A novel tankyrase inhibitor decreases canonical Wnt signaling in colon carcinoma cells and reduces tumor growth in conditional APC mutant mice

Cancer Research

Volumn 72, Issue 11, 2012, Pages 2822-2832

  Waaler, Jo ^a,b   Machon, Ondrej ^a,e   Tumova, Lucie ^e   Dinh, Huyen ^a   Korinek, Vladimir ^e   Wilson, Steven Ray ^b   Paulsen, Jan Erik ^c   Pedersen, Nina Marie ^d   Eide, Tor J ^d   Machonova, Olga ^a,e   Gradl, Dietmar ^f   Voronkov, Andrey ^a   Von Kries, Jens Peter ^g   Krauss, Stefan ^a  

^a OSLO UNIVERSITY HOSPITAL   (Norway)

^b UNIVERSITY OF OSLO   (Norway)

^c NORWEGIAN UNIVERSITY OF LIFE SCIENCES   (Norway)

^d OSLO UNIVERSITY HOSPITAL   (Norway)

^e INSTITUTE OF MOLECULAR GENETICS   (Czech Republic)

^f KARLSRUHE INSTITUTE OF TECHNOLOGY   (Germany)

^g LEIBNIZ INSTITUT FÜR MOLEKULARE PHARMAKOLOGIE   (Germany)

Author keywords

[No Author keywords available]

Indexed keywords

ANTINEOPLASTIC AGENT; BETA CATENIN; JW 55; NICOTINAMIDE ADENINE DINUCLEOTIDE ADENOSINE DIPHOSPHATE RIBOSYLTRANSFERASE; PROTEIN AXIN2; TAMOXIFEN; TANKYRASE; TANKYRASE 1; TANKYRASE 2; TANKYRASE INHIBITOR; UNCLASSIFIED DRUG; WNT PROTEIN;

ADENOMATOUS POLYPOSIS COLI GENE; ADENOSINE DIPHOSPHATE RIBOSYLATION; ALLELE; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CANCER INHIBITION; CARCINOMA CELL; COLON CARCINOMA; COLON POLYPOSIS; CONCENTRATION RESPONSE; CONTROLLED STUDY; EMBRYO; EMBRYO DEVELOPMENT; ENZYME ACTIVITY; ENZYME INHIBITION; FEMALE; GENE; GENE LOCUS; GENE MUTATION; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROTEIN DEFECT; PROTEIN DEGRADATION; PROTEIN DOMAIN; PROTEIN PROTEIN INTERACTION; PROTEIN STABILITY; PROTEIN TARGETING; SIGNAL TRANSDUCTION; XENOPUS;

4-AMINOBENZOIC ACID; ANIMALS; AXIN PROTEIN; BETA CATENIN; CELL LINE, TUMOR; CELL PROLIFERATION; COLONIC NEOPLASMS; DOSE-RESPONSE RELATIONSHIP, DRUG; ENZYME INHIBITORS; FEMALE; GENES, APC; HUMANS; MICE; MICE, KNOCKOUT; TANKYRASES; WNT SIGNALING PATHWAY; XENOPUS LAEVIS;

EID: 84861843671     PISSN: 00085472     EISSN: 15387445     Source Type: Journal    
DOI: 10.1158/0008-5472.CAN-11-3336     Document Type: Article

References (50)

