Dishevelled, a Wnt signalling component, is involved in mitotic progression in cooperation with Plk1

EMBO Journal

Volumn 29, Issue 20, 2010, Pages 3470-3483

  Kikuchi, Koji ^a   Niikura, Yohei ^b   Kitagawa, Katsumi ^b   Kikuchi, Akira ^a  

^a OSAKA UNIVERSITY GRADUATE SCHOOL OF MEDICINE   (Japan)

^b NATIONWIDE CHILDREN S HOSPITAL   (United States)

Author keywords

dishevelled; microtubule plus end; mitosis; Plk1; Wnt signalling

Indexed keywords

BUB1 RELATED PROTEIN; DISHEVELLED 2; NOCODAZOLE; POLO LIKE KINASE 1; SPINDLE ASSEMBLY CHECKPOINT KINASE; UNCLASSIFIED DRUG; WNT PROTEIN;

ARTICLE; CELL CYCLE G1 PHASE; CELL CYCLE S PHASE; CENTROMERE; CONTROLLED STUDY; FEMALE; GENE EXPRESSION; HUMAN; HUMAN CELL; MITOSIS; PRIORITY JOURNAL; PROTEIN ANALYSIS; PROTEIN FUNCTION; PROTEIN PHOSPHORYLATION; SIGNAL TRANSDUCTION;

ADAPTOR PROTEINS, SIGNAL TRANSDUCING; ANIMALS; AUTOANTIGENS; CELL CYCLE PROTEINS; CELL LINE; CHROMOSOMAL PROTEINS, NON-HISTONE; FRIZZLED RECEPTORS; HUMANS; KINETOCHORES; MITOSIS; MITOTIC SPINDLE APPARATUS; NOCODAZOLE; PHOSPHOPROTEINS; PROTEIN-SERINE-THREONINE KINASES; PROTO-ONCOGENE PROTEINS; RECEPTORS, G-PROTEIN-COUPLED; RECEPTORS, LDL; RECOMBINANT FUSION PROTEINS; RNA, SMALL INTERFERING; SIGNAL TRANSDUCTION; TUBULIN MODULATORS; WNT PROTEINS;

EID: 77958462847     PISSN: 02614189     EISSN: 14602075     Source Type: Journal    
DOI: 10.1038/emboj.2010.221     Document Type: Article

References (67)

