Protein phosphatase 2A is required for mesalazine-dependent inhibition of Wnt/β-catenin pathway activity

Carcinogenesis

Volumn 27, Issue 12, 2006, Pages 2371-2382

  Bos, Carina L ^a,c   Diks, Sander H ^b   Hardwick, James C H ^a   Walburg, Kimberley V ^a   Peppelenbosch, Maikel P ^b   Richel, Dick J ^a  

^a UNIVERSITY OF AMSTERDAM   (Netherlands)

^b UNIVERSITY OF GRONINGEN   (Netherlands)

^c ACADEMIC MEDICAL CENTER   (Netherlands)

Author keywords

[No Author keywords available]

Indexed keywords

BETA CATENIN; MESALAZINE; MUTANT PROTEIN; PHOSPHOPROTEIN PHOSPHATASE 2A; WNT PROTEIN;

ARTICLE; CANCER CELL CULTURE; CANCER PREVENTION; CELL CULTURE; CELL STRAIN HCT116; COLON POLYPOSIS; COLORECTAL CANCER; CONTROLLED STUDY; DRUG MECHANISM; ENTERITIS; ENZYME INHIBITION; GENE TARGETING; GENETIC TRANSFECTION; HUMAN; HUMAN CELL; IMMUNOPRECIPITATION; MOLECULAR MECHANICS; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN PHOSPHORYLATION; WESTERN BLOTTING;

ANTI-INFLAMMATORY AGENTS, NON-STEROIDAL; BETA CATENIN; CELL LINE, TUMOR; COLITIS, ULCERATIVE; COLONIC NEOPLASMS; COLORECTAL NEOPLASMS; HUMANS; KINETICS; MESALAMINE; PHOSPHOPROTEIN PHOSPHATASE; WNT PROTEINS;

EID: 33845352518     PISSN: 01433334     EISSN: 14602180     Source Type: Journal    
DOI: 10.1093/carcin/bgl071     Document Type: Article

References (58)

