Release of Mps1 from kinetochores is crucial for timely anaphase onset

Journal of Cell Biology

Volumn 191, Issue 2, 2010, Pages 281-290

  Jelluma, Nannette ^a   Dansen, Tobias B ^a   Sliedrecht, Tale ^a,b   Kwiatkowski, Nicholas P ^c,d   Kops, Geert J P L ^a,b  

^a UNIVERSITY MEDICAL CENTER UTRECHT   (Netherlands)

^b NETHERLANDS PROTEOMICS CENTRE   (Netherlands)

^c DANA FARBER CANCER INSTITUTE   (United States)

^d HARVARD MEDICAL SCHOOL   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

MSP1 EMZYME; PHOSPHOTRANSFERASE; PROTEIN MAD1; PROTEIN MAD2; UNCLASSIFIED DRUG;

ANAPHASE; ARTICLE; CENTROMERE; ENZYME ACTIVITY; ENZYME INHIBITION; HUMAN; HUMAN CELL; MITOSIS; PRIORITY JOURNAL; PROTEIN DEPLETION; PROTEIN SECRETION;

ANAPHASE; CALCIUM-BINDING PROTEINS; CELL CYCLE PROTEINS; CHROMOSOME SEGREGATION; HELA CELLS; HUMANS; KINETOCHORES; MODELS, BIOLOGICAL; NUCLEAR PROTEINS; PROTEIN-SERINE-THREONINE KINASES; REPRESSOR PROTEINS;

EID: 77958508464     PISSN: 00219525     EISSN: 00219525     Source Type: Journal    
DOI: 10.1083/jcb.201003038     Document Type: Article

References (46)