1. Abrieu A, Magnaghi-Jaulin L, Kahana JA, Peter M, Castro A, Vigneron S, Lorca T, Cleveland DW, Labbe JC (2001) Mps1 is a kinetochore-associated kinase essential for the vertebrate mitotic checkpoint. Cell 106: 83-93
2. Akhmanova A, Hoogenraad CC (2005) Microtubule plus-end-tracking proteins: mechanisms and functions. Curr Opin Cell Biol 17: 47-54
3. Andersen SS (2000) Spindle assembly and the art of regulating microtubule dynamics by MAPs and Stathmin/Op18. Trends Cell Biol 10 : 261-267
4. Arnaud L, Pines J, Nigg EA (1998) GFP tagging reveals human Pololike kinase 1 at the kinetochore/centromere region of mitotic chromosomes. Chromosoma 107: 424-429
5. Bahmanyar S, Kaplan DD, Deluca JG, Giddings Jr TH, O'Toole ET, Winey M, Salmon ED, Casey PJ, Nelson WJ, Barth AI (2008) b-Catenin is a Nek2 substrate involved in centrosome separation. Genes Dev 22: 91-105
6. Ban R, Matsuzaki H, Akashi T, Sakashita G, Taniguchi H, Park SY, Tanaka H, Furukawa K, Urano T (2009) Mitotic regulation of the stability of microtubule plus-end tracking protein EB3 by ubiqui-tin ligase SIAH-1 and Aurora mitotic kinases. J Biol Chem 284: 28367-28381
7. Casenghi M, Meraldi P, Weinhart U, Duncan PI, Korner R, Nigg EA (2003) Polo-like kinase 1 regulates Nlp, a centrosome protein involved in microtubule nucleation. Dev Cell 5: 113-125
8. Ciani L, Krylova O, Smalley MJ, Dale TC, Salinas PC (2004) A divergent canonical WNT-signaling pathway regulates micro-tubule dynamics: dishevelled signals locally to stabilize micro-tubules. J Cell Biol 164: 243-253
9. Cleveland DW, Mao Y, Sullivan KF (2003) Centromeres and kine-tochores: from epigenetics to mitotic checkpoint signaling. Cell 112: 407-421
10. Davidson G, Shen J, Huang YL, Su Y, Karaulanov E, Bartscherer K, Hassler C, Stannek P, Boutros M, Niehrs C (2009) Cell cycle control of wnt receptor activation. Dev Cell 17: 788-799
11. Davidson G, Wu W, Shen J, Bilic J, Fenger U, Stannek P, Glinka A, Niehrs C (2005) Casein kinase 1g couples Wnt receptor activation to cytoplasmic signal transduction. Nature 438: 867-872
12. Dephoure N, Zhou C, Villén J, Beausoleil SA, Bakalarski CE, Elledge SJ, Gygi SP (2008) A quantitative atlas of mitotic phosphoryla-tion. Proc Natl Acad Sci USA 105: 10762-10767
13. Draviam VM, Shapiro I, Aldridge B, Sorger PK (2006) Misorientation and reduced stretching of aligned sister kineto-chores promote chromosome missegregation in EB1-or APC-depleted cells. EMBO J 25: 2814-2827
14. Elia AE, Cantley LC, Yaffe MB (2003) Proteomic screen finds pSer/ pThr-binding domain localizing Plk1 to mitotic substrates. Science 299: 1228-1231
15. Elowe S, Hummer S, Uldschmid A, Li X, Nigg EA (2007) Tension-sensitive Plk1 phosphorylation on BubR1 regulates the stability of kinetochore microtubule interactions. Genes Dev 21: 2205-2219
16. Feng J, Huang H, Yen TJ (2006) CENP-F is a novel microtubule-binding protein that is essential for kinetochore attachments and affects the duration of the mitotic checkpoint delay. Chromosoma 115: 320-329
17. Fumoto K, Lee PC, Saya H, Kikuchi A (2008) AIP regulates stability of Aurora-A at early mitotic phase coordinately with GSK-3b. Oncogene 27: 4478-4487
18. Green JL, Kuntz SG, Sternberg PW (2008) Ror receptor tyrosine kinases: orphans no more. Trends Cell Biol 18: 536-544
19. Hadjihannas MV, Bruckner M, Jerchow B, Birchmeier W, Dietmaier W, Behrens J (2006) Aberrant Wnt/b-catenin signaling can induce chromosomal instability in colon cancer. Proc Natl Acad Sci USA 103: 10747-10752
20. Izumi N, Fumoto K, Izumi S, Kikuchi A (2008) GSK-3b regulates proper mitotic spindle formation in cooperation with a component of the g-tubulin ring complex, GCP5. J Biol Chem 283: 12981-12991
21. Jelluma N, Brenkman AB, McLeod I, Yates III JR, Cleveland DW, Medema RH, Kops GJ (2008a) Chromosomal instability by inefficient Mps1 auto-activation due to a weakened mitotic checkpoint and lagging chromosomes. PLoS One 3: e2415
