Aurora B controls kinetochore-microtubule attachments by inhibiting Ska complex-KMN network interaction

Journal of Cell Biology

Volumn 196, Issue 5, 2012, Pages 563-571

  Chan, Ying Wai ^a   Jeyaprakash, A Arockia ^b   Nigg, Erich A ^a   Santamaria, Anna ^a  

^a UNIVERSITY OF BASEL   (Switzerland)

^b MAX PLANCK INSTITUTE OF BIOCHEMISTRY   (Germany)

Author keywords

[No Author keywords available]

Indexed keywords

AURORA B KINASE; CELL PROTEIN; KMN PROTEIN COMPLEX; SKA1 PROTEIN; SKA2 PROTEIN; SKA3 PROTEIN; UNCLASSIFIED DRUG;

ANAPHASE; ANIMAL CELL; ARTICLE; CENTROMERE; ENZYME ACTIVITY; HUMAN; HUMAN CELL; IN VITRO STUDY; MICROTUBULE; MITOSIS; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN PHOSPHORYLATION; PROTEIN PROTEIN INTERACTION; PROTEIN SYNTHESIS REGULATION;

AMINO ACID SEQUENCE; ANIMALS; CHROMOSOMAL PROTEINS, NON-HISTONE; HELA CELLS; HUMANS; KINETOCHORES; MICROTUBULE-ASSOCIATED PROTEINS; MICROTUBULES; MITOSIS; MOLECULAR SEQUENCE DATA; NUCLEAR PROTEINS; PHOSPHORYLATION; PROTEIN BINDING; PROTEIN-SERINE-THREONINE KINASES; RECOMBINANT FUSION PROTEINS; RNA, SMALL INTERFERING; SEQUENCE ALIGNMENT;

EID: 84859991512     PISSN: 00219525     EISSN: 15408140     Source Type: Journal    
DOI: 10.1083/jcb.201109001     Document Type: Article

References (46)

