Molecular regulation and pharmacological targeting of the β-catenin destruction complex

British Journal of Pharmacology

Volumn 174, Issue 24, 2017, Pages 4575-4588

  van Kappel, Eline C ^a   Maurice, Madelon M ^a  

^a UNIVERSITY MEDICAL CENTER UTRECHT   (Netherlands)

Author keywords

[No Author keywords available]

Indexed keywords

APC PROTEIN; AXIN; AXIN2; BETA CATENIN DESTRUCTION COMPLEX; CASEIN KINASE I; GLYCOGEN SYNTHASE KINASE 3; MULTIPROTEIN COMPLEX; UNCLASSIFIED DRUG; ANTINEOPLASTIC AGENT;

ADENOSINE DIPHOSPHATE RIBOSYLATION; BINDING AFFINITY; BINDING SITE; CELL ACTIVITY; ENZYME ACTIVITY; GENE MUTATION; HUMAN; NONHUMAN; PRIORITY JOURNAL; PROTEIN BINDING; PROTEIN DEPHOSPHORYLATION; PROTEIN INTERACTION; PROTEIN PROCESSING; PROTEIN TARGETING; REVIEW; WNT SIGNALING; ANIMAL; ANTAGONISTS AND INHIBITORS; DRUG EFFECT; METABOLISM; NEOPLASM; PATHOLOGY;

ANIMALS; ANTINEOPLASTIC AGENTS; AXIN SIGNALING COMPLEX; HUMANS; NEOPLASMS; WNT SIGNALING PATHWAY;

EID: 85037973416     PISSN: 00071188     EISSN: 14765381     Source Type: Journal    
DOI: 10.1111/bph.13922     Document Type: Review

References (167)

1. Albuquerque C, Breukel C, van der Luijt R, Fidalgo P, Lage P, Slors FJ et al. (2002). The ‘just-right’ signaling model: APC somatic mutations are selected based on a specific level of activation of the beta-catenin signaling cascade. Hum Mol Genet 11: 1549–1560.
2. Alexander SPH, Davenport AP, Kelly E, Marrion N, Peters JA, Benson HE et al. (2015a). The Concise Guide to PHARMACOLOGY 2015/16: G protein-coupled receptors. Br J Pharmacol 172: 5744–5869.
3. Alexander SPH, Fabbro D, Kelly E, Marrion N, Peters JA, Benson HE et al. (2015b). The Concise Guide to PHARMACOLOGY 2015/16: Enzymes. Br J Pharmacol 172: 6024–6109.
4. Amit S, Hatzubai A, Birman Y, Andersen JS, Ben-Shushan E, Mann M et al. (2002). Axin-mediated CKI phosphorylation of beta-catenin at Ser 45: a molecular switch for the Wnt pathway. Genes Dev 16: 1066–1076.
5. Anvarian Z, Nojima H, van Kappel EC, Madl T, Spit M, Viertler M et al. (2016). Axin cancer mutants form nanoaggregates to rewire the Wnt signaling network. Nat Struct Mol Biol 23: 324–332.
6. Aristizabal-Pachon AF, Carvalho TI, Carrara HH, Andrade J, Takahashi CS (2015). AXIN2 Polymorphisms, the beta-catenin destruction complex expression profile and breast cancer susceptibility. Asian Pac J Cancer Prev 16: 7277–7284.
7. Bahl C, Sharma S, Singh N, Behera D (2017). Association study between genetic variations in axin2 gene and lung cancer risk in North Indian population: a multiple interaction analysis. Tumour Biol 39 1010428317695533.
8. Behrens J, Jerchow BA, Wurtele M, Grimm J, Asbrand C, Wirtz R et al. (1998). Functional interaction of an axin homolog, conductin, with beta-catenin, APC, and GSK3beta. Science 280: 596–599.
9. Behrens J, von Kries JP, Kuhl M, Bruhn L, Wedlich D, Grosschedl R et al. (1996). Functional interaction of beta-catenin with the transcription factor LEF-1. Nature 382: 638–642.
10. Bell DA (2005). Origins and molecular pathology of ovarian cancer. Mod Pathol 18 (Suppl 2): S19–S32.
11. Bernkopf DB, Hadjihannas MV, Behrens J (2015). Negative-feedback regulation of the Wnt pathway by conductin/axin2 involves insensitivity to upstream signalling. J Cell Sci 128: 33–39.
12. Beroud C, Soussi T (1996). APC gene: database of germline and somatic mutations in human tumors and cell lines. Nucleic Acids Res 24: 121–124.
13. Bienz M (2014). Signalosome assembly by domains undergoing dynamic head-to-tail polymerization. Trends Biochem Sci 39: 487–495.
14. Bilic J, Huang YL, Davidson G, Zimmermann T, Cruciat CM, Bienz M et al. (2007). Wnt induces LRP6 signalosomes and promotes dishevelled-dependent LRP6 phosphorylation. Science 316: 1619–1622.
