A TPR domain-containing N-terminal module of MPS1 is required for its kinetochore localization by Aurora B

Journal of Cell Biology

Volumn 201, Issue 2, 2013, Pages 217-231

  Nijenhuis, Wilco ^a   Von Castelmur, Eleonore ^b   Littler, Dene ^b   De Marco, Valeria ^b   Tromer, Eelco ^a,c   Vleugel, Mathijs ^a   Van Osch, Maria H J ^a   Snel, Berend ^c   Perrakis, Anastassis ^b   Kops, Geert J P L ^a  

^a UNIVERSITY MEDICAL CENTER UTRECHT   (Netherlands)

^b NETHERLANDS CANCER INSTITUTE   (Netherlands)

^c UTRECHT UNIVERSITY   (Netherlands)

Author keywords

[No Author keywords available]

Indexed keywords

AURORA B KINASE; CALPONIN; PROTEIN MPS 1; PROTEIN SERINE THREONINE KINASE; UNCLASSIFIED DRUG;

AMINO TERMINAL SEQUENCE; ARTICLE; BINDING AFFINITY; CENTROMERE; CONTROLLED STUDY; CRYSTAL STRUCTURE; HUMAN; HUMAN CELL; MOLECULAR MECHANICS; PRIORITY JOURNAL; PROTEIN BINDING; PROTEIN LOCALIZATION; PROTEIN PHOSPHORYLATION; PROTEIN STRUCTURE; SEQUENCE HOMOLOGY; TETRATRICOPEPTIDE REPEAT;

AMINO ACID SEQUENCE; CELL CYCLE CHECKPOINTS; CELL CYCLE PROTEINS; CONSERVED SEQUENCE; CRYSTALLOGRAPHY, X-RAY; EVOLUTION, MOLECULAR; HELA CELLS; HUMANS; KINETOCHORES; MICROTUBULES; MITOSIS; MOLECULAR SEQUENCE DATA; NUCLEAR PROTEINS; PROTEIN BINDING; PROTEIN STRUCTURE, SECONDARY; PROTEIN STRUCTURE, TERTIARY; PROTEIN TRANSPORT; PROTEIN-SERINE-THREONINE KINASES; PROTEIN-TYROSINE KINASES; STRUCTURE-ACTIVITY RELATIONSHIP;

EID: 84876697755     PISSN: 00219525     EISSN: 15408140     Source Type: Journal    
DOI: 10.1083/jcb.201210033     Document Type: Article

References (65)

