Polo-box domain inhibitor poloxin activates the spindle assembly checkpoint and inhibits tumor growth in vivo

American Journal of Pathology

Volumn 179, Issue 4, 2011, Pages 2091-2099

  Yuan, Juping ^a   Sanhaji, Mourad ^a   Krmer, Andrea ^a   Reindl, Wolfgang ^a   Hofmann, Matthias ^b   Kreis, Nina Naomi ^a   Zimmer, Brigitte ^a   Berg, Thorsten ^a,c   Strebhardt, Klaus ^a  

^a GOETHE UNIVERSITY   (Germany)

^b MAX PLANCK INSTITUTE OF BIOCHEMISTRY   (Germany)

^c UNIVERSITY OF LEIPZIG   (Germany)

Author keywords

[No Author keywords available]

Indexed keywords

ANTINEOPLASTIC AGENT; POLO LIKE KINASE 1; POLOXIN; QUINONE DERIVATIVE; THYMOQUINONE; UNCLASSIFIED DRUG;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; APOPTOSIS; ARTICLE; CANCER CELL; CANCER TISSUE; CELL CYCLE PHASE; CELL PROLIFERATION; CENTROSOME; CHROMOSOME SIZE; CONTROLLED STUDY; FLUORESCENCE POLARIZATION IMMUNOASSAY; HUMAN; HUMAN CELL; IN VITRO STUDY; IN VIVO STUDY; MITOSIS; MOUSE; NONHUMAN; PHENOTYPE; POLO BOX DOMAIN; PRIORITY JOURNAL; PROTEIN DOMAIN; PROTEIN FUNCTION; SPINDLE CELL; SUBSTRATE INDUCED RESPIRATION; TUMOR GROWTH; XENOGRAFT;

ANIMALS; APOPTOSIS; BENZOATES; BENZOQUINONES; CELL CYCLE PROTEINS; CELL LINE, TUMOR; CELL PROLIFERATION; CENTROSOME; CHROMOSOMES, HUMAN; HUMANS; M PHASE CELL CYCLE CHECKPOINTS; MICE; NEOPLASMS; PROTEIN STRUCTURE, TERTIARY; PROTEIN-SERINE-THREONINE KINASES; PROTO-ONCOGENE PROTEINS; QUINONES; XENOGRAFT MODEL ANTITUMOR ASSAYS;

EID: 80053229630     PISSN: 00029440     EISSN: 15252191     Source Type: Journal    
DOI: 10.1016/j.ajpath.2011.06.031     Document Type: Article

References (50)

