Nek2 phosphorylates and stabilizes ß-catenin at mitotic centrosomes downstream of Plk1

Molecular Biology of the Cell

Volumn 25, Issue 7, 2014, Pages 977-991

  Mbom, Bertrade C ^a   Siemers, Kathleen A ^a   Ostrowski, Maggie A ^b   Nelson, W James ^a,c   Barth, Angela I M ^a  

^a STANFORD UNIVERSITY   (United States)

^b Stanford University   (United States)

^c STANFORD UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ANTIBODY; BETA CATENIN; GLYCOGEN SYNTHASE KINASE 3BETA; POLO LIKE KINASE 1; PROTEIN KINASE; PROTEIN NEK2; UBIQUITIN PROTEIN LIGASE E3; UNCLASSIFIED DRUG; CASEIN KINASE I; CELL CYCLE PROTEIN; GLYCOGEN SYNTHASE KINASE 3; GLYCOGEN SYNTHASE KINASE 3 BETA; NEK2 PROTEIN, HUMAN; ONCOPROTEIN; POLO-LIKE KINASE 1; PROTEIN SERINE THREONINE KINASE; SERINE;

AMINO TERMINAL SEQUENCE; ARTICLE; BIOACCUMULATION; CELL ADHESION; CENTROSOME; CONTROLLED STUDY; HUMAN; HUMAN CELL; IN VITRO STUDY; MITOSIS; PRIORITY JOURNAL; PROTEIN DEGRADATION; PROTEIN PHOSPHORYLATION; PROTEIN STABILITY; REGULATORY MECHANISM; SIGNAL TRANSDUCTION; UBIQUITINATION; GENE DELETION; HCT116 CELL LINE; HEK293 CELL LINE; METABOLISM; PHOSPHORYLATION; SPINDLE APPARATUS;

BETA CATENIN; CASEIN KINASE I; CELL CYCLE PROTEINS; CENTROSOME; GLYCOGEN SYNTHASE KINASE 3; HCT116 CELLS; HEK293 CELLS; HUMANS; MITOSIS; PHOSPHORYLATION; PROTEIN STABILITY; PROTEIN-SERINE-THREONINE KINASES; PROTO-ONCOGENE PROTEINS; SEQUENCE DELETION; SERINE; SPINDLE APPARATUS;

EID: 84898756756     PISSN: 10591524     EISSN: 19394586     Source Type: Journal    
DOI: 10.1091/mbc.E13-06-0349     Document Type: Article

References (61)

