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Vesicular trafficking plays a role in centriole disengagement and duplication

Centrosomes are the major microtubule-nucleating and microtubule-organizing centers of cells and play crucial roles in microtubule anchoring, organelle positioning, and ciliogenesis. At the centrosome core lies a tightly associated or “engaged” mother–daughter centriole pair.  During mitotic exit, r...

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Autores principales: Xie, Shuwei, Reinecke, James B., Farmer, Trey, Bahl, Kriti, Yeow, Ivana, Nichols, Benjamin J., McLamarrah, Tiffany A., Naslavsky, Naava, Rogers, Gregory C., Caplan, Steve
Formato: Online Artículo Texto
Lenguaje:English
Publicado: The American Society for Cell Biology 2018
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC6249839/
https://www.ncbi.nlm.nih.gov/pubmed/30188792
http://dx.doi.org/10.1091/mbc.E18-04-0241
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author Xie, Shuwei
Reinecke, James B.
Farmer, Trey
Bahl, Kriti
Yeow, Ivana
Nichols, Benjamin J.
McLamarrah, Tiffany A.
Naslavsky, Naava
Rogers, Gregory C.
Caplan, Steve
author_facet Xie, Shuwei
Reinecke, James B.
Farmer, Trey
Bahl, Kriti
Yeow, Ivana
Nichols, Benjamin J.
McLamarrah, Tiffany A.
Naslavsky, Naava
Rogers, Gregory C.
Caplan, Steve
author_sort Xie, Shuwei
collection PubMed
description Centrosomes are the major microtubule-nucleating and microtubule-organizing centers of cells and play crucial roles in microtubule anchoring, organelle positioning, and ciliogenesis. At the centrosome core lies a tightly associated or “engaged” mother–daughter centriole pair.  During mitotic exit, removal of centrosomal proteins pericentrin and Cep215 promotes “disengagement” by the dissolution of intercentriolar linkers, ensuring a single centriole duplication event per cell cycle.  Herein, we explore a new mechanism involving vesicular trafficking for the removal of centrosomal Cep215. Using small interfering RNA and CRISPR/Cas9 gene-edited cells, we show that the endocytic protein EHD1 regulates Cep215 transport from centrosomes to the spindle midbody, thus facilitating disengagement and duplication. We demonstrate that EHD1 and Cep215 interact and show that Cep215 displays increased localization to vesicles containing EHD1 during mitosis. Moreover, Cep215-containing vesicles are positive for internalized transferrin, demonstrating their endocytic origin. Thus, we describe a novel relationship between endocytic trafficking and the centrosome cycle, whereby vesicles of endocytic origin are used to remove key regulatory proteins from centrosomes to control centriole duplication.
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spelling pubmed-62498392019-01-16 Vesicular trafficking plays a role in centriole disengagement and duplication Xie, Shuwei Reinecke, James B. Farmer, Trey Bahl, Kriti Yeow, Ivana Nichols, Benjamin J. McLamarrah, Tiffany A. Naslavsky, Naava Rogers, Gregory C. Caplan, Steve Mol Biol Cell Brief Report Centrosomes are the major microtubule-nucleating and microtubule-organizing centers of cells and play crucial roles in microtubule anchoring, organelle positioning, and ciliogenesis. At the centrosome core lies a tightly associated or “engaged” mother–daughter centriole pair.  During mitotic exit, removal of centrosomal proteins pericentrin and Cep215 promotes “disengagement” by the dissolution of intercentriolar linkers, ensuring a single centriole duplication event per cell cycle.  Herein, we explore a new mechanism involving vesicular trafficking for the removal of centrosomal Cep215. Using small interfering RNA and CRISPR/Cas9 gene-edited cells, we show that the endocytic protein EHD1 regulates Cep215 transport from centrosomes to the spindle midbody, thus facilitating disengagement and duplication. We demonstrate that EHD1 and Cep215 interact and show that Cep215 displays increased localization to vesicles containing EHD1 during mitosis. Moreover, Cep215-containing vesicles are positive for internalized transferrin, demonstrating their endocytic origin. Thus, we describe a novel relationship between endocytic trafficking and the centrosome cycle, whereby vesicles of endocytic origin are used to remove key regulatory proteins from centrosomes to control centriole duplication. The American Society for Cell Biology 2018-11-01 /pmc/articles/PMC6249839/ /pubmed/30188792 http://dx.doi.org/10.1091/mbc.E18-04-0241 Text en © 2018 Xie, Reinecke, 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. http://creativecommons.org/licenses/by-nc-sa/3.0 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 3.0 Unported Creative Commons License.
spellingShingle Brief Report
Xie, Shuwei
Reinecke, James B.
Farmer, Trey
Bahl, Kriti
Yeow, Ivana
Nichols, Benjamin J.
McLamarrah, Tiffany A.
Naslavsky, Naava
Rogers, Gregory C.
Caplan, Steve
Vesicular trafficking plays a role in centriole disengagement and duplication
title Vesicular trafficking plays a role in centriole disengagement and duplication
title_full Vesicular trafficking plays a role in centriole disengagement and duplication
title_fullStr Vesicular trafficking plays a role in centriole disengagement and duplication
title_full_unstemmed Vesicular trafficking plays a role in centriole disengagement and duplication
title_short Vesicular trafficking plays a role in centriole disengagement and duplication
title_sort vesicular trafficking plays a role in centriole disengagement and duplication
topic Brief Report
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC6249839/
https://www.ncbi.nlm.nih.gov/pubmed/30188792
http://dx.doi.org/10.1091/mbc.E18-04-0241
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