Loss of BubR1 acetylation causes defects in spindle assembly checkpoint signaling and promotes tumor formation

Journal of Cell Biology

Volumn 202, Issue 2, 2013, Pages 295-309

  Park, Inai ^a   Lee, Hae ock ^a   Choi, Eunhee ^a   Lee, Yoo Kyung ^a   Kwon, Mi Sun ^a   Min, Jaewon ^a   Park, Pil Gu ^a   Lee, Seonju ^a   Kong, Young Yun ^a   Gong, Gyungyub ^b   Lee, Hyunsook ^a  

^a Seoul National University   (South Korea)

^b University of Ulsan College of Medicine   (South Korea)

Author keywords

[No Author keywords available]

Indexed keywords

AURORA B KINASE; BUB1 RELATED PROTEIN; NDC80 COMPLEX; NOCODAZOLE; PROTEIN MAD2; PROTEIN P53;

ACETYLATION; ALLELE; ANEUPLOIDY; ANIMAL CELL; ARTICLE; CARCINOGENESIS; CENTROMERE; CHROMATID; CHROMOSOME; CONTROLLED STUDY; EMBRYO; EMBRYO DEVELOPMENT; ENZYME ACTIVITY; FIBROBLAST; GENE MUTATION; K243R GENE; LEUKEMIA; LIVER CELL; LIVER CELL CARCINOMA; LYMPHOMA; M PHASE CELL CYCLE CHECKPOINT; MICRONUCLEUS; MITOSIS; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROTEIN DEGRADATION; PROTEIN LOCALIZATION;

ACETYLATION; ALLELES; ANEUPLOIDY; ANIMALS; CELL CYCLE PROTEINS; CELL TRANSFORMATION, NEOPLASTIC; CHROMOSOMES, MAMMALIAN; EMBRYONIC DEVELOPMENT; GENOMIC INSTABILITY; HETEROZYGOTE; KINETOCHORES; M PHASE CELL CYCLE CHECKPOINTS; MICE; MICE, 129 STRAIN; MICROTUBULE-ASSOCIATED PROTEINS; MITOSIS; MITOTIC SPINDLE APPARATUS; NEOPLASMS, EXPERIMENTAL; PHOSPHORYLATION; PROTEIN-SERINE-THREONINE KINASES; SIGNAL TRANSDUCTION; TIME FACTORS;

EID: 84880803876     PISSN: 00219525     EISSN: 15408140     Source Type: Journal    
DOI: 10.1083/jcb.201210099     Document Type: Article

References (49)