1. Aberle H, Butz S, Stappert J, Weissig H, Kemler R, Hoschuetzky H (1994). Assembly of the cadherin-catenin complex in vitro with recombinant proteins. J Cell Sci 107, 3655-3663.
2. Arias AM, Brown AM, Brennan K (1999). Wnt signalling: pathway or network? Curr Opin Genet Dev 9, 447-454. (Pubitemid 29385343)
3. Azimzadeh J, Bornens M (2007). Structure and duplication of the centrosome. J Cell Sci 120, 2139-2142. (Pubitemid 47074119)
4. Bahe S, Stierhof YD, Wilkinson CJ, Leiss F, Nigg EA (2005). Rootletin forms centriole-associated filaments and functions in centrosome cohesion. J Cell Biol 171, 27-33. (Pubitemid 41434599)
5. Bahmanyar S, Guiney EL, Hatch EM, Nelson WJ, Barth AI (2010). Formation of extra centrosomal structures is dependent on beta-catenin. J Cell Sci 123, 3125-3135.
6. Bahmanyar S, Kaplan DD, Deluca JG, Giddings TH Jr, O'Toole ET, Winey M, Salmon ED, Casey PJ, Nelson WJ, Barth AI (2008). beta-Catenin is a Nek2 substrate involved in centrosome separation. Genes Dev 22, 91-105.
7. Baker RT, Catanzariti AM, Karunasekara Y, Soboleva TA, Sharwood R, Whitney S, Board PG (2005). Using deubiquitylating enzymes as research tools. Methods Enzymol 398, 540-554. (Pubitemid 41578912)
8. Barth AI, Stewart DB, Nelson WJ (1999). T cell factor-activated transcription is not sufficient to induce anchorage-independent growth of epithelial cells expressing mutant beta-catenin. Proc Natl Acad Sci USA 96, 4947-4952. (Pubitemid 29214516)
9. Bek S, Kemler R (2002). Protein kinase CKII regulates the interaction of beta-catenin with alpha-catenin and its protein stability. J Cell Sci 115, 4743-4753. (Pubitemid 36054629)
10. Bornens M, Paintrand M, Berges J, Marty MC, Karsenti E (1987). Structural and chemical characterization of isolated centrosomes. Cell Motil Cytoskeleton 8, 238-249.
11. Chang P, Stearns T (2000). Delta-tubulin and epsilon-tubulin: two new human centrosomal tubulins reveal new aspects of centrosome structure and function. Nat Cell Biol 2, 30-35.
12. Chilov D, Sinjushina N, Rita H, Taketo MM, Makela TP, Partanen J (2011). Phosphorylated beta-catenin localizes to centrosomes of neuronal progenitors and is required for cell polarity and neurogenesis in developing midbrain. Dev Biol 357, 259-268.
13. Deng L, Wang C, Spencer E, Yang L, Braun A, You J, Slaughter C, Pickart C, Chen ZJ (2000). Activation of the IkappaB kinase complex by TRAF6 requires a dimeric ubiquitin-conjugating enzyme complex and a unique polyubiquitin chain. Cell 103, 351-361.
14. Eto M, Elliott E, Prickett TD, Brautigan DL (2002). Inhibitor-2 regulates protein phosphatase-1 complexed with NimA-related kinase to induce centrosome separation. J Biol Chem 277, 44013-44020. (Pubitemid 36157827)
15. Faragher AJ, Fry AM (2003). Nek2A kinase stimulates centrosome disjunction and is required for formation of bipolar mitotic spindles. Mol Biol Cell 14, 2876-2889. (Pubitemid 36871528)
16. Fry AM (2002). The Nek2 protein kinase: A novel regulator of centrosome structure. Oncogene 21, 6184-6194.
17. Fry AM, Mayor T, Meraldi P, Stierhof YD, Tanaka K, Nigg EA (1998). C-Nap1, a novel centrosomal coiled-coil protein and candidate substrate of the cell cycle-regulated protein kinase Nek2. J Cell Biol 141, 1563-1574. (Pubitemid 28309171)
18. Fujioka T, Takebayashi Y, Ito M, Uchida T (2000). Nek2 expression and localization in porcine oocyte during maturation. Biochem Biophys Res Commun 279, 799-802. (Pubitemid 32042858)
19. Gao ZH, Seeling JM, Hill V, Yochum A, Virshup DM (2002). Casein kinase I phosphorylates and destabilizes the beta-catenin degradation complex. Proc Natl Acad Sci USA 99, 1182-1187. (Pubitemid 34136467)
20. Hadjihannas MV, Bruckner M, Behrens J (2010). Conductin/axin2 and Wnt signalling regulates centrosome cohesion. EMBO Rep 11, 317-324.
21. 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 USA 103, 10747-10752. (Pubitemid 44078047)
