Wnt-mediated protein stabilization ensures proper mitotic microtubule assembly and chromosome segregation

EMBO Reports

Volumn 16, Issue 4, 2015, Pages 490-499

  Stolz, Ailine ^a   Neufeld, Kim ^a   Ertych, Norman ^a   Bastians, Holger ^a  

^a UNIVERSITY MEDICAL CENTER GÖTTINGEN   (Germany)

Author keywords

aneuploidy; chromosome segregation; mitosis; Wnt signaling

Indexed keywords

BETA CATENIN; DICKKOPF 1 PROTEIN; DISHEVELLED 2; LOW DENSITY LIPOPROTEIN RECEPTOR RELATED PROTEIN 5; LOW DENSITY LIPOPROTEIN RECEPTOR RELATED PROTEIN 6; WNT PROTEIN; BASIC HELIX LOOP HELIX LEUCINE ZIPPER TRANSCRIPTION FACTOR; CTNNB1 PROTEIN, HUMAN; DISHEVELLED PROTEINS; DKK1 PROTEIN, HUMAN; LOW DENSITY LIPOPROTEIN RECEPTOR RELATED PROTEIN; MAP6 PROTEIN, HUMAN; MICROTUBULE ASSOCIATED PROTEIN; PHOSPHOPROTEIN; RECOMBINANT PROTEIN; SIGNAL PEPTIDE; SIGNAL TRANSDUCING ADAPTOR PROTEIN; SMALL INTERFERING RNA; TCF4 PROTEIN, HUMAN; TRANSCRIPTION FACTOR; WNT3A PROTEIN; WNT3A PROTEIN, HUMAN;

ANEUPLOIDY; ARTICLE; CELL CLONE; CELL CYCLE PROGRESSION; CELL CYCLE REGULATION; CELL PROLIFERATION; CENTROMERE; CHROMOSOME; CHROMOSOME SEGREGATION; CONTROLLED STUDY; GENE REPRESSION; GENETIC TRANSCRIPTION; HCT116 CELL LINE; HUMAN; HUMAN CELL; KARYOTYPE; METAPHASE; MICROTUBULE ASSEMBLY; MITOSIS; MITOSIS SPINDLE; PRIORITY JOURNAL; PROTEIN DEGRADATION; PROTEIN STABILITY; SIGNAL TRANSDUCTION; SOMATIC CELL; ANTAGONISTS AND INHIBITORS; GENE EXPRESSION REGULATION; GENETICS; METABOLISM; MICROTUBULE; SPINDLE APPARATUS; ULTRASTRUCTURE; WNT SIGNALING PATHWAY;

ADAPTOR PROTEINS, SIGNAL TRANSDUCING; BASIC HELIX-LOOP-HELIX LEUCINE ZIPPER TRANSCRIPTION FACTORS; BETA CATENIN; CHROMOSOME SEGREGATION; GENE EXPRESSION REGULATION; HCT116 CELLS; HUMANS; INTERCELLULAR SIGNALING PEPTIDES AND PROTEINS; LDL-RECEPTOR RELATED PROTEINS; MICROTUBULE-ASSOCIATED PROTEINS; MICROTUBULES; MITOSIS; PHOSPHOPROTEINS; PROTEIN STABILITY; RECOMBINANT PROTEINS; RNA, SMALL INTERFERING; SPINDLE APPARATUS; TRANSCRIPTION FACTORS; WNT SIGNALING PATHWAY; WNT3A PROTEIN;

EID: 84926256399     PISSN: 1469221X     EISSN: 14693178     Source Type: Journal    
DOI: 10.15252/embr.201439410     Document Type: Article

References (39)

