Inhibitors of Polo-like kinase reveal roles in spindle-pole maintenance

Nature Chemical Biology

Volumn 2, Issue 11, 2006, Pages 608-617

  McInnes, Campbell ^a,d   Mazumdar, Aveek ^b   Mezna, Mokdad ^a,e   Meades, Christopher ^a   Midgley, Carol ^a   Scaerou, Fred ^a   Carpenter, Lee ^b   Mackenzie, Mairi ^a   Taylor, Paul ^c   Walkinshaw, Malcolm ^c   Fischer, Peter M ^a,f   Glover, David ^a,b  

^a CYCLACEL LTD   (United Kingdom)

^b UNIVERSITY OF CAMBRIDGE   (United Kingdom)

^c UNIVERSITY OF EDINBURGH   (United Kingdom)

^d UNIVERSITY OF SOUTH CAROLINA   (United States)

^e BEATSON INSTITUTE FOR CANCER RESEARCH   (United Kingdom)

^f UNIVERSITY OF NOTTINGHAM   (United Kingdom)

Author keywords

[No Author keywords available]

Indexed keywords

CYCLAPOLIN; GAMMA TUBULIN; PHOSPHOTRANSFERASE INHIBITOR; POLO LIKE KINASE; THIAZOLE DERIVATIVE; UNCLASSIFIED DRUG;

ARTICLE; CENTROSOME; CONTROLLED STUDY; DRUG EFFECT; DRUG POTENCY; DRUG SELECTIVITY; ENZYME INHIBITION; FEMALE; HUMAN; HUMAN CELL; METAPHASE; MICROTUBULE; MITOSIS SPINDLE; NONHUMAN; NUCLEOTIDE SEQUENCE; PRIORITY JOURNAL; RNA INTERFERENCE;

EID: 33750227695     PISSN: 15524450     EISSN: 15524469     Source Type: Journal    
DOI: 10.1038/nchembio825     Document Type: Article

References (49)

