Cell Cycle Control of Wnt Receptor Activation

Developmental Cell

Volumn 17, Issue 6, 2009, Pages 788-799

  Davidson, Gary ^a,b   Shen, Jinlong ^a   Huang, Ya Lin ^a   Su, Yi ^b   Karaulanov, Emil ^a   Bartscherer, Kerstin ^a   Hassler, Christine ^a   Stannek, Peter ^a   Boutros, Michael ^a   Niehrs, Christof ^a  

^a GERMAN CANCER RESEARCH CENTER DKFZ   (Germany)

^b KARLSRUHE INSTITUTE OF TECHNOLOGY   (Germany)

Author keywords

CELLCYCLE; DEVBIO; SIGNALING

Indexed keywords

BETA CATENIN; COP9 SIGNALOSOME; CYCLIN DEPENDENT KINASE; CYCLIN DEPENDENT KINASE L63; CYCLIN Y; CYCLINE; FRIZZLED PROTEIN; LOW DENSITY LIPOPROTEIN RECEPTOR RELATED PROTEIN 5; LOW DENSITY LIPOPROTEIN RECEPTOR RELATED PROTEIN 6; PROLINE; PROTEIN TYROSINE PHOSPHATASE; SERINE; UNCLASSIFIED DRUG;

ANIMAL CELL; ANIMAL EMBRYO; ARTICLE; BINDING AFFINITY; CELL CYCLE ARREST; CELL CYCLE G2 PHASE; CELL CYCLE M PHASE; CELL CYCLE REGULATION; COMPLEX FORMATION; CONTROLLED STUDY; EMBRYO; EMBRYO DEVELOPMENT; EMBRYO PATTERN FORMATION; ENZYME ANALYSIS; HUMAN; HUMAN CELL; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROTEIN FUNCTION; PROTEIN PHOSPHORYLATION; SIGNAL TRANSDUCTION; XENOPUS;

ANIMALS; CELL CYCLE; CELL LINE; CYCLINS; DROSOPHILA; HUMANS; PHOSPHORYLATION; PROTEOMICS; RECEPTORS, LDL; WNT PROTEINS; XENOPUS LAEVIS;

VERTEBRATA;

EID: 71649108294     PISSN: 15345807     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.devcel.2009.11.006     Document Type: Article

References (82)