1. F.A. Barr, H.H. Sillje, and E.A. Nigg Polo-like kinases and the orchestration of cell division Nat Rev Mol Cell Biol 5 2004 429 440 (Pubitemid 38745493)
2. V. Archambault, and D.M. Glover Polo-like kinases: conservation and divergence in their functions and regulation Nat Rev Mol Cell Biol 10 2009 265 275
3. Z. Andrysik, W.Z. Bernstein, L. Deng, D.L. Myer, Y.Q. Li, J.A. Tischfield, P.J. Stambrook, and E.M. Bahassi The novel mouse Polo-like kinase 5 responds to DNA damage and localizes in the nucleolus Nucleic Acids Res 38 2010 2931 2943
4. G. de Cárcer, B. Escobar, A.M. Higuero, L. Garcia, A. Ansón, G. Pérez, M. Mollejo, G. Manning, B. Meléndez, J. Abad-Rodríguez, and M. Malumbres Plk5, a polo box domain-only protein with specific roles in neuron differentiation and glioblastoma suppression Mol Cell Biol 31 2011 1225 1239
5. K. Strebhardt Multifaceted polo-like kinases: drug targets and antitargets for cancer therapy Nat Rev Drug Discov 9 2010 643 660
6. R.M. Golsteyn, K.E. Mundt, A.M. Fry, and E.A. Nigg Cell cycle regulation of the activity and subcellular localization of Plk1, a human protein kinase implicated in mitotic spindle function J Cell Biol 129 1995 1617 1628
7. K.S. Lee, Y.L. Yuan, R. Kuriyama, and R.L. Erikson Plk is an M-phase-specific protein kinase and interacts with a kinesin-like protein, CHO1/MKLP-1 Mol Cell Biol 15 1995 7143 7151
8. L. Arnaud, J. Pines, and E.A. Nigg GFP tagging reveals human Polo-like kinase 1 at the kinetochore/centromere region of mitotic chromosomes Chromosoma 107 1998 424 429 (Pubitemid 29057535)
9. A.E. Elia, P. Rellos, L.F. Haire, J.W. Chao, F.J. Ivins, K. Hoepker, D. Mohammad, L.C. Cantley, S.J. Smerdon, and M.B. Yaffe The molecular basis for phosphodependent substrate targeting and regulation of Plks by the Polo-box domain Cell 115 2003 83 95 (Pubitemid 37255320)
10. S.M. Yun, T. Moulaei, D. Lim, J.K. Bang, J.E. Park, S.R. Shenoy, F. Liu, Y.H. Kang, C. Liao, N.K. Soung, S. Lee, D.Y. Yoon, Y. Lim, D.H. Lee, A. Otaka, E. Appella, J.B. McMahon, M.C. Nicklaus, T.R. Burke Jr, M.B. Yaffe, A. Wlodawer, and K.S. Lee Structural and functional analyses of minimal phosphopeptides targeting the polo-box domain of polo-like kinase 1 Nat Struct Mol Biol 16 2009 876 882
11. K. Strebhardt, and A. Ullrich Targeting polo-like kinase 1 for cancer therapy Nat Rev Cancer 6 2006 321 330
12. M.R. Smith, M.L. Wilson, R. Hamanaka, D. Chase, H. Kung, D.L. Longo, and D.K. Ferris Malignant transformation of mammalian cells initiated by constitutive expression of the polo-like kinase Biochem Biophys Res Commun 234 1997 397 405 (Pubitemid 27243915)
13. B.C. van de Weerdt, and R.H. Medema Polo-like kinases: a team in control of the division Cell Cycle 5 2006 853 864 (Pubitemid 44145580)
14. S. Xie, H. Wu, Q. Wang, J.P. Cogswell, I. Husain, C. Conn, P. Stambrook, M. Jhanwar-Uniyal, and W. Dai Plk3 functionally links DNA damage to cell cycle arrest and apoptosis at least in part via the p53 pathway J Biol Chem 276 2001 43305 43312
15. P. Smith, N. Syed, and T. Crook Epigenetic inactivation implies a tumor suppressor function in hematologic malignancies for Polo-like kinase 2 but not Polo-like kinase 3 Cell Cycle 5 2006 1262 1264 (Pubitemid 43894276)
16. W. Reindl, J. Yuan, A. Kramer, K. Strebhardt, and T. Berg Inhibition of polo-like kinase 1 by blocking polo-box domain-dependent protein-protein interactions Chem Biol 15 2008 459 466 (Pubitemid 351645109)
