Selective aurora kinase inhibitors identified using a taxol-induced checkpoint sensitivity screen

ACS Chemical Biology

Volumn 7, Issue 1, 2012, Pages 185-196

  Kwiatkowski, Nicholas ^a,b   Deng, Xianming ^a,b   Wang, Jinhua ^a,b   Tan, Li ^a,b   Villa, Fabrizio ^d   Santaguida, Stefano ^d,f   Huang, Hsiao Chun ^c   Mitchison, Tim ^c   Musacchio, Andrea ^d,e   Gray, Nathanael ^a,b  

^a DANA FARBER CANCER INSTITUTE   (United States)

^b Department of Biological Chemistry and Molecular Pharmacology ^*  (United States)

^c HARVARD MEDICAL SCHOOL   (United States)

^d EUROPEAN INSTITUTE OF ONCOLOGY   (Italy)

^e MAX PLANCK INSTITUTE OF MOLECULAR PHYSIOLOGY   (Germany)

^f MASSACHUSETTS INSTITUTE OF TECHNOLOGY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

4 [[9 CHLORO 7 (2,6 DIFLUOROPHENYL) 5H PYRIMIDO[5,4 D][2]BENZAZEPIN 2 YL]AMINO]BENZOIC ACID; AURORA A KINASE; AURORA B KINASE; AURORA C KINASE; AURORA KINASE INHIBITOR; BARASERTIB; BENZO[E]PYRIMIDO[5,4 B][1,4]DIAZEPIN 6(11H) ONE; HISTONE H3; LEUCINE RICH REPEAT KINASE 2; PACLITAXEL; SERINE; TOZASERTIB; UNCLASSIFIED DRUG;

ANTIPROLIFERATIVE ACTIVITY; ARTICLE; CELL DEATH; CELL STRAIN HCT116; CELL STRAIN HT29; CELL VIABILITY; CONCENTRATION RESPONSE; CONTROLLED STUDY; CRYSTAL STRUCTURE; DRUG DETERMINATION; DRUG IDENTIFICATION; DRUG POTENCY; DRUG POTENTIATION; DRUG SELECTIVITY; DRUG STRUCTURE; ENDOREDUPLICATION; ENZYME INHIBITION; FEMALE; HELA CELL; HUMAN; HUMAN CELL; IC 50; M PHASE CELL CYCLE CHECKPOINT; MITOSIS INHIBITION; PRIORITY JOURNAL; PROTEIN PHOSPHORYLATION; STRUCTURE ACTIVITY RELATION;

ANIMALS; ANTINEOPLASTIC AGENTS, PHYTOGENIC; ANTINEOPLASTIC COMBINED CHEMOTHERAPY PROTOCOLS; BENZAZEPINES; CELL LINE, TUMOR; CELL SURVIVAL; CRYSTALLOGRAPHY, X-RAY; HIGH-THROUGHPUT SCREENING ASSAYS; HUMANS; INHIBITORY CONCENTRATION 50; ISOENZYMES; M PHASE CELL CYCLE CHECKPOINTS; MODELS, MOLECULAR; PACLITAXEL; PHOSPHORIC ACID ESTERS; PIPERAZINES; PROTEIN KINASE INHIBITORS; PROTEIN-SERINE-THREONINE KINASES; PYRIMIDINES; QUINAZOLINES; STRUCTURE-ACTIVITY RELATIONSHIP; XENOPUS LAEVIS;

EID: 84862946285     PISSN: 15548929     EISSN: 15548937     Source Type: Journal    
DOI: 10.1021/cb200305u     Document Type: Article

References (49)