1. Wend P, Holland JD, Ziebold U, Birchmeier W. Wnt signaling in stem and cancer stem cells. Semin Cell Dev Biol 2010;21:855-63.
2. Clevers H. Wnt/beta-catenin signaling in development and disease. Cell 2006;127:469-80.
3. Heuberger J, Birchmeier W. Interplay of cadherin-mediated cell adhesion and canonical Wnt signaling. Cold Spring Harb Perspect Biol 2010;2:a002915.
4. Huang SM, Mishina YM, Liu S, Cheung A, Stegmeier F, Michaud GA, et al. Tankyrase inhibition stabilizes axin and antagonizes Wnt signalling. Nature 2009;461:614-20.
5. Kimelman D, Xu W. beta-catenin destruction complex: insights and questions from a structural perspective. Oncogene 2006;25:7482-91. (Pubitemid 44885747)
6. Fearon ER. PARsing the phrase "all in for Axin"- Wnt pathway targets in cancer. Cancer Cell 2009;16:366-8.
7. Yeh TY, Sbodio JI, Chi NW. Mitotic phosphorylation of tankyrase, a PARP that promotes spindle assembly, by GSK3. Biochem Biophys Res Commun 2006;350:574-9. (Pubitemid 44547886)
8. Zhang Y, Liu S, Mickanin C, Feng Y, Charlat O, Michaud GA, et al. RNF146 is a poly(ADP-ribose)-directed E3 ligase that regulates axin degradation and Wnt signalling. Nat Cell Biol 2011;13:623-9.
9. Callow MG, Tran H, Phu L, Lau T, Lee J, Sandoval WN, et al. Ubiquitin ligase RNF146 regulates tankyrase and axin to promote Wnt signaling. PLoS One 2011;6:e22595.
10. Liu C, Li Y, Semenov M, Han C, Baeg GH, Tan Y, et al. Control of beta-catenin phosphorylation/degradation by a dual-kinase mechanism. Cell 2002;108:837-47. (Pubitemid 34327534)
11. Winston JT, Strack P, Beer-Romero P, Chu CY, Elledge SJ, Harper JW. The SCFbeta-TRCP-ubiquitin ligase complex associates specifically with phosphorylated destruction motifs in IkappaBalpha and beta-catenin and stimulates IkappaBalpha ubiquitination in vitro. Genes Dev 1999;13:270-83. (Pubitemid 29095799)
12. Goessling W, North TE, Loewer S, Lord AM, Lee S, Stoick-Cooper CL, et al. Genetic interaction of PGE2 and Wnt signaling regulates developmental specification of stem cells and regeneration. Cell 2009;136:1136-47.
13. Li X, Deng W, Lobo-Ruppert SM, Ruppert JM. Gli1 acts through Snail and E-cadherin to promote nuclear signaling by beta-catenin. Oncogene 2007;26:4489-98. (Pubitemid 47037042)
14. 2 regulates stem cells through Wnt/beta-catenin signalling. Nat Cell Biol 2010;12:1007-13.
15. Previdi S, Maroni P, Matteucci E, Broggini M, Bendinelli P, Desiderio MA. Interaction between human-breast cancer metastasis and bone microenvironment through activated hepatocyte growth factor/Met and beta-catenin/Wnt pathways. Eur J Cancer 2010;46:1679-91.
16. Lancaster MA, Schroth J, Gleeson JG. Subcellular spatial regulation of canonical Wnt signalling at the primary cilium. Nat Cell Biol 2011;13:700-7.
17. Jamieson C, Sharma M, Henderson BR. Regulation of beta-catenin nuclear dynamics by GSK-3beta involves a LEF-1 positive feedback loop. Traffic 2011;12:983-99.
18. Barker N, Clevers H. Mining the Wnt pathway for cancer therapeutics. Nat Rev Drug Discov 2006;5:997-1014. (Pubitemid 44835127)
19. MacDonald BT, Tamai K, He X. Wnt/beta-catenin signaling: components, mechanisms, and diseases. Dev Cell 2009;17:9-26.
20. Najdi R, Holcombe RF, Waterman ML. Wnt signaling and colon carcinogenesis: beyond APC. J Carcinog 2011;10:5.
21. Nieuwenhuis MH, Vasen HF. Correlations between mutation site in APC and phenotype of familial adenomatous polyposis (FAP): a review of the literature. Crit Rev Oncol Hematol 2007;61:153-61. (Pubitemid 46073779)
22. Chen B, Dodge ME, Tang W, Lu J, Ma Z, Fan CW, et al. Small molecule-mediated disruption of Wnt-dependent signaling in tissue regeneration and cancer. Nat Chem Biol 2009;5:100-7.
23. Curtin JC, Lorenzi MV. Drug discovery approaches to target Wnt signaling in cancer stem cells. Oncotarget 2010;1:563-77.
24. Thorne CA, Hanson AJ, Schneider J, Tahinci E, Orton D, Cselenyi CS, et al. Small-molecule inhibition of Wnt signaling through activation of casein kinase 1alpha. Nat Chem Biol 2010;6:829-36.
25. Verkaar F, Zaman GJ. New avenues to target Wnt/beta-catenin signaling. Drug Discov Today 2011;16:35-41.
26. Bodine PV, Stauffer B, Ponce-de-Leon H, Bhat RA, Mangine A, Seestaller-Wehr LM, et al. A small molecule inhibitor of the Wnt antagonist secreted frizzled-related protein-1 stimulates bone formation. Bone 2009;44:1063-8.
27. Chen M, Wang J, Lu J, Bond MC, Ren XR, Lyerly HK, et al. The antihelminthic niclosamide inhibits Wnt/Frizzled1 signaling. Biochemistry 2009;48:10267-74.
