Wnt5a enhances the response of CML cells to Imatinib Mesylate through JNK activation and γ-catenin inhibition

Leukemia Research

Volumn 37, Issue 11, 2013, Pages 1532-1537

  Niu, Chang Chun ^a   Zhao, Chen ^a,b   Zhang, Xiao Li ^a   Pan, Jing ^a   Wu, Wei Ru ^a   Li, Zhi Qiang ^a   Liu, Tao ^a   Yang, Zhong ^a   Si, Wei Ke ^a  

^a THIRD MILITARY MEDICAL UNIVERSITY   (China)

^b CHONGQING MEDICAL UNIVERSITY   (China)

Author keywords

Catenin; Catenin; Chronic myeloid leukaemia; Imatinib Mesylate; JNK; Wnt5a

Indexed keywords

BETA CATENIN; IMATINIB; JANUS KINASE; PLAKOGLOBIN; SURVIVIN; WNT5A PROTEIN;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ANTIPROLIFERATIVE ACTIVITY; ARTICLE; CHRONIC MYELOID LEUKEMIA; CONTROLLED STUDY; DRUG CYTOTOXICITY; DRUG EFFECT; DRUG MECHANISM; DRUG RESPONSE; DRUG TARGETING; ENZYME ACTIVITY; ENZYME ASSAY; FEMALE; GROWTH INHIBITION; IN VIVO STUDY; MOLECULAR DYNAMICS; MOUSE; NONHUMAN; ONCOGENE; PRIORITY JOURNAL; PROTEIN DETERMINATION; PROTEIN EXPRESSION; PROTEIN FUNCTION; SIGNAL TRANSDUCTION; SURVIVIN GENE; TUMOR XENOGRAFT;

Β-CATENIN; Γ-CATENIN; CHRONIC MYELOID LEUKAEMIA; IMATINIB MESYLATE; JNK; WNT5A;

ANIMALS; ANTINEOPLASTIC AGENTS; APOPTOSIS; BENZAMIDES; BLOTTING, WESTERN; CELL PROLIFERATION; FLOW CYTOMETRY; GAMMA CATENIN; HUMANS; LEUKEMIA, MYELOGENOUS, CHRONIC, BCR-ABL POSITIVE; MAP KINASE KINASE 4; MICE; MICE, INBRED NOD; MICE, SCID; PHOSPHORYLATION; PIPERAZINES; PROTO-ONCOGENE PROTEINS; PYRIMIDINES; TUMOR CELLS, CULTURED; WNT PROTEINS;

EID: 84886775056     PISSN: 01452126     EISSN: 18735835     Source Type: Journal    
DOI: 10.1016/j.leukres.2013.07.013     Document Type: Article

References (40)

