Wnt inhibition leads to improved chemosensitivity in paediatric acute lymphoblastic leukaemia

British Journal of Haematology

Volumn 167, Issue 1, 2014, Pages 87-99

  Dandekar, Smita ^a   Romanos Sirakis, Eleny ^a,b   Pais, Faye ^c   Bhatla, Teena ^a   Jones, Courtney ^a   Bourgeois, Wallace ^d   Hunger, Stephen P ^e   Raetz, Elizabeth A ^a   Hermiston, Michelle L ^c   Dasgupta, Ramanuj ^a   Morrison, Debra J ^a   Carroll, William L ^a,d  

^a NEW YORK UNIVERSITY MEDICAL CENTER   (United States)

^b STATEN ISLAND UNIVERSITY HOSPITAL   (United States)

^c UNIVERSITY OF CALIFORNIA   (United States)

^d NEW YORK UNIVERSITY SCHOOL OF MEDICINE   (United States)

^e UNIVERSITY OF COLORADO SCHOOL OF MEDICINE   (United States)

Author keywords

Acute lymphoblastic leukaemia; Chemosensitivity; Phosphoflow cytometry; Relapse; Wnt inhibition

Indexed keywords

BETA CATENIN; CYTARABINE; DOXORUBICIN; ETOPOSIDE; ICRT 14; PREDNISOLONE; PROTEIN INHIBITOR; SURVIVIN; TIOGUANINE; UNCLASSIFIED DRUG; WNT PROTEIN; WNT PROTEIN INHIBITOR; ANTINEOPLASTIC AGENT;

ACUTE LYMPHOBLASTIC LEUKEMIA; APOPTOSIS; ARTICLE; BLAST CELL; CANCER PROGNOSIS; CANCER RECURRENCE; CELL VIABILITY; CHEMOSENSITIVITY; CHILDHOOD LEUKEMIA; DOWN REGULATION; DRUG EFFICACY; DRUG POTENTIATION; FLOW CYTOMETRY; GENE TARGETING; GENETIC ANALYSIS; HUMAN; HUMAN CELL; LEUKEMIA CELL LINE; PRIORITY JOURNAL; PROTEIN EXPRESSION; WNT SIGNALING PATHWAY; ANTAGONISTS AND INHIBITORS; CELL SURVIVAL; DRUG EFFECTS; DRUG RESISTANCE; GENE EXPRESSION REGULATION; GENETICS; IMMUNOPHENOTYPING; METABOLISM; TUMOR CELL LINE; TUMOR RECURRENCE;

ANTINEOPLASTIC AGENTS; APOPTOSIS; CELL LINE, TUMOR; CELL SURVIVAL; DRUG RESISTANCE, NEOPLASM; DRUG SYNERGISM; GENE EXPRESSION REGULATION, NEOPLASTIC; HUMANS; IMMUNOPHENOTYPING; NEOPLASM RECURRENCE, LOCAL; PRECURSOR CELL LYMPHOBLASTIC LEUKEMIA-LYMPHOMA; WNT PROTEINS; WNT SIGNALING PATHWAY;

EID: 84911008752     PISSN: 00071048     EISSN: 13652141     Source Type: Journal    
DOI: 10.1111/bjh.13011     Document Type: Article

References (52)

