A minimal number of MELT repeats supports all the functions of KNL1 in chromosome segregation

Journal of Cell Science

Volumn 127, Issue 4, 2014, Pages 871-884

  Zhang, Gang ^a   Lischetti, Tiziana ^a   Nilsson, Jakob ^a  

^a University of Copenhagen   (Denmark)

Author keywords

Bub1; BubR1; Kinetochore; KNL1; SAC; Spindle assembly checkpoint

Indexed keywords

BUB1; BUBR1; KINETOCHORE; KNL1; SAC; SPINDLE ASSEMBLY CHECKPOINT;

BINDING SITES; CELL CYCLE PROTEINS; CHROMOSOME SEGREGATION; HELA CELLS; HUMANS; MICROTUBULE-ASSOCIATED PROTEINS; PHOSPHORYLATION; PROMETAPHASE; PROTEIN BINDING; PROTEIN INTERACTION DOMAINS AND MOTIFS; PROTEIN INTERACTION MAPPING; PROTEIN PROCESSING, POST-TRANSLATIONAL; PROTEIN TRANSPORT; PROTEIN-SERINE-THREONINE KINASES; RECEPTORS, NEUROPEPTIDE Y; REPETITIVE SEQUENCES, AMINO ACID;

EID: 84894090345     PISSN: 00219533     EISSN: 14779137     Source Type: Journal    
DOI: 10.1242/jcs.139725     Document Type: Article

References (43)