15. Brannon AR, Vakiani E, Sylvester BE, Scott SN, McDermott G, Shah RH et al. (2014). Comparative sequencing analysis reveals high genomic concordance between matched primary and metastatic colorectal cancer lesions. Genome Biol 15: 454.
16. Breitman M, Zilberberg A, Caspi M, Rosin-Arbesfeld R (2008). The armadillo repeat domain of the APC tumor suppressor protein interacts with Striatin family members. Biochim Biophys Acta 1783: 1792–1802.
17. Callow MG, Tran H, Phu L, Lau T, Lee J, Sandoval WN et al. (2011). Ubiquitin ligase RNF146 regulates tankyrase and axin to promote Wnt signaling. PLoS One 6: e22595.
18. Cegielska A, Gietzen KF, Rivers A, Virshup DM (1998). Autoinhibition of casein kinase I epsilon (CKI epsilon) is relieved by protein phosphatases and limited proteolysis. J Biol Chem 273: 1357–1364.
19. Cerami E, Gao J, Dogrusoz U, Gross BE, Sumer SO, Aksoy BA et al. (2012). The cBio cancer genomics portal: an open platform for exploring multidimensional cancer genomics data. Cancer Discov 2: 401–404.
20. Cha PH, Cho YH, Lee SK, Lee J, Jeong WJ, Moon BS et al. (2016). Small-molecule binding of the axin RGS domain promotes beta-catenin and Ras degradation. Nat Chem Biol 12: 593–600.
21. Chia IV, Costantini F (2005). Mouse axin and axin2/conductin proteins are functionally equivalent in vivo. Mol Cell Biol 25: 4371–4376.
22. Choi SH, Estaras C, Moresco JJ, Yates JR 3rd, Jones KA (2013). alpha-Catenin interacts with APC to regulate beta-catenin proteolysis and transcriptional repression of Wnt target genes. Genes Dev 27: 2473–2488.
23. Clements WM, Lowy AM, Groden J (2003). Adenomatous polyposis coli/beta-catenin interaction and downstream targets: altered gene expression in gastrointestinal tumors. Clin Colorectal Cancer 3: 113–120.
24. Clevers H (2006). Wnt/beta-catenin signaling in development and disease. Cell 127: 469–480.
25. Clevers H (2016). Modeling development and disease with organoids. Cell 165: 1586–1597.
26. Cliffe A, Hamada F, Bienz M (2003). A role of dishevelled in relocating axin to the plasma membrane during wingless signaling. Curr Biol 13: 960–966.
27. Conlin A, Smith G, Carey FA, Wolf CR, Steele RJ (2005). The prognostic significance of K-ras, p53, and APC mutations in colorectal carcinoma. Gut 54: 1283–1286.
28. Croy HE, Fuller CN, Giannotti J, Robinson P, Foley AV, Yamulla RJ et al. (2016). The poly(ADP-ribose) polymerase enzyme tankyrase antagonizes activity of the beta-catenin destruction complex through ADP-ribosylation of axin and APC2. J Biol Chem 291: 12747–12760.
29. Cruciat CM (2014). Casein kinase 1 and Wnt/beta-catenin signaling. Curr Opin Cell Biol 31: 46–55.
30. Cselenyi CS, Jernigan KK, Tahinci E, Thorne CA, Lee LA, Lee E (2008). LRP6 transduces a canonical Wnt signal independently of axin degradation by inhibiting GSK3's phosphorylation of beta-catenin. Proc Natl Acad Sci U S A 105: 8032–8037.
31. Dajani R, Fraser E, Roe SM, Yeo M, Good VM, Thompson V et al. (2003). Structural basis for recruitment of glycogen synthase kinase 3beta to the axin-APC scaffold complex. EMBO J 22: 494–501.
32. Davidson G, Niehrs C (2014). Wnt signaling at the membrane. In: Wnt Signaling in Development and Disease. John Wiley & Sons, Inc.: Hoboken, New Jersey, USA, pp. 15–32.
33. Davidson G, Wu W, Shen J, Bilic J, Fenger U, Stannek P et al. (2005). Casein kinase 1 gamma couples Wnt receptor activation to cytoplasmic signal transduction. Nature 438: 867–872.
34. Ding VW, Chen RH, McCormick F (2000). Differential regulation of glycogen synthase kinase 3beta by insulin and Wnt signaling. J Biol Chem 275: 32475–32481.
35. Doble BW, Patel S, Wood GA, Kockeritz LK, Woodgett JR (2007). Functional redundancy of GSK-3alpha and GSK-3beta in Wnt/beta-catenin signaling shown by using an allelic series of embryonic stem cell lines. Dev Cell 12: 957–971.
36. Dow LE, O'Rourke KP, Simon J, Tschaharganeh DF, van Es JH, Clevers H et al. (2015). Apc Restoration promotes cellular differentiation and reestablishes crypt homeostasis in colorectal cancer. Cell 161: 1539–1552.
