Dynamic autophosphorylation of mps1 kinase is required for faithful mitotic progression

PLoS ONE

Volumn 9, Issue 9, 2014, Pages

  Wang, Xinghui ^a,b   Yu, Huijuan ^a,b   Xu, Leilei ^a,b   Zhu, Tongge ^a,b   Zheng, Fan ^c,d   Fu, Chuanhai ^c,d   Wang, Zhiyong ^a,b   Dou, Zhen ^a,b  

^a UNIVERSITY OF SCIENCE AND TECHNOLOGY OF CHINA   (China)

^b UNIVERSITY OF SCIENCE AND TECHNOLOGY OF CHINA   (China)

^c UNIVERSITY OF HONG KONG   (Hong Kong)

^d UNIVERSITY OF HONG KONG   (China)

Author keywords

[No Author keywords available]

Indexed keywords

BUB1 RELATED PROTEIN; MITOTIC KINASE; MPS1 KINASE; PHOSPHOTRANSFERASE; PROTEIN MAD2; UNCLASSIFIED DRUG; CELL CYCLE PROTEIN; PROTEIN SERINE THREONINE KINASE; PROTEIN TYROSINE KINASE; SERINE; THREONINE; TTK PROTEIN, HUMAN;

AMINO TERMINAL SEQUENCE; ANAPHASE; ARTICLE; AUTOPHOSPHORYLATION; CELL CYCLE PROGRESSION; CENTROMERE; CHROMOSOME SEGREGATION; CONTROLLED STUDY; ENZYME ACTIVE SITE; ENZYME LOCALIZATION; ENZYME PHOSPHORYLATION; HUMAN; HUMAN CELL; M PHASE CELL CYCLE CHECKPOINT; METAPHASE CHROMOSOME; MITOSIS; CHEMISTRY; HELA CELL LINE; METABOLISM; PHOSPHORYLATION;

CELL CYCLE PROTEINS; HELA CELLS; HUMANS; MITOSIS; PHOSPHORYLATION; PROTEIN-SERINE-THREONINE KINASES; PROTEIN-TYROSINE KINASES; SERINE; THREONINE;

EID: 84907546727     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0104723     Document Type: Article

References (51)