1. Clevers H, Nusse R, (2012) Wnt/beta-catenin signaling and disease. Cell 149: 1192-1205
2. Liu CC, Tsai CW, Deak F, Rogers J, Penuliar M, Sung YM, Maher JN, Fu Y, Li X, Xu H, et al, (2014) Deficiency in LRP6-mediated Wnt signaling contributes to synaptic abnormalities and amyloid pathology in Alzheimer's disease. Neuron 84: 63-77
3. Inestrosa CN, Varela-Nallar L, Grabowski PC, Colombres M, (2007) Synaptotoxicity in Alzheimer's disease: the Wnt signaling pathway as a molecular target. IUBMB Life 59: 316-321
4. Bilic J, Huang YL, Davidson G, Zimmermann T, Cruciat CM, Bienz M, Niehrs C, (2007) Wnt induces LRP6 signalosomes and promotes dishevelled-dependent LRP6 phosphorylation. Science 316: 1619-1622
5. Davidson G, Wu W, Shen J, Bilic J, Fenger U, Stannek P, Glinka A, Niehrs C, (2005) Casein kinase 1 gamma couples Wnt receptor activation to cytoplasmic signal transduction. Nature 438: 867-872
6. Zeng X, Tamai K, Doble B, Li S, Huang H, Habas R, Okamura H, Woodgett J, He X, (2005) A dual-kinase mechanism for Wnt co-receptor phosphorylation and activation. Nature 438: 873-877
7. Mi K, Dolan JP, Johnson VG, (2006) The low density lipoprotein receptor-related protein 6 interacts with glycogen synthase kinase 3 and attenuates activity. J Biol Chem 281: 4787-4794
8. Piao S, Lee SH, Kim H, Yum S, Stamos JL, Xu Y, Lee SJ, Lee J, Oh S, Han JK, et al, (2008) Direct inhibition of GSK3beta by the phosphorylated cytoplasmic domain of LRP6 in Wnt/beta-catenin signaling. PLoS ONE 3: e4046
9. Taelman VF, Dobrowolski R, Plouhinec JL, Fuentealba LC, Vorwald PP, Gumper I, Sabatini DD, De Robertis EM, (2010) Wnt signaling requires sequestration of glycogen synthase kinase 3 inside multivesicular endosomes. Cell 143: 1136-1148
10. Vinyoles M, Del Valle-Perez B, Curto J, Vinas-Castells R, Alba-Castellon L, de Garcia Herreros A, Dunach M, (2014) Multivesicular GSK3 sequestration upon Wnt signaling is controlled by p120-catenin/cadherin interaction with LRP5/6. Mol Cell 53: 444-457
11. He TC, Sparks AB, Rago C, Hermeking H, Zawel L, da Costa LT, Morin PJ, Vogelstein B, Kinzler KW, (1998) Identification of c-MYC as a target of the APC pathway. Science 281: 1509-1512
12. Tetsu O, McCormick F, (1999) Beta-catenin regulates expression of cyclin D1 in colon carcinoma cells. Nature 398: 422-426
13. Niehrs C, Acebron PS, (2012) Mitotic and mitogenic Wnt signalling. EMBO J 31: 2705-2713
14. 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
15. Hadjihannas MV, Bruckner M, Jerchow B, Birchmeier W, Dietmaier W, Behrens J, (2006) Aberrant Wnt/beta-catenin signaling can induce chromosomal instability in colon cancer. Proc Natl Acad Sci U S A 103: 10747-10752
16. Olmeda D, Castel S, Vilaro S, Cano A, (2003) Beta-catenin regulation during the cell cycle: implications in G2/M and apoptosis. Mol Biol Cell 14: 2844-2860
17. Kim GN, Xu C, Gumbiner MB, (2009) Identification of targets of the Wnt pathway destruction complex in addition to beta-catenin. Proc Natl Acad Sci U S A 106: 5165-5170
18. Acebron SP, Karaulanov E, Berger BS, Huang YL, Niehrs C, (2014) Mitotic wnt signaling promotes protein stabilization and regulates cell size. Mol Cell 54: 663-674
19. Hadjihannas VM, Behrens J, (2006) CIN By WNT: growth pathways, mitotic control and chromosomal instability in cancer. Cell Cycle 5: 2077-2081
