermis |
title_full | Sensory axons induce epithelial lipid microdomain remodeling and determine the distribution of junctions in the epidermis |
title_fullStr | Sensory axons induce epithelial lipid microdomain remodeling and determine the distribution of junctions in the epidermis |
title_full_unstemmed | Sensory axons induce epithelial lipid microdomain remodeling and determine the distribution of junctions in the epidermis |
title_short | Sensory axons induce epithelial lipid microdomain remodeling and determine the distribution of junctions in the epidermis |
title_sort | sensory axons induce epithelial lipid microdomain remodeling and determine the distribution of junctions in the epidermis |
topic | Articles |
url | https://www.ncbi.nlm.nih.gov/pmc/articles/PMC9816649/ https://www.ncbi.nlm.nih.gov/pubmed/36322392 http://dx.doi.org/10.1091/mbc.E22-09-0396 |
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