Characterization of ibrutinib-sensitive and -resistant mantle lymphoma cells

British Journal of Haematology

Volumn 166, Issue 6, 2014, Pages 849-861

  Ma, Jiao ^a   Lu, Pin ^b   Guo, Ailin ^b   Cheng, Shuhua ^a   Zong, Hongliang ^a   Martin, Peter ^a   Coleman, Morton ^a   Wang, Y Lynn ^b  

^a WEILL CORNELL MEDICAL COLLEGE   (United States)

^b UNIVERSITY OF CHICAGO   (United States)

Author keywords

B cell receptor signalling; Bruton tyrosine kinase; Ibrutinib; Mantle cell lymphoma; PCI 32765

Indexed keywords

BRUTON TYROSINE KINASE; IBRUTINIB; MITOGEN ACTIVATED PROTEIN KINASE 1; MITOGEN ACTIVATED PROTEIN KINASE 3; MYC PROTEIN; PROTEIN CCND1; PROTEIN KINASE B; REGULATOR PROTEIN; SMALL INTERFERING RNA; UNCLASSIFIED DRUG;

ANTINEOPLASTIC ACTIVITY; ARTICLE; B LYMPHOCYTE; CANCER CELL LINE; CANCER GROWTH; CANCER INHIBITION; CANCER RESISTANCE; CANCER SURVIVAL; CELL CYCLE ARREST; CELL CYCLE G0 PHASE; CELL CYCLE G1 PHASE; CELL CYCLE S PHASE; CELL DEATH; CELL FUNCTION; CELL PROLIFERATION; CELL RESISTANCE; CELLULAR PARAMETERS; CELLULAR SENSITIVITY; CONCENTRATION RESPONSE; CONTROLLED CLINICAL TRIAL; CONTROLLED STUDY; ENZYME ACTIVITY; ENZYME INHIBITION; ENZYME PHOSPHORYLATION; GENE SILENCING; GENETIC TRANSFECTION; HUMAN; HUMAN CELL; IC 50; LYMPHOMA CELL; MANTLE CELL LYMPHOMA; MAXIMUM PLASMA CONCENTRATION; MOLECULAR BIOLOGY; PHARMACODYNAMICS; PRIMARY CELL LINE; PRIMARY TUMOR; PRIORITY JOURNAL; PROTEIN PHOSPHORYLATION; SIGNAL TRANSDUCTION;

B-CELL RECEPTOR SIGNALLING; BRUTON TYROSINE KINASE; IBRUTINIB; MANTLE CELL LYMPHOMA; PCI-32765;

ANTINEOPLASTIC AGENTS; CELL CYCLE; CELL DEATH; CELL PROLIFERATION; CELL SURVIVAL; DRUG RESISTANCE, NEOPLASM; GENE KNOCKDOWN TECHNIQUES; HUMANS; LYMPHOMA, MANTLE-CELL; MAP KINASE SIGNALING SYSTEM; PHOSPHORYLATION; PROTEIN-TYROSINE KINASES; PYRAZOLES; PYRIMIDINES; TUMOR CELLS, CULTURED;

EID: 84907312674     PISSN: 00071048     EISSN: 13652141     Source Type: Journal    
DOI: 10.1111/bjh.12974     Document Type: Article

References (39)

