Mps1 phosphorylation of condensin II controls chromosome condensation at the onset of mitosis

Journal of Cell Biology

Volumn 205, Issue 6, 2014, Pages 781-790

  Kagami, Yuya ^a,b   Nihira, Keishi ^b   Wada, Shota ^a,b   Ono, Masaya ^c   Honda, Mariko ^a   Yoshida, Kiyotsugu ^a  

^a JIKEI UNIVERSITY SCHOOL OF MEDICINE   (Japan)

^b TOKYO MEDICAL AND DENTAL UNIVERSITY   (Japan)

^c NATIONAL CANCER CENTER RESEARCH INSTITUTE   (Japan)

Author keywords

2DICAL; KD; Kinase dead; Two dimensional image converted analysis of liquid chromatography and mass spectrometry; Wild type; WT

Indexed keywords

CELL PROTEIN; CONDENSIN; CONDENSIN II; GENOMIC DNA; SERINE; UNCLASSIFIED DRUG;

ARTICLE; CELL CYCLE G2 PHASE; CELL CYCLE PROGRESSION; CHROMOSOME CONDENSATION; CHROMOSOME SEGREGATION; CHROMOSOME STRUCTURE; CONTROLLED STUDY; DAUGHTER CELL; HUMAN; HUMAN CELL; MITOSIS; PRIORITY JOURNAL; PROPHASE; PROTEIN PHOSPHORYLATION;

ADENOSINE TRIPHOSPHATASES; CELL CYCLE PROTEINS; CELL NUCLEUS; CHROMOSOMAL PROTEINS, NON-HISTONE; CHROMOSOMES; DNA-BINDING PROTEINS; G2 PHASE CELL CYCLE CHECKPOINTS; HEK293 CELLS; HELA CELLS; HUMANS; MITOSIS; MULTIPROTEIN COMPLEXES; PHOSPHORYLATION; PROTEIN-SERINE-THREONINE KINASES; PROTEIN-TYROSINE KINASES; SERINE;

EID: 84903188542     PISSN: 00219525     EISSN: 15408140     Source Type: Journal    
DOI: 10.1083/jcb.201308172     Document Type: Article

References (25)