1. Husain,S.S., Szabo,I.L. and Tamawski,A.S. (2002) NSAID inhibition of GI cancer growth: Clinical implications and molecular mechanisms of action. Am. J. Gastroenterol., 97, 542-553.
2. Bjarnason,I., Hayllar,J., MacPherson,A.J. and Russell,A.S. (1993) Side effects of nonsteroidal anti-inflammatory drugs on the small and large intestine in humans. Gastroenterology, 104, 1832-1847.
3. Gabriel,S.E., Jaakkimainen,L. and Bombardier,C. (1991) Risk for serious gastrointestinal complications related to use of nonsteroidal anti-inflammatory drugs. A meta-analysis. Ann. Intern. Med., 115, 787-796.
4. Simon,L.S. (1996) Actions and toxicity of nonsteroidal anti-inflammatory drugs. Curr. Opin. Rheumatol., 8, 169-175.
5. Koehne,C.H. and Dubois,R.N. (2004) COX-2 inhibition and colorectal cancer. Semin. Oncol., 31, 12-21.
6. Schroeder,K.W. (2002) Role of mesalazine in acute and long-term treatment of ulcerative colitis and its complications. Scand. J. Gastroenterol. Suppl., 236, 42-47.
7. Stein,R.B. and Hanauer,S.B. (2000) Comparative tolerability of treatments for inflammatory bowel disease. Drug Saf., 23, 429-448.
8. Brown,W.A., Farmer,K.C., Skinner,S.A., Malcontenti-Wilson,C., Misajon,A. and O'Brien,P.E. (2000) 5-aminosalicyclic acid and olsalazine inhibit tumor growth in a rodent model of colorectal cancer. Dig. Dis. Sci., 45, 1578-1584.
9. Bus,P.J., Nagtegaal,I.D., Verspaget,H.W., Lamers,C.B., Geldof,H., Van Krieken,J.H. and Griffioen,G. (1999) Mesalazine-induced apoptosis of colorectal cancer: On the verge of a new chemopreventive era? Aliment. Pharmacol. Ther., 13, 1397-1402.
10. Reinacher-Schick,A., Seidensticker,F., Petrasch,S., Reiser,M., Philippou,S., Theegarten,D., Freitag,G. and Schmiegel,W. (2000) Mesalazine changes apoptosis and proliferation in normal mucosa of patients with sporadic polyps of the large bowel. Endoscopy, 32, 245-254.
11. Pinczowski,D., Ekbom,A., Baron,J., Yuen,J. and Adami,H.O. (1994) Risk factors for colorectal cancer in patients with ulcerative colitis: A case- control study. Gastroenterology, 107, 117-120.
12. Bansal,P. and Sonnenberg,A. (1996) Risk factors of colorectal cancer in inflammatory bowel disease. Am. J. Gastroenterol., 91, 44-48.
13. Eaden,J., Abrams,K., Ekbom,A., Jackson,E. and Mayberry,J. (2000) Colorectal cancer prevention in ulcerative colitis: A case-control study. Aliment. Pharmacol. Ther., 14, 145-153.
14. Moody,G.A., Jayanthi,V., Probert,C.S., Mac Kay,H. and Mayberry,J.F. (1996) Long-term therapy with sulphasalazine protects against colorectal cancer in ulcerative colitis: A retrospective study of colorectal cancer risk and compliance with treatment in Leicestershire. Eur. J. Gastroenterol. Hepatol., 8, 1179-1183.
15. Carter,M.J., Lobo,A.J. and Travis,S.P. (2004) Guidelines for the management of inflammatory bowel disease in adults. Gut, 53 (Suppl. 5), V1-V16.
16. Polakis,P. (2000) Wnt signaling and cancer. Genes Dev., 14, 1837-1851.
17. Behrens,J. and Lustig,B. (2004) The Wnt connection to tumorigenesis. Int. J. Dev. Biol., 48, 477-487.
18. Oving,I.M. and Clevers,H.C. (2002) Molecular causes of colon cancer. Eur. J. Clin. Invest., 32, 448-457.
19. Orford,K., Crockett,C., Jensen,J.P., Weissman,A.M. and Byers,S.W. (1997) Serine phosphorylation-regulated ubiquitination and degradation of beta-catenin. J. Biol. Chem., 272, 24735-24738.
20. Miller,J.R., Hocking,A.M., Brown,J.D. and Moon,R.T. (1999) Mechanism and function of signal transduction by the Wnt/beta-catenin and Wnt/Ca2+ pathways. Oncogene, 18, 7860-7872.
21. Mann,B., Gelos,M., Siedow,A. et al. (1999) Target genes of beta-catenin T-cell-factor/lymphoid-enhancer-factor signaling in human colorectal carcinomas. Proc. Natl Acad. Sci. USA, 96, 1603-1608.
