Polo-like kinase 1 regulates the stability of the mitotic centromere-associated kinesin in mitosis

Oncotarget

Volumn 5, Issue 10, 2014, Pages 3130-3144

  Sanhaji, Mourad ^a,c   Ritter, Andreas ^a   Belsham, Hannah R ^b   Friel, Claire T ^b   Roth, Susanne ^a   Louwen, Frank ^a   Yuan, Juping ^a  

^a GOETHE UNIVERSITY   (Germany)

^b UNIVERSITY OF NOTTINGHAM   (United Kingdom)

^c JENA UNIVERSITY HOSPITAL   (Germany)

Author keywords

Chromosome alignment spindle assembly; MCAK; Plk1; Protein stability

Indexed keywords

CELL CYCLE PROTEIN 20; KINESIN; MCAK PROTEIN; POLO LIKE KINASE 1; PROTEASOME; UBIQUITIN; UNCLASSIFIED DRUG; CELL CYCLE PROTEIN; KIF2C PROTEIN, HUMAN; ONCOPROTEIN; POLO-LIKE KINASE 1; PROTEIN SERINE THREONINE KINASE;

ARTICLE; CARBOXY TERMINAL SEQUENCE; CELL SIGNALING ASSAY; CENTROMERE; CHROMOSOME DISPLACEMENT; CHROMOSOMES AND CHROMOSOMAL PHENOMENA; CONTROLLED STUDY; DEPOLYMERIZATION; ENZYME INHIBITION; ENZYME REGULATION; IN VITRO STUDY; INTER KINETOCHORE DISTANCE; INTRACELLULAR SIGNALING; MITOSIS; MITOSIS INHIBITION; MITOSIS SPINDLE; MUTATION; PROTEIN DEGRADATION; PROTEIN DOMAIN; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN MOTIF; PROTEIN PHOSPHORYLATION; PROTEIN STABILITY; PROTEIN TARGETING; SPINDLE FORMATION DEFECT; CONFOCAL MICROSCOPY; FLUORESCENT ANTIBODY TECHNIQUE; GENETIC TRANSFECTION; HUMAN; IMMUNOPRECIPITATION; METABOLISM; PATHOLOGY; PHYSIOLOGY; SPINDLE APPARATUS; TUMOR CELL LINE; WESTERN BLOTTING;

BLOTTING, WESTERN; CELL CYCLE PROTEINS; CELL LINE, TUMOR; FLUORESCENT ANTIBODY TECHNIQUE; HUMANS; IMMUNOPRECIPITATION; KINESIN; MICROSCOPY, CONFOCAL; MITOSIS; PROTEIN STABILITY; PROTEIN-SERINE-THREONINE KINASES; PROTO-ONCOGENE PROTEINS; SPINDLE APPARATUS; TRANSFECTION;

EID: 84902118710     PISSN: None     EISSN: 19492553     Source Type: Journal    
DOI: 10.18632/oncotarget.1861     Document Type: Article

References (59)