37. Drost J, van Jaarsveld RH, Ponsioen B, Zimberlin C, van Boxtel R, Buijs A et al. (2015). Sequential cancer mutations in cultured human intestinal stem cells. Nature 521: 43–47.
38. Eisemann T, McCauley M, Langelier MF, Gupta K, Roy S, Van Duyne GD et al. (2016). Tankyrase-1 ankyrin repeats form an adaptable binding platform for targets of ADP-ribose modification. Structure 24: 1679–1692.
39. Eklof Spink K, Fridman SG, Weis WI (2001). Molecular mechanisms of beta-catenin recognition by adenomatous polyposis coli revealed by the structure of an APC-beta-catenin complex. EMBO J 20: 6203–6212.
40. Fagotto F, Jho E, Zeng L, Kurth T, Joos T, Kaufmann C et al. (1999). Domains of axin involved in protein-protein interactions, Wnt pathway inhibition, and intracellular localization. J Cell Biol 145: 741–756.
41. Fiedler M, Mendoza-Topaz C, Rutherford TJ, Mieszczanek J, Bienz M (2011). Dishevelled interacts with the DIX domain polymerization interface of axin to interfere with its function in down-regulating beta-catenin. Proc Natl Acad Sci U S A 108: 1937–1942.
42. Figeac N, Zammit PS (2015). Coordinated action of axin1 and axin2 suppresses beta-catenin to regulate muscle stem cell function. Cell Signal 27: 1652–1665.
43. Frame S, Cohen P (2001). GSK3 takes centre stage more than 20 years after its discovery. Biochem J 359: 1–16.
44. Fumagalli A, Drost J, Suijkerbuijk SJ, van Boxtel R, de Ligt J, Offerhaus GJ et al. (2017). Genetic dissection of colorectal cancer progression by orthotopic transplantation of engineered cancer organoids. Proc Natl Acad Sci U S A 114: E2357–E2364.
45. Gao J, Aksoy BA, Dogrusoz U, Dresdner G, Gross B, Sumer SO et al. (2013). Integrative analysis of complex cancer genomics and clinical profiles using the cBioPortal. Sci Signal 6: pl1.
46. Gaspar C, Franken P, Molenaar L, Breukel C, van der Valk M, Smits R et al. (2009). A targeted constitutive mutation in the APC tumor suppressor gene underlies mammary but not intestinal tumorigenesis. PLoS Genet 5: e1000547.
47. Gerlach JP, Emmink BL, Nojima H, Kranenburg O, Maurice MM (2014). Wnt signalling induces accumulation of phosphorylated beta-catenin in two distinct cytosolic complexes. Open Biol 4: 140120.
48. Graves PR, Haas DW, Hagedorn CH, DePaoli-Roach AA, Roach PJ (1993). Molecular cloning, expression, and characterization of a 49-kilodalton casein kinase I isoform from rat testis. J Biol Chem 268: 6394–6401.
49. Ha NC, Tonozuka T, Stamos JL, Choi HJ, Weis WI (2004). Mechanism of phosphorylation-dependent binding of APC to beta-catenin and its role in beta-catenin degradation. Mol Cell 15: 511–521.
50. Hsu W, Zeng L, Costantini F (1999). Identification of a domain of axin that binds to the serine/threonine protein phosphatase 2A and a self-binding domain. J Biol Chem 274: 3439–3445.
51. Huang SM, Mishina YM, Liu S, Cheung A, Stegmeier F, Michaud GA et al. (2009). Tankyrase inhibition stabilizes axin and antagonizes Wnt signalling. Nature 461: 614–620.
52. Ikeda S, Kishida M, Matsuura Y, Usui H, Kikuchi A (2000). GSK-3beta-dependent phosphorylation of adenomatous polyposis coli gene product can be modulated by beta-catenin and protein phosphatase 2A complexed with axin. Oncogene 19: 537–545.
53. Ikeda S, Kishida S, Yamamoto H, Murai H, Koyama S, Kikuchi A (1998). Axin, a negative regulator of the Wnt signaling pathway, forms a complex with GSK-3beta and beta-catenin and promotes GSK-3beta-dependent phosphorylation of beta-catenin. EMBO J 17: 1371–1384.
54. Janssens V, Goris J (2001). Protein phosphatase 2A: a highly regulated family of serine/threonine phosphatases implicated in cell growth and signalling. Biochem J 353: 417–439.
55. Jho EH, Zhang T, Domon C, Joo CK, Freund JN, Costantini F (2002). Wnt/beta-catenin/Tcf signaling induces the transcription of axin2, a negative regulator of the signaling pathway. Mol Cell Biol 22: 1172–1183.
56. Jiang J, Struhl G (1998). Regulation of the Hedgehog and Wingless signalling pathways by the F-box/WD40-repeat protein Slimb. Nature 391: 493–496.
57. Jimbo T, Kawasaki Y, Koyama R, Sato R, Takada S, Haraguchi K et al. (2002). Identification of a link between the tumour suppressor APC and the kinesin superfamily. Nat Cell Biol 4: 323–327.
