BubR1 acetylation at prometaphase is required for modulating APC/C activity and timing of mitosis

EMBO Journal

Volumn 28, Issue 14, 2009, Pages 2077-2089

  Choi, Eunhee ^a   Choe, Hyerim ^a   Min, Jaewon ^a   Choi, Ji Yoon ^a   Kim, Jimi ^a   Lee, Hyunsook ^a  

^a Seoul National University   (South Korea)

Author keywords

Acetylation; APC C; BubR1; Cdc20; Spindle assembly checkpoint (SAC)

Indexed keywords

ANAPHASE PROMOTING COMPLEX; BUB1 RELATED PROTEIN; CELL CYCLE PROTEIN 20; LYSINE; MUTANT PROTEIN; PROTEIN K250Q; UBIQUITIN; UNCLASSIFIED DRUG;

ACETYLATION; ANAPHASE; ARTICLE; CHROMOSOME SEGREGATION; COMPLEX FORMATION; CONTROLLED STUDY; HUMAN; HUMAN CELL; MASS SPECTROMETRY; MITOSIS; PRIORITY JOURNAL; PROMETAPHASE; PROTEIN DEGRADATION; PROTEIN EXPRESSION; PROTEIN PROTEIN INTERACTION; REGULATORY MECHANISM;

ACETYLATION; AMINO ACID SEQUENCE; ANIMALS; CELL CYCLE PROTEINS; GENES, CDC; HELA CELLS; HUMANS; KINETOCHORES; MITOSIS; MITOTIC SPINDLE APPARATUS; MOLECULAR SEQUENCE DATA; P300-CBP TRANSCRIPTION FACTORS; PROTEIN STABILITY; PROTEIN-SERINE-THREONINE KINASES; SEQUENCE ALIGNMENT; UBIQUITIN-PROTEIN LIGASE COMPLEXES; UBIQUITINATION;

EID: 67651161889     PISSN: 02614189     EISSN: 14602075     Source Type: Journal    
DOI: 10.1038/emboj.2009.123     Document Type: Article

References (49)

