MPH1 kinetochore localization is crucial and upstream in the hierarchy of spindle assembly checkpoint protein recruitment to kinetochores

Journal of Cell Science

Volumn 125, Issue 20, 2012, Pages 4720-4727

  Heinrich, Stephanie ^a   Windecker, Hanna ^a,b   Hustedt, Nicole ^a,c   Hauf, Silke ^a  

^a FRIEDRICH MIESCHER LABORATORY OF THE MAX PLANCK SOCIETY   (Germany)

^b Septomics Research Centre   (Germany)

^c FRIEDRICH MIESCHER INSTITUTE FOR BIOMEDICAL RESEARCH   (Switzerland)

Author keywords

Kinetochore; Mitosis; MPH1; Spindle assembly checkpoint

Indexed keywords

AURORA A KINASE; ENZYME; MPH1 ENZYME; UNCLASSIFIED DRUG;

ARTICLE; CELL DIVISION; CENTROMERE; CHROMOSOME; M PHASE CELL CYCLE CHECKPOINT; MITOSIS SPINDLE; PRIORITY JOURNAL; PROTEIN FUNCTION; SIGNAL TRANSDUCTION;

CELL CYCLE PROTEINS; KINETOCHORES; M PHASE CELL CYCLE CHECKPOINTS; MUTATION; PROTEIN KINASES; PROTEIN-SERINE-THREONINE KINASES; SCHIZOSACCHAROMYCES; SCHIZOSACCHAROMYCES POMBE PROTEINS; SIGNAL TRANSDUCTION;

SCHIZOSACCHAROMYCETACEAE;

EID: 84868097717     PISSN: 00219533     EISSN: 14779137     Source Type: Journal    
DOI: 10.1242/jcs.110387     Document Type: Article

References (72)

