Regulation of kinetochore recruitment of two essential mitotic spindle checkpoint proteins by Mpsl phosphorylation

Molecular Biology of the Cell

Volumn 20, Issue 1, 2009, Pages 10-20

  Xu, Quanbin ^a,b   Zhu, Songcheng ^a,b   Wang, Wei ^a   Zhang, Xiaojuan ^a   Old, William ^a   Ahn, Natalie ^a   Liu, Xuedong ^a  

^a UNIVERSITY OF COLORADO   (United States)

^b FUDAN UNIVERSITY   (China)

Author keywords

[No Author keywords available]

Indexed keywords

PROTEIN KINASE; PROTEIN KINASE MPS1; UNCLASSIFIED DRUG; CALCIUM BINDING PROTEIN; CELL CYCLE PROTEIN; HYBRID PROTEIN; MAD2L1 PROTEIN, HUMAN; PROTEIN SERINE THREONINE KINASE; REPRESSOR PROTEIN; SMALL INTERFERING RNA; TTK PROTEIN, HUMAN;

ARTICLE; AUTOPHOSPHORYLATION; CELLULAR DISTRIBUTION; CENTROMERE; CONTROLLED STUDY; ENZYME ACTIVITY; ENZYME PHOSPHORYLATION; GENE MUTATION; HUMAN; HUMAN CELL; IN VITRO STUDY; IN VIVO STUDY; MITOSIS SPINDLE; PRIORITY JOURNAL; PROTEIN LOCALIZATION; PROTEIN TARGETING; SIGNAL TRANSDUCTION; AMINO ACID SEQUENCE; ANIMAL; CELL LINE; GENETICS; METABOLISM; MOLECULAR GENETICS; PHOSPHORYLATION; PHYSIOLOGY;

AMINO ACID SEQUENCE; ANIMALS; CALCIUM-BINDING PROTEINS; CELL CYCLE PROTEINS; CELL LINE; HUMANS; KINETOCHORES; MITOTIC SPINDLE APPARATUS; MOLECULAR SEQUENCE DATA; PHOSPHORYLATION; PROTEIN-SERINE-THREONINE KINASES; RECOMBINANT FUSION PROTEINS; REPRESSOR PROTEINS; RNA, SMALL INTERFERING; SIGNAL TRANSDUCTION;

EID: 63049092834     PISSN: 10591524     EISSN: None     Source Type: Journal    
DOI: 10.1091/mbc.E08-03-0324     Document Type: Article

References (49)