22. Polakis,P. (1997) The adenomatous polyposis coli (APC) tumor suppressor. Biochim. Biophys. Acta, 1332, F127-F147.
23. Jass,J.R., Whitehall,V.L., Young,J. and Leggett,B.A. (2002) Emerging concepts in colorectal neoplasia. Gastroenterology, 123, 862-876.
24. Seidensticker,M.J. and Behrens,J. (2000) Biochemical interactions in the Wnt pathway. Biochim. Biophys. Acta, 1495, 168-182.
25. Seeling,J.M., Miller,J.R., Gil,R., Moon,R.T., White,R. and Virshup,D.M. (1999) Regulation of beta-catenin signaling by the B56 subunit of protein phosphatase 2A. Science, 283, 2089-2091.
26. Ratcliffe,M.J., Itoh,K. and Sokol,S.Y. (2000) A positive role for the PP2A catalytic subunit in Wnt signal transduction. J. Biol. Chem., 275, 35680-35683.
27. Schonthal,A.H. (2001) Role of serine/threonine protein phosphatase 2A in cancer. Cancer Lett., 170, 1-13.
28. van de Wetering,M., Cavallo,R., Dooijes,D. et al. (1997) Armadillo coactivates transcription driven by the product of the Drosophila segment polarity gene dTCF. Cell, 88, 789-799.
29. Versteeg,H.H., Spek,C.A., Slofstra,S.H., Diks,S.H., Richel,D.J. and Peppelenbosch,M.P. (2004) FVIIa:TF induces cell survival via G12/ G13-dependent Jak/STAT activation and BclXL production. Circ. Res., 94, 1032-1040.
30. Chung,H., Nairn,A.C., Murata,K. and Brautigan,D.L. (1999) Mutation of Tyr307 and Leu309 in the protein phosphatase 2A catalytic subunit favors association with the alpha 4 subunit which promotes dephosphorylation of elongation factor-2. Biochemistry, 38, 10371-10376.
31. Morin,P.J. (1999) Beta-catenin signaling and cancer. Bioessays, 21, 1021-1030.
32. Boon,E.M., van der Neut,R., van de Wetering,M., Clevers,H. and Pals,S.T. (2002) Wnt signaling regulates expression of the receptor tyrosine kinase met in colorectal cancer. Cancer Res., 62, 5126-5128.
33. Munemitsu,S., Albert,I., Souza,B., Rubinfeld,B. and Polakis,P. (1995) Regulation of intracellular beta-catenin levels by the adenomatous polyposis coli (APC) tumor-suppressor protein. Proc. Natl Acad. Sci. USA, 92, 3046-3050.
34. van Noort,M., van de Wetering,M. and Clevers,H. (2002) Identification of two novel regulated serines in the N terminus of beta-catenin. Exp. Cell Res., 276, 264-272.
35. Aberle,H., Bauer,A., Stappert,J., Kispert,A. and Kemler,R. (1997) Betacatenin is a target for the ubiquitin-proteasome pathway. EMBO J., 16, 3797-3804.
36. Morin,P.J., Sparks,A.B., Korinek,V., Barker,N., Clevers,H., Vogelstein,B. and Kinzler,K.W. (1997) Activation of beta-catenin-Tcf signaling in colon cancer by mutations in beta-catenin or APC. Science, 275, 1787-1790.
37. Serres,M., Grangeasse,C., Haftek,M., Durocher,Y., Duclos,B. and Schmitt,D. (1997) Hyperphosphorylation of beta-catenin on serine-threonine residues and loss of cell-cell contacts induced by calyculin A and okadaic acid in human epidermal cells. Exp. Cell Res., 231, 163-172.
38. Mistry,S.J., Li,H.C. and Atweh,G.F. (1998) Role for protein phosphatases in the cell-cycle-regulated phosphorylation of stathmin. Biochem. J., 334, 23-29.
39. Xie,H., Litersky,J.M., Hartigan,J.A., Jope,R.S. and Johnson,G.V. (1998) The interrelationship between selective tau phosphorylation and microtubule association. Brain Res., 798, 173-183.
40. Smal,C., Cardoen,S., Bertrand,L., Delacauw,A., Ferrant,A., Van den Berghe,G., Van Den Neste,E. and Bontemps,F. (2004) Activation of deoxycytidine kinase by protein kinase inhibitors and okadaic acid in leukemic cells. Biochem. Pharmacol., 68, 95-103.
41. Favre,B., Turowski,P. and Hemmings,B.A. (1997) Differential inhibition and posttranslational modification of protein phosphatase 1 and 2A in MCF7 cells treated with calyculin-A, okadaic acid, and tautomycin. J. Biol. Chem., 272, 13856-13863.
