The pericentriolar material (PCM) that accumulates around the centriole expands during mitosis and nucleates microtubules. Here, we show the cooperative roles of the centriole and PCM scaffold proteins, pericentrin and CDK5RAP2, in the recruitment of CEP192 to spindle poles during mitosis. Systematic depletion of PCM proteins revealed that CEP192, but not pericentrin and/or CDK5RAP2, was crucial for bipolar spindle assembly in HeLa, RPE1, and A549 cells with centrioles. Upon double depletion of pericentrin and CDK5RAP2, CEP192 that remained at centriole walls was sufficient for bipolar spindle formation. In contrast, through centriole removal, we found that pericentrin and CDK5RAP2 recruited CEP192 at the acentriolar spindle pole and facilitated bipolar spindle formation in mitotic cells with one centrosome. Furthermore, the perturbation of PLK1, a critical kinase for PCM assembly, efficiently suppressed bipolar spindle formation in mitotic cells with one centrosome. Overall, these data suggest that the centriole and PCM scaffold proteins cooperatively recruit CEP192 to spindle poles and facilitate bipolar spindle formation.
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1 February 2021
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January 14 2021
Centriole and PCM cooperatively recruit CEP192 to spindle poles to promote bipolar spindle assembly
Takumi Chinen
,
1
Department of Physiological Chemistry, Graduate School of Pharmaceutical Science, The University of Tokyo, Bunkyo, Tokyo, Japan
Correspondence to Takumi Chinen: takumi.chinen@mol.f.u-tokyo.ac.jp
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Kaho Yamazaki
,
1
Department of Physiological Chemistry, Graduate School of Pharmaceutical Science, The University of Tokyo, Bunkyo, Tokyo, Japan
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Kaho Hashimoto
,
Kaho Hashimoto
1
Department of Physiological Chemistry, Graduate School of Pharmaceutical Science, The University of Tokyo, Bunkyo, Tokyo, Japan
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Ken Fujii
,
Ken Fujii
2
Department of Molecular Genetics, Division of Centrosome Biology, National Institute of Genetics, Mishima, Shizuoka, Japan
3
Department of Genetics, School of Life Science, The Graduate University for Advanced Studies (SOKENDAI), Mishima, Shizuoka, Japan
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Koki Watanabe
,
Koki Watanabe
1
Department of Physiological Chemistry, Graduate School of Pharmaceutical Science, The University of Tokyo, Bunkyo, Tokyo, Japan
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Yutaka Takeda
,
Yutaka Takeda
1
Department of Physiological Chemistry, Graduate School of Pharmaceutical Science, The University of Tokyo, Bunkyo, Tokyo, Japan
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Shohei Yamamoto
,
Shohei Yamamoto
1
Department of Physiological Chemistry, Graduate School of Pharmaceutical Science, The University of Tokyo, Bunkyo, Tokyo, Japan
4
Graduate Program in Bioscience, Graduate School of Science, University of Tokyo, Hongo, Tokyo, Japan
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Yuka Nozaki
,
Yuka Nozaki
2
Department of Molecular Genetics, Division of Centrosome Biology, National Institute of Genetics, Mishima, Shizuoka, Japan
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Yuki Tsuchiya
,
Yuki Tsuchiya
2
Department of Molecular Genetics, Division of Centrosome Biology, National Institute of Genetics, Mishima, Shizuoka, Japan
3
Department of Genetics, School of Life Science, The Graduate University for Advanced Studies (SOKENDAI), Mishima, Shizuoka, Japan
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Daisuke Takao
,
Daisuke Takao
1
Department of Physiological Chemistry, Graduate School of Pharmaceutical Science, The University of Tokyo, Bunkyo, Tokyo, Japan
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Daiju Kitagawa
1