17. N.N. Kreis, K. Sommer, M. Sanhaji, A. Krmer, Y. Matthess, M. Kaufmann, K. Strebhardt, and J. Yuan Long-term downregulation of Polo-like kinase 1 increases the cyclin-dependent kinase inhibitor p21(WAF1/CIP1) Cell Cycle 8 2009 460 472
18. J. Yuan, A. Kramer, Y. Matthess, R. Yan, B. Spankuch, R. Gatje, R. Knecht, M. Kaufmann, and K. Strebhardt Stable gene silencing of cyclin B1 in tumor cells increases susceptibility to taxol and leads to growth arrest in vivo Oncogene 25 2006 1753 1762
19. N.N. Kreis, M. Sanhaji, A. Krmer, K. Sommer, F. Rödel, K. Strebhardt, and J. Yuan Restoration of the tumor suppressor p53 by downregulating cyclin B1 in human papillomavirus 16/18-infected cancer cells Oncogene 29 2010 5591 5603
20. M. Sanhaji, C.T. Friel, N.N. Kreis, A. Kramer, C. Martin, J. Howard, K. Strebhardt, and J. Yuan Functional and spatial regulation of mitotic centromere-associated kinesin by cyclin-dependent kinase 1 Mol Cell Biol 30 2010 2594 2607
21. F.R. Yarm Plk phosphorylation regulates the microtubule-stabilizing protein TCTP Mol Cell Biol 22 2002 6209 6221 (Pubitemid 34857840)
22. Y. Feng, D.R. Hodge, G. Palmieri, D.L. Chase, D.L. Longo, and D.K. Ferris Association of polo-like kinase with alpha-, beta- and gamma-tubulins in a stable complex Biochem J 339 Pt 2 1999 435 442 (Pubitemid 29209976)
23. N. Oshimori, M. Ohsugi, and T. Yamamoto The Plk1 target Kizuna stabilizes mitotic centrosomes to ensure spindle bipolarity Nat Cell Biol 8 2006 1095 1101 (Pubitemid 44473604)
24. M.A. van Vugt, B.C. van de Weerdt, G. Vader, H. Janssen, J. Calafat, R. Klompmaker, R.M. Wolthuis, and R.H. Medema 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 (Pubitemid 39129033)
25. A. Santamaria, R. Neef, U. Eberspacher, K. Eis, M. Husemann, D. Mumberg, S. Prechtl, V. Schulze, G. Siemeister, L. Wortmann, F.A. Barr, and E.A. Nigg Use of the novel Plk1 inhibitor ZK-thiazolidinone to elucidate functions of Plk1 in early and late stages of mitosis Mol Biol Cell 18 2007 4024 4036 (Pubitemid 47519493)
26. P. Lenart, M. Petronczki, M. Steegmaier, F.B. Di, J.J. Lipp, M. Hoffmann, W.J. Rettig, N. Kraut, and J.M. Peters The small-molecule inhibitor BI 2536 reveals novel insights into mitotic roles of polo-like kinase 1 Curr Biol 17 2007 304 315
27. S. Elowe, S. Hummer, A. Uldschmid, X. Li, and E.A. Nigg Tension-sensitive Plk1 phosphorylation on BubR1 regulates the stability of kinetochore microtubule interactions Genes Dev 21 2007 2205 2219 (Pubitemid 47360842)
28. O.K. Wong, and G. Fang Plx1 is the 3F3/2 kinase responsible for targeting spindle checkpoint proteins to kinetochores J Cell Biol 170 2005 709 719 (Pubitemid 41242104)
29. L.J. Ahonen, M.J. Kallio, J.R. Daum, M. Bolton, I.A. Manke, M.B. Yaffe, P.T. Stukenberg, and G.J. Gorbsky 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 (Pubitemid 40841350)
30. X. Liu, and R.L. Erikson Polo-like kinase (Plk)1 depletion induces apoptosis in cancer cells Proc Natl Acad Sci U S A 100 2003 5789 5794 (Pubitemid 36576886)
31. X. Liu, M. Lei, and R.L. Erikson Normal cells, but not cancer cells, survive severe Plk1 depletion Mol Cell Biol 26 2006 2093 2108 (Pubitemid 43346913)
32. H. Yim, and R.L. Erikson Polo-like kinase 1 depletion induces DNA damage in early S prior to caspase activation Mol Cell Biol 29 2009 2609 2621
33. J. Yuan, A. Kramer, F. Eckerdt, M. Kaufmann, and K. Strebhardt Efficient internalization of the polo-box of polo-like kinase 1 fused to an Antennapedia peptide results in inhibition of cancer cell proliferation Cancer Res 62 2002 4186 4190 (Pubitemid 34827268)