1. Nigg EA (2001) Mitotic kinases as regulators of cell division and its checkpoints. Nat Rev Mol Cell Biol 2: 21-32
2. Ma HT, Poon RY (2011) How protein kinases co-ordinate mitosis in animal cells. Biochem J 435: 17-31
3. Yuan K, Huang Y, Yao X (2011) Illumination of mitotic orchestra during cell division: a Polo view. Cell Signal 23: 1-5
4. Musacchio A, Salmon ED (2007) The spindle-assembly checkpoint in space and time. Nat Rev Mol Cell Biol 8: 379-393
5. Foley EA, Kapoor TM (2013) Microtubule attachment and spindle assembly checkpoint signalling at the kinetochore. Nat Rev Mol Cell Biol 14: 25-37
6. Sudakin V, Chan GK, Yen TJ (2001) Checkpoint inhibition of the APC/C in HeLa cells is mediated by a complex of BUBR1, BUB3, CDC20, and MAD2. J Cell Biol 154: 925-936
7. Chao WC, Kulkarni K, Zhang Z, Kong EH, Barford D (2012) Structure of the mitotic checkpoint complex. Nature 484: 208-213
8. Liu X, Winey M (2012) The MPS1 family of protein kinases. Annu Rev Biochem 81: 561-585
9. Stucke VM, Sillje HH, Arnaud L, Nigg EA (2002) Human Mps1 kinase is required for the spindle assembly checkpoint but not for centrosome duplication. The EMBO journal 21: 1723-1732
10. Dou Z, Sawagechi A, Zhang J, Luo H, Brako L, et al. (2003) Dynamic distribution of TTK in HeLa cells: insights from an ultrastructural study. Cell Res 13: 443-449
11. Liu ST, Chan GK, Hittle JC, Fujii G, Lees E, et al. (2003) Human MPS1 kinase is required for mitotic arrest induced by the loss of CENP-E from kinetochores. Mol Biol Cell 14: 1638-1651
12. Hewitt L, Tighe A, Santaguida S, White AM, Jones CD, et al. (2010) Sustained Mps1 activity is required in mitosis to recruit O-Mad2 to the Mad1-C-Mad2 core complex. J Cell Biol 190: 25-34
13. Maciejowski J, George KA, Terret ME, Zhang C, Shokat KM, et al. (2010) Mps1 directs the assembly of Cdc20 inhibitory complexes during interphase and mitosis to control M phase timing and spindle checkpoint signaling. J Cell Biol 190: 89-100
14. Sliedrecht T, Zhang C, Shokat KM, Kops GJ (2010) Chemical genetic inhibition of Mps1 in stable human cell lines reveals novel aspects of Mps1 function in mitosis. PLoS One 5: e10251
15. Jelluma N, Brenkman AB, van den Broek NJ, Cruijsen CW, van Osch MH, et al. (2008) Mps1 phosphorylates Borealin to control Aurora B activity and chromosome alignment. Cell 132: 233-246
16. Santaguida S, Tighe A, D'Alise AM, Taylor SS, Musacchio A (2010) Dissecting the role of MPS1 in chromosome biorientation and the spindle checkpoint through the small molecule inhibitor reversine. J Cell Biol 190: 73-87
17. Maure JF, Kitamura E, Tanaka TU (2007) Mps1 kinase promotes sisterkinetochore bi-orientation by a tension-dependent mechanism. Curr Biol 17: 2175-2182
18. Kwiatkowski N, Jelluma N, Filippakopoulos P, Soundararajan M, Manak MS, et al. (2010) Small-molecule kinase inhibitors provide insight into Mps1 cell cycle function. Nat Chem Biol 6: 359-368
19. Lan W, Cleveland DW (2010) A chemical tool box defines mitotic and interphase roles for Mps1 kinase. J Cell Biol 190: 21-24
20. Yamagishi Y, Yang CH, Tanno Y, Watanabe Y (2012) MPS1/Mph1 phosphorylates the kinetochore protein KNL1/Spc7 to recruit SAC components. Nat Cell Biol 14: 746-752
21. London N, Ceto S, Ranish JA, Biggins S (2012) Phosphoregulation of Spc105 by Mps1 and PP1 regulates Bub1 localization to kinetochores. Curr Biol 22: 900-906
22. Shepperd LA, Meadows JC, Sochaj AM, Lancaster TC, Zou J, et al. (2012) Phosphodependent recruitment of Bub1 and Bub3 to Spc7/KNL1 by Mph1 kinase maintains the spindle checkpoint. Curr Biol 22: 891-899
23. Stucke VM, Baumann C, Nigg EA (2004) Kinetochore localization and microtubule interaction of the human spindle checkpoint kinase Mps1. Chromosoma 113: 1-15
24. Lee S, Thebault P, Freschi L, Beaufils S, Blundell TL, et al. (2012) Characterization of spindle checkpoint kinase Mps1 reveals domain with functional and structural similarities to tetratricopeptide repeat motifs of Bub1 and BubR1 checkpoint kinases. J Biol Chem 287: 5988-6001
25. Thebault P, Chirgadze DY, Dou Z, Blundell TL, Elowe S, et al. (2012) Structural and functional insights into the role of the N-terminal Mps1 TPR domain in the SAC (spindle assembly checkpoint). Biochem J 448: 321-328
26. Dou Z, von Schubert C, Korner R, Santamaria A, Elowe S, et al. (2011) Quantitative mass spectrometry analysis reveals similar substrate consensus motif for human Mps1 kinase and Plk1. PLoS One 6: e18793