1. Abrieu A, Kahana JA, Wood KW, Cleveland DW (2000) CENP-E as an essential component of the mitotic checkpoint in vitro. Cell 102:817-826
2. Bharadwaj R, Yu H (2004) The spindle checkpoint, aneuploidy, and cancer. Oncogene 23: 2016-2027
3. Burton JL, Solomon MJ (2007) Mad3p, a pseudosubstrate inhibitor of APCCdc20 in the spindle assembly checkpoint. Genes Dev 21:655-667
4. Chan GK, Jablonski SA, Sudakin V, Hittle JC, Yen TJ (1999) Human BUBR1 is a mitotic checkpoint kinase that monitors CENP-E functions at kinetochores and binds the cyclosome/APC. J Cell Biol 146:941-954
5. Chan GK, Yen TJ (2003) The mitotic checkpoint: a signaling pathway that allows a single unattached kinetochore to inhibit mitotic exit. Prog Cell Cycle Res 5: 431-439
6. Chen RH (2002) BubR1 is essential for kinetochore localization of other spindle checkpoint proteins and its phosphorylation requires Mad1. J Cell Biol 158:487-496
7. Choi E, Lee H (2008) Chromosome damage in mitosis induces BubR1 activation and prometaphase arrest. FEBS Lett 582:1700-1706
8. Davis FM, Tsao TY, Fowler SK, Rao PN (1983) Monoclonal antibodies to mitotic cells. Proc Natl Acad Sci USA 80:2926-2930
9. 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
10. Elowe S, Hummer S, Uldschmid A, Li X, Nigg EA (2007) Tension-sensitive Plk1 phosphorylation on BubR1 regulates the stability of kinetochore microtubule interactions. Genes Dev 21:2205-2219
11. Gillett ES, Sorger PK (2001) Tracing the pathway of spindle assembly checkpoint signaling. Dev Cell 1: 162-164
12. Glotzer M, Murray AW, Kirschner MW (1991) Cyclin is degraded by the ubiquitin pathway. Nature 349:132-138
13. Herzog F, Primorac I, Dube P, Lenart P, Sander B, Mechtler K, Stark H, Peters J-M (2009) Structure of the Anaphase-Promoting Complex/Cyclosome Interacting with a Mitotic Checkpoint Complex. Science 323:1477-1481
14. Huang H, Hittle J, Zappacosta F, Annan RS, Hershko A, Yen TJ (2008) Phosphorylation sites in BubR1 that regulate kinetochore attachment, tension, and mitotic exit. J Cell Biol 183:667-680
15. Ishii S, Kurasawa Y, Wong J, Yu-Lee LY (2008) Histone deacetylase 3 localizes to the mitotic spindle and is required for kinetochore-microtubule attachment. Proc Natl Acad Sci USA 105:4179-4184
16. King EM, van der Sar SJ, Hardwick KG (2007) Mad3 KEN boxes mediate both Cdc20 and Mad3 turnover, and are critical for the spindle checkpoint. PLoS ONE 2, e342
17. King RW, Deshaies RJ, Peters JM, Kirschner MW (1996a) How proteolysis drives the cell cycle. Science 274:1652-1659
18. King RW, Glotzer M, Kirschner MW (1996b) Mutagenic analysis of the destruction signal of mitotic cyclins and structural characterization of ubiquitinated intermediates. Mol Biol Cell 7: 1343-1357
19. Kops GJ, Weaver BA, Cleveland DW (2005) On the road to cancer: aneuploidy and the mitotic checkpoint. Nat Rev Cancer 5: 773-785
20. Lampson MA, Kapoor TM (2005) The human mitotic checkpoint protein BubR1 regulates chromosome-spindle attachments. Nat Cell Biol 7: 93-98
21. Lindon C, Pines J (2004) Ordered proteolysis in anaphase inactivates Plk1 to contribute to proper mitotic exit in human cells. J Cell Biol 164:233-241
22. Mao Y Abrieu A, Cleveland DW (2003) Activating and silencing the mitotic checkpoint through CENP-E-dependent activation/inacti-vation of BubR1. Cell 114:87-98
23. Mao Y, Desai A, Cleveland DW (2005) Microtubule capture by CENP-E silences BubR1-dependent mitotic checkpoint signaling. J Cell Biol 170:873-880
24. Meraldi P, Draviam VM, Sorger PK (2004) Timing and checkpoints in the regulation of mitotic progression. Dev Cell 7: 45-60
25. Miller JJ, Summers MK, Hansen DV, Nachury MV, Lehman NL, Loktev A, Jackson PK (2006) Emi1 stably binds and inhibits the anaphase-promoting complex/cyclosome as a pseudosubstrate inhibitor. Genes Dev 20:2410-2420
26. Minucci S, Pelicci PG (2006) Histone deacetylase inhibitors and the promise of epigenetic (and more) treatments for cancer. Nat Rev Cancer 6: 38-51
27. 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 118:3639-3652
28. Murray AW, Marks D (2001) Can sequencing shed light on cell cycling? Nature 409:844-846
29. Musacchio A, Hardwick KG (2002) The spindle checkpoint: structural insights into dynamic signalling. Nat Rev Mol Cell Biol 3: 731-741
30. Nilsson J, Yekezare M, Minshull J, Pines J (2008) The APC/C maintains the spindle assembly checkpoint by targeting Cdc20 for destruction. Nat Cell Biol 10:1411-1420
31. Passmore LA, Barford D (2005) Coactivator functions in a stoichiometric complex with anaphase-promoting complex/cyclosome to mediate substrate recognition. EMBO Rep 6: 873-878
32. Peters JM (2006) The anaphase promoting complex/cyclosome: a machine designed to destroy. Nat Rev Mol Cell Biol 7: 644-656
33. Pfleger CM, Kirschner MW (2000) The KEN box: an APC recognition signal distinct from the D box targeted by Cdh1. Genes Dev 14:655-665
34. Pines J, Lindon C (2005) Proteolysis: anytime, any place, anywhere? Nat Cell Biol 7: 731-735
35. Qi W Yu H (2007) KEN-box-dependent degradation of the Bub1 spindle checkpoint kinase by the anaphase-promoting complex/cyclosome. J Biol Chem 282:3672-3679
36. Rieder CL, Maiato H (2004) Stuck in division or passing through: what happens when cells cannot satisfy the spindle assembly checkpoint. Dev Cell 7: 637-651
37. Sczaniecka M, Feoktistova A, May KM, Chen JS, Blyth J, Gould KL, Hardwick KG (2008) The spindle checkpoint functions of Mad3 and Mad2 depend on a Mad3 KEN box-mediated interaction with Cdc20-APC/C. J Biol Chem 283:23039-23047
38. Sudakin V, Chan GK, Yen TJ (2001) Checkpoint inhibition of the APC/C in HeLa cells is mediated by a complex of BUBR1, BUB3, CDC20, and MAD2. J Cell Biol 154:925-936
39. Tang Z, Bharadwaj R, Li B, Yu H (2001) Mad2-Independent inhibition of APCCdc20 by the mitotic checkpoint protein BubR1. Dev Cell 1: 227-237
40. 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 114:4385-4395
41. Taylor SS, Scott MI, Holland AJ (2004) The spindle checkpoint: a quality control mechanism which ensures accurate chromosome segregation. Chromosome Res 12:599-616
42. Thornton BR, Toczyski DP (2006) Precise destruction: an emerging picture of the APC. Genes Dev 20:3069-3078
43. Weaver BA, Bonday ZQ, Putkey FR, Kops GJ, Silk AD, Cleveland DW (2003) Centromere-associated protein-E is essential for the mammalian mitotic checkpoint to prevent aneuploidy due to single chromosome loss. J Cell Biol 162:551-563
44. Wong OK, Fang G (2007) Cdk1 phosphorylation of BubR1 controls spindle checkpoint arrest and Plk1-mediated formation of the 3F3/2 epitope. J Cell Biol 179:611-617
45. Yamano H, Gannon J, Mahbubani H, Hunt T (2004) Cell cycle-regulated recognition of the destruction box of cyclin B by the APC/C in Xenopus egg extracts. Mol Cell 13:137-147
46. Yao X, Abrieu A, Zheng Y, Sullivan KF, Cleveland DW (2000) CENP-E forms a link between attachment of spindle microtubules to kinetochores and the mitotic checkpoint. Nat Cell Biol 2: 484-491
47. Yu H (2002) Regulation of APC-Cdc20 by the spindle checkpoint. Curr Opin Cell Biol 14:706-714
48. Yu H (2007) Cdc20: a WD40 activator for a cell cycle degradation machine. Mol Cell 27:3-16
49. Zhang XD, Goeres J, Zhang H, Yen TJ, Porter AC, Matunis MJ (2008) SUMO-2/3 modification and binding regulate the association of CENP-E with kinetochores and progression through mitosis. Mol Cell 29:729-741