1. Gadde S, Heald R: Mechanisms and molecules of the mitotic spindle. Curr Biol 2004, 14: R797-R805.
2. Loughlin R, Riggs B, Heald R: SnapShot: motor proteins in spindle assembly. Cell 2008, 134: 548.
3. Desai A, Verma S, Mitchison TJ, Walczak CE: Kin I kinesins are microtubule-destabilizing enzymes. Cell 1999, 96: 69-78.
4. Ogawa T, Nitta R, Okada Y, Hirokawa N: A common mechanism for microtubule destabilizers-M type kinesins stabilize curling of the protofilament using the class-specific neck and loops. Cell 2004, 116: 591-602.
5. Ganem NJ, Upton K, Compton DA: Efficient mitosis in human cells lacking poleward microtubule flux. Curr Biol 2005, 15: 1827-1832.
6. Manning AL, Ganem NJ, Bakhoum SF, Wagenbach M, Wordeman L, Compton DA: The kinesin-13 proteins Kif2a, Kif2b, and Kif2c/MCAK have distinct roles during mitosis in human cells. Mol Biol Cell 2007, 18: 2970-2979.
7. Lawrence CJ, Dawe RK, Christie KR, Cleveland DW, Dawson SC, Endow SA, Goldstein LS, Goodson HV, Hirokawa N, Howard J, Malmberg RL, McIntosh JR, Miki H, Mitchison TJ, Okada Y, Reddy AS et al.: A standardized kinesin nomenclature. J Cell Biol 2004, 167: 19-22.
8. Tournebize R, Popov A, Kinoshita K, Ashford AJ, Rybina S, Pozniakovsky A, Mayer TU, Walczak CE, Karsenti E, Hyman AA: Control of microtubule dynamics by the antagonistic activities of XMAP215 and XKCM1 in Xenopus egg extracts. Nat Cell Biol 2000, 2: 13-19.
9. Wordeman L, Mitchison TJ: Identification and partial characterization of mitotic centromere-associated kinesin, a kinesin-related protein that associates with centromeres during mitosis. J Cell Biol 1995, 128: 95-104.
10. Moore AT, Rankin KE, von DG, Peris L, Wagenbach M, Ovechkina Y, Andrieux A, Job D, Wordeman L: MCAK associates with the tips of polymerizing microtubules. J Cell Biol 2005, 169: 391-397.
11. Maney T, Hunter AW, Wagenbach M, Wordeman L: Mitotic centromere-associated kinesin is important for anaphase chromosome segregation. J Cell Biol 1998, 142: 787-801.
12. Zhang L, Shao H, Huang Y, Yan F, Chu Y, Hou H, Zhu M, Fu C, Aikhionbare F, Fang G, Ding X, Yao X: PLK1 phosphorylates mitotic centromere-associated kinesin and promotes its depolymerase activity. J Biol Chem 2011, 286: 3033-3046.
13. Zhang X, Ems-McClung SC, Walczak CE: Aurora A phosphorylates MCAK to control ran-dependent spindle bipolarity. Mol Biol Cell 2008, 19: 2752-2765.
14. Zhang X, Lan W, Ems-McClung SC, Stukenberg PT, Walczak CE: Aurora B phosphorylates multiple sites on mitotic centromere-associated kinesin to spatially and temporally regulate its function. Mol Biol Cell 2007, 18: 3264-3276.
15. Sanhaji M, Friel CT, Kreis NN, Kramer A, Martin C, Howard J, Strebhardt K, Yuan J: Functional and spatial regulation of mitotic centromere-associated kinesin by cyclin-dependent kinase 1. Mol Cell Biol 2010, 30: 2594-2607.
16. Lan W, Zhang X, Kline-Smith SL, Rosasco SE, Barrett-Wilt GA, Shabanowitz J, Hunt DF, Walczak CE, Stukenberg PT: Aurora B phosphorylates centromeric MCAK and regulates its localization and microtubule depolymerization activity. Curr Biol 2004, 14: 273-286.
17. Andrews PD, Ovechkina Y, Morrice N, Wagenbach M, Duncan K, Wordeman L, Swedlow JR: Aurora B regulates MCAK at the mitotic centromere. Dev Cell 2004, 6: 253-268.
18. Hood EA, Kettenbach AN, Gerber SA, Compton DA: Plk1 regulates the kinesin-13 protein Kif2b to promote faithful chromosome segregation. Mol Biol Cell 2012, 23: 2264-2274.
19. Shimo A, Tanikawa C, Nishidate T, Lin ML, Matsuda K, Park JH, Ueki T, Ohta T, Hirata K, Fukuda M, Nakamura Y, Katagiri T: Involvement of kinesin family member 2C/mitotic centromere-associated kinesin overexpression in mammary carcinogenesis. Cancer Sci 2008, 99: 62-70.
