Negative feedback at kinetochores underlies a responsive spindle checkpoint signal

Nature Cell Biology

Volumn 16, Issue 12, 2014, Pages 1257-1264

  Nijenhuis, Wilco ^a   Vallardi, Giulia ^b   Teixeira, Antoinette ^a   Kops, Geert J P L ^a   Saurin, Adrian T ^b  

^a UNIVERSITY MEDICAL CENTER UTRECHT   (Netherlands)

^b UNIVERSITY OF DUNDEE   (United Kingdom)

Author keywords

[No Author keywords available]

Indexed keywords

AURORA B KINASE; B56 PROTEIN; CELL PROTEIN; PHOSPHATASE; PP1 PROTEIN; PP2A PROTEIN; UNCLASSIFIED DRUG; AURKB PROTEIN, HUMAN; BUB1 PROTEIN, HUMAN; CASC5 PROTEIN, HUMAN; CELL CYCLE PROTEIN; MICROTUBULE ASSOCIATED PROTEIN; NOCODAZOLE; PHOSPHOPROTEIN PHOSPHATASE 2; PP2A-B56ALPHA PROTEIN, HUMAN; PROTEIN BINDING; PROTEIN SERINE THREONINE KINASE; PROTEIN TYROSINE KINASE; SGOL1 PROTEIN, HUMAN; SMAD2 PROTEIN; SMAD2 PROTEIN, HUMAN; SMALL INTERFERING RNA; TTK PROTEIN, HUMAN; TUBULIN MODULATOR;

ARTICLE; BINDING AFFINITY; BINDING SITE; CELL ASSAY; CELL FUNCTION; CENTROMERE; CONTROLLED STUDY; ENZYME ACTIVITY; ENZYME ASSAY; HUMAN; HUMAN CELL; M PHASE CELL CYCLE CHECKPOINT; MOLECULAR DYNAMICS; NEGATIVE FEEDBACK; PRIORITY JOURNAL; PROTEIN BINDING; PROTEIN DETERMINATION; PROTEIN FUNCTION; PROTEIN LOCALIZATION; PROTEIN PHOSPHORYLATION; SIGNAL TRANSDUCTION; ANTAGONISTS AND INHIBITORS; BIOSYNTHESIS; CHROMOSOME SEGREGATION; FEEDBACK SYSTEM; GENETICS; HELA CELL LINE; METABOLISM; MICROTUBULE; PHOSPHORYLATION; PROTEIN MOTIF; PROTEIN TERTIARY STRUCTURE; RNA INTERFERENCE; SPINDLE APPARATUS; TUMOR CELL LINE;

AMINO ACID MOTIFS; AURORA KINASE B; CELL CYCLE PROTEINS; CELL LINE, TUMOR; CHROMOSOME SEGREGATION; FEEDBACK, PHYSIOLOGICAL; HELA CELLS; HUMANS; KINETOCHORES; M PHASE CELL CYCLE CHECKPOINTS; MICROTUBULE-ASSOCIATED PROTEINS; MICROTUBULES; NOCODAZOLE; PHOSPHORYLATION; PROTEIN BINDING; PROTEIN PHOSPHATASE 2; PROTEIN STRUCTURE, TERTIARY; PROTEIN-SERINE-THREONINE KINASES; PROTEIN-TYROSINE KINASES; RNA INTERFERENCE; RNA, SMALL INTERFERING; SIGNAL TRANSDUCTION; SMAD2 PROTEIN; SPINDLE APPARATUS; TUBULIN MODULATORS;

EID: 84923173533     PISSN: 14657392     EISSN: 14764679     Source Type: Journal    
DOI: 10.1038/ncb3065     Document Type: Article

References (42)