1. Altschul, S.F., W. Gish, W. Miller, E.W. Myers, and D.J. Lipman. 1990. Basic local alignment search tool. J. Mol. Biol. 215:403-410.
2. Beaufils, S., J.G. Grossmann, A. Renault, and V.M. Bolanos-Garcia. 2008. Characterization of the tetratricopeptide-containing domain of BUB1, BUBR1, and PP5 proves that domain amphiphilicity over amino acid sequence specificity governs protein adsorption and interfacial activity. J. Phys. Chem. B. 112:7984-7991. http://dx.doi.org/10.1021/jp711222s
3. Blanc, E., P. Roversi, C. Vonrhein, C. Flensburg, S.M. Lea, and G. Bricogne. 2004. Refinement of severely incomplete structures with maximum likelihood in BUSTER-TNT. Acta Crystallogr. D Biol. Crystallogr. 60:2210-2221. http://dx.doi.org/10.1107/S0907444904016427
4. Bolanos-Garcia, V.M., S. Beaufils, A. Renault, J.G. Grossmann, S. Brewerton, M. Lee, A. Venkitaraman, and T.L. Blundell. 2005. The conserved N-terminal region of the mitotic checkpoint protein BUBR1: a putative TPR motif of high surface activity. Biophys. J. 89:2640-2649. http://dx.doi.org/10.1529/biophysj.105.063511
5. Bolanos-Garcia, V.M., T. Kiyomitsu, S. D'Arcy, D.Y. Chirgadze, J.G. Grossmann, D. Matak-Vinkovic, A.R. Venkitaraman, M. Yanagida, C.V. Robinson, and T.L. Blundell. 2009. The crystal structure of the N-terminal region of BUB1 provides insight into the mechanism of BUB1 recruitment to kinetochores. Structure. 17:105-116. http://dx.doi.org/10.1016/j.str.2008.10.015
6. Bolanos-Garcia, V.M., T. Lischetti, D. Matak-Vinkovic, E. Cota, P.J. Simpson, D.Y. Chirgadze, D.R. Spring, C.V. Robinson, J. Nilsson, and T.L. Blundell. 2011. Structure of a Blinkin-BUBR1 complex reveals an interaction crucial for kinetochore-mitotic checkpoint regulation via an unanticipated binding Site. Structure. 19:1691-1700. http://dx.doi.org/10.1016/j.str.2011.09.017
7. Chao, W.C., K. Kulkarni, Z. Zhang, E.H. Kong, and D. Barford. 2012. Structure of the mitotic checkpoint complex. Nature. 484:208-213. http://dx.doi.org/10.1038/nature10896
8. Cowtan, K. 2006. The Buccaneer software for automated model building. 1. Tracing protein chains. Acta Crystallogr. D Biol. Crystallogr. 62:1002- 1011. http://dx.doi.org/10.1107/S0907444906022116
9. D'Arcy, S., O.R. Davies, T.L. Blundell, and V.M. Bolanos-Garcia. 2010. Defining the molecular basis of BubR1 kinetochore interactions and APC/C-CDC20 inhibition. J. Biol. Chem. 285:14764-14776. http://dx.doi.org/10.1074/jbc.M109.082016
10. Daub, H., J.V. Olsen, M. Bairlein, F. Gnad, F.S. Oppermann, R. Körner, Z. Greff, G. Kéri, O. Stemmann, and M. Mann. 2008. Kinase-selectiveenrichment enables quantitative phosphoproteomics of the kinome across the cell cycle. Mol. Cell. 31:438-448. http://dx.doi.org/10.1016/j.molcel.2008.07.007
11. DeLuca, K.F., S.M. Lens, and J.G. DeLuca. 2011. Temporal changes in Hec1 phosphorylation control kinetochore-microtubule attachment stability during mitosis. J. Cell Sci. 124:622-634. http://dx.doi.org/10.1242/jcs.072629
12. Dephoure, N., C. Zhou, J. Villén, S.A. Beausoleil, C.E. Bakalarski, S.J. Elledge, and S.P. Gygi. 2008. A quantitative atlas of mitotic phosphorylation. Proc. Natl. Acad. Sci. USA. 105:10762-10767. http://dx.doi.org/10.1073/pnas.0805139105
13. 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. http://dx.doi.org/10.1083/jcb.200208091
