PI 3-kinase-dependent phosphorylation of Plk1-Ser99 promotes association with 14-3-3γ and is required for metaphase-anaphase transition

Nature Communications

Volumn 4, Issue , 2013, Pages

  Kasahara, Kousuke ^a,b   Goto, Hidemasa ^a,c   Izawa, Ichiro ^a   Kiyono, Tohru ^d   Watanabe, Nobumoto ^e   Elowe, Sabine ^f,g   Nigg, Erich A ^h   Inagaki, Masaki ^a,c  

^a AICHI CANCER CENTER HOSPITAL   (Japan)

^b NAGOYA CITY UNIVERSITY   (Japan)

^c NAGOYA UNIVERSITY GRADUATE SCHOOL OF MEDICINE   (Japan)

^d NATIONAL CANCER CENTER RESEARCH INSTITUTE   (Japan)

^e RIKEN   (Japan)

^f University Laval   (Canada)

^g UNIVERSITÉ LAVAL   (Canada)

^h UNIVERSITY OF BASEL   (Switzerland)

Author keywords

[No Author keywords available]

Indexed keywords

CASEIN; CYCLIN B1; CYCLIN DEPENDENT KINASE 1; MYC PROTEIN; PHOSPHATIDYLINOSITOL 3 KINASE; POLO LIKE KINASE 1; PROTEIN; PROTEIN 14 3 3 GAMMA; PROTEIN KINASE B; SMALL INTERFERING RNA; UNCLASSIFIED DRUG; VIMENTIN;

CATALYSIS; ENZYME ACTIVITY; INHIBITION; PROTEIN; SIGNAL;

ANAPHASE; ARTICLE; CATALYSIS; CELL CYCLE ARREST; DROSOPHILA MELANOGASTER; ENZYME ACTIVATION; ENZYME ACTIVITY; ENZYME PHOSPHORYLATION; FEMALE; HELA CELL; HUMAN; HUMAN CELL; METAPHASE; NONHUMAN; PROMETAPHASE; PROTEIN BINDING; PROTEIN LOCALIZATION; PROTEIN PROTEIN INTERACTION; WILD TYPE;

14-3-3 PROTEINS; ANAPHASE; ANIMALS; BIOCATALYSIS; CAENORHABDITIS ELEGANS; CELL CYCLE PROTEINS; DROSOPHILA MELANOGASTER; ENZYME ACTIVATION; HELA CELLS; HUMANS; M PHASE CELL CYCLE CHECKPOINTS; METAPHASE; MODELS, BIOLOGICAL; PHOSPHATIDYLINOSITOL 3-KINASES; PHOSPHORYLATION; PHOSPHOSERINE; PROTEIN BINDING; PROTEIN-SERINE-THREONINE KINASES; PROTO-ONCOGENE PROTEINS; PROTO-ONCOGENE PROTEINS C-AKT; SIGNAL TRANSDUCTION;

EID: 84878710374     PISSN: None     EISSN: 20411723     Source Type: Journal    
DOI: 10.1038/ncomms2879     Document Type: Article

References (46)

