Constitutive Mad1 targeting to kinetochores uncouples checkpoint signalling from chromosome biorientation

Nature Cell Biology

Volumn 13, Issue 4, 2011, Pages 475-483

  Maldonado, Maria ^a   Kapoor, Tarun M ^a  

^a ROCKEFELLER UNIVERSITY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

AURORA KINASE; BUB1 RELATED PROTEIN; PHOSPHOTRANSFERASE; POLO LIKE KINASE; PROTEIN MAD1; PROTEIN MAD2; PROTEIN MPS1; UNCLASSIFIED DRUG;

ANIMAL CELL; ARTICLE; CELL CYCLE ARREST; CELL DIVISION; CENTROMERE; CHROMOSOME; CONTROLLED STUDY; ENZYME ACTIVITY; ENZYME DEFECT; METAPHASE; MOLECULAR DYNAMICS; NONHUMAN; PRIORITY JOURNAL; PROTEIN BINDING; PROTEIN LOCALIZATION; SIGNAL TRANSDUCTION;

CALCIUM-BINDING PROTEINS; CELL CYCLE PROTEINS; CHROMOSOME SEGREGATION; HELA CELLS; HUMANS; KINETOCHORES; MICROTUBULES; MITOSIS; MITOTIC SPINDLE APPARATUS; NUCLEAR PROTEINS; RECOMBINANT FUSION PROTEINS; REPRESSOR PROTEINS; SIGNAL TRANSDUCTION;

EUKARYOTA;

EID: 79953299278     PISSN: 14657392     EISSN: None     Source Type: Journal    
DOI: 10.1038/ncb2223     Document Type: Article

References (36)