58. Julius MA, Schelbert B, Hsu W, Fitzpatrick E, Jho E, Fagotto F et al. (2000). Domains of axin and disheveled required for interaction and function in Wnt signaling. Biochem Biophys Res Commun 276: 1162–1169.
59. Kaidanovich-Beilin O, Woodgett JR (2011). GSK-3: functional insights from cell biology and animal models. Front Mol Neurosci 4: 40.
60. Kandoth C, McLellan MD, Vandin F, Ye K, Niu B, Lu C et al. (2013). Mutational landscape and significance across 12 major cancer types. Nature 502: 333–339.
61. Karlberg T, Markova N, Johansson I, Hammarstrom M, Schutz P, Weigelt J et al. (2010). Structural basis for the interaction between tankyrase-2 and a potent Wnt-signaling inhibitor. J Med Chem 53: 5352–5355.
62. Kawasaki Y, Senda T, Ishidate T, Koyama R, Morishita T, Iwayama Y et al. (2000). Asef, a link between the tumor suppressor APC and G-protein signaling. Science 289: 1194–1197.
63. Kikuchi A (1999). Modulation of Wnt signaling by axin and Axil. Cytokine Growth Factor Rev 10: 255–265.
64. Kim SE, Huang H, Zhao M, Zhang X, Zhang A, Semonov MV et al. (2013). Wnt stabilization of beta-catenin reveals principles for morphogen receptor-scaffold assemblies. Science 340: 867–870.
65. Kimelman D, Xu W (2006). Beta-catenin destruction complex: insights and questions from a structural perspective. Oncogene 25: 7482–7491.
66. Kinzler KW, Vogelstein B (1996). Lessons from hereditary colorectal cancer. Cell 87: 159–170.
67. Kirby CA, Cheung A, Fazal A, Shultz MD, Stams T (2012). Structure of human tankyrase 1 in complex with small-molecule inhibitors PJ34 and XAV939. Acta Crystallogr Sect F Struct Biol Cryst Commun 68: 115–118.
68. Kishida S, Yamamoto H, Hino S, Ikeda S, Kishida M, Kikuchi A (1999). DIX domains of Dvl and axin are necessary for protein interactions and their ability to regulate beta-catenin stability. Mol Cell Biol 19: 4414–4422.
69. Kishida S, Yamamoto H, Ikeda S, Kishida M, Sakamoto I, Koyama S et al. (1998). Axin, a negative regulator of the Wnt signaling pathway, directly interacts with adenomatous polyposis coli and regulates the stabilization of beta-catenin. J Biol Chem 273: 10823–10826.
70. Kohler EM, Chandra SH, Behrens J, Schneikert J (2009). Beta-catenin degradation mediated by the CID domain of APC provides a model for the selection of APC mutations in colorectal, desmoid and duodenal tumours. Hum Mol Genet 18: 213–226.
71. Kohler EM, Derungs A, Daum G, Behrens J, Schneikert J (2008). Functional definition of the mutation cluster region of adenomatous polyposis coli in colorectal tumours. Hum Mol Genet 17: 1978–1987.
72. −/− colon carcinoma. Science 275: 1784–1787.
73. Kunttas-Tatli E, Roberts DM, McCartney BM (2014). Self-association of the APC tumor suppressor is required for the assembly, stability, and activity of the Wnt signaling destruction complex. Mol Biol Cell 25: 3424–3436.
74. Kunttas-Tatli E, Von Kleeck RA, Greaves BD, Vinson D, Roberts DM, McCartney BM (2015). The two SAMP repeats and their phosphorylation state in Drosophila adenomatous polyposis coli-2 play mechanistically distinct roles in negatively regulating Wnt signaling. Mol Biol Cell 26: 4503–4518.
75. Lee E, Salic A, Kruger R, Heinrich R, Kirschner MW (2003). The roles of APC and axin derived from experimental and theoretical analysis of the Wnt pathway. PLoS Biol 1: E10.
76. Li S, Wang C, Liu X, Hua S, Liu X (2015). The roles of AXIN2 in tumorigenesis and epigenetic regulation. Fam Cancer 14: 325–331.
77. Li VS, Ng SS, Boersema PJ, Low TY, Karthaus WR, Gerlach JP et al. (2012). Wnt signaling through inhibition of beta-catenin degradation in an intact axin1 complex. Cell 149: 1245–1256.
78. Li Z, Kroboth K, Newton IP, Nathke IS (2008). Novel self-association of the APC molecule affects APC clusters and cell migration. J Cell Sci 121: 1916–1925.
79. Li Z, Nathke IS (2005). Tumor-associated NH2-terminal fragments are the most stable part of the adenomatous polyposis coli protein and can be regulated by interactions with COOH-terminal domains. Cancer Res 65: 5195–5204.
80. Liu C, Li Y, Semenov M, Han C, Baeg GH, Tan Y et al. (2002). Control of beta-catenin phosphorylation/degradation by a dual-kinase mechanism. Cell 108: 837–847.