1. Hazlehurst L.A., Bewry N.N., Nair R.R., Pinilla-Ibarz J. Signaling networks associated with BCR-ABL-dependent transformation. Cancer Control 2009, 16:100-107.
2. Quintas-Cardama A., Cortes J. Molecular biology of bcr-abl1-positive chronic myeloid leukemia. Blood 2009, 113:1619-1630.
3. Deininger M.W., Goldman J.M., Melo J.V. The molecular biology of chronic myeloid leukemia. Blood 2000, 96:3343-3356.
4. Gregory M.A., Phang T.L., Neviani P., Alvarez-Calderon F., Eide C.A., O'Hare T., et al. Wnt/Ca2+/NFAT signaling maintains survival of Ph+ leukemia cells upon inhibition of Bcr-Abl. Cancer Cell 2010, 18:74-87.
5. Coluccia A.M., Vacca A., Dunach M., Mologni L., Redaelli S., Bustos V.H., et al. Bcr-Abl stabilizes beta-catenin in chronic myeloid leukemia through its tyrosine phosphorylation. EMBO J 2007, 26:1456-1466.
6. Wang Z., Sampath J., Fukuda S., Pelus L.M. Disruption of the inhibitor of apoptosis protein survivin sensitizes Bcr-abl-positive cells to STI571-induced apoptosis. Cancer Res 2005, 65:8224-8232.
7. Zhao C., Blum J., Chen A., Kwon H.Y., Jung S.H., Cook J.M., et al. Loss of beta-catenin impairs the renewal of normal and CML stem cells in vivo. Cancer Cell 2007, 12:528-541.
8. Hu Y., Chen Y., Douglas L., Li S. beta-Catenin is essential for survival of leukemic stem cells insensitive to kinase inhibition in mice with BCR-ABL-induced chronic myeloid leukemia. Leukemia 2009, 23:109-116.
9. Heidel F.H., Bullinger L., Feng Z., Wang Z., Neff T.A., Stein L., et al. Genetic and pharmacologic inhibition of beta-catenin targets imatinib-resistant leukemia stem cells in CML. Cell Stem Cell 2012, 10:412-424.
10. Carter B.Z., Mak D.H., Schober W.D., Cabreira-Hansen M., Beran M., McQueen T., et al. Regulation of survivin expression through Bcr-Abl/MAPK cascade: targeting survivin overcomes imatinib resistance and increases imatinib sensitivity in imatinib-responsive CML cells. Blood 2006, 107:1555-1563.
11. Zhang T., Otevrel T., Gao Z., Ehrlich S.M., Fields J.Z., Boman B.M. Evidence that APC regulates survivin expression: a possible mechanism contributing to the stem cell origin of colon cancer. Cancer Res 2001, 61:8664-8667.
12. McDonald S.L., Silver A. The opposing roles of Wnt-5a in cancer. Br J Cancer 2009, 101:209-214.
13. Nomachi A., Nishita M., Inaba D., Enomoto M., Hamasaki M., Minami Y. Receptor tyrosine kinase Ror2 mediates Wnt5a-induced polarized cell migration by activating c-Jun N-terminal kinase via actin-binding protein filamin A. J Biol Chem 2008, 283:27973-27981.
14. Oishi I., Suzuki H., Onishi N., Takada R., Kani S., Ohkawara B., et al. The receptor tyrosine kinase Ror2 is involved in non-canonical Wnt5a/JNK signalling pathway. Genes Cells 2003, 8:645-654.
15. Kollmann K., Heller G., Ott R.G., Scheicher R., Zebedin-Brandl E., Schneckenleithner C., et al. c-JUN promotes BCR-ABL-induced lymphoid leukemia by inhibiting methylation of the 5' region of Cdk6. Blood 2011, 117:4065-4075.
16. Hess P., Pihan G., Sawyers C.L., Flavell R.A., Davis R.J. Survival signaling mediated by c-Jun NH(2)-terminal kinase in transformed B lymphoblasts. Nat Genet 2002, 32:201-205.
17. Redig A.J., Vakana E., Platanias L.C. Regulation of mammalian target of rapamycin and mitogen activated protein kinase pathways by BCR-ABL. Leuk Lymphoma 2011, 52(Suppl. 1):45-53.
18. Mancini M., Veljkovic N., Corradi V., Zuffa E., Corrado P., Pagnotta E., et al. 14-3-3 ligand prevents nuclear import of c-ABL protein in chronic myeloid leukemia. Traffic 2009, 10:637-647.
19. Yu C., Krystal G., Varticovksi L., McKinstry R., Rahmani M., Dent P., et al. Pharmacologic mitogen-activated protein/extracellular signal-regulated kinase kinase/mitogen-activated protein kinase inhibitors interact synergistically with STI571 to induce apoptosis in Bcr/Abl-expressing human leukemia cells. Cancer Res 2002, 62:188-199.
20. Yu C., Krystal G., Dent P., Grant S. Flavopiridol potentiates STI571-induced mitochondrial damage and apoptosis in BCR-ABL-positive human leukemia cells. Clin Cancer Res 2002, 8:2976-2984.