1. Sunkel, C.E. & Glover, D.M. Polo, a mitotic mutant of Drosophila displaying abnormal spindle poles. J. Cell Sci. 89, 25-38 (1988).
2. Llamazares, S. et al. Polo encodes a protein kinase homolog required for mitosis in Drosophila. Genes Dev. 5, 2153-2165 (1991).
3. McInnes, C., Mezna, M. & Fischer, P.M. Progress in the discovery of polo-like kinase inhibitors. Curr. Top. Med. Chem. 5, 181-197 (2005).
4. Glover, D.M., Hagan, I.M. & Tavares, A.A. Polo-like kinases: a team that plays throughout mitosis. Genes Dev. 12, 3777-3787 (1998).
5. Elia, A.E., Cantley, L.C. & Yaffe, M.B. Proteomic screen finds pSer/pThr-binding domain localizing Plk1 to mitotic substrates. Science 299, 1228-1231 (2003).
6. Leung, G.C. et al. The Sak polo-box comprises a structural domain sufficient for mitotic subcellular localization. Nat. Struct. Biol. 9, 719-724 (2002).
7. Elia, A.E. et al. The molecular basis for phosphodependent substrate targeting and regulation of Plks by the Polo-box domain. Cell 115, 83-95 (2003).
8. Jang, Y.J. et al. Polo-box motif targets a centrosome regulator, RanGTPase. Biochem. Biophys. Res. Commun. 325, 257-264 (2004).
9. Kumagai, A. & Dunphy, W.G. Purification and molecular cloning of Plx1, a Cdc25-regulatory kinase from Xenopus egg extracts. Science 273, 1377-1380 (1996).
10. Watanabe, N. et al. Cyclin-dependent kinase (CDK) phosphorylation destabilizes somatic Wee1 via multiple pathways. Proc. Natl. Acad. Sci. USA 102, 11663-11668 (2005).
11. van Vugt, M.A. & Medema, R.H. Getting in and out of mitosis with Polo-like kinase-1. Oncogene 24, 2844-2859 (2005).
12. Glover, D.M. Polo kinase and progression through M phase in Drosophila: a perspective from the spindle poles. Oncogene 24, 230-237 (2005).
13. Hansen, D.V., Loktev, A.V., Ban, K.H. & 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, 5623-5634 (2004).
14. Moshe, Y., Boulaire, J., Pagano, M. & 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, 7937-7942 (2004).
15. Rauh, N.R., Schmidt, A., Bormann, J., Nigg, E.A. & Mayer, T.U. Calcium triggers exit from meiosis II by targeting the APC/C inhibitor XErp1 for degradation. Nature 437, 1048-1052 (2005).
16. Liu, J. & Maller, J.L. Calcium elevation at fertilization coordinates phosphorylation of XErp1/Emi2 by Plx1 and CaMK II to release metaphase arrest by cytostatic factor. Curr. Biol. 15, 1458-1468 (2005).
17. Tung, J.J. et al. A role for the anaphase-promoting complex inhibitor Emi2/XErp1, a homolog of early mitotic inhibitor1, incytostatic factor arrest of Xenopus eggs. Proc. Natl. Acad. Sci. USA 102, 4318-4323 (2005).
18. Hauf, S. et al. Dissociation of cohesin from chromosome arms and loss of arm cohesion during early mitosis depends on phosphorylation of SA2. PLoS Biol. 3, e69 (2005).
19. Clarke, A.S., Tang, T.T., Ooi, D.L. & Orr-Weaver, T.L. POLO kinase regulates the Drosophila centromere cohesion protein MEI-S332. Dev. Cell 8, 53-64 (2005).
20. Hornig, N.C. & Uhlmann, F. Preferential cleavage of chromatin-bound cohesin after targeted phosphorylation by Polo-like kinase. EMBO J. 23, 3144-3153 (2004).
21. Wong, O.K. & Fang, G. Plx1 is the 3F3/2 kinase responsible for targeting spindle checkpoint proteins to kinetochores. J. Cell Biol. 170, 709-719 (2005).
22. Ahonen, L.J. et al. Polo-like kinase 1 creates the tension-sensing 3F3/2 phosphoepitope and modulates the association of spindle-checkpoint proteins at kinetochores. Curr. Biol. 15, 1078-1089 (2005).
23. Carmena, M. et al. Drosophila polo kinase is required for cytokinesis. J. Cell Biol. 143, 659-671 (1998).
24. Lee, K.S., Yuan, Y.L., Kuriyama, R. & Erikson, R.L. Plk is an M-phase-specific protein kinase and interacts with a kinesin-like protein, CHO1/MKLP-1. Mol. Cell. Biol. 15, 7143-7151 (1995).
25. Neef, R. et al. Phosphorylation of mitotic kinesin-like protein 2 by polo-like kinase 1 is required for cytokinesis. J. Cell Biol. 162, 863-875 (2003).
26. Liu, X., Zhou, T., Kuriyama, R. & Erikson, R.L. Molecular interactions of Polo-like-kinase 1 with the mitotic kinesin-like protein CHO1/MKLP-1. J. Cell Sci. 117, 3233-3246 (2004).