81. Liu D, Li L, Yang Y, Liu W, Wu J (2014). The axin2 rs2240308 polymorphism and susceptibility to lung cancer in a Chinese population. Tumour Biol 35: 10987–10991.
82. Liu J, Xing Y, Hinds TR, Zheng J, Xu W (2006). The third 20 amino acid repeat is the tightest binding site of APC for beta-catenin. J Mol Biol 360: 133–144.
83. Liu YT, Dan QJ, Wang J, Feng Y, Chen L, Liang J et al. (2011). Molecular basis of Wnt activation via the DIX domain protein Ccd1. J Biol Chem 286: 8597–8608.
84. Luchtenborg M, Weijenberg MP, Wark PA, Saritas AM, Roemen GM, van Muijen GN et al. (2005). Mutations in APC, CTNNB1 and K-ras genes and expression of hMLH1 in sporadic colorectal carcinomas from the Netherlands Cohort Study. BMC Cancer 5: 160.
85. Luo W, Peterson A, Garcia BA, Coombs G, Kofahl B, Heinrich R et al. (2007). Protein phosphatase 1 regulates assembly and function of the beta-catenin degradation complex. EMBO J 26: 1511–1521.
86. Lustig B, Jerchow B, Sachs M, Weiler S, Pietsch T, Karsten U et al. (2002). Negative feedback loop of Wnt signaling through upregulation of conductin/axin2 in colorectal and liver tumors. Mol Cell Biol 22: 1184–1193.
87. MacDonald BT, He X (2012). Frizzled and LRP5/6 receptors for Wnt/beta-catenin signaling. Cold Spring Harb Perspect Biol 4: a007880.
88. MacDonald BT, Tamai K, He X (2009). Wnt/beta-catenin signaling: components, mechanisms, and diseases. Dev Cell 17: 9–26.
89. MacDonald BT, Yokota C, Tamai K, Zeng X, He X (2008). Wnt signal amplification via activity, cooperativity, and regulation of multiple intracellular PPPSP motifs in the Wnt co-receptor LRP6. J Biol Chem 283: 16115–16123.
90. Mao J, Wang J, Liu B, Pan W, Farr GH 3rd, Flynn C et al. (2001). Low-density lipoprotein receptor-related protein-5 binds to axin and regulates the canonical Wnt signaling pathway. Mol Cell 7: 801–809.
91. Marin O, Bustos VH, Cesaro L, Meggio F, Pagano MA, Antonelli M et al. (2003). A noncanonical sequence phosphorylated by casein kinase 1 in beta-catenin may play a role in casein kinase 1 targeting of important signaling proteins. Proc Natl Acad Sci U S A 100: 10193–10200.
92. Mariotti L, Templeton CM, Ranes M, Paracuellos P, Cronin N, Beuron F et al. (2016). Tankyrase requires SAM domain-dependent polymerization to support Wnt-beta-catenin signaling. Mol Cell 63: 498–513.
93. Martino-Echarri E, Brocardo MG, Mills KM, Henderson BR (2016). Tankyrase inhibitors stimulate the ability of tankyrases to bind axin and drive assembly of beta-catenin degradation-competent axin puncta. PLoS One 11: e0150484.
94. Matano M, Date S, Shimokawa M, Takano A, Fujii M, Ohta Y et al. (2015). Modeling colorectal cancer using CRISPR-Cas9-mediated engineering of human intestinal organoids. Nat Med 21: 256–262.
95. Mazzoni SM, Fearon ER (2014). AXIN1 and AXIN2 variants in gastrointestinal cancers. Cancer Lett 355: 1–8.
96. McCartney BM, Nathke IS (2008). Cell regulation by the Apc protein Apc as master regulator of epithelia. Curr Opin Cell Biol 20: 186–193.
97. McCartney BM, Price MH, Webb RL, Hayden MA, Holot LM, Zhou M et al. (2006). Testing hypotheses for the functions of APC family proteins using null and truncation alleles in Drosophila. Development 133: 2407–2418.
98. Melo FS, Kurtova AV, Harnoss JM, Kljavin N, Hoeck JD, Hung J et al. (2017). A distinct role for Lgr5+ stem cells in primary and metastatic colon cancer. Nature 543: 676–680.
99. Metcalfe C, Bienz M (2011). Inhibition of GSK3 by Wnt signalling – two contrasting models. J Cell Sci 124: 3537–3544.
100. Minde DP, Radli M, Forneris F, Maurice MM, Rudiger SG (2013). Large extent of disorder in adenomatous polyposis coli offers a strategy to guard Wnt signalling against point mutations. PLoS One 8: e77257.
101. Molenaar M, van de Wetering M, Oosterwegel M, Peterson-Maduro J, Godsave S, Korinek V et al. (1996). XTcf-3 transcription factor mediates beta-catenin-induced axis formation in Xenopus embryos. Cell 86: 391–399.
102. Morin PJ, Sparks AB, Korinek V, Barker N, Clevers H, Vogelstein B et al. (1997). Activation of beta-catenin-Tcf signaling in colon cancer by mutations in beta-catenin or APC. Science 275: 1787–1790.