14. Dulla, K., H. Daub, R. Hornberger, E.A. Nigg, and R. Körner. 2010. Quantitative site-specific phosphorylation dynamics of human protein kinases during mitotic progression. Mol. Cell. Proteomics. 9:1167-1181. http://dx.doi.org/10.1074/mcp.M900335-MCP200
15. Eddy, S.R. 2011. Accelerated Profile HMM Searches. PLOS Comput. Biol. 7:e1002195. http://dx.doi.org/10.1371/journal.pcbi.1002195
16. Emsley, P., B. Lohkamp, W.G. Scott, and K. Cowtan. 2010. Features and development of Coot. Acta Crystallogr. D Biol. Crystallogr. 66:486-501. http://dx.doi.org/10.1107/S0907444910007493
17. Evans, P. 2006. Scaling and assessment of data quality. Acta Crystallogr. D Biol. Crystallogr. 62:72-82. http://dx.doi.org/10.1107/S0907444905036693
18. Guimaraes, G.J., Y. Dong, B.F. McEwen, and J.G. Deluca. 2008. Kinetochoremicrotubule attachment relies on the disordered N-terminal tail domain of Hec1. Curr. Biol. 18:1778-1784. http://dx.doi.org/10.1016/j.cub.2008.08.012
19. Hached, K., S.Z. Xie, E. Buffin, D. Cladière, C. Rachez, M. Sacras, P.K. Sorger, and K. Wassmann. 2011. Mps1 at kinetochores is essential for female mouse meiosis I. Development. 138:2261-2271. http://dx.doi.org/10.1242/dev.061317
20. Hardwick, K.G., R.C. Johnston, D.L. Smith, and A.W. Murray. 2000. MAD3 encodes a novel component of the spindle checkpoint which interacts with Bub3p, Cdc20p, and Mad2p. J. Cell Biol. 148:871-882. http://dx.doi.org/10.1083/jcb.148.5.871
21. 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 O-Mad2 to the Mad1-C-Mad2 core complex. J. Cell Biol. 190:25-34. http://dx.doi.org/10.1083/jcb.201002133
22. Holm, L., and P. Rosenström. 2010. Dali server: conservation mapping in 3D. Nucleic Acids Res. 38(Suppl. 2):W545-W549. http://dx.doi.org/10.1093/nar/gkq366
23. Janicki, S.M., T. Tsukamoto, S.E. Salghetti, W.P. Tansey, R. Sachidanandam, K.V. Prasanth, T. Ried, Y. Shav-Tal, E. Bertrand, R.H. Singer, and D.L. Spector. 2004. From silencing to gene expression: real-time analysis in single cells. Cell. 116:683-698. http://dx.doi.org/10.1016/S0092-8674(04)00171-0
24. Janssen, A., M. van der Burg, K. Szuhai, G.J. Kops, and R.H. Medema. 2011. Chromosome segregation errors as a cause of DNA damage and structural chromosome aberrations. Science. 333:1895-1898. http://dx.doi.org/10.1126/science.1210214
25. Jelluma, N., A.B. Brenkman, I. McLeod, J.R. Yates III, D.W. Cleveland, R.H. Medema, and G.J. Kops. 2008a. Chromosomal instability by inefficient Mps1 auto-activation due to a weakened mitotic checkpoint and lagging chromosomes. PLoS ONE. 3:e2415. http://dx.doi.org/10.1371/journal.pone.0002415
26. 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. 2008b. 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
27. Jelluma, N., T.B. Dansen, T. Sliedrecht, N.P. Kwiatkowski, and G.J. Kops. 2010. Release of Mps1 from kinetochores is crucial for timely anaphase onset. J. Cell Biol. 191:281-290. http://dx.doi.org/10.1083/jcb.201003038
28. Katoh, K., and D.M. Standley. 2013. MAFFT multiple sequence alignment software version 7: Improvements in performance and usability. Mol. Biol. Evol. In press http://dx.doi.org/10.1093/molbev/mst010
29. 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
30. Klebig, C., D. Korinth, and P. Meraldi. 2009. Bub1 regulates chromosome segregation in a kinetochore-independent manner. J. Cell Biol. 185:841-858. http://dx.doi.org/10.1083/jcb.200902128
31. Kops, G.J.P.L., and J.V. Shah. 2012. Connecting up and clearing out: how kinetochore attachment silences the spindle assembly checkpoint. Chromosoma. 121:509-525. http://dx.doi.org/10.1007/s00412-012-0378-5
