S-adenosylmethionine and methylthioadenosine inhibit β-catenin signaling by multiple mechanisms in liver and colon cancers

Molecular Pharmacology

Volumn 87, Issue 1, 2015, Pages 77-86

  Li, Tony W H ^a,b   Peng, Hui ^a,b   Yang, Heping ^a,b   Kurniawidjaja, Steven ^b   Panthaki, Parizad ^b   Zheng, Yuhua ^c   Mato, José M ^d   Lu, Shelly C ^a,b  

^a CEDARS SINAI MEDICAL CENTER   (United States)

^b UNIVERSITY OF SOUTHERN CALIFORNIA   (United States)

^c Department of Pediatric Gastroenterology Hepatology And Nutrition ^*  (United States)

^d INSTITUTO DE SALUD CARLOS III   (Spain)

Author keywords

[No Author keywords available]

Indexed keywords

5' METHYLTHIOADENOSINE; BETA CATENIN; CYCLIN D1; GLYCOGEN SYNTHASE KINASE 3BETA; METHIONINE ADENOSYLTRANSFERASE; METHIONINE ADENOSYLTRANSFERASE 1A; PHOSPHATIDYLINOSITOL 3 KINASE; PHOSPHOPROTEIN PHOSPHATASE 2A; PROTEIN KINASE B; S ADENOSYLMETHIONINE; UNCLASSIFIED DRUG; WNT PROTEIN; 5'-METHYLTHIOADENOSINE; DEOXYADENOSINE DERIVATIVE; NUCLEOSIDE;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CANCER MODEL; CANCER PREVENTION; CELL COMPARTMENTALIZATION; CELL NUCLEUS; COLITIS; COLON CANCER; CONTROLLED STUDY; DRUG MECHANISM; ENZYME INACTIVATION; HUMAN; HUMAN CELL; IMMUNOHISTOCHEMISTRY; LIVER CANCER; MALE; MOUSE; NONHUMAN; PROTEIN DEGRADATION; PROTEIN EXPRESSION; SIGNAL TRANSDUCTION; ANIMAL; COLONIC NEOPLASMS; DRUG EFFECTS; GENE EXPRESSION REGULATION; HCT116 CELL LINE; HEPG2 CELL LINE; LIVER NEOPLASMS; METABOLISM; NEOPLASMS, EXPERIMENTAL; PATHOLOGY; TUMOR CELL LINE;

ANIMALS; BETA CATENIN; CELL LINE, TUMOR; COLONIC NEOPLASMS; DEOXYADENOSINES; GENE EXPRESSION REGULATION, NEOPLASTIC; HCT116 CELLS; HEP G2 CELLS; HUMANS; LIVER NEOPLASMS; MICE; NEOPLASMS, EXPERIMENTAL; S-ADENOSYLMETHIONINE; SIGNAL TRANSDUCTION; THIONUCLEOSIDES;

EID: 84919764012     PISSN: 0026895X     EISSN: 15210111     Source Type: Journal    
DOI: 10.1124/mol.114.095679     Document Type: Article

References (42)

