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© The Rockefeller University Press, 0021-9525/2003/4/267 $5.00
The Journal of Cell Biology, Volume 161, Number 2, 267-280

Aurora B couples chromosome alignment with anaphase by targeting BubR1, Mad2, and Cenp-E to kinetochores

¹ School of Biological Sciences, University of Manchester, Manchester M13 9PT, UK
² Cancer and Infection Research Area, AstraZeneca Pharmaceuticals, Mereside, Cheshire SK10 4TG, UK

Address correspondence to Stephen S. Taylor, School of Biological Sciences, University of Manchester, 2.205 Stopford Building, Oxford Rd., Manchester M13 9PT, UK. Tel.: 44-161-275-5100. Fax: 44-161-275-5763. E-mail: stephen.taylor{at}man.ac.uk

The Aurora/Ipl1 family of protein kinases plays multiple roles in mitosis and cytokinesis. Here, we describe ZM447439, a novel selective Aurora kinase inhibitor. Cells treated with ZM447439 progress through interphase, enter mitosis normally, and assemble bipolar spindles. However, chromosome alignment, segregation, and cytokinesis all fail. Despite the presence of maloriented chromosomes, ZM447439-treated cells exit mitosis with normal kinetics, indicating that the spindle checkpoint is compromised. Indeed, ZM447439 prevents mitotic arrest after exposure to paclitaxel. RNA interference experiments suggest that these phenotypes are due to inhibition of Aurora B, not Aurora A or some other kinase. In the absence of Aurora B function, kinetochore localization of the spindle checkpoint components BubR1, Mad2, and Cenp-E is diminished. Furthermore, inhibition of Aurora B kinase activity prevents the rebinding of BubR1 to metaphase kinetochores after a reduction in centromeric tension. Aurora B kinase activity is also required for phosphorylation of BubR1 on entry into mitosis. Finally, we show that BubR1 is not only required for spindle checkpoint function, but is also required for chromosome alignment. Together, these results suggest that by targeting checkpoint proteins to kinetochores, Aurora B couples chromosome alignment with anaphase onset.

Key Words: mitosis; spindle checkpoint; chemical biology; aneuploidy; ZM447439

^* Abbreviation used in this paper: RNAi, RNA interference.

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• Girdler, F., Gascoigne, K. E., Eyers, P. A., Hartmuth, S., Crafter, C., Foote, K. M., Keen, N. J., Taylor, S. S. (2006). Validating Aurora B as an anti-cancer drug target. J. Cell Sci. 119: 3664-3675 [Abstract] [Full Text]  
• Holland, A. J., Taylor, S. S. (2006). Cyclin-B1-mediated inhibition of excess separase is required for timely chromosome disjunction. J. Cell Sci. 119: 3325-3336 [Abstract] [Full Text]  
• Gizatullin, F., Yao, Y., Kung, V., Harding, M. W., Loda, M., Shapiro, G. I. (2006). The Aurora Kinase Inhibitor VX-680 Induces Endoreduplication and Apoptosis Preferentially in Cells with Compromised p53-Dependent Postmitotic Checkpoint Function.. Cancer Res. 66: 7668-7677 [Abstract] [Full Text]  
• Qi, W., Tang, Z., Yu, H. (2006). Phosphorylation- and Polo-Box-dependent Binding of Plk1 to Bub1 Is Required for the Kinetochore Localization of Plk1. Mol. Biol. Cell 17: 3705-3716 [Abstract] [Full Text]  
• Warner, S. L., Bashyam, S., Vankayalapati, H., Bearss, D. J., Han, H., Von Hoff, D. D., Hurley, L. H. (2006). Identification of a lead small-molecule inhibitor of the Aurora kinases using a structure-assisted, fragment-based approach.. Molecular Cancer Therapeutics 5: 1764-1773 [Abstract] [Full Text]  
• Soncini, C., Carpinelli, P., Gianellini, L., Fancelli, D., Vianello, P., Rusconi, L., Storici, P., Zugnoni, P., Pesenti, E., Croci, V., Ceruti, R., Giorgini, M. L., Cappella, P., Ballinari, D., Sola, F., Varasi, M., Bravo, R., Moll, J. (2006). PHA-680632, a Novel Aurora Kinase Inhibitor with Potent Antitumoral Activity.. Clin. Cancer Res. 12: 4080-4089 [Abstract] [Full Text]  
• Wong, J., Fang, G. (2006). HURP controls spindle dynamics to promote proper interkinetochore tension and efficient kinetochore capture. JCB 173: 879-891 [Abstract] [Full Text]  
• Vader, G., Medema, R. H., Lens, S. M.A. (2006). The chromosomal passenger complex: guiding Aurora-B through mitosis. JCB 173: 833-837 [Abstract] [Full Text]  
• Bouzinba-Segard, H., Guais, A., Francastel, C. (2006). Accumulation of small murine minor satellite transcripts leads to impaired centromeric architecture and function. Proc. Natl. Acad. Sci. USA 103: 8709-8714 [Abstract] [Full Text]  
• Spankuch, B., Heim, S., Kurunci-Csacsko, E., Lindenau, C., Yuan, J., Kaufmann, M., Strebhardt, K. (2006). Down-regulation of Polo-like Kinase 1 Elevates Drug Sensitivity of Breast Cancer Cells In vitro and In vivo. Cancer Res. 66: 5836-5846 [Abstract] [Full Text]  
• Klein, U. R., Nigg, E. A., 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 [Abstract] [Full Text]  

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