1. Adida, C., Haioun, C., Gaulard, P., Lepage, E., Morel, P., Briere, J., Dombret, H., Reyes, F., Diebold, J., Gisselbrecht, C., Salles, G., Altieri, D.C. & Molina, T.J. (2000) Prognostic significance of survivin expression in diffuse large B-cell lymphomas. Blood, 96, 1921-1925.
2. van den Berg, H., de Groot-Kruseman, H.A., Damen-Korbijn, C.M., de Bont, E.S., Schouten-van Meeteren, A.Y. & Hoogerbrugge, P.M. (2011) Outcome after first relapse in children with acute lymphoblastic leukemia: a report based on the Dutch Childhood Oncology Group (DCOG) relapse all 98 protocol. Pediatric Blood & Cancer, 57, 210-216.
3. Bhatla, T., Wang, J., Morrison, D.J., Raetz, E.A., Burke, M.J., Brown, P. & Carroll, W.L. (2012) Epigenetic reprogramming reverses the relapse-specific gene expression signature and restores chemosensitivity in childhood B-lymphoblastic leukemia. Blood, 119, 5201-5210.
4. Chou, T.C. (2010) Drug combination studies and their synergy quantification using the Chou-Talalay method. Cancer Research, 70, 440-446.
5. Derksen, P.W., Tjin, E., Meijer, H.P., Klok, M.D., MacGillavry, H.D., van Oers, M.H., Lokhorst, H.M., Bloem, A.C., Clevers, H., Nusse, R., van der Neut, R., Spaargaren, M. & Pals, S.T. (2004) Illegitimate WNT signaling promotes proliferation of multiple myeloma cells. Proc Natl Acad Sci U S A, 101, 6122-6127.
6. Emami, K.H., Nguyen, C., Ma, H., Kim, D.H., Jeong, K.W., Eguchi, M., Moon, R.T., Teo, J.L., Kim, H.Y., Moon, S.H., Ha, J.R. & Kahn, M. (2004) A small molecule inhibitor of beta-catenin/CREB-binding protein transcription [corrected]. Proc Natl Acad Sci U S A, 101, 12682-12687.
7. Fangusaro, J.R., Caldas, H., Jiang, Y. & Altura, R.A. (2006) Survivin: an inhibitor of apoptosis in pediatric cancer. Pediatric Blood & Cancer, 47, 4-13.
8. Fuerer, C. & Nusse, R. (2010) Lentiviral vectors to probe and manipulate the Wnt signaling pathway. PLoS ONE, 5, e9370.
9. Gang, E.J., Hsieh, Y.T., Pham, J., Zhao, Y., Nguyen, C., Huantes, S., Park, E., Naing, K., Klemm, L., Swaminathan, S., Conway, E.M., Pelus, L.M., Crispino, J., Mullighan, C.G., McMillan, M., Muschen, M., Kahn, M. & Kim, Y.M. (2013) Small-molecule inhibition of CBP/catenin interactions eliminates drug-resistant clones in acute lymphoblastic leukemia. Oncogene, 33, 2169-2178.
10. Gehrke, I., Gandhirajan, R.K. & Kreuzer, K.A. (2009) Targeting the WNT/beta-catenin/TCF/LEF1 axis in solid and haematological cancers: multiplicity of therapeutic options. European Journal of Cancer, 45, 2759-2767.
11. Gonsalves, F.C., Klein, K., Carson, B.B., Katz, S., Ekas, L.A., Evans, S., Nagourney, R., Cardozo, T., Brown, A.M. & DasGupta, R. (2011) An RNAi-based chemical genetic screen identifies three small-molecule inhibitors of the Wnt/wingless signaling pathway. Proc Natl Acad Sci U S A, 108, 5954-5963.
12. Guo, Z., Dose, M., Kovalovsky, D., Chang, R., O'Neil, J., Look, A.T., von Boehmer, H., Khazaie, K. & Gounari, F. (2007) Beta-catenin stabilization stalls the transition from double-positive to single-positive stage and predisposes thymocytes to malignant transformation. Blood, 109, 5463-5472.
13. He, T.C., Sparks, A.B., Rago, C., Hermeking, H., Zawel, L., da Costa, L.T., Morin, P.J., Vogelstein, B. & Kinzler, K.W. (1998) Identification of c-MYC as a target of the APC pathway. Science, 281, 1509-1512.