1. Abrieu, A., J.A. Kahana, K.W. Wood, and D.W. Cleveland. 2000. CENP-E as an essential component of the mitotic checkpoint in vitro. Cell. 102:817-826. http://dx.doi.org/10.1016/S0092-8674(00)00070-2
2. Baker, D.J., K.B. Jeganathan, J.D. Cameron, M. Thompson, S. Juneja, A. Kopecka, R. Kumar, R.B. Jenkins, P.C. de Groen, P. Roche, and J.M. van Deursen. 2004. BubR1 insufficiency causes early onset of aging-associated phenotypes and infertility in mice. Nat. Genet. 36:744-749. http://dx.doi.org/10.1038/ng1382
3. Bolanos-Garcia, V.M., T. Lischetti, D. Matak-Vinkovic, E. Cota, P.J. Simpson, D.Y. Chirgadze, D.R. Spring, C.V. Robinson, J. Nilsson, and T.L. Blundell. 2011. Structure of a Blinkin-BUBR1 complex reveals an interaction crucial for kinetochore-mitotic checkpoint regulation via an unanticipated binding Site. Structure. 19:1691-1700. http://dx.doi.org/10.1016/j.str.2011.09.017
4. Chan, G.K., S.A. Jablonski, V. Sudakin, J.C. Hittle, and T.J. Yen. 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. http://dx.doi.org/10.1083/jcb.146.5.941
5. 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
6. 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
7. Choi, E., and H. Lee. 2008. Chromosome damage in mitosis induces BubR1 activation and prometaphase arrest. FEBS Lett. 582:1700-1706. http://dx.doi.org/10.1016/j.febslet.2008.04.028
8. Choi, E., H. Choe, J. Min, J.Y. Choi, J. Kim, and H. Lee. 2009. BubR1 acetylation at prometaphase is required for modulating APC/C activity and timing of mitosis. EMBO J. 28:2077-2089. http://dx.doi.org/10.1038/emboj.2009.123
9. Choi, E., P.G. Park, H.O. Lee, Y.K. Lee, G.H. Kang, J.W. Lee, W. Han, H.C. Lee, D.Y. Noh, S. Lekomtsev, and H. Lee. 2012. BRCA2 fine-tunes the spindle assembly checkpoint through reinforcement of BubR1 acetylation. Dev. Cell. 22:295-308. http://dx.doi.org/10.1016/j.devcel.2012.01.009
10. Crasta, K., N.J. Ganem, R. Dagher, A.B. Lantermann, E.V. Ivanova, Y. Pan, L. Nezi, A. Protopopov, D. Chowdhury, and D. Pellman. 2012. DNA breaks and chromosome pulverization from errors in mitosis. Nature. 482:53-58. http://dx.doi.org/10.1038/nature10802
11. De Antoni, A., C.G. Pearson, D. Cimini, J.C. Canman, V. Sala, L. Nezi, M. Mapelli, L. Sironi, M. Faretta, E.D. Salmon, and A. Musacchio. 2005. The Mad1/Mad2 complex as a template for Mad2 activation in the spindle assembly checkpoint. Curr. Biol. 15:214-225. http://dx.doi.org/10.1016/j.cub.2005.01.038
12. 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
13. DeLuca, K.F., S.M. Lens, and J.G. DeLuca. 2011. Temporal changes in Hec1 phosphorylation control kinetochore-microtubule attachment stability during mitosis. J. Cell Sci. 124:622-634. http://dx.doi.org/10.1242/jcs.072629
14. Guo, Y., C. Kim, S. Ahmad, J. Zhang, and Y. Mao. 2012. CENP-E-dependent BubR1 autophosphorylation enhances chromosome alignment and the mitotic checkpoint. J. Cell Biol. 198:205-217. http://dx.doi.org/10.1083/jcb.201202152
15. Hao, X., M.S. Shin, J.X. Zhou, C.H. Lee, C.F. Qi, Z. Naghashfar, J.W. Hartley, T.N. Fredrickson, J.M. Ward, and H.C. Morse III. 2006. Histologic and molecular characterizations of megakaryocytic leukemia in mice. Leuk. Res. 30:397-406. http://dx.doi.org/10.1016/j.leukres.2005.08.021
16. Johnson, V.L., M.I. Scott, S.V. Holt, D. Hussein, and S.S. Taylor. 2004. Bub1 is required for kinetochore localization of BubR1, Cenp-E, Cenp-F and Mad2, and chromosome congression. J. Cell Sci. 117:1577-1589. http://dx.doi.org/10.1242/jcs.01006