22. Jelluma N, Brenkman AB, van den Broek NJ, Cruijsen CW, van Osch MH, Lens SM, Medema RH, Kops GJ (2008b) Mps1 phos-phorylates Borealin to control Aurora B activity and chromosome alignment. Cell 132: 233-246
23. Kang J, Chen Y, Zhao Y, Yu H (2007) Autophosphorylation-depen-dent activation of human Mps1 is required for the spindle checkpoint. Proc Natl Acad Sci USA 104: 20232-20237
24. Kaplan KB, Burds AA, Swedlow JR, Bekir SS, Sorger PK, Näthke IS (2001) A role for the Adenomatous Polyposis Coli protein in chromosome segregation. Nat Cell Biol 3: 429-432
25. Kawano Y, Kypta R (2003) Secreted antagonists of the Wnt signalling pathway. J Cell Sci 116: 2627-2634
26. Kikuchi A, Yamamoto H, Sato A (2009) Selective activation mechanisms of Wnt signaling pathways. Trends Cell Biol 19: 119-129
27. Kiyomitsu T, Obuse C, Yanagida M (2007) Human Blinkin/AF15q14 is required for chromosome alignment and the mitotic checkpoint through direct interaction with Bub1 and BubR1. Dev Cell 13: 663-676
28. Kline-Smith SL, Walczak CE (2004) Mitotic spindle assembly and chromosome segregation: refocusing on microtubule dynamics. Mol Cell 15: 317-327
29. Kurayoshi M, Oue N, Yamamoto H, Kishida M, Inoue A, Asahara T, Yasui W, Kikuchi A (2006) Expression of Wnt-5a is correlated with aggressiveness of gastric cancer by stimulating cell migration and invasion. Cancer Res 66: 10439-10448
30. Lampson MA, Kapoor TM (2005) The human mitotic checkpoint protein BubR1 regulates chromosome-spindle attachments. Nat Cell Biol 7: 93-98
31. Lane HA, Nigg EA (1996) 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
32. Lee YN, Gao Y, Wang HY (2008) Differential mediation of the Wnt canonical pathway by mammalian Dishevelleds-1,-2, and-3. Cell Signal 20: 443-452
33. Lénárt P, Petronczki M, Steegmaier M, Di Fiore B, Lipp JJ, Hoffmann M, Rettig WJ, Kraut N, Peters JM (2007) The small-molecule inhibitor BI 2536 reveals novel insights into mitotic roles of pololike kinase 1. Curr Biol 17: 304-315
34. Liu ST, Chan GK, Hittle JC, Fujii G, Lees E, Yen TJ (2003) Human MPS1 kinase is required for mitotic arrest induced by the loss of CENP-E from kinetochores. Mol Biol Cell 14: 1638-1651
35. Logan CY, Nusse R (2004) The Wnt signaling pathway in development and disease. Annu Rev Cell Dev Biol 20: 781-810
36. MacDonald BT, Tamai K, He X (2009) Wnt/b-catenin signaling: components, mechanisms, and diseases. Dev Cell 17: 9-26
37. Matsumoto S, Fumoto K, Okamoto T, Kaibuchi K, Kikuchi A (2010) Binding of APC and dishevelled mediates Wnt5a-regulated focal adhesion dynamics in migrating cells. EMBO J 29: 1192-1204
38. Matsumura S, Toyoshima F, Nishida E (2007) Polo-like kinase 1 facilitates chromosome alignment during prometaphase through BubR1. J Biol Chem 282: 15217-15227
39. McCartney BM, Näthke IS (2008) Cell regulation by the Apc protein Apc as master regulator of epithelia. Curr Opin Cell Biol 20: 186-193
40. Meraldi P, Sorger PK (2005) A dual role for Bub1 in the spindle checkpoint and chromosome congression. EMBO J 24: 1621-1633
41. Musacchio A, Salmon ED (2007) The spindle-assembly checkpoint in space and time. Nat Rev Mol Cell Biol 8: 379-393
42. Niehrs C (2006) Function and biological roles of the Dickkopf family of Wnt modulators. Oncogene 25: 7469-7481
43. Niikura Y, Ohta S, Vandenbeldt KJ, Abdulle R, McEwen BF, Kitagawa K (2006) 17-AAG, an Hsp90 inhibitor, causes kineto-chore defects: a novel mechanism by which 17-AAG inhibits cell proliferation. Oncogene 25: 4133-4146
44. Oshimori N, Ohsugi M, Yamamoto T (2006) The Plk1 target Kizuna stabilizes mitotic centrosomes to ensure spindle bipolarity. Nat Cell Biol 8: 1095-1101
45. Petronczki M, Lénárt P, Peters JM (2008) Polo on the rise-from mitotic entry to cytokinesis with Plk1. Dev Cell 14: 646-659