14. Hogan, L.E., Meyer, J.A., Yang, J., Wang, J., Wong, N., Yang, W., Condos, G., Hunger, S.P., Raetz, E., Saffery, R., Relling, M.V., Bhojwani, D., Morrison, D.J. & Carroll, W.L. (2011) Integrated genomic analysis of relapsed childhood acute lymphoblastic leukemia reveals therapeutic strategies. Blood, 118, 5218-5226.
15. Huang, S.M., Mishina, Y.M., Liu, S., Cheung, A., Stegmeier, F., Michaud, G.A., Charlat, O., Wiellette, E., Zhang, Y., Wiessner, S., Hild, M., Shi, X., Wilson, C.J., Mickanin, C., Myer, V., Fazal, A., Tomlinson, R., Serluca, F., Shao, W., Cheng, H., Shultz, M., Rau, C., Schirle, M., Schlegl, J., Ghidelli, S., Fawell, S., Lu, C., Curtis, D., Kirschner, M.W., Lengauer, C., Finan, P.M., Tallarico, J.A., Bouwmeester, T., Porter, J.A., Bauer, A. & Cong, F. (2009) Tankyrase inhibition stabilizes axin and antagonizes Wnt signalling. Nature, 461, 614-620.
16. Hunger, S.P., Lu, X., Devidas, M., Camitta, B.M., Gaynon, P.S., Winick, N.J., Reaman, G.H. & Carroll, W.L. (2012) Improved survival for children and adolescents with acute lymphoblastic leukemia between 1990 and 2005: a report from the children's oncology group. Journal of Clinical Oncology, 30, 1663-1669.
17. Jamieson, C.H., Ailles, L.E., Dylla, S.J., Muijtjens, M., Jones, C., Zehnder, J.L., Gotlib, J., Li, K., Manz, M.G., Keating, A., Sawyers, C.L. & Weissman, I.L. (2004) Granulocyte-macrophage progenitors as candidate leukemic stem cells in blast-crisis CML. New England Journal of Medicine, 351, 657-667.
18. Khan, N.I., Bradstock, K.F. & Bendall, L.J. (2007) Activation of Wnt/beta-catenin pathway mediates growth and survival in B-cell progenitor acute lymphoblastic leukaemia. British Journal of Haematology, 138, 338-348.
19. Kim, M., Kim, H. & Jho, E.H. (2010) Identification of ptpro as a novel target gene of Wnt signaling and its potential role as a receptor for Wnt. FEBS Letters, 584, 3923-3928.
20. Kleber, M. & Sommer, L. (2004) Wnt signaling and the regulation of stem cell function. Current Opinion in Cell Biology, 16, 681-687.
21. Klumper, E., Pieters, R., Veerman, A.J., Huismans, D.R., Loonen, A.H., Hahlen, K., Kaspers, G.J., van Wering, E.R., Hartmann, R. & Henze, G. (1995) In vitro cellular drug resistance in children with relapsed/refractory acute lymphoblastic leukemia. Blood, 86, 3861-3868.
22. Lee, E., Madar, A., David, G., Garabedian, M.J., Dasgupta, R. & Logan, S.K. (2013) Inhibition of androgen receptor and beta-catenin activity in prostate cancer. Proc Natl Acad Sci U S A, 110, 15710-15715.
23. Lu, D., Zhao, Y., Tawatao, R., Cottam, H.B., Sen, M., Leoni, L.M., Kipps, T.J., Corr, M. & Carson, D.A. (2004) Activation of the Wnt signaling pathway in chronic lymphocytic leukemia. Proc Natl Acad Sci U S A, 101, 3118-3123.
24. Lu, J., Ma, Z., Hsieh, J.C., Fan, C.W., Chen, B., Longgood, J.C., Williams, N.S., Amatruda, J.F., Lum, L. & Chen, C. (2009) Structure-activity relationship studies of small-molecule inhibitors of Wnt response. Bioorganic & Medicinal Chemistry Letters, 19, 3825-3827.
25. Mazieres, J., You, L., He, B., Xu, Z., Lee, A.Y., Mikami, I., McCormick, F. & Jablons, D.M. (2005) Inhibition of Wnt16 in human acute lymphoblastoid leukemia cells containing the t(1;19) translocation induces apoptosis. Oncogene, 24, 5396-5400.