17. Kapoor, T.M., M.A. Lampson, P. Hergert, L. Cameron, D. Cimini, E.D. Salmon, B.F. McEwen, and A. Khodjakov. 2006. Chromosomes can congress to the metaphase plate before biorientation. Science. 311:388-391. http://dx.doi.org/10.1126/science.1122142
18. Kim, S., and H. Yu. 2011. Mutual regulation between the spindle checkpoint and APC/C. Semin. Cell Dev. Biol. 22:551-558. http://dx.doi.org/10.1016/j.semcdb.2011.03.008
19. Kim, Y., A.J. Holland, W. Lan, and D.W. Cleveland. 2010. Aurora kinases and protein phosphatase 1 mediate chromosome congression through regulation of CENP-E. Cell. 142:444-455. http://dx.doi.org/10.1016/j.cell.2010.06.039
20. 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
21. Kloosterman, W.P., M. Tavakoli-Yaraki, M.J. van Roosmalen, E. van Binsbergen, I. Renkens, K. Duran, L. Ballarati, S. Vergult, D. Giardino, K. Hansson, et al. 2012. Constitutional chromothripsis rearrangements involve clustered double-stranded DNA breaks and nonhomologous repair mechanisms. Cell Rep. 1:648-655. http://dx.doi.org/10.1016/j.celrep.2012.05.009
22. Kruse, T., G. Zhang, M.S. Larsen, T. Lischetti, W. Streicher, T. Kragh Nielsen, S.P. Bjørn, and J. Nilsson. 2013. Direct binding between BubR1 and B56-PP2A phosphatase complexes regulate mitotic progression. J. Cell Sci. 126:1086-1092. http://dx.doi.org/10.1242/jcs.122481
23. 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
24. Lampson, M.A., and T.M. Kapoor. 2005. The human mitotic checkpoint protein BubR1 regulates chromosome-spindle attachments. Nat. Cell Biol. 7:93-98. http://dx.doi.org/10.1038/ncb1208
25. 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. http://dx.doi.org/10.1038/ncb1102
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. Lee, Y.K., E. Choi, M.A. Kim, P.G. Park, N.H. Park, and H. Lee. 2009. BubR1 as a prognostic marker for recurrence-free survival rates in epithelial ovarian cancers. Br. J. Cancer. 101:504-510. http://dx.doi.org/10.1038/sj.bjc.6605161
28. Malureanu, L.A., K.B. Jeganathan, M. Hamada, L. Wasilewski, J. Davenport, and J.M. van Deursen. 2009. BubR1 N terminus acts as a soluble inhibitor of cyclin B degradation by APC/C(Cdc20) in interphase. Dev. Cell. 16:118-131. http://dx.doi.org/10.1016/j.devcel.2008.11.004
29. Mao, Y., A. Abrieu, and D.W. Cleveland. 2003. Activating and silencing the mitotic checkpoint through CENP-E-dependent activation/inactivation of BubR1. Cell. 114:87-98. http://dx.doi.org/10.1016/S0092-8674(03)00475-6
30. Michel, L.S., V. Liberal, A. Chatterjee, R. Kirchwegger, B. Pasche, W. Gerald, M. Dobles, P.K. Sorger, V.V. Murty, and R. Benezra. 2001. MAD2 haploinsufficiency causes premature anaphase and chromosome instability in mammalian cells. Nature. 409:355-359. http://dx.doi.org/10.1038/35053094
31. Mitchell, C., and H. Willenbring. 2008. A reproducible and well-tolerated method for 2/3 partial hepatectomy in mice. Nat. Protoc. 3:1167-1170. http://dx.doi.org/10.1038/nprot.2008.80
32. Oromendia, A.B., S.E. Dodgson, and A. Amon. 2012. Aneuploidy causes proteotoxic stress in yeast. Genes Dev. 26:2696-2708. http://dx.doi.org/10.1101/gad.207407.112
33. Rausch, T., D.T. Jones, M. Zapatka, A.M. Stütz, T. Zichner, J. Weischenfeldt, N. Jäger, M. Remke, D. Shih, P.A. Northcott, et al. 2012. Genome sequencing of pediatric medulloblastoma links catastrophic DNA rearrangements with TP53 mutations. Cell. 148:59-71. http://dx.doi.org/10.1016/j.cell.2011.12.013