42. Nunbhakdi-Craig,V., Machleidt,T., Ogris,E., Bellotto,D., White,C.L.,II and Sontag,E. (2002) Protein phosphatase 2A associates with and regulates atypical PKC and the epithelial tight junction complex. J. Cell. Biol., 158, 967-978.
43. Schmiegel,W., Pox,C.P. and Reiser,M. (2004) Effect of 5-aminosalicylate (5-ASA) on the recurrence rate of sporadic colorectal adenomas. Gastroenterology, 126, A452.
44. Ritland,S.R., Leighton,J.A., Hirsch,R.E., Morrow,J.D., Weaver,A.L. and Gendler,S.J. (1999) Evaluation of 5-aminosalicylic acid (5-ASA) for cancer chemoprevention: Lack of efficacy against nascent adenomatous polyps in the Apc(Min) mouse. Clin. Cancer Res., 5, 855-863.
45. MacGregor,D.J., Kim,Y.S., Sleisenger,M.H. and Johnson,L.K. (2000) Chemoprevention of colon cancer carcinogenesis by balsalazide: inhibition of azoxymethane-induced aberrant crypt formation in the rat colon and intestinal tumor formation in the B6-Min/+ mouse. Int. J. Oncol., 17, 173-179.
46. Kaiser,G.C., Yan,F. and Polk,D.B. (1999) Mesalamine blocks tumor necrosis factor growth inhibition and nuclear factor kappaB activation in mouse colonocytes. Gastroenterology, 116, 602-609.
47. Yan,F. and Polk,D.B. (1999) Aminosalicylic acid inhibits IkappaB kinase alpha phosphorylation of IkappaBalpha in mouse intestinal epithelial cells. J. Biol. Chem., 274, 36631-36636.
48. Dooley,T.P., Curto,E.V., Reddy,S.P., Davis,R.L., Lambert,G.W., Wilborn,T.W. and Elson,C.O. (2004) Regulation of gene expression in inflammatory bowel disease and correlation with IBD drugs: Screening by DNA microarrays. Inflamm. Bowel Dis., 10, 1-14.
49. Egan,L.J., Mays,D.C., Huntoon,C.J., Bell,M.P., Pike,M.G., Sandborn,W.J., Lipsky,J.J. and McKean,D.J. (1999) Inhibition of interleukin-1-stimulated NF-kappaB RelA/p65 phosphorylation by mesalamine is accompanied by decreased transcriptional activity. J. Biol. Chem., 274, 26448-26453.
50. Gasche,C., Goel,A., Natarajan,L. and Boland,C.R. (2005) Mesalazine improves replication fidelity in cultured colorectal cells. Cancer Res., 65, 3993-3997.
51. Reinacher-Schick,A., Schoeneck,A., Graeven,U., Schwarte-Waldhoff,I. and Schmiegel,W. (2003) Mesalazine causes a mitotic arrest and induces caspase-dependent apoptosis in colon carcinoma cells. Carcinogenesis, 24, 443-451.
52. Allgayer,H. (2003) Review article: Mechanisms of action of mesalazine in preventing colorectal carcinoma in inflammatory bowel disease. Aliment. Pharmacol. Ther., 18 (Suppl. 2), 10-14.
53. Lauritsen,K., Hansen,J., Ryde,M. and Rask-Madsen,J. (1984) Colonic azodisalicylate metabolism determined by in vivo dialysis in healthy volunteers and patients with ulcerative colitis. Gastroenterology, 86, 1496-1500.
54. Frieri,G., Pimpo,M.T., Palumbo,G.C., Onori,L., Viscido,A., Latella,G., Galletti,B., Pantaleoni,G.C. and Caprilli,R. (1999) Rectal and colonic mesalazine concentration in ulcerative colitis: Oral vs. oral plus topical treatment. Aliment. Pharmacol. Ther., 13, 1413-1417.
55. Staal,F.J., Noort Mv,M., Strous,G.J. and Clevers,H.C. (2002) Wnt signals are transmitted through N-terminally dephosphorylated beta-catenin. EMBO Rep., 3, 63-68.
56. Sadot,E., Conacci-Sorrell,M., Zhurinsky,J., Shnizer,D., Lando,Z., Zharhary,D., Kam,Z., Ben-Ze'ev,A. and Geiger,B. (2002) Regulation of S33/ S37 phosphorylated beta-catenin in normal and transformed cells. J. Cell. Sci., 115, 2771-2780.
57. Yang,J., Wu,J., Tan,C. and Klein,P.S. (2003) PP2A:B56epsilon is required for Wnt/beta-catenin signaling during embryonic development. Development, 130, 5569-5578.
58. Everett,A.D., Kamibayashi,C. and Brautigan,D.L. (2002) Transgenic expression of protein phosphatase 2A regulatory subunit B56gamma disrupts distal lung differentiation. Am. J. Physiol. Lung Cell. Mol. Physiol., 282, L1266-L1271.