The activation of beta-catenin by Wnt signaling mediates the effects of histone deacetylase inhibitors

Experimental Cell Research

Volumn 313, Issue 8, 2007, Pages 1652-1666

  Bordonaro, Michael ^a   Lazarova, Darina L ^a   Sartorelli, Alan C ^a  

^a YALE CANCER CENTER   (United States)

Author keywords

Apoptosis; Butyrate; Colorectal carcinomas; Histone deacetylase inhibitor; Wnt signaling

Indexed keywords

BETA ACTIN; BUTYRIC ACID; DNA; HISTONE DEACETYLASE INHIBITOR; LITHIUM CHLORIDE; LUCIFERASE; WNT PROTEIN;

APOPTOSIS; ARTICLE; CANCER CELL; CELL CULTURE; CELL DEATH; CELL STRAIN HEK293; COLORECTAL CARCINOMA; CONTROLLED STUDY; DEPHOSPHORYLATION; EMBRYO; ENZYME ASSAY; ENZYME INHIBITION; GENETIC TRANSFECTION; HUMAN; HUMAN CELL; PLASMID; PRIORITY JOURNAL; SIGNAL TRANSDUCTION; TRANSCRIPTION REGULATION; WESTERN BLOTTING;

EID: 34247157352     PISSN: 00144827     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.yexcr.2007.02.008     Document Type: Article

References (72)