22. Ha Kim Y, Yeol Choi J, Jeong Y, Wolgemuth DJ, Rhee K (2002). Nek2 localizes to multiple sites in mitotic cells, suggesting its involvement inmultiple cellular functions during the cell cycle. Biochem Biophys Res Commun 290, 730-736. (Pubitemid 34687501)
23. Haren L, Stearns T, Luders J (2009). Plk1-dependent recruitment of gamma-tubulin complexes to mitotic centrosomes involves multiple PCM components. PLoS One 4, e5976.
24. Harris ES, Nelson WJ (2010). Adenomatous polyposis coli regulates endothelial cell migration independent of roles in beta-catenin signaling and cell-cell adhesion. Mol Biol Cell 21, 2611-2623.
25. Hart M et al. (1999). The F-box protein beta-TrCP associates with phosphorylated beta-catenin and regulates its activity in the cell. Curr Biol 9, 207-210. (Pubitemid 29120385)
26. Hino S, Tanji C, Nakayama KI, Kikuchi A (2005). Phosphorylation of beta-catenin by cyclic AMP-dependent protein kinase stabilizes beta-catenin through inhibition of its ubiquitination. Mol Cell Biol 25, 9063-9072. (Pubitemid 41429094)
27. Huang P, Senga T, Hamaguchi M (2007). A novel role of phospho-beta-catenin in microtubule regrowth at centrosome. Oncogene 26, 4357-4371. (Pubitemid 47014458)
28. Huber AH, Nelson WJ, Weis WI (1997). Three-dimensional structure of the armadillo repeat region of beta-catenin. Cell 90, 871-882.
29. Huelsken J, Behrens J (2002). The Wnt signalling pathway. J Cell Sci 115, 3977-3978. (Pubitemid 35446796)
30. Kaplan DD, Meigs TE, Kelly P, Casey PJ (2004). Identification of a role for beta-catenin in the establishment of a bipolar mitotic spindle. J Biol Chem 279, 10829-10832. (Pubitemid 38401570)
31. Kapoor TM, Mayer TU, Coughlin ML, Mitchison TJ (2000). Probing spindle assembly mechanisms with monastrol, a small molecule inhibitor of the mitotic kinesin, Eg5. J Cell Biol 150, 975-988.
32. Kim EA, Kim JE, Sung KS, Choi DW, Lee BJ, Choi CY (2010). Homeodomain-interacting protein kinase 2 (HIPK2) targets beta-catenin for phosphorylation and proteasomal degradation. Biochem Biophys Res Commun 394, 966-971.
33. Kim JS, Crooks H, Dracheva T, Nishanian TG, Singh B, Jen J, Waldman T (2002a). Oncogenic beta-catenin is required for bone morphogenetic protein 4 expression in human cancer cells. Cancer Res 62, 2744-2748. (Pubitemid 34525754)
34. Kim JS, Crooks H, Foxworth A, Waldman T (2002b). Proof-of-principle: oncogenic beta-catenin is a valid molecular target for the development of pharmacological inhibitors. Mol Cancer Ther 1, 1355-1359.
35. Kuriyama R, Bettencourt-Dias M, Hoffmann I, Arnold M, Sandvig L (2009). Gamma-tubulin-containing abnormal centrioles are induced by insufficient Plk4 in human HCT116 colorectal cancer cells. J Cell Sci 122, 2014-2023.
36. Lenart 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 polo-like kinase 1. Curr Biol 17, 304-315.
37. Liu C, Li Y, Semenov M, Han C, Baeg GH, Tan Y, Zhang Z, Lin X, He X (2002). Control of beta-catenin phosphorylation/degradation by a dual-kinase mechanism. Cell 108, 837-847. (Pubitemid 34327534)
38. Logan CY, Nusse R (2004). The Wnt signaling pathway in development and disease. Annu Rev Cell Dev Biol 20, 781-810. (Pubitemid 39488658)
39. Louie RK, Bahmanyar S, Siemers KA, Votin V, Chang P, Stearns T, Nelson WJ, Barth AI (2004). Adenomatous polyposis coli and EB1 localize in close proximity of the mother centriole and EB1 is a functional component of centrosomes. J Cell Sci 117, 1117-1128. (Pubitemid 38456093)
40. MacLaine NJ, Oster B, Bundgaard B, Fraser JA, Buckner C, Lazo PA, Meek DW, Hollsberg P, Hupp TR (2008). A central role for CK1 in catalyzing phosphorylation of the p53 transactivation domain at serine 20 after HHV-6B viral infection. J Biol Chem 283, 28563-28573.
41. Mardin BR, Agircan FG, Lange C, Schiebel E (2011). Plk1 controls the Nek2A-PP1gamma antagonism in centrosome disjunction. Curr Biol 21, 1145-1151.