1. Alvarez B., Martinez A.C., Burgering B.M., and Carrera A.C. Forkhead transcription factors contribute to execution of the mitotic programme in mammals. Nature 413 (2001) 744-747
2. Aoki K., and Taketo M.M. Adenomatous polyposis coli (APC): a multi-functional tumor suppressor gene. J. Cell Sci. 120 (2007) 3327-3335
3. Arziman Z., Horn T., and Boutros M. E-RNAi: a web application to design optimized RNAi constructs. Nucleic Acids Res. 33 (2005) W582-W588
4. Bahmanyar S., Kaplan D.D., Deluca J.G., Giddings Jr. T.H., O'Toole E.T., Winey M., Salmon E.D., Casey P.J., Nelson W.J., and Barth A.I. beta-Catenin is a Nek2 substrate involved in centrosome separation. Genes Dev. 22 (2008) 91-105
5. Bartscherer K., Pelte N., Ingelfinger D., and Boutros M. Secretion of Wnt ligands requires Evi, a conserved transmembrane protein. Cell 125 (2006) 523-533
6. Benhamouche S., Decaens T., Godard C., Chambrey R., Rickman D.S., Moinard C., Vasseur-Cognet M., Kuo C.J., Kahn A., Perret C., and Colnot S. Apc tumor suppressor gene is the "zonation-keeper" of mouse liver. Dev. Cell 10 (2006) 759-770
7. Bettencourt-Dias M., Giet R., Sinka R., Mazumdar A., Lock W.G., Balloux F., Zafiropoulos P.J., Yamaguchi S., Winter S., Carthew R.W., et al. Genome-wide survey of protein kinases required for cell cycle progression. Nature 432 (2004) 980-987
8. Bhanot P., Brink M., Harryman Samos C., Hsieh J.-C., Wang Y., Macke J.P., Andrew D., Nathans J., and Nusse R. A new member of the frizzled family from Drosophila functions as a Wingless receptor. Nature 382 (1996) 225-230
9. Bilic J., Huang Y.L., Davidson G., Zimmermann T., Cruciat C.M., Bienz M., and Niehrs C. Wnt induces LRP6 signalosomes and promotes dishevelled-dependent LRP6 phosphorylation. Science 316 (2007) 1619-1622
10. Binnerts M.E., Kim K.A., Bright J.M., Patel S.M., Tran K., Zhou M., Leung J.M., Liu Y., Lomas III W.E., Dixon M., et al. R-Spondin1 regulates Wnt signaling by inhibiting internalization of LRP6. Proc. Natl. Acad. Sci. USA 104 (2007) 14700-14705
11. Boutros M., Kiger A.A., Armknecht S., Kerr K., Hild M., Koch B., Haas S.A., Consortium H.F., Paro R., and Perrimon N. Genome-wide RNAi analysis of growth and viability in Drosophila cells. Science 303 (2004) 832-835
12. Bryja V., Gradl D., Schambony A., Arenas E., and Schulte G. Beta-arrestin is a necessary component of Wnt/beta-catenin signaling in vitro and in vivo. Proc. Natl. Acad. Sci. USA 104 (2007) 6690-6695
13. Charrasse S., Carena I., Hagmann J., Woods-Cook K., and Ferrari S. PCTAIRE-1: characterization, subcellular distribution, and cell cycle-dependent kinase activity. Cell Growth Differ. 10 (1999) 611-620
14. Clevers H. Wnt/beta-catenin signaling in development and disease. Cell 127 (2006) 469-480
15. Cselenyi C.S., Jernigan K.K., Tahinci E., Thorne C.A., Lee L.A., and Lee E. LRP6 transduces a canonical Wnt signal independently of Axin degradation by inhibiting GSK3's phosphorylation of beta-catenin. Proc. Natl. Acad. Sci. USA 105 (2008) 8032-8037
16. Dailey L., Ambrosetti D., Mansukhani A., and Basilico C. Mechanisms underlying differential responses to FGF signaling. Cytokine Growth Factor Rev. 16 (2005) 233-247
17. Davidson G., Wu W., Shen J., Bilic J., Fenger U., Stannek P., Glinka A., and Niehrs C. Casein kinase 1 gamma couples Wnt receptor activation to cytoplasmic signal transduction. Nature 438 (2005) 867-872
18. Edgar B.A., and O'Farrell P.H. Genetic control of cell division patterns in the Drosophila embryo. Cell 57 (1989) 177-187
19. Fodde R., and Brabletz T. Wnt/beta-catenin signaling in cancer stemness and malignant behavior. Curr. Opin. Cell Biol. 19 (2007) 150-158
20. Gautier J., Solomon M.J., Booher R.N., Bazan J.F., and Kirschner M.W. cdc25 is a specific tyrosine phosphatase that directly activates p34cdc2. Cell 67 (1991) 197-211