1. Marks P.A., and Dokmanovic M. Histone deacetylase inhibitors: discovery and development as anticancer agents. Expert Opin. Investig. Drugs 12 (2005) 1497-1511
2. Bolden J.E., Peart M.J., and Johnstone R.W. Anticancer activities of histone deacetylase inhibitors. Nat. Rev. 5 (2006) 769-784
3. Di Gennaro E., Bruzzese F., Caraglia M., Abruzzese A., and Budillon A. Acetylation of proteins as novel target for antitumor therapy: review article. Amino Acids 26 (2004) 435-441
4. Villar-Garea A., and Esteller M. Histone deacetylase inhibitors: understanding a new wave of anticancer agents. Int. J. Cancer 112 (2004) 171-178
5. Monneret C. Histone deacetylase inhibitors. Eur. J. Med. Chem. 40 (2005) 1-13
6. Lin H.-Y., Chen C.-S., Lin S.-P., Weng J.-R., and Chen C.-S. Targeting histone deacetylase in cancer therapy. Med. Res. Rev. 26 (2006) 397-413
7. Bordonaro M., Mariadason J.M., Aslam F., Heerdt B.G., and Augenlicht L.H. Butyrate-induced apoptotic cascade in colonic carcinoma cells: modulation of the beta-catenin-Tcf pathway and concordance with effects of sulindac and trichostatin A but not curcumin. Cell Growth Differ. 10 (1999) 713-720
8. Bordonaro M., Lazarova D.L., Augenlicht L.H., and Sartorelli A.C. Cell type- and promoter-dependent modulation of the wnt signaling pathway by sodium butyrate. Int. J. Cancer 97 (2002) 42-51
9. Klingensmith J., Nusse R., and Perrimon N. The Drosophila segment polarity gene dishevelled encodes a novel protein required for response to the wingless signal. Genes Dev. 8 (1994) 118-130
10. Theisen H., Purcell J., Bennett M., Kansagara D., Syed A., and Marsh J.L. Dishevelled is required during wingless signaling to establish both cell polarity and cell identity. Development 120 (1994) 347-360
11. Woodgett J. Regulation and functions of the glycogen synthase kinase-3 subfamily. Semin. Cancer Biol. 5 (1994) 269-275
12. Cook D., Fry M., Hughes K., Sumathipala R., Woodgett J., and Dale T. Wingless inactivates glycogen synthase kinase-3 via an intracellular signaling pathway which involves a protein kinase C. EMBO J. 15 (1996) 4526-4536
13. Rubinfeld B., Souza B., Albert I., Muller O., Chamberlain S.H., Masiarz F.R., Munimetsu S., and Polakis P. Association of the APC gene product with β-catenin. Science 262 (1993) 1731-1734
14. Su L.-K., Vogelstein B., and Kinzler K.W. Association of the APC tumor suppresser protein with catenins. Science 262 (1993) 1734-1737
15. Munemitsu S., Albert I., Souza B., Rubinfeld B., and Polakis P. Regulation of intracellular β-catenin levels by the adenomatous polyposis coli (APC) tumor-suppressor protein. Proc. Natl. Acad. Sci. U. S. A. 92 (1995) 3046-3050
16. Van de Wetering M., Osterwegel M., Dooijes D., and Clevers H. Identification and cloning of Tcf-1, a T lymphocyte-specific transcription factor containing a sequence-specific HMG box. EMBO J. 10 (1991) 123-132
17. Behrens J., Von Kries J.P., Kuhl M., Bruhn L., Wedlich D., Grosschedl R., and Birchmeier W. Functional interaction of β-catenin with the transcriptional factor LEF-1. Nature 382 (1996) 638-642
18. Molenaar M., Van De Wetering M., and Osterwegel M. XTcf-3 transcription factor mediates β-catenin-induced axis formation in Xenopus embryos. Cell 86 (1996) 391-399
19. Korinek V., Barker N., Morin P.J., Van Wichen D., De Weger R., Kinzler K.W., Vogelstein B., and Clevers H. Constitutive transcriptional activation by a beta-catenin-Tcf complex in APC-/- colon carcinoma. Science 275 (1997) 1784-1787
20. Morin J., Sparks A.B., Korinek V., Barker N., Clevers H., Vogelstein B., and Kinzler K.W. Activation of beta-catenin-Tcf signaling in colon cancer by mutations in beta-catenin or APC. Science 275 (1997) 1787-1790
21. Kinzler K.W., and Vogelstein B. Lessons from hereditary colorectal cancer. Cell 8 (1996) 159-170
22. Miyaki M., Iijima T., Kimura J., Yasuno M., Mori T., Hayashi Y., Koike M., Hitara N., Iwama T., and Kuroki T. Frequent mutation of β-catenin and APC genes in primary colorectal tumors from patients with hereditary nonpolyposis colorectal cancer. Cancer Res. 59 (1999) 4506-4509
23. Roose J., and Clevers H. Tcf transcription factors: molecular switches in carcinogenesis. Biochim. Biophys. Acta 87456 (1999) M23-M27
24. Ahmed Y., Hayashi S., Levine A., and Wieschaus E. Regulation of Armadillo by a Drosophila APC inhibits neuronal apoptosis during retinal development. Cell 93 (1998) 1171-1182
25. Romagnolo B., Berrebi D., Saadi-Keddoucci S., Porteu A., Pichard A.-I., Peuchmaur M., Vandewalle A., Kahn A., and Perret C. Intestinal dysplasia and adenoma in transgenic mice after overexpression of an activated β-catenin. Cancer Res. 59 (1999) 3875-3879
26. Albuquerque C., Breukel C., van der Luijt R., Fidalgo P., Lage P., Slors F.J., Leitao C.N., Fodde R., and Smits R. 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 (2002) 549-1560
