Evidence that Aurora B is implicated in spindle checkpoint signalling independently of error correction

EMBO Journal

Volumn 30, Issue 8, 2011, Pages 1508-1519

  Santaguida, Stefano ^a   Vernieri, Claudio ^b   Villa, Fabrizio ^a   Ciliberto, Andrea ^b   Musacchio, Andrea ^a,c  

^a EUROPEAN INSTITUTE OF ONCOLOGY   (Italy)

^b FIRC INSTITUTE OF MOLECULAR ONCOLOGY   (Italy)

^c MAX PLANCK INSTITUTE OF MOLECULAR PHYSIOLOGY   (Germany)

Author keywords

centromere; hesperadin; kinetochore; reversine; tension

Indexed keywords

AURORA B KINASE; CHECKPOINT KINASE 1; NDC80 COMPLEX; PROTEIN; PROTEIN MPS1; UNCLASSIFIED DRUG;

ARTICLE; CENTROMERE; INHIBITION KINETICS; INTRACELLULAR SIGNALING; MITOSIS; PRIORITY JOURNAL; SPINDLE CELL;

CHROMOSOME SEGREGATION; ENZYME INHIBITORS; HELA CELLS; HUMANS; KINETOCHORES; MITOSIS; MITOTIC SPINDLE APPARATUS; PROTEIN-SERINE-THREONINE KINASES; RNA, SMALL INTERFERING; SIGNAL TRANSDUCTION;

EID: 79954999102     PISSN: 02614189     EISSN: 14602075     Source Type: Journal    
DOI: 10.1038/emboj.2011.70     Document Type: Article

References (58)