1. Walczak, C. E., Cai, S. & Khodjakov, A. Mechanisms of chromosome behaviour during mitosis. Nat. Rev. Mol. Cell. Biol. 11, 91-102 (2010)
2. Schvartzman, J. M., Sotillo, R. & Benezra, R. Mitotic chromosomal instability and cancer: mouse modelling of the human disease. Nat. Rev. Cancer 10, 102-115 (2010)
3. Nigg, E. A. Mitotic kinases as regulators of cell division and its checkpoints. Nat. Rev. Mol. Cell. Biol. 2, 21-32 (2001) (Pubitemid 33676958)
4. Taylor, S. & Peters, J. M. Polo and aurora kinases: lessons derived from chemical biology. Curr. Opin. Cell. Biol. 20, 77-84 (2008)
5. Carmena, M., Ruchaud, S. & Earnshaw, W. C. Making the Auroras glow: regulation of Aurora A and B kinase function by interacting proteins. Curr. Opin. Cell. Biol. 21, 796-805 (2009)
6. Lens, S. M., Voest, E. E. & Medema, R. H. Shared and separate functions of polo-like kinases and aurora kinases in cancer. Nat. Rev. Cancer 10, 825-841 (2010)
7. Archambault, V. & Glover, D. M. Polo-like kinases: conservation and divergence in their functions and regulation. Nat. Rev. Mol. Cell. Biol. 10, 265-275 (2009)
8. Barr, F. A., Sillje, H. H. & Nigg, E. A. Polo-like kinases and the orchestration of cell division. Nat. Rev. Mol. Cell. Biol. 5, 429-440 (2004) (Pubitemid 38745493)
9. Petronczki, M., Lenart, P. & Peters, J. M. Polo on the rise-from mitotic entry to cytokinesis with Plk1. Dev. Cell 14, 646-659 (2008) (Pubitemid 351622626)
10. Seki, A., Coppinger, J. A., Jang, C. Y., Yates, J. R. & Fang, G. Bora and the kinase Aurora A cooperatively activate the kinase Plk1 and control mitotic entry. Science 320, 1655-1658 (2008) (Pubitemid 351931258)
11. Macurek, L. et al. Polo-like kinase-1 is activated by aurora A to promote checkpoint recovery. Nature 455, 119-123 (2008)
12. Carmena, M. et al. The chromosomal passenger complex activates Polo kinase at centromeres. PLoS Biol. 10, e1001250 (2012)
13. Kasahara, K. et al. 14-3-3gamma mediates Cdc25A proteolysis to block premature mitotic entry after DNA damage. EMBO J. 29, 2802-2812 (2010)
14. Goto, H., Izawa, I., Li, P. & Inagaki, M. Novel regulation of checkpoint kinase 1: is checkpoint kinase 1 a good candidate for anti-cancer therapy? Cancer Sci. 103, 1195-1200 (2012)
15. Goto, H. et al. Identification of a novel phosphorylation site on histone H3 coupled with mitotic chromosome condensation. J. Biol. Chem. 274, 25543-25549 (1999)
16. Hirota, T. et al. Aurora-A and an interacting activator, the LIM protein Ajuba, are required for mitotic commitment in human cells. Cell 114, 585-598 (2003) (Pubitemid 37159255)
17. Kanda, T., Sullivan, K. F. & Wahl, G. M. Histone-GFP fusion protein enables sensitive analysis of chromosome dynamics in living mammalian cells. Curr. Biol. 8, 377-385 (1998) (Pubitemid 28173996)
18. Kops, G. J. & Shah, J. V. Connecting up and clearing out: how kinetochore attachment silences the spindle assembly checkpoint. Chromosoma 121, 509-525 (2012)
19. Musacchio, A. & Salmon, E. D. The spindle-assembly checkpoint in space and time. Nat. Rev. Mol. Cell. Biol. 8, 379-393 (2007) (Pubitemid 46643240)
20. Mohammad, D. H. & Yaffe, M. B. 14-3-3 proteins, FHA domains and BRCT domains in the DNA damage response. DNA Repair (Amst) 8, 1009-1017 (2009)
21. Hermeking, H. The 14-3-3 cancer connection. Nat. Rev. Cancer 3, 931-943 (2003) (Pubitemid 37500178)
22. Meek, S. E., Lane, W. S. & Piwnica-Worms, H. Comprehensive proteomic analysis of interphase and mitotic 14-3-3-binding proteins. J. Biol. Chem. 279, 32046-32054 (2004) (Pubitemid 39014649)
23. Pozuelo Rubio, M. et al. 14-3-3-affinity purification of over 200 human phosphoproteins reveals new links to regulation of cellular metabolism, proliferation and trafficking. Biochem. J. 379, 395-408 (2004) (Pubitemid 38570113)
24. Elowe, S., Hummer, S., Uldschmid, A., Li, X. & Nigg, E. A. Tension-sensitive Plk1 phosphorylation on BubR1 regulates the stability of kinetochore microtubule interactions. Genes Dev. 21, 2205-2219 (2007) (Pubitemid 47360842)