20. Nakamura Y, Tanaka F, Haraguchi N, Mimori K, Matsumoto T, Inoue H, Yanaga K, Mori M: Clinicopathological and biological significance of mitotic centromere-associated kinesin overexpression in human gastric cancer. Br J Cancer 2007, 97: 543-549.
21. Ishikawa K, Kamohara Y, Tanaka F, Haraguchi N, Mimori K, Inoue H, Mori M: Mitotic centromere-associated kinesin is a novel marker for prognosis and lymph node metastasis in colorectal cancer. Br J Cancer 2008, 98: 1824-1829.
22. Yuan J, Horlin A, Hock B, Stutte HJ, Rubsamen-Waigmann H, Strebhardt K: Polo-like kinase, a novel marker for cellular proliferation. Am J Pathol 1997, 150: 1165-1172.
23. Yuan J, Sanhaji M, Kramer A, Reindl W, Hofmann M, Kreis NN, Zimmer B, Berg T, Strebhardt K: Polo-box domain inhibitor poloxin activates the spindle assembly checkpoint and inhibits tumor growth in vivo. Am J Pathol 2011, 179: 2091-2099.
24. Strebhardt K: Multifaceted polo-like kinases: drug targets and antitargets for cancer therapy. Nat Rev Drug Discov 2010, 9: 643-660.
25. Barr FA, Sillje HH, Nigg EA: Polo-like kinases and the orchestration of cell division. Nat Rev Mol Cell Biol 2004, 5: 429-440.
26. Zhang N, Panigrahi AK, Mao Q, Pati D: Interaction of Sororin protein with polo-like kinase 1 mediates resolution of chromosomal arm cohesion. J Biol Chem 2011, 286: 41826-41837.
27. Zhang N, Pati D: Sororin is a master regulator of sister chromatid cohesion and separation. Cell Cycle 2012, 11: 2073-2083.
28. Lane HA, Nigg EA: Antibody microinjection reveals an essential role for human polo-like kinase 1 (Plk1) in the functional maturation of mitotic centrosomes. J Cell Biol 1996, 135: 1701-1713.
29. Elowe S, Hummer S, Uldschmid A, Li X, Nigg EA: Tension-sensitive Plk1 phosphorylation on BubR1 regulates the stability of kinetochore microtubule interactions. Genes Dev 2007, 21: 2205-2219.
30. Neef R, Gruneberg U, Kopajtich R, Li X, Nigg EA, Sillje H, Barr FA: Choice of Plk1 docking partners during mitosis and cytokinesis is controlled by the activation state of Cdk1. Nat Cell Biol 2007, 9: 436-444.
31. Neef R, Preisinger C, Sutcliffe J, Kopajtich R, Nigg EA, Mayer TU, Barr FA: Phosphorylation of mitotic kinesin-like protein 2 by polo-like kinase 1 is required for cytokinesis. J Cell Biol 2003, 162: 863-875.
32. Jang CY, Coppinger JA, Seki A, Yates JR, III, Fang G: Plk1 and Aurora A regulate the depolymerase activity and the cellular localization of Kif2a. J Cell Sci 2009, 122: 1334-1341.
33. Kreis NN, Sommer K, Sanhaji M, Kramer A, Matthess Y, Kaufmann M, Strebhardt K, Yuan J: Long-term downregulation of Polo-like kinase 1 increases the cyclin-dependent kinase inhibitor p21(WAF1/CIP1). Cell Cycle 2009, 8: 460-472.
34. Ganguly A, Bhattacharya R, Cabral F: Control of MCAK degradation and removal from centromeres. Cytoskeleton (Hoboken ) 2012, 69: 303-311.
35. Yuan J, Yan R, Kramer A, Eckerdt F, Roller M, Kaufmann M, Strebhardt K: Cyclin B1 depletion inhibits proliferation and induces apoptosis in human tumor cells. Oncogene 2004, 23: 5843-5852.
36. Lenart P, Petronczki M, Steegmaier M, Di FB, Lipp JJ, Hoffmann M, Rettig WJ, Kraut N, Peters JM: The small-molecule inhibitor BI 2536 reveals novel insights into mitotic roles of polo-like kinase 1. Curr Biol 2007, 17: 304-315.
37. 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 U S A 2004, 101: 7937-7942.
38. Sumara I, Gimenez-Abian JF, Gerlich D, Hirota T, Kraft C, de la Torre C, Ellenberg J, Peters JM: Roles of polo-like kinase 1 in the assembly of functional mitotic spindles. Curr Biol 2004, 14: 1712-1722.