32. Krenn, V., A. Wehenkel, X. Li, S. Santaguida, and A. Musacchio. 2012. Structural analysis reveals features of the spindle checkpoint kinase Bub1-kinetochore subunit Knl1 interaction. J. Cell Biol. 196:451-467. http://dx.doi.org/10.1083/jcb.201110013
33. 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. http://dx.doi.org/10.1083/jcb.201006080
34. Langer, G., S.X. Cohen, V.S. Lamzin, and A. Perrakis. 2008. Automated macromolecular model building for X-ray crystallography using ARP/wARP version 7. Nat. Protoc. 3:1171-1179. http://dx.doi.org/10.1038/nprot.2008.91
35. Lee, S., P. Thebault, L. Freschi, S. Beaufils, T.L. Blundell, C.R. Landry, V.M. Bolanos-Garcia, and S. Elowe. 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. http://dx.doi.org/10.1074/jbc.M111.307355
36. Leslie, A.G. 2006. The integration of macromolecular diffraction data. Acta Crystallogr. D Biol. Crystallogr. 62:48-57. http://dx.doi.org/10.1107/S0907444905039107
37. Letunic, I., and P. Bork. 2007. Interactive Tree Of Life (iTOL): an online tool for phylogenetic tree display and annotation. Bioinformatics. 23:127-128. http://dx.doi.org/10.1093/bioinformatics/btl529
38. 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 CENPE from kinetochores. Mol. Biol. Cell. 14:1638-1651. http://dx.doi.org/10.1091/mbc.02-05-0074
39. 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. http://dx.doi.org/10.1083/jcb.201001050
40. 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. http://dx.doi.org/10.1126/science.1075596
41. McCoy, A.J., R.W. Grosse-Kunstleve, P.D. Adams, M.D. Winn, L.C. Storoni, and R.J. Read. 2007. Phaser crystallographic software. J. Appl. Cryst. 40:658-674. http://dx.doi.org/10.1107/S0021889807021206
42. Meraldi, P., V.M. Draviam, and P.K. Sorger. 2004. Timing and checkpoints in the regulation of mitotic progression. Dev. Cell. 7:45-60. http://dx.doi.org/10.1016/j.devcel.2004.06.006
43. Miller, S.A., M.L. Johnson, and P.T. Stukenberg. 2008. Kinetochore attachments require an interaction between unstructured tails on microtubules and Ndc80(Hec1). Curr. Biol. 18:1785-1791. http://dx.doi.org/10.1016/j.cub.2008.11.007
44. Morin, V., S. Prieto, S. Melines, S. Hem, M. Rossignol, T. Lorca, J. Espeut, N. Morin, and A. Abrieu. 2012. CDK-dependent potentiation of MPS1 kinase activity is essential to the mitotic checkpoint. Curr. Biol. 22:289- 295. http://dx.doi.org/10.1016/j.cub.2011.12.048
45. Murshudov, G.N., P. Skubák, A.A. Lebedev, N.S. Pannu, R.A. Steiner, R.A. Nicholls, M.D. Winn, F. Long, and A.A. Vagin. 2011. REFMAC5 for the refinement of macromolecular crystal structures. Acta Crystallogr. D Biol. Crystallogr. 67:355-367. http://dx.doi.org/10.1107/S0907444911001314
46. Musacchio, A., and E.D. Salmon. 2007. The spindle-assembly checkpoint in space and time. Nat. Rev. Mol. Cell Biol. 8:379-393. http://dx.doi.org/10.1038/nrm2163
47. Newman, J., D. Egan, T.S. Walter, R. Meged, I. Berry, M. Ben Jelloul, J.L. Sussman, D.I. Stuart, and A. Perrakis. 2005. Towards rationalization of crystallization screening for small- to medium-sized academic laboratories: the PACT/JCSG+ strategy. Acta Crystallogr. D Biol. Crystallogr. 61:1426-1431. http://dx.doi.org/10.1107/S0907444905024984
48. Oppermann, F.S., F. Gnad, J.V. Olsen, R. Hornberger, Z. Greff, G. Kéri, M. Mann, and H. Daub. 2009. Large-scale proteomics analysis of the human kinome. Mol. Cell. Proteomics. 8:1751-1764. http://dx.doi.org/10.1074/mcp.M800588-MCP200