1. Advani, R.H., Buggy, J.J., Sharman, J.P., Smith, S.M., Boyd, T.E., Grant, B., Kolibaba, K.S., Furman, R.R., Rodriguez, S., Chang, B.Y., Sukbuntherng, J., Izumi, R., Hamdy, A., Hedrick, E. & Fowler, N.H. (2013) Bruton tyrosine kinase inhibitor ibrutinib (PCI-32765) has significant activity in patients with relapsed/refractory B-cell malignancies. Journal of Clinical Oncology, 31, 88-94.
2. Boyd, R.S., Jukes-Jones, R., Walewska, R., Brown, D., Dyer, M.J. & Cain, K. (2009) Protein profiling of plasma membranes defines aberrant signaling pathways in mantle cell lymphoma. Molecular & Cellular Proteomics, 8, 1501-1515.
3. Buggy, J.J. & Elias, L. (2012) Bruton tyrosine kinase (BTK) and its role in B-cell malignancy. International Reviews of Immunology, 31, 119-132.
4. Chang, B.Y., Furman, R.R., Zapatka, M., Barrientos, J.C., Li, D., Steggerda, S., Eckert, K., Francesco, M., Woyach, J.A. & Johnson, A.J. (2013a) Use of tumor genomic profiling to reveal mechanisms of resistance to the BTK inhibitor ibrutinib in chronic lymphocytic leukemia (CLL). Journal of Clinical Oncology, 31 (Suppl; abtract 7014).
5. Chang, B.Y., Francesco, M., De Rooij, M.F., Magadala, P., Steggerda, S.M., Huang, M.M., Kuil, A., Herman, S.E., Chang, S., Pals, S.T., Wilson, W., Wiestner, A., Spaargaren, M., Buggy, J.J. & Elias, L. (2013b) Egress of CD19(+)CD5(+) cells into peripheral blood following treatment with the Bruton tyrosine kinase inhibitor ibrutinib in mantle cell lymphoma patients. Blood, 122, 2412-2424.
6. Cheng, S., Coffey, G., Zhang, X.H., Shaknovich, R., Song, Z., Lu, P., Pandey, A., Melnick, A.M., Sinha, U. & Wang, Y.L. (2011) SYK inhibition and response prediction in diffuse large B-cell lymphoma. Blood, 118, 6342-6352.
7. Cheng, S., Ma, J., Guo, A., Lu, P., Coleman, M., Liu, M., Buggy, J.J., Furman, R.R. & Wang, Y.L. (2014) BTK inhibition targets in vivo CLL proliferation through its effects on B-cell receptor signaling activity. Leukemia, 28, 649-657.
8. Chiorazzi, N., Rai, K.R. & Ferrarini, M. (2005) Chronic lymphocytic leukemia. New England Journal of Medicine, 352, 804-815.
9. Cinar, M., Hamedani, F., Mo, Z., Cinar, B., Amin, H.M. & Alkan, S. (2013) Bruton tyrosine kinase is commonly overexpressed in mantle cell lymphoma and its attenuation by Ibrutinib induces apoptosis. Leukemia Research, 37, 1271-1277.
10. Dal Porto, J.M., Gauld, S.B., Merrell, K.T., Mills, D., Pugh-Bernard, A.E. & Cambier, J. (2004) B cell antigen receptor signaling 101. Molecular Immunology, 41, 599-613.
11. Dasmahapatra, G., Patel, H., Dent, P., Fisher, R.I., Friedberg, J. & Grant, S. (2013) The Bruton tyrosine kinase (BTK) inhibitor PCI-32765 synergistically increases proteasome inhibitor activity in diffuse large-B cell lymphoma (DLBCL) and mantle cell lymphoma (MCL) cells sensitive or resistant to bortezomib. British Journal of Haematology, 161, 43-56.
12. Davis, R.E., Ngo, V.N., Lenz, G., Tolar, P., Young, R.M., Romesser, P.B., Kohlhammer, H., Lamy, L., Zhao, H., Yang, Y., Xu, W., Shaffer, A.L., Wright, G., Xiao, W., Powell, J., Jiang, J.K., Thomas, C.J., Rosenwald, A., Ott, G., Muller-Hermelink, H.K., Gascoyne, R.D., Connors, J.M., Johnson, N.A., Rimsza, L.M., Campo, E., Jaffe, E.S., Wilson, W.H., Delabie, J., Smeland, E.B., Fisher, R.I., Braziel, R.M., Tubbs, R.R., Cook, J.R., Weisenburger, D.D., Chan, W.C., Pierce, S.K. & Staudt, L.M. (2010) Chronic active B-cell-receptor signalling in diffuse large B-cell lymphoma. Nature, 463, 88-92.
13. Deng, C., Lee, S. & O'Connor, O.A. (2012) New strategies in the treatment of mantle cell lymphoma. Clinical Cancer Research, 18, 3499-3508.
14. Fluckiger, A.C., Li, Z., Kato, R.M., Wahl, M.I., Ochs, H.D., Longnecker, R., Kinet, J.P., Witte, O.N., Scharenberg, A.M. & Rawlings, D.J. (1998) Btk/Tec kinases regulate sustained increases in intracellular Ca2+ following B-cell receptor activation. EMBO Journal, 17, 1973-1985.