1. Abrieu, A., Magnaghi-Jaulin, L., Kahana, J. A., Peter, M., Castro, A., Vigneron, S., Lorca, T., Cleveland, D. W., and Labbe, J. C. (2001). Mps1 is a kinetochore-associated kinase essential for the vertebrate mitotic checkpoint. Cell 106, 83-93.
2. Amon, A. (1999). The spindle checkpoint. Curr. Opin. Genet. Dev. 9, 69-75.
3. Boyle, W. J., van der Geer, P., and Hunter, T. (1991). Phosphopeptide mapping and phosphoamino acid analysis by two-dimensional separation on thin-layer cellulose plates. Methods Enzymol. 201, 110-149.
4. Cui, Y., and Guadagno, T. M. (2008). B-Raf(V600E) signaling deregulates the mitotic spindle checkpoint through stabilizing Mps1 levels in melanoma cells. Oncogene 27, 3122-3133.
5. DeLuca, J. G., Dong, Y., Hergert, P., Strauss, J., Hickey, J. M., Salmon, E. D., and McEwen, B. F. (2005). Hec1 and nuf2 are core components of the kinet-ochore outer plate essential for organizing microtubule attachment sites. Mol. Biol. Cell 16,519-531.
6. Draviam, V. M., Xie, S., and Sorger, P. K. (2004). Chromosome segregation and genomic stability. Curr. Opin. Genet. Dev. 14, 120-125.
7. Fang, G., Yu, H., and Kirschner, M. W. (1998). The checkpoint protein MAD2 and the mitotic regulator CDC20 form a ternary complex with the anaphase-promoting complex to control anaphase initiation. Genes Dev. 12, 1871-1883.
8. Fisk, H. A., Mattison, C. P., and Winey, M. (2004). A field guide to the Mps1 family of protein kinases. Cell Cycle 3, 439-442.
9. Fisk, H. A., and Winey, M. (2001). The mouse Mps1p-like kinase regulates centrosome duplication. Cell 106, 95-104.
10. Hoffman, D. B., Pearson, C. G., Yen, T. J., Howell, B. J., and Salmon, E. D. (2001). Microtubule-dependent changes in assembly of microtubule motor proteins and mitotic spindle checkpoint proteins at PtK1 kinetochores. Mol. Biol. Cell 12, 1995-2009.
11. 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.
12. Hoyt, M. A., Totis, L., and Roberts, B. T. (1991). S. cerevisiae genes required for cell cycle arrest in response to loss of microtubule function. Cell 66, 507-517.
13. Jelluma, N., Brenkman, A. B., McLeod, I., Yates, J. R., 3rd, Cleveland, D. W., Medema, R. H., and Kops, G. J. (2008a). Chromosomal instability by inefficient Mps1 auto-activation due to a weakened mitotic checkpoint and lagging chromosomes. PLoS ONE 3, e2415.
14. Jelluma, N., Brenkman, A. B., van den Broek, N. J., Cruijsen, C. W., van Osch, M. H., Lens, S. M., Medema, R. H., and Kops, G. J. (2008b). Mps1 phosphorylates borealin to control aurora B activity and chromosome alignment. Cell 132, 233-246.
15. Kang, J., Chen, Y., Zhao, Y., and Yu, H. (2007). Autophosphorylation- dependent activation of human Mps1 is required for the spindle checkpoint. Proc.Natl. Acad. Sci. USA 104, 20232-20237.
16. Kasbek, C., Yang, C. H., Yusof, A. M., Chapman, H. M., Winey, M., and Fisk, H. A. (2007). Preventing the degradation of mps1 at centrosomes is sufficient to cause centrosome reduplication in human cells. Mol. Biol. Cell 18, 4457-4469.
17. Kops, G. J., Weaver, B. A., and Cleveland, D. W. (2005). On the road to cancer: aneuploidy and the mitotic checkpoint. Nat. Rev. Cancer 5, 773-785.
18. Lengauer, C., Kinzler, K. W., and Vogelstein, B. (1997). Genetic instability in colorectal cancers. Nature 386, 623-627.
19. Li, R., and Murray, A. W. (1991). Feedback control of mitosis in budding yeast. Cell 66, 519 -531.
20. Lindberg, R. A., Fischer, W. H., and Hunter, T. (1993). Characterization of a human protein threonine kinase isolated by screening an expression library with antibodies to phosphotyrosine. Oncogene 8, 351-359.
21. 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.
22. Liu, X., Constantinescu, S. N., Sun, Y., Bogan, J. S., Hirsch, D., Weinberg, R. A., and Lodish, H. F. (2000). Generation of mammalian cells stably expressing multiple genes at predetermined levels. Anal. Biochem. 280, 20-28.
23. Liu, X., Sun, Y., Constantinescu, S. N., Karam, E., Weinberg, R. A., and Lodish, H. F. (1997). Transforming growth factor beta-induced phosphorylation of Smad3 is required for growth inhibition and transcriptional induction in epithelial cells. Proc. Natl. Acad. Sci. USA 94, 10669 -10674.