49. 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. http://dx.doi.org/10.1083/jcb.201001036
50. Santaguida, S., C. Vernieri, F. Villa, A. Ciliberto, and A. Musacchio. 2011. Evidence that Aurora B is implicated in spindle checkpoint signalling independently of error correction. EMBO J. 30:1508-1519. http://dx.doi.org/10.1038/emboj.2011.70
51. Saurin, A.T., M.S. van der Waal, R.H. Medema, S.M. Lens, and G.J. Kops. 2011. Aurora B potentiates Mps1 activation to ensure rapid checkpoint establishment at the onset of mitosis. Nat Commun. 2:316. http://dx.doi.org/10.1038/ncomms1319
52. 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. http://dx.doi.org/10.1371/journal.pone.0010251
53. Stamatakis, A., T. Ludwig, and H. Meier. 2005. RAxML-III: a fast program for maximum likelihood-based inference of large phylogenetic trees. Bioinformatics. 21:456-463. http://dx.doi.org/10.1093/bioinformatics/bti191
54. 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
55. Stucke, V.M., C. Baumann, and E.A. Nigg. 2004. Kinetochore localization and microtubule interaction of the human spindle checkpoint kinase Mps1. Chromosoma. 113:1-15. http://dx.doi.org/10.1007/s00412-004-0288-2
56. Sudakin, V., G.K. Chan, and T.J. Yen. 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. http://dx.doi.org/10.1083/jcb.200102093
57. Suijkerbuijk, S.J., T.J. van Dam, G.E. Karagöz, E. von Castelmur, N.C. Hubner, A.M. Duarte, M. Vleugel, A. Perrakis, S.G. Rüdiger, B. Snel, and G.J. Kops. 2012. The vertebrate mitotic checkpoint protein BUBR1 is an unusual pseudokinase. Dev. Cell. 22:1321-1329. http://dx.doi.org/10.1016/j.devcel.2012.03.009
58. 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. http://dx.doi.org/10.1083/jcb.200712028
59. Tooley, J., and P.T. Stukenberg. 2011. The Ndc80 complex: integrating the kinetochore's many movements. Chromosome Res. 19:377-391. http://dx.doi.org/10.1007/s10577-010-9180-5
60. Vink, M., M. Simonetta, P. Transidico, K. Ferrari, M. Mapelli, A. De Antoni, L. Massimiliano, A. Ciliberto, M. Faretta, E.D. Salmon, and A. Musacchio. 2006. In vitro FRAP identifies the minimal requirements for Mad2 kinetochore dynamics. Curr. Biol. 16:755-766. http://dx.doi.org/10.1016/j.cub.2006.03.057
61. Vleugel, M., E. Hoogendoorn, B. Snel, and G.J. Kops. 2012. Evolution and function of the mitotic checkpoint. Dev. Cell. 23:239-250. http://dx.doi.org/10.1016/j.devcel.2012.06.013
62. Vonrhein, C., E. Blanc, P. Roversi, and G. Bricogne. 2007. Automated structure solution with autoSHARP. Methods Mol. Biol. 364:215-230.
63. Xu, Q., S. Zhu, W. Wang, X. Zhang, W. Old, N. Ahn, and X. Liu. 2009. Regulation of kinetochore recruitment of two essential mitotic spindle checkpoint proteins by Mps1 phosphorylation. Mol. Biol. Cell. 20:10-20. http://dx.doi.org/10.1091/mbc.E08-03-0324
64. Zemp, I., T. Wild, M.F. O'Donohue, F. Wandrey, B. Widmann, P.E. Gleizes, and U. Kutay. 2009. Distinct cytoplasmic maturation steps of 40S ribosomal subunit precursors require hRio2. J. Cell Biol. 185:1167-1180. http://dx.doi.org/10.1083/jcb.200904048
65. Zwart, P.H., R.W. Grosse-Kunstleve, A.A. Lebedev, G.N. Murshudov, and P.D. Adams. 2008. Surprises and pitfalls arising from (pseudo)symmetry. Acta Crystallogr. D Biol. Crystallogr. 64:99-107. http://dx.doi.org/10.1107/S090744490705531X