Functionality of the chromosomal passenger complex in cancer

Biochemical Society Transactions

Volumn 43, Issue , 2015, Pages 23-32

  Hindriksen, Sanne ^a   Meppelink, Amanda ^a   Lens, Susanne M A ^a  

^a UNIVERSITY MEDICAL CENTER UTRECHT   (Netherlands)

Author keywords

Aurora B; Cancer; Chromosomal instability; Chromosomal passenger complex; Error correction

Indexed keywords

AURORA B KINASE; AURKB PROTEIN, HUMAN; BIRC5 PROTEIN, HUMAN; CDCA8 PROTEIN, HUMAN; CELL CYCLE PROTEIN; INCENP PROTEIN, HUMAN; INHIBITOR OF APOPTOSIS PROTEIN; MULTIPROTEIN COMPLEX; NONHISTONE PROTEIN;

ANEUPLOIDY; ARTICLE; CHROMOSOMAL INSTABILITY; CHROMOSOMAL PASSENGER COMPLEX; CHROMOSOME ABERRATION; CHROMOSOME SEGREGATION; GAIN OF FUNCTION MUTATION; GENE AMPLIFICATION; GENE DISRUPTION; GENE EXPRESSION; GENE FUNCTION; GENE MUTATION; GENE REGULATORY NETWORK; HUMAN; M PHASE CELL CYCLE CHECKPOINT; MALIGNANT NEOPLASTIC DISEASE; NONHUMAN; POINT MUTATION; PRIORITY JOURNAL; PROTEIN DEFECT; PROTEIN PHOSPHORYLATION; SISTER CHROMATID; ANIMAL; CYTOKINESIS; GENETICS; METABOLISM; NEOPLASM; PATHOLOGY; PHYSIOLOGY;

ANIMALS; AURORA KINASE B; CELL CYCLE PROTEINS; CHROMOSOMAL INSTABILITY; CHROMOSOMAL PROTEINS, NON-HISTONE; CHROMOSOME SEGREGATION; CYTOKINESIS; HUMANS; INHIBITOR OF APOPTOSIS PROTEINS; MULTIPROTEIN COMPLEXES; NEOPLASMS;

EID: 84921714972     PISSN: 03005127     EISSN: 14708752     Source Type: Journal    
DOI: 10.1042/BST20140275     Document Type: Article

References (111)

1. Duijf, P.H., Schultz, N. and Benezra, R. (2013) Cancer cells preferentially lose small chromosomes. Int. J. Cancer 132, 2316-2326 CrossRef PubMed
2. Duijf, P.H. and Benezra, R. (2013) The cancer biology of whole-chromosome instability. Oncogene 32, 4727-4736 CrossRef PubMed
3. Sheltzer, J.M. (2013) A transcriptional and metabolic signature of primary aneuploidy is present in chromosomally unstable cancer cells and informs clinical prognosis. Cancer Res. 73, 6401-6412 CrossRef PubMed
4. Davoli, T., Xu, A.W., Mengwasser, K.E., Sack, L.M., Yoon, J.C., Park, P.J. and Elledge, S.J. (2013) Cumulative haploinsufficiency and triplosensitivity drive aneuploidy patterns and shape the cancer genome. Cell 155, 948-962 CrossRef PubMed
5. Komarova, N.L., Lengauer, C., Vogelstein, B. and Nowak, M.A. (2002) Dynamics of genetic instability in sporadic and familial colorectal cancer. Cancer Biol. Ther. 1, 685-692 CrossRef PubMed
6. Roschke, A.V., Stover, K., Tonon, G., Schäffer, A.A. and Kirsch, I.R. (2002) Stable karyotypes in epithelial cancer cell lines despite high rates of ongoing structural and numerical chromosomal instability. Neoplasia 4, 19-31 CrossRef PubMed
7. Kops, G.J., Weaver, B.A. and Cleveland, D.W. (2005) On the road to cancer: aneuploidy and the mitotic checkpoint. Nat. Rev. Cancer 5, 773-785 CrossRef PubMed
8. Janssen, A., Kops, G.J. and Medema, R.H. (2009) Elevating the frequency of chromosome mis-segregation as a strategy to kill tumor cells. Proc. Natl. Acad. Sci. U.S.A. 106, 19108-19113 CrossRef PubMed
9. Silk, A.D., Zasadil, L.M., Holland, A.J., Vitre, B., Cleveland, D.W. and Weaver, B.A. (2013) Chromosome missegregation rate predicts whether aneuploidy will promote or suppress tumors. Proc. Natl. Acad. Sci. U.S.A. 110, E4134-E4141 CrossRef PubMed
10. Cheeseman, I.M. and Desai, A. (2008) Molecular architecture of the kinetochore-microtubule interface. Nat. Rev. Mol. Cell Biol. 9, 33-46 CrossRef PubMed
11. Cimini, D. and Degrassi, F. (2005) Aneuploidy: a matter of bad connections. Trends Cell Biol. 15, 442-451 CrossRef PubMed
12. Cimini, D., Howell, B., Maddox, P., Khodjakov, A., Degrassi, F. and Salmon, E.D. (2001) Merotelic kinetochore orientation is a major mechanism of aneuploidy in mitotic mammalian tissue cells. J. Cell Biol. 153, 517-527 CrossRef PubMed
13. Janssen, A., van der Burg, M., Szuhai, K., Kops, G.J. and Medema, R.H. (2011) Chromosome segregation errors as a cause of DNA damage and structural chromosome aberrations. Science 333, 1895-1898 CrossRef PubMed
14. Crasta, K., Ganem, N.J., Dagher, R., Lantermann, A.B., Ivanova, E.V., Pan, Y., Nezi, L., Protopopov, A., Chowdhury, D. and Pellman, D. (2012) DNA breaks and chromosome pulverization from errors in mitosis. Nature 482, 53-58 CrossRef PubMed
15. Foley, E.A. and Kapoor, T.M. (2013) Microtubule attachment and spindle assembly checkpoint signalling at the kinetochore. Nat. Rev. Mol. Cell Biol. 14, 25-37 CrossRef PubMed
16. Silkworth, W.T., Nardi, I.K., Scholl, L.M. and Cimini, D. (2009) Multipolar spindle pole coalescence is a major source of kinetochore mis-attachment and chromosome mis-segregation in cancer cells. PLoS ONE 4, e6564 CrossRef PubMed
17. Ganem, N.J., Godinho, S.A. and Pellman, D. (2009) A mechanism linking extra centrosomes to chromosomal instability. Nature 460, 278-282 CrossRef PubMed
18. Barber, T.D., McManus, K., Yuen, K.W., Reis, M., Parmigiani, G., Shen, D., Barrett, I., Nouhi, Y., Spencer, F., Markowitz, S. et al. (2008) Chromatid cohesion defects may underlie chromosome instability in human colorectal cancers. Proc. Natl. Acad. Sci. U.S.A. 105, 3443-3448 CrossRef PubMed
19. Solomon, D.A., Kim, T., Diaz-Martinez, L.A., Fair, J., Elkahloun, A.G., Harris, B.T., Toretsky, J.A., Rosenberg, S.A., Shukla, N., Ladanyi, M. et al. (2011) Mutational inactivation of STAG2 causes aneuploidy in human cancer. Science 333, 1039-1043 CrossRef PubMed
20. Tanaka, T., Fuchs, J., Loidl, J. and Nasmyth, K. (2000) Cohesin ensures bipolar attachment of microtubules to sister centromeres and resists their precocious separation. Nat. Cell Biol. 2, 492-499 CrossRef PubMed
21. Sonoda, E., Matsusaka, T., Morrison, C., Vagnarelli, P., Hoshi, O., Ushiki, T., Nojima, K., Fukagawa, T., Waizenegger, I.C., Peters, J.M. et al. (2001) Scc1/Rad21/Mcd1 is required for sister chromatid cohesion and kinetochore function in vertebrate cells. Dev. Cell 1, 759-770 CrossRef PubMed
22. Bakhoum, S.F., Genovese, G. and Compton, D.A. (2009) Deviant kinetochore microtubule dynamics underlie chromosomal instability. Curr. Biol. 19, 1937-1942 CrossRef PubMed
23. Bakhoum, S.F., Thompson, S.L., Manning, A.L. and Compton, D.A. (2009) Genome stability is ensured by temporal control of kinetochore-microtubule dynamics. Nat. Cell Biol. 11, 27-35 CrossRef PubMed
24. Weaver, B.A. and Cleveland, D.W. (2006) Does aneuploidy cause cancer? Curr. Opin. Cell Biol. 18, 658-667 CrossRef
25. Gascoigne, K.E. and Taylor, S.S. (2008) Cancer cells display profound intra-and interline variation following prolonged exposure to antimitotic drugs. Cancer Cell 14, 111-122 CrossRef PubMed
26. Thompson, S.L. and Compton, D.A. (2008) Examining the link between chromosomal instability and aneuploidy in human cells. J. Cell Biol. 180, 665-672 CrossRef PubMed
27. Cahill, D.P., Lengauer, C., Yu, J., Riggins, G.J., Willson, J.K., Markowitz, S.D., Kinzler, K.W. and Vogelstein, B. (1998) Mutations of mitotic checkpoint genes in human cancers. Nature 392, 300-303 CrossRef PubMed
28. Michel, L.S., Liberal, V., Chatterjee, A., Kirchwegger, R., Pasche, B., Gerald, W., Dobles, M., Sorger, P.K., Murty, V.V. and Benezra, R. (2001) MAD2 haplo-insufficiency causes premature anaphase and chromosome instability in mammalian cells. Nature 409, 355-359 CrossRef PubMed
29. Lampson, M.A. and Cheeseman, I.M. (2011) Sensing centromere tension: Aurora B and the regulation of kinetochore function. Trends Cell Biol. 21, 133-140 CrossRef PubMed
30. Tanaka, T.U., Rachidi, N., Janke, C., Pereira, G., Galova, M., Schiebel, E., Stark, M.J. and Nasmyth, K. (2002) Evidence that the Ipl1-Sli15 (Aurora kinase-INCENP) complex promotes chromosome bi-orientation by altering kinetochore-spindle pole connections. Cell 108, 317-329 CrossRef PubMed
31. Cheeseman, I.M., Chappie, J.S., Wilson-Kubalek, E.M. and Desai, A. (2006) The conserved KMN network constitutes the core microtubule-binding site of the kinetochore. Cell 127, 983-997 CrossRef PubMed
32. van der Waal, M.S., Hengeveld, R.C., van der Horst, A. and Lens, S.M. (2012) Cell division control by the chromosomal passenger complex. Exp. Cell Res. 318, 1407-1420 CrossRef PubMed
33. Nicklas, R.B. and Ward, S.C. (1994) Elements of error correction in mitosis: microtubule capture, release, and tension. J. Cell Biol. 126, 1241-1253 CrossRef PubMed
34. Loncarek, J., Kisurina-Evgenieva, O., Vinogradova, T., Hergert, P., La Terra, S., Kapoor, T.M. and Khodjakov, A. (2007) The centromere geometry essential for keeping mitosis error free is controlled by spindle forces. Nature 450, 745-749 CrossRef PubMed
35. Indjeian, V.B. and Murray, A.W. (2007) Budding yeast mitotic chromosomes have an intrinsic bias to biorient on the spindle. Curr. Biol. 17, 1837-1846 CrossRef PubMed
36. Andrews, P.D., Ovechkina, Y., Morrice, N., Wagenbach, M., Duncan, K., Wordeman, L. and Swedlow, J.R. (2004) Aurora B regulates MCAK at the mitotic centromere. Dev. Cell 6, 253-268 CrossRef PubMed
37. Liu, D., Vader, G., Vromans, M.J., Lampson, M.A. and Lens, S.M. (2009) Sensing chromosome bi-orientation by spatial separation of Aurora B kinase from kinetochore substrates. Science 323, 1350-1353 CrossRef PubMed
38. Welburn, J.P., Vleugel, M., Liu, D., Yates, 3rd, J.R., Lampson, M.A., Fukagawa, T. and Cheeseman, I.M. (2010) Aurora B phosphorylates spatially distinct targets to differentially regulate the kinetochore-microtubule interface. Mol. Cell 38, 383-392 CrossRef PubMed
39. Liu, D., Vleugel, M., Backer, C.B., Hori, T., Fukagawa, T., Cheeseman, I.M. and Lampson, M.A. (2010) Regulated targeting of protein phosphatase 1 to the outer kinetochore by KNL1 opposes Aurora B kinase. J. Cell Biol. 188, 809-820 CrossRef PubMed
40. Foley, E.A., Maldonado, M. and Kapoor, T.M. (2011) Formation of stable attachments between kinetochores and microtubules depends on the B56-PP2A phosphatase. Nat. Cell Biol. 13, 1265-1271 CrossRef PubMed
41. Suijkerbuijk, S.J., van Osch, M.H., Bos, F.L., Hanks, S., Rahman, N. and Kops, G.J. (2010) Molecular causes for BUBR1 dysfunction in the human cancer predisposition syndrome mosaic variegated aneuploidy. Cancer Res. 70, 4891-4900 CrossRef PubMed
42. Kruse, T., Zhang, G., Larsen, M.S., Lischetti, T., Streicher, W., Kragh Nielsen, T., Bjørn, S.P. and Nilsson, J. (2013) Direct binding between BubR1 and B56-PP2A phosphatase complexes regulate mitotic progression. J. Cell Sci. 126, 1086-1092 CrossRef PubMed
43. Xu, P., Raetz, E.A., Kitagawa, M., Virshup, D.M. and Lee, S.H. (2013) BUBR1 recruits PP2A via the B56 family of targeting subunits to promote chromosome congression. Biol. Open 2, 479-486 CrossRef PubMed
44. Vader, G., Cruijsen, C.W., van Harn, T., Vromans, M.J., Medema, R.H. and Lens, S.M. (2007) The chromosomal passenger complex controls spindle checkpoint function independent from its role in correcting microtubule kinetochore interactions. Mol. Biol. Cell 18, 4553-4564 CrossRef PubMed
45. Saurin, A.T., van der Waal, M.S., Medema, R.H., Lens, S.M. and Kops, G.J. (2011) Aurora B potentiates Mps1 activation to ensure rapid checkpoint establishment at the onset of mitosis. Nat. Commun. 2, 316 CrossRef PubMed
46. Santaguida, S., Vernieri, C., Villa, F., Ciliberto, A. and Musacchio, A. (2011) Evidence that Aurora B is implicated in spindle checkpoint signalling independently of error correction. EMBO J. 30, 1508-1519 CrossRef PubMed
47. Terada, Y., Tatsuka, M., Suzuki, F., Yasuda, Y., Fujita, S. and Otsu, M. (1998) AIM-1: a mammalian midbody-associated protein required for cytokinesis. EMBO J. 17, 667-676 CrossRef PubMed
48. Severson, A.F., Hamill, D.R., Carter, J.C., Schumacher, J. and Bowerman, B. (2000) The Aurora-related kinase AIR-2 recruits ZEN-4/CeMKLP1 to the mitotic spindle at metaphase and is required for cytokinesis. Curr. Biol. 10, 1162-1171 CrossRef PubMed
49. Adams, R.R., Maiato, H., Earnshaw, W.C. and Carmena, M. (2001) Essential roles of Drosophila inner centromere protein (INCENP) and Aurora B in histone H3 phosphorylation, metaphase chromosome alignment, kinetochore disjunction, and chromosome segregation. J. Cell Biol. 153, 865-880 CrossRef PubMed
50. Giet, R. and Glover, D.M. (2001) Drosophila Aurora B kinase is required for histone H3 phosphorylation and condensin recruitment during chromosome condensation and to organize the central spindle during cytokinesis. J. Cell Biol. 152, 669-682 CrossRef PubMed
51. Kallio, M.J., McCleland, M.L., Stukenberg, P.T. and Gorbsky, G.J. (2002) Inhibition of Aurora B kinase blocks chromosome segregation, overrides the spindle checkpoint, and perturbs microtubule dynamics in mitosis. Curr. Biol. 12, 900-905 CrossRef PubMed
52. Ditchfield, C., Johnson, V.L., Tighe, A., Ellston, R., Haworth, C., Johnson, T., Mortlock, A., Keen, N. and Taylor, S.S. (2003) Aurora B couples chromosome alignment with anaphase by targeting BubR1, Mad2, and Cenp-E to kinetochores. J. Cell Biol. 161, 267-280 CrossRef PubMed
53. Hauf, S., Cole, R.W., LaTerra, S., Zimmer, C., Schnapp, G., Walter, R., Heckel, A., van Meel, J., Rieder, C.L. and Peters, J.M. (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 CrossRef PubMed
54. Cimini, D., Wan, X., Hirel, C.B. and Salmon, E.D. (2006) Aurora kinase promotes turnover of kinetochore microtubules to reduce chromosome segregation errors. Curr. Biol. 16, 1711-1718 CrossRef PubMed
55. Lens, S.M., Rodriguez, J.A., Vader, G., Span, S.W., Giaccone, G. and Medema, R.H. (2006) Uncoupling the central spindle-associated function of the chromosomal passenger complex from its role at centromeres. Mol. Biol. Cell 17, 1897-1909 CrossRef PubMed
56. Gassmann, R., Carvalho, A., Henzing, A.J., Ruchaud, S., Hudson, D.F., Honda, R., Nigg, E.A., Gerloff, D.L. and Earnshaw, W.C. (2004) Borealin: a novel chromosomal passenger required for stability of the bipolar mitotic spindle. J. Cell Biol. 166, 179-191 CrossRef PubMed
57. Jeyaprakash, A.A., Klein, U.R., Lindner, D., Ebert, J., Nigg, E.A. and Conti, E. (2007) Structure of a Survivin-Borealin-INCENP core complex reveals how chromosomal passengers travel together. Cell 131, 271-285 CrossRef PubMed
58. M͡ oz-Barrera, M. and Monje-Casas, F. (2014) Increased Aurora B activity causes continuous disruption of kinetochore-microtubule attachments and spindle instability. Proc. Natl. Acad. Sci. U.S.A. 111, E3996-E4005 CrossRef PubMed
59. Ota, T., Suto, S., Katayama, H., Han, Z.B., Suzuki, F., Maeda, M., Tanino, M., Terada, Y. and Tatsuka, M. (2002) Increased mitotic phosphorylation of histone H3 attributable to AIM-1/Aurora-B overexpression contributes to chromosome number instability. Cancer Res. 62, 5168-5177 PubMed
60. Tatsuka, M., Katayama, H., Ota, T., Tanaka, T., Odashima, S., Suzuki, F. and Terada, Y. (1998) Multinuclearity and increased ploidy caused by overexpression of the Aurora-and Ipl1-like midbody-associated protein mitotic kinase in human cancer cells. Cancer Res. 58, 4811-4816 PubMed
61. Nguyen, H.G., Chinnappan, D., Urano, T. and Ravid, K. (2005) Mechanism of Aurora-B degradation and its dependency on intact KEN and A-boxes: identification of an aneuploidy-promoting property. Mol. Cell. Biol. 25, 4977-4992 CrossRef PubMed
62. Nguyen, H.G., Makitalo, M., Yang, D., Chinnappan, D., St Hilaire, C. and Ravid, K. (2009) Deregulated Aurora-B induced tetraploidy promotes tumorigenesis. FASEB J. 23, 2741-2748 CrossRef PubMed
63. Lens, S.M., Voest, E.E. and Medema, R.H. (2010) Shared and separate functions of Polo-like kinases and Aurora kinases in cancer. Nat. Rev. Cancer 10, 825-841 CrossRef PubMed
64. Carter, S.L., Eklund, A.C., Kohane, I.S., Harris, L.N. and Szallasi, Z. (2006) A signature of chromosomal instability inferred from gene expression profiles predicts clinical outcome in multiple human cancers. Nat. Genet. 38, 1043-1048 CrossRef PubMed
65. Kimura, M., Kotani, S., Hattori, T., Sumi, N., Yoshioka, T., Todokoro, K. and Okano, Y. (1997) Cell cycle-dependent expression and spindle pole localization of a novel human protein kinase, Aik, related to Aurora of Drosophila and yeast Ipl1. J. Biol. Chem. 272, 13766-13771 CrossRef PubMed
66. Bischoff, J.R., Anderson, L., Zhu, Y., Mossie, K., Ng, L., Souza, B., Schryver, B., Flanagan, P., Clairvoyant, F., Ginther, C. et al. (1998) A homologue of Drosophila Aurora kinase is oncogenic and amplified in human colorectal cancers. EMBO J. 17, 3052-3065 CrossRef PubMed
67. Thiru, P., Kern, D.M., McKinley, K.L., Monda, J.K., Rago, F., Su, K.C., Tsinman, T., Yarar, D., Bell, G.W. and Cheeseman, I.M. (2014) Kinetochore genes are coordinately up-regulated in human tumors as part of a FoxM1-related cell division program. Mol. Biol. Cell 25, 1983-1994 CrossRef PubMed