27. Zhu T, Dou Z, Qin B, Jin C, Wang X, et al. (2013) Phosphorylation of microtubule-binding protein Hec1 by mitotic kinase Aurora B specifies spindle checkpoint kinase Mps1 signaling at the kinetochore. J Biol Chem 288: 36149-36159
28. Jelluma N, Dansen TB, Sliedrecht T, Kwiatkowski NP, Kops GJ (2010) Release of Mps1 from kinetochores is crucial for timely anaphase onset. J Cell Biol 191: 281-290
29. Tyler RK, Chu ML, Johnson H, McKenzie EA, Gaskell SJ, et al. (2009) Phosphoregulation of human Mps1 kinase. Biochem J 417: 173-181
30. Jelluma N, Brenkman AB, McLeod I, Yates JR 3rd, Cleveland DW, et al. (2008) Chromosomal instability by inefficient Mps1 auto-activation due to a weakened mitotic checkpoint and lagging chromosomes. PLoS One 3: e2415
31. Xu Q, Zhu S, Wang W, Zhang X, Old W, et al. (2009) Regulation of kinetochore recruitment of two essential mitotic spindle checkpoint proteins by Mps1 phosphorylation. Mol Biol Cell 20: 10-20
32. Kang J, Chen Y, Zhao Y, Yu H (2007) Autophosphorylation-dependent activation of human Mps1 is required for the spindle checkpoint. Proc Natl Acad Sci U S A 104: 20232-20237
33. Mattison CP, Old WM, Steiner E, Huneycutt BJ, Resing KA, et al. (2007) Mps1 activation loop autophosphorylation enhances kinase activity. J Biol Chem 282: 30553-30561
34. Poser I, Sarov M, Hutchins JR, Heriche JK, Toyoda Y, et al. (2008) BAC TransgeneOmics: a high-throughput method for exploration of protein function in mammals. Nat Methods 5: 409-415
35. Elowe S, Hummer S, Uldschmid A, Li X, Nigg EA (2007) Tension-sensitive Plk1 phosphorylation on BubR1 regulates the stability of kinetochore microtubule interactions. Genes Dev 21: 2205-2219
36. Fava LL, Kaulich M, Nigg EA, Santamaria A (2011) Probing the in vivo function of Mad1: C-Mad2 in the spindle assembly checkpoint. EMBO J 30: 3322-3336
37. Cao X, Ding X, Guo Z, Zhou R, Wang F, et al. (2005) PALS1 specifies the localization of ezrin to the apical membrane of gastric parietal cells. J Biol Chem 280: 13584-13592
38. Fang Z, Miao Y, Ding X, Deng H, Liu S, et al. (2006) Proteomic identification and functional characterization of a novel ARF6 GTPase-activating protein, ACAP4. Mol Cell Proteomics 5: 1437-1449
39. Yuan K, Li N, Jiang K, Zhu T, Huo Y, et al. (2009) PinX1 is a novel microtubule-binding protein essential for accurate chromosome segregation. J Biol Chem 284: 23072-23082
40. Daub H, Olsen JV, Bairlein M, Gnad F, Oppermann FS, et al. (2008) Kinaseselective enrichment enables quantitative phosphoproteomics of the kinome across the cell cycle. Mol Cell 31: 438-448
41. Tighe A, Staples O, Taylor S (2008) Mps1 kinase activity restrains anaphase during an unperturbed mitosis and targets Mad2 to kinetochores. J Cell Biol 181: 893-901
42. Taylor SS, Kornev AP (2011) Protein kinases: evolution of dynamic regulatory proteins. Trends Biochem Sci 36: 65-77
43. Morin V, Prieto S, Melines S, Hem S, Rossignol M, et al. (2012) CDKdependent potentiation of MPS1 kinase activity is essential to the mitotic checkpoint. Curr Biol 22: 289-295
44. Schmidt M, Budirahardja Y, Klompmaker R, Medema RH (2005) Ablation of the spindle assembly checkpoint by a compound targeting Mps1. EMBO Rep 6: 866-872
45. Cohen P (2000) The regulation of protein function by multisite phosphorylation- a 25 year update. Trends Biochem Sci 25: 596-601
46. Heinrich S, Geissen EM, Kamenz J, Trautmann S, Widmer C, et al. (2013) Determinants of robustness in spindle assembly checkpoint signalling. Nat Cell Biol 15: 1328-1339
47. Dick AE, Gerlich DW (2013) Kinetic framework of spindle assembly checkpoint signalling. Nat Cell Biol 15: 1370-1377
48. Collin P, Nashchekina O, Walker R, Pines J (2013) The spindle assembly checkpoint works like a rheostat rather than a toggle switch. Nat Cell Biol 15: 1378-1385
49. Petsalaki E, Zachos G (2013) Chk1 and Mps1 jointly regulate correction of merotelic kinetochore attachments. J Cell Sci 126: 1235-1246
50. Yeh CW, Yu ZC, Chen PH, Cheng YC, Shieh SY (2014) Phosphorylation at Threonine 288 by Cell Cycle Checkpoint Kinase 2 (CHK2) Controls Human Monopolar Spindle 1 (Mps1) Kinetochore Localization. J Biol Chem 289: 15319-15327
51. Petsalaki E, Zachos G (2014) Chk2 prevents mitotic exit when the majority of kinetochores are unattached. J Cell Biol 205: 339-356