Department of Physiological Chemistry, Graduate School of Pharmaceutical Science, The University of Tokyo, Bunkyo, Tokyo, Japan
2
Department of Molecular Genetics, Division of Centrosome Biology, National Institute of Genetics, Mishima, Shizuoka, Japan
3
Department of Genetics, School of Life Science, The Graduate University for Advanced Studies (SOKENDAI), Mishima, Shizuoka, Japan
Daiju Kitagawa: dkitagawa@mol.f.u-tokyo.ac.jp
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Takumi Chinen
1
Department of Physiological Chemistry, Graduate School of Pharmaceutical Science, The University of Tokyo, Bunkyo, Tokyo, Japan
Kaho Yamazaki
1
Department of Physiological Chemistry, Graduate School of Pharmaceutical Science, The University of Tokyo, Bunkyo, Tokyo, Japan
Kaho Hashimoto
1
Department of Physiological Chemistry, Graduate School of Pharmaceutical Science, The University of Tokyo, Bunkyo, Tokyo, Japan
Ken Fujii
2
Department of Molecular Genetics, Division of Centrosome Biology, National Institute of Genetics, Mishima, Shizuoka, Japan
3
Department of Genetics, School of Life Science, The Graduate University for Advanced Studies (SOKENDAI), Mishima, Shizuoka, Japan
Koki Watanabe
1
Department of Physiological Chemistry, Graduate School of Pharmaceutical Science, The University of Tokyo, Bunkyo, Tokyo, Japan
Yutaka Takeda
1
Department of Physiological Chemistry, Graduate School of Pharmaceutical Science, The University of Tokyo, Bunkyo, Tokyo, Japan
Shohei Yamamoto
1
Department of Physiological Chemistry, Graduate School of Pharmaceutical Science, The University of Tokyo, Bunkyo, Tokyo, Japan
4
Graduate Program in Bioscience, Graduate School of Science, University of Tokyo, Hongo, Tokyo, Japan
Yuka Nozaki
2
Department of Molecular Genetics, Division of Centrosome Biology, National Institute of Genetics, Mishima, Shizuoka, Japan
Yuki Tsuchiya
2
Department of Molecular Genetics, Division of Centrosome Biology, National Institute of Genetics, Mishima, Shizuoka, Japan
3
Department of Genetics, School of Life Science, The Graduate University for Advanced Studies (SOKENDAI), Mishima, Shizuoka, Japan
Daisuke Takao
1
Department of Physiological Chemistry, Graduate School of Pharmaceutical Science, The University of Tokyo, Bunkyo, Tokyo, Japan
Daiju Kitagawa
1
Department of Physiological Chemistry, Graduate School of Pharmaceutical Science, The University of Tokyo, Bunkyo, Tokyo, Japan
2
Department of Molecular Genetics, Division of Centrosome Biology, National Institute of Genetics, Mishima, Shizuoka, Japan
3
Department of Genetics, School of Life Science, The Graduate University for Advanced Studies (SOKENDAI), Mishima, Shizuoka, Japan
Correspondence to Takumi Chinen: takumi.chinen@mol.f.u-tokyo.ac.jp
Daiju Kitagawa: dkitagawa@mol.f.u-tokyo.ac.jp
*
T. Chinen and K. Yamazaki contributed equally to this paper.
Received:
June 15 2020
Revision Received:
October 12 2020
Accepted:
December 15 2020
Online Issn: 1540-8140
Print Issn: 0021-9525
Funding:
Daiichi Sankyo Foundation of Life Science
(NO AWARD)
Japan Society for the Promotion of Science
(24687026, 19H05651, 16H06168, 18K14705, 17J02833)
Ministry of Education, Culture, Sports, Science and Technology
(NO AWARD)
Mochida Memorial Foundation for Medical and Pharmaceutical Research
(NO AWARD)
Takeda Science Foundation
(NO AWARD)
© 2021 Chinen et al.
2021
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/).
J Cell Biol (2021) 220 (2): e202006085.
Article history
Received:
June 15 2020
Revision Received:
October 12 2020
Accepted:
December 15 2020
Citation
Takumi Chinen, Kaho Yamazaki, Kaho Hashimoto, Ken Fujii, Koki Watanabe, Yutaka Takeda, Shohei Yamamoto, Yuka Nozaki, Yuki Tsuchiya, Daisuke Takao, Daiju Kitagawa; Centriole and PCM cooperatively recruit CEP192 to spindle poles to promote bipolar spindle assembly. J Cell Biol 1 February 2021; 220 (2): e202006085. doi: https://doi.org/10.1083/jcb.202006085
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