1. Andrews, P.D., Y. Ovechkina, N. Morrice, M. Wagenbach, K. Duncan, L. Wordeman, and J.R. Swedlow. 2004. Aurora B regulates MCAK at the mitotic centromere. Dev. Cell. 6:253-268. http://dx.doi.org/10.1016/S1534-5807(04)00025-5
2. Chan, Y.W., L.L. Fava, A. Uldschmid, M.H. Schmitz, D.W. Gerlich, E.A. Nigg, and A. Santamaria. 2009. Mitotic control of kinetochore-associated dynein and spindle orientation by human Spindly. J. Cell Biol. 185:859-874. http://dx.doi.org/10.1083/jcb.200812167
3. Cheeseman, I.M., J.S. Chappie, E.M. Wilson-Kubalek, and A. Desai. 2006. The conserved KMN network constitutes the core microtubule-binding site of the kinetochore. Cell. 127:983-997. http://dx.doi.org/10.1016/j.cell.2006.09.039
4. Ciferri, C., S. Pasqualato, E. Screpanti, G. Varetti, S. Santaguida, G. Dos Reis, A. Maiolica, J. Polka, J.G. De Luca, P. De Wulf, et al. 2008. Implications for kinetochore-microtubule attachment from the structure of an engineered Ndc80 complex. Cell. 133:427-439. http://dx.doi.org/10.1016/j.cell.2008.03.020
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. http://dx.doi.org/10.1016/j.cub.2009.07.017
6. Daum, J.R., T.A. Potapova, S. Sivakumar, J.J. Daniel, J.N. Flynn, S. Rankin, and G.J. Gorbsky. 2011. Cohesion fatigue induces chromatid separation in cells delayed at metaphase. Curr. Biol. 21:1018-1024. http://dx.doi.org/10.1016/j.cub.2011.05.032
7. DeLuca, J.G., W.E. Gall, C. Ciferri, D. Cimini, A. Musacchio, and E.D. Salmon. 2006. Kinetochore microtubule dynamics and attachment stability are regulated by Hec1. Cell. 127:969-982. http://dx.doi.org/10.1016/j.cell.2006.09.047
8. 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 chromosomealignment 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
9. 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. http://dx.doi.org/10.1038/emboj.2009.96
10. 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. http://dx.doi.org/10.1101/gad.1886810
11. 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
12. 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. http://dx.doi.org/10.1038/sj.emboj.7601426
13. Hübner, N.C., L.H. Wang, M. Kaulich, P. Descombes, I. Poser, and E.A. Nigg. 2010. Re-examination of siRNA specificity questions role of PICH and Tao1 in the spindle checkpoint and identifies Mad2 as a sensitive target for small RNAs. Chromosoma. 119:149-165. http://dx.doi.org/10.1007/s00412-009-0244-2
14. Kapoor, T.M., T.U. Mayer, M.L. Coughlin, and T.J. Mitchison. 2000. Probing spindle assembly mechanisms with monastrol, a small molecule inhibitor of the mitotic kinesin, Eg5. J. Cell Biol. 150:975-988. http://dx.doi.org/10.1083/jcb.150.5.975
15. Kiyomitsu, T., O. Iwasaki, C. Obuse, and M. Yanagida. 2010. Inner centromere formation requires hMis14, a trident kinetochore protein that specifically recruits HP1 to human chromosomes. J. Cell Biol. 188:791-807. http://dx.doi.org/10.1083/jcb.200908096
16. 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.
17. Lampert, F., P. Hornung, and S. Westermann. 2010. The Dam1 complex confers microtubule plus end-tracking activity to the Ndc80 kinetochore complex. J. Cell Biol. 189:641-649.
18. Lampson, M.A., K. Renduchitala, A. Khodjakov, and T.M. Kapoor. 2004. Correcting improper chromosome-spindle attachments during cell division. Nat. Cell Biol. 6:232-237.
19. Lan, W., X. Zhang, S.L. Kline-Smith, S.E. Rosasco, G.A. Barrett-Wilt, J. Shabanowitz, D.F. Hunt, C.E. Walczak, and P.T. Stukenberg. 2004. Aurora B phosphorylates centromeric MCAK and regulates its localization and microtubule depolymerization activity. Curr. Biol. 14:273-286.
20. Liu, D., G. Vader, M.J. Vromans, M.A. Lampson, and S.M. Lens. 2009. Sensing chromosome bi-orientation by spatial separation of aurora B kinase from kinetochore substrates. Science. 323:1350-1353.
21. Liu, D., M. Vleugel, C.B. Backer, T. Hori, T. Fukagawa, I.M. Cheeseman, and M.A. Lampson. 2010. Regulated targeting of protein phosphatase 1 to the outer kinetochore by KNL1 opposes Aurora B kinase. J. Cell Biol. 188:809-820. http://dx.doi.org/10.1083/jcb.201001006
22. Maresca, T.J., and E.D. Salmon. 2010. Welcome to a new kind of tension: Translating kinetochore mechanics into a wait-anaphase signal. J. Cell Sci. 123:825-835. http://dx.doi.org/10.1242/jcs.064790
23. Maure, J.F., S. Komoto, Y. Oku, A. Mino, S. Pasqualato, K. Natsume, L. Clayton, A. Musacchio, and T.U. Tanaka. 2011. The Ndc80 loop region facilitates formation of kinetochore attachment to the dynamic microtubule plus end. Curr. Biol. 21:207-213. http://dx.doi.org/10.1016/j.cub.2010.12.050
24. 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
25. Nezi, L., and A. Musacchio. 2009. Sister chromatid tension and the spindle assembly checkpoint. Curr. Opin. Cell Biol. 21:785-795. http://dx.doi.org/10.1016/j.ceb.2009.09.007