46. Piehl M, Tulu US, Wadsworth P, Cassimeris L (2004) Centrosome maturation: measurement of microtubule nucleation throughout the cell cycle by using GFP-tagged EB1. Proc Natl Acad Sci USA 101 : 1584-1588
47. Purro SA, Ciani L, Hoyos-Flight M, Stamatakou E, Siomou E, Salinas PC (2008) Wnt regulates axon behavior through changes in microtubule growth directionality: a new role for adenomatous polyposis coli. J Neurosci 28: 8644-8654
48. Sakane H, Yamamoto H, Kikuchi A (2010) LRP6 is internalized by Dkk1 to suppress its phosphorylation in the lipid raft and is recycled for reuse. J Cell Sci 123: 360-368
49. Santamaria A, Neef R, Eberspacher U, Eis K, Husemann M, Mumberg D, Prechtl S, Schulze V, Siemeister G, Wortmann L, Barr FA, Nigg EA (2007) Use of the novel Plk1 inhibitor ZK-thiazolidinone to elucidate functions of Plk1 in early and late stages of mitosis. Mol Biol Cell 18: 4024-4036
50. Sato A, Yamamoto H, Sakane H, Koyama H, Kikuchi A (2010) Wnt5a regulates distinct signalling pathways by binding to Frizzled2. EMBO J 29: 41-54
51. Sillje HH, Nagel S, Korner R, Nigg EA (2006) HURP is a Ran-importin b-regulated protein that stabilizes kinetochore micro-tubules in the vicinity of chromosomes. Curr Biol 16: 731-742
52. Stucke VM, Sillje HH, Arnaud L, Nigg EA (2002) Human Mps1 kinase is required for the spindle assembly checkpoint but not for centrosome duplication. EMBO J 21 : 1723-1732
53. Sumara I, Gimenez-Abian JF, Gerlich D, Hirota T, Kraft C, de la Torre C, Ellenberg J, Peters JM (2004) Roles of polo-like kinase 1 in the assembly of functional mitotic spindles. Curr Biol 14: 1712-1722
54. Tanaka TU, Stark MJ, Tanaka K (2005) Kinetochore capture and bi-orientation on the mitotic spindle. Nat Rev Mol Cell Biol 6: 929-942 (Pubitemid 41778712)
55. Taylor SS, McKeon F (1997) Kinetochore localization of murine Bub1 is required for normal mitotic timing and checkpoint response to spindle damage. Cell 89: 727-735
56. Tetsu O, McCormick F (1999) b-Catenin regulates expression of cyclin D1 in colon carcinoma cells. Nature 398: 422-426
57. Thoma CR, Toso A, Gutbrodt KL, Reggi SP, Frew IJ, Schraml P, Hergovich A, Moch H, Meraldi P, Krek W (2009) VHL loss causes spindle misorientation and chromosome instability. Nat Cell Biol 11 : 994-1001
58. Toyoshima F, Nishida E (2007) Integrin-mediated adhesion orients the spindle parallel to the substratum in an EB1-and myosin X-dependent manner. EMBO J 26: 1487-1498
59. Uchida KS, Takagaki K, Kumada K, Hirayama Y, Noda T, Hirota T (2009) Kinetochore stretching inactivates the spindle assembly checkpoint. J Cell Biol 184: 383-390
60. van Vugt MA, van de Weerdt BC, Vader G, Janssen H, Calafat J, Klompmaker R, Wolthuis RM, Medema RH (2004) 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: 36841-36854
61. Vigneron S, Prieto S, Bernis C, Labbe JC, Castro A, Lorca T (2004) Kinetochore localization of spindle checkpoint proteins: who controls whom? Mol Biol Cell 15: 4584-4596
62. Walston T, Tuskey C, Edgar L, Hawkins N, Ellis G, Bowerman B, Wood W, Hardin J (2004) Multiple Wnt signaling pathways converge to orient the mitotic spindle in early C. elegans embryos. Dev Cell 7: 831-841
63. Wharton KAJ (2003) Runnin' with the Dvl: proteins that associatewith Dsh/Dvl and their significance to Wnt signal transduction. Dev Biol 253: 1-17
64. Xue Y, Zhou F, Zhu M, Ahmed K, Chen G, Yao X (2005) GPS: a comprehensive www server for phosphorylation sites prediction. Nucleic Acids Res 33: W184-W187
65. Yamamoto H, Sakane H, Yamamoto H, Michiue T, Kikuchi A (2008) Wnt3a and Dkk1 regulate distinct internalization pathways of LRP6 to tune the activation of b-catenin signaling. Dev Cell 15: 37-48
66. Yasuda S, Oceguera-Yanez F, Kato T, Okamoto M, Yonemura S, Terada Y, Ishizaki T, Narumiya S (2004) Cdc42 and mDia3 regulate microtubule attachment to kinetochores. Nature 428: 767-771
67. Yu H (2007) Cdc20: a WD40 activator for a cell cycle degradation machine. Mol Cell 27: 3-16