27. Hasegawa S., Sato T., Akazawa H., Okada H., Maeno A., Ito M., Sugitani Y., Shibata H., Miyazaki J., Katsuki M., Yamauchi Y., Yamamura K., Katamine S., and Noda T. Apoptosis in neural crest cells by functional loss of APC tumor suppressor gene. Proc. Natl. Acad. Sci. U. S. A. 99 (2002) 297-302
28. Wong M.H., Huelsken J., Birchmeier W., and Gordon J.I. Selection of multipotent stem cells during morphogenesis of small intestinal crypts of Lieberkühn is perturbed by stimulation of Lef1/β-catenin signaling. J. Biol. Chem. 277 (2002) 15843-15850
29. Lazarova D.L., Bordonaro M., Carbone R., and Sartorelli A.C. Linear relationship between WNT activity levels and apoptosis in colorectal carcinoma cells exposed to butyrate. Int. J. Cancer 110 (2004) 523-531
30. Scheppach W., Bartram P., Richter A., Richter F., Liepold H., Dusel G., Hofstetter G., Ruthlein J., and Kasper H. Effect of short-chain fatty acids on the human colonic mucosa in vitro. J. Parenter. Enteral Nutr. 16 (1992) 43-48
31. Bingham S.A., Day N.E., Luben R., Ferrari P., Slimani N., Norat T., Clavel-Chapelon F., Kesse E., Nieters A., Boeing H., Tjonneland A., Overvad K., Martinez C., Dorronsoro M., Gonzalez C.A., Key T.J., Trichopoulou A., Naska A., Vineis P., Tumino R., Krogh V., Bueno-de-Mesquita H.B., Peeters P.H.M., Berglund G., Hallmans G., Lund E., Skeie G., Kaaks R., and Riboli E. Dietary fibre in food and protection against colorectal cancer in the European Prospective Investigation into Cancer and Nutrition (EPIC): an observational study. The Lancet 361 (2003) 1496-1501
32. Peters U., Sinha R., Chaterjee N., Subar A.F., Ziegler R.G., Kuldorf M., Bresalier R., Weissfeld J.L., Flood A., Schtzkin A., and Hayes R.B. Dietary fibre and colorectal adenoma in a colorectal cancer early detection programme. The Lancet 361 (2003) 1491-1495
33. Lazarova D.L., Bordonaro M., and Sartorelli A.C. Transcriptional regulation of the vitamin D (3) receptor gene by ZEB. Cell Growth Differ. 12 (2001) 319-326
34. Van de Wetering M., Castrop J., Korinek V., and Clevers H. Extensive alternative splicing and dual promoter usage generate Tcf-1 protein isoforms with differential transcription control properties. Mol. Cell. Biol. 16 (1996) 745-752
35. Staal F.J., Noort My.M., Strous G.J., and Clevers H.C. Wnt signals are transmitted through N-terminally dephosphorylated beta-catenin. EMBO Rep. 3 (2002) 63-68
36. Van Noort N., Meeldjik J., van der Zee R., Destree O., and Clevers H. Wnt signaling controls the phosphorylation status of beta-catenin. J. Biol. Chem. 277 (2002) 17901-17905
37. Seeling J.M., Miller J.R., Gil R., Moon R.T., White R., and Virshup D.M. Regulation of beta-catenin signaling by the B56 subunit of protein phosphatase 2A. Science 283 (1999) 2089-2091
38. Ratcliffe M.J., Itoh K., and Sokol S.Y. A positive role for the PP2A catalytic subunit in Wnt signal transduction. J. Biol. Chem. 275 (2000) 35680-35683
39. Li X., Yost H.J., Virshup D.M., and Seeling J.M. Protein phosphatase 2A and its B56 regulatory subunit inhibit Wnt signaling in Xenopus. EMBO J. 20 (2001) 4122-4131
40. Wilson J., Velcich A., Arango D., Kurland A.R., Shenoy S.M., Pezo R.C., Levsky J.M., Singer R.H., and Augenlicht L.H. Novel detection and differential utilization of a c-myc transcriptional block in colon cancer chemoprevention. Cancer Res. 62 (2002) 6006-6010
41. Heruth D.P., Zirnstein G.W., Bradley J.F., and Rothberg P.G. Sodium butyrate causes an increase in the block to transcriptional elongation in the c-myc gene in SW837 rectal carcinoma cells. J. Biol. Chem. 268 (1993) 20466-20472
42. Yu X., Riese J., Eresh S., and Bienz M. Transcriptional repression due to high levels of Wingless signaling. EMBO J. 17 (1998) 7021-7032
43. Ziegler S., Rohrs S., Tickenbrock L., Moroy T., Klein-Hitpass L., Vetter I.R., and Muller O. Novel target genes of the Wnt pathway and statistical insights into Wnt target promoter regulation. FEBS J. 272 (2005) 1600-1615
44. Garcia A., Cereghini S., and Sontag E. Protein phosphatase 2A and phosphatidylinositol 3-kinase regulate the activity of Sp1-responsive promoters. J. Biol. Chem. 275 (2000) 9385-9389
45. Bafico A., Liu G., Yaniv A., Gazit A., and Aaronson S.A. Novel mechanism of Wnt signaling inhibition mediated by Dickkopf-1 interaction with LRP6/Arrow. Nat. Cell Biol. 3 (2001) 683-686
46. Mao B., Wu W., Li Y., Hoppe D., Stannek P., Glinka A., and Niehrs C. LDL-receptor-related protein 6 is a receptor for Dickkopf proteins. Nature 411 (2001) 321-325
47. Semenov M.V., Tamai K., Brott B.K., Kuhl M., Sokol S., and He X. Head inducer Dickkopf-1 is a ligand for Wnt coreceptor LRP6. Curr. Biol. 11 (2001) 951-961
48. Holcombe R.F., Marsh J.L., Waterman M.L., Lin F., Milovanovic T., and Truong T. Expression of Wnt ligands and Frizzled receptors in colonic mucosa and in colon carcinoma. Mol. Pathol. 55 (2002) 220-226