1. Santaguida, S. &Musacchio, A. The life and miracles of kinetochores. EMBO J. 28, 2511-2531 (2009).
2. Foley, E. A. &Kapoor, T. M. Microtubule attachment and spindle assembly checkpoint signalling at the kinetochore. Nat. Rev. Mol. Cell Biol. 14, 25-37 (2013).
3. Kops, G. J. &Shah, J. V. Connecting up and clearing out: how kinetochore attachment silences the spindle assembly checkpoint. Chromosoma 121, 509-525 (2012).
4. Funabiki, H. &Wynne, D. J. Making an effective switch at the kinetochore by phosphorylation and dephosphorylation. Chromosoma 122, 135-158 (2013).
5. Bomont, P., Maddox, P., Shah, J. V., Desai, A. B. &Cleveland, D. W. Unstable microtubule capture at kinetochores depleted of the centromere-Associated protein CENP-F. EMBO J. 24, 3927-3939 (2005).
6. Dick, A. E. &Gerlich, D. W. Kinetic framework of spindle assembly checkpoint signalling. Nat. Cell Biol. 15, 1370-1377 (2013).
7. Santaguida, S., Tighe, A., DAlise, A. M., Taylor, S. S. &Musacchio, A. Dissecting the role of MPS1 in chromosome biorientation and the spindle checkpoint through the small molecule inhibitor reversine. J. Cell Biol. 190, 73-87 (2010).
8. Espeut, J., Cheerambathur, D. K., Krenning, L., Oegema, K. &Desai, A. Microtubule binding by KNL-1 contributes to spindle checkpoint silencing at the kinetochore. J. Cell Biol. 196, 469-482 (2012).
9. Vanoosthuyse, V. &Hardwick, K. G. A novel protein phosphatase 1-dependent spindle checkpoint silencing mechanism. Curr. Biol. 19, 1176-1181 (2009).
10. Meadows, J. C. et al. Spindle checkpoint silencing requires association of PP1 to both Spc7 and kinesin-8 motors. Dev. Cell 20, 739-750 (2011).
11. Rosenberg, J. S., Cross, F. R. &Funabiki, H. KNL1/Spc105 recruits PP1 to silence the spindle assembly checkpoint. Curr. Biol. 21, 942-947 (2011).
12. Pinsky, B. A., Nelson, C. R. &Biggins, S. Protein phosphatase 1 regulates exit from the spindle checkpoint in budding yeast. Curr. Biol. 19, 1182-1187 (2009).
13. Gutierrez-Caballero, C., Cebollero, L. R. &Pendas, A. M. Shugoshins: from protectors of cohesion to versatile adaptors at the centromere. Trends Genet. 28, 351-360 (2012).
14. Foley, E. A., Maldonado, M. &Kapoor, T. M. Formation of stable attachments between kinetochores and microtubules depends on the B56-PP2A phosphatase. Nat. Cell Biol. 13, 1265-1271 (2011).
15. Xu, P., Virshup, D. M. &Lee, S. H. B56-PP2A regulates motor dynamics for mitotic chromosome alignment. J. Cell Sci. http://dx.doi.org/10.1242/jcs.154609 (2014).
16. Akopyan, K. et al. Assessing kinetics from fixed cells reveals activation of the mitotic entry network at the S/G2 transition. Mol. Cell 53, 843-853 (2014).
17. Suijkerbuijk, S. J., Vleugel, M., Teixeira, A. &Kops, G. J. Integration of kinase and phosphatase activities by BUBR1 ensures formation of stable kinetochoremicrotubule attachments. Dev. Cell 23, 745-755 (2012).
18. Kruse, T. et al. Direct binding between BubR1 and B56-PP2A phosphatase complexes regulate mitotic progression. J. Cell Sci. 126, 1086-1092 (2013).
19. Xu, P., Raetz, E. A., Kitagawa, M., Virshup, D. M. &Lee, S. H. BUBR1 recruits PP2A via the B56 family of targeting subunits to promote chromosome congression. Biol. Open 2, 479-486 (2013).
20. Hewitt, L. et al. Sustained Mps1 activity is required in mitosis to recruit O-Mad2 to the Mad1-C-Mad2 core complex. J. Cell Biol. 190, 25-34 (2010).
21. Liu, D. et al. Regulated targeting of protein phosphatase 1 to the outer kinetochore by KNL1 opposes Aurora B kinase. J. Cell Biol. 188, 809-820 (2010).
