Biological rational for sequential targeting of Bruton tyrosine kinase and Bcl-2 to overcome CD40-induced ABT-199 resistance in mantle cell lymphoma

Oncotarget

Volumn 6, Issue 11, 2015, Pages 8750-8759

  Chiron, David ^a   Dousset, Christelle ^a,b,c   Brosseau, Carole ^a   Touzeau, Cyrille ^a,b   Maïga, Sophie ^a,b   Moreau, Philippe ^a,b   Pellat Deceunynck, Catherine ^a,b   Gouill, Steven Le ^a,b,c   Amiot, Martine ^a,b  

^a UNIVERSITÉ DE NANTES   (France)

^b NANTES UNIVERSITY HOSPITAL   (France)

^c INSERM   (France)

Author keywords

ABT 199; Apoptosis; Bcl 2 family members; Ibrutinib; Mantle cell lymphoma

Indexed keywords

BRUTON TYROSINE KINASE; CD40 ANTIGEN; CD40 LIGAND; IBRUTINIB; IMMUNOGLOBULIN ENHANCER BINDING PROTEIN; MESSENGER RNA; PROTEIN BCL 2; PROTEIN BCL XL; PROTEIN MCL 1; VENETOCLAX; AGAMMAGLOBULINAEMIA TYROSINE KINASE; ANTINEOPLASTIC AGENT; BCL2 PROTEIN, HUMAN; BCL2L1 PROTEIN, HUMAN; FUSED HETEROCYCLIC RINGS; MCL1 PROTEIN, HUMAN; PROTEIN BCL X; PROTEIN TYROSINE KINASE; PYRAZOLE DERIVATIVE; PYRIMIDINE DERIVATIVE; RNA; SULFONAMIDE; TUMOR PROTEIN;

ARTICLE; CANCER RESISTANCE; CELL VIABILITY; CONTROLLED STUDY; DRUG EFFICACY; DRUG SENSITIVITY; FIBROBLAST; GENE EXPRESSION; GENETIC TRANSFECTION; HUMAN; HUMAN CELL; IMMUNOBLOTTING; LYMPHOCYTOSIS; LYMPHOMA CELL LINE; MANTLE CELL LYMPHOMA; MANTLE CELL LYMPHOMA CELL; REAL TIME POLYMERASE CHAIN REACTION; TUMOR MICROENVIRONMENT; UPREGULATION; ANTAGONISTS AND INHIBITORS; APOPTOSIS; BIOSYNTHESIS; DRUG EFFECTS; DRUG RESISTANCE; ENZYMOLOGY; GENE EXPRESSION REGULATION; GENETICS; LYMPH NODE; LYMPHOMA, MANTLE-CELL; METABOLISM; MOLECULARLY TARGETED THERAPY; PATHOLOGY; PHYSIOLOGY; TUMOR CELL LINE;

ANTIGENS, CD40; ANTINEOPLASTIC AGENTS; APOPTOSIS; BCL-X PROTEIN; BRIDGED BICYCLO COMPOUNDS, HETEROCYCLIC; CELL LINE, TUMOR; DRUG RESISTANCE, NEOPLASM; GENE EXPRESSION REGULATION, NEOPLASTIC; HUMANS; LYMPH NODES; LYMPHOMA, MANTLE-CELL; MOLECULAR TARGETED THERAPY; MYELOID CELL LEUKEMIA SEQUENCE 1 PROTEIN; NEOPLASM PROTEINS; NF-KAPPA B; PROTEIN-TYROSINE KINASES; PROTO-ONCOGENE PROTEINS C-BCL-2; PYRAZOLES; PYRIMIDINES; RNA, MESSENGER; RNA, NEOPLASM; SULFONAMIDES; TUMOR MICROENVIRONMENT;

EID: 84928734902     PISSN: None     EISSN: 19492553     Source Type: Journal    
DOI: 10.18632/oncotarget.3275     Document Type: Article

References (30)

1. Dreyling M, Kluin-Nelemans HC, Beà S, Klapper W, Vogt N, Delfau-Larue M-H, Hutter G, Cheah C, Chiappella A, Cortelazzo S, Pott C, Hess G, Visco C, et al. Update on the molecular pathogenesis and clinical treatment of mantle cell lymphoma: report of the 11th annual conference of the European Mantle Cell Lymphoma Network. Leuk Lymphoma. 2013;54:699-707.
2. Kluin-Nelemans HC, Hoster E, Hermine O, Walewski J, Trneny M, Geisler CH, Stilgenbauer S, Thieblemont C, Vehling-Kaiser U, Doorduijn JK, Coiffier B, Forstpointner R, Tilly H, et al. Treatment of older patients with mantle-cell lymphoma. N Engl J Med. 2012;367:520-31.
3. Jares P, Colomer D, Campo E. Molecular pathogenesis of mantle cell lymphoma. J Clin Invest. 2012;122:3416-3423.
4. Bàe S, Salaverria I, Armengol L, Pinyol M, Fernández V, Hartmann EM, Jares P, Amador V, Hernández L, Navarro A, Ott G, Rosenwald A, Estivill X, Campo E. Uniparental disomies, homozygous deletions, amplifications, and target genes in mantle cell lymphoma revealed by integrative high-resolution whole-genome profiling. Blood. 2009;113:3059-69.
5. Ek S, Högerkorp C-M, Dictor M, Ehinger M, Borrebaeck CAK. Mantle Cell Lymphