The chromosomal passenger complex (CPC) as a key orchestrator of orderly mitotic exit and cytokinesis

Frontiers in Cell and Developmental Biology

Volumn 3, Issue MAR, 2015, Pages

  Kitagawa, Mayumi ^a   Lee, Sang Hyun ^a  

^a DUKE NUS MEDICAL SCHOOL   (Singapore)

Author keywords

Abscission; Aurora B kinase; Chromosomal passenger complex; Chromosome condensation; Chromosome segregation; Cytokinesis; Mitotic exit; Nuclear envelope reformation

Indexed keywords

EID: 85008657434     PISSN: None     EISSN: 2296634X     Source Type: Journal    
DOI: 10.3389/fcell.2015.00014     Document Type: Review

References (120)

1. 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. doi: 10.1083/jcb.153.4.865
2. Adams, R. R., Wheatley, S. P., Gouldsworthy, A. M., Kandels-Lewis, S. E., Carmena, M., Smythe, C., et al. (2000). INCENP binds the Aurora-related kinase AIRK2 and is required to target it to chromosomes, the central spindle and cleavage furrow. Curr. Biol. 10, 1075-1078. doi: 10.1016/S0960-9822(00)00673-4
3. Afonso, O., Matos, I., Pereira, A. J., Aguiar, P., Lampson, M. A., and Maiato, H. (2014). Feedback control of chromosome separation by a midzone Aurora B gradient. Science 345, 332-336. doi: 10.1126/science.1251121
4. Agromayor, M., and Martin-Serrano, J. (2013). Knowing when to cut and run: mechanisms that control cytokinetic abscission. Trends Cell Biol. 23, 433-441. doi: 10.1016/j.tcb.2013.04.006
5. Ahonen, L., Kukkonen, A., Pouwels, J., Bolton, M., Jingle, C., Stukenberg, P. T., et al. (2009). Perturbation of Incenp function impedes anaphase chromatid movements and chromosomal passenger protein flux at centromeres. Chromosoma 118, 71-84. doi: 10.1007/s00412-008-0178-0
6. Ainsztein, A. M., Kandels-Lewis, S. E., Mackay, A. M., and Earnshaw, W. C. (1998). INCENP centromere and spindle targeting: identification of essential conserved motifs and involvement of heterochromatin protein HP1. J. Cell Biol. 143, 1763-1774. doi: 10.1083/jcb.143.7.1763
7. Andrews, P. D. (2005). Aurora kinases: shining lights on the therapeutic horizon? Oncogene 24, 5005-5015. doi: 10.1038/sj.onc.1208752
8. Barr, F. A., Elliott, P. R., and Gruneberg, U. (2011). Protein phosphatases and the regulation of mitosis. J. Cell Sci. 124, 2323-2334. doi: 10.1242/jcs.087106
9. Bastos, R. N., Cundell, M. J., and Barr, F. A. (2014). KIF4A and PP2A-B56 form a spatially restricted feedback loop opposing Aurora B at the anaphase central spindle. J. Cell Biol. 207, 683-693. doi: 10.1083/jcb.201409129
10. Boss, D. S., Witteveen, P. O., Van Der Sar, J., Lolkema, M. P., Voest, E. E., Stockman, P. K., et al. (2011). Clinical evaluation of AZD1152, an i.v. inhibitor of Aurora B kinase, in patients with solid malignant tumors. Ann. Oncol. 22, 431-437. doi: 10.1093/annonc/mdq344
11. Bouchoux, C., and Uhlmann, F. (2011). A quantitative model for ordered Cdk substrate dephosphorylation during mitotic exit. Cell 147, 803-814. doi: 10.1016/j.cell.2011.09.047
12. Capalbo, L., Montembault, E., Takeda, T., Bassi, Z. I., Glover, D. M., and Avino, P. P. (2012). The chromosomal passenger complex controls the function of endosomal sorting complex required for transport-III Snf7 proteins during cytokinesis. Open Biol. 2:120070. doi: 10.1098/rsob.120070
13. Carlton, J. G., Caballe, A., Agromayor, M., Kloc, M., and Martin-Serrano, J. (2012). ESCRT-III governs the Aurora B-mediated abscission checkpoint through CHMP4C. Science 336, 220-225. doi: 10.1126/science.1217180
14. 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. doi: 10.1038/nrm3474
15. Cesario, J. M., Jang, J. K., Redding, B., Shah, N., Rahman, T., and McKim, K. S. (2006). Kinesin 6 family member Subito participates in mitotic spindle assembly and interacts with mitotic regulators. J. Cell Sci. 119, 4770-4780. doi: 10.1242/jcs.03235
16. Cooke, C. A., Heck, M. M., and Earnshaw, W. C. (1987). The inner centromere protein (INCENP) antigens: movement from inner centromere to midbody during mitosis. J. Cell Biol. 105, 2053-2067. doi: 10.1083/jcb.105.5.2053
17. Dennis, M., Davies, M., Oliver, S., D'Souza, R., Pike, L., and Stockman, P. (2012). Phase I study of the Aurora B kinase inhibitor barasertib (AZD1152) to assess the pharmacokinetics, metabolism and excretion in patients with acute myeloid leukemia. Cancer Chemother. Pharmacol. 70, 461-469. doi: 10.1007/s00280-012-1939-2
18. Dobrynin, G., Popp, O., Romer, T., Bremer, S., Schmitz, M. H. A., Gerlich, D. W., et al. (2011). Cdc48/p97-Ufd1-Npl4 antagonizes Aurora B during chromosome segregation in HeLa cells. J. Cell Sci. 124, 1571-1580. doi: 10.1242/jcs.069500
19. Douglas, M. E., Davies, T., Joseph, N., and Mishima, M. (2010). Aurora B and 14-3-3 coordinately regulate clustering of centralspindlin during cytokinesis. Curr. Biol. 20, 927-933. doi: 10.1016/j.cub.2010.03.055
20. Dukes, J. D., Richardson, J. D., Simmons, R., and Whitley, P. (2008). A dominant-negative ESCRT-III protein perturbs cytokinesis and trafficking to lysosomes. Biochem. J. 411, 233-239. doi: 10.1042/BJ20071296
21. Dultz, E. I., Zanin, E., Wurzenberger, C., Braun, M., Rabut, G., Sironi, L., et al. (2008). Systematic kinetic analysis of mitotic dis-and reassembly of the nuclear pore in living cells. J. Cell Biol. 180, 857-865. doi: 10.1083/jcb.200707026
22. Earnshaw, W. C., and Bernat, R. L. (1991). Chromosomal passengers: toward an integrated view of mitosis. Chromosoma 100, 139-146. doi: 10.1007/BF00337241
23. Earnshaw, W. C., and Cooke, C. A. (1991). Analysis of the distribution of the INCENPs throughout mitosis reveals the existence of a pathway of structural changes in the chromosomes during metaphase and early events in cleavage furrow formation. J. Cell Sci. 98, 443-461
24. Elia, N., Sougrat, R., Spurlin, T. A., Hurley, J. H., and Lippincott-Schwartz, J. (2011). Dynamics of endosomal sorting complex required for transport (ESCRT) machinery during cytokinesis and its role in abscission. Proc. Natl. Acad. Sci. U.S.A. 108, 4846-4851. doi: 10.1073/pnas.1102714108
25. Espert, A., Uluocak, P., Bastos, R. N., Mangat, D., Graab, P., and Gruneberg, U. (2014). PP2A-B56 opposes Mps1 phosphorylation of Knl1 and thereby promotes spindle assembly checkpoint silencing. J. Cell Biol. 206, 833-842. doi: 10.1083/jcb.201406109
26. Fededa, J. P., and Gerlich, D. W. (2012). Molecular control of animal cell cytokinesis. Nat. Cell Biol. 14, 440-447. doi: 10.1038/ncb2482
27. Fischle, W., Tseng, B. S., Dormann, H. L., Ueberheide, B. M., Garcia, B. A., Shabanowitz, J., et al. (2005). Regulation of HP1-chromatin binding by histone H3 methylation and phosphorylation. Nature 438, 1116-1122. doi: 10.1038/nature04219
28. 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. doi: 10.1038/ncb2327
29. Fujiwara, T., Bandi, M., Nitta, M., Ivanova, E. V., Bronson, R. T., and Pellman, D. (2005). Cytokinesis failure generating tetraploids promotes tumorigenesis in p53-null cells. Nature 437, 1043-1047. doi: 10.1038/nature04217
30. Fuller, B. G., Lampson, M. A., Foley, E. A., Rosasco-Nitcher, S., Le, K. V., Tobelmann, P., et al. (2008). Midzone activation of aurora B in anaphase produces an intracellular phosphorylation gradient. Nature 453, 1132-1136. doi: 10.1038/nature06923
31. Funabiki, H., and Wynne, D. (2013). Making an effective switch at the kinetochore by phosphorylation and dephosphorylation. Chromosoma 122, 135-158. doi: 10.1007/s00412-013-0401-5
32. Gassmann, R., Carvalho, A., Henzing, A. J., Ruchaud, S., Hudson, D. F., Honda, R., et al. (2004). Borealin: a novel chromosomal passenger required for stability of the bipolar mitotic spindle. J. Cell Biol. 166, 179-191. doi: 10.1083/jcb.200404001
33. 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. doi: 10.1083/jcb.152.4.669
34. Goto, H. (2006). Complex formation of Plk1 and INCENP required for metaphase-anaphase transition. Nat. Cell Biol. 8, 180-187. doi: 10.1038/ncb1350
35. 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. doi: 10.1083/jcb.200403084
36. Guse, A., Mishima, M., and Glotzer, M. (2005). Phosphorylation of ZEN-4/MKLP1 by Aurora B Regulates completion of cytokinesis. Curr. Biol. 15, 778-786. doi: 10.1016/j.cub.2005.03.041
37. Guttinger, S., Laurell, E., and Kutay, U. (2009). Orchestrating nuclear envelope disassembly and reassembly during mitosis. Nat. Rev. Mol. Cell. Biol. 10, 178-191. doi: 10.1038/nrm2641
38. Hill, E., Clarke, M., and Barr, F. A. (2000). The Rab6-binding kinesin, Rab6-KIFL, is required for cytokinesis. EMBO J. 19, 5711-5719. doi: 10.1093/emboj/19.21.5711
39. Hirota, T., Lipp, J. J., Toh, B. H., and Peters, J. M. (2005). Histone H3 serine 10 phosphorylation by Aurora B causes HP1 dissociation from heterochromatin. Nature 438, 1176-1180. doi: 10.1038/nature04254
40. Honda, R., Korner, R., and Nigg, E. A. (2003). Exploring the functional interactions between Aurora B, INCENP, and survivin in mitosis. Mol. Biol. Cell 14, 3325-3341. doi: 10.1091/mbc.E02-11-0769
41. Hu, C.-K., Coughlin, M., Field, C. M., and Mitchison, T. J. (2008). Cell polarization during monopolar cytokinesis. J. Cell Biol. 181, 195-202. doi: 10.1083/jcb.200711105
42. Hudson, D. F., Vagnarelli, P., Gassmann, R., and Earnshaw, W. C. (2003). Condensin is required for nonhistone protein assembly and structural integrity of vertebrate mitotic chromosomes. Dev. Cell 5, 323-336. doi: 10.1016/S1534-5807(03)00199-0
43. Hudson, D., Marshall, K., and Earnshaw, W. (2009). Condensin: architect of mitotic chromosomes. Chromosome Res. 17, 131-144. doi: 10.1007/s10577-008-9009-7
44. Hummer, S., and Mayer, T. U. (2009). Cdk1 negatively regulates midzone localization of the mitotic kinesin mklp2 and the chromosomal passenger complex. Curr. Biol. 19, 607-612. doi: 10.1016/j.cub.2009.02.046
45. Janssen, A., Van Der Burg, M., Szuhai, K., Kops, G. J. P. L., and Medema, R. H. (2011). Chromosome segregation errors as a cause of DNA damage and structural chromosome aberrations. Science 333, 1895-1898. doi: 10.1126/science.1210214
46. 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. doi: 10.1016/j.cell.2007.07.045
47. Kaitna, S., Mendoza, M., Jantsch-Plunger, V., and Glotzer, M. (2000). Incenp and an Aurora-like kinase form a complex essential for chromosome segregation and efficient completion of cytokinesis. Curr. Biol. 10, 1172-1181. doi: 10.1016/S0960-9822(00)00721-1
48. Kaitna, S., Pasierbek, P., Jantsch, M., Loidl, J., and Glotzer, M. (2002). The aurora B kinase AIR-2 regulates kinetochores during mitosis and is required for separation of homologous Chromosomes during meiosis. Curr. Biol. 12, 798-812. doi: 10.1016/S0960-9822(02)00820-5
49. Kawashima, S. A., Yamagishi, Y., Honda, T., Ishiguro, K., and Watanabe, Y. (2010). Phosphorylation of H2A by Bub1 prevents chromosomal instability through localizing shugoshin. Science 327, 172-177. doi: 10.1126/science.1180189
50. 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. doi: 10.1126/science.1189505
51. Kim, Y., Holland, A. J., Lan, W., and Cleveland, D. W. (2010). Aurora kinases and protein phosphatase 1 mediate chromosome congression through regulation of CENP-E. Cell 142, 444-455. doi: 10.1016/j.cell.2010.06.039
52. Kitagawa, M., Fung, S. Y., Hameed, U. F., Goto, H., Inagaki, M., and Lee, S. H. (2014). Cdk1 coordinates timely activation of MKlp2 kinesin with relocation of the chromosome passenger complex for cytokinesis. Cell Rep. 7, 166-179. doi: 10.1016/j.celrep.2014.02.034
53. Kitagawa, M., Fung, S. Y. S., Onishi, N., Saya, H., and Lee, S. H. (2013). Targeting Aurora B to the equatorial cortex by MKlp2 is required for cytokinesis. PLoS ONE 8:e64826. doi: 10.1371/journal.pone.0064826
54. Klein, U. R., Nigg, E. A., and Gruneberg, U. (2006). Centromere targeting of the chromosomal passenger complex requires a ternary subcomplex of Borealin, Survivin, and the N-terminal domain of INCENP. Mol. Biol. Cell 17, 2547-2558. doi: 10.1091/mbc.E05-12-1133
55. Kruse, T., Zhang, G., Larsen, M. S. Y., Lischetti, T., Streicher, W., Kragh Nielsen, T., et al. (2013). Direct binding between BubR1 and B56-PP2A phosphatase complexes regulate mitotic progression. J. Cell Sci. 126, 1086-1092. doi: 10.1242/jcs.122481
56. Kurasawa, Y., Earnshaw, W. C., Mochizuki, Y., Dohmae, N., and Todokoro, K. (2004). Essential roles of KIF4 and its binding partner PRC1 in organized central spindle midzone formation. EMBO J. 23, 3237-3248. doi: 10.1038/sj.emboj.7600347
57. Kuriyama, R., Gustus, C., Terada, Y., Uetake, Y., and Matuliene, J. (2002). CHO1, a mammalian kinesin-like protein, interacts with F-actin and is involved in the terminal phase of cytokinesis. J. Cell Biol. 156, 783-790. doi: 10.1083/jcb.200109090
58. Lafaurie-Janvore, J., Maiuri, P., Wang, I., Pinot, M., Manneville, J.-B., Betz, T., et al. (2013). ESCRT-III assembly and cytokinetic abscission are induced by tension release in the intercellular bridge. Science 339, 1625-1629. doi: 10.1126/science.1233866
59. Lavoie, B. D., Hogan, E., and Koshland, D. (2004). In vivo requirements for rDNA chromosome condensation reveal two cell-cycle-regulated pathways for mitotic chromosome folding. Genes Dev. 18, 76-87. doi: 10.1101/gad.1150404
60. Lee, S. H., McCormick, F., and Saya, H. (2010). Mad2 inhibits the mitotic kinesin MKlp2. J. Cell Biol. 191, 1069-1077. doi: 10.1083/jcb.201003095
61. Lipp, J. J., Hirota, T., Poser, I., and Peters, J.-M. (2007). Aurora B controls the association of condensin I but not condensin II with mitotic chromosomes. J. Cell Sci. 120, 1245-1255. doi: 10.1242/jcs.03425
62. Liu, D., Vleugel, M., Backer, C. B., Hori, T., Fukagawa, T., Cheeseman, I. M., et al. (2010). Regulated targeting of protein phosphatase 1 to the outer kinetochore by KNL1 opposes Aurora B kinase. J. Cell Biol. 188, 809-820. doi: 10.1083/jcb.201001006
63. Löwenberg, B., Muus, P., Ossenkoppele, G., Rousselot, P., Cahn, J.-Y., Ifrah, N., et al. (2011). Phase 1/2 study to assess the safety, efficacy, and pharmacokinetics of barasertib (AZD1152) in patients with advanced acute myeloid leukemia. Blood 118, 6030-6036. doi: 10.1182/blood-2011-07-366930
64. Mackay, D. R., Elgort, S. W., and Ullman, K. S. (2009). The nucleoporin Nup153 has separable roles in both early mitotic progression and the resolution of mitosis. Mol. Biol. Cell 20, 1652-1660. doi: 10.1091/mbc.E08-08-0883
65. Mackay, D. R., Makise, M., and Ullman, K. S. (2010). Defects in nuclear pore assembly lead to activation of an Aurora B-mediated abscission checkpoint. J. Cell Biol. 191, 923-931. doi: 10.1083/jcb.201007124
66. Maerki, S., Olma, M. H., Staubli, T., Steigemann, P., Gerlich, D. W., Quadroni, M., et al. (2009). The Cul3-KLHL21 E3 ubiquitin ligase targets Aurora B to midzone microtubules in anaphase and is required for cytokinesis. J. Cell Biol. 187, 791-800. doi: 10.1083/jcb.200906117
67. Marzo, I., and Naval, J. (2013). Antimitotic drugs in cancer chemotherapy: promises and pitfalls. Biochem. Pharmacol. 86, 703-710. doi: 10.1016/j.bcp.2013.07.010
68. Matuliene, J., and Kuriyama, R. (2002). Kinesin-like protein CHO1 is required for the formation of midbody matrix and the completion of cytokinesis in mammalian cells. Mol. Biol. Cell 13, 1832-1845. doi: 10.1091/mbc.01-10-0504
69. Meyer, H., Drozdowska, A., and Dobrynin, G. (2010). A role for Cdc48/p97 and Aurora B in controlling chromatin condensation during exit from mitosis. Biochem. Cell Biol. 88, 23-28. doi: 10.1139/O09-119
70. Mirchenko, L., and Uhlmann, F. (2010). Sli15(INCENP) dephosphorylation prevents mitotic checkpoint reengagement due to loss of tension at anaphase onset. Curr. Biol. 20, 1396-1401. doi: 10.1016/j.cub.2010.06.023
71. Mishima, M., Kaitna, S., and Glotzer, M. (2002). Central spindle assembly and cytokinesis require a kinesin-like protein/RhoGAP complex with microtubule bundling activity. Dev. Cell 2, 41-54. doi: 10.1016/S1534-5807(01)00110-1
72. Miyauchi, K., Zhu, X., Foong, C., Hosoya, H., and Murata-Hori, M. (2007). Aurora B kinase activity is required to prevent polar cortical ingression during cytokinesis. Cell Cycle 6, 2549-2553. doi: 10.4161/cc.6.20.4817
73. Mocciaro, A., Berdougo, E., Zeng, K., Black, E., Vagnarelli, P., Earnshaw, W., et al. (2010). Vertebrate cells genetically deficient for Cdc14A or Cdc14B retain DNA damage checkpoint proficiency but are impaired in DNA repair. J. Cell Biol. 189, 631-639. doi: 10.1083/jcb.200910057
74. Mollinari, C., Kleman, J.-P., Jiang, W., Schoehn, G., Hunter, T., and Margolis, R. L. (2002). PRC1 is a microtubule binding and bundling protein essential to maintain the mitotic spindle midzone. J. Cell Biol. 157, 1175-1186. doi: 10.1083/jcb.200111052