1. Abrieu, A., L. Magnaghi-Jaulin, J.A. Kahana, M. Peter, A. Castro, S. Vigneron, T. Lorca, D.W. Cleveland, and J.C. Labbé. 2001. Mps1 is a kinetochore-associated kinase essential for the vertebrate mitotic checkpoint. Cell. 106:83-93. doi:10.1016/S00928674(01)00410X
2. Barisic, M., B. Sohm, P. Mikolcevic, C. Wandke, V. Rauch, T. Ringer, M. Hess, G. Bonn, and S. Geley. 2010. Spindly/CCDC99 is required for efficient chromosome congression and mitotic checkpoint regulation. Mol. Biol. Cell. 21:1968-1981. doi:10.1091/mbc.E09040356
3. Bourhis, E., A. Lingel, Q. Phung, W.J. Fairbrother, and A.G. Cochran. 2009. Phosphorylation of a borealin dimerization domain is required for proper chromosome segregation. Biochemistry. 48:6783-6793. doi:10.1021/bi900530v
4. Cheeseman, I.M., S. Niessen, S. Anderson, F. Hyndman, J.R. Yates III, K. Oegema, and A. Desai. 2004. A conserved protein network controls assembly of the outer kinetochore and its ability to sustain tension. Genes Dev. 18:2255-2268. doi:10.1101/gad.1234104
5. Daum, J.R., J.D. Wren, J.J. Daniel, S. Sivakumar, J.N. McAvoy, T.A. Potapova, and G.J. Gorbsky. 2009. Ska3 is required for spindle checkpoint silencing and the maintenance of chromosome cohesion in mitosis. Curr. Biol. 19:1467-1472. doi:10.1016/j.cub.2009.07.017
6. Ditchfield, C., V.L. Johnson, A. Tighe, R. Ellston, C. Haworth, T. Johnson, A. Mortlock, N. Keen, and S.S. Taylor. 2003. Aurora B couples chromosome alignment with anaphase by targeting BubR1, Mad2, and Cenp-E to kinetochores. J. Cell Biol. 161:267-280. doi:10.1083/jcb.200208091
7. Espeut, J., A. Gaussen, P. Bieling, V. Morin, S. Prieto, D. Fesquet, T. Surrey, and A. Abrieu. 2008. Phosphorylation relieves autoinhibition of the kinetochore motor Cenp-E. Mol. Cell. 29:637-643. doi:10.1016/j.molcel.2008.01. 004
8. Fischer, M.G., S. Heeger, U. Häcker, and C.F. Lehner. 2004. The mitotic arrest in response to hypoxia and of polar bodies during early embryogenesis requires Drosophila Mps1. Curr. Biol. 14:2019-2024. doi:10.1016/j.cub.2004.11.008
9. Fisk, H.A., and M. Winey. 2001. The mouse Mps1p-like kinase regulates centrosome duplication. Cell. 106:95-104. doi:10.1016/S00928674(01)004111
10. Gaitanos, T.N., A. Santamaria, A.A. Jeyaprakash, B. Wang, E. Conti, and E.A. Nigg. 2009. Stable kinetochore-microtubule interactions depend on the Ska complex and its new component Ska3/C13Orf3. EMBO J. 28:1442-1452. doi:10.1038/emboj.2009.96
11. Gassmann, R., A.J. Holland, D. Varma, X. Wan, F. Civril, D.W. Cleveland, K. Oegema, E.D. Salmon, and A. Desai. 2010. Removal of Spindly from microtubule-attached kinetochores controls spindle checkpoint silencing in human cells. Genes Dev. 24:957-971. doi:10.1101/gad.1886810
12. Gould, S.J., G.A. Keller, N. Hosken, J. Wilkinson, and S. Subramani. 1989. A conserved tripeptide sorts proteins to peroxisomes. J. Cell Biol. 108:1657-1664. doi:10.1083/jcb.108.5.1657
13. Hanisch, A., H.H. Silljé, and E.A. Nigg. 2006. Timely anaphase onset requires a novel spindle and kinetochore complex comprising Ska1 and Ska2. EMBO J. 25:5504-5515. doi:10.1038/sj.emboj.7601426 (Pubitemid 44847191)
14. Hardwick, K.G., E. Weiss, F.C. Luca, M. Winey, and A.W. Murray. 1996. Activation of the budding yeast spindle assembly checkpoint without mitotic spindle disruption. Science. 273:953-956. doi:10.1126/science.273.5277.953 (Pubitemid 26275171)
15. Hauf, S., R.W. Cole, S. LaTerra, C. Zimmer, G. Schnapp, R. Walter, A. Heckel, J. van Meel, C.L. Rieder, and J.M. Peters. 2003. 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. doi:10.1083/jcb.200208092 (Pubitemid 36529847)