24. 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.
25. Mattison, C. P., Old, W. M., Steiner, E., Huneycutt, B. J., Resing, K. A., Ahn, N. G., and Winey, M. (2007). Mps1 activation loop autophosphorylation enhances kinase activity. J. Biol. Chem. 282, 30553-30561.
26. McIntosh, J. R. (1991). Structural and mechanical control of mitotic progression. Cold Spring Harb. Symp. Quant. Biol. 56, 613-619.
27. Mills, G. B., Schmandt, R., McGill, M., Amendola, A., Hill, M., Jacobs, K., May, C., Rodricks, A. M., Campbell, S., and Hogg, D. (1992). Expression of TTK, a novel human protein kinase, is associated with cell proliferation. J. Biol. Chem. 267, 16000-16006.
28. Montembault, E., Dutertre, S., Prigent, C., and Giet, R. (2007). PRP4 is a spindle assembly checkpoint protein required for MPS1, MAD1, and MAD2 localization to the kinetochores. J. Cell Biol. 179, 601-609.
29. Nasmyth, K. (2001). Disseminating the genome: oining, resolving, and separating sister chromatids during mitosis and meiosis. Annu. Rev. Genet. 35, 673-745.
30. Nasmyth, K. (2002). Segregating sister genomes: the molecular biology of chromosome separation. Science 297, 559-565.
31. Naviaux, R. K., Costanzi, E., Haas, M., and Verma, I. M. (1996). The pCL vector system: rapid production of helper-free, high-titer, recombinant retroviruses. J. Virol. 70, 5701-5705.
32. Nicklas, R. B. (1997). How cells get the right chromosomes. Science 275, 632-637.
33. Rieder, C. L., Schultz, A., Cole, R., and Sluder, G. (1994). 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.
34. Schmidt, M., and Medema, R. H. (2006). Exploiting the compromised spindle assembly checkpoint function of tumor cells: dawn on the horizon? Cell Cycle 5, 159-163.
35. Stucke, V. M., Baumann, C., and Nigg, E. A. (2004). Kinetochore localization and microtubule interaction of the human spindle checkpoint kinase Mps1. Chromosoma 113, 1-15.
36. Stucke, V. M., Sillje, H. H., Arnaud, L., and Nigg, E. A. (2002). Human Mps1 kinase is required for the spindle assembly checkpoint but not for centrosome duplication. EMBO J. 21, 1723-1732.
37. Sudakin, V., Chan, G. K., and Yen, T. J. (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.
38. Tang, Z., Shu, H., Oncel, D., Chen, S., and Yu, H. (2004). Phosphorylation of Cdc20 by Bub1 provides a catalytic mechanism for APC/C inhibition by the spindle checkpoint. Mol. Cell 16, 387-397.
39. Tighe, A., Johnson, V. L., Albertella, M., and Taylor, S. S. (2001). Aneuploid colon cancer cells have a robust spindle checkpoint. EMBO Rep. 2, 609-614.
40. Uhlmann, F., Lottspeich, F., and Nasmyth, K. (1999). Sister-chromatid separation at anaphase onset is promoted by cleavage of the cohesin subunit Scc1. Nature 400, 37-42.
41. Vigneron, S., Prieto, S., Bernis, C., Labbe, J. C., Castro, A., and Lorca, T. (2004). Kinetochore localization of spindle checkpoint proteins: who controls whom? Mol. Biol. Cell 15, 4584-4596.
42. Wassmann, K., and Benezra, R. (2001). Mitotic checkpoints: from yeast to cancer. Curr. Opin. Genet. Dev. 11, 83-90.
43. Weaver, B. A., and Cleveland, D. W. (2005). Decoding the links between mitosis, cancer, and chemotherapy: the mitotic checkpoint, adaptation, and cell death. Cancer Cell 8, 7-12.
44. 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.
45. Williamson, B. L., Marchese, J., and Morrice, N. A. (2006). Automated identification and quantification of protein phosphorylation sites by LC/MS on a hybrid triple quadrupole linear ion trap mass spectrometer. Mol. Cell Proteomics 5, 337-346.
46. Winey, M., Goetsch, L., Baum, P., and Byers, B. (1991). MPS1 and MPS2, novel yeast genes defining distinct steps of spindle pole body duplication. J. Cell Biol. 114, 745-754.
47. Yu, H. (2002). Regulation of APC-Cdc20 by the spindle checkpoint. Curr. Opin. Cell Biol. 14, 706-714.
48. 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.
49. Zhu, S., Wang, W., Clarke, D. C., and Liu, X. (2007). Activation of Mps1 promotes transforming growth factor-beta-independent Smad signaling. J. Biol. Chem. 282, 18327-18338.