22. Vleugel, M. et al. Arrayed BUB recruitment modules in the kinetochore scaffold KNL1 promote accurate chromosome segregation. J. Cell Biol. 203, 943-955 (2013).
23. Primorac, I. et al. Bub3 reads phosphorylated MELT repeats to promote spindle assembly checkpoint signaling. eLife 2, e01030 (2013).
24. Zhang, G., Lischetti, T. &Nilsson, J. A minimal number of MELT repeats supports all the functions of KNL1 in chromosome segregation. J. Cell Sci. 127, 871-884 (2014).
25. Yamagishi, Y., Yang, C. H., Tanno, Y. &Watanabe, Y. MPS1/Mph1 phosphorylates the kinetochore protein KNL1/Spc7 to recruit SAC components. Nat. Cell Biol. 14, 746-752 (2012).
26. London, N., Ceto, S., Ranish, J. A. &Biggins, S. Phosphoregulation of Spc105 by Mps1 and PP1 regulates Bub1 localization to kinetochores. Curr. Biol. 22, 900-906 (2012).
27. Shepperd, L. A. et al. Phosphodependent recruitment of Bub1 and Bub3 to Spc7/KNL1 by Mph1 kinase maintains the spindle checkpoint. Curr. Biol. 22, 891-899 (2012).
28. Krenn, V., Overlack, K., Primorac, I., van Gerwen, S. &Musacchio, A. KI motifs of human Knl1 enhance assembly of comprehensive spindle checkpoint complexes around MELT repeats. Curr. Biol. 24, 29-39 (2014).
29. Posch, M. et al. Sds22 regulates aurora B activity and microtubule-kinetochore interactions at mitosis. J. Cell Biol. 191, 61-74 (2010).
30. Espert, A. et al. PP2A-B56 opposes Mps1 phosphorylation of Knl1 and thereby promotes spindle assembly checkpoint silencing. J. Cell Biol. 206, 833-842 (2014).
31. Bollen, M., Peti, W., Ragusa, M. J. &Beullens, M. The extended PP1 toolkit: designed to create specificity. Trends Biochem. Sci. 35, 450-458 (2010).
32. Barr, F. A., Elliott, P. R. &Gruneberg, U. Protein phosphatases and the regulation of mitosis. J. Cell Sci. 124, 2323-2334 (2011).
33. Liu, D., Vader, G., Vromans, M. J., Lampson, M. A. &Lens, S. M. Sensing chromosome bi-orientation by spatial separation of aurora B kinase from kinetochore substrates. Science 323, 1350-1353 (2009).
34. Nijenhuis, W. et al. A TPR domain-containing N-terminal module of MPS1 is required for its kinetochore localization by Aurora B. J. Cell Biol. 201, 217-231 (2013).
35. Santaguida, S., Vernieri, C., Villa, F., Ciliberto, A. &Musacchio, A. Evidence that Aurora B is implicated in spindle checkpoint signalling independently of error correction. EMBO J. 30, 1508-1519 (2011).
36. Pines, J. Cubism and the cell cycle: the many faces of the APC/C. Nat. Rev. Mol. Cell Biol. 12, 427-438 (2011).
37. Morin, V. et al. CDK-dependent potentiation of MPS1 kinase activity is essential to the mitotic checkpoint. Curr. Biol. 22, 289-295 (2012).
38. DAngiolella, V., Mari, C., Nocera, D., Rametti, L. &Grieco, D. The spindle checkpoint requires cyclin-dependent kinase activity. Genes Dev. 17, 2520-2525 (2003).
39. Vazquez-Novelle, M. D. et al. Cdk1 inactivation terminates mitotic checkpoint surveillance and stabilizes kinetochore attachments in anaphase. Curr. Biol. 24, 638-645 (2014).
40. Welburn, J. P. et al. Aurora B phosphorylates spatially distinct targets to differentially regulate the kinetochore-microtubule interface. Mol. Cell 38, 383-392 (2010).
41. Gascoigne, K. E. et al. Induced ectopic kinetochore assembly bypasses the requirement for CENP-A nucleosomes. Cell 145, 410-422 (2011).
42. Saurin, A. T., van der Waal, M. S., Medema, R. H., Lens, S. M. &Kops, G. J. Aurora B potentiates Mps1 activation to ensure rapid checkpoint establishment at the onset of mitosis. Nat. Commun. 2, 316 (2011).