1. Huang, H. C., Shi, J., Orth, J. D., and Mitchison, T. J. (2009) Evidence that mitotic exit is a better cancer therapeutic target than spindle assembly Cancer Cell 16, 347-358
2. Rieder, C. L. and Maiato, H. (2004) Stuck in division or passing through: What happens when cells cannot satisfy the spindle assembly checkpoint Dev. Cell 7, 637-651 (Pubitemid 39462685)
3. Shi, J., Orth, J. D, and Mitchison, T. (2008) Cell type variation in responses to antimitotic drugs that target microtubules and kinesin-5 Cancer Res. 68, 3269-3276
4. George, J., Banik, N. L., and Ray, S. K. (2009) Combination of taxol and Bcl-2 siRNA induces apoptosis in human glioblastoma cells and inhibits invasion, angiogenesis and tumour growth J. Cell. Mol. Med. 13, 4205-4218
5. Tan, N., Malek, M., Zha, J., Yue, P., Kassees, R., Berry, L., Fairbrother, W. J., Sampath, D., and Belmont, L. D. (2011) Navitoclax enhances the efficacy of taxanes in non-small cell lung cancer models Clin. Cancer Res. 17, 1394-1404
6. Wertz, I. E., Kusam, S., Lam, C., Okamoto, T., Sandoval, W., Anderson, D. J., Helgason, E., Ernst, J. A., Eby, M., Liu, J., Belmont, L. D., Kaminker, J. S., O'Rourke, K. M., Pujara, K., Kohli, P. B., Johnson, A. R., Chiu, M. L., Lill, J. R., Jackson, P. K., Fairbrother, W. J., Seshagiri, S., Ludlam, M. J., Leong, K. G., Dueber, E. C., Maecker, H., Huang, D. C., and Dixit, V. M. (2011) Sensitivity to antitubulin chemotherapeutics is regulated by MCL1 and FBW7 Nature 471, 110-114
7. Bayliss, R., Sardon, T., Vernos, I., and Conti, E. (2003) Structural basis of Aurora-A activation by TPX2 at the mitotic spindle Mol. Cell 12, 851-862 (Pubitemid 37352779)
8. 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 (Pubitemid 34966697)
9. Bolton, M. A., Lan, W., Powers, S. E., McCleland, M. L., Kuang, J., and Stukenberg, P. T. (2002) Aurora B kinase exists in a complex with survivin and INCENP and its kinase activity is stimulated by survivin binding and phosphorylation Mol. Biol. Cell 13, 3064-3077 (Pubitemid 35034246)
10. Chen, J., Jin, S., Tahir, S. K., Zhang, H., Liu, X., Sarthy, A. V., McGonigal, T. P., Liu, Z., Rosenberg, S. H., and Ng, S. C. (2003) Survivin enhances Aurora-B kinase activity and localizes Aurora-B in human cells J. Biol. Chem. 278, 486-490 (Pubitemid 36043600)
11. Eyers, P. A., Erikson, E., Chen, L. G., and Maller, J. L. (2003) A novel mechanism for activation of the protein kinase Aurora A Curr. Biol. 13, 691-697 (Pubitemid 36453320)
12. 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 (Pubitemid 37013130)
13. Hutterer, A., Berdnik, D., Wirtz-Peitz, F., Zigman, M., Schleiffer, A., and Knoblich, J. A. (2006) Mitotic activation of the kinase Aurora-A requires its binding partner Bora Dev. Cell 11, 147-157 (Pubitemid 44138495)
14. Jelluma, N., Brenkman, A. B., van den Broek, N. J., Cruijsen, C. W., van Osch, M. H., Lens, S. M., Medema, R. H., and Kops, G. J. (2008) Mps1 phosphorylates Borealin to control Aurora B activity and chromosome alignment Cell 132, 233-246 (Pubitemid 351172430)
15. 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 (Pubitemid 47576137)
16. Kelly, A. E., Sampath, S. C., Maniar, T. A., Woo, E. M., Chait, B. T., and Funabiki, H. (2007) Chromosomal enrichment and activation of the aurora B pathway are coupled to spatially regulate spindle assembly Dev. Cell 12, 31-43 (Pubitemid 46002596)
17. Kufer, T. A., Sillje, H. H., Korner, R., Gruss, O. J., Meraldi, P., and Nigg, E. A. (2002) Human TPX2 is required for targeting Aurora-A kinase to the spindle J. Cell Biol. 158, 617-623 (Pubitemid 34920101)
18. 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 (Pubitemid 41350542)
19. 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