34. H. Gali-Muhtasib, M. Ocker, D. Kuester, S. Krueger, Z. El-Hajj, A. Diestel, M. Evert, N. El-Najjar, B. Peters, A. Jurjus, A. Roessner, and R. Schneider-Stock Thymoquinone reduces mouse colon tumor cell invasion and inhibits tumor growth in murine colon cancer models J Cell Mol Med 12 2008 330 342
35. J.R. Jackson, D.R. Patrick, M.M. Dar, and P.S. Huang Targeted anti-mitotic therapies: can we improve on tubulin agents? Nat Rev Cancer 7 2007 107 117 (Pubitemid 46160987)
36. T.L. Schmit, M.C. Ledesma, and N. Ahmad Modulating polo-like kinase 1 as a means for cancer chemoprevention Pharm Res 27 2010 989 998
37. Y. Degenhardt, and T. Lampkin Targeting Polo-like kinase in cancer therapy Clin Cancer Res 16 2010 384 389
38. P. Schoffski Polo-like kinase (PLK) inhibitors in preclinical and early clinical development in oncology Oncologist 14 2009 559 570
39. N. Watanabe, T. Sekine, M. Takagi, J. Iwasaki, N. Imamoto, H. Kawasaki, and H. Osada Deficiency in chromosome congression by the inhibition of Plk1 polo box domain-dependent recognition J Biol Chem 284 2009 2344 2353
40. H.A. Lane, and E.A. Nigg 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 (Pubitemid 27036434)
41. I. Sumara, J.F. Gimenez-Abian, D. Gerlich, T. Hirota, C. Kraft, C. de la Torre, J. Ellenberg, and J.M. Peters Roles of polo-like kinase 1 in the assembly of functional mitotic spindles Curr Biol 14 2004 1712 1722 (Pubitemid 39301160)
42. W. Reindl, J. Yuan, A. Krmer, K. Strebhardt, and T. Berg A pan-specific inhibitor of the polo-box domains of polo-like kinases arrests cancer cells in mitosis Chembiochem 10 2009 1145 1148
43. Y.S. Seong, K. Kamijo, J.S. Lee, E. Fernandez, R. Kuriyama, T. Miki, and K.S. Lee A spindle checkpoint arrest and a cytokinesis failure by the dominant-negative polo-box domain of Plk1 in U-2 OS cells J Biol Chem 277 2002 32282 32293 (Pubitemid 34969045)
44. A. Hanisch, A. Wehner, E.A. Nigg, and H.H. Sillje Different Plk1 functions show distinct dependencies on Polo-Box domain-mediated targeting Mol Biol Cell 17 2006 448 459 (Pubitemid 43049496)
45. X. Wang, Y. Yang, Q. Duan, N. Jiang, Y. Huang, Z. Darzynkiewicz, and W. Dai sSgo1, a major splice variant of Sgo1, functions in centriole cohesion where it is regulated by Plk1 Dev Cell 14 2008 331 341
46. G. Eot-Houllier, M. Venoux, S. Vidal-Eychenié, M.T. Hoang, D. Giorgi, and S. Rouquier Plk1 regulates both ASAP localization and its role in spindle pole integrity J Biol Chem 285 2010 29556 29568
47. M. Steegmaier, M. Hoffmann, A. Baum, P. Lenart, M. Petronczki, M. Krssak, U. Gurtler, P. Garin-Chesa, S. Lieb, J. Quant, M. Grauert, G.R. Adolf, N. Kraut, J.M. Peters, and W.J. Rettig BI 2536, a potent and selective inhibitor of polo-like kinase 1, inhibits tumor growth in vivo Curr Biol 17 2007 316 322 (Pubitemid 46241881)
48. B. Spankuch-Schmitt, J. Bereiter-Hahn, M. Kaufmann, and K. Strebhardt Effect of RNA silencing of polo-like kinase-1 (PLK1) on apoptosis and spindle formation in human cancer cells J Natl Cancer Inst 94 2002 1863 1877 (Pubitemid 36104631)
49. M. Lei, and R.L. Erikson Plk1 depletion in nontransformed diploid cells activates the DNA-damage checkpoint Oncogene 27 2008 3935 3943 (Pubitemid 351913640)
50. S.M. Lens, E.E. Voest, and R.H. Medema Shared and separate functions of polo-like kinases and aurora kinases in cancer Nat Rev Cancer 10 2010 825 841