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Cingulin and actin mediate midbody-dependent apical lumen formation during polarization of epithelial cells

Coordinated polarization of epithelial cells is a key step during morphogenesis that leads to the formation of an apical lumen. Rab11 and its interacting protein FIP5 are necessary for the targeting of apical endosomes to the midbody and apical membrane initiation site (AMIS) during lumenogenesis. H...

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Autores principales: Mangan, Anthony J., Sietsema, Daniel V., Li, Dongying, Moore, Jeffrey K., Citi, Sandra, Prekeris, Rytis
Formato: Online Artículo Texto
Lenguaje:English
Publicado: Nature Publishing Group 2016
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC4976216/
https://www.ncbi.nlm.nih.gov/pubmed/27484926
http://dx.doi.org/10.1038/ncomms12426
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author Mangan, Anthony J.
Sietsema, Daniel V.
Li, Dongying
Moore, Jeffrey K.
Citi, Sandra
Prekeris, Rytis
author_facet Mangan, Anthony J.
Sietsema, Daniel V.
Li, Dongying
Moore, Jeffrey K.
Citi, Sandra
Prekeris, Rytis
author_sort Mangan, Anthony J.
collection PubMed
description Coordinated polarization of epithelial cells is a key step during morphogenesis that leads to the formation of an apical lumen. Rab11 and its interacting protein FIP5 are necessary for the targeting of apical endosomes to the midbody and apical membrane initiation site (AMIS) during lumenogenesis. However, the machinery that mediates AMIS establishment and FIP5-endosome targeting remains unknown. Here we identify a FIP5-interacting protein, Cingulin, which localizes to the AMIS and functions as a tether mediating FIP5-endosome targeting. We analysed the machinery mediating AMIS recruitment to the midbody and determined that both branched actin and microtubules are required for establishing the site of the nascent lumen. We demonstrate that the Rac1-WAVE/Scar complex mediates Cingulin recruitment to the AMIS by inducing branched actin formation, and that Cingulin directly binds to microtubule C-terminal tails through electrostatic interactions. We propose a new mechanism for apical endosome targeting and AMIS formation around the midbody during epithelial lumenogenesis.
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spelling pubmed-49762162016-08-19 Cingulin and actin mediate midbody-dependent apical lumen formation during polarization of epithelial cells Mangan, Anthony J. Sietsema, Daniel V. Li, Dongying Moore, Jeffrey K. Citi, Sandra Prekeris, Rytis Nat Commun Article Coordinated polarization of epithelial cells is a key step during morphogenesis that leads to the formation of an apical lumen. Rab11 and its interacting protein FIP5 are necessary for the targeting of apical endosomes to the midbody and apical membrane initiation site (AMIS) during lumenogenesis. However, the machinery that mediates AMIS establishment and FIP5-endosome targeting remains unknown. Here we identify a FIP5-interacting protein, Cingulin, which localizes to the AMIS and functions as a tether mediating FIP5-endosome targeting. We analysed the machinery mediating AMIS recruitment to the midbody and determined that both branched actin and microtubules are required for establishing the site of the nascent lumen. We demonstrate that the Rac1-WAVE/Scar complex mediates Cingulin recruitment to the AMIS by inducing branched actin formation, and that Cingulin directly binds to microtubule C-terminal tails through electrostatic interactions. We propose a new mechanism for apical endosome targeting and AMIS formation around the midbody during epithelial lumenogenesis. Nature Publishing Group 2016-08-03 /pmc/articles/PMC4976216/ /pubmed/27484926 http://dx.doi.org/10.1038/ncomms12426 Text en Copyright © 2016, The Author(s) http://creativecommons.org/licenses/by/4.0/ This work is licensed under a Creative Commons Attribution 4.0 International License. The images or other third party material in this article are included in the article's Creative Commons license, unless indicated otherwise in the credit line; if the material is not included under the Creative Commons license, users will need to obtain permission from the license holder to reproduce the material. To view a copy of this license, visit http://creativecommons.org/licenses/by/4.0/
spellingShingle Article
Mangan, Anthony J.
Sietsema, Daniel V.
Li, Dongying
Moore, Jeffrey K.
Citi, Sandra
Prekeris, Rytis
Cingulin and actin mediate midbody-dependent apical lumen formation during polarization of epithelial cells
title Cingulin and actin mediate midbody-dependent apical lumen formation during polarization of epithelial cells
title_full Cingulin and actin mediate midbody-dependent apical lumen formation during polarization of epithelial cells
title_fullStr Cingulin and actin mediate midbody-dependent apical lumen formation during polarization of epithelial cells
title_full_unstemmed Cingulin and actin mediate midbody-dependent apical lumen formation during polarization of epithelial cells
title_short Cingulin and actin mediate midbody-dependent apical lumen formation during polarization of epithelial cells
title_sort cingulin and actin mediate midbody-dependent apical lumen formation during polarization of epithelial cells
topic Article
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC4976216/
https://www.ncbi.nlm.nih.gov/pubmed/27484926
http://dx.doi.org/10.1038/ncomms12426
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