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Wip1 controls the translocation of the chromosomal passenger complex to the central spindle for faithful mitotic exit

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Abstract

Dramatic cellular reorganization in mitosis critically depends on the timely and temporal phosphorylation of a broad range of proteins, which is mediated by the activation of the mitotic kinases and repression of counteracting phosphatases. The mitosis-to-interphase transition, which is termed mitotic exit, involves the removal of mitotic phosphorylation by protein phosphatases. Although protein phosphatase 1 (PP1) and protein phosphatase 2A (PP2A) drive this reversal in animal cells, the phosphatase network associated with ordered bulk dephosphorylation in mitotic exit is not fully understood. Here, we describe a new mitotic phosphatase relay in which Wip1/PPM1D phosphatase activity is essential for chromosomal passenger complex (CPC) translocation to the anaphase central spindle after release from the chromosome via PP1-mediated dephosphorylation of histone H3T3. Depletion of endogenous Wip1 and overexpression of the phosphatase-dead mutant disturbed CPC translocation to the central spindle, leading to failure of cytokinesis. While Wip1 was degraded in early mitosis, its levels recovered in anaphase and the protein functioned as a Cdk1-counteracting phosphatase at the anaphase central spindle and midbody. Mechanistically, Wip1 dephosphorylated Thr-59 in inner centromere protein (INCENP), which, subsequently bound to MKLP2 and recruited other components to the central spindle. Furthermore, Wip1 overexpression is associated with the overall survival rate of patients with breast cancer, suggesting that Wip1 not only functions as a weak oncogene in the DNA damage network but also as a tumor suppressor in mitotic exit. Altogether, our findings reveal that sequential dephosphorylation of mitotic phosphatases provides spatiotemporal regulation of mitotic exit to prevent tumor initiation and progression.

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Acknowledgements

We thank Dr. Cha for the Wip1 inducible cell lines. We acknowledge METABRIC for generating the data. This work is supported in part by grants from the National Research Foundation of Korea (NRF-2019R1F1A1062913 and NRF-2020R1A2C1013663) and a grant from the Korea Institute of Radiological and Medical Sciences (KIRAMS) from the Ministry of Science and ICT (MSIT) of Korea (50543-2019).

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  1. Xianghua Zhang, Ji Eun Park and Eun Ho Kim contributed equally to this study.

Authors and Affiliations

  1. Drug Information Research Institute, College of Pharmacy, Sookmyung Women’s University, Seoul, 04310, Republic of Korea

    Xianghua Zhang, Ji Eun Park, Jihee Hong & Chang-Young Jang

  2. Department of Biochemistry, School of Medicine, Catholic University of Daegu, Daegu, 42472, Republic of Korea

    Eun Ho Kim

  3. Department of Surgery, Seoul National University Boramae Medical Center, Seoul, 07061, Republic of Korea

    Ki-Tae Hwang

  4. Department of Pathology, Seoul National University Boramae Medical Center, Seoul, 07061, Republic of Korea

    Young A. Kim

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Contributions

All authors contributed to project planning and data analysis of their respective experiments. CYJ and YAK coordinated the work. ZJ, JH, and JEP performed all of the biochemical experiments and imaging experiments, except analysis of the expression profile of Wip1 in the cell cycle, which was performed by EHK. KTH and YAK performed an analysis of the data obtained from the METABRIC database. All authors contributed to the writing of the paper.

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Correspondence to Young A. Kim or Chang-Young Jang.

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Zhang, X., Park, J.E., Kim, E.H. et al. Wip1 controls the translocation of the chromosomal passenger complex to the central spindle for faithful mitotic exit. Cell. Mol. Life Sci. 78, 2821–2838 (2021). https://doi.org/10.1007/s00018-020-03665-x

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