25. Watanabe, N. et al. Cyclin-dependent kinase (CDK) phosphorylation destabilizes somatic Wee1 via multiple pathways. Proc. Natl Acad. Sci. USA 102, 11663-11668 (2005) (Pubitemid 41170783)
26. Jang, Y. J., Ma, S., Terada, Y. & Erikson, R. L. Phosphorylation of threonine 210 and the role of serine 137 in the regulation of mammalian polo-like kinase. J. Biol. Chem. 277, 44115-44120 (2002) (Pubitemid 36157840)
27. Tang, J., Yang, X. & Liu, X. Phosphorylation of Plk1 at Ser326 regulates its functions during mitotic progression. Oncogene 27, 6635-6645 (2008)
28. Nishizawa, K. et al. Specific localization of phosphointermediate filament protein in the constricted area of dividing cells. J. Biol. Chem. 266, 3074-3079 (1991) (Pubitemid 21909176)
29. Goto, H. & Inagaki, M. Production of a site- and phosphorylation state-specific antibody. Nat. Protoc. 2, 2574-2581 (2007)
30. Chan, E. H., Santamaria, A., Sillje, H. H. & Nigg, E. A. Plk1 regulates mitotic Aurora A function through betaTrCP-dependent degradation of hBora. Chromosoma 117, 457-469 (2008)
31. Seki, A. et al. Plk1- and beta-TrCP-dependent degradation of Bora controls mitotic progression. J. Cell. Biol. 181, 65-78 (2008) (Pubitemid 351519765)
32. Hanisch, A. Different Plk1 functions show distinct dependencies on polo-box domain-mediated targeting. Mol. Biol. Cell. 17, 448-459 (2005) (Pubitemid 43049496)
33. Okumura, E. et al. Akt inhibits Myt1 in the signalling pathway that leads to meiotic G2/M-phase transition. Nat. Cell. Biol. 4, 111-116 (2002) (Pubitemid 34141476)
34. Shtivelman, E., Sussman, J. & Stokoe, D. A role for PI 3-kinase and PKB activity in the G2/M phase of the cell cycle. Curr. Biol. 12, 919-924 (2002) (Pubitemid 34689227)
35. Lindsley, C. W. The Akt/PKB family of protein kinases: a review of small molecule inhibitors and progress towards target validation: a 2009 update. Curr. Top. Med. Chem. 10, 458-477 (2010)
36. Meuillet, E. J. et al. Molecular pharmacology and antitumor activity of PHT- 427, a novel Akt/phosphatidylinositide-dependent protein kinase 1 pleckstrin homology domain inhibitor. Mol. Cancer Ther. 9, 706-717 (2010)
37. Yang, L. et al. Akt/protein kinase B signaling inhibitor-2, a selective small molecule inhibitor of Akt signaling with antitumor activity in cancer cells overexpressing Akt. Cancer Res. 64, 4394-4399 (2004) (Pubitemid 38856907)
38. Mabuchi, S. et al. Inhibition of phosphorylation of BAD and Raf-1 by Akt sensitizes human ovarian cancer cells to paclitaxel. J. Biol. Chem. 277, 33490-33500 (2002) (Pubitemid 34984873)
39. Tran, N. L., Adams, D. G., Vaillancourt, R. R. & Heimark, R. L. Signal transduction from N-cadherin increases Bcl-2. Regulation of the phosphatidylinositol 3-kinase/Akt pathway by homophilic adhesion and actin cytoskeletal organization. J. Biol. Chem. 277, 32905-32914 (2002) (Pubitemid 34984804)
40. Goto, H. et al. Complex formation of Plk1 and INCENP required for metaphase-anaphase transition. Nat. Cell. Biol. 8, 180-187 (2005)
41. Tsujimura, K. et al. Visualization and function of vimentin phosphorylation by cdc2 kinase during mitosis. J. Biol. Chem. 269, 31097-31106 (1994) (Pubitemid 24377604)
42. Enomoto, M. et al. Novel positive feedback loop between Cdk1 and Chk1 in the nucleus during G2/M transition. J. Biol. Chem. 284, 34223-34230 (2009)
43. Li, P. et al. P90 RSK arranges Chk1 in the nucleus for monitoring of genomic integrity during cell proliferation. Mol. Biol. Cell. 23, 1582-1592 (2012)
44. Shiromizu, T. et al. Regulation of mitotic function of Chk1 through phosphorylation at novel sites by cyclin-dependent kinase 1 (Cdk1). Genes Cells 11, 477-485 (2006)
45. Yamaguchi, T. et al. Phosphorylation by Cdk1 induces Plk1-mediated vimentin phosphorylation during mitosis. J. Cell. Biol. 171, 431-436 (2005) (Pubitemid 41586932)
46. Inoko, A. et al. Trichoplein and Aurora A block aberrant primary cilia assembly in proliferating cells. J. Cell. Biol. 197, 391-405 (2012).