Inhibition of the Wnt/β-catenin signaling pathway improves the anti-tumor effects of sorafenib against hepatocellular carcinoma

Cancer Letters

Volumn 381, Issue 1, 2016, Pages 58-66

  Lin, Hsiao Hui ^a   Feng, Wen Chi ^a   Lu, Li Chun ^a,b   Shao, Yu Yun ^a,b   Hsu, Chih Hung ^a,b   Cheng, Ann Lii ^a,b  

^a NATIONAL TAIWAN UNIVERSITY   (Taiwan)

^b NATIONAL TAIWAN UNIVERSITY HOSPITAL   (Taiwan)

Author keywords

Hepatocellular carcinoma; ICG 001; Sorafenib; Wnt catenin

Indexed keywords

BETA CATENIN; N BENZYL 1,2,3,4,8,9 HEXAHYDRO 6 (4 HYDROXYBENZYL) 8 (1 NAPHTHYLMETHYL) 4,7 DIOXO 2H PYRAZINO[1,2 A]PYRIMIDINE 1(6H) CARBOXAMIDE; PROTEIN MCL 1; SORAFENIB; WNT PROTEIN; ANTINEOPLASTIC AGENT; APOPTOSIS REGULATORY PROTEIN; CARBANILAMIDE DERIVATIVE; CTNNB1 PROTEIN, HUMAN; FUSED HETEROCYCLIC RINGS; MCL1 PROTEIN, HUMAN; NICOTINAMIDE; PROTEIN KINASE INHIBITOR; PYRIMIDINONE DERIVATIVE;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; APOPTOSIS; ARTICLE; CANCER COMBINATION CHEMOTHERAPY; CHEMOSENSITIVITY; CONTROLLED STUDY; DRUG EFFECT; DRUG POTENTIATION; HUMAN; HUMAN CELL; IN VITRO STUDY; IN VIVO STUDY; LIVER CELL CARCINOMA; MALE; MONOTHERAPY; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; RNA INTERFERENCE; SIGNAL TRANSDUCTION; TUMOR XENOGRAFT; ANALOGS AND DERIVATIVES; ANIMAL; ANTAGONISTS AND INHIBITORS; BAGG ALBINO MOUSE; CARCINOMA, HEPATOCELLULAR; CELL PROLIFERATION; DOSE RESPONSE; DRUG EFFECTS; DRUG SCREENING; GENE EXPRESSION REGULATION; GENETIC TRANSFECTION; GENETICS; HEP-G2 CELL LINE; LIVER NEOPLASMS; METABOLISM; NUDE MOUSE; PATHOLOGY; RNAI THERAPEUTICS; WNT SIGNALING PATHWAY;

ANIMALS; ANTINEOPLASTIC COMBINED CHEMOTHERAPY PROTOCOLS; APOPTOSIS; APOPTOSIS REGULATORY PROTEINS; BETA CATENIN; BRIDGED BICYCLO COMPOUNDS, HETEROCYCLIC; CARCINOMA, HEPATOCELLULAR; CELL PROLIFERATION; DOSE-RESPONSE RELATIONSHIP, DRUG; GENE EXPRESSION REGULATION, NEOPLASTIC; HEP G2 CELLS; HUMANS; LIVER NEOPLASMS; MALE; MICE, INBRED BALB C; MICE, NUDE; MYELOID CELL LEUKEMIA SEQUENCE 1 PROTEIN; NIACINAMIDE; PHENYLUREA COMPOUNDS; PROTEIN KINASE INHIBITORS; PYRIMIDINONES; RNA INTERFERENCE; RNAI THERAPEUTICS; TRANSFECTION; WNT SIGNALING PATHWAY; XENOGRAFT MODEL ANTITUMOR ASSAYS;

EID: 84979704138     PISSN: 03043835     EISSN: 18727980     Source Type: Journal    
DOI: 10.1016/j.canlet.2016.07.013     Document Type: Article

References (38)

