Identification of a novel Wnt5a-CK1ε-Dvl2-Plk1-mediated primary cilia disassembly pathway

EMBO Journal

Volumn 31, Issue 14, 2012, Pages 3104-3117

  Lee, Kyung Ho ^a,e   Johmura, Yoshikazu ^a   Yu, Li Rong ^b   Park, Jung Eun ^a   Gao, Yuan ^b   Bang, Jeong K ^c   Zhou, Ming ^d   Veenstra, Timothy D ^d   Yeon Kim, Bo ^e   Lee, Kyung S ^a  

^a NATIONAL CANCER INSTITUTE   (United States)

^b NATIONAL CENTER FOR TOXICOLOGICAL RESEARCH   (United States)

^c Korea Basic Science Institute (KBSI)   (South Korea)

^d SAIC FREDERICK INC   (United States)

^e Korea Research Institute of Bioscience and Biotechnology (KRIBB)   (South Korea)

Author keywords

Cilia; CK1; Dvl2; Plk1; Wnt

Indexed keywords

ALPHA TUBULIN; AURORA A KINASE; BETA CATENIN; CASEIN KINASE IDELTA; CASEIN KINASE IEPSILON; DISHEVELLED 2; LIGAND; POLO LIKE KINASE 1; SMAD2 PROTEIN; SMAD3 PROTEIN; WNT5A PROTEIN;

ANIMAL CELL; ARTICLE; CELL CYCLE; CELLULAR DISTRIBUTION; COMPLEX FORMATION; CONTROLLED STUDY; EUKARYOTIC FLAGELLUM; INTERPHASE; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROTEIN DEGRADATION; PROTEIN LOCALIZATION; PROTEIN PHOSPHORYLATION; PROTEIN PROTEIN INTERACTION; REGULATORY MECHANISM;

ADAPTOR PROTEINS, SIGNAL TRANSDUCING; ANIMALS; CASEIN KINASE IEPSILON; CELL CYCLE PROTEINS; CILIA; HELA CELLS; HUMANS; L CELLS (CELL LINE); MICE; MULTIENZYME COMPLEXES; PHOSPHOPROTEINS; PROTEIN-SERINE-THREONINE KINASES; PROTO-ONCOGENE PROTEINS; WNT PROTEINS;

EID: 84864145764     PISSN: 02614189     EISSN: 14602075     Source Type: Journal    
DOI: 10.1038/emboj.2012.144     Document Type: Article

References (69)