26. McWhirter, J.R., Neuteboom, S.T., Wancewicz, E.V., Monia, B.P., Downing, J.R. & Murre, C. (1999) Oncogenic homeodomain transcription factor E2A-Pbx1 activates a novel WNT gene in pre-B acute lymphoblastoid leukemia. Proc Natl Acad Sci U S A, 96, 11464-11469.
27. Miyoshi, K. & Hennighausen, L. (2003) Beta-catenin: a transforming actor on many stages. Breast Cancer Research, 5, 63-68.
28. Miyoshi, K., Rosner, A., Nozawa, M., Byrd, C., Morgan, F., Landesman-Bollag, E., Xu, X., Seldin, D.C., Schmidt, E.V., Taketo, M.M., Robinson, G.W., Cardiff, R.D. & Hennighausen, L. (2002) Activation of different Wnt/beta-catenin signaling components in mammary epithelium induces transdifferentiation and the formation of pilar tumors. Oncogene, 21, 5548-5556.
29. Moon, R.T., Kohn, A.D., De Ferrari, G.V. & Kaykas, A. (2004) WNT and beta-catenin signalling: diseases and therapies. Nature Reviews Genetics, 5, 691-701.
30. Morrison, D.J., Hogan, L.E., Condos, G., Bhatla, T., Germino, N., Moskowitz, N.P., Lee, L., Bhojwani, D., Horton, T.M., Belitskaya-Levy, I., Greenberger, L.M., Horak, I.D., Grupp, S.A., Teachey, D.T., Raetz, E.A. & Carroll, W.L. (2012) Endogenous knockdown of survivin improves chemotherapeutic response in ALL models. Leukemia, 26, 271-279.
31. Mudry, R.E., Fortney, J.E., York, T., Hall, B.M. & Gibson, L.F. (2000) Stromal cells regulate survival of B-lineage leukemic cells during chemotherapy. Blood, 96, 1926-1932.
32. Muller-Tidow, C., Steffen, B., Cauvet, T., Tickenbrock, L., Ji, P., Diederichs, S., Sargin, B., Kohler, G., Stelljes, M., Puccetti, E., Ruthardt, M., de Vos, S., Hiebert, S.W., Koeffler, H.P., Berdel, W.E. & Serve, H. (2004) Translocation products in acute myeloid leukemia activate the Wnt signaling pathway in hematopoietic cells. Molecular and Cellular Biology, 24, 2890-2904.
33. Murdoch, B., Chadwick, K., Martin, M., Shojaei, F., Shah, K.V., Gallacher, L., Moon, R.T. & Bhatia, M. (2003) Wnt-5A augments repopulating capacity and primitive hematopoietic development of human blood stem cells in vivo. Proc Natl Acad Sci U S A, 100, 3422-3427.
34. Nelson, W.J. & Nusse, R. (2004) Convergence of Wnt, beta-catenin, and cadherin pathways. Science, 303, 1483-1487.
35. Nguyen, K., Devidas, M., Cheng, S.C., La, M., Raetz, E.A., Carroll, W.L., Winick, N.J., Hunger, S.P., Gaynon, P.S. & Loh, M.L. (2008) Factors influencing survival after relapse from acute lymphoblastic leukemia: a Children's Oncology Group study. Leukemia, 22, 2142-2150.
36. Nusse, R. (1999) WNT targets. Repression and activation. Trends in Genetics, 15, 1-3.
37. Paik, S., Shak, S., Tang, G., Kim, C., Baker, J., Cronin, M., Baehner, F.L., Walker, M.G., Watson, D., Park, T., Hiller, W., Fisher, E.R., Wickerham, D.L., Bryant, J. & Wolmark, N. (2004) A multigene assay to predict recurrence of tamoxifen-treated, node-negative breast cancer. New England Journal of Medicine, 351, 2817-2826.
38. Pennati, M., Folini, M. & Zaffaroni, N. (2007) Targeting survivin in cancer therapy: fulfilled promises and open questions. Carcinogenesis, 28, 1133-1139.
39. Polakis, P. (2000) Wnt signaling and cancer. Genes & Development, 14, 1837-1851.
40. Raetz, E.A., Borowitz, M.J., Devidas, M., Linda, S.B., Hunger, S.P., Winick, N.J., Camitta, B.M., Gaynon, P.S. & Carroll, W.L. (2008) Reinduction platform for children with first marrow relapse of acute lymphoblastic Leukemia: a Children's Oncology Group Study[corrected]. Journal of Clinical Oncology, 26, 3971-3978.
