The Small-Molecule Inhibitor BI 2536 Reveals Novel Insights into Mitotic Roles of Polo-like Kinase 1

Current Biology

Volumn 17, Issue 4, 2007, Pages 304-315

  Lénárt, Péter ^a   Petronczki, Mark ^a   Steegmaier, Martin ^b   Di Fiore, Barbara ^c   Lipp, Jesse J ^a   Hoffmann, Matthias ^d   Rettig, Wolfgang J ^b   Kraut, Norbert ^b   Peters, Jan Michael ^a  

^a RESEARCH INSTITUTE OF MOLECULAR PATHOLOGY   (Austria)

^b BOEHRINGER INGELHEIM RCV GMBH AND CO KG   (Austria)

^c WELLCOME TRUST SANGER INSTITUTE   (United Kingdom)

^d BOEHRINGER INGELHEIM PHARMA GMBH AND CO KG   (Germany)

Author keywords

CELLBIO

Indexed keywords

BI 2536; CELL CYCLE PROTEIN; ENZYME INHIBITOR; F BOX PROTEIN; FBXO5 PROTEIN, HUMAN; ONCOPROTEIN; POLO LIKE KINASE 1; POLO-LIKE KINASE 1; PROTEIN SERINE THREONINE KINASE; PTERIDINE DERIVATIVE; UNCLASSIFIED DRUG;

ARTICLE; COMPARATIVE STUDY; DOSE RESPONSE; DRUG ANTAGONISM; DRUG EFFECT; FLUORESCENCE MICROSCOPY; HELA CELL; HUMAN; IMAGE PROCESSING; METABOLISM; MICROTUBULE; MITOSIS; MITOSIS SPINDLE; PHYSIOLOGY; TRANSMISSION ELECTRON MICROSCOPY;

CELL CYCLE PROTEINS; DOSE-RESPONSE RELATIONSHIP, DRUG; ENZYME INHIBITORS; F-BOX PROTEINS; HELA CELLS; HUMANS; IMAGE PROCESSING, COMPUTER-ASSISTED; MICROSCOPY, ELECTRON, TRANSMISSION; MICROSCOPY, FLUORESCENCE; MICROTUBULES; MITOSIS; MITOTIC SPINDLE APPARATUS; PROTEIN-SERINE-THREONINE KINASES; PROTO-ONCOGENE PROTEINS; PTERIDINES;

EID: 33846931644     PISSN: 09609822     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.cub.2006.12.046     Document Type: Article

References (47)