75. Mora-Bermudez, F., Gerlich, D., and Ellenberg, J. (2007). Maximal chromosome compaction occurs by axial shortening in anaphase and depends on Aurora kinase. Nat. Cell Biol. 9, 822-831. doi: 10.1038/ncb1606
76. Morishita, J., Matsusaka, T., Goshima, G., Nakamura, T., Tatebe, H., and Yanagida, M. (2001). Bir1/Cut17 moving from chromosome to spindle upon the loss of cohesion is required for condensation, spindle elongation and repair. Genes Cells 6, 743-763. doi: 10.1046/j.1365-2443.2001.00459.x
77. Murata-Hori, M., and Wang, Y.-L. (2002). Both midzone and astral microtubules are involved in the delivery of cytokinesis signals: insights from the mobility of aurora B. J. Cell Biol. 159, 45-53. doi: 10.1083/jcb.200207014
78. Nakajima, Y., Cormier, A., Tyers, R. G., Pigula, A., Peng, Y., Drubin, D. G., et al. (2011). Ipl1/Aurora-dependent phosphorylation of Sli15/INCENP regulates CPC-spindle interaction to ensure proper microtubule dynamics. J. Cell Biol. 194, 137-153. doi: 10.1083/jcb.201009137
79. Nakazawa, N., Mehrotra, R., Ebe, M., and Yanagida, M. (2011). Condensin phosphorylated by the Aurora-B-like kinase Ark1 is continuously required until telophase in a mode distinct from Top2. J. Cell Sci. 124, 1795-1807. doi: 10.1242/jcs.078733
80. Nakazawa, N., Nakamura, T., Kokubu, A., Ebe, M., Nagao, K., and Yanagida, M. (2008). Dissection of the essential steps for condensin accumulation at kinetochores and rDNAs during fission yeast mitosis. J. Cell Biol. 180, 1115-1131. doi: 10.1083/jcb.200708170
81. Neurohr, G., Naegeli, A., Titos, I., Theler, D., Greber, B., Díez, J., et al. (2011). A midzone-based ruler adjusts chromosome compaction to anaphase spindle length. Science 332, 465-468. doi: 10.1126/science.1201578
82. 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. doi: 10.1128/MCB.25.12.4977-4992.2005
83. Nguyen, H. G., Makitalo, M., Yang, D., Chinnappan, D. S., Hilaire, C., and Ravid, K. (2009). Deregulated Aurora-B induced tetraploidy promotes tumorigenesis. FASEB J. 23, 2741-2748. doi: 10.1096/fj.09-130963
84. Norden, C., Mendoza, M., Dobbelaere, J., Kotwaliwale, C. V., Biggins, S., and Barral, Y. (2006). The NoCut pathway links completion of cytokinesis to spindle midzone function to prevent chromosome breakage. Cell 125, 85-98. doi: 10.1016/j.cell.2006.01.045
85. Nozawa, R.-S., Nagao, K., Masuda, H.-T., Iwasaki, O., Hirota, T., Nozaki, N., et al. (2010). Human POGZ modulates dissociation of HP1a from mitotic chromosome arms through Aurora B activation. Nat. Cell Biol. 12, 719-727. doi: 10.1038/ncb2075
86. Nunes Bastos, R., Gandhi, S. R., Baron, R. D., Gruneberg, U., Nigg, E. A., and Barr, F. A. (2013). Aurora B suppresses microtubule dynamics and limits central spindle size by locally activating KIF4A. J. Cell Biol. 202, 605-621. doi: 10.1083/jcb.201301094
87. Ono, T., Fang, Y., Spector, D. L., and Hirano, T. (2004). Spatial and temporal regulation of condensins I and II in mitotic chromosome assembly in human cells. Mol. Biol. Cell 15, 3296-3308. doi: 10.1091/mbc.E04-03-0242
88. Ono, T., Losada, A., Hirano, M., Myers, M. P., Neuwald, A. F., and Hirano, T. (2003). Differential contributions of condensin I and condensin II to mitotic chromosome architecture in vertebrate cells. Cell 115, 109-121. doi: 10.1016/S0092-8674(03)00724-4
89. Ota, T., Suto, S., Katayama, H., Han, Z. B., Suzuki, F., and Maeda, 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