1. Adams M, Smith UM, Logan CV, Johnson CA (2008) Recent advances in the molecular pathology, cell biology and genetics of ciliopathies. J Med Genet 45: 257-267 (Pubitemid 351685144)
2. Alieva IB, Gorgidze LA, Komarova YA, Chernobelskaya OA, Vorobjev IS (1999) Experimental model for studying the primary cilia in tissue culture cells. Membr Cell Biol 12: 895-905 (Pubitemid 29438496)
3. Angers S, Moon RT (2009) Proximal events in Wnt signal transduction. Nat Rev Mol Cell Biol 10: 468-477
4. Archambault V, Glover DM (2009) Polo-like kinases: conservation and divergence in their functions and regulation. Nat Rev Mol Cell Biol 10: 265-275
5. Barr FA, Sillje HH, Nigg EA (2004) Polo-like kinases and the orchestration of cell division. Nat Rev Mol Cell Biol 5: 429-440 (Pubitemid 38745493)
6. Berbari NF, O'Connor AK, Haycraft CJ, Yoder BK (2009) The primary cilium as a complex signaling center. Curr Biol 19: R526-R535
7. Bershteyn M, Atwood SX, Woo WM, Li M, Oro AE (2010) MIM and cortactin antagonism regulates ciliogenesis and hedgehog signaling. Dev Cell 19: 270-283
8. Bryja V, Schulte G, Rawal N, Grahn A, Arenas E (2007) Wnt-5a induces Dishevelled phosphorylation and dopaminergic differentiation via a CK1-dependent mechanism. J Cell Sci 120: 586-595 (Pubitemid 46437893)
9. Burkard ME, Randall CL, Larochelle S, Zhang C, Shokat KM, Fisher RP, Jallepalli PV (2007) Chemical genetics reveals the requirement for Polo-like kinase 1 activity in positioning RhoA and triggering cytokinesis in human cells. Proc Natl Acad Sci USA 104: 4383-4388 (Pubitemid 47186235)
10. Capelluto DG, Kutateladze TG, Habas R, Finkielstein CV, He X, Overduin M (2002) The DIX domain targets dishevelled to actin stress fibres and vesicular membranes. Nature 419: 726-729 (Pubitemid 35177958)
11. Cheng KY, Lowe ED, Sinclair J, Nigg EA, Johnson LN (2003) The crystal structure of the human polo-like kinase-1 polo box domain and its phospho-peptide complex. EMBO J 22: 5757-5768 (Pubitemid 37408815)
12. Clevers H (2006) Wnt/beta-catenin signaling in development and disease. Cell 127: 469-480
13. Corbit KC, Shyer AE, Dowdle WE, Gaulden J, Singla V, Chen MH, Chuang PT, Reiter JF (2008) Kif3a constrains beta-catenindependent Wnt signalling through dual ciliary and non-ciliary mechanisms. Nat Cell Biol 10: 70-76
14. Dahlberg CL, Nguyen EZ, Goodlett D, Kimelman D (2009) Interactions between casein kinase Iepsilon (CKIepsilon) and two substrates from disparate signaling pathways reveal mechanisms for substrate-kinase specificity. PLoS One 4: e4766
15. Davenport JR, Yoder BK (2005) An incredible decade for the primary cilium: a look at a once-forgotten organelle. Am J Physiol Renal Physiol 289: F1159-F1169 (Pubitemid 41681349)
16. Dawe HR, Farr H, Gull K (2007) Centriole/basal body morphogenesis and migration during ciliogenesis in animal cells. J Cell Sci 120: 7-15 (Pubitemid 46206644)
17. Elia AE, Rellos P, Haire L, Chao JW, Ivins FJ, Hoepker K, Mohammad D, Cantley LC, Smerdon SJ, Yaffe MB (2003) The molecular basis for phospho-dependent substrate targeting and regulation of Plks by the polo-box domain. Cell 115: 83-95 (Pubitemid 37255320)
18. Fliegauf M, Benzing T, Omran H (2007) When cilia go bad: cilia defects and ciliopathies. Nat Rev Mol Cell Biol 8: 880-893 (Pubitemid 47622564)
19. Gao C, Chen YG (2010) Dishevelled: The hub of Wnt signaling. Cell Signal 22: 717-727
20. 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)
21. Gerdes JM, Katsanis N (2008) Ciliary function and Wnt signal modulation. Curr Top Dev Biol 85: 175-195
22. Habas R, Dawid IB (2005) Dishevelled and Wnt signaling: is the nucleus the final frontier. J Biol 4: 2
23. Habas R, Kato Y, He X (2001) Wnt/Frizzled activation of Rho regulates vertebrate gastrulation and requires a novel Formin homology protein Daam1. Cell 107: 843-854 (Pubitemid 34084976)
24. He X (2008) Cilia put a brake on Wnt signalling. Nat Cell Biol 10: 11-13