103. Morrone S, Cheng Z, Moon RT, Cong F, Xu W (2012). Crystal structure of a tankyrase-axin complex and its implications for axin turnover and tankyrase substrate recruitment. Proc Natl Acad Sci U S A 109: 1500–1505.
104. Munemitsu S, Albert I, Souza B, Rubinfeld B, Polakis P (1995). Regulation of intracellular beta-catenin levels by the adenomatous polyposis coli (APC) tumor-suppressor protein. Proc Natl Acad Sci U S A 92: 3046–3050.
105. Nathke I (2006). Cytoskeleton out of the cupboard: colon cancer and cytoskeletal changes induced by loss of APC. Nat Rev Cancer 6: 967–974.
106. Ng SS, Mahmoudi T, Danenberg E, Bejaoui I, de Lau W, Korswagen HC et al. (2009). Phosphatidylinositol 3-kinase signaling does not activate the Wnt cascade. J Biol Chem 284: 35308–35313.
107. Noutsou M, Duarte AM, Anvarian Z, Didenko T, Minde DP, Kuper I et al. (2011). Critical scaffolding regions of the tumor suppressor axin1 are natively unfolded. J Mol Biol 405: 773–786.
108. Okada K, Bartolini F, Deaconescu AM, Moseley JB, Dogic Z, Grigorieff N et al. (2010). Adenomatous polyposis coli protein nucleates actin assembly and synergizes with the formin mDia1. J Cell Biol 189: 1087–1096.
109. Oosterveen T, Coudreuse DY, Yang PT, Fraser E, Bergsma J, Dale TC et al. (2007). Two functionally distinct axin-like proteins regulate canonical Wnt signaling in C. elegans. Dev Biol 308: 438–448.
110. 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.
111. Peterson-Nedry W, Erdeniz N, Kremer S, Yu J, Baig-Lewis S, Wehrli M (2008). Unexpectedly robust assembly of the axin destruction complex regulates Wnt/Wg signaling in Drosophila as revealed by analysis in vivo. Dev Biol 320: 226–241.
112. Piao S, Lee SH, Kim H, Yum S, Stamos JL, Xu Y et al. (2008). Direct inhibition of GSK3beta by the phosphorylated cytoplasmic domain of LRP6 in Wnt/beta-catenin signaling. PLoS One 3: e4046.
113. Polakis P (2007). The many ways of Wnt in cancer. Curr Opin Genet Dev 17: 45–51.
114. Polakis P (2012). Wnt signaling in cancer. Cold Spring Harb Perspect Biol 4: a008052.
115. Pronobis MI, Deuitch N, Posham V, Mimori-Kiyosue Y, Peifer M (2017). Reconstituting regulation of the canonical Wnt pathway by engineering a minimal beta-catenin destruction machine. Mol Biol Cell 28: 41–53.
116. Pronobis MI, Rusan NM, Peifer M (2015). A novel GSK3-regulated APC:axin interaction regulates Wnt signaling by driving a catalytic cycle of efficient betacatenin destruction. Elife 4: e08022.
117. Ratcliffe MJ, Itoh K, Sokol SY (2000). A positive role for the PP2A catalytic subunit in Wnt signal transduction. J Biol Chem 275: 35680–35683.
118. Roberts DM, Pronobis MI, Poulton JS, Waldmann JD, Stephenson EM, Hanna S et al. (2011). Deconstructing the sscatenin destruction complex: mechanistic roles for the tumor suppressor APC in regulating Wnt signaling. Mol Biol Cell 22: 1845–1863.
119. de la Roche M, Ibrahim AE, Mieszczanek J, Bienz M (2014). LEF1 and B9L shield beta-catenin from inactivation by axin, desensitizing colorectal cancer cells to tankyrase inhibitors. Cancer Res 74: 1495–1505.
120. Rosales-Reynoso MA, Arredondo-Valdez AR, Wence-Chavez LI, Barros-Nunez P, Gallegos-Arreola MP, Flores-Martinez SE et al. (2016). AXIN2 polymorphisms and their association with colorectal cancer in Mexican patients. Genet Test Mol Biomarkers 20: 438–444.
121. Rubinfeld B, Albert I, Porfiri E, Fiol C, Munemitsu S, Polakis P (1996). Binding of GSK3beta to the APC-beta-catenin complex and regulation of complex assembly. Science 272: 1023–1026.
122. Rubinfeld B, Albert I, Porfiri E, Munemitsu S, Polakis P (1997a). Loss of beta-catenin regulation by the APC tumor suppressor protein correlates with loss of structure due to common somatic mutations of the gene. Cancer Res 57: 4624–4630.
123. Rubinfeld B, Robbins P, El-Gamil M, Albert I, Porfiri E, Polakis P (1997b). Stabilization of beta-catenin by genetic defects in melanoma cell lines. Science 275: 1790–1792.
124. Rubinfeld B, Tice DA, Polakis P (2001). Axin-dependent phosphorylation of the adenomatous polyposis coli protein mediated by casein kinase 1epsilon. J Biol Chem 276: 39037–39045.