1. Biggins S, Murray AW (2001) The budding yeast protein kinase Ipl1/ Aurora allows the absence of tension to activate the spindle checkpoint. Genes Dev 15: 3118-3129 (Pubitemid 33115676)
2. Biggins S, Severin FF, Bhalla N, Sassoon I, Hyman AA, Murray AW (1999) The conserved protein kinase Ipl1 regulates microtubule binding to kinetochores in budding yeast. Genes Dev 13: 532-544 (Pubitemid 29131878)
3. Brito DA, Rieder CL (2006) Mitotic checkpoint slippage in humans occurs via cyclin B destruction in the presence of an active checkpoint. Curr Biol 16: 1194-1200 (Pubitemid 43867292)
4. Carmena M, Ruchaud S, Earnshaw WC (2009) Making the Auroras glow: regulation of Aurora A and B kinase function by interacting proteins. Curr Opin Cell Biol 21 : 796-805
5. Cheeseman IM, Chappie JS, Wilson-Kubalek EM, Desai A (2006) The conserved KMN network constitutes the core microtubule-binding site of the kinetochore. Cell 127: 983-997 (Pubitemid 44792248)
6. Cheeseman IM, Desai A (2008) Molecular architecture of the kinetochore-microtubule interface. Nat Rev Mol Cell Biol 9: 33-46
7. Chou TC (1991) The median-effect principle and the combination index for quantitation of synergism and antagonism. In Synergism and Antagonism in Chemotherapy, Chou TC, Rideout DC (eds) pp 61-102. San Diego: Academic Press
8. Chou TC (2006) Theoretical basis, experimental design, and computerized simulation of synergism and antagonism in drug combination studies. Pharmacol Rev 58: 621-681
9. Chou TC, Talalay P (1981) Generalized equations for the analysis of inhibitions of Michaelis-Menten and higher-order kinetic systems with two or more mutually exclusive and nonexclusive inhibitors. Eur J Biochem 115: 207-216
10. Chou TC, Talalay P (1984) Quantitative analysis of dose-effect relationships: the combined effects of multiple drugs or enzyme inhibitors. Adv Enzyme Regul 22: 27-55
11. Civril F, Wehenkel A, Giorgi FM, Santaguida S, Di Fonzo A, Grigorean G, Ciccarelli FD, Musacchio A (2010) Structural analysis of the RZZ complex reveals common ancestry with multi-subunit vesicle tethering machinery. Structure 18: 616-626
12. De Antoni A, Pearson CG, Cimini D, Canman JC, Sala V, Nezi L, Mapelli M, Sironi L, Faretta M, Salmon ED, Musacchio A (2005) The Mad1/Mad2 complex as a template for Mad2 activation in the spindle assembly checkpoint. Curr Biol 15: 214-225 (Pubitemid 40205701)
13. DeLuca JG, Gall WE, Ciferri C, Cimini D, Musacchio A, Salmon ED (2006) Kinetochore microtubule dynamics and attachment stability are regulated by Hec1. Cell 127: 969-982 (Pubitemid 44792254)
14. DeLuca JG, Howell BJ, Canman JC, Hickey JM, Fang G, Salmon ED (2003) Nuf2 and Hec1 are required for retention of the checkpoint proteins Mad1 and Mad2 to kinetochores. Curr Biol 13: 2103-2109 (Pubitemid 37502528)
15. Ditchfield C, Johnson VL, Tighe A, Ellston R, Haworth C, Johnson T, Mortlock A, Keen N, Taylor SS (2003) Aurora B couples chromosome alignment with anaphase by targeting BubR1, Mad2, and Cenp-E to kinetochores. J Cell Biol 161: 267-280 (Pubitemid 36529846)
16. Emanuele MJ, Lan W, Jwa M, Miller SA, Chan CS, Stukenberg PT (2008) Aurora B kinase and protein phosphatase 1 have opposing roles in modulating kinetochore assembly. J Cell Biol 181: 241-254 (Pubitemid 351574550)
17. Girdler F, Gascoigne KE, Eyers PA, Hartmuth S, Crafter C, Foote KM, Keen NJ, Taylor SS (2006) Validating Aurora B as an anti-cancer drug target. J Cell Sci 11 9 (Pt 17): 3664-3675 (Pubitemid 44501870)
18. Hauf S, Cole RW, LaTerra S, Zimmer C, Schnapp G, Walter R, Heckel A, Van Meel J, Rieder CL, Peters JM (2003) The small molecule Hesperadin reveals a role for Aurora B in correcting kinetochore-microtubule attachment and in maintaining the spindle assembly checkpoint. J Cell Biol 161: 281-294 (Pubitemid 36529847)