39. Sanhaji M, Kreis NN, Zimmer B, Berg T, Louwen F, Yuan J: p53 is not directly relevant to the response of Polo-like kinase 1 inhibitors. Cell Cycle 2012, 11.
40. Lane SI, Chang HY, Jennings PC, Jones KT: The Aurora kinase inhibitor ZM447439 accelerates first meiosis in mouse oocytes by overriding the spindle assembly checkpoint. Reproduction 2010, 140: 521-530.
41. Peters U, Cherian J, Kim JH, Kwok BH, Kapoor TM: Probing cell-division phenotype space and Polo-like kinase function using small molecules. Nat Chem Biol 2006, 2: 618-626.
42. Glotzer M, Murray AW, Kirschner MW: Cyclin is degraded by the ubiquitin pathway. Nature 1991, 349: 132-138.
43. Clute P, Pines J: Temporal and spatial control of cyclin B1 destruction in metaphase. Nat Cell Biol 1999, 1: 82-87.
44. Thornton BR, Ng TM, Matyskiela ME, Carroll CW, Morgan DO, Toczyski DP: An architectural map of the anaphase-promoting complex. Genes Dev 2006, 20: 449-460.
45. Kimata Y, Baxter JE, Fry AM, Yamano H: A role for the Fizzy/Cdc20 family of proteins in activation of the APC/C distinct from substrate recruitment. Mol Cell 2008, 32: 576-583.
46. Wang R, Li KM, Zhou CH, Xue JL, Ji CN, Chen JZ: Cdc20 mediates D-box-dependent degradation of Sp100. Biochem Biophys Res Commun 2011, 415: 702-706.
47. Li L, Zhou Y, Wang GF, Liao SC, Ke YB, Wu W, Li XH, Zhang RL, Fu YC: Anaphase-promoting complex/cyclosome controls HEC1 stability. Cell Prolif 2011, 44: 1-9.
48. Helenius J, Brouhard G, Kalaidzidis Y, Diez S, Howard J: The depolymerizing kinesin MCAK uses lattice diffusion to rapidly target microtubule ends. Nature 2006, 441: 115-119.
49. Domnitz SB, Wagenbach M, Decarreau J, Wordeman L: MCAK activity at microtubule tips regulates spindle microtubule length to promote robust kinetochore attachment. J Cell Biol 2012, 197: 231-237.
50. Tanenbaum ME, Medema RH: Localized Aurora B activity spatially controls non-kinetochore microtubules during spindle assembly. Chromosoma 2011, 120: 599-607.
51. Vassilev LT, Tovar C, Chen S, Knezevic D, Zhao X, Sun H, Heimbrook DC, Chen L: Selective small-molecule inhibitor reveals critical mitotic functions of human CDK1. Proc Natl Acad Sci U S A 2006, 103: 10660-10665.
52. Stout JR, Rizk RS, Kline SL, Walczak CE: Deciphering protein function during mitosis in PtK cells using RNAi. BMC Cell Biol 2006, 7: 26.
53. Holmfeldt P, Zhang X, Stenmark S, Walczak CE, Gullberg M: CaMKIIgamma-mediated inactivation of the Kin I kinesin MCAK is essential for bipolar spindle formation. EMBO J 2005, 24: 1256-1266.
54. Hedrick DG, Stout JR, Walczak CE: Effects of anti-microtubule agents on microtubule organization in cells lacking the kinesin-13 MCAK. Cell Cycle 2008, 7: 2146-2156.
55. Sanhaji M, Friel CT, Wordeman L, Louwen F, Yuan J: Mitotic centromere-associated kinesin (MCAK): a potential cancer drug target. Oncotarget 2011, 2: 935-947.
56. Ems-McClung SC, Hertzer KM, Zhang X, Miller MW, Walczak CE: The interplay of the N-and C-terminal domains of MCAK control microtubule depolymerization activity and spindle assembly. Mol Biol Cell 2007, 18: 282-294.
57. Ems-McClung SC, Hainline SG, Devare J, Zong H, Cai S, Carnes SK, Shaw SL, Walczak CE: Aurora B Inhibits MCAK Activity through a Phosphoconformational Switch that Reduces Microtubule Association. Curr Biol 2013, 23: 2491-2499.
58. Kreis NN, Sanhaji M, Rieger MA, Louwen F, Yuan J: p21Waf1/Cip1 deficiency causes multiple mitotic defects in tumor cells. Oncogene 2013.
59. Muschol-Steinmetz C, Friemel A, Kreis NN, Reinhard J, Yuan J, Louwen F: Function of survivin in trophoblastic cells of the placenta. PLoS One 2013, 8: e73337.