125. Salahshor S, Woodgett JR (2005). The links between axin and carcinogenesis. J Clin Pathol 58: 225–236.
126. Schwarz-Romond T, Fiedler M, Shibata N, Butler PJ, Kikuchi A, Higuchi Y et al. (2007a). The DIX domain of dishevelled confers Wnt signaling by dynamic polymerization. Nat Struct Mol Biol 14: 484–492.
127. Schwarz-Romond T, Metcalfe C, Bienz M (2007b). Dynamic recruitment of axin by dishevelled protein assemblies. J Cell Sci 120: 2402–2412.
128. Seeling JM, Miller JR, Gil R, Moon RT, White R, Virshup DM (1999). Regulation of beta-catenin signaling by the B56 subunit of protein phosphatase 2A. Science 283: 2089–2091.
129. Shiomi K, Uchida H, Keino-Masu K, Masu M (2003). Ccd1, a novel protein with a DIX domain, is a positive regulator in the Wnt signaling during zebrafish neural patterning. Curr Biol 13: 73–77.
130. Smith S, Giriat I, Schmitt A, de Lange T (1998). Tankyrase, a poly(ADP-ribose) polymerase at human telomeres. Science 282: 1484–1487.
131. Smits R, Kielman MF, Breukel C, Zurcher C, Neufeld K, Jagmohan-Changur S et al. (1999). Apc1638T: a mouse model delineating critical domains of the adenomatous polyposis coli protein involved in tumorigenesis and development. Genes Dev 13: 1309–1321.
132. Sobrado P, Jedlicki A, Bustos VH, Allende CC, Allende JE (2005). Basic region of residues 228-231 of protein kinase CK1alpha is involved in its interaction with axin: binding to axin does not affect the kinase activity. J Cell Biochem 94: 217–224.
133. Southan C, Sharman JL, Benson HE, Faccenda E, Pawson AJ, Alexander SPH et al. (2016). The IUPHAR/BPS guide to PHARMACOLOGY in 2016: towards curated quantitative interactions between 1300 protein targets and 6000 ligands. Nucl Acids Res 44: D1054–D1068.
134. Spink KE, Polakis P, Weis WI (2000). Structural basis of the axin-adenomatous polyposis coli interaction. EMBO J 19: 2270–2279.
135. Stamos JL, Chu ML, Enos MD, Shah N, Weis WI (2014). Structural basis of GSK-3 inhibition by N-terminal phosphorylation and by the Wnt receptor LRP6. Elife 3: e01998.
136. Stamos JL, Weis WI (2013). The beta-catenin destruction complex. Cold Spring Harb Perspect Biol 5: a007898.
137. Su Y, Fu C, Ishikawa S, Stella A, Kojima M, Shitoh K et al. (2008). APC is essential for targeting phosphorylated beta-catenin to the SCFbeta-TrCP ubiquitin ligase. Mol Cell 32: 652–661.
138. Taelman VF, Dobrowolski R, Plouhinec JL, Fuentealba LC, Vorwald PP, Gumper I et al. (2010). Wnt signaling requires sequestration of glycogen synthase kinase 3 inside multivesicular endosomes. Cell 143: 1136–1148.
139. Tamai K, Zeng X, Liu C, Zhang X, Harada Y, Chang Z et al. (2004). A mechanism for Wnt coreceptor activation. Mol Cell 13: 149–156.
140. Tanaka N, Mashima T, Mizutani A, Sato A, Aoyama A, Gong B et al. (2017). APC mutations as a potential biomarker for sensitivity to tankyrase inhibitors in colorectal cancer. Mol Cancer Ther 16: 752–762.
141. Thorne CA, Hanson AJ, Schneider J, Tahinci E, Orton D, Cselenyi CS et al. (2010). Small-molecule inhibition of Wnt signaling through activation of casein kinase 1alpha. Nat Chem Biol 6: 829–836.
142. Thorstensen L, Lind GE, Lovig T, Diep CB, Meling GI, Rognum TO et al. (2005). Genetic and epigenetic changes of components affecting the WNT pathway in colorectal carcinomas stratified by microsatellite instability. Neoplasia 7: 99–108.
143. Thorvaldsen TE, Pedersen NM, Wenzel EM, Schultz SW, Brech A, Liestol K et al. (2015). Structure, dynamics, and functionality of tankyrase inhibitor-induced degradasomes. Mol Cancer Res 13: 1487–1501.
144. Thorvaldsen TE, Pedersen NM, Wenzel EM, Stenmark H (2017). Differential roles of AXIN1 and AXIN2 in tankyrase inhibitor-induced formation of degradasomes and beta-catenin degradation. PLoS One 12: e0170508.
145. Tolwinski NS, Wehrli M, Rives A, Erdeniz N, DiNardo S, Wieschaus E (2003). Wg/Wnt signal can be transmitted through arrow/LRP5,6 and axin independently of Zw3/Gsk3beta activity. Dev Cell 4: 407–418.