21. Gawantka V., Delius H., Hirschfeld K., Blumenstock C., and Niehrs C. Antagonizing the Spemann organizer: role of the homeobox gene Xvent-1. EMBO J. 14 (1995) 6268-6279
22. Gottesfeld J.M., and Forbes D.J. Mitotic repression of the transcriptional machinery. Trends Biochem. Sci. 22 (1997) 197-202
23. Hadjihannas M.V., Bruckner M., Jerchow B., Birchmeier W., Dietmaier W., and Behrens J. Aberrant Wnt/beta-catenin signaling can induce chromosomal instability in colon cancer. Proc. Natl. Acad. Sci. USA 103 (2006) 10747-10752
24. Hassler C., Cruciat C.M., Huang Y.L., Kuriyama S., Mayor R., and Niehrs C. Kremen is required for neural crest induction in Xenopus and promotes LRP6-mediated Wnt signaling. Development 134 (2007) 4255-4263
25. Hata A., Seoane J., Lagna G., Montalvo E., Hemmati-Brivanlou A., and Massague J. OAZ uses distinct DNA- and protein-binding zinc fingers in separate BMP-Smad and Olf signaling pathways. Cell 100 (2000) 229-240
26. He T.C., Sparks A.B., Rago C., Hermeking H., Zawel L., da Costa L.T., Morin P.J., Vogelstein B., and Kinzler K.W. Identification of c-MYC as a target of the APC pathway. Science 281 (1998) 1509-1512
27. He X., Semenov M., Tamai K., and Zeng X. LDL receptor-related proteins 5 and 6 in Wnt/beta-catenin signaling: arrows point the way. Development 131 (2004) 1663-1677
28. Heasman J., Kofron M., and Wylie C. Beta-catenin signaling activity dissected in the early Xenopus embryo: a novel antisense approach. Dev. Biol. 222 (2000) 124-134
29. Higa M.M., Ullman K.S., and Prunuske A.J. Studying nuclear disassembly in vitro using Xenopus egg extract. Methods 39 (2006) 284-290
30. Huang P., Senga T., and Hamaguchi M. A novel role of phospho-beta-catenin in microtubule regrowth at centrosome. Oncogene 26 (2007) 4357-4371
31. Jiang M., Gao Y., Yang T., Zhu X., and Chen J. Cyclin Y, a novel membrane-associated cyclin, interacts with PFTK1. FEBS Lett. 583 (2009) 2171-2178
32. Kao K.R., and Elinson R.P. The entire mesodermal mantle behaves as Spemann's organizer in dorsoanterior enhanced Xenopus laevis embryos. Dev. Biol. 127 (1988) 64-77
33. Kaplan D.D., Meigs T.E., Kelly P., and Casey P.J. Identification of a role for beta-catenin in the establishment of a bipolar mitotic spindle. J. Biol. Chem. 279 (2004) 10829-10832
34. Katoh M., and Katoh M. Cross-talk of WNT and FGF signaling pathways at GSK3beta to regulate beta-catenin and SNAIL signaling cascades. Cancer Biol. Ther. 5 (2006) 1059-1064
35. Khan Z., Vijayakumar S., de la Torre T.V., Rotolo S., and Bafico A. Analysis of endogenous LRP6 function reveals a novel feedback mechanism by which Wnt negatively regulates its receptor. Mol. Cell. Biol. 27 (2007) 7291-7301
36. Kockeritz L., Doble B., Patel S., and Woodgett J.R. Glycogen synthase kinase-3-an overview of an over-achieving protein kinase. Curr. Drug Targets 7 (2006) 1377-1388
37. Lee G., White L.S., Hurov K.E., Stappenbeck T.S., and Piwnica-Worms H. Response of small intestinal epithelial cells to acute disruption of cell division through CDC25 deletion. Proc. Natl. Acad. Sci. USA 106 (2009) 4701-4706
38. Liu H., Xu S., Wang Y., Mazerolle C., Thurig S., Coles B.L., Ren J.C., Taketo M.M., van der Kooy D., and Wallace V.A. Ciliary margin transdifferentiation from neural retina is controlled by canonical Wnt signaling. Dev. Biol. 308 (2007) 54-67
39. Logan C.Y., and Nusse R. The Wnt signaling pathway in development and disease. Annu. Rev. Cell Dev. Biol. 20 (2004) 781-810
40. Macdonald B.T., Yokota C., Tamai K., Zeng X., and He X. Wnt signal amplification: activity, cooperativity and regulation of multiple intracellular PPPSP motifs in the Wnt coreceptor LRP6. J. Biol. Chem. 283 (2008) 16115-16123