26. Nousiainen, M., H.H. Silljé, G. Sauer, E.A. Nigg, and R. Körner. 2006. Phosphoproteome analysis of the human mitotic spindle. Proc. Natl. Acad. Sci. USA. 103:5391-5396. http://dx.doi.org/10.1073/pnas.0507066103
27. 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. http://dx.doi.org/10.1038/ncb1187
28. Ohta, S., J.C. Bukowski-Wills, L. Sanchez-Pulido, Fde.L. Alves, L. Wood, Z.A. Chen, M. Platani, L. Fischer, D.F. Hudson, C.P. Ponting, et al. 2010. The protein composition of mitotic chromosomes determined using multiclassifier combinatorial proteomics. Cell. 142:810-821. http://dx.doi.org/10.1016/j.cell.2010.07.047
29. Olsen, J.V., M. Vermeulen, A. Santamaria, C. Kumar, M.L. Miller, L.J. Jensen, F. Gnad, J. Cox, T.S. Jensen, E.A. Nigg, et al. 2010. Quantitativephosphoproteomics reveals widespread full phosphorylation site occupancy during mitosis. Sci. Signal. 3:ra3. http://dx.doi.org/10.1126/scisignal.2000475
30. 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. http://dx.doi.org/10.1242/jcs.051912
31. Sanchez-Perez, I., S.J. Renwick, K. Crawley, I. Karig, V. Buck, J.C. Meadows, A. Franco-Sanchez, U. Fleig, T. Toda, and J.B. Millar. 2005. The DASH complex and Klp5/Klp6 kinesin coordinate bipolar chromosome attachment in fission yeast. EMBO J. 24:2931-2943. http://dx.doi.org/10.1038/sj.emboj.7600761
32. Santaguida, S., and A. Musacchio. 2009. The life and miracles of kinetochores. EMBO J. 28:2511-2531. http://dx.doi.org/10.1038/emboj.2009.173
33. 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
34. 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
35. Santamaria, A., R. Neef, U. Eberspächer, K. Eis, M. Husemann, D. Mumberg, S. Prechtl, V. Schulze, G. Siemeister, L. Wortmann, et al. 2007. Use of the novel Plk1 inhibitor ZK-thiazolidinone to elucidate functions of Plk1 in early and late stages of mitosis. Mol. Biol. Cell. 18:4024-4036. http:// dx.doi.org/10.1091/mbc.E07-05-0517
36. Santamaria, A., B. Wang, S. Elowe, R. Malik, F. Zhang, M. Bauer, A. Schmidt, H.H. Silljé, R. Körner, and E.A. Nigg. 2011. The Plk1-dependent phosphoproteome of the early mitotic spindle. Mol. Cell. Proteomics. 10:M110: 004457.
37. Schmidt, J.C., T. Kiyomitsu, T. Hori, C.B. Backer, T. Fukagawa, and I.M. Cheeseman. 2010. Aurora B kinase controls the targeting of the Astrin- SKAP complex to bioriented kinetochores. J. Cell Biol. 191:269-280.
38. Sessa, F., M. Mapelli, C. Ciferri, C. Tarricone, L.B. Areces, T.R. Schneider, P.T. Stukenberg, and A. Musacchio. 2005. Mechanism of Aurora B activation by INCENP and inhibition by hesperadin. Mol. Cell. 18:379-391.
39. Silljé, H.H., S. Nagel, R. Körner, and E.A. Nigg. 2006. HURP is a Ran-importin beta-regulated protein that stabilizes kinetochore microtubules in the vicinity of chromosomes. Curr. Biol. 16:731-742.
40. Sui, S., J. Wang, B. Yang, L. Song, J. Zhang, M. Chen, J. Liu, Z. Lu, Y. Cai, S. Chen, et al. 2008. Phosphoproteome analysis of the human Chang liver cells using SCX and a complementary mass spectrometric strategy. Proteomics. 8:2024-2034.
41. Theis, M., M. Slabicki, M. Junqueira, M. Paszkowski-Rogacz, J. Sontheimer, R. Kittler, A.K. Heninger, T. Glatter, K. Kruusmaa, I. Poser, et al. 2009. Comparative profiling identifies C13orf3 as a component of the Ska complex required for mammalian cell division. EMBO J. 28:1453-1465. http://dx.doi.org/10.1038/emboj.2009.114
42. Tien, J.F., N.T. Umbreit, D.R. Gestaut, A.D. Franck, J. Cooper, L. Wordeman, T. Gonen, C.L. Asbury, and T.N. Davis. 2010. Cooperation of the Dam1 and Ndc80 kinetochore complexes enhances microtubule coupling and is regulated by aurora B. J. Cell Biol. 189:713-723. http://dx.doi.org/10.1083/jcb.200910142
43. Wang, E., E.R. Ballister, and M.A. Lampson. 2011. Aurora B dynamics at centromeres create a diffusion-based phosphorylation gradient. J. Cell Biol. 194:539-549. http://dx.doi.org/10.1083/jcb.201103044
44. Welburn, J.P., E.L. Grishchuk, C.B. Backer, E.M. Wilson-Kubalek, J.R. Yates III, and I.M. Cheeseman. 2009. The human kinetochore Ska1 complex facilitates microtubule depolymerization-coupled motility. Dev. Cell. 16:374-385. http://dx.doi.org/10.1016/j.devcel.2009.01.011
45. Welburn, J.P., M. Vleugel, D. Liu, J.R. Yates III, M.A. Lampson, T. Fukagawa, and I.M. Cheeseman. 2010. Aurora B phosphorylates spatially distinct targets to differentially regulate the kinetochore-microtubule interface. Mol. Cell. 38:383-392. http://dx.doi.org/10.1016/j.molcel.2010.02.034
46. Yang, Y., F. Wu, T. Ward, F. Yan, Q. Wu, Z. Wang, T. McGlothen, W. Peng, T. You, M. Sun, et al. 2008. Phosphorylation of HsMis13 by Aurora B kinase is essential for assembly of functional kinetochore. J. Biol. Chem. 283:26726-26736. http://dx.doi.org/10.1074/jbc.M804207200