21. Yu C., Rahmani M., Almenara J., Subler M., Krystal G., Conrad D., et al. Histone deacetylase inhibitors promote STI571-mediated apoptosis in STI571-sensitive and -resistant Bcr/Abl+ human myeloid leukemia cells. Cancer Res 2003, 63:2118-2126.
22. Niu C.C., Zhao C., Yang Z.D., Zhang X.L., Wu W.R., Pan J., et al. Downregulation of gamma-catenin inhibits CML cell growth and potentiates the response of CML cells to imatinib through beta-catenin inhibition. Int J Mol Med 2013, 31:453-458.
23. La Rosee P., Johnson K., Corbin A.S., Stoffregen E.P., Moseson E.M., Willis S., et al. In vitro efficacy of combined treatment depends on the underlying mechanism of resistance in imatinib-resistant Bcr-Abl-positive cell lines. Blood 2004, 103:208-215.
24. Deng G., Li Z.Q., Zhao C., Yuan Y., Niu C.C., Pan J., et al. WNT5A expression is regulated by the status of its promoter methylation in leukaemia and can inhibit leukemic cell malignant proliferation. Oncol Rep 2011, 25:367-376.
25. Ying J., Li H., Chen Y.W., Srivastava G., Gao Z., Tao Q. WNT5A is epigenetically silenced in hematologic malignancies and inhibits leukemia cell growth as a tumor suppressor. Blood 2007, 110:4130-4132.
26. Chang-chun N., Wei-ke S., Jun L., Chen Z., Wei D., Zhao-quan L., et al. Effects of stable Wnt5a overexpression on biological characers of K562 cells. Acta Academiae Medicinae Militaris Tertiae 2009, 31:2199-2201.
27. Yuan Y., Niu C.C., Deng G., Li Z.Q., Pan J., Zhao C., et al. The Wnt5a/Ror2 noncanonical signaling pathway inhibits canonical Wnt signaling in K562 cells. Int J Mol Med 2011, 27:63-69.
28. Liang H., Chen Q., Coles A.H., Anderson S.J., Pihan G., Bradley A., et al. Wnt5a inhibits B cell proliferation and functions as a tumor suppressor in hematopoietic tissue. Cancer Cell 2003, 4:349-360.
29. Rodel F., Sprenger T., Kaina B., Liersch T., Rodel C., Fulda S., et al. Survivin as a prognostic/predictive marker and molecular target in cancer therapy. Curr Med Chem 2012, 19:3679-3688.
30. Yamamoto H., Ngan C.Y., Monden M. Cancer cells survive with survivin. Cancer Sci 2008, 99:1709-1714.
31. Conte E., Stagno F., Guglielmo P., Scuto A., Consoli C., Messina A. Survivin expression in chronic myeloid leukemia. Cancer Lett 2005, 225:105-110.
32. Reis F.R., Vasconcelos F.C., Pereira D.L., Moellman-Coelho A., Silva K.L., Maia R.C. Survivin and P-glycoprotein are associated and highly expressed in late phase chronic myeloid leukemia. Oncol Rep 2011, 26:471-478.
33. Hu D., Fang W., Han A., Gallagher L., Davis R.J., Xiong B., et al. c-Jun N-terminal kinase 1 interacts with and negatively regulates Wnt/beta-catenin signaling through GSK3beta pathway. Carcinogenesis 2008, 29:2317-2324.
34. Hu D., Bi X., Fang W., Han A., Yang W. GSK3beta is involved in JNK2-mediated beta-catenin inhibition. PLoS ONE 2009, 4:e6640.
35. Lee M.H., Koria P., Qu J., Andreadis S.T. JNK phosphorylates beta-catenin and regulates adherens junctions. FASEB J 2009, 23:3874-3883.
36. Liao G., Tao Q., Kofron M., Chen J.S., Schloemer A., Davis R.J., et al. Jun NH2-terminal kinase (JNK) prevents nuclear beta-catenin accumulation and regulates axis formation in Xenopus embryos. Proc Natl Acad Sci USA 2006, 103:16313-16318.
37. Wu X., Tu X., Joeng K.S., Hilton M.J., Williams D.A., Long F. Rac1 activation controls nuclear localization of beta-catenin during canonical Wnt signaling. Cell 2008, 133:340-353.
38. Nateri A.S., Spencer-Dene B., Behrens A. Interaction of phosphorylated c-Jun with TCF4 regulates intestinal cancer development. Nature 2005, 437:281-285.
39. Bradley R.S., Cowin P., Brown A.M. Expression of Wnt-1 in PC12 cells results in modulation of plakoglobin and E-cadherin and increased cellular adhesion. J Cell Biol 1993, 123:1857-1865.
40. Kim Y.M., Ma H., Oehler V.G., Gang E.J., Nguyen C., Masiello D., et al. The gamma catenin/CBP complex maintains survivin transcription in beta-catenin deficient/depleted cancer cells. Curr Cancer Drug Targets 2011, 11:213-225.