41. Manning G., Whyte D.B., Martinez R., Hunter T., and Sudarsanam S. The protein kinase complement of the human genome. Science 298 (2002) 1912-1934
42. Miller J.R., and Moon R.T. Analysis of the signaling activities of localization mutants of beta-catenin during axis specification in Xenopus. J. Cell Biol. 139 (1997) 229-243
43. Mir A., and Heasman J. How the mother can help: studying maternal Wnt signaling by anti-sense-mediated depletion of maternal mRNAs and the host transfer technique. In: Vincan E. (Ed). Wnt Signaling (2009), Humana Press, New York 417-429
44. Moon R.T., Kohn A.D., De Ferrari G.V., and Kaykas A. WNT and beta-catenin signalling: diseases and therapies. Nat. Rev. Genet. 5 (2004) 691-701
45. Morgan D.O. Cyclin-dependent kinases: engines, clocks, and microprocessors. Annu. Rev. Cell Dev. Biol. 13 (1997) 261-291
46. Murray A.W. Cell cycle extracts. Methods Cell Biol. 36 (1991) 581-605
47. Murray A.W. Recycling the cell cycle: cyclins revisited. Cell 116 (2004) 221-234
48. Niehrs C. The Spemann organizer and embryonic head induction. EMBO J. 20 (2001) 631-637
49. Niehrs C. Regionally specific induction by the Spemann-Mangold organizer. Nat. Rev. Genet. 5 (2004) 425-434
50. Okuda T., Cleveland J.L., and Downing J.R. PCTAIRE-1 and PCTAIRE-3, two members of a novel cdc2/CDC28-related protein kinase gene family. Oncogene 7 (1992) 2249-2258
51. Olmeda D., Castel S., Vilaro S., and Cano A. Beta-catenin regulation during the cell cycle: implications in G2/M and apoptosis. Mol. Biol. Cell 14 (2003) 2844-2860
52. Orford K., Orford C.C., and Byers S.W. Exogenous expression of beta-catenin regulates contact inhibition, anchorage-independent growth, anoikis, and radiation-induced cell cycle arrest. J. Cell Biol. 146 (1999) 855-868
53. Piao S., Lee S.H., Kim H., Yum S., Stamos J.L., Xu Y., Lee S.J., Lee J., Oh S., Han J.K., et al. Direct inhibition of GSK3beta by the phosphorylated cytoplasmic domain of LRP6 in Wnt/beta-catenin signaling. PLoS ONE 3 (2008) e4046
54. Pinson K.I., Brennan J., Monkley S., Avery B.J., and Skarnes W.C. An LDL-receptor-related protein mediates Wnt signalling in mice. Nature 407 (2000) 535-538
55. Polakis P. Wnt signaling and cancer. Genes Dev. 14 (2000) 1837-1851
56. Reya T., and Clevers H. Wnt signalling in stem cells and cancer. Nature 434 (2005) 843-850
57. Salinas P.C. Retrograde signalling at the synapse: a role for Wnt proteins. Biochem. Soc. Trans. 33 (2005) 1295-1298
58. Sauer K., Weigmann K., Sigrist S., and Lehner C.F. Novel members of the cdc2-related kinase family in Drosophila: cdk4/6, cdk5, PFTAIRE, and PITSLRE kinase. Mol. Biol. Cell 7 (1996) 1759-1769
59. Shackleford G.M., MacArthur C.A., Kwan H.C., and Varmus H.E. Mouse mammary tumor virus infection accelerates mammary carcinogenesis in Wnt-1 transgenic mice by insertional activation of int-2/Fgf-3 and hst/Fgf-4. Proc. Natl. Acad. Sci. USA 90 (1993) 740-744
60. Shibamoto S., Higano K., Takada R., Ito F., Takeichi M., and Takada S. Cytoskeletal reorganization by soluble Wnt-3a protein signalling. Genes Cells 3 (1998) 659-670
61. Shu F., Lv S., Qin Y., Ma X., Wang X., Peng X., Luo Y., Xu B.E., Sun X., and Wu J. Functional characterization of human PFTK1 as a cyclin-dependent kinase. Proc. Natl. Acad. Sci. USA 104 (2007) 9248-9253
62. Sive H.L., Grainger R.M., and Harland R.M. Early development of Xenopus laevis: a laboratory manual (2000), Cold Spring Harbor Laboratory Press, Cold Spring Harbor, NY
63. Stadeli R., Hoffmans R., and Basler K. Transcription under the control of nuclear Arm/beta-catenin. Curr. Biol. 16 (2006) R378-R385
