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Cartwheel disassembly regulated by CDK1-cyclin B kinase allows human centriole disengagement and licensing

Cartwheel assembly is considered the first step in the initiation of procentriole biogenesis; however, the reason for persistence of the assembled human cartwheel structure from S phase to late mitosis remains unclear. Here, we demonstrate mainly using cell synchronization, RNA interference, immunof...

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Autores principales: Huang, Fan, Xu, Xiaowei, Xin, Guangwei, Zhang, Boyan, Jiang, Qing, Zhang, Chuanmao
Formato: Online Artículo Texto
Lenguaje:English
Publicado: American Society for Biochemistry and Molecular Biology 2022
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC9763691/
https://www.ncbi.nlm.nih.gov/pubmed/36356903
http://dx.doi.org/10.1016/j.jbc.2022.102658
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author Huang, Fan
Xu, Xiaowei
Xin, Guangwei
Zhang, Boyan
Jiang, Qing
Zhang, Chuanmao
author_facet Huang, Fan
Xu, Xiaowei
Xin, Guangwei
Zhang, Boyan
Jiang, Qing
Zhang, Chuanmao
author_sort Huang, Fan
collection PubMed
description Cartwheel assembly is considered the first step in the initiation of procentriole biogenesis; however, the reason for persistence of the assembled human cartwheel structure from S phase to late mitosis remains unclear. Here, we demonstrate mainly using cell synchronization, RNA interference, immunofluorescence and time-lapse-microscopy, biochemical analysis, and methods that the cartwheel persistently assembles and maintains centriole engagement and centrosome integrity during S phase to late G2 phase. Blockade of the continuous accumulation of centriolar Sas-6, a major cartwheel protein, after procentriole formation induces premature centriole disengagement and disrupts pericentriolar matrix integrity. Additionally, we determined that during mitosis, CDK1-cyclin B phosphorylates Sas-6 at T495 and S510, disrupting its binding to cartwheel component STIL and pericentriolar component Nedd1 and promoting cartwheel disassembly and centriole disengagement. Perturbation of this phosphorylation maintains the accumulation of centriolar Sas-6 and retains centriole engagement during mitotic exit, which results in the inhibition of centriole reduplication. Collectively, these data demonstrate that persistent cartwheel assembly after procentriole formation maintains centriole engagement and that this configuration is relieved through phosphorylation of Sas-6 by CDK1-cyclin B during mitosis in human cells.
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spelling pubmed-97636912022-12-23 Cartwheel disassembly regulated by CDK1-cyclin B kinase allows human centriole disengagement and licensing Huang, Fan Xu, Xiaowei Xin, Guangwei Zhang, Boyan Jiang, Qing Zhang, Chuanmao J Biol Chem Research Article Cartwheel assembly is considered the first step in the initiation of procentriole biogenesis; however, the reason for persistence of the assembled human cartwheel structure from S phase to late mitosis remains unclear. Here, we demonstrate mainly using cell synchronization, RNA interference, immunofluorescence and time-lapse-microscopy, biochemical analysis, and methods that the cartwheel persistently assembles and maintains centriole engagement and centrosome integrity during S phase to late G2 phase. Blockade of the continuous accumulation of centriolar Sas-6, a major cartwheel protein, after procentriole formation induces premature centriole disengagement and disrupts pericentriolar matrix integrity. Additionally, we determined that during mitosis, CDK1-cyclin B phosphorylates Sas-6 at T495 and S510, disrupting its binding to cartwheel component STIL and pericentriolar component Nedd1 and promoting cartwheel disassembly and centriole disengagement. Perturbation of this phosphorylation maintains the accumulation of centriolar Sas-6 and retains centriole engagement during mitotic exit, which results in the inhibition of centriole reduplication. Collectively, these data demonstrate that persistent cartwheel assembly after procentriole formation maintains centriole engagement and that this configuration is relieved through phosphorylation of Sas-6 by CDK1-cyclin B during mitosis in human cells. American Society for Biochemistry and Molecular Biology 2022-11-07 /pmc/articles/PMC9763691/ /pubmed/36356903 http://dx.doi.org/10.1016/j.jbc.2022.102658 Text en © 2022 The Authors https://creativecommons.org/licenses/by-nc-nd/4.0/This is an open access article under the CC BY-NC-ND license (http://creativecommons.org/licenses/by-nc-nd/4.0/).
spellingShingle Research Article
Huang, Fan
Xu, Xiaowei
Xin, Guangwei
Zhang, Boyan
Jiang, Qing
Zhang, Chuanmao
Cartwheel disassembly regulated by CDK1-cyclin B kinase allows human centriole disengagement and licensing
title Cartwheel disassembly regulated by CDK1-cyclin B kinase allows human centriole disengagement and licensing
title_full Cartwheel disassembly regulated by CDK1-cyclin B kinase allows human centriole disengagement and licensing
title_fullStr Cartwheel disassembly regulated by CDK1-cyclin B kinase allows human centriole disengagement and licensing
title_full_unstemmed Cartwheel disassembly regulated by CDK1-cyclin B kinase allows human centriole disengagement and licensing
title_short Cartwheel disassembly regulated by CDK1-cyclin B kinase allows human centriole disengagement and licensing
title_sort cartwheel disassembly regulated by cdk1-cyclin b kinase allows human centriole disengagement and licensing
topic Research Article
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC9763691/
https://www.ncbi.nlm.nih.gov/pubmed/36356903
http://dx.doi.org/10.1016/j.jbc.2022.102658
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