20. Glover, D. M., Leibowitz, M. H., McLean, D. A., and Parry, H. (1995) Mutations in aurora prevent centrosome separation leading to the formation of monopolar spindles Cell 81, 95-105
21. Hirota, T., Kunitoku, N., Sasayama, T., Marumoto, T., Zhang, D., Nitta, M., Hatakeyama, K., and Saya, H. (2003) Aurora-A and an interacting activator, the LIM protein Ajuba, are required for mitotic commitment in human cells Cell 114, 585-598 (Pubitemid 37159255)
22. 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 (Pubitemid 27224814)
23. Bird, A. W. and Hyman, A. A. (2008) Building a spindle of the correct length in human cells requires the interaction between TPX2 and Aurora A J. Cell Biol. 182, 289-300
24. Koffa, M. D., Casanova, C. M., Santarella, R., Kocher, T., Wilm, M., and Mattaj, I. W. (2006) HURP is part of a Ran-dependent complex involved in spindle formation Curr. Biol. 16, 743-754
25. Tsai, M. Y., Wiese, C., Cao, K., Martin, O., Donovan, P., Ruderman, J., Prigent, C., and Zheng, Y. (2003) A Ran signalling pathway mediated by the mitotic kinase Aurora A in spindle assembly Nat. Cell Biol. 5, 242-248 (Pubitemid 36322252)
26. Cheeseman, I. M., Anderson, S., Jwa, M., Green, E. M., Kang, J., Yates, J. R., 3rd, Chan, C. S., Drubin, D. G., and Barnes, G. (2002) Phospho-regulation of kinetochore-microtubule attachments by the Aurora kinase Ipl1p Cell 111, 163-172 (Pubitemid 35292437)
27. 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 (Pubitemid 38344361)
28. 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-orientationby altering kinetochore-spindle pole connections Cell 108, 317-329 (Pubitemid 34178397)
29. Santaguida, S., Tighe, A., D'Alise, A. M., Taylor, S. S., and Musacchio, A. (2010) Dissecting the role of MPS1 in chromosome biorientation and the spindle checkpoint through the small molecule inhibitor reversine J. Cell Biol. 190, 73-87
30. 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
31. 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
32. Giet, R., McLean, D., Descamps, S., Lee, M. J., Raff, J. W., Prigent, C., and Glover, D. M. (2002) Drosophila Aurora A kinase is required to localize D-TACC to centrosomes and to regulate astral microtubules J. Cell Biol. 156, 437-451 (Pubitemid 34839893)
33. 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 (Pubitemid 28062046)
34. Aliagas-Martin, I., Burdick, D., Corson, L., Dotson, J., Drummond, J., Fields, C., Huang, O. W., Hunsaker, T., Kleinheinz, T., Krueger, E., Liang, J., Moffat, J., Phillips, G., Pulk, R., Rawson, T. E., Ultsch, M., Walker, L., Wiesmann, C., Zhang, B., Zhu, B. Y., and Cochran, A. G. (2009) A class of 2,4-bisanilinopyrimidine Aurora A inhibitors with unusually high selectivity against Aurora B J. Med. Chem. 52, 3300-3307
35. Harrington, E. A., Bebbington, D., Moore, J., Rasmussen, R. K., Ajose-Adeogun, A. O., Nakayama, T., Graham, J. A., Demur, C., Hercend, T., Diu-Hercend, A., Su, M., Golec, J. M., and Miller, K. M. (2004) VX-680, a potent and selective small-molecule inhibitor of the Aurora kinases, suppresses tumor growth in vivo Nat. Med. 10, 262-267 (Pubitemid 38667616)
36. Manfredi, M. G., Ecsedy, J. A., Meetze, K. A., Balani, S. K., Burenkova, O., Chen, W., Galvin, K. M., Hoar, K. M., Huck, J. J., LeRoy, P. J., Ray, E. T., Sells, T. B., Stringer, B., Stroud, S. G., Vos, T. J., Weatherhead, G. S., Wysong, D. R., Zhang, M., Bolen, J. B., and Claiborne, C. F. (2007) Antitumor activity of MLN8054, an orally active small-molecule inhibitor of Aurora A kinase Proc. Natl. Acad. Sci. U.S.A. 104, 4106-4111 (Pubitemid 47181586)