1. Barr F.A., Sillje H.H., and Nigg E.A. Polo-like kinases and the orchestration of cell division. Nat. Rev. Mol. Cell Biol. 5 (2004) 429-440
2. Watanabe N., Arai H., Nishihara Y., Taniguchi M., Hunter T., and Osada H. M-phase kinases induce phospho-dependent ubiquitination of somatic Wee1 by SCFbeta-TrCP. Proc. Natl. Acad. Sci. USA 101 (2004) 4419-4424
3. Toyoshima-Morimoto F., Taniguchi E., Shinya N., Iwamatsu A., and Nishida E. Polo-like kinase 1 phosphorylates cyclin B1 and targets it to the nucleus during prophase. Nature 410 (2001) 215-220
4. Toyoshima-Morimoto F., Taniguchi E., and Nishida E. Plk1 promotes nuclear translocation of human Cdc25C during prophase. EMBO Rep. 3 (2002) 341-348
5. Jackman M., Lindon C., Nigg E.A., and Pines J. Active cyclin B1-Cdk1 first appears on centrosomes in prophase. Nat. Cell Biol. 5 (2003) 143-148
6. Lane H.A., and Nigg E.A. Antibody microinjection reveals an essential role for human polo-like kinase 1 (Plk1) in the functional maturation of mitotic centrosomes. J. Cell Biol. 135 (1996) 1701-1713
7. Losada A., Hirano M., and Hirano T. Cohesin release is required for sister chromatid resolution, but not for condensin-mediated compaction, at the onset of mitosis. Genes Dev. 16 (2002) 3004-3016
8. Sumara I., Vorlaufer E., Stukenberg P.T., Kelm O., Redemann N., Nigg E.A., and Peters J.M. The dissociation of cohesin from chromosomes in prophase is regulated by Polo-like kinase. Mol. Cell 9 (2002) 515-525
9. Gimenez-Abian J.F., Sumara I., Hirota T., Hauf S., Gerlich D., de la Torre C., Ellenberg J., and Peters J.M. Regulation of sister chromatid cohesion between chromosome arms. Curr. Biol. 14 (2004) 1187-1193
10. Golan A., Yudkovsky Y., and Hershko A. The cyclin-ubiquitin ligase activity of cyclosome/APC is jointly activated by protein kinases Cdk1-cyclin B and Plk. J. Biol. Chem. 277 (2002) 15552-15557
11. Kraft C., Herzog F., Gieffers C., Mechtler K., Hagting A., Pines J., and Peters J.M. Mitotic regulation of the human anaphase-promoting complex by phosphorylation. EMBO J. 22 (2003) 6598-6609
12. Hansen D.V., Loktev A.V., Ban K.H., and Jackson P.K. Plk1 regulates activation of the anaphase promoting complex by phosphorylating and triggering SCFbetaTrCP-dependent destruction of the APC Inhibitor Emi1. Mol. Biol. Cell 15 (2004) 5623-5634
13. Moshe Y., Boulaire J., Pagano M., and Hershko A. Role of Polo-like kinase in the degradation of early mitotic inhibitor 1, a regulator of the anaphase promoting complex/cyclosome. Proc. Natl. Acad. Sci. USA 101 (2004) 7937-7942
14. van Vugt M.A., van de Weerdt B.C., Vader G., Janssen H., Calafat J., Klompmaker R., Wolthuis R.M., and Medema R.H. Polo-like kinase-1 is required for bipolar spindle formation but is dispensable for anaphase promoting complex/Cdc20 activation and initiation of cytokinesis. J. Biol. Chem. 279 (2004) 36841-36854
15. Sumara I., Gimenez-Abian J.F., Gerlich D., Hirota T., Kraft C., de la Torre C., Ellenberg J., and Peters J.M. Roles of polo-like kinase 1 in the assembly of functional mitotic spindles. Curr. Biol. 14 (2004) 1712-1722
16. Ahonen L.J., Kallio M.J., Daum J.R., Bolton M., Manke I.A., Yaffe M.B., Stukenberg P.T., and Gorbsky G.J. Polo-like kinase 1 creates the tension-sensing 3F3/2 phosphoepitope and modulates the association of spindle-checkpoint proteins at kinetochores. Curr. Biol. 15 (2005) 1078-1089
17. Wong O.K., and Fang G. Plx1 is the 3F3/2 kinase responsible for targeting spindle checkpoint proteins to kinetochores. J. Cell Biol. 170 (2005) 709-719
18. Kang Y.H., Park J.E., Yu L.R., Soung N.K., Yun S.M., Bang J.K., Seong Y.S., Yu H., Garfield S., Veenstra T.D., et al. Self-regulated Plk1 recruitment to kinetochores by the Plk1-PBIP1 interaction is critical for proper chromosome segregation. Mol. Cell 24 (2006) 409-422
19. Elia A.E., Rellos P., Haire L.F., Chao J.W., Ivins F.J., Hoepker K., Mohammad D., Cantley L.C., Smerdon S.J., and Yaffe M.B. The molecular basis for phosphodependent substrate targeting and regulation of Plks by the Polo-box domain. Cell 115 (2003) 83-95
20. Elia A.E., Cantley L.C., and Yaffe M.B. Proteomic screen finds pSer/pThr-binding domain localizing Plk1 to mitotic substrates. Science 299 (2003) 1228-1231
21. Neef R., Preisinger C., Sutcliffe J., Kopajtich R., Nigg E.A., Mayer T.U., and Barr F.A. Phosphorylation of mitotic kinesin-like protein 2 by polo-like kinase 1 is required for cytokinesis. J. Cell Biol. 162 (2003) 863-875
22. van de Weerdt B.C., and Medema R.H. Polo-like kinases: A team in control of the division. Cell Cycle 5 (2006) 853-864