68. Fernández-Miranda, G., Trakala, M., Martin, J., Escobar, B., González, A., Ghyselinck, N.B., Ortega, S., Cañamero, M., Pérez de Castro, I. and Malumbres, M. (2011) Genetic disruption of Aurora B uncovers an essential role for Aurora C during early mammalian development. Development 138, 2661-2672 CrossRef PubMed
69. Honda, R., Körner, R. and Nigg, E.A. (2003) Exploring the functional interactions between Aurora B, INCENP, and survivin in mitosis. Mol. Biol. Cell 14, 3325-3341 CrossRef PubMed
70. Lens, S.M., Wolthuis, R.M., Klompmaker, R., Kauw, J., Agami, R., Brummelkamp, T., Kops, G. and Medema, R.H. (2003) Survivin is required for a sustained spindle checkpoint arrest in response to lack of tension. EMBO J. 22, 2934-2947 CrossRef PubMed
71. Carvalho, A., Carmena, M., Sambade, C., Earnshaw, W.C. and Wheatley, S.P. (2003) Survivin is required for stable checkpoint activation in taxol-treated HeLa cells. J Cell Sci. 116, 2987-2998 CrossRef PubMed
72. Uren, A.G., Wong, L., Pakusch, M., Fowler, K.J., Burrows, F.J., Vaux, D.L. and Choo, K.H. (2000) Survivin and the inner centromere protein INCENP show similar cell-cycle localization and gene knockout phenotype. Curr. Biol. 10, 1319-1328 CrossRef PubMed
73. Yamanaka, Y., Heike, T., Kumada, T., Shibata, M., Takaoka, Y., Kitano, A., Shiraishi, K., Kato, T., Nagato, M., Okawa, K. et al. (2008) Loss of Borealin/DasraB leads to defective cell proliferation, p53 accumulation and early embryonic lethality. Mech. Dev. 125, 441-450 CrossRef PubMed
74. Cutts, S.M., Fowler, K.J., Kile, B.T., Hii, L.L., O'Dowd, R.A., Hudson, D.F., Saffery, R., Kalitsis, P., Earle, E. and Choo, K.H. (1999) Defective chromosome segregation, microtubule bundling and nuclear bridging in inner centromere protein gene (Incenp)-disrupted mice. Hum. Mol. Genet. 8, 1145-1155 CrossRef PubMed
75. Jung, H.L., Wang, K.C., Kim, S.K., Sung, K.W., Koo, H.H., Shin, H.Y., Ahn, H.S., Shin, H.J. and Cho, B.K. (2004) Loss of heterozygosity analysis of chromosome 17p13.1-13.3 and its correlation with clinical outcome in medulloblastomas. J. Neurooncol. 67, 41-46 CrossRef PubMed
76. Grebe, S.K., McIver, B., Hay, I.D., Wu, P.S., Maciel, L.M., Drabkin, H.A., Goellner, J.R., Grant, C.S., Jenkins, R.B. and Eberhardt, N.L. (1997) Frequent loss of heterozygosity on chromosomes 3p and 17p without VHL or p53 mutations suggests involvement of unidentified tumor suppressor genes in follicular thyroid carcinoma. J. Clin. Endocrinol. Metab. 82, 3684-3691 PubMed
77. Eiriksdottir, G., Barkardottir, R.B., Agnarsson, B.A., Johannesdottir, G., Olafsdottir, K., Egilsson, V. and Ingvarsson, S. (1998) High incidence of loss of heterozygosity at chromosome 17p13 in breast tumours from BRCA2 mutation carriers. Oncogene 16, 21-26 CrossRef PubMed
78. Christiansen, D.H., Andersen, M.K. and Pedersen-Bjergaard, J. (2001) Mutations with loss of heterozygosity of p53 are common in therapy-related myelodysplasia and acute myeloid leukemia after exposure to alkylating agents and significantly associated with deletion or loss of 5q, a complex karyotype, and a poor prognosis. J. Clin. Oncol. 19, 1405-1413 PubMed
79. Campo, E., de la Calle-Martin, O., Miquel, R., Palacin, A., Romero, M., Fabregat, V., Vives, J., Cardesa, A. and Yague, J. (1991) Loss of heterozygosity of p53 gene and p53 protein expression in human colorectal carcinomas. Cancer Res. 51, 4436-4442 PubMed