1. Abrieu, A., Magnaghi-Jaulin, L., Kahana, J. A., Peter, M., Castro, A., Vigneron, S., Lorca, T., Cleveland, D. W. and Labbé, J. C. (2001). Mps1 is a kinetochoreassociated kinase essential for the vertebrate mitotic checkpoint. Cell 106, 83-93.
2. Bähler, J., Wu, J. Q., Longtine, M. S., Shah, N. G., McKenzie, A., 3rd, Steever, A. B., Wach, A., Philippsen, P. and Pringle, J. R. (1998). Heterologous modules for efficient and versatile PCR-based gene targeting in Schizosaccharomyces pombe. Yeast 14, 943-951.
3. Basi, G., Schmid, E. and Maundrell, K. (1993). TATA box mutations in the Schizosaccharomyces pombe nmt1 promoter affect transcription efficiency but not the transcription start point or thiamine repressibility. Gene 123, 131-136.
4. Bolanos-Garcia, V. M., Lischetti, T., Matak-Vinković, D., Cota, E., Simpson, P. J., Chirgadze, D. Y., Spring, D. R., Robinson, C. V., Nilsson, J. and Blundell, T. L. (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.
5. Burke, D. J. and Stukenberg, P. T. (2008). Linking kinetochore-microtubule binding to the spindle checkpoint. Dev. Cell 14, 474-479.
6. Chen, R. H. (2002). BubR1 is essential for kinetochore localization of other spindle checkpoint proteins and its phosphorylation requires Mad1. J. Cell Biol. 158, 487-496.
7. De Antoni, A., Pearson, C. G., Cimini, D., Canman, J. C., Sala, V., Nezi, L., Mapelli, M., Sironi, L., Faretta, M., Salmon, E. D. et al. (2005). The Mad1/Mad2 complex as a template for Mad2 activation in the spindle assembly checkpoint. Curr. Biol. 15, 214-225.
8. Dischinger, S., Krapp, A., Xie, L., Paulson, J. R. and Simanis, V. (2008). Chemical genetic analysis of the regulatory role of Cdc2p in the S. pombe septation initiation network. J. Cell Sci. 121, 843-853.
9. Essex, A., Dammermann, A., Lewellyn, L., Oegema, K. and Desai, A. (2009). Systematic analysis in Caenorhabditis elegans reveals that the spindle checkpoint is composed of two largely independent branches. Mol. Biol. Cell 20, 1252-1267.
10. Fraschini, R., Beretta, A., Lucchini, G. and Piatti, S. (2001). Role of the kinetochore protein Ndc10 in mitotic checkpoint activation in Saccharomyces cerevisiae. Mol. Genet. Genomics 266, 115-125.
11. Garcia, M. A., Koonrugsa, N. and Toda, T. (2002). Spindle-kinetochore attachment requires the combined action of Kin I-like Klp5/6 and Alp14/Dis1-MAPs in fission yeast. EMBO J. 21, 6015-6024.
12. Gardner, R. D., Poddar, A., Yellman, C., Tavormina, P. A., Monteagudo, M. C. and Burke, D. J. (2001). The spindle checkpoint of the yeast Saccharomyces cerevisiae requires kinetochore function and maps to the CBF3 domain. Genetics 157, 1493-1502.
13. Gillett, E. S., Espelin, C. W. and Sorger, P. K. (2004). Spindle checkpoint proteins and chromosome-microtubule attachment in budding yeast. J. Cell Biol. 164, 535-546.
14. Hached, K., Xie, S. Z., Buffin, E., Cladie're, D., Rachez, C., Sacras, M., Sorger, P. K. and Wassmann, K. (2011). Mps1 at kinetochores is essential for female mouse meiosis I. Development 138, 2261-2271.
15. Hagan, I. and Yanagida, M. (1990). Novel potential mitotic motor protein encoded by the fission yeast cut7+ gene. Nature 347, 563-566.
16. Hardwick, K. G., Weiss, E., Luca, F. C., Winey, M. and Murray, A. W. (1996). Activation of the budding yeast spindle assembly checkpoint without mitotic spindle disruption. Science 273, 953-956.
17. Hauf, S., Biswas, A., Langegger, M., Kawashima, S. A., Tsukahara, T. and Watanabe, Y. (2007). Aurora controls sister kinetochore mono-orientation and homolog bi-orientation in meiosis-I. EMBO J. 26, 4475-4486.