49. Jones S.E., and Jomary C. Secreted Frizzled-related proteins: searching for relationships and patterns. BioEssays 24 (2002) 811-820
50. Kawano Y., and Kypta R. Secreted antagonists of the Wnt signaling pathway. J. Cell Sci. 116 (2003) 2627-2634
51. Scheppach W., and Weiler F. The butyrate story: old wine in new bottles?. Curr. Opin. Clin. Nutr. Metab. Care 7 (2004) 563-567
52. Hurlstone A., and Clevers H. T-cell factors: turn-ons and turn-offs. EMBO J. 21 (2002) 2303-2311
53. Freeman M., and Bienz M. EGF receptor/rolled MAP kinase signalling protects cells against activated Armadillo in the Drosophila eye. EMBO Rep. 2 (2001) 157-162
54. 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
55. Gaspar C., and Fodde R. APC dosage effects in tumorigenesis and stem cell differentiation. Int. J. Dev. Biol. 48 (2004) 377-386
56. Waltzer L., Vandel L., and Bienz M. Teashirt is required for transcriptional repression mediated by high Wingless levels. EMBO J. 20 (2001) 137-145
57. Battaille F., Rogler G., Modes K., Poser I., Schuierer M., Dietmaier W., Ruemmele P., Muhlbauer M., Wallner S., Hellerbrand C., and Bosserhoff A.K. Strong expression of methylthioadenosine phosphorylase (MTAP) in human colon carcinoma cells is regulated by TCF1/[beta]-catenin. Lab. Invest. 85 (2005) 124-136
58. Crawford H.C., Fingleton B.M., Rudolph-Owen L.A., Goss K.J., Rubinfeld B., Polakis P., and Matrisian L.M. The metalloproteinase matrilysin is a target of beta-catenin transactivation in intestinal tumors. Oncogene 18 (1999) 2883-2891
59. Bafico A., Liu G., Goldin L., Harris V., and Aaronson S.A. An autocrine mechanism for constitutive Wnt pathway activation in human cancer cells. Cancer Cell 6 (2004) 497-506
60. Suzuki H., Watkins D.N., Jair K.-W., Schuebel K.E., Markowitz S.D., Chen W.D., Pretlow T.P., Yang B., Akiyama Y., van Engeland M., Toyota M., Tokino T., Hinoda Y., Imai K., Herman J.G., and Baylin S.B. Epigenetic inactivation of SFRP genes allows constitutive WNT signaling in colorectal cancer. Nat. Gen. 36 (2004) 417-422
61. Smith K., Bui T.D., Poulsom R., Kaklamanis L., Williams G., and Harris A.L. Up-regulation of macrophage wnt gene expression in adenoma-carcinoma progression of human colorectal cancer. Br. J. Cancer 81 (1999) 496-502
62. Dimitriadis A., Vincan E., Mohammed I.M., Roczo N., Phillips W.A., and Baindur-Hudson S. Expression of Wnt genes in human colon cancers. Cancer Lett. 166 (2001) 185-191
63. Roose J., Huls G., van Beest M., Moerer P., van der Horn K., Goldschmeding R., Logtenberg T., and Clevers H. Synergy between tumor suppressor APC and the beta-catenin-Tcf4 target Tcf1. Science 285 (1999) 1923-1926
64. Gregorieff A., Pinto D., Begthel H., Destree O., Kielman M., and Clevers H. Expression pattern of wnt signaling components in the adult intestine. Gastroenterology 129 (2005) 626-638
65. Ishitani T., Ninomiya-Tsuji J., Nagaii S., Nishita M., Meneghini M., Barker N., Waterman M., Bowerman B., Clevers H., Shibuya H., and Matsumoto K. TAK1-NLK-MAPK-related pathway antagonizes signalling between beta-catenin and transcription factor TCF. Nature 399 (1999) 798-802
66. Snider L., Thirlwell H., Miller J.R., Moon R.T., Groudine M., and Tapscott S.J. Inhibition of Tcf3 binding by I-mfa domain proteins. Mol. Cell. Biol. 21 (2001) 1866-1873
67. Park M.W., Choi K.H., and Jeong S. Inhibition of the DNA binding by the TCF-1 binding RNA aptamer. Biochem. Biophys. Res. Commun. 330 (2005) 11-17
68. Park C.H., Hahm E.R., Lee J.H., Jung K.C., Lee H.S., and Yang C.H. Ionomycin downregulates {beta}-catenin/Tcf signaling in colon cancer cell line. Carcinogenesis 26 (2005) 1929-1933
69. Xu W., Ngo L., Perez G., Dokmanovic M., and Marks P. Intrinsic apoptotic and thioredoxin pathways in human prostate cancer cell response to histone deacetylase inhibitor. Proc. Natl. Acad. Sci. U. S. A. 103 (2006) 15540-15545
70. Zhu H., Mazor M., Kawano Y., Walker M.M., Leung H.Y., Armstrong K., Waxman J., and Kypta R.M. Analysis of Wnt gene expression in prostate cancer: mutual inhibition by WNT11 and the androgen receptor. Cancer Res. 64 (2004) 7918-7926
71. Yang X., Chen M.-W., Terry S., Vacherot F., Chopin D.K., Bemis D.L., Kitajewski J., Benson M.C., Guo Y., and Buttyan R. A human- and male-specific protocadherin that acts through the Wnt signaling pathway to induce neuroendocrine transdifferentiation of prostate cancer cells. Cancer Res. 65 (2005) 5263-5271
72. Zi X., Guo Y., Simoneau A.R., Hope C., Xie J., Holcombe R.F., and Hoang B.H. Expression of frzb/secreted frizzled-related protein 3, a secreted Wnt antagonist, in human androgen-independent prostate cancer PC-3 cells suppresses tumor growth and cellular invasiveness. Cancer Res. 65 (2005) 9762-9770