80. Hegyi, K., Egervári, K., Sándor, Z. and Méhes, G. (2012) Aurora kinase B expression in breast carcinoma: cell kinetic and genetic aspects. Pathobiology 79, 314-322 CrossRef PubMed
81. Margolis, R.L., Lohez, O.D. and Andreassen, P.R. (2003) G1 tetraploidy checkpoint and the suppression of tumorigenesis. J. Cell. Biochem. 88, 673-683 CrossRef PubMed
82. Thompson, S.L. and Compton, D.A. (2010) Proliferation of aneuploid human cells is limited by a p53-dependent mechanism. J. Cell Biol. 188, 369-381 CrossRef PubMed
83. Vogelstein, B., Papadopoulos, N., Velculescu, V.E., Zhou, S., Diaz, Jr, L.A. and Kinzler, K.W. (2013) Cancer genome landscapes. Science 339, 1546-1558 CrossRef PubMed
84. Ponder, B.A. (2001) Cancer genetics. Nature 411, 336-341 CrossRef PubMed
85. Chin, L., Hahn, W.C., Getz, G. and Meyerson, M. (2011) Making sense of cancer genomic data. Genes Dev. 25, 534-555 CrossRef PubMed
86. Stratton, M.R. (2011) Exploring the genomes of cancer cells: progress and promise. Science 331, 1553-1558 CrossRef PubMed
87. Vogelstein, B. and Kinzler, K.W. (2004) Cancer genes and the pathways they control. Nat. Med. 10, 789-799 CrossRef PubMed
88. Hengeveld, R.C., Hertz, N.T., Vromans, M.J., Zhang, C., Burlingame, A.L., Shokat, K.M. and Lens, S.M. (2012) Development of a chemical genetic approach for human Aurora B kinase identifies novel substrates of the chromosomal passenger complex. Mol. Cell. Proteomics 11, 47-59 CrossRef PubMed
89. Kettenbach, A.N., Schweppe, D.K., Faherty, B.K., Pechenick, D., Pletnev, A.A. and Gerber, S.A. (2011) Quantitative phosphoproteomics identifies substrates and functional modules of Aurora and Polo-like kinase activities in mitotic cells. Sci. Signal. 4, rs5 CrossRef PubMed
90. Koch, A., Krug, K., Pengelley, S., Macek, B. and Hauf, S. (2011) Mitotic substrates of the kinase Aurora with roles in chromatin regulation identified through quantitative phosphoproteomics of fission yeast. Sci. Signal. 4, rs6 CrossRef PubMed
91. Ricke, R.M., Jeganathan, K.B. and van Deursen, J.M. (2011) Bub1 overexpression induces aneuploidy and tumor formation through Aursora B kinase hyperactivation. J. Cell Biol. 193, 1049-1064 CrossRef PubMed
92. Park, I., Lee, H.O., Choi, E., Lee, Y.K., Kwon, M.S., Min, J., Park, P.G., Lee, S., Kong, Y.Y., Gong, G. and Lee, H. (2013) Loss of BubR1 acetylation causes defects in spindle assembly checkpoint signaling and promotes tumor formation. J. Cell Biol. 202, 295-309 CrossRef PubMed
93. Suijkerbuijk, S.J., Vleugel, M., Teixeira, A. and Kops, G.J. (2012) Integration of kinase and phosphatase activities by BUBR1 ensures formation of stable kinetochore-microtubule attachments. Dev. Cell 23, 745-755 CrossRef PubMed
94. Lampson, M.A., Renduchitala, K., Khodjakov, A. and Kapoor, T.M. (2004) Correcting improper chromosome-spindle attachments during cell division. Nat. Cell Biol. 6, 232-237 CrossRef PubMed
95. Hanks, S., Coleman, K., Reid, S., Plaja, A., Firth, H., Fitzpatrick, D., Kidd, A., Méhes, K., Nash, R., Robin, N. et al. (2004) Constitutional aneuploidy and cancer predisposition caused by biallelic mutations in BUB1B. Nat. Genet. 36, 1159-1161 CrossRef PubMed
96. Sotillo, R., Hernando, E., Diaz-Rodriguez, E., Teruya-Feldstein, J., Cordón-Cardo, C., Lowe, S.W. and Benezra, R. (2007) Mad2 overexpression promotes aneuploidy and tumorigenesis in mice. Cancer Cell 11, 9-23 CrossRef PubMed