18. Hiraoka, Y., Toda, T. and Yanagida, M. (1984). The NDA3 gene of fission yeast encodes beta-tubulin: a cold-sensitive nda3 mutation reversibly blocks spindle formation and chromosome movement in mitosis. Cell 39, 349-358.
19. Howell, B. J., Moree, B., Farrar, E. M., Stewart, S., Fang, G. and Salmon, E. D. (2004). Spindle checkpoint protein dynamics at kinetochores in living cells. Curr. Biol. 14, 953-964.
20. Ito, D., Saito, Y. and Matsumoto, T. (2012). Centromere-tethered Mps1 pombe homolog (Mph1) kinase is a sufficient marker for recruitment of the spindle checkpoint protein Bub1, but not Mad1. Proc. Natl. Acad. Sci. USA 109, 209-214.
21. Jelluma, N., Dansen, T. B., Sliedrecht, T., Kwiatkowski, N. P. and Kops, G. J. (2010). Release of Mps1 from kinetochores is crucial for timely anaphase onset. J. Cell Biol. 191, 281-290.
22. Kadura, S., He, X., Vanoosthuyse, V., Hardwick, K. G. and Sazer, S. (2005). The A78V mutation in the Mad3-like domain of Schizosaccharomyces pombe Bub1p perturbs nuclear accumulation and kinetochore targeting of Bub1p, Bub3p, and Mad3p and spindle assembly checkpoint function. Mol. Biol. Cell 16, 385-395.
23. Kallio, M. J., McCleland, M. L., Stukenberg, P. T. and Gorbsky, G. J. (2002). Inhibition of aurora B kinase blocks chromosome segregation, overrides the spindle checkpoint, and perturbs microtubule dynamics in mitosis. Curr. Biol. 12, 900-905.
24. Kawashima, S. A., Tsukahara, T., Langegger, M., Hauf, S., Kitajima, T. S. and Watanabe, Y. (2007). Shugoshin enables tension-generating attachment of kinetochores by loading Aurora to centromeres. Genes Dev. 21, 420-435.
25. Kawashima, S. A., Yamagishi, Y., Honda, T., Ishiguro, K. and Watanabe, Y. (2010). Phosphorylation of H2A by Bub1 prevents chromosomal instability through localizing shugoshin. Science 327, 172-177.
26. Kemmler, S., Stach, M., Knapp, M., Ortiz, J., Pfannstiel, J., Ruppert, T. and Lechner, J. (2009). Mimicking Ndc80 phosphorylation triggers spindle assembly checkpoint signalling. EMBO J. 28, 1099-1110.
27. Kerscher, O., Crotti, L. B. and Basrai, M. A. (2003). Recognizing chromosomes in trouble: association of the spindle checkpoint protein Bub3p with altered kinetochores and a unique defective centromere. Mol. Cell. Biol. 23, 6406-6418.
28. Kiyomitsu, T., Obuse, C. and Yanagida, M. (2007). Human Blinkin/AF15q14 is required for chromosome alignment and the mitotic checkpoint through direct interaction with Bub1 and BubR1. Dev. Cell 13, 663-676.
29. Kiyomitsu, T., Murakami, H. and Yanagida, M. (2011). Protein interaction domain mapping of human kinetochore protein Blinkin reveals a consensus motif for binding of spindle assembly checkpoint proteins Bub1 and BubR1. Mol. Cell. Biol. 31, 998-1011.
30. Klebig, C., Korinth, D. and Meraldi, P. (2009). Bub1 regulates chromosome segregation in a kinetochore-independent manner. J. Cell Biol. 185, 841-858.
31. Koch, A., Rode, H. B., Richters, A., Rauh, D. and Hauf, S. (2012). A chemical genetic approach for covalent inhibition of analogue-sensitive aurora kinase. ACS Chem. Biol. 7, 723-731.
32. Krenn, V., Wehenkel, A., Li, X., Santaguida, S. and Musacchio, A. (2012). Structural analysis reveals features of the spindle checkpoint kinase Bub1-kinetochore subunit Knl1 interaction. J. Cell Biol. 196, 451-467.
33. Kulukian, A., Han, J. S. and Cleveland, D. W. (2009). Unattached kinetochores catalyze production of an anaphase inhibitor that requires a Mad2 template to prime Cdc20 for BubR1 binding. Dev. Cell 16, 105-117.
34. Liu, S. T., Chan, G. K., Hittle, J. C., Fujii, G., Lees, E. and Yen, T. J. (2003). Human MPS1 kinase is required for mitotic arrest induced by the loss of CENP-E from kinetochores. Mol. Biol. Cell 14, 1638-1651.