1. Abe, S., K. Nagasaka, Y. Hirayama, H. Kozuka-Hata, M. Oyama, Y. Aoyagi, C. Obuse, and T. Hirota. 2011. The initial phase of chromosome condensation requires Cdk1-mediated phosphorylation of the CAP-D3 subunit of condensin II. Genes Dev. 25:863-874. http://dx.doi.org/10.1101/gad.2016411
2. Giet, R., and D.M. Glover. 2001. Drosophila aurora B kinase is required for histone H3 phosphorylation and condensin recruitment during chromosome condensation and to organize the central spindle during cytokinesis. J. Cell Biol. 152:669-682. http://dx.doi.org/10.1083/jcb.152.4.669
3. Hirano, T. 2012. Condensins: universal organizers of chromosomes with diverse functions. Genes Dev. 26:1659-1678. http://dx.doi.org/10.1101/gad .194746.112
4. Hirota, T., D. Gerlich, B. Koch, J. Ellenberg, and J.M. Peters. 2004. Distinct functions of condensin I and II in mitotic chromosome assembly. J. Cell Sci. 117:6435-6445. http://dx.doi.org/10.1242/jcs.01604
5. Jelluma, N., A.B. Brenkman, N.J. van den Broek, C.W. Cruijsen, M.H. van Osch, S.M. Lens, R.H. Medema, and G.J. Kops. 2008. Mps1 phosphorylates Borealin to control Aurora B activity and chromosome alignment. Cell. 132:233-246. http://dx.doi.org/10.1016/j.cell.2007.11.046
6. Kemmler, S., M. Stach, M. Knapp, J. Ortiz, J. Pfannstiel, T. Ruppert, and J. Lechner. 2009. Mimicking Ndc80 phosphorylation triggers spindle assembly checkpoint signalling. EMBO J. 28:1099-1110. http://dx.doi.org/10.1038/emboj.2009.62
7. Kimura, K., M. Hirano, R. Kobayashi, and T. Hirano. 1998. Phosphorylation and activation of 13S condensin by Cdc2 in vitro. Science. 282:487-490. http://dx.doi.org/10.1126/science.282.5388.487
8. Leng, M., D.W. Chan, H. Luo, C. Zhu, J. Qin, and Y. Wang. 2006. MPS1-dependent mitotic BLM phosphorylation is important for chromosome stability. Proc. Natl. Acad. Sci. USA. 103:11485-11490. http://dx.doi.org/10.1073/pnas.0601828103
9. Lipp, J.J., T. Hirota, I. Poser, and J.M. Peters. 2007. Aurora B controls the association of condensin I but not condensin II with mitotic chromosomes. J. Cell Sci. 120:1245-1255. http://dx.doi.org/10.1242/jcs.03425
10. Liu, X., and M. Winey. 2012. The MPS1 family of protein kinases. Annu. Rev. Biochem. 81:561-585. http://dx.doi.org/10.1146/annurev-biochem-061611-090435
11. London, N., S. Ceto, J.A. Ranish, and S. Biggins. 2012. Phosphoregulation of Spc105 by Mps1 and PP1 regulates Bub1 localization to kinetochores. Curr. Biol. 22:900-906. http://dx.doi.org/10.1016/j.cub.2012.03.052
12. Matsubara, J., M. Ono, A. Negishi, H. Ueno, T. Okusaka, J. Furuse, K. Furuta, E. Sugiyama, Y. Saito, N. Kaniwa, et al. 2009. Identification of a predictive biomarker for hematologic toxicities of gemcitabine. J. Clin. Oncol. 27:2261-2268. http://dx.doi.org/10.1200/JCO.2008.19.9745
13. Méndez, J., and B. Stillman. 2000. Chromatin association of human origin recognition complex, cdc6, and minichromosome maintenance proteins during the cell cycle: assembly of prereplication complexes in late mitosis. Mol. Cell. Biol. 20:8602-8612. http://dx.doi.org/10.1128/MCB.20.22.8602-8612.2000
14. Miyamoto, T., N. Kitamura, M. Ono, Y. Nakamura, M. Yoshida, H. Kamino, R. Murai, T. Yamada, and H. Arakawa. 2012. Identification of 14-3-3γ as a Mieap-interacting protein and its role in mitochondrial quality control. Sci Rep. 2:379. http://dx.doi.org/10.1038/srep00379
15. Nihira, K., N. Taira, Y. Miki, and K. Yoshida. 2008. TTK/Mps1 controls nuclear targeting of c-Abl by 14-3-3-coupled phosphorylation in response to oxidative stress. Oncogene. 27:7285-7295. http://dx.doi.org/10.1038/onc.2008.334
16. Ono, M., J. Matsubara, K. Honda, T. Sakuma, T. Hashiguchi, H. Nose, S. Nakamori, T. Okusaka, T. Kosuge, N. Sata, et al. 2009. Prolyl 4-hydroxylation of alpha-fibrinogen: a novel protein modification revealed by plasma proteomics. J. Biol. Chem. 284:29041-29049. http://dx.doi.org/10.1074/jbc.M109 .041749
17. Ono, M., M. Kamita, Y. Murakoshi, J. Matsubara, K. Honda, B. Miho, T. Sakuma, and T. Yamada. 2012. Biomarker discovery of pancreatic and gastrointestinal cancer by 2DICAL: 2-dimensional image-converted analysis of liquid chromatography and mass spectrometry. Int. J. Proteomics. 2012:897412. http://dx.doi.org/10.1155/2012/897412
18. Ono, T., Y. Fang, D.L. Spector, and T. Hirano. 2004. Spatial and temporal regulation of Condensins I and II in mitotic chromosome assembly in human cells. Mol. Biol. Cell. 15:3296-3308. http://dx.doi.org/10.1091/mbc.E04-03-0242
19. Shepperd, L.A., J.C. Meadows, A.M. Sochaj, T.C. Lancaster, J. Zou, G.J. Buttrick, J. Rappsilber, K.G. Hardwick, and J.B. Millar. 2012. Phosphodependent recruitment of Bub1 and Bub3 to Spc7/KNL1 by Mph1 kinase maintains the spindle checkpoint. Curr. Biol. 22:891-899. http://dx.doi .org/10.1016/j.cub.2012.03.051
20. Shimogawa, M.M., B. Graczyk, M.K. Gardner, S.E. Francis, E.A. White, M. Ess, J.N. Molk, C. Ruse, S. Niessen, J.R. Yates III, et al. 2006. Mps1 phosphorylation of Dam1 couples kinetochores to microtubule plus ends at metaphase. Curr. Biol. 16:1489-1501. http://dx.doi.org/10.1016/j.cub.2006 .06.063
21. St-Pierre, J., M. Douziech, F. Bazile, M. Pascariu, E. Bonneil, V. Sauvé, H. Ratsima, and D. D'Amours. 2009. Polo kinase regulates mitotic chromosome condensation by hyperactivation of condensin DNA supercoiling activity. Mol. Cell. 34:416-426. http://dx.doi.org/10.1016/j.molcel.2009.04.013
22. Stucke, V.M., H.H. Silljé, L. Arnaud, and E.A. Nigg. 2002. Human Mps1 kinase is required for the spindle assembly checkpoint but not for centrosome duplication. EMBO J. 21:1723-1732. http://dx.doi.org/10.1093/emboj/21.7.1723
23. Tada, K., H. Susumu, T. Sakuno, and Y. Watanabe. 2011. Condensin association with histone H2A shapes mitotic chromosomes. Nature. 474:477-483. http://dx.doi.org/10.1038/nature10179
24. Takemoto, A., A. Murayama, M. Katano, T. Urano, K. Furukawa, S. Yokoyama, J. Yanagisawa, F. Hanaoka, and K. Kimura. 2007. Analysis of the role of Aurora B on the chromosomal targeting of condensin I. Nucleic Acids Res. 35:2403-2412. http://dx.doi.org/10.1093/nar/gkm157
25. Yamagishi, Y., C.H. Yang, Y. Tanno, and Y. Watanabe. 2012. MPS1/Mph1 phosphorylates the kinetochore protein KNL1/Spc7 to recruit SAC components. Nat. Cell Biol. 14:746-752. http://dx.doi.org/10.1038/ncb2515