16. He, X., M.H. Jones, M. Winey, and S. Sazer. 1998. Mph1, a member of the Mps1-like family of dual specificity protein kinases, is required for the spindle checkpoint in S. pombe. J. Cell Sci. 111:1635-1647. (Pubitemid 28330551)
17. Hewitt, L., A. Tighe, S. Santaguida, A.M. White, C.D. Jones, A. Musacchio, S. Green, and S.S. Taylor. 2010. Sustained Mps1 activity is required in mitosis to recruit OMad-2 to the Mad1-CMad-2 core complex. J. Cell Biol. 190:25-34. doi:10.1083/jcb.201002133
18. Howell, B.J., B.F. McEwen, J.C. Canman, D.B. Hoffman, E.M. Farrar, C.L. Rieder, and E.D. Salmon. 2001. Cytoplasmic dynein/dynactin drives kinetochore protein transport to the spindle poles and has a role in mitotic spindle checkpoint inactivation. J. Cell Biol. 155:1159-1172. doi:10.1083/jcb.200105093
19. Howell, B.J., B. Moree, E.M. Farrar, S. Stewart, G. Fang, and E.D. Salmon. 2004. Spindle checkpoint protein dynamics at kinetochores in living cells. Curr. Biol. 14:953-964. doi:10.1016/j.cub.2004.05.053
20. Jelluma, N., A.B. Brenkman, I. McLeod, J.R. Yates III, D.W. Cleveland, R.H. Medema, and G.J.P.L. Kops. 2008a. Chromosomal instability by inefficient Mps1 auto-activation due to a weakened mitotic checkpoint and lagging chromosomes. PLoS One. 3:e2415. doi:10.1371/journal.pone.0002415
21. Jelluma, N., A.B. Brenkman, N.J.F. van den Broek, C.W.A. Cruijsen, M.H.J. van Osch, S.M.A. Lens, R.H. Medema, and G.J.P.L. Kops. 2008b. Mps1 phosphorylates Borealin to control Aurora B activity and chromosome alignment. Cell. 132:233-246. doi:10.1016/j.cell.2007.11.046 (Pubitemid 351172430)
22. Kang, J., Y. Chen, Y. Zhao, and H. Yu. 2007. Autophosphorylationdependent activation of human Mps1 is required for the spindle checkpoint. Proc. Natl. Acad. Sci. USA. 104:20232-20237. doi:10.1073/pnas.0710519105
23. Kops, G.J., D.R. Foltz, and D.W. Cleveland. 2004. Lethality to human cancer cells through massive chromosome loss by inhibition of the mitotic checkpoint. Proc. Natl. Acad. Sci. USA. 101:8699-8704. doi:10.1073/pnas. 0401142101
24. Kops, G.J., Y. Kim, B.A. Weaver, Y. Mao, I. McLeod, J.R. Yates III, M. Tagaya, and D.W. Cleveland. 2005. ZW10 links mitotic checkpoint signaling to the structural kinetochore. J. Cell Biol. 169:49-60. doi:10.1083/jcb.200411118
25. Kwiatkowski, N., N. Jelluma, P. Filippakopoulos, M. Soundararajan, M.S. Manak, M. Kwon, H.G. Choi, T. Sim, Q.L. Deveraux, S. Rottmann, et al. 2010. Small-molecule kinase inhibitors provide insight into Mps1 cell cycle function. Nat. Chem. Biol. 6:359-368. doi:10.1038/nchembio.345
26. Lan, W., and D.W. Cleveland. 2010. A chemical tool box defines mitotic and interphase roles for Mps1 kinase. J. Cell Biol. 190:21-24. doi:10.1083/jcb.201006080
27. Liu, D., G. Vader, M.J.M. Vromans, M.A. Lampson, and S.M.A. Lens. 2009. Sensing chromosome bi-orientation by spatial separation of aurora B kinase from kinetochore substrates. Science. 323:1350-1353. doi:10.1126/science.1167000
28. Liu, S.T., G.K. Chan, J.C. Hittle, G. Fujii, E. Lees, and T.J. Yen. 2003. Human MPS1 kinase is required for mitotic arrest induced by the loss of CENP-E from kinetochores. Mol. Biol. Cell. 14:1638-1651. doi:10.1091/mbc.02050074
29. Maciejowski, J., K.A. George, M.E. Terret, C. Zhang, K.M. Shokat, and P.V. Jallepalli. 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. doi:10.1083/jcb.201001050