146. Valvezan AJ, Zhang F, Diehl JA, Klein PS (2012). Adenomatous polyposis coli (APC) regulates multiple signaling pathways by enhancing glycogen synthase kinase-3 (GSK-3) activity. J Biol Chem 287: 3823–3832.
147. Vinyoles M, Del Valle-Perez B, Curto J, Vinas-Castells R, Alba-Castellon L, Garcia de Herreros A et al. (2014). Multivesicular GSK3 sequestration upon Wnt signaling is controlled by p120-catenin/cadherin interaction with LRP5/6. Mol Cell 53: 444–457.
148. Voloshanenko O, Erdmann G, Dubash TD, Augustin I, Metzig M, Moffa G et al. (2013). Wnt secretion is required to maintain high levels of Wnt activity in colon cancer cells. Nat Commun 4: 2610.
149. Watanabe T, Wang S, Noritake J, Sato K, Fukata M, Takefuji M et al. (2004). Interaction with IQGAP1 links APC to Rac1, Cdc42, and actin filaments during cell polarization and migration. Dev Cell 7: 871–883.
150. Woodgett JR (1990). Molecular cloning and expression of glycogen synthase kinase-3/factor A. EMBO J 9: 2431–2438.
151. Wu G, Huang H, Garcia Abreu J, He X (2009). Inhibition of GSK3 phosphorylation of beta-catenin via phosphorylated PPPSPXS motifs of Wnt coreceptor LRP6. PLoS One 4: e4926.
152. 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.
153. Xing Y, Clements WK, Kimelman D, Xu W (2003). Crystal structure of a beta-catenin/axin complex suggests a mechanism for the beta-catenin destruction complex. Genes Dev 17: 2753–2764.
154. Xing Y, Clements WK, Le Trong I, Hinds TR, Stenkamp R, Kimelman D et al. (2004). Crystal structure of a beta-catenin/APC complex reveals a critical role for APC phosphorylation in APC function. Mol Cell 15: 523–533.
155. Xu W, Kimelman D (2007). Mechanistic insights from structural studies of beta-catenin and its binding partners. J Cell Sci 120: 3337–3344.
156. Xue B, Romero PR, Noutsou M, Maurice MM, Rudiger SG, William AM Jr et al. (2013). Stochastic machines as a colocalization mechanism for scaffold protein function. FEBS Lett 587: 1587–1591.
157. Yamamoto H, Hinoi T, Michiue T, Fukui A, Usui H, Janssens V et al. (2001). Inhibition of the Wnt signaling pathway by the PR61 subunit of protein phosphatase 2A. J Biol Chem 276: 26875–26882.
158. Yamamoto H, Kishida S, Kishida M, Ikeda S, Takada S, Kikuchi A (1999). Phosphorylation of axin, a Wnt signal negative regulator, by glycogen synthase kinase-3beta regulates its stability. J Biol Chem 274: 10681–10684.
159. Yang E, Tacchelly-Benites O, Wang Z, Randall MP, Tian A, Benchabane H et al. (2016). Wnt pathway activation by ADP-ribosylation. Nat Commun 7: 11430.
160. Yu N, Kakunda M, Pham V, Lill JR, Du P, Wongchenko M et al. (2015). HSP105 recruits protein phosphatase 2A to dephosphorylate beta-catenin. Mol Cell Biol 35: 1390–1400.
161. Zeng L, Fagotto F, Zhang T, Hsu W, Vasicek TJ, Perry WL 3rd et al. (1997). The mouse fused locus encodes axin, an inhibitor of the Wnt signaling pathway that regulates embryonic axis formation. Cell 90: 181–192.
162. Zeng X, Tamai K, Doble B, Li S, Huang H, Habas R et al. (2005). A dual-kinase mechanism for Wnt co-receptor phosphorylation and activation. Nature 438: 873–877.
163. Zhan T, Rindtorff N, Boutros M (2017). Wnt signaling in cancer. Oncogene 36: 1461–1473.
164. Zhang W, Yang J, Liu Y, Chen X, Yu T, Jia J et al. (2009). PR55 alpha, a regulatory subunit of PP2A, specifically regulates PP2A-mediated beta-catenin dephosphorylation. J Biol Chem 284: 22649–22656.
165. Zhang X, Lou Y, Zheng X, Wang H, Sun J, Dong Q et al. (2015). Wnt blockers inhibit the proliferation of lung cancer stem cells. Drug Des Devel Ther 9: 2399–2407.
166. Zhang Y, Liu S, Mickanin C, Feng Y, Charlat O, Michaud GA et al. (2011). RNF146 is a poly(ADP-ribose)-directed E3 ligase that regulates axin degradation and Wnt signalling. Nat Cell Biol 13: 623–629.
167. Zhang Y, Qiu WJ, Chan SC, Han J, He X, Lin SC (2002). Casein kinase I and casein kinase II differentially regulate axin function in Wnt and JNK pathways. J Biol Chem 277: 17706–17712.