90. Pereira, G., and Schiebel, E. (2003). Separase regulates INCENP-Aurora B anaphase spindle function through Cdc14. Science 302, 2120-2124. doi: 10.1126/science.1091936
91. Petersen, J., and Hagan, I. M. (2003). S. pombe Aurora kinase/Survivin is required for chromosome condensation and the spindle checkpoint attachment response. Curr. Biol. 13, 590-597. doi: 10.1016/S0960-9822(03)00205-7
92. Qian, J., Beullens, M., Lesage, B., and Bollen, M. (2013). Aurora B defines its own chromosomal targeting by opposing the recruitment of the phosphatase scaffold Repo-Man. Curr. Biol. 23, 1136-1143. doi: 10.1016/j.cub.2013.05.017
93. Qian, J., Lesage, B., Beullens, M., Van Eynde, A., and Bollen, M. (2011). PP1/Repo-Man dephosphorylates mitotic histone H3 at T3 and regulates chromosomal Aurora B targeting. Curr. Biol. 21, 766-773. doi: 10.1016/j.cub.2011.03.047
94. Ramadan, K., Bruderer, R., Spiga, F. M., Popp, O., Baur, T., Gotta, M., et al. (2007). Cdc48/p97 promotes reformation of the nucleus by extracting the kinase Aurora B from chromatin. Nature 450, 1258-1262. doi: 10.1038/nature06388
95. Ricke, R. M., Jeganathan, K. B., and Van Deursen, J. M. (2011). Bub1 overexpression induces aneuploidy and tumor formation through Aurora B kinase hyperactivation. J. Cell Biol. 193, 1049-1064. doi: 10.1083/jcb.201012035
96. 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. doi: 10.1016/j.devcel.2012.09.005
97. Steigemann, P., Wurzenberger, C., Schmitz, M. H. A., Held, M., Guizetti, J., Maar, S., et al. (2009). Aurora B-mediated abscission checkpoint protects against tetraploidization. Cell 136, 473-484. doi: 10.1016/j.cell.2008.12.020
98. Sumara, I., Quadroni, M., Frei, C., Olma, M. H., Sumara, G., Ricci, R., et al. (2007). A Cul3-based E3 ligase removes Aurora B from mitotic chromosomes, regulating mitotic progression and completion of cytokinesis in human cells. Dev. Cell 12, 887-900. doi: 10.1016/j.devcel.2007.03.019
99. Tada, K., Susumu, H., Sakuno, T., and Watanabe, Y. (2011). Condensin association with histone H2A shapes mitotic chromosomes. Nature 474, 477-483. doi: 10.1038/nature10179
100. Takemoto, A., Maeshima, K., Ikehara, T., Yamaguchi, K., Murayama, A., Imamura, S., et al. (2009). The chromosomal association of condensin II is regulated by a noncatalytic function of PP2A. Nat. Struct. Mol. Biol. 16, 1302-1308. doi: 10.1038/nsmb.1708
101. Takemoto, A., Murayama, A., Katano, M., Urano, T., Furukawa, K., Yokoyama, S., et al. (2007). Analysis of the role of Aurora B on the chromosomal targeting of condensin I. Nucleic Acids Res. 35, 2403-2412. doi: 10.1093/nar/gkm157
102. Thadani, R., Uhlmann, F., and Heeger, S. (2012). Condensin, chromatin crossbarring and chromosome condensation. Curr. Biol. 22, 1012-1021. doi: 10.1016/j.cub.2012.10.023
103. Thoresen, S. B., Campsteijn, C., Vietri, M., Schink, K. O., Liestøl, K., Andersen, J. S., et al. (2014). ANCHR mediates Aurora-B-dependent abscission checkpoint control through retention of VPS4. Nat. Cell Biol. 16, 547-557. doi: 10.1038/ncb2959
104. Tsukahara, T., Tanno, Y., and Watanabe, Y. (2010). Phosphorylation of the CPC by Cdk1 promotes chromosome bi-orientation. Nature 467, 719-723. doi: 10.1038/nature09390
105. Uehara, R., Tsukada, Y., Kamasaki, T., Poser, I., Yoda, K., Gerlich, D. W., et al. (2013). Aurora B and Kif2A control microtubule length for assembly of a functional central spindle during anaphase. J. Cell Biol. 202, 623-636. doi: 10.1083/jcb.201302123