1. [1] Hsu, C.H., Shen, Y.C., Shao, Y.Y., Hsu, C., Cheng, A.L., Sorafenib in advanced hepatocellular carcinoma: current status and future perspectives. J. Hepat. Carcino 1 (2014), 85–99.
2. [2] Former, A., Llovet, J.M., Bruix, J., Hepatocellular carcinoma. Lancet 379 (2012), 1245–1255.
3. [3] Cheng, A.L., Kang, Y.K., Chen, Z., Tsao, C.J., Qin, S., Kim, J.S., et al. Efficacy and safety of sorafenib in patients in the Asia-Pacific region with advanced hepatocellular carcinoma: a phase III randomised, double-blind, placebo-controlled trial. Lancet Oncol 10 (2009), 25–34.
4. [4] Llovet, J.M., Ricci, S., Mazzaferro, V., Hilgard, P., Gane, E., Blanc, J.F., et al. Sorafenib in advanced hepatocellular carcinoma. N. Engl. J. Med 359 (2008), 378–390.
5. [5] Wilhelm, S.M., Carter, C., Tang, L., Wilkie, D., McNabola, A., Rong, H., et al. BAY 43–9006 exhibits broad spectrum oral antitumor activity and targets the RAF/MEK/ERK pathway and receptor tyrosine kinases involved in tumor progression and angiogenesis. Cancer Res 64 (2004), 7099–7109.
6. [6] Wilhelm, S., Carter, C., Lynch, M., Lowinger, T., Dumas, J., Smith, R.A., et al. Discovery and development of sorafenib: a multikinase inhibitor for treating cancer. Nat. Rev. Drug Discov 5 (2006), 835–844.
7. [7] Wilhelm, S.M., Adnane, L., Newell, P., Villanueva, A., Llovet, J.M., Lynch, M., Preclinical overview of sorafenib, a multikinase inhibitor that targets both Raf and VEGF and PDGF receptor tyrosine kinase signaling. Mol. Cancer Ther 10 (2008), 3129–3140.
8. [8] Hikita, H., Takehara, T., Shimizu, S., Kodama, T., Shigekawa, M., Iwase, K., et al. The Bcl-xL inhibitor, ABT737, efficiently induces apoptosis and suppresses growth of hepatoma cells in combination with sorafenib. Hepatology 52 (2010), 1310–1321.
9. [9] Galmiche, A., Ezzoukhry, Z., François, C., Louandre, C., Sabbagh, C., Nguyen-Khac, E., et al. BAD, a proapoptotic member of the BCL2 family, is a potential therapeutic target in hepatocellular carcinoma. Mol. Cancer Res 8 (2010), 1116–1125.
10. [10] Sonntag, R., Gassler, N., Bangen, J.M., Trautwein, C., Liedtke, C., Pro apoptotic Sorafenib signaling in murine hepatocytes depends on malignancy and is associated with PUMA expression in vitro and in vivo. Cell Death Dis, 5, 2014, e1030.
11. [11] Ou, D.L., Shen, Y.C., Liang, J.D., Liou, J.Y., Yu, S.L., Fan, H.H., et al. Induction of Bim expression contributes to the antitumor synergy between sorafenib and mitogen-activated protein kinase/extracellular signal-regulated kinase kinase inhibitor CI-1040 in hepatocellular carcinoma. Clin. Cancer Res 15 (2009), 5820–5828.
12. [12] Clevers, H., Wnt/beta-catenin signaling in development and disease. Cell 127 (2006), 469–480.
13. [13] Clevers, H., Nusse, R., Wnt/β-catenin signaling and disease. Cell 149 (2012), 1192–1205.
14. [14] Lachenmayer, A., Alsinet, C., Savic, R., Cabellos, L., Toffanin, S., Hoshida, Y., et al. Wnt-pathway activation in two molecular classes of hepatocellular carcinoma and experimental modulation by sorafenib. Clin. Cancer Res 18 (2012), 4997–5007.
15. [15] Guichard, C., Amaddeo, G., Imbeaud, S., Ladeiro, Y., Pelletier, L., Maad, I.B., et al. Integrated analysis of somatic mutations and focal copy-number changes identifies key genes and pathways in hepatocellular carcinoma. Nat. Genet 44 (2012), 694–698.
16. [16] Kan, Z., Zheng, H., Liu, X., Li, S., Barber, T.D., Gong, Z., et al. Whole-genome sequencing identifies recurrent mutations in hepatocellular carcinoma. Genome Res 23 (2013), 1422–1433.
17. [17] Amaddeo, G., Guichard, C., Imbeaud, S., Zucman-Rossi, J., Next-generation sequencing identified new oncogenes and tumor suppressor genes in human hepatic tumors. Oncoimmunology 1 (2012), 1612–1613.
18. [18] Hoshida, Y., Nijman, S.M., Kobayashi, M., Chan, J.A., Brunet, J.P., Chiang, D.Y., et al. Integrative transcriptome analysis reveals common molecular subclasses of human hepatocellular carcinoma. Cancer Res 69 (2009), 7385–7392.
19. [19] Cui, J., Jiang, W., Wang, S., Wang, L., Xie, K., Role of Wnt/β-catenin signaling in drug resistance of pancreatic cancer. Curr. Pharm. Des 18 (2012), 2464–2471.