1. Anastas JN and Moon RT (2013) WNT signalling pathways as therapeutic targets in cancer. Nat Rev Cancer 13:11-26.
2. Ansorena E, García-Trevijano ER, Martínez-Chantar ML, Huang ZZ, Chen L, Mato JM, Iraburu M, Lu SC, and Avila MA (2002) S-adenosylmethionine and methylthioadenosine are antiapoptotic in cultured rat hepatocytes but proapoptotic in human hepatoma cells. Hepatology 35:274-280.
3. Bengochea A, de SouzaMM, Lefrançois L, Le Roux E, Galy O, Chemin I, KimM, Wands JR, Trepo C, and Hainaut P, et al. (2008) Common dysregulation of Wnt/Frizzled receptor elements in human hepatocellular carcinoma. Br J Cancer 99:143-150.
4. Brunet A, Kanai F, Stehn J, Xu J, Sarbassova D, Frangioni JV, Dalal SN, DeCaprio JA, Greenberg ME, and Yaffe MB (2002) 14-3-3 transits to the nucleus and participates in dynamic nucleocytoplasmic transport. J Cell Biol 156:817-828.
5. Carnero A (2010) The PKB/AKT pathway in cancer. Curr Pharm Des 16:34-44.
6. Chen H, Xia M, Lin M, Yang H, Kuhlenkamp J, Li T, Sodir NM, Chen YH, Josef-Lenz H, and Laird PW, et al. (2007) Role of methionine adenosyltransferase 2A and S-adenosylmethionine in mitogen-induced growth of human colon cancer cells. Gastroenterology 133:207-218.
7. Chen L. , Zeng Y., Yang H., Lee T.D., French S.W., Corrales F.J., García-Trevijano E.R., Avila M.A., Mato J.M., and Lu S.C. (2004) Impaired liver regeneration in mice lacking methionine adenosyltransferase 1A. FASEB J 18:914-916 .
8. Clevers H (2006) Wnt/beta-catenin signaling in development and disease. Cell 127: 469-480.
9. de La Coste A, Romagnolo B, Billuart P, Renard CA, Buendia MA, Soubrane O, Fabre M, Chelly J, Beldjord C, and Kahn A, et al. (1998) Somatic mutations of the betacatenin gene are frequent in mouse and human hepatocellular carcinomas. Proc Natl Acad Sci USA 95:8847-8851.
10. Desbois-Mouthon C, Cadoret A, Blivet-Van Eggelpoël MJ, Bertrand F, Cherqui G, Perret C, and Capeau J (2001) Insulin and IGF-1 stimulate the beta-catenin pathway through two signalling cascades involving GSK-3beta inhibition and Ras activation. Oncogene 20:252-259.
11. Fang D, Hawke D, Zheng Y, Xia Y, Meisenhelder J, Nika H, Mills GB, Kobayashi R, Hunter T, and Lu Z (2007) Phosphorylation of beta-catenin by AKT promotes betacatenin transcriptional activity. J Biol Chem 282:11221-11229.
12. nd of July 2014.
13. Gayet J, Zhou XP, Duval A, Rolland S, Hoang JM, Cottu P, and Hamelin R (2001) Extensive characterization of genetic alterations in a series of human colorectal cancer cell lines. Oncogene 20:5025-5032.
14. Giles RH, van Es JH, and Clevers H (2003) Caught up in a Wnt storm: Wnt signaling in cancer. Biochim Biophys Acta 1653:1-24.
15. Holland JD, Klaus A, Garratt AN, and Birchmeier W (2013) Wnt signaling in stem and cancer stem cells. Curr Opin Cell Biol 25:254-264.
16. Howe LR and Brown AM (2004) Wnt signaling and breast cancer. Cancer Biol Ther 3: 36-41.
17. Jacobs KM, Bhave SR, Ferraro DJ, Jaboin JJ, Hallahan DE, and Thotala D (2012) GSK-3β: a bifunctional role in cell death pathways. Int J Cell Biol 2012: 930710.
18. Janssens V and Goris J (2001) Protein phosphatase 2A: a highly regulated family of serine/threonine phosphatases implicated in cell growth and signalling. Biochem J 353:417-39.
19. Klaus A and Birchmeier W (2008) Wnt signalling and its impact on development and cancer. Nat Rev Cancer 8:387-398.
20. Kuo YC, Huang KY, Yang CH, Yang YS, Lee WY, and Chiang CW (2008) Regulation of phosphorylation of Thr-308 of Akt, cell proliferation, and survival by the B55alpha regulatory subunit targeting of the protein phosphatase 2A holoenzyme to Akt. J Biol Chem 283:1882-1892.
21. Lee CH, Hung HW, Hung PH, and Shieh YS (2010) Epidermal growth factor receptor regulates beta-catenin location, stability, and transcriptional activity in oral cancer. Mol Cancer 9:64.
22. Leulliot N, Quevillon-Cheruel S, Sorel I, Li de La Sierra-Gallay I, Collinet B, Graille M, Blondeau K, Bettache N, Poupon A, and Janin J, et al. (2004) Structure of protein phosphatase methyltransferase 1 (PPM1), a leucine carboxyl methyltransferase involved in the regulation of protein phosphatase 2A activity. J Biol Chem 279:8351-8358.