34. Rieder, C.L. 1981. The structure of the cold-stable kinetochore fiber in metaphase PtK1 cells. Chromosoma. 84:145-158. http://dx.doi.org/10.1007/BF00293368
35. Rivera, T., and A. Losada. 2009. Shugoshin regulates cohesion by driving relocalization of PP2A in Xenopus extracts. Chromosoma. 118:223-233. http://dx.doi.org/10.1007/s00412-008-0190-4
36. Sheltzer, J.M., H.M. Blank, S.J. Pfau, Y. Tange, B.M. George, T.J. Humpton, I.L. Brito, Y. Hiraoka, O. Niwa, and A. Amon. 2011. Aneuploidy drives genomic instability in yeast. Science. 333:1026-1030. http://dx.doi.org/10.1126/science.1206412
37. Sotillo, R., E. Hernando, E. Díaz-Rodríguez, J. Teruya-Feldstein, C. Cordón- Cardo, S.W. Lowe, and R. Benezra. 2007. Mad2 overexpression promotes aneuploidy and tumorigenesis in mice. Cancer Cell. 11:9-23. http://dx.doi.org/10.1016/j.ccr.2006.10.019
38. Stephens, P.J., C.D. Greenman, B. Fu, F. Yang, G.R. Bignell, L.J. Mudie, E.D. Pleasance, K.W. Lau, D. Beare, L.A. Stebbings, et al. 2011. Massive genomic rearrangement acquired in a single catastrophic event during cancer development. Cell. 144:27-40. http://dx.doi.org/10.1016/j.cell.2010.11.055
39. Sudakin, V., G.K. Chan, and T.J. Yen. 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. http://dx.doi.org/10.1083/jcb.200102093
40. Suijkerbuijk, S.J., M. Vleugel, A. Teixeira, and G.J. Kops. 2012. Integration of kinase and phosphatase activities by BUBR1 ensures formation of stable kinetochore-microtubule attachments. Dev. Cell. 23:745-755. http://dx.doi.org/10.1016/j.devcel.2012.09.005
41. Sundin, L.J., and J.G. Deluca. 2010. Kinetochores: NDC80 toes the line. Curr. Biol. 20:R1083-R1085. http://dx.doi.org/10.1016/j.cub.2010.11.033
42. Tang, Z., H. Shu, W. Qi, N.A. Mahmood, M.C. Mumby, and H. Yu. 2006. PP2A is required for centromeric localization of Sgo1 and proper chromosome segregation. Dev. Cell. 10:575-585. http://dx.doi.org/10.1016/j.devcel.2006.03.010
43. Wang, Q., T. Liu, Y. Fang, S. Xie, X. Huang, R. Mahmood, G. Ramaswamy, K.M. Sakamoto, Z. Darzynkiewicz, M. Xu, and W. Dai. 2004. BUBR1 deficiency results in abnormal megakaryopoiesis. Blood. 103:1278-1285. http://dx.doi.org/10.1182/blood-2003-06-2158
44. Weaver, B.A., Z.Q. Bonday, F.R. Putkey, G.J. Kops, A.D. Silk, and D.W. Cleveland. 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. http://dx.doi.org/10.1083/jcb.200303167
45. Weaver, B.A., A.D. Silk, C. Montagna, P. Verdier-Pinard, and D.W. Cleveland. 2007. Aneuploidy acts both oncogenically and as a tumor suppressor. Cancer Cell. 11:25-36. http://dx.doi.org/10.1016/j.ccr.2006.12.003
46. Wei, R.R., J. Al-Bassam, and S.C. Harrison. 2007. The Ndc80/HEC1 complex is a contact point for kinetochore-microtubule attachment. Nat. Struct. Mol. Biol. 14:54-59. http://dx.doi.org/10.1038/nsmb1186
47. 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
48. Yang, F., L. Hu, C. Chen, J. Yu, C.B. O'Connell, A. Khodjakov, M. Pagano, and W. Dai. 2012a. BubR1 is modified by sumoylation during mitotic progression. J. Biol. Chem. 287:4875-4882. http://dx.doi.org/10.1074/jbc.M111.318261
49. Yang, F., Y. Huang, and W. Dai. 2012b. Sumoylated BubR1 plays an important role in chromosome segregation and mitotic timing. Cell Cycle. 11:797-806.