Multiple assembly mechanisms anchor the KMN spindle checkpoint platform at human mitotic kinetochores

Journal of Cell Biology

Volumn 208, Issue 2, 2015, Pages 181-196

  Kim, Soonjoung ^a   Yu, Hongtao ^a  

^a UNIVERSITY OF TEXAS SOUTHWESTERN MEDICAL CENTER   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

AURORA B KINASE; CENP C PROTEIN; CENP T PROTEIN; KMN COMPLEX; MIS12C PROTEIN; MULTIPROTEIN COMPLEX; UNCLASSIFIED DRUG; AURKB PROTEIN, HUMAN; CASC5 PROTEIN, HUMAN; DSN1 PROTEIN, HUMAN; MICROTUBULE ASSOCIATED PROTEIN; MIS12 PROTEIN, HUMAN; NDC80 PROTEIN, HUMAN; NONHISTONE PROTEIN; NUCLEAR PROTEIN; PROTEIN BINDING; PROTEIN SUBUNIT;

ARTICLE; BINDING AFFINITY; CENTROMERE; CONTROLLED STUDY; HUMAN; HUMAN CELL; M PHASE CELL CYCLE CHECKPOINT; MICROTUBULE ASSEMBLY; PRIORITY JOURNAL; PROTEIN ASSEMBLY; PROTEIN BINDING; PROTEIN PHOSPHORYLATION; HELA CELL LINE; METABOLISM; PHOSPHORYLATION; PROTEIN PROCESSING; PROTEIN SUBUNIT;

AURORA KINASE B; CHROMOSOMAL PROTEINS, NON-HISTONE; HELA CELLS; HUMANS; KINETOCHORES; M PHASE CELL CYCLE CHECKPOINTS; MICROTUBULE-ASSOCIATED PROTEINS; NUCLEAR PROTEINS; PHOSPHORYLATION; PROTEIN BINDING; PROTEIN PROCESSING, POST-TRANSLATIONAL; PROTEIN SUBUNITS;

EID: 84921757340     PISSN: 00219525     EISSN: 15408140     Source Type: Journal    
DOI: 10.1083/jcb.201407074     Document Type: Article

References (55)