35. Liu, D., Vader, G., Vromans, M. J., Lampson, M. A. and Lens, S. M. (2009). Sensing chromosome bi-orientation by spatial separation of aurora B kinase from kinetochore substrates. Science 323, 1350-1353.
36. London, N., Ceto, S., Ranish, J. A. and Biggins, S. (2012). Phosphoregulation of Spc105 by Mps1 and PP1 regulates Bub1 localization to kinetochores. Curr. Biol. 22, 900-906.
37. Maciejowski, J., George, K. A., Terret, M. E., Zhang, C., Shokat, K. M. and Jallepalli, P. V. (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.
38. Maldonado, M. and Kapoor, T. M. (2011). Constitutive Mad1 targeting to kinetochores uncouples checkpoint signalling from chromosome biorientation. Nat. Cell Biol. 13, 475-482.
39. Mapelli, M. and Musacchio, A. (2007). MAD contortions: conformational dimerization boosts spindle checkpoint signaling. Curr. Opin. Struct. Biol. 17, 716-725.
40. Maresca, T. J. and Salmon, E. D. (2010). Welcome to a new kind of tension: translating kinetochore mechanics into a wait-anaphase signal. J. Cell Sci. 123, 825-835.
41. Martin-Lluesma, S., Stucke, V. M. and Nigg, E. A. (2002). Role of Hec1 in spindle checkpoint signaling and kinetochore recruitment of Mad1/Mad2. Science 297, 2267-2270.
42. Maure, J. F., Kitamura, E. and Tanaka, T. U. (2007). Mps1 kinase promotes sisterkinetochore bi-orientation by a tension-dependent mechanism. Curr. Biol. 17, 2175-2182.
43. McCleland, M. L., Gardner, R. D., Kallio, M. J., Daum, J. R., Gorbsky, G. J., Burke, D. J. and Stukenberg, P. T. (2003). The highly conserved Ndc80 complex is required for kinetochore assembly, chromosome congression, and spindle checkpoint activity. Genes Dev. 17, 101-114.
44. Meraldi, P., Draviam, V. M. and Sorger, P. K. (2004). Timing and checkpoints in the regulation of mitotic progression. Dev. Cell 7, 45-60.
45. Millband, D. N. and Hardwick, K. G. (2002). Fission yeast Mad3p is required for Mad2p to inhibit the anaphase-promoting complex and localizes to kinetochores in a Bub1p-, Bub3p-, and Mph1p-dependent manner. Mol. Cell. Biol. 22, 2728-2742.
46. Moreno, S., Hayles, J. and Nurse, P. (1989). Regulation of p34cdc2 protein kinase during mitosis. Cell 58, 361-372.
47. Moreno, S., Klar, A. and Nurse, P. (1991). Molecular genetic analysis of fission yeast Schizosaccharomyces pombe. Methods Enzymol. 194, 795-823.
48. Mulvihill, D. P., Petersen, J., Ohkura, H., Glover, D. M. and Hagan, I. M. (1999). Plo1 kinase recruitment to the spindle pole body and its role in cell division in Schizosaccharomyces pombe. Mol. Biol. Cell 10, 2771-2785.
49. Musacchio, A. and Hardwick, K. G. (2002). The spindle checkpoint: structural insights into dynamic signalling. Nat. Rev. Mol. Cell Biol. 3, 731-741.
50. Musacchio, A. and Salmon, E. D. (2007). The spindle-assembly checkpoint in space and time. Nat. Rev. Mol. Cell Biol. 8, 379-393.
51. Nabetani, A., Koujin, T., Tsutsumi, C., Haraguchi, T. and Hiraoka, Y. (2001). A conserved protein, Nuf2, is implicated in connecting the centromere to the spindle during chromosome segregation: a link between the kinetochore function and the spindle checkpoint. Chromosoma 110, 322-334.
52. Nezi, L. and Musacchio, A. (2009). Sister chromatid tension and the spindle assembly checkpoint. Curr. Opin. Cell Biol. 21, 785-795.
53. Peters, J. M. (2006). The anaphase promoting complex/cyclosome: a machine designed to destroy. Nat. Rev. Mol. Cell Biol. 7, 644-656.
54. Petersen, J. and Hagan, I. M. (2003). S. pombe aurora kinase/survivin is required for chromosome condensation and the spindle checkpoint attachment response. Curr. Biol. 13, 590-597.