28. Shan J, Shi DL, Wang J, Zheng J. Identification of a specific inhibitor of the dishevelled PDZ domain. Biochemistry 2005;44:15495-503. (Pubitemid 41706133)
29. Chen Z, Venkatesan AM, Dehnhardt CM, Dos SO, Delos SE, yral-Kaloustian S, et al. 2,4-Diamino-quinazolines as inhibitors of betacatenin/Tcf-4 pathway: Potential treatment for colorectal cancer. Bioorg Med Chem Lett 2009;19:4980-3.
30. Emami KH, Nguyen C, Ma H, Kim DH, Jeong KW, Eguchi M, et al. A small molecule inhibitor of beta-catenin/CREB-binding protein transcription [corrected]. Proc Natl Acad Sci U S A 2004;101:12682-7. (Pubitemid 39122083)
31. Lepourcelet M, Chen YN, France DS, Wang H, Crews P, Petersen F, et al. Small-molecule antagonists of the oncogenic Tcf/beta-catenin protein complex. Cancer Cell 2004;5:91-102. (Pubitemid 38121599)
32. Park CH, Chang JY, Hahm ER, Park S, Kim HK, Yang CH. Quercetin, a potent inhibitor against beta-catenin/Tcf signaling in SW480 colon cancer cells. Biochem Biophys Res Commun 2005;328:227-34. (Pubitemid 40164659)
33. Hsiao SJ, Smith S. Tankyrase function at telomeres, spindle poles, and beyond. Biochimie 2008;90:83-92. (Pubitemid 350216209)
34. Waaler J, Machon O, von Kries JP, Wilson SR, Lundenes E, Wedlich D, et al. Novel synthetic antagonists of canonical Wnt signaling inhibit colorectal cancer cell growth. Cancer Res 2011;71:197-205.
35. Phiel CJ, Klein PS. Molecular targets of lithium action. Annu Rev Pharmacol Toxicol 2001;41:789-813. (Pubitemid 32385907)
36. Wang Z, Vogelstein B, Kinzler KW. Phosphorylation of beta-catenin at S33, S37, or T41 can occur in the absence of phosphorylation at T45 in colon cancer cells. Cancer Res 2003;63:5234-5. (Pubitemid 37139834)
37. Yang J, Zhang W, Evans PM, Chen X, He X, Liu C. Adenomatous polyposis coli (APC) differentially regulates beta-catenin phosphorylation and ubiquitination in colon cancer cells. J Biol Chem 2006;281:17751-7. (Pubitemid 44035574)
38. Hart MJ, de los SR, Albert IN, Rubinfeld B, Polakis P. Downregulation of beta-catenin by human Axin and its association with the APC tumor suppressor, beta-catenin and GSK3 beta. Curr Biol 1998;8:573-81. (Pubitemid 28222891)
39. Shultz MD, Kirby CA, Stams T, Chin DN, Blank J, Charlat O, et al. [1,2,4]Triazol-3-ylsulfanylmethyl)-3-phenyl-[1,2,4]oxadiazoles: Antagonists of the Wnt pathway that inhibit tankyrase 1&2 via novel adenosine pocket binding. J Med Chem 2012;55:1127-36.
40. Narwal M, Venkannagari H, Lehtio L. Structural basis of selective inhibition of human tankyrases. J Med Chem 2012;55:1360-7.
41. Parker GJ, Law TL, Lenoch FJ, Bolger RE. Development of high throughput screening assays using fluorescence polarization: nuclear receptor-ligand- binding and kinase/phosphatase assays. J Biomol Screen 2000;5:77-88. (Pubitemid 30243877)
42. Suzuki H, Watkins DN, Jair KW, Schuebel KE, Markowitz SD, Chen WD, et al. Epigenetic inactivation of SFRP genes allows constitutive WNT signaling in colorectal cancer. Nat Genet 2004;36:417-22. (Pubitemid 38437267)
43. Tetsu O, McCormick F. Beta-catenin regulates expression of cyclin D1 in colon carcinoma cells. Nature 1999;398:422-6. (Pubitemid 29180374)
44. van de WM, Sancho E, Verweij C, de Lau W, Oving I, Hurlstone A, et al. The beta-catenin/TCF-4 complex imposes a crypt progenitor phenotype on colorectal cancer cells. Cell 2002;111:241-50.
45. Barker N, van Es JH, Kuipers J, Kujala P, van den BM, Cozijnsen M, et al. Identification of stem cells in small intestine and colon by marker gene Lgr5. Nature 2007;449:1003-7. (Pubitemid 350014593)
46. Kuraguchi M, Wang XP, Bronson RT, Rothenberg R, Ohene-Baah NY, Lund JJ, et al. Adenomatous polyposis coli (APC) is required for normal development of skin and thymus. PLoS Genet 2006;2:e146.
47. Moser AR, Pitot HC, Dove WF. A dominant mutation that predisposes to multiple intestinal neoplasia in the mouse. Science 1990;247:322-4.
48. Barker N, Ridgway RA, van Es JH, van de WM, Begthel H, van den BM, et al. Crypt stem cells as the cells-of-origin of intestinal cancer. Nature 2009;457:608-11.
49. Batlle E, Henderson JT, Beghtel H, van den Born MM, Sancho E, Huls G, et al. Beta-catenin and TCF mediate cell positioning in the intestinal epithelium by controlling the expression of EphB/ephrinB. Cell 2002;111:251-63. (Pubitemid 35292445)
50. Merlos-Suarez A, Barriga FM, Jung P, Iglesias M, Cespedes MV, Rossell D, et al. The intestinal stem cell signature identifies colorectal cancer stem cells and predicts disease relapse. Cell Stem Cell 2011;8:511-24.