42. Mardin BR, Lange C, Baxter JE, Hardy T, Scholz SR, Fry AM, Schiebel E (2010). Components of the Hippo pathway cooperate with Nek2 kinase to regulate centrosome disjunction. Nat Cell Biol 12, 1166-1176.
43. Meijer L et al. (2003). GSK-3-selective inhibitors derived from Tyrian purple indirubins. Chem Biol 10, 1255-1266. (Pubitemid 38050973)
44. Merle P et al. (2005). Oncogenic role of the frizzled-7/beta-catenin pathway in hepatocellular carcinoma. J Hepatol 43, 854-862. (Pubitemid 41414512)
45. Morin PJ, Sparks AB, Korinek V, Barker N, Clevers H, Vogelstein B, Kinzler KW (1997). Activation of beta-catenin-Tcf signaling in colon cancer by mutations in beta-catenin or APC. Science 275, 1787-1790. (Pubitemid 27136715)
46. Nathke IS, Hinck L, Swedlow JR, Papkoff J, Nelson WJ (1994). Defining interactions and distributions of cadherin and catenin complexes in polarized epithelial cells. J Cell Biol 125, 1341-1352. (Pubitemid 24189537)
47. Nelson WJ, Nusse R (2004). Convergence of Wnt, beta-catenin, and cadherin pathways. Science 303, 1483-1487. (Pubitemid 38314410)
48. Ohta T, Xiong Y (2001). Phosphorylation- and Skp1-independent in vitro ubiquitination of E2F1 by multiple ROC-cullin ligases. Cancer Res 61, 1347-1353. (Pubitemid 34292554)
49. Orford K, Crockett C, Jensen JP, Weissman AM, Byers SW (1997). Serine phosphorylation-regulated ubiquitination and degradation of beta-catenin. J Biol Chem 272, 24735-24738. (Pubitemid 27415637)
50. Piedra J, Martinez D, Castano J, Miravet S, Dunach M, de Herreros AG (2001). Regulation of beta-catenin structure and activity by tyrosine phosphorylation. J Biol Chem 276, 20436-20443.
51. Piedra J, Miravet S, Castano J, Palmer HG, Heisterkamp N, Garcia de Herreros A, Dunach M (2003). p120 catenin-associated Fer and Fyn tyrosine kinases regulate beta-catenin Tyr-142 phosphorylation and beta-catenin-alpha- catenin Interaction. Mol Cell Biol 23, 2287-2297. (Pubitemid 36351012)
52. Quarmby LM, Mahjoub MR (2005). Caught Nek-ing: cilia and centrioles. J Cell Sci 118, 5161-5169. (Pubitemid 41819580)
53. Roura S, Miravet S, Piedra J, Garcia de Herreros A, Dunach M (1999). Regulation of E-cadherin/catenin association by tyrosine phosphorylation. J Biol Chem 274, 36734-36740.
54. Steegmaier M et al. (2007). BI 2536, a potent and selective inhibitor of polo-like kinase 1, inhibits tumor growth in vivo. Curr Biol 17, 316-322. (Pubitemid 46241881)
55. Thotala DK, Hallahan DE, Yazlovitskaya EM (2008). Inhibition of glycogen synthase kinase 3 beta attenuates neurocognitive dysfunction resulting from cranial irradiation. Cancer Res 68, 5859-5868.
56. Vassilev LT, Tovar C, Chen S, Knezevic D, Zhao X, Sun H, Heimbrook DC, Chen L (2006). Selective small-molecule inhibitor reveals critical mitotic functions of human CDK1. Proc Natl Acad Sci USA 103, 10660-10665. (Pubitemid 44078033)
57. Wang G, Chen Q, Zhang X, Zhang B, Zhuo X, Liu J, Jiang Q, Zhang C (2013). PCM1 recruits Plk1 to pericentriolar matrix to promote primary cilia disassembly before mitotic entry. J Cell Sci 126, 1355-1365.
58. Weis WI, Nelson WJ (2006). Re-solving the cadherin-catenin-actin conundrum. J Biol Chem 281, 35593-35597. (Pubitemid 46043241)
59. White MC, Quarmby LM (2008). The NIMA-family kinase, Nek1 affects the stability of centrosomes and ciliogenesis. BMC Cell Biol 9, 29.
60. Wu G, Xu G, Schulman BA, Jeffrey PD, Harper JW, Pavletich NP (2003). Structure of a beta-TrCP1-Skp1-beta-catenin complex: destruction motif binding and lysine specificity of the SCF(beta-TrCP1) ubiquitin ligase. Mol Cell 11, 1445-1456. (Pubitemid 36776532)
61. Zhang F, Phiel CJ, Spece L, Gurvich N, Klein PS (2003). Inhibitory phosphorylation of glycogen synthase kinase-3 (GSK-3) in response to lithium. Evidence for autoregulation of GSK-3. J Biol Chem 278, 33067-33077. (Pubitemid 37055753)