64. Stanyon C.A., Liu G., Mangiola B.A., Patel N., Giot L., Kuang B., Zhang H., Zhong J., and Finley Jr. R.L. A Drosophila protein-interaction map centered on cell-cycle regulators. Genome Biol. 5 (2004) R96
65. Stowers R.S., Garza D., Rascle A., and Hogness D.S. The L63 gene is necessary for the ecdysone-induced 63E late puff and encodes CDK proteins required for Drosophila development. Dev. Biol. 221 (2000) 23-40
66. Strausfeld U., Labbe J.C., Fesquet D., Cavadore J.C., Picard A., Sadhu K., Russell P., and Doree M. Dephosphorylation and activation of a p34cdc2/cyclin B complex in vitro by human CDC25 protein. Nature 351 (1991) 242-245
67. Tamai K., Semenov M., Kato Y., Spokony R., Liu C., Katsuyama Y., Hess F., Saint-Jeannet J.P., and He X. LDL-receptor-related proteins in Wnt signal transduction. Nature 407 (2000) 530-535
68. Tamai K., Zeng X., Liu C., Zhang X., Harada Y., Chang Z., and He X. A mechanism for Wnt coreceptor activation. Mol. Cell 13 (2004) 149-156
69. Ten Berge D., Brugmann S.A., Helms J.A., and Nusse R. Wnt and FGF signals interact to coordinate growth with cell fate specification during limb development. Development 135 (2008) 3247-3257
70. Tetsu O., and McCormick F. Beta-catenin regulates expression of cyclin D1 in colon carcinoma cells. Nature 398 (1999) 422-426
71. Ueda H.R., Hayashi S., Chen W., Sano M., Machida M., Shigeyoshi Y., Iino M., and Hashimoto S. System-level identification of transcriptional circuits underlying mammalian circadian clocks. Nat. Genet. 37 (2005) 187-192
72. Ueno H., Nakajo N., Watanabe M., Isoda M., and Sagata N. FoxM1-driven cell division is required for neuronal differentiation in early Xenopus embryos. Development 135 (2008) 2023-2030
73. Walston T.D., and Hardin J. Wnt-dependent spindle polarization in the early C. elegans embryo. Semin. Cell Dev. Biol. 17 (2006) 204-213
74. Wehrli M., Dougan S.T., Caldwell K., O'Keefe L., Schwartz S., Vaizel-Ohayon D., Schejter E., Tomlinson A., and DiNardo S. arrow encodes an LDL-receptor-related protein essential for Wingless signalling. Nature 407 (2000) 527-530
75. Wodarz A., and Nusse R. Mechanisms of Wnt signaling in development. Annu. Rev. Cell Dev. Biol. 14 (1998) 59-88
76. Wolf J., Palmby T.R., Gavard J., Williams B.O., and Gutkind J.S. Multiple PPPS/TP motifs act in a combinatorial fashion to transduce Wnt signaling through LRP6. FEBS Lett. 582 (2008) 255-261
77. Wu G., Huang H., Garcia Abreu J., and He X. Inhibition of GSK3 phosphorylation of beta-catenin via phosphorylated PPPSPXS motifs of Wnt coreceptor LRP6. PLoS ONE 4 (2009) e4926 10.1371/journal.pone.0004926
78. Yum S., Lee S.J., Piao S., Xu Y., Jung J., Jung Y., Oh S., Lee J., Park B.J., and Ha N.C. The role of the Ser/Thr cluster in the phosphorylation of PPPSP motifs in Wnt coreceptors. Biochem. Biophys. Res. Commun. 381 (2009) 345-349
79. Zaghetto A.A., Paina S., Mantero S., Platonova N., Peretto P., Bovetti S., Puche A., Piccolo S., and Merlo G.R. Activation of the Wnt-beta catenin pathway in a cell population on the surface of the forebrain is essential for the establishment of olfactory axon connections. J. Neurosci. 27 (2007) 9757-9768
80. Zeng X., Tamai K., Doble B., Li S., Huang H., Habas R., Okamura H., Woodgett J., and He X. A dual-kinase mechanism for Wnt co-receptor phosphorylation and activation. Nature 438 (2005) 873-877
81. Zeng X., Huang H., Tamai K., Zhang X., Harada Y., Yokota C., Almeida K., Wang J., Doble B., Woodgett J., et al. Initiation of Wnt signaling: control of Wnt coreceptor Lrp6 phosphorylation/activation via frizzled, dishevelled and axin functions. Development 135 (2008) 367-375
82. Zuck M.V., Wylie C.C., and Heasman J. A Comparative Methods Approach to the Study of Oocytes and Embryos. In: Richter J.D. (Ed) (1998), Oxford University Press, Oxford 341-354