27. Lindon, C. & Pines, J. Ordered proteolysis in anaphase inactivates Plk1 to contribute to proper mitotic exit in human cells. J. Cell Biol. 164, 233-241 (2004).
28. Spankuch-Schmitt, B., Bereiter-Hahn, J., Kaufmann, M. & Strebhardt, K. Effect of RNA silencing of polo-like kinase-1 (PLK1) on apoptosis and spindle formation in human cancer cells. J. Natl. Cancer Inst. 94, 1863-1877 (2002).
29. Elez, R. et al. Tumor regression by combination antisense therapy against Plk1 and Bcl-2. Oncogene 22, 69-80 (2003).
30. Wu, S.Y. et al. Discovery of a novel family of CDK inhibitors with the program LIDAEUS: structural basis for ligand-induced disordering of the activation loop. Structure 11, 399-410 (2003).
31. Lane, H.A. & 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, 1701-1713 (1996).
32. Sumara, I. et al. Roles of polo-like kinase 1 in the assembly of functional mitotic spindles. Curr. Biol. 14, 1712-1722 (2004).
33. Bettencourt-Dias, M. et al. Genome-wide survey of protein kinases required for cell cycle progression. Nature 432, 980-987 (2004).
34. Donaldson, M.M., Tavares, A., Ohkura, H., Deak, P. & Glover, D.M. Metaphase arrest with centromere separation in polo mutants of Drosophila. J. Cell Biol. 153, 663-675 (2001).
35. do Carmo Avides, M., Tavares, A. & Glover, D.M. Polo kinase and Asp are needed to promote the mitotic organizing activity of centrosomes. Nat. Cell Biol. 3, 421-424 (2001).
36. Goshima, G. & Vale, R.D. The roles of microtubule-based motor proteins in mitosis: comprehensive RNAi analysis in the Drosophila S2 cell line. J. Cell Biol. 162, 1003-1016 (2003).
37. Laycock, J.E., Savoian, M.S. & Glover, D.M. Antagonistic activities of Klp10A and Orbit regulate spindle length, bipolarity and function in vivo. J. Cell Sci. 119, 2354-2361 (2006).
38. Sampaio, P., Rebollo, E., Varmark, H., Sunkel, C.E. & Gonzalez, C. Organized microtubule arrays in gamma-tubulin-depleted Drosophila spermatocytes. Curr. Biol. 11, 1788-1793 (2001).
39. Barbosa, V., Gatt, M., Rebollo, E., Gonzalez, C. & Glover, D.M. Drosophila dd4 mutants reveal that gammaTuRC is required to maintain juxtaposed half spindles in spermatocytes. J. Cell Sci. 116, 929-941 (2003).
40. Tavares, A.A., Glover, D.M. & Sunkel, C.E. The conserved mitotic kinase polo is regulated by phosphorylation and has preferred microtubule-associated substrates in Drosophila embryo extracts. EMBO J. 15, 4873-4883 (1996).
41. Liu, X., Zhou, T., Kuriyama, R. & Erikson, R.L. Molecular interactions of Polo-like-kinase 1 with the mitotic kinesin-like protein CHO1/MKLP-1. J. Cell Sci. 117, 3233-3246 (2004).
42. Blagden, S.P. & Glover, D.M. Polar expeditions-provisioning the centrosome for mitosis. Nat. Cell Biol. 5, 505-511 (2003).
43. Moritz, M., Zheng, Y., Alberts, B.M. & Oegema, K. Recruitment of the gamma-tubulin ring complex to Drosophila salt-stripped centrosome scaffolds. J. Cell Biol. 142, 775-786 (1998).
44. do Carmo Avides, M. & Glover, D.M. Abnormal spindle protein, Asp, and the integrity of mitotic centrosomal microtubule organizing centers. Science 283, 1733-1735 (1999).
45. de Carcer, G., do Carmo Avides, M., Lallena, M.J., Glover, D.M. & Gonzalez, C. Requirement of Hsp90 for centrosomal function reflects its regulation of Polo kinase stability. EMBO J. 20, 2878-2884 (2001).
46. Logarinho, E. & Sunkel, C.E. The Drosophila POLO kinase localises to multiple compartments of the mitotic apparatus and is required for the phosphorylation of MPM2 reactive epitopes. J. Cell Sci. 111, 2897-2909 (1998).
47. Morales-Mulia, S. & Scholey, J.M. Spindle pole organization in Drosophila S2 cells by dynein, abnormal spindle protein (Asp), and KLP10A. Mol. Biol. Cell 16, 3176-3186 (2005).
48. Moritz, M. & Alberts, B.M. Isolation of centrosomes from Drosophila embryos. Methods Cell Biol. 61, 1-12 (1999).
49. Bettencourt-Dias, M. et al. SAK/PLK4 is required for centriole duplication and flagella development. Curr. Biol. 15, 2199-2207 (2005).