30. Mapelli, M., F.V. Filipp, G. Rancati, L. Massimiliano, L. Nezi, G. Stier, R.S. Hagan, S. Confalonieri, S. Piatti, M. Sattler, and A. Musacchio. 2006. Determinants of conformational dimerization of Mad2 and its inhibition by p31comet. EMBO J. 25:1273-1284. doi:10.1038/sj.emboj.7601033
31. Martin-Lluesma, S., V.M. Stucke, and E.A. Nigg. 2002. Role of Hec1 in spindle checkpoint signaling and kinetochore recruitment of Mad1/Mad2. Science. 297:2267-2270. doi:10.1126/science.1075596
32. Mattison, C.P., W.M. Old, E. Steiner, B.J. Huneycutt, K.A. Resing, N.G. Ahn, and M. Winey. 2007. Mps1 activation loop autophosphorylation enhances kinase activity. J. Biol. Chem. 282:30553-30561. doi:10.1074/jbc.M707063200
33. Meraldi, P., V.M. Draviam, and P.K. Sorger. 2004. Timing and checkpoints in the regulation of mitotic progression. Dev. Cell. 7:45-60. doi:10.1016/j.devcel.2004.06.006 (Pubitemid 39172687)
34. Musacchio, A., and E.D. Salmon. 2007. The spindle-assembly checkpoint in space and time. Nat. Rev. Mol. Cell Biol. 8:379-393. doi:10.1038/nrm2163
35. Obuse, C., O. Iwasaki, T. Kiyomitsu, G. Goshima, Y. Toyoda, and M. Yanagida. 2004. A conserved Mis12 centromere complex is linked to heterochromatic HP1 and outer kinetochore protein Zwint-1. Nat. Cell Biol. 6:1135-1141. doi:10.1038/ncb1187 (Pubitemid 39468016)
36. Raaijmakers, J.A., M.E. Tanenbaum, A.F. Maia, and R.H. Medema. 2009. RAMA1 is a novel kinetochore protein involved in kinetochore-microtubule attachment. J. Cell Sci. 122:2436-2445. doi:10.1242/jcs.051912
37. Reddy, S.K., M. Rape, W.A. Margansky, and M.W. Kirschner. 2007. Ubiquitination by the anaphase-promoting complex drives spindle checkpoint inactivation. Nature. 446:921-925. doi:10.1038/nature05734
38. Santaguida, S., A. Tighe, A.M. D'Alise, S.S. Taylor, and A. Musacchio. 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. doi:10.1083/jcb.201001036
39. Sliedrecht, T., C. Zhang, K.M. Shokat, and G.J. Kops. 2010. Chemical genetic inhibition of Mps1 in stable human cell lines reveals novel aspects of Mps1 function in mitosis. PLoS One. 5:e10251. doi:10.1371/journal.pone.0010251
40. 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. doi:10.1093/emboj/21.7.1723
41. Tighe, A., O. Staples, and S. Taylor. 2008. Mps1 kinase activity restrains anaphase during an unperturbed mitosis and targets Mad2 to kinetochores. J. Cell Biol. 181:893-901. doi:10.1083/jcb.200712028
42. Vasquez, R.J., B. Howell, A.M. Yvon, P. Wadsworth, and L. Cassimeris. 1997. Nanomolar concentrations of nocodazole alter microtubule dynamic instability in vivo and in vitro. Mol. Biol. Cell. 8:973-985.
43. Weiss, E., and M. Winey. 1996. The Saccharomyces cerevisiae spindle pole body duplication gene MPS1 is part of a mitotic checkpoint. J. Cell Biol. 132:111-123. doi:10.1083/jcb.132.1.111
44. Xia, G., X. Luo, T. Habu, J. Rizo, T. Matsumoto, and H. Yu. 2004. Conformation-specific binding of p31(comet) antagonizes the function of Mad2 in the spindle checkpoint. EMBO J. 23:3133-3143. doi:10.1038/sj.emboj.7600322
45. Yang, Z., A.E. Kenny, D.A. Brito, and C.L. Rieder. 2009. Cells satisfy the mitotic checkpoint in Taxol, and do so faster in concentrations that stabilize syntelic attachments. J. Cell Biol. 186:675-684. doi:10.1083/jcb. 200906150
46. Zhou, J., K. Gupta, J. Yao, K. Ye, D. Panda, P. Giannakakou, and H.C. Joshi. 2002. Paclitaxel-resistant human ovarian cancer cells undergo c-Jun NH2-terminal kinase-mediated apoptosis in response to noscapine. J. Biol. Chem. 277:39777-39785. doi:10.1074/jbc.M203927200