1. Hartwell, L. H. & Weinert, T. A. Checkpoints: controls that ensure the order of cell cycle events. Science 246, 629-634 (1989). (Pubitemid 19283354)
2. Rieder, C. L., Schultz, A., Cole, R. & Sluder, G. Anaphase onset in vertebrate somatic cells is controlled by a checkpoint that monitors sister kinetochore attachment to the spindle. J. Cell Biol. 127, 1301-1310 (1994). (Pubitemid 24362564)
3. Musacchio, A. & Salmon, E. D. The spindle-assembly checkpoint in space and time. Nat. Rev. Mol. Cell Biol. 8, 379-393 (2007). (Pubitemid 46643240)
4. Chen, R. H., Waters, J. C., Salmon, E. D. & Murray, A. W. Association of spindle assembly checkpoint component XMAD2 with unattached kinetochores. Science 274, 242-246 (1996). (Pubitemid 26353200)
5. Li, Y. & Benezra, R. Identication of a human mitotic checkpoint gene: hsMAD2. Science 274, 246-248 (1996).
6. Chen, R. H., Shevchenko, A., Mann, M. & Murray, A. W. Spindle checkpoint protein Xmad1 recruits Xmad2 to unattached kinetochores. J. Cell Biol. 143, 283-295 (1998). (Pubitemid 28487850)
7. Meraldi, P., Honda, R. & Nigg, E. A. Aurora kinases link chromosome segregation and cell division to cancer susceptibility. Curr. Opin. Genet. Dev. 14, 29-36 (2004). (Pubitemid 38167474)
8. Pinsky, B. A. & Biggins, S. The spindle checkpoint: tension versus attachment. Trends. Cell Biol. 15, 486-493 (2005). (Pubitemid 41253468)
9. Luo, X. & Yu, H. Protein metamorphosis: the two-state behaviour of Mad2. Structure 16, 1616-1625 (2008).
10. Sironi, L. et al. Crystal structure of the tetrameric Mad1 mad2 core complex: implications of a ̀safety belt' binding mechanism for the spindle checkpoint. EMBO J. 21, 2496-2506 (2002). (Pubitemid 34546721)
11. Hardwick, K. G., Johnston, R. C., Smith, D. L. & Murray, A. W. MAD3 encodes a novel component of the spindle checkpoint which interacts with Bub3p, Cdc20p, and Mad2p. J. Cell Biol. 148, 871-882 (2000).
12. Sudakin, V., Chan, G. K. & Yen, T. J. 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 (2001). (Pubitemid 34286173)
13. Cheeseman, I. M. et al. A conserved protein network controls assembly of the outer kinetochore and its ability to sustain tension. Genes Dev. 18, 2255-2268 (2004). (Pubitemid 39209574)
14. Santaguida, S. & Musacchio, A. The life and miracles of kinetochores. EMBO J. 28, 2511-2531 (2009).
15. Hoffman, D. B., Pearson, C. G., Yen, T. J., Howell, B. J. & Salmon, E. D. Microtubule-dependent changes in assembly of microtubule motor proteins and mitotic spindle checkpoint proteins at PtK1 kinetochores. Mol. Biol. Cell 12, 1995-2009 (2001). (Pubitemid 33049694)
16. Jablonski, S. A., Chan, G. K., Cooke, C. A., Earnshaw, W. C. & Yen, T. J. The hBUB1 and hBUBR1 kinases sequentially assemble onto kinetochores during prophase with hBUBR1 concentrating at the kinetochore plates in mitosis. Chromosoma 107, 386-396 (1998). (Pubitemid 29057531)
17. Karess, R. Rod-Zw10-Zwilch: a key player in the spindle checkpoint. Trends. Cell Biol. 15, 386-392 (2005). (Pubitemid 40943528)
18. Meraldi, P., Draviam, V. M. & Sorger, P. K. Timing and checkpoints in the regulation of mitotic progression. Dev. Cell 7, 45-60 (2004). (Pubitemid 39172687)
19. Petronczki, M., Lenart, P. & Peters, J. M. Polo on the rise-from mitotic entry to cytokinesis with Plk1. Dev. Cell 14, 646-659 (2008). (Pubitemid 351622626)
20. Lan, W. & Cleveland, D. W. A chemical tool box denes mitotic and interphase roles for Mps1 kinase. J. Cell Biol. 190, 21-24 (2010).
21. Jelluma, N., Dansen, T. B., Sliedrecht, T., Kwiatkowski, N. P. & Kops, G. J. Release of Mps1 from kinetochores is crucial for timely anaphase onset. J. Cell Biol. 191, 281-290 (2010).
22. Kwiatkowski, N. et al. Small-molecule kinase inhibitors provide insight into Mps1 cell cycle function. Nat. Chem. Biol. 6, 359-368 (2010).
23. Santaguida, S., Tighe, A., D'Alise, A. M., Taylor, S. S. & Musacchio, A. Dissecting the role of MPS1 in chromosome biorientation and the spindle checkpoint through the small molecule inhibitor reversine. J. Cell Biol. 190, 73-87 (2010).
24. Ditcheld, C. et al. Aurora B couples chromosome alignment with anaphase by targeting BubR1, Mad2, and Cenp-E to kinetochores. J. Cell Biol. 161, 267-280 (2003).
25. Hauf, S. et al. The small molecule Hesperadin reveals a role for Aurora B in correcting kinetochore microtubule attachment and in maintaining the spindle assembly checkpoint. J. Cell Biol. 161, 281-294 (2003). (Pubitemid 36529847)
26. Simonetta, M. et al. The inuence of catalysis on mad2 activation dynamics. PLoS Biol. 7, e10 (2009).
27. Burke, D. J. & Stukenberg, P. T. Linking kinetochore microtubule binding to the spindle checkpoint. Dev. Cell 14, 474-479 (2008). (Pubitemid 351479945)
28. Kang, J. & Yu, H. Kinase signaling in the spindle checkpoint. J. Biol. Chem. 284, 15359-15363 (2009).
29. Pinsky, B. A., Kung, C., Shokat, K. M. & Biggins, S. The Ipl1-Aurora protein kinase activates the spindle checkpoint by creating unattached kinetochores. Nat. Cell Biol. 8, 78-83 (2006). (Pubitemid 43064800)
30. Emanuele, M. J. et al. Aurora B kinase and protein phosphatase 1 have opposing roles in modulating kinetochore assembly. J. Cell Biol. 181, 241-254 (2008). (Pubitemid 351574550)
31. Kallio, M. J., McCleland, M. L., Stukenberg, P. T. & Gorbsky, G. J. Inhibition of aurora B kinase blocks chromosome segregation, overrides the spindle checkpoint, and perturbs microtubule dynamics in mitosis. Curr Biol. 12, 900-905 (2002). (Pubitemid 34689224)
32. Petersen, J. & Hagan, I. M. S. pombe aurora kinase/survivin is required for chromosome condensation and the spindle checkpoint attachment response. Curr. Biol. 13, 590-597 (2003). (Pubitemid 36391938)
33. Vanoosthuyse, V. & Hardwick, K. G. A novel protein phosphatase 1-dependent spindle checkpoint silencing mechanism. Curr. Biol. 19, 1176-1181 (2009).
34. Liu, D., Vader, G., Vromans, M. J., Lampson, M. A. & Lens, S. M. Sensing chromosome bi-orientation by spatial separation of aurora B kinase from kinetochore substrates. Science 323, 1350-1353 (2009).
35. Kulukian, A., Han, J. S. & Cleveland, D. W. Unattached kinetochores catalyze production of an anaphase inhibitor that requires a Mad2 template to prime Cdc20 for BubR1 binding. Dev. Cell 16, 105-117 (2009).
36. Wan, X. et al. Protein architecture of the human kinetochore microtubule attachment site. Cell 137, 672-684 (2009).