Multimodal mechanisms of human centriole engagement and disengagement

Centrioles are unique cellular structures that replicate to produce identical copies, ensuring accurate chromosome segregation during mitosis. A new centriole, the "daughter", is assembled adjacent to an existing "mother" centriole. Only after the daughter centriole is fully developed as a complete replica, does it disengage and become the core of a new functional centrosome. The mechanisms preventing precocious disengagement of the immature daughter centriole have remained unclear. Here, we identify three key mechanisms maintaining mother-daughter centriole engagement: the cartwheel, the torus, and the pericentriolar material (PCM). Among these, the torus critically establishes the characteristic orthogonal engagement. We also demonstrate that engagement mediated by the cartwheel and torus is progressively released during centriole maturation. This release involves structural changes in the daughter, known as centriole blooming and distancing, respectively. Disrupting these structural transitions blocks subsequent steps, preventing centriole disengagement and centrosome conversion in the G1 phase. This study provides a comprehensive understanding of how the maturing daughter centriole progressively disengages from its mother through multiple steps, ensuring its complete structure and conversion into an independent centrosome.

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Publication Details

Journal
The EMBO Journal
Published
2025-02-04
DOI
https://doi.org/10.1038/s44318-024-00350-8
Citations
5
Primary Topic
Microtubule and mitosis dynamics
Type
article
Field-Weighted Citation Impact
5.76

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article

Multimodal mechanisms of human centriole engagement and disengagement

Shoji Hata, Takumi Chinen, Hirokazu Sakamoto, Kei Ito et al.
5 citations
The EMBO Journal
Microtubule and mitosis dynamics
5.76
article

Multimodal mechanisms of human centriole engagement and disengagement

Shoji Hata, Takumi Chinen, Hirokazu Sakamoto, Kei Ito, Kyohei Matsuhashi, Masamitsu Fukuyama, Daiju Kitagawa, Kasuga Takumi, Shohei Yamamoto, Kaho Nagai
article en
5 citations

Abstract

Centrioles are unique cellular structures that replicate to produce identical copies, ensuring accurate chromosome segregation during mitosis. A new centriole, the "daughter", is assembled adjacent to an existing "mother" centriole. Only after the daughter centriole is fully developed as a complete replica, does it disengage and become the core of a new functional centrosome. The mechanisms preventing precocious disengagement of the immature daughter centriole have remained unclear. Here, we identify three key mechanisms maintaining mother-daughter centriole engagement: the cartwheel, the torus, and the pericentriolar material (PCM). Among these, the torus critically establishes the characteristic orthogonal engagement. We also demonstrate that engagement mediated by the cartwheel and torus is progressively released during centriole maturation. This release involves structural changes in the daughter, known as centriole blooming and distancing, respectively. Disrupting these structural transitions blocks subsequent steps, preventing centriole disengagement and centrosome conversion in the G1 phase. This study provides a comprehensive understanding of how the maturing daughter centriole progressively disengages from its mother through multiple steps, ensuring its complete structure and conversion into an independent centrosome.

The EMBO JournalVol. 44(5)
Bunkyo University (JP), Japan Science and Technology Agency (JP), The University of Tokyo (JP)
Naito Foundation, Takeda Science Foundation, Sumitomo Foundation, Uehara Memorial Foundation, Heiwa Nakajima Foundation, Inamori Foundation, Kato Memorial Bioscience Foundation, Astellas Pharma, Astellas Foundation for Research on Metabolic Disorders, Kanae Foundation for the Promotion of Medical Science, Japan Society for the Promotion of Science, Japan Science and Technology Agency, Core Research for Evolutional Science and Technology, Precursory Research for Embryonic Science and Technology
Openalex Percentile: Top 5%
Microtubule and mitosis dynamics
5.76
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