20. Fodde R, Kuipers J, Rosenberg C, Smits R, Kielman M, Gaspar C, van Es JH, Breukel C, Wiegant J, Giles RH, et al, (2001) Mutations in the APC tumour suppressor gene cause chromosomal instability. Nat Cell Biol 3: 433-438
21. Kikuchi K, Niikura Y, Kitagawa K, Kikuchi A, (2010) Dishevelled, a Wnt signalling component, is involved in mitotic progression in cooperation with Plk1. EMBO J 29: 3470-3483
22. Kaplan KB, Burds AA, Swedlow JR, Bekir SS, Sorger PK, Nathke IS, (2001) A role for the Adenomatous Polyposis Coli protein in chromosome segregation. Nat Cell Biol 3: 429-432
23. Mbom CB, Nelson JW, Barth A, (2013) beta-catenin at the centrosome: discrete pools of beta-catenin communicate during mitosis and may co-ordinate centrosome functions and cell cycle progression. BioEssays 35: 804-809
24. Kaplan DD, Meigs ET, Kelly P, Casey JP, (2004) Identification of a role for beta-catenin in the establishment of a bipolar mitotic spindle. J Biol Chem 279: 10829-10832
25. Hadjihannas VM, Bruckner M, Behrens J, (2010) Conductin/axin2 and Wnt signalling regulates centrosome cohesion. EMBO Rep 11: 317-324
26. Oromendia BA, Amon A, (2014) Aneuploidy: implications for protein homeostasis and disease. Dis Model Mech 7: 15-20
27. Thompson LS, Bakhoum FS, Compton AD, (2010) Mechanisms of chromosomal instability. Curr Biol 20: R285-R295
28. Ertych N, Stolz A, Stenzinger A, Weichert W, Kaulfuß S, Burfeind P, Aigner A, Wordeman L, Bastians H, (2014) Increased microtubule assembly rates influence chromosomal instability in colorectal cancer. Nat Cell Biol 16: 779-791
29. Cimini D, (2008) Merotelic kinetochore orientation, aneuploidy, and cancer. Biochim Biophys Acta 1786: 32-40
30. Stepanova T, Slemmer J, Hoogenraad CC, Lansbergen G, Dortland B, De Zeeuw CI, Grosveld F, van Cappellen G, Akhmanova A, Galjart N, (2003) Visualization of microtubule growth in cultured neurons via the use of EB3-GFP (end-binding protein 3-green fluorescent protein). J Neurosci 23: 2655-2664
31. Brouhard GJ, Stear JH, Noetzel TL, Al-Bassam J, Kinoshita K, Harrison SC, Howard J, Hyman AA, (2008) XMAP215 is a processive microtubule polymerase. Cell 132: 79-88
32. Niehrs C, (2006) Function and biological roles of the Dickkopf family of Wnt modulators. Oncogene 25: 7469-7481
33. Silkworth TW, Cimini D, (2012) Transient defects of mitotic spindle geometry and chromosome segregation errors. Cell Div 7: 19
34. Gregan J, Polakova S, Zhang L, Tolic-Norrelykke IM, Cimini D, (2011) Merotelic kinetochore attachment: causes and effects. Trends Cell Biol 21: 374-381
35. Bakhoum FS, Genovese G, Compton AD, (2009) Deviant kinetochore microtubule dynamics underlie chromosomal instability. Curr Biol 19: 1937-1942
36. Lengauer C, Kinzler WK, Vogelstein B, (1997) Genetic instability in colorectal cancers. Nature 386: 623-627
37. Knutsen T, Padilla-Nash HM, Wangsa D, Barenboim-Stapleton L, Camps J, McNeil N, Difilippantonio MJ, Ried T, (2010) Definitive molecular cytogenetic characterization of 15 colorectal cancer cell lines. Genes Chromosom Cancer 49: 204-223
38. Caricasole A, Copani A, Caraci F, Aronica E, Rozemuller AJ, Caruso A, Storto M, Gaviraghi G, Terstappen GC, Nicoletti F, (2004) Induction of Dickkopf-1, a negative modulator of the Wnt pathway, is associated with neuronal degeneration in Alzheimer's brain. J Neurosci 24: 6021-6027
39. Llorens-Martin M, Jurado J, Hernandez F, Avila J, (2014) GSK-3beta, a pivotal kinase in Alzheimer disease. Front Mol Neurosci 7: 46