1. Akiyoshi, B., C.R. Nelson, and S. Biggins. 2013. The Aurora B kinase promotes inner and outer kinetochore interactions in budding yeast. Genetics. 194:785-789. http://dx.doi.org/10.1534/genetics.113.150839
2. Basilico, F., S. Maffini, J.R. Weir, D. Prumbaum, A.M. Rojas, T. Zimniak, A. De Antoni, S. Jeganathan, B. Voss, S. van Gerwen, et al. 2014. The pseudo GTPase CENP-M drives human kinetochore assembly. eLife. 3:e02978. http://dx.doi.org/10.7554/eLife.02978
3. Bharadwaj, R., W. Qi, and H. Yu. 2004. Identification of two novel components of the human NDC80 kinetochore complex. J. Biol. Chem. 279: 13076-13085. http://dx.doi.org/10.1074/jbc.M310224200
4. Black, B.E., and D.W. Cleveland. 2011. Epigenetic centromere propagation and the nature of CENP-a nucleosomes. Cell. 144:471-479. http://dx.doi.org/10.1016/j.cell.2011.02.002
5. Bock, L.J., C. Pagliuca, N. Kobayashi, R.A. Grove, Y. Oku, K. Shrestha, C. Alfieri, C. Golfieri, A. Oldani, M. Dal Maschio, et al. 2012. Cnn1 inhibits the interactions between the KMN complexes of the yeast kinetochore. Nat. Cell Biol. 14: 614-624. http://dx.doi.org/10.1038/ncb2495
6. Cheeseman, I.M., and A. Desai. 2008. Molecular architecture of the kinetochoremicrotubule interface. Nat. Rev. Mol. Cell Biol. 9: 33-46. http://dx.doi.org/10.1038/nrm2310
7. 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
8. Cheeseman, I.M., T. Hori, T. Fukagawa, and A. Desai. 2008. KNL1 and the CENP-H/I/K complex coordinately direct kinetochore assembly in vertebrates. Mol. Biol. Cell. 19:587-594. http://dx.doi.org/10.1091/mbc.E07-10-1051
9. Cleveland, D.W., Y. Mao, and K.F. Sullivan. 2003. Centromeres and kinetochores: from epigenetics to mitotic checkpoint signaling. Cell. 112:407-421. http://dx.doi.org/10.1016/S0092-8674(03)00115-6
10. Collin, P., O. Nashchekina, R. Walker, and J. Pines. 2013. The spindle assembly checkpoint works like a rheostat rather than a toggle switch. Nat. Cell Biol. 15: 1378-1385. http://dx.doi.org/10.1038/ncb2855
11. Dick, A.E., and D.W. Gerlich. 2013. Kinetic framework of spindle assembly checkpoint signalling. Nat. Cell Biol. 15: 1370-1377. http://dx.doi.org/10.1038/ncb2842
12. Emanuele, M.J., W. Lan, M. Jwa, S.A. Miller, C.S. Chan, and P.T. Stukenberg. 2008. Aurora B kinase and protein phosphatase 1 have opposing roles in modulating kinetochore assembly. J. Cell Biol. 181: 241-254. http://dx.doi.org/10.1083/jcb.200710019
13. Foley, E.A., and T.M. Kapoor. 2013. Microtubule attachment and spindle assembly checkpoint signalling at the kinetochore. Nat. Rev. Mol. Cell Biol. 14: 25-37. http://dx.doi.org/10.1038/nrm3494
14. Foltz, D.R., L.E. Jansen, B.E. Black, A.O. Bailey, J.R. Yates III, and D.W. Cleveland. 2006. The human CENP-A centromeric nucleosomeassociated complex. Nat. Cell Biol. 8: 458-469. http://dx.doi.org/10.1038/ncb1397
15. Gascoigne, K.E., and I.M. Cheeseman. 2013. CDK-dependent phosphorylation and nuclear exclusion coordinately control kinetochore assembly state. J. Cell Biol. 201: 23-32. http://dx.doi.org/10.1083/jcb.201301006
16. Gascoigne, K.E., K. Takeuchi, A. Suzuki, T. Hori, T. Fukagawa, and I.M. Cheeseman. 2011. Induced ectopic kinetochore assembly bypasses the requirement for CENP-A nucleosomes. Cell. 145:410-422. http://dx.doi.org/10.1016/j.cell.2011.03.031
17. Heinrich, S., E.M. Geissen, J. Kamenz, S. Trautmann, C. Widmer, P. Drewe, M. Knop, N. Radde, J. Hasenauer, and S. Hauf. 2013. Determinants of robustness in spindle assembly checkpoint signalling. Nat. Cell Biol. 15: 1328-1339. http://dx.doi.org/10.1038/ncb2864
18. Hori, T., M. Amano, A. Suzuki, C.B. Backer, J.P. Welburn, Y. Dong, B.F. McEwen, W.H. Shang, E. Suzuki, K. Okawa, et al. 2008. CCAN makes multiple contacts with centromeric DNA to provide distinct pathways to the outer kinetochore. Cell. 135:1039-1052. http://dx.doi.org/10.1016/j.cell.2008.10.019