23. Ditchfield C., Johnson V.L., Tighe A., Ellston R., Haworth C., Johnson T., Mortlock A., Keen N., and Taylor S.S. Aurora B couples chromosome alignment with anaphase by targeting BubR1, Mad2, and Cenp-E to kinetochores. J. Cell Biol. 161 (2003) 267-280
24. 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. 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 (2003) 281-294
25. 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., et al. VX-680, a potent and selective small-molecule inhibitor of the Aurora kinases, suppresses tumor growth in vivo. Nat. Med. 10 (2004) 262-267
26. Girdler F., Gascoigne K.E., Eyers P.A., Hartmuth S., Crafter C., Foote K.M., Keen N.J., and Taylor S.S. Validating Aurora B as an anti-cancer drug target. J. Cell Sci. 119 (2006) 3664-3675
27. Collins I., and Garrett M.D. Targeting the cell division cycle in cancer: CDK and cell cycle checkpoint kinase inhibitors. Curr. Opin. Pharmacol. 5 (2005) 366-373
28. Gumireddy K., Reddy M.V., Cosenza S.C., Boominathan R., Baker S.J., Papathi N., Jiang J., Holland J., and Reddy E.P. ON01910, a non-ATP-competitive small molecule inhibitor of Plk1, is a potent anticancer agent. Cancer Cell 7 (2005) 275-286
29. Steegmaier M., Hoffmann M., Baum A., Lénárt P., Petronczki M., Krššák M., Gürtler U., Garin-Chesa P., Lieb S., Quant J., et al. BI 2536, a potent and selective inhibitor of Polo-like kinase 1, inhibits tumor growth in vivo. Curr. Biol. 17 (2007) 316-322 this issue
30. McInnes C., Mazumdar A., Mezna M., Meades C., Midgley C., Scaerou F., Carpenter L., Mackenzie M., Taylor P., Walkinshaw M., et al. Inhibitors of Polo-like kinase reveal roles in spindle-pole maintenance. Nat. Chem. Biol. 2 (2006) 608-617
31. Peters U., Cherian J., Kim J.H., Kwok B.H., and Kapoor T.M. Probing cell-division phenotype space and Polo-like kinase function using small molecules. Nat. Chem. Biol. 2 (2006) 618-626
32. Palazzo R.E., Vogel J.M., Schnackenberg B.J., Hull D.R., and Wu X. Centrosome maturation. Curr. Top. Dev. Biol. 49 (2000) 449-470
33. Qian Y.W., Erikson E., Taieb F.E., and Maller J.L. The polo-like kinase Plx1 is required for activation of the phosphatase Cdc25C and cyclin B-Cdc2 in Xenopus oocytes. Mol. Biol. Cell 12 (2001) 1791-1799
34. Mayer T.U., Kapoor T.M., Haggarty S.J., King R.W., Schreiber S.L., and Mitchison T.J. Small molecule inhibitor of mitotic spindle bipolarity identified in a phenotype-based screen. Science 286 (1999) 971-974
35. Clute P., and Pines J. Temporal and spatial control of cyclin B1 destruction in metaphase. Nat. Cell Biol. 1 (1999) 82-87
36. den Elzen N., and Pines J. Cyclin A is destroyed in prometaphase and can delay chromosome alignment and anaphase. J. Cell Biol. 153 (2001) 121-136
37. Grosskortenhaus R., and Sprenger F. Rca1 inhibits APC-Cdh1(Fzr) and is required to prevent cyclin degradation in G2. Dev. Cell 2 (2002) 29-40
38. Hoffman D.B., Pearson C.G., Yen T.J., Howell B.J., and Salmon E.D. Microtubule-dependent changes in assembly of microtubule motor proteins and mitotic spindle checkpoint proteins at PtK1 kinetochores. Mol. Biol. Cell 12 (2001) 1995-2009
39. Waters J.C., Chen R.H., Murray A.W., and Salmon E.D. Localization of Mad2 to kinetochores depends on microtubule attachment, not tension. J. Cell Biol. 141 (1998) 1181-1191
40. Taylor S.S., Hussein D., Wang Y., Elderkin S., and Morrow C.J. Kinetochore localisation and phosphorylation of the mitotic checkpoint components Bub1 and BubR1 are differentially regulated by spindle events in human cells. J. Cell Sci. 114 (2001) 4385-4395
41. Hanisch A., Wehner A., Nigg E.A., and Sillje H.H. Different Plk1 functions show distinct dependencies on Polo-Box domain-mediated targeting. Mol. Biol. Cell 17 (2006) 448-459
42. Qi W., Tang Z., and Yu H. Phosphorylation- and Polo-box-dependent binding of Plk1 to Bub1 is required for the kinetochore localization of Plk1. Mol. Biol. Cell 17 (2006) 3705-3716
43. Nishino M., Kurasawa Y., Evans R., Lin S.H., Brinkley B.R., and Yu-Lee L.Y. NudC is required for Plk1 targeting to the kinetochore and chromosome congression. Curr. Biol. 16 (2006) 1414-1421
44. Sunkel C.E., and Glover D.M. polo, a mitotic mutant of Drosophila displaying abnormal spindle poles. J. Cell Sci. 89 (1988) 25-38
45. Goshima G., Nedelec F., and Vale R.D. Mechanisms for focusing mitotic spindle poles by minus end-directed motor proteins. J. Cell Biol. 171 (2005) 229-240
46. DeLuca J.G., Moree B., Hickey J.M., Kilmartin J.V., and Salmon E.D. hNuf2 inhibition blocks stable kinetochore-microtubule attachment and induces mitotic cell death in HeLa cells. J. Cell Biol. 159 (2002) 549-555
47. Lampson M.A., and Kapoor T.M. The human mitotic checkpoint protein BubR1 regulates chromosome-spindle attachments. Nat. Cell Biol. 7 (2005) 93-98