41. Reya, T. & Clevers, H. (2005) Wnt signalling in stem cells and cancer. Nature, 434, 843-850.
42. Reya, T., Duncan, A.W., Ailles, L., Domen, J., Scherer, D.C., Willert, K., Hintz, L., Nusse, R. & Weissman, I.L. (2003) A role for Wnt signalling in self-renewal of haematopoietic stem cells. Nature, 423, 409-414.
43. Roman-Gomez, J., Cordeu, L., Agirre, X., Jimenez-Velasco, A., San Jose-Eneriz, E., Garate, L., Calasanz, M.J., Heiniger, A., Torres, A. & Prosper, F. (2007) Epigenetic regulation of Wnt-signaling pathway in acute lymphoblastic leukemia. Blood, 109, 3462-3469.
44. Staal, F.J. & Clevers, H. (2000) Tcf/Lef transcription factors during T-cell development: unique and overlapping functions. Hematol J, 1, 3-6.
45. Staal, F.J. & Clevers, H.C. (2005) WNT signalling and haematopoiesis: a WNT-WNT situation. Nature Reviews Immunology, 5, 21-30.
46. Takahashi-Yanaga, F. & Kahn, M. (2010) Targeting Wnt signaling: can we safely eradicate cancer stem cells? Clinical Cancer Research, 16, 3153-3162.
47. Tetsu, O. & McCormick, F. (1999) Beta-catenin regulates expression of cyclin D1 in colon carcinoma cells. Nature, 398, 422-426.
48. Thorne, C.A., Hanson, A.J., Schneider, J., Tahinci, E., Orton, D., Cselenyi, C.S., Jernigan, K.K., Meyers, K.C., Hang, B.I., Waterson, A.G., Kim, K., Melancon, B., Ghidu, V.P., Sulikowski, G.A., LaFleur, B., Salic, A., Lee, L.A., Miller, D.M. 3rd & Lee, E. (2010) Small-molecule inhibition of Wnt signaling through activation of casein kinase 1alpha. Nature Chemical Biology, 6, 829-836.
49. Wang, Y., Krivtsov, A.V., Sinha, A.U., North, T.E., Goessling, W., Feng, Z., Zon, L.I. & Armstrong, S.A. (2010) The Wnt/beta-catenin pathway is required for the development of leukemia stem cells in AML. Science, 327, 1650-1653.
50. Yang, Y., Mallampati, S., Sun, B., Zhang, J., Kim, S.B., Lee, J.S., Gong, Y., Cai, Z. & Sun, X. (2013) Wnt pathway contributes to the protection by bone marrow stromal cells of acute lymphoblastic leukemia cells and is a potential therapeutic target. Cancer Letters, 333, 9-17.
51. Zhang, T., Otevrel, T., Gao, Z., Ehrlich, S.M., Fields, J.Z. & Boman, B.M. (2001) Evidence that APC regulates survivin expression: a possible mechanism contributing to the stem cell origin of colon cancer. Cancer Research, 61, 8664-8667.
52. Zhang, J., Ding, L., Holmfeldt, L., Wu, G., Heatley, S.L., Payne-Turner, D., Easton, J., Chen, X., Wang, J., Rusch, M., Lu, C., Chen, S.C., Wei, L., Collins-Underwood, J.R., Ma, J., Roberts, K.G., Pounds, S.B., Ulyanov, A., Becksfort, J., Gupta, P., Huether, R., Kriwacki, R.W., Parker, M., McGoldrick, D.J., Zhao, D., Alford, D., Espy, S., Bobba, K.C., Song, G., Pei, D., Cheng, C., Roberts, S., Barbato, M.I., Campana, D., Coustan-Smith, E., Shurtleff, S.A., Raimondi, S.C., Kleppe, M., Cools, J., Shimano, K.A., Hermiston, M.L., Doulatov, S., Eppert, K., Laurenti, E., Notta, F., Dick, J.E., Basso, G., Hunger, S.P., Loh, M.L., Devidas, M., Wood, B., Winter, S., Dunsmore, K.P., Fulton, R.S., Fulton, L.L., Hong, X., Harris, C.C., Dooling, D.J., Ochoa, K., Johnson, K.J., Obenauer, J.C., Evans, W.E., Pui, C.H., Naeve, C.W., Ley, T.J., Mardis, E.R., Wilson, R.K., Downing, J.R. & Mullighan, C.G. (2012) The genetic basis of early T-cell precursor acute lymphoblastic leukaemia. Nature, 481, 157-163.