20. [20] Amado, N.G., Predes, D., Fonseca, B.F., Cerqueira, D.M., Reis, A.H., Dudenhoeffer, A.C., et al. Isoquercitrin suppresses colon cancer cell growth in vitro by targeting the Wnt/β-catenin signaling pathway. J. Biol. Chem 289 (2014), 35456–35467.
21. [21] Loh, Y.N., Hedditch, E.L., Baker, L.A., Jary, E., Ward, R.L., Ford, C.E., The Wnt signalling pathway is upregulated in an in vitro model of acquired tamoxifen resistant breast cancer. BMC Cancer, 13, 2013, 174.
22. [22] Fung, T.K., So, C.W., Overcoming treatment resistance in acute promyelocytic leukemia and beyond. Oncotarget 4 (2013), 1128–1129.
23. [23] Liu, Y., Ye, X., Zhang, J.B., Ouyang, H., Shen, Z., Wu, Y., et al. PROX1 promotes hepatocellular carcinoma proliferation and sorafenib resistance by enhancing β-catenin expression and nuclear translocation. Oncogene 34 (2015), 5524–5535.
24. [24] Emami, K.H., Nguyen, C., Ma, H., Kim, D.H., Jeong, K.W., Eguchi, M., et al. A small molecule inhibitor of beta-catenin/CREB-binding protein transcription. Proc. Natl. Acad. Sci. U.S.A. 101 (2004), 12682–12687.
25. [25] Eguchi, M., Nguyen, C., Lee, S.C., Kahn, M., ICG-001, a novel small molecule regulator of TCF/beta-catenin transcription. Med. Chem 1 (2005), 467–472.
26. [26] Arensman, M.D., Telesca, D., Lay, A.R., Kershaw, K.M., Wu, N., Donahue, T.R., et al. The CREB-binding protein inhibitor ICG-001 suppresses pancreatic cancer growth. Mol. Cancer Ther 13 (2014), 2303–2314.
27. [27] Ma, H., Nguyen, C., Lee, K.S., Kahn, M., Differential roles for the coactivators CBP and p300 on TCF/beta-catenin-mediated survivin gene expression. Oncogene 24 (2005), 3619–3631.
28. [28] Takahashi-Yanaga, F., Kahn, M., Targeting Wnt signaling: can we safely eradicate cancer stem cells?. Clin. Cancer Res 16 (2010), 3153–3162.
29. [29] Yu, C., Bruzek, L.M., Meng, X.W., Gores, G.J., Carter, C.A., Kaufmann, S.H., et al. The role of Mcl-1 downregulation in the proapoptotic activity of the multikinase inhibitor BAY 43–9006. Oncogene 24 (2005), 6861–6869.
30. [30] Rahmani, M., Davis, E.M., Bauer, C., Dent, P., Grant, S., Apoptosis induced by the kinase inhibitor BAY 43–9006 in human leukemia cells involves down-regulation of Mcl-1 through inhibition of translation. J. Biol. Chem 280 (2005), 35217–35227.
31. [31] Yang, L., Perez, A.A., Fujie, S., Warden, C., Li, J., Wang, Y., et al. Wnt modulates MCL1 to control cell survival in triple negative breast cancer. BMC Cancer, 14, 2014, 124.
32. [32] Iqbal, S., Zhang, S., Driss, A., Liu, Z.R., Kim, H.R., Wang, Y., et al. PDGF upregulates Mcl-1 through activation of β-catenin and HIF-1α-dependent signaling in human prostate cancer cells. PLoS ONE, 7, 2012 e30764.
33. [33] Wei, Y., Shen, N., Wang, Z., Yang, G., Yi, B., Yang, N., et al. Sorafenib sensitizes hepatocellular carcinoma cell to cisplatin via suppression of Wnt/β-catenin signaling. Mol. Cell. Biochem 381 (2013), 139–144.
34. [34] Lin, Y.T., Chao, C.C., Identification of the β-catenin/JNK/prothymosin-alpha axis as a novel target of sorafenib in hepatocellular carcinoma cells. Oncotarget 6 (2015), 38999–39017.
35. [35] Muche, S., Kirschnick, M., Schwarz, M., Braeuning, A., Synergistic effects of β-catenin inhibitors and sorafenib in hepatoma cells. Anticancer Res 34 (2014), 4677–4683.
36. [36] Galuppo, R., Maynard, E., Shah, M., Daily, M.F., Chen, C., Spear, B.T., et al. Synergistic inhibition of HCC and liver cancer stem cell proliferation by targeting RAS/RAF/MAPK and Wnt/β-catenin pathways. Anticancer Res 34 (2014), 1709–1713.
37. [37] El-Khoueiry, A.B., Ning, Y., Yang, D., Cole, S., Kahn, M., Zoghbi, M., et al. A phase I first-in-human study of PRI-724 in patients (pts) with advanced solid tumors. J. Clin. Oncol, 31(Suppl.), 2013 Abstract 2501.
38. [38] Jimeno, A., Gordon, M.S., Chugh, R., Messersmith, W.A., Mendelson, D.S., Dupont, J., et al. A first-in-human phase 1 study of anticancer stem cell agent OMP-54F28 (FZD8-Fc), decoy receptor for WNT ligands, in patients with advanced solid tumors. J. Clin. Oncol, 32(Suppl.), 2014 Abstract 2505.