19. Hoffman DB, Pearson CG, Yen TJ, Howell BJ, Salmon ED (2001) Microtubule-dependent changes in assembly of microtubule motor proteins and mitotic spindle checkpoint proteins at PtK1 kinetochores. Mol Biol Cell 12: 1995-2009 (Pubitemid 33049694)
20. Hori T, Haraguchi T, Hiraoka Y, Kimura H, Fukagawa T (2003) Dynamic behavior of Nuf2-Hec1 complex that localizes to the centrosome and centromere and is essential for mitotic progression in vertebrate cells. J Cell Sci 11 6 (Pt 16): 3347-3362 (Pubitemid 37038983)
21. Jelluma N, Brenkman AB, Van den Broek NJ, Cruijsen CW, Van Osch MH, Lens SM, Medema RH, Kops GJ (2008) Mps1 phos-phorylates borealin to control Aurora B activity and chromosome alignment. Cell 132: 233-246 (Pubitemid 351172430)
22. Kallio MJ, McCleland ML, Stukenberg PT, Gorbsky GJ (2002) Inhibition of aurora B kinase blocks chromosome segregation, overrides the spindle checkpoint, and perturbs microtubule dynamics in mitosis. Curr Biol 12: 900-905 (Pubitemid 34689224)
23. Khodjakov A, Pines J (2010) Centromere tension: a divisive issue. Nat Cell Biol 12: 919-923
24. Khodjakov A, Rieder CL (2009) The nature of cell-cycle checkpoints: facts and fallacies. J Biol 8: 88
25. King EM, Rachidi N, Morrice N, Hardwick KG, Stark MJ (2007) Ipl1p-dependent phosphorylation of Mad3p is required for the spindle checkpoint response to lack of tension at kinetochores. Genes Dev 21: 1163-1168 (Pubitemid 46789874)
26. Kline SL, Cheeseman IM, Hori T, Fukagawa T, Desai A (2006) The human Mis12 complex is required for kinetochore assembly and proper chromosome segregation. J Cell Biol 173: 9-17
27. Kwiatkowski N, Jelluma N, Filippakopoulos P, Soundararajan M, Manak MS, Kwon M, Choi HG, Sim T, Deveraux QL, Rottmann S, Pellman D, Shah JV, Kops GJ, Knapp S, Gray NS (2010) Small-molecule kinase inhibitors provide insight into Mps1 cell cycle function. Nat Chem Biol 6: 359-368
28. Lampson MA, Cheeseman IM (2010) Sensing centromere tension: Aurora B and the regulation of kinetochore function. Trends Cell Biol (advance online publication 22 November 2010)
29. Liu D, Vader G, Vromans M, Lampson M, Lens S (2009) Sensing chromosome bi-orientation by spatial separation of Aurora B kinase from kinetochore substrates. Science 323: 1350-1353
30. Liu D, Vleugel M, Backer CB, Hori T, Fukagawa T, Cheeseman IM, Lampson MA (2010) Regulated targeting of protein phosphatase 1 to the outer kinetochore by KNL1 opposes Aurora B kinase. J Cell Biol 188: 809-820
31. Liu ST, Rattner JB, Jablonski SA, Yen TJ (2006) Mapping the assembly pathways that specify formation of the trilaminar kinetochore plates in human cells. J Cell Biol 175: 41-53 (Pubitemid 44537197)
32. Loewe S (1953) The problem of synergism and antagonism of combined drugs. Arzneimittelforschung 3: 285-290
33. Maresca TJ, Salmon ED (2009) Intrakinetochore stretch is associated with changes in kinetochore phosphorylation and spindle assembly checkpoint activity. J Cell Biol 184: 373-381
34. Maresca TJ, Salmon ED (2010) Welcome to a new kind of tension: translating kinetochore mechanics into a wait-anaphase signal. J Cell Sci 123 (Pt 6): 825-835
35. Martin-Lluesma S, Stucke VM, Nigg EA (2002) Role of Hec1 in spindle checkpoint signaling and kinetochore recruitment of Mad1/Mad2. Science 297: 2267-2270
36. McAinsh AD, Meraldi P, Draviam VM, Toso A, Sorger PK (2006) The human kinetochore proteins Nnf1R and Mcm21R are required for accurate chromosome segregation. EMBO J 25: 4033-4049 (Pubitemid 44338745)
37. McCleland ML, Gardner RD, Kallio MJ, Daum JR, Gorbsky GJ, Burke DJ, Stukenberg PT (2003) The highly conserved Ndc80 complex is required for kinetochore assembly, chromosome con-gression, and spindle checkpoint activity. Genes Dev 17: 101-114 (Pubitemid 36062512)
38. Meraldi P, Draviam VM, Sorger PK (2004) Timing and checkpoints in the regulation of mitotic progression. Dev Cell 7: 45-60 (Pubitemid 39172687)