23. Li FQ, Mofunanya A, Harris K, and Takemaru K (2008) Chibby cooperates with 14-3-3 to regulate beta-catenin subcellular distribution and signaling activity. J Cell Biol 181:1141-1154.
24. Li J, Ramani K, Sun Z, Zee C, Grant EG, Yang H, XiaM, Oh P, Ko K, and Mato JM, et al. (2010) Forced expression of methionine adenosyltransferase 1A in human hepatoma cells suppresses in vivo tumorigenicity in mice. Am J Pathol 176:2456-2466.
25. Li TW, Yang H, Peng H, Xia M, Mato JM, and Lu SC (2012) Effects of S-adenosylmethionine and methylthioadenosine on inflammation-induced colon cancer in mice. Carcinogenesis 33:427-435.
26. Li TW, Zhang Q, Oh P, Xia M, Chen H, Bemanian S, Lastra N, Circ M, Moyer MP, and Mato JM, et al. (2009) S-Adenosylmethionine and methylthioadenosine inhibit cellular FLICE inhibitory protein expression and induce apoptosis in colon cancer cells. Mol Pharmacol 76:192-200.
27. Lu SC, Alvarez L, Huang ZZ, Chen L, An W, Corrales FJ, Avila MA, Kanel G, and Mato JM (2001) Methionine adenosyltransferase 1A knockout mice are predisposed to liver injury and exhibit increased expression of genes involved in proliferation. Proc Natl Acad Sci USA 98:5560-5565.
28. Lu SC and Mato JM (2012) S-adenosylmethionine in liver health, injury, and cancer. Physiol Rev 92:1515-1542.
29. Mazieres J, He B, You L, Xu Z, and Jablons DM (2005) Wnt signaling in lung cancer. Cancer Lett 222:1-10.
30. Mishra R (2010) Glycogen synthase kinase 3 beta: can it be a target for oral cancer. Mol Cancer 9:144.
31. Paul I, Bhattacharya S, Chatterjee A, and Ghosh MK (2013) Current understanding on EGFR and Wnt/β-catenin signaling in glioma and their possible crosstalk. Genes Cancer 4:427-446.
32. Peng H, Dara L, Li TW, Zheng Y, Yang H, Tomasi ML, Tomasi I, Giordano P, Mato JM, and Lu SC (2013) MAT2B-GIT1 interplay activates MEK1/ERK 1 and 2 to induce growth in human liver and colon cancer. Hepatology 57:2299-2313.
33. Pilarsky C, Wenzig M, Specht T, Saeger HD, and Grützmann R (2004) Identification and validation of commonly overexpressed genes in solid tumors by comparison of microarray data. Neoplasia 6:744-750.
34. Ramani K, Yang H, Xia M, Ara AI, Mato JM, and Lu SC (2008) Leptin's mitogenic effect in human liver cancer cells requires induction of both methionine adenosyltransferase 2A and 2beta. Hepatology 47:521-531.
35. Sharma M, Jamieson C, Johnson M, Molloy MP, and Henderson BR (2012) Specific armadillo repeat sequences facilitate β-catenin nuclear transport in live cells via direct binding to nucleoporins Nup62, Nup153, and RanBP2/Nup358. J Biol Chem 287:819-831.
36. Tomasi ML, Iglesias-Ara A, Yang H, Ramani K, Feo F, Pascale MR, Martínez-Chantar ML, Mato JM, and Lu SC (2009) S-adenosylmethionine regulates apurinic/apyrimidinic endonuclease 1 stability: implication in hepatocarcinogenesis. Gastroenterology 136:1025-1036.
37. Wei W, Chua MS, Grepper S, and So SK (2011) Soluble Frizzled-7 receptor inhibits Wnt signaling and sensitizes hepatocellular carcinoma cells towards doxorubicin. Mol Cancer 10: 16.
38. Yamaji S, Droggiti A, Lu SC, Martinez-Chantar ML, Warner A, and Varela-Rey M (2011) S-Adenosylmethionine regulates connexins sub-types expressed by hepatocytes. Eur J Cell Biol 90:312-322.
39. Yang H, Cho ME, Li TW, Peng H, Ko KS, Mato JM, and Lu SC (2013) MicroRNAs regulate methionine adenosyltransferase 1A expression in hepatocellular carcinoma. J Clin Invest 123:285-298.
40. Yang H, Sadda MR, Li M, Zeng Y, Chen L, Bae W, Ou X, Runnegar MT, Mato JM, and Lu SC (2004) S-adenosylmethionine and its metabolite induce apoptosis in HepG2 cells: role of protein phosphatase 1 and Bcl-x(S). Hepatology 40:221-231.
41. Zhai X, Yan K, Fan J, Niu M, Zhou Q, Zhou Y, Chen H, and Zhou Y (2013) The β-catenin pathway contributes to the effects of leptin on SREBP-1c expression in rat hepatic stellate cells and liver fibrosis. Br J Pharmacol 169:197-212.
42. Zhang N, Wei P, Gong A, Chiu WT, Lee HT, Colman H, Huang H, Xue J, Liu M, and Wang Y, et al. (2011) FoxM1 promotes β-catenin nuclear localization and controls Wnt target-gene expression and glioma tumorigenesis. Cancer Cell 20:427-442.