37. Mortlock, A. A., Foote, K. M., Heron, N. M., Jung, F. H., Pasquet, G., Lohmann, J. J., Warin, N., Renaud, F., De Savi, C., Roberts, N. J., Johnson, T., Dousson, C. B., Hill, G. B., Perkins, D., Hatter, G., Wilkinson, R. W., Wedge, S. R., Heaton, S. P., Odedra, R., Keen, N. J., Crafter, C., Brown, E., Thompson, K., Brightwell, S., Khatri, L., Brady, M. C., Kearney, S., McKillop, D., Rhead, S., Parry, T., and Green, S. (2007) Discovery, synthesis, and in vivo activity of a new class of pyrazoloquinazolines as selective inhibitors of aurora B kinase J. Med. Chem. 50, 2213-2224 (Pubitemid 46683074)
38. Girdler, F., Sessa, F., Patercoli, S., Villa, F., Musacchio, A., and Taylor, S. (2008) Molecular basis of drug resistance in aurora kinases Chem. Biol. 15, 552-562 (Pubitemid 351815053)
39. Deng, X., Dzamko, N., Prescott, A., Davies, P., Liu, Q., Yang, Q., Lee, J. D., Patricelli, M. P., Nomanbhoy, T. K., Alessi, D. R., and Gray, N. S. (2011) Characterization of a selective inhibitor of the Parkinson's disease kinase LRRK2 Nat. Chem. Biol. 7, 203-205
40. Deng, X., Yang, Q., Kwiatkowski, N., Sim, T., McDermott, U., Settleman, J. E., Lee, J. D., and Gray, N. S. (2011) Discovery of a benzo[ e ]pyrimido-[5,4- b ][1,4]diazepin-6(11 H)-one as a potent and selective inhibitor of big MAP Kinase 1 ACS Med. Chem. Lett. 2, 195-200
41. Kwiatkowski, N., Jelluma, N., Filippakopoulos, P., Soundararajan, M., Manak, M. S., Kwon, M., Choi, H. G., Sim, T., Deveraux, Q. L., Rottmann, S., Pellman, D., Shah, J. V., Kops, G. J., Knapp, S., and Gray, N. S. (2010) Small-molecule kinase inhibitors provide insight into Mps1 cell cycle function Nat.Chem. Biol. 6, 359-368
42. Lenart, P., Petronczki, M., Steegmaier, M., Di Fiore, B., Lipp, J. J., Hoffmann, M., Rettig, W. J., Kraut, N., and Peters, J. M. (2007) The small-molecule inhibitor BI 2536 reveals novel insights into mitotic roles of polo-like kinase 1 Curr. Biol. 17, 304-315
43. Fabian, M. A., Biggs, W. H., 3rd, Treiber, D. K., Atteridge, C. E., Azimioara, M. D., Benedetti, M. G., Carter, T. A., Ciceri, P., Edeen, P. T., Floyd, M., Ford, J. M., Galvin, M., Gerlach, J. L., Grotzfeld, R. M., Herrgard, S., Insko, D. E., Insko, M. A., Lai, A. G., Lelias, J. M., Mehta, S. A., Milanov, Z. V., Velasco, A. M., Wodicka, L. M., Patel, H. K., Zarrinkar, P. P., and Lockhart, D. J. (2005) A small molecule-kinase interaction map for clinical kinase inhibitors Nat. Biotechnol. 23, 329-336 (Pubitemid 41094421)
44. Patricelli, M. P., Szardenings, A. K., Liyanage, M., Nomanbhoy, T. K., Wu, M., Weissig, H., Aban, A., Chun, D., Tanner, S., and Kozarich, J. W. (2007) Functional interrogation of the kinome using nucleotide acyl phosphates Biochemistry 46, 350-358 (Pubitemid 46105428)
45. Yasui, Y., Urano, T., Kawajiri, A., Nagata, K., Tatsuka, M., Saya, H., Furukawa, K., Takahashi, T., Izawa, I., and Inagaki, M. (2004) Autophosphorylation of a newly identified site of Aurora-B is indispensable for cytokinesis J. Biol. Chem. 279, 12997-13003 (Pubitemid 38445876)
46. Abe, Y., Ohsugi, M., Haraguchi, K., Fujimoto, J., and Yamamoto, T. (2006) LATS2-Ajuba complex regulates gamma-tubulin recruitment to centrosomes and spindle organization during mitosis FEBS Lett. 580, 782-788 (Pubitemid 43152297)
47. Hannak, E., Kirkham, M., Hyman, A. A., and Oegema, K. (2001) Aurora-A kinase is required for centrosome maturation in Caenorhabditis elegans J. Cell Biol. 155, 1109-1116
48. Mori, D., Yano, Y., Toyo-oka, K., Yoshida, N., Yamada, M., Muramatsu, M., Zhang, D., Saya, H., Toyoshima, Y. Y., Kinoshita, K., Wynshaw-Boris, A., and Hirotsune, S. (2007) NDEL1 phosphorylation by Aurora-A kinase is essential for centrosomal maturation, separation, and TACC3 recruitment Mol. Cell. Biol. 27, 352-367 (Pubitemid 46013256)
49. Toji, S., Yabuta, N., Hosomi, T., Nishihara, S., Kobayashi, T., Suzuki, S., Tamai, K., and Nojima, H. (2004) The centrosomal protein Lats2 is a phosphorylation target of Aurora-A kinase Genes Cells 9, 383-397 (Pubitemid 38771930)