106. Vader, G., Kauw, J. J., Medema, R. H., and Lens, S. M. (2006). Survivin mediates targeting of the chromosomal passenger complex to the centromere and midbody. EMBO Rep. 7, 85-92. doi: 10.1038/sj.embor.7400562
107. Vagnarelli, P., Hudson, D. F., Ribeiro, S. A., Trinkle-Mulcahy, L., Spence, J. M., Lai, F., et al. (2006). Condensin and Repo-Man-PP1 co-operate in the regulation of chromosome architecture during mitosis. Nat. Cell Biol. 8, 1133-1142. doi: 10.1038/ncb1475
108. Vagnarelli, P., Ribeiro, S., Sennels, L., Sanchez-Pulido, L., De lima alves, F., Verheyen, T., et al. (2011). Repo-Man coordinates chromosomal reorganization with nuclear envelope reassembly during mitotic exit. Dev. Cell 21, 328-342. doi: 10.1016/j.devcel.2011.06.020
109. van der Horst, A., and Lens, S. A. (2014). Cell division: control of the chromosomal passenger complex in time and space. Chromosoma 123, 25-42. doi: 10.1007/s00412-013-0437-6
110. Varela, E., Shimada, K., Laroche, T., Leroy, D., and Gasser, S. M. (2009). Lte1, Cdc14 and MEN-controlled Cdk inactivation in yeast coordinate rDNA decompaction with late telophase progression. EMBO J. 28, 1562-1575. doi: 10.1038/emboj.2009.111
111. Vazquez-Novelle, M. D., and Petronczki, M. (2010). Relocation of the chromosomal passenger complex prevents mitotic checkpoint engagement at anaphase. Curr. Biol. 20, 1402-1407. doi: 10.1016/j.cub.2010.06.036
112. Wang, F. (2010). Histone H3 Thr-3 phosphorylation by Haspin positions Aurora B at centromeres in mitosis. Science 330, 231-235. doi: 10.1126/science.1189435
113. Wurzenberger, C., Held, M., Lampson, M. A., Poser, I., Hyman, A. A., and Gerlich, D. W. (2012). Sds22 and Repo-Man stabilize chromosome segregation by counteracting Aurora B on anaphase kinetochores. J. Cell Biol. 198, 173-183. doi: 10.1083/jcb.201112112
114. 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. doi: 10.1242/bio.20134051
115. Xu, P., Virshup, D. M., and Lee, S. H. (2014). B56-PP2A regulates motor dynamics for mitotic chromosome alignment. J. Cell Sci. 127, 4567-4573. doi: 10.1242/jcs.154609
116. Xu, Z., Ogawa, H., Vagnarelli, P., Bergmann, J. H., Hudson, D. F., Ruchaud, S., et al. (2009). INCENP-aurora B interactions modulate kinase activity and chromosome passenger complex localization. J. Cell Biol. 187, 637-653. doi: 10.1083/jcb.200906053
117. 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. doi: 10.1126/science.1194498
118. Yeong, F. M., Hombauer, H., Wendt, K. S., Hirota, T., Mudrak, I., Mechtler, K., et al. (2003). Identification of a subunit of a novel Kleisin-beta/SMC complex as a potential substrate of protein phosphatase 2A. Curr. Biol. 13, 2058-2064. doi: 10.1016/j.cub.2003.10.032
119. Zasadil, L. M., Andersen, K. A., Yeum, D., Rocque, G. B., Wilke, L. G., Tevaarwerk, A. J., et al. (2014). Cytotoxicity of paclitaxel in breast cancer is due to chromosome missegregation on multipolar spindles. Sci. Transl. Med. 6, 229-243. doi: 10.1126/scitranslmed.3007965
120. Zimniak, T., Fitz, V., Zhou, H., Lampert, F., Opravil, S., Mechtler, K., et al. (2012). Spatiotemporal regulation of Ipl1/Aurora activity by direct Cdk1 phosphorylation. Curr. Biol. 22, 787-793. doi: 10.1016/j.cub.2012.03.007