19. Hori, T., W.H. Shang, K. Takeuchi, and T. Fukagawa. 2013. The CCAN recruits CENP-A to the centromere and forms the structural core for kinetochore assembly. J. Cell Biol. 200: 45-60. http://dx.doi.org/10.1083/jcb.201210106
20. Jia, L., S. Kim, and H. Yu. 2013. Tracking spindle checkpoint signals from kinetochores to APC/C. Trends Biochem. Sci. 38: 302-311. http://dx.doi.org/10.1016/j.tibs.2013.03.004
21. Kang, J., M. Yang, B. Li, W. Qi, C. Zhang, K.M. Shokat, D.R. Tomchick, M. Machius, and H. Yu. 2008. Structure and substrate recruitment of the human spindle checkpoint kinase Bub1. Mol. Cell. 32:394-405. http://dx.doi.org/10.1016/j.molcel.2008.09.017
22. Kim, S., H. Sun, D.R. Tomchick, H. Yu, and X. Luo. 2012. Structure of human Mad1 C-terminal domain reveals its involvement in kinetochore targeting. Proc. Natl. Acad. Sci. USA. 109:6549-6554. http://dx.doi.org/10.1073/pnas.1118210109
23. Kiyomitsu, T., C. Obuse, and M. Yanagida. 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. http://dx.doi.org/10.1016/j.devcel.2007.09.005
24. Krenn, V., K. Overlack, I. Primorac, S. van Gerwen, and A. Musacchio. 2014. KI motifs of human Knl1 enhance assembly of comprehensive spindle checkpoint complexes around MELT repeats. Curr. Biol. 24: 29-39. http://dx.doi.org/10.1016/j.cub.2013.11.046
25. Lampson, M.A., and I.M. Cheeseman. 2011. Sensing centromere tension: Aurora B and the regulation of kinetochore function. Trends Cell Biol. 21: 133-140. http://dx.doi.org/10.1016/j.tcb.2010.10.007
26. Lara-Gonzalez, P., F.G. Westhorpe, and S.S. Taylor. 2012. The spindle assembly checkpoint. Curr. Biol. 22: R966-R980. http://dx.doi.org/10.1016/j.cub.2012.10.006
27. London, N., S. Ceto, J.A. Ranish, and S. Biggins. 2012. Phosphoregulation of Spc105 by Mps1 and PP1 regulates Bub1 localization to kinetochores. Curr. Biol. 22: 900-906. http://dx.doi.org/10.1016/j.cub.2012.03.052
28. Mali, P., K.M. Esvelt, and G.M. Church. 2013. Cas9 as a versatile tool for engineering biology. Nat. Methods. 10:957-963. http://dx.doi.org/10.1038/nmeth.2649
29. Malvezzi, F., G. Litos, A. Schleiffer, A. Heuck, K. Mechtler, T. Clausen, and S. Westermann. 2013. A structural basis for kinetochore recruitment of the Ndc80 complex via two distinct centromere receptors. EMBO J.32:409-423. http://dx.doi.org/10.1038/emboj.2012.356
30. 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
31. Matson, D.R., and P.T. Stukenberg. 2014. CENP-I and Aurora B act as a molecular switch that ties RZZ/Mad1 recruitment to kinetochore attachment status. J. Cell Biol. 205: 541-554. http://dx.doi.org/10.1083/jcb.201307137
32. Matson, D.R., P.B. Demirel, P.T. Stukenberg, and D.J. Burke. 2012. A conserved role for COMA/CENP-H/I/N kinetochore proteins in the spindle checkpoint. Genes Dev. 26: 542-547. http://dx.doi.org/10.1101/gad.184184.111
33. McCleland, M.L., R.D. Gardner, M.J. Kallio, J.R. Daum, G.J. Gorbsky, D.J. Burke, and P.T. Stukenberg. 2003. The highly conserved Ndc80 complex is required for kinetochore assembly, chromosome congression, and spindle checkpoint activity. Genes Dev. 17: 101-114. http://dx.doi.org/10.1101/gad.1040903
34. Mikami, Y., T. Hori, H. Kimura, and T. Fukagawa. 2005. The functional region of CENP-H interacts with the Nuf2 complex that localizes to centromere during mitosis. Mol. Cell. Biol. 25: 1958-1970. http://dx.doi.org/10.1128/MCB.25.5.1958-1970.2005
35. Nijenhuis, W., E. von Castelmur, D. Littler, V. De Marco, E. Tromer, M. Vleugel, M.H. van Osch, B. Snel, A. Perrakis, and G.J. Kops. 2013. A TPR domain-containing N-terminal module of MPS1 is required for its kinetochore localization by Aurora B. J. Cell Biol. 201: 217-231. http://dx.doi.org/10.1083/jcb.201210033
36. Nishino, T., F. Rago, T. Hori, K. Tomii, I.M. Cheeseman, and T. Fukagawa. 2013. CENP-T provides a structural platform for outer kinetochore assembly. EMBO J.32:424-436. http://dx.doi.org/10.1038/emboj.2012.348