25. Johmura Y, Soung NK, Park JE, Yu LR, Zhou M, Bang JK, Kim BY, Veenstra TD, Erikson RL, Lee KS (2011) Regulation of microtubule-based microtubule nucleation by mammalian polo-like kinase 1. Proc Natl Acad Sci USA 108: 11446-11451
26. Kang YH, Park J-E, Yu L-R, Soung N-K, Yun S-M, Bang JK, Seong Y-S, Yu H, Veenstra TD, Lee KS (2006) Self-regulation of Plk1 recruitment to the kinetochores is critical for chromosome congression and spindle checkpoint signaling. Mol Cell 24: 409-422 (Pubitemid 44754942)
27. 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
28. Kim J, Lee JE, Heynen-Genel S, Suyama E, Ono K, Lee K, Ideker T, Aza-Blanc P, Gleeson JG (2010) Functional genomic screen for modulators of ciliogenesis and cilium length. Nature 464: 1048-1051
29. Klimowski LK, Garcia BA, Shabanowitz J, Hunt DF, Virshup DM (2006) Site-specific casein kinase 1epsilon-dependent phosphorylation of Dishevelled modulates beta-catenin signaling. FEBS J 273: 4594-4602 (Pubitemid 44506903)
30. Knippschild U, Gocht A, Wolff S, Huber N, Löhler J, Stöter M (2005) The casein kinase 1 family: participation in multiple cellular processes in eukaryotes. Cell Signal 17: 675-689 (Pubitemid 40250168)
31. Law SF, Zhang YZ, Klein-Szanto AJ, Golemis EA (1998) Cell cycleregulated processing of HEF1 to multiple protein forms differentially targeted to multiple subcellular compartments. Mol Cell Biol 18: 3540-3551 (Pubitemid 28240526)
32. Lee KS, Yuan Y-L, Kuriyama R, Erikson RL (1995) Plk is an M-phasespecific protein kinase and interacts with a kinesin-like protein, CHO1/MKLP-1. Mol Cell Biol 15: 7143-7151
33. 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
34. Liu F, Park JE, Qian WJ, Lim D, Gräber M, Berg T, Yaffe MB, Lee KS, Burke TR (2011) Serendipitous alkylation of a Plk1 ligand uncovers a new binding channel. Nat Chem Biol 7: 595-601
35. Liu X, Elia AE, Law SF, Golemis EA, Farley J,Wang T (2000) A novel ability of Smad3 to regulate proteasomal degradation of a Cas family member HEF1. EMBO J 19: 6759-6769 (Pubitemid 32011669)
36. Logan CY, Nusse R (2004) The Wnt signaling pathway in development and disease. Annu Rev Cell Dev Biol 20: 781-810 (Pubitemid 39488658)
37. Macu°rek L, Lindqvist A, Lim D, Lampson MA, Klompmaker R, Freire R, Clouin C, Taylor SS, Yaffe MB, Medema RH (2008) Polo-like kinase-1 is activated by aurora A to promote checkpoint recovery. Nature 455: 119-123
38. Marlow F, Topczewski J, Sepich D, Solnica-Krezel L (2002) Zebrafish Rho kinase 2 acts downstream of Wnt11 to mediate cell polarity and effective convergence and extension movements. Curr Biol 12: 876-884 (Pubitemid 34689221)
39. McKay RM, Peters JM, Graff JM (2001) The casein kinase I family in Wnt signaling. Dev Biol 235: 388-396 (Pubitemid 32661179)
40. Michaud EJ, Yoder BK (2006) The primary cilium in cell signaling and cancer. Cancer Res 66: 6463-6467 (Pubitemid 44085596)
41. Miyamoto T, Porazinski S, Wang H, Borovina A, Ciruna B, Shimizu A, Kajii T, Kikuchi A, Furutani-Seiki M, Matsuura S (2011) Insufficiency of BUBR1, a mitotic spindle checkpoint regulator, causes impaired ciliogenesis in vertebrates. Hum Mol Genet 20: 2058-2070
42. Moon RT, Bowerman B, Boutros M, Perrimon N (2002) The promise and perils of Wnt signaling through beta-catenin. Science 296: 1644-1646 (Pubitemid 34579151)
43. Moon RT, Kohn AD, De Ferrari GV, Kaykas A (2004) WNTand betacatenin signalling: diseases and therapies. Nat Rev Genet 5: 691-701 (Pubitemid 39150127)
44. Nourry C, Maksumova L, Pang M, Liu X, Wang T (2004) Direct interaction between Smad3, APC10, CDH1 and HEF1 in proteasomal degradation of HEF1. BMC Cell Biol 5: 1-17
45. Nusse R (2005) Wnt signaling in disease and in development. Cell Res 15: 28-32 (Pubitemid 41653961)
46. Pan J, Snell W (2007) The primary cilium: keeper of the key to cell division. Cell 129: 1255-1257 (Pubitemid 46970712)
47. Park J-E, Li L, Park J, Knecht R, Strebhardt K, Yuspa SH, Lee KS (2009) Direct quantification of polo-like kinase 1 activity in cells and tissues using a highly sensitive and specific ELISA assay. Proc Natl Acad Sci USA 106: 1725-1730