1. 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.
2. Cheeseman, I. M., Niessen, S., Anderson, S., Hyndman, F., Yates, J. R., III, Oegema, K. and Desai, A. (2004). A conserved protein network controls assembly of the outer kinetochore and its ability to sustain tension. Genes Dev. 18, 2255-2268.
3. Cheeseman, I. M., Chappie, J. S., Wilson-Kubalek, E. M. and Desai, A. (2006). The conserved KMN network constitutes the core microtubule-binding site of the kinetochore. Cell 127, 983-997.
4. 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 kinetochore outer plate essential for organizing microtubule attachment sites. Mol. Biol. Cell 16, 519-531.
5. DeLuca, J. G., Gall, W. E., Ciferri, C., Cimini, D., Musacchio, A. and Salmon, E. D. (2006). Kinetochore microtubule dynamics and attachment stability are regulated by Hec1. Cell 127, 969-982.
6. Ditchfield, C., Johnson, V. L., Tighe, A., Ellston, R., Haworth, C., Johnson, T., Mortlock, A., Keen, N. and Taylor, S. S. (2003). Aurora B couples chromosome alignment with anaphase by targeting BubR1, Mad2, and Cenp-E to kinetochores. J. Cell Biol. 161, 267-280.
7. Espeut, J., Cheerambathur, D. K., Krenning, L., Oegema, K. and Desai, A. (2012). Microtubule binding by KNL-1 contributes to spindle checkpoint silencing at the kinetochore. J. Cell Biol. 196, 469-482.
8. Foley, E. A., Maldonado, M. and Kapoor, T. M. (2011). Formation of stable attachments between kinetochores and microtubules depends on the B56-PP2A phosphatase. Nat. Cell Biol. 13, 1265-1271.
9. Guimaraes, G. J., Dong, Y., McEwen, B. F. and Deluca, J. G. (2008). Kinetochore-microtubule attachment relies on the disordered N-terminal tail domain of Hec1. Curr. Biol. 18, 1778-1784.
10. 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.
11. 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.
12. 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.
13. Kops, G. J. P. L., Kim, Y., Weaver, B. A. A., Mao, Y., McLeod, I., Yates, J. R., III, Tagaya, M. and Cleveland, D. W. (2005). ZW10 links mitotic checkpoint signaling to the structural kinetochore. J. Cell Biol. 169, 49-60.
14. 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.
15. Kruse, T., Zhang, G., Larsen, M. S. Y., Lischetti, T., Streicher, W., Kragh Nielsen, T., Bjørn, S. P. and Nilsson, J. (2013). Direct binding between BubR1 and B56-PP2A phosphatase complexes regulate mitotic progression. J. Cell Sci. 126, 1086-1092.
16. Lampson, M. A. and Kapoor, T. M. (2005). The human mitotic checkpoint protein BubR1 regulates chromosome-spindle attachments. Nat. Cell Biol. 7, 93-98.
17. Lara-Gonzalez, P., Scott, M. I. F., Diez, M., Sen, O. and Taylor, S. S. (2011). BubR1 blocks substrate recruitment to the APC/C in a KEN-box-dependent manner. J. Cell Sci. 124, 4332-4345.
18. Lara-Gonzalez, P., Westhorpe, F. G. and Taylor, S. S. (2012). The spindle assembly checkpoint. Curr. Biol. 22, R966-R980.
19. Liu, D., Vleugel, M., Backer, C. B., Hori, T., Fukagawa, T., Cheeseman, I. M. and Lampson, M. A. (2010). Regulated targeting of protein phosphatase 1 to the outer kinetochore by KNL1 opposes Aurora B kinase. J. Cell Biol. 188, 809-820.
20. 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.
21. Meadows, J. C., Shepperd, L. A., Vanoosthuyse, V., Lancaster, T. C., Sochaj, A. M., Buttrick, G. J., Hardwick, K. G. and Millar, J. B. A. (2011). Spindle checkpoint silencing requires association of PP1 to both Spc7 and kinesin-8 motors. Dev. Cell 20, 739-750.
22. Meraldi, P. and Sorger, P. K. (2005). A dual role for Bub1 in the spindle checkpoint and chromosome congression. EMBO J. 24, 1621-1633.
23. Meraldi, P., Draviam, V. M. and Sorger, P. K. (2004). Timing and checkpoints in the regulation of mitotic progression. Dev. Cell 7, 45-60.
24. Miller, S. A., Johnson, M. L. and Stukenberg, P. T. (2008). Kinetochore attachments require an interaction between unstructured tails on microtubules and Ndc80(Hec1). Curr. Biol. 18, 1785-1791.
25. Pagliuca, C., Draviam, V. M., Marco, E., Sorger, P. K. and De Wulf, P. (2009). Roles for the conserved spc105p/kre28p complex in kinetochore-microtubule binding and the spindle assembly checkpoint. PLoS ONE 4, e7640.
26. Primorac, I., Weir, J. R., Chiroli, E., Gross, F., Hoffmann, I., van Gerwen, S., Ciliberto, A. and Musacchio, A. (2013). Bub3 reads phosphorylated MELT repeats to promote spindle assembly checkpoint signaling. Elife 2, e01030.
27. Przewloka, M. R., Venkei, Z., Bolanos-Garcia, V. M., Debski, J., Dadlez, M. and Glover, D. M. (2011). CENP-C is a structural platform for kinetochore assembly. Curr. Biol. 21, 399-405.
28. Ricke, R. M. and van Deursen, J. M. (2013). Aneuploidy in health, disease, and aging. J. Cell Biol. 201, 11-21.
29. Rosenberg, J. S., Cross, F. R. and Funabiki, H. (2011). KNL1/Spc105 recruits PP1 to silence the spindle assembly checkpoint. Curr. Biol. 21, 942-947.
30. Santaguida, S. and Musacchio, A. (2009). The life and miracles of kinetochores. EMBO J. 28, 2511-2531.
31. Screpanti, E., De Antoni, A., Alushin, G. M., Petrovic, A., Melis, T., Nogales, E. and Musacchio, A. (2011). Direct binding of Cenp-C to the Mis12 complex joins the inner and outer kinetochore. Curr. Biol. 21, 391-398.
32. Shah, J. V., Botvinick, E., Bonday, Z., Furnari, F., Berns, M. and Cleveland, D. W. (2004). Dynamics of centromere and kinetochore proteins; implications for checkpoint signaling and silencing. Curr. Biol. 14, 942-952.
33. 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. A. (2012). Phosphodependent recruitment of Bub1 and Bub3 to Spc7/KNL1 by Mph1 kinase maintains the spindle checkpoint. Curr. Biol. 22, 891-899.
34. Suijkerbuijk, S. J. E., Vleugel, M., Teixeira, A. and Kops, G. J. P. L. (2012). Integration of kinase and phosphatase activities by BUBR1 ensures formation of stable kinetochore-microtubule attachments. Dev. Cell 23, 745-755.
35. Takeuchi, K. and Fukagawa, T. (2012). Molecular architecture of vertebrate kinetochores. Exp. Cell Res. 318, 1367-1374.
36. Taylor, S. S., Ha, E. and McKeon, F. (1998). The human homologue of Bub3 is required for kinetochore localization of Bub1 and a Mad3/Bub1-related protein kinase. J. Cell Biol. 142, 1-11.
37. Trinkle-Mulcahy, L., Andrews, P. D., Wickramasinghe, S., Sleeman, J., Prescott, A., Lam, Y. W., Lyon, C., Swedlow, J. R. and Lamond, A. I. (2003). Time-lapse imaging reveals dynamic relocalization of PP1gamma throughout the mammalian cell cycle. Mol. Biol. Cell 14, 107-117.
38. Vanoosthuyse, V. and Hardwick, K. G. (2009). A novel protein phosphatase 1-dependent spindle checkpoint silencing mechanism. Curr. Biol. 19, 1176-1181.
39. Vleugel, M., Hoogendoorn, E., Snel, B. and Kops, G. J. P. L. (2012). Evolution and function of the mitotic checkpoint. Dev. Cell 23, 239-250.
40. Wang, H., Hu, X., Ding, X., Dou, Z., Yang, Z., Shaw, A. W., Teng, M., Cleveland, D. W., Goldberg, M. L., Niu, L. et al. (2004). Human Zwint-1 specifies localization of Zeste White 10 to kinetochores and is essential for mitotic checkpoint signaling. J. Biol. Chem. 279, 54590-54598.
41. Wei, R. R., Al-Bassam, J. and Harrison, S. C. (2007). The Ndc80/HEC1 complex is a contact point for kinetochore-microtubule attachment.Nat.Struct.Mol.Biol. 14, 54-59.
42. 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.
43. Zhang, G., Kelstrup, C. D., Hu, X.-W., Kaas Hansen, M. J., Singleton, M. R., Olsen, J. V. and Nilsson, J. (2012). The Ndc80 internal loop is required for recruitment of the Ska complex to establish end-on microtubule attachment to kinetochores. J. Cell Sci. 125, 3243-3253.