55. Rieder, C. L., Cole, R. W., Khodjakov, A. and Sluder, G. (1995). The checkpoint delaying anaphase in response to chromosome monoorientation is mediated by an inhibitory signal produced by unattached kinetochores. J. Cell Biol. 130, 941-948.
56. Santaguida, S., Tighe, A., D'Alise, A. M., Taylor, S. S. and 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.
57. Santaguida, S., Vernieri, C., Villa, F., Ciliberto, A. and Musacchio, A. (2011). Evidence that Aurora B is implicated in spindle checkpoint signalling independently of error correction. EMBO J. 30, 1508-1519.
58. Saurin, A. T., van der Waal, M. S., Medema, R. H., Lens, S. M. and Kops, G. J. (2011). Aurora B potentiates Mps1 activation to ensure rapid checkpoint establishment at the onset of mitosis. Nat. Commun. 2, 316.
59. Sharp-Baker, H. and Chen, R. H. (2001). Spindle checkpoint protein Bub1 is required for kinetochore localization of Mad1, Mad2, Bub3, and CENP-E, independently of its kinase activity. J. Cell Biol. 153, 1239-1250.
60. Shepperd, L. A., Meadows, J. C., Sochaj, A. M., Lancaster, T. C., Zou, J., Buttrick, G. J., Rappsilber, J., Hardwick, K. G. and Millar, J. B. (2012). Phosphodependent recruitment of Bub1 and Bub3 to Spc7/KNL1 by Mph1 kinase maintains the spindle checkpoint. Curr. Biol. 22, 891-899.
61. Skoufias, D. A., Andreassen, P. R., Lacroix, F. B., Wilson, L. and Margolis, R. L. (2001). Mammalianmad2 and bub1/bubR1 recognize distinct spindle-attachment and kinetochore-tension checkpoints. Proc. Natl. Acad. Sci. USA 98, 4492-4497.
62. Sliedrecht, T., Zhang, C., Shokat, K. M. and Kops, G. J. (2010). Chemical genetic inhibition of Mps1 in stable human cell lines reveals novel aspects of Mps1 function in mitosis. PLoS ONE 5, e10251.
63. Tsukahara, T., Tanno, Y. and Watanabe, Y. (2010). Phosphorylation of the CPC by Cdk1 promotes chromosome bi-orientation. Nature 467, 719-723.
64. Vanoosthuyse, V., Valsdottir, R., Javerzat, J. P. and Hardwick, K. G. (2004). Kinetochore targeting of fission yeast Mad and Bub proteins is essential for spindle checkpoint function but not for all chromosome segregation roles of Bub1p. Mol. Cell. Biol. 24, 9786-9801.
65. Vanoosthuyse, V., Meadows, J. C., van der Sar, S. J., Millar, J. B. and Hardwick, K. G. (2009). Bub3p facilitates spindle checkpoint silencing in fission yeast. Mol. Biol. Cell 20, 5096-5105.
66. Vázquez-Novelle, M. D. and Petronczki, M. (2010). Relocation of the chromosomal passenger complex prevents mitotic checkpoint engagement at anaphase. Curr. Biol. 20, 1402-1407.
67. Vigneron, S., Prieto, S., Bernis, C., Labbé, J. C., Castro, A. and Lorca, T. (2004). Kinetochore localization of spindle checkpoint proteins: who controls whom? Mol. Biol. Cell 15, 4584-4596.
68. Walczak, C. E., Cai, S. and Khodjakov, A. (2010). Mechanisms of chromosome behaviour during mitosis. Nat. Rev. Mol. Cell Biol. 11, 91-102.
69. Weiss, E. and Winey, M. (1996). The Saccharomyces cerevisiae spindle pole body duplication gene MPS1 is part of a mitotic checkpoint. J. Cell Biol. 132, 111-123.
70. Windecker, H., Langegger, M., Heinrich, S. and Hauf, S. (2009). Bub1 and Bub3 promote the conversion from monopolar to bipolar chromosome attachment independently of shugoshin. EMBO Rep. 10, 1022-1028.
71. Yamagishi, Y., Yang, C. H., Tanno, Y. and Watanabe, Y. (2012). MPS1/Mph1 phosphorylates the kinetochore protein KNL1/Spc7 to recruit SAC components. Nat. Cell Biol. 14, 746-752.
72. Zhao, Y. and Chen, R. H. (2006). Mps1 phosphorylation by MAP kinase is required for kinetochore localization of spindle-checkpoint proteins. Curr. Biol. 16, 1764-1769.