48. Park JE, Soung NK, Johmura Y, Kang YH, Liao C, Lee KH, Park CH, Nicklaus MC, Lee KS (2010) Polo-box domain: a versatile mediator of polo-like kinase function. Cell Mol Life Sci 67: 1957-1970
49. Park TJ, Mitchell BJ, Abitua PB, Kintner C, Wallingford JB (2008) Dishevelled controls apical docking and planar polarization of basal bodies in ciliated epithelial cells. Nat Genet 40: 871-879 (Pubitemid 351913644)
50. Petronczki M, Lénárt P, Peters JM (2008) Polo on the Rise-from Mitotic Entry to Cytokinesis with Plk1. Dev Cell 14: 646-659 (Pubitemid 351622626)
51. Pitaval A, Tseng Q, Bornens M, Théry M (2010) Cell shape and contractility regulate ciliogenesis in cell cycle-arrested cells. J Cell Biol 191: 303-312
52. Plotnikova OV, Golemis EA, Pugacheva EN (2008) Cell cycledependent ciliogenesis and cancer. Cancer Res 68: 2058-2061
53. Price MA (2006) CKI, there's more than one: casein kinase I family members in Wnt and Hedgehog signaling. Genes Dev 20: 399-410
54. Pugacheva EN, Jablonski SA, Hartman TR, Henske EP, Golemis EA (2007) HEF1-dependent Aurora A activation induces disassembly of the primary cilium. Cell 129: 1351-1363 (Pubitemid 46962087)
55. Quarmby LM, Parker JD (2005) Cilia and the cell cycle? J Cell Biol 169: 707-710 (Pubitemid 41002875)
56. Santos N, Reiter JF (2008) Building it up and taking it down: the regulation of vertebrate ciliogenesis. Dev Dyn 237: 1972-1981
57. Seeley ES, Nachury MV (2010) The perennial organelle: assembly and disassembly of the primary cilium. J Cell Sci 123: 511-518
58. Seki A, Coppinger JA, Jang CY, Yates JR, Fang G (2008) Bora and the kinase Aurora A cooperatively activate the kinase Plk1 and control mitotic entry. Science 320: 1655-1658 (Pubitemid 351931258)
59. Sharma N, Berbari NF, Yoder BK (2008) Ciliary dysfunction in developmental abnormalities and diseases. Curr Top Dev Biol 85: 371-427
60. Soung NK, Park JE, Yu LR, Lee KH, Lee JM, Bang JK, Veenstra TD, Rhee K, Lee KS (2009) Plk1-dependent and-independent roles of an ODF2, splice variant, hCenexin1, at the centrosome of somatic cells. Dev Cell 16: 539-550
61. Strebhardt K, Ullrich A (2006) Targeting polo-like kinase 1 for cancer therapy. Nat Rev Cancer 6: 321-330
62. Tillement V, Lajoie-Mazenc I, Casanova A, Froment C, Penary M, Tovar D, Marquez R, Monsarrat B, Favre G, Pradines A (2008) Phosphorylation of RhoB by CK1 impedes actin stress fiber organization and epidermal growth factor receptor stabilization. Exp Cell Res 314: 2811-2821
63. van de Weerdt BC, Medema RH (2006) Polo-like kinases: a team in control of the division. Cell Cycle 5: 853-864 (Pubitemid 44145580)
64. Veeman MT, Axelrod JD, Moon RT (2003) A second canon. Functions and mechanisms of beta-catenin-independent Wnt signaling. Dev Cell 5: 367-377 (Pubitemid 37107667)
65. Warner DR, Greene RM, Pisano MM (2005) Interaction between Smad 3 and Dishevelled in murine embryonic craniofacial mesenchymal cells. Orthod Craniofac Res 8: 123-130
66. Warner DR, Pisano MM, Roberts EA, Greene RM (2003) Identification of three novel Smad binding proteins involved in cell polarity. FEBS Lett 539: 167-173 (Pubitemid 36351306)
67. Yun SM, Moulaei T, Lim D, Bang JK, Park JE, Shenoy SR, Liu F, Kang YH, Liao C, Soung NK, Lee S, Yoon DY, Lim Y, Lee DH, Otaka A, Appella E, McMahon JB, Nicklaus MC, Burke Jr TR, Yaffe MB et al (2009) Structural and functional analyses of minimal phosphopeptides targeting the polo-box domain of polo-like kinase 1. Nat Struct Mol Biol 16: 876-882
68. Zeng K, Bastos RN, Barr FA, Gruneberg U (2010) Protein phosphatase 6 regulates mitotic spindle formation by controlling the T-loop phosphorylation state of Aurora A bound to its activator TPX2. J Cell Biol 191: 1315-1332
69. Zhang X, Zhu J, Yang GY,Wang QJ, Qian L, Chen YM, Chen F, Tao Y, Hu HS, Wang T., Luo ZG (2007) Dishevelled promotes axon differentiation by regulating atypical protein kinase C. Nat Cell Biol 9: 743-754 (Pubitemid 47019461)