15. Furman, R.R., Cheng, S., Lu, P., Setty, M., Perez, A., Guo, A., Racchumi, J., Ma, J., Coleman, M., Venkataraman, J., Xu, G.Z., Chen, W., Wu, H., Betty, Y.C., Leslie, C. & Wang, Y.L. (2013) A Novel BTK Mutation reactivates BCR signaling and confers acquired resistance of CLL to ibrutinib. Blood (ASH Annual Meeting Abstract), 122, 4914.
16. Furman, R.R., Cheng, S., Lu, P., Setty, M., Perez, S.A., Guo, A., Racchumi, J., Xu, G.Z., Wu, H., Ma, J., Susanne, M., Coleman, M., Leslie, C. & Wang, Y.L. (2014) A novel mutation in Bruton tyrosine kinase confers acquired resistance to ibrutinib in chronic lymphocytic leukemia. New England Journal of Medicine, doi:10.1056/NEJMc1402716.
17. de Gorter, D.J., Beuling, E.A., Kersseboom, R., Middendorp, S., van Gils, J.M., Hendriks, R.W., Pals, S.T. & Spaargaren, M. (2007) Bruton's tyrosine kinase and phospholipase Cgamma2 mediate chemokine-controlled B cell migration and homing. Immunity, 26, 93-104.
18. Hadzidimitriou, A., Agathangelidis, A., Darzentas, N., Murray, F., Delfau-Larue, M.H., Pedersen, L.B., Lopez, A.N., Dagklis, A., Rombout, P., Beldjord, K., Kolstad, A., Dreyling, M.H., Anagnostopoulos, A., Tsaftaris, A., Mavragani-Tsipidou, P., Rosenwald, A., Ponzoni, M., Groenen, P., Ghia, P., Sander, B., Papadaki, T., Campo, E., Geisler, C., Rosenquist, R., Davi, F., Pott, C. & Stamatopoulos, K. (2011) Is there a role for antigen selection in mantle cell lymphoma? Immunogenetic support from a series of 807 cases. Blood, 118, 3088-3095.
19. Harwood, N.E. & Batista, F.D. (2010) Early events in B cell activation. Annual Reviews of Immunology, 28, 185-210.
20. Honigberg, L.A., Smith, A.M., Sirisawad, M., Verner, E., Loury, D., Chang, B., Li, S., Pan, Z., Thamm, D.H., Miller, R.A. & Buggy, J.J. (2010) The Bruton tyrosine kinase inhibitor PCI-32765 blocks B-cell activation and is efficacious in models of autoimmune disease and B-cell malignancy. Proceedings of the National Academy of Sciences of the United States of America, 107, 13075-13080.
21. Humphries, L.A., Dangelmaier, C., Sommer, K., Kipp, K., Kato, R.M., Griffith, N., Bakman, I., Turk, C.W., Daniel, J.L. & Rawlings, D.J. (2004) Tec kinases mediate sustained calcium influx via site-specific tyrosine phosphorylation of the phospholipase Cgamma Src homology 2-Src homology 3 linker. Journal of Biological Chemistry, 279, 37651-37661.
22. Irish, J.M., Czerwinski, D.K., Nolan, G.P. & Levy, R. (2006) Altered B-cell receptor signaling kinetics distinguish human follicular lymphoma B cells from tumor-infiltrating nonmalignant B cells. Blood, 108, 3135-3142.
23. Jares, P., Colomer, D. & Campo, E. (2007) Genetic and molecular pathogenesis of mantle cell lymphoma: perspectives for new targeted therapeutics. Nature Reviews Cancer, 7, 750-762.
24. Jiang, A., Craxton, A., Kurosaki, T. & Clark, E.A. (1998) Different protein tyrosine kinases are required for B cell antigen receptor-mediated activation of extracellular signal-regulated kinase, c-Jun NH2-terminal kinase 1, and p38 mitogen-activated protein kinase. Journal of Experimental Medicine, 188, 1297-1306.
25. Kuppers, R. (2005) Mechanisms of B-cell lymphoma pathogenesis. Nature Reviews Cancer, 5, 251-262.
26. Kurosaki, T., Shinohara, H. & Baba, Y. (2010) B cell signaling and fate decision. Annual Review of Immunology, 28, 21-55.
27. Lu, P., Yang, C., Harrington, G.W., Wang, Y.L. & Cesarman, E. (2009) Early events of B-cell receptor signaling are not essential for the proliferation and viability of AIDS-related lymphoma. Leukemia, 23, 807-810.
28. Macias-Perez, I.M. & Flinn, I.W. (2012) B-cell receptor pathobiology and targeting in NHL. Current Oncology Reports, 14, 411-418.