37. Okada, M., I.M. Cheeseman, T. Hori, K. Okawa, I.X. McLeod, J.R. Yates III, A. Desai, and T. Fukagawa. 2006. The CENP-H-I complex is required for the efficient incorporation of newly synthesized CENP-A into centromeres. Nat. Cell Biol. 8: 446-457. http://dx.doi.org/10.1038/ncb1396
38. Petrovic, A., S. Pasqualato, P. Dube, V. Krenn, S. Santaguida, D. Cittaro, S. Monzani, L. Massimiliano, J. Keller, A. Tarricone, et al. 2010. The MIS12 complex is a protein interaction hub for outer kinetochore assembly. J. Cell Biol. 190: 835-852. http://dx.doi.org/10.1083/jcb.201002070
39. Petrovic, A., S. Mosalaganti, J. Keller, M. Mattiuzzo, K. Overlack, V. Krenn, A. De Antoni, S. Wohlgemuth, V. Cecatiello, S. Pasqualato, et al. 2014. Modular assembly of RWD domains on the Mis12 complex underlies outer kinetochore organization. Mol. Cell. 53:591-605. http://dx.doi.org/10.1016/j.molcel.2014.01.019
40. Primorac, I., J.R. Weir, E. Chiroli, F. Gross, I. Hoffmann, S. van Gerwen, A. Ciliberto, and A. Musacchio. 2013. Bub3 reads phosphorylated MELT repeats to promote spindle assembly checkpoint signaling. eLife. 2:e01030. http://dx.doi.org/10.7554/eLife.01030
41. Rieder, C.L., R.W. Cole, A. Khodjakov, and G. Sluder. 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. http://dx.doi.org/10.1083/jcb.130.4.941
42. Ruchaud, S., M. Carmena, and W.C. Earnshaw. 2007. Chromosomal passengers: conducting cell division. Nat. Rev. Mol. Cell Biol. 8: 798-812. http://dx.doi.org/10.1038/nrm2257
43. 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
44. 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
45. Schleiffer, A., M. Maier, G. Litos, F. Lampert, P. Hornung, K. Mechtler, and S. Westermann. 2012. CENP-T proteins are conserved centromere receptors of the Ndc80 complex. Nat. Cell Biol. 14: 604-613. http://dx.doi.org/10.1038/ncb2493
46. Screpanti, E., A. De Antoni, G.M. Alushin, A. Petrovic, T. Melis, E. Nogales, and A. Musacchio. 2011. Direct binding of Cenp-C to the Mis12 complex joins the inner and outer kinetochore. Curr. Biol. 21: 391-398. http://dx.doi.org/10.1016/j.cub.2010.12.039
47. Shepperd, L.A., J.C. Meadows, A.M. Sochaj, T.C. Lancaster, J. Zou, G.J. Buttrick, J. Rappsilber, K.G. Hardwick, and J.B. Millar. 2012. Phosphodependent recruitment of Bub1 and Bub3 to Spc7/KNL1 by Mph1 kinase maintains the spindle checkpoint. Curr. Biol. 22: 891-899. http://dx.doi.org/10.1016/j.cub.2012.03.051
48. 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
49. Subramanian, R., and T.M. Kapoor. 2013. Slipping past the spindle assembly checkpoint. Nat. Cell Biol. 15: 1261-1263. http://dx.doi.org/10.1038/ncb2876
50. Takeuchi, K., and T. Fukagawa. 2012. Molecular architecture of vertebrate kinetochores. Exp. Cell Res. 318: 1367-1374. http://dx.doi.org/10.1016/j.yexcr.2012.02.016
51. Tanaka, T.U., N. Rachidi, C. Janke, G. Pereira, M. Galova, E. Schiebel, M.J. Stark, and K. Nasmyth. 2002. Evidence that the Ipl1-Sli15 (Aurora kinase-INCENP) complex promotes chromosome bi-orientation by altering kinetochore-spindle pole connections. Cell. 108:317-329. http://dx.doi.org/10.1016/S0092-8674(02)00633-5
52. Vleugel, M., E. Tromer, M. Omerzu, V. Groenewold, W. Nijenhuis, B. Snel, and G.J. Kops. 2013. Arrayed BUB recruitment modules in the kinetochore scaffold KNL1 promote accurate chromosome segregation. J. Cell Biol. 203: 943-955. http://dx.doi.org/10.1083/jcb.201307016
53. 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
54. Yamagishi, Y., C.H. Yang, Y. Tanno, and Y. Watanabe. 2012. MPS1/Mph1 phosphorylates the kinetochore protein KNL1/Spc7 to recruit SAC components. Nat. Cell Biol. 14: 746-752. http://dx.doi.org/10.1038/ncb2515
55. 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