97. Kabeche, L. and Compton, D.A. (2012) Checkpoint-independent stabilization of kinetochore-microtubule attachments by Mad2 in human cells. Curr. Biol. 22, 638-644 CrossRef PubMed
98. Bian, Y., Kitagawa, R., Bansal, P.K., Fujii, Y., Stepanov, A. and Kitagawa, K. (2014) Synthetic genetic array screen identifies PP2A as a therapeutic target in Mad2-overexpressing tumors. Proc. Natl. Acad. Sci. U.S.A. 111, 1628-1633 CrossRef PubMed
99. Britigan, E.M., Wan, J., Zasadil, L.M., Ryan, S.D. and Weaver, B.A. (2014) The ARF tumor suppressor prevents chromosomal instability and ensures mitotic checkpoint fidelity through regulation of Aurora B. Mol. Biol. Cell 25, 2761-2773 CrossRef PubMed
100. Sherr, C.J. (1996) Cancer cell cycles. Science 274, 1672-1677 CrossRef PubMed
101. Kefford, R.F., Newton Bishop, J.A., Bergman, W. and Tucker, M.A. (1999) Counseling and DNA testing for individuals perceived to be genetically predisposed to melanoma: a consensus statement of the Melanoma Genetics Consortium. J. Clin. Oncol. 17, 3245-3251 PubMed
102. Pomerantz, J., Schreiber-Agus, N., Liégeois, N.J., Silverman, A., Alland, L., Chin, L., Potes, J., Chen, K., Orlow, I., Lee, H.W. et al. (1998) The Ink4a tumor suppressor gene product, p19Arf, interacts with MDM2 and neutralizes MDM2-s inhibition of p53. Cell 92, 713-723 CrossRef PubMed
103. Carmena, M., Wheelock, M., Funabiki, H. and Earnshaw, W.C. (2012) The chromosomal passenger complex (CPC): from easy rider to the godfather of mitosis. Nat. Rev. Mol. Cell Biol. 13, 789-803 CrossRef PubMed
104. Sessa, F., Mapelli, M., Ciferri, C., Tarricone, C., Areces, L.B., Schneider, T.R., Stukenberg, P.T. and Musacchio, A. (2005) Mechanism of Aurora B activation by INCENP and inhibition by hesperadin. Mol. Cell 18, 379-391 CrossRef PubMed
105. Petsalaki, E., Akoumianaki, T., Black, E.J., Gillespie, D.A. and Zachos, G. (2011) Phosphorylation at serine 331 is required for Aurora B activation. J. Cell Biol. 195, 449-466 CrossRef PubMed
106. Bishop, J.D. and Schumacher, J.M. (2002) Phosphorylation of the carboxyl terminus of inner centromere protein (INCENP) by the Aurora B kinase stimulates Aurora B kinase activity. J. Biol. Chem. 277, 27577-27580 CrossRef PubMed
107. Wang, F., Dai, J., Daum, J.R., Niedzialkowska, E., Banerjee, B., Stukenberg, P.T., Gorbsky, G.J. and Higgins, J.M. (2010) Histone H3 Thr-3 phosphorylation by haspin positions Aurora B at centromeres in mitosis. Science 330, 231-235 CrossRef PubMed
108. Kelly, A.E., Ghenoiu, C., Xue, J.Z., Zierhut, C., Kimura, H. and Funabiki, H. (2010) Survivin reads phosphorylated histone H3 threonine 3 to activate the mitotic kinase Aurora B. Science 330, 235-239 CrossRef PubMed
109. Tsukahara, T., Tanno, Y. and Watanabe, Y. (2010) Phosphorylation of the CPC by Cdk1 promotes chromosome bi-orientation. Nature 467, 719-723 CrossRef PubMed
110. Yamagishi, Y., Honda, T., Tanno, Y. and Watanabe, Y. (2010) Two histone marks establish the inner centromere and chromosome bi-orientation. Science 330, 239-243 CrossRef PubMed
111. Gruneberg, U., Neef, R., Honda, R., Nigg, E.A. and Barr, F.A. (2004) Relocation of Aurora B from centromeres to the central spindle at the metaphase to anaphase transition requires MKlp2. J. Cell Biol. 166, 167-172 CrossRef PubMed