29. Pan, Z., Scheerens, H., Li, S.J., Schultz, B.E., Sprengeler, P.A., Burrill, L.C., Mendonca, R.V., Sweeney, M.D., Scott, K.C., Grothaus, P.G., Jeffery, D.A., Spoerke, J.M., Honigberg, L.A., Young, P.R., Dalrymple, S.A. & Palmer, J.T. (2007) Discovery of selective irreversible inhibitors for Bruton's tyrosine kinase. ChemMedChem, 2, 58-61.
30. Parekh, S., Weniger, M.A. & Wiestner, A. (2011) New molecular targets in mantle cell lymphoma. Seminars in Cancer Biology, 21, 335-346.
31. Perez-Galan, P., Dreyling, M. & Wiestner, A. (2011) Mantle cell lymphoma: biology, pathogenesis, and the molecular basis of treatment in the genomic era. Blood, 117, 26-38.
32. Pighi, C., Gu, T.L., Dalai, I., Barbi, S., Parolini, C., Bertolaso, A., Pedron, S., Parisi, A., Ren, J., Cecconi, D., Chilosi, M., Menestrina, F. & Zamo, A. (2011) Phospho-proteomic analysis of mantle cell lymphoma cells suggests a pro-survival role of B-cell receptor signaling. Cellular Oncology (Dordrecht), 34, 141-153.
33. Rinaldi, A., Kwee, I., Taborelli, M., Largo, C., Uccella, S., Martin, V., Poretti, G., Gaidano, G., Calabrese, G., Martinelli, G., Baldini, L., Pruneri, G., Capella, C., Zucca, E., Cotter, F.E., Cigudosa, J.C., Catapano, C.V., Tibiletti, M.G. & Bertoni, F. (2006) Genomic and expression profiling identifies the B-cell associated tyrosine kinase Syk as a possible therapeutic target in mantle cell lymphoma. British Journal of Haematology, 132, 303-316.
34. Song, Z., Lu, P., Furman, R.R., Leonard, J.P., Martin, P., Tyrell, L., Lee, F.Y., Knowles, D.M., Coleman, M. & Wang, Y.L. (2010) Activities of SYK and PLCgamma2 predict apoptotic response of CLL cells to SRC tyrosine kinase inhibitor dasatinib. Clinical Cancer Research, 16, 587-599.
35. Wang, M.L., Rule, S., Martin, P., Goy, A., Auer, R., Kahl, B.S., Jurczak, W., Advani, R.H., Romaguera, J.E., Williams, M.E., Barrientos, J.C., Chmielowska, E., Radford, J., Stilgenbauer, S., Dreyling, M., Jedrzejczak, W.W., Johnson, P., Spurgeon, S.E., Li, L., Zhang, L., Newberry, K., Ou, Z., Cheng, N., Fang, B., McGreivy, J., Clow, F., Buggy, J.J., Chang, B.Y., Beaupre, D.M., Kunkel, L.A. & Blum, K.A. (2013) Targeting BTK with ibrutinib in relapsed or refractory mantle-cell lymphoma. New England Journal of Medicine, 369, 507-516.
36. Wilson, W.H., Gerecitano, J.F., Goy, A., de Vos, S., Kenkre, V.P., Barr, P.M., Blum, K.A., Shustov, A.R., Advani, R.H., Lih, J., Williams, M., Schmitz, R., Yang, Y., Pittaluga, S., Wright, G., Kunkel, L.A., McGreivy, J., Balasubramanian, S., Cheng, M., Moussa, D., Buggy, J.J. & Staudt, L.M. (2012) The Bruton's tyrosine kinase (BTK) inhibitor, ibrutinib (PCI-32765), has preferential activity in the ABC subtype of relapsed/refractory de novo diffuse large B-cell lymphoma (DLBCL): interim results of a multicenter, open-label, phase 2 study. Blood (ASH Annual Meeting Abstracts), 120, 686.
37. Yang, C., Lu, P., Lee, F.Y., Chadburn, A., Barrientos, J.C., Leonard, J.P., Ye, F., Zhang, D., Knowles, D.M. & Wang, Y.L. (2008) Tyrosine kinase inhibition in diffuse large B-cell lymphoma: molecular basis for antitumor activity and drug resistance of dasatinib. Leukemia, 22, 1755-1766.
38. Yang, Y., Shaffer, A.L. 3rd, Emre, N.C., Ceribelli, M., Zhang, M., Wright, G., Xiao, W., Powell, J., Platig, J., Kohlhammer, H., Young, R.M., Zhao, H., Yang, Y., Xu, W., Buggy, J.J., Balasubramanian, S., Mathews, L.A., Shinn, P., Guha, R., Ferrer, M., Thomas, C., Waldmann, T.A. & Staudt, L.M. (2012) Exploiting synthetic lethality for the therapy of ABC diffuse large B cell lymphoma. Cancer Cell, 21, 723-737.
39. Young, R.M. & Staudt, L.M. (2013) Targeting pathological B cell receptor signalling in lymphoid malignancies. Nature Reviews. Drug Discovery, 12, 229-243.