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Crumbs complex–directed apical membrane dynamics in epithelial cell ingression

Epithelial cells often leave their tissue context and ingress to form new cell types or acquire migratory ability to move to distant sites during development and tumor progression. Cells lose their apical membrane and epithelial adherens junctions during ingression. However, how factors that organiz...

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Autores principales: Simões, Sérgio, Lerchbaumer, Gerald, Pellikka, Milena, Giannatou, Paraskevi, Lam, Thomas, Kim, Dohyun, Yu, Jessica, ter Stal, David, Al Kakouni, Kenana, Fernandez-Gonzalez, Rodrigo, Tepass, Ulrich
Formato: Online Artículo Texto
Lenguaje:English
Publicado: Rockefeller University Press 2022
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC9123285/
https://www.ncbi.nlm.nih.gov/pubmed/35588693
http://dx.doi.org/10.1083/jcb.202108076
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author Simões, Sérgio
Lerchbaumer, Gerald
Pellikka, Milena
Giannatou, Paraskevi
Lam, Thomas
Kim, Dohyun
Yu, Jessica
ter Stal, David
Al Kakouni, Kenana
Fernandez-Gonzalez, Rodrigo
Tepass, Ulrich
author_facet Simões, Sérgio
Lerchbaumer, Gerald
Pellikka, Milena
Giannatou, Paraskevi
Lam, Thomas
Kim, Dohyun
Yu, Jessica
ter Stal, David
Al Kakouni, Kenana
Fernandez-Gonzalez, Rodrigo
Tepass, Ulrich
author_sort Simões, Sérgio
collection PubMed
description Epithelial cells often leave their tissue context and ingress to form new cell types or acquire migratory ability to move to distant sites during development and tumor progression. Cells lose their apical membrane and epithelial adherens junctions during ingression. However, how factors that organize apical–basal polarity contribute to ingression is unknown. Here, we show that the dynamic regulation of the apical Crumbs polarity complex is crucial for normal neural stem cell ingression. Crumbs endocytosis and recycling allow ingression to occur in a normal timeframe. During early ingression, Crumbs and its complex partner the RhoGEF Cysts support myosin and apical constriction to ensure robust ingression dynamics. During late ingression, the E3-ubiquitin ligase Neuralized facilitates the disassembly of the Crumbs complex and the rapid endocytic removal of the apical cell domain. Our findings reveal a mechanism integrating cell fate, apical polarity, endocytosis, vesicle trafficking, and actomyosin contractility to promote cell ingression, a fundamental morphogenetic process observed in animal development and cancer.
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spelling pubmed-91232852023-01-04 Crumbs complex–directed apical membrane dynamics in epithelial cell ingression Simões, Sérgio Lerchbaumer, Gerald Pellikka, Milena Giannatou, Paraskevi Lam, Thomas Kim, Dohyun Yu, Jessica ter Stal, David Al Kakouni, Kenana Fernandez-Gonzalez, Rodrigo Tepass, Ulrich J Cell Biol Article Epithelial cells often leave their tissue context and ingress to form new cell types or acquire migratory ability to move to distant sites during development and tumor progression. Cells lose their apical membrane and epithelial adherens junctions during ingression. However, how factors that organize apical–basal polarity contribute to ingression is unknown. Here, we show that the dynamic regulation of the apical Crumbs polarity complex is crucial for normal neural stem cell ingression. Crumbs endocytosis and recycling allow ingression to occur in a normal timeframe. During early ingression, Crumbs and its complex partner the RhoGEF Cysts support myosin and apical constriction to ensure robust ingression dynamics. During late ingression, the E3-ubiquitin ligase Neuralized facilitates the disassembly of the Crumbs complex and the rapid endocytic removal of the apical cell domain. Our findings reveal a mechanism integrating cell fate, apical polarity, endocytosis, vesicle trafficking, and actomyosin contractility to promote cell ingression, a fundamental morphogenetic process observed in animal development and cancer. Rockefeller University Press 2022-05-19 /pmc/articles/PMC9123285/ /pubmed/35588693 http://dx.doi.org/10.1083/jcb.202108076 Text en © 2022 Simoes et al. https://creativecommons.org/licenses/by-nc-sa/4.0/http://www.rupress.org/terms/This article is distributed under the terms of an Attribution–Noncommercial–Share Alike–No Mirror Sites license for the first six months after the publication date (see http://www.rupress.org/terms/). After six months it is available under a Creative Commons License (Attribution–Noncommercial–Share Alike 4.0 International license, as described at https://creativecommons.org/licenses/by-nc-sa/4.0/).
spellingShingle Article
Simões, Sérgio
Lerchbaumer, Gerald
Pellikka, Milena
Giannatou, Paraskevi
Lam, Thomas
Kim, Dohyun
Yu, Jessica
ter Stal, David
Al Kakouni, Kenana
Fernandez-Gonzalez, Rodrigo
Tepass, Ulrich
Crumbs complex–directed apical membrane dynamics in epithelial cell ingression
title Crumbs complex–directed apical membrane dynamics in epithelial cell ingression
title_full Crumbs complex–directed apical membrane dynamics in epithelial cell ingression
title_fullStr Crumbs complex–directed apical membrane dynamics in epithelial cell ingression
title_full_unstemmed Crumbs complex–directed apical membrane dynamics in epithelial cell ingression
title_short Crumbs complex–directed apical membrane dynamics in epithelial cell ingression
title_sort crumbs complex–directed apical membrane dynamics in epithelial cell ingression
topic Article
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC9123285/
https://www.ncbi.nlm.nih.gov/pubmed/35588693
http://dx.doi.org/10.1083/jcb.202108076
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