39. Meraldi P, Sorger PK (2005) A dual role for Bub1 in the spindle checkpoint and chromosome congression. EMBO J 24: 1621-1633 (Pubitemid 40646451)
40. Morrow CJ, Tighe A, Johnson VL, Scott MI, Ditchfield C, Taylor SS (2005) Bub1 and aurora B cooperate to maintain BubR1-mediated inhibition of APC/CCdc20. J Cell Sci 11 8 (Pt 16): 3639-3652 (Pubitemid 41309411)
41. Mortlock AA, Foote KM, Heron NM, Jung FH, Pasquet G, Lohmann JJ, Warin N, Renaud F, De Savi C, Roberts NJ, Johnson T, Dousson CB, Hill GB, Perkins D, Hatter G, Wilkinson RW, Wedge SR, Heaton SP, Odedra R, Keen NJ et al (2007) Discovery, synthesis, and in vivo activity of a new class of pyrazoloquinazolines as selective inhibitors of aurora B kinase. J Med Chem 50: 2213-2224 (Pubitemid 46683074)
42. Musacchio A, Salmon ED (2007) The spindle-assembly checkpoint in space and time. Nat Rev Mol Cell Biol 8: 379-393 (Pubitemid 46643240)
43. Nezi L, Musacchio A (2009) Sister chromatid tension and the spindle assembly checkpoint. Curr Opin Cell Biol 21: 785-795
44. Nicklas RB, Koch CA (1969) Chromosome micromanipulation. 3. Spindle fiber tension and the reorientation of mal-oriented chromosomes. J Cell Biol 43: 40-50
45. Perera D, Tilston V, Hopwood JA, Barchi M, Boot-Handford RP, Taylor SS (2007) Bub1 maintains centromeric cohesion by activation of the spindle checkpoint. Dev Cell 13: 566-579 (Pubitemid 47500808)
46. Petersen J, Hagan IM (2003) Spombe aurora kinase/survivin is required for chromosome condensation and the spindle checkpoint attachment response. Curr Biol 13: 590-597 (Pubitemid 36391938)
47. Rieder CL, Cole RW, Khodjakov A, Sluder G (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
48. Santaguida S, Musacchio A (2009) The life and miracles of kine-tochores. EMBO J 28: 2511-2531
49. Santaguida S, Tighe A, D'Alise AM, Taylor SS, Musacchio A (2010) Dissecting the role of MPS1 in chromosome biorientation and the spindle checkpoint through the small molecule inhibitor rever-sine. J Cell Biol 190: 73-87
50. Tanaka TU, Rachidi N, Janke C, Pereira G, Gálová M, Schiebel E, Stark MJ, Nasmyth K (2002) Evidence that the Ipl1-Sli15 (Aurora kinase-INCENP) complex promotes chromosome bi-or-ientation by altering kinetochore-spindle pole connections. Cell 108: 317-329 (Pubitemid 34178397)
51. Taylor SS, Hussein D, Wang Y, Elderkin S, Morrow CJ (2001) Kinetochore localisation and phosphorylation of the mitotic checkpoint components Bub1 and BubR1 are differentially regulated by spindle events in human cells. J Cell Sci 114 (Pt 24): 4385-4395 (Pubitemid 34082859)
52. Traut TW (1994) Physiological concentrations of purines and pyrimidines. Mol Cell Biochem 140: 1-22 (Pubitemid 24379884)
53. Trazzi S, Perini G, Bernardoni R, Zoli M, Reese JC, Musacchio A, Della Valle G (2009) The C-terminal domain of CENP-C displays multiple and critical functions for mammalian centromere formation. PLoS One 4: e5832
54. Uchida KS, Takagaki K, Kumada K, Hirayama Y, Noda T, Hirota T (2009) Kinetochore stretching inactivates the spindle assembly checkpoint. J Cell Biol 184: 383-390
55. Vader G, Cruijsen CW, Van Harn T, Vromans MJ, Medema RH, Lens SM (2007) The chromosomal passenger complex controls spindle checkpoint function independent from its role in correcting microtubule kinetochore interactions. Mol Biol Cell 18: 4553-4564 (Pubitemid 350060181)
56. Vanoosthuyse V, Hardwick KG (2009) A novel protein phosphatase 1-dependent spindle checkpoint silencing mechanism. Curr Biol 19: 1176-1181
57. Welburn JPI, Vleugel M, Liu D, Yates III JR, Lampson MA, Fukagawa T, Cheeseman IM (2010) Aurora B phosphorylates spatially distinct targets to differentially regulate the kineto-chore-microtubule interface. Mol Cell 38: 383-392
58. Yang Z, Kenny AE, Brito DA, Rieder CL (2009) Cells satisfy the mitotic checkpoint in Taxol, and do so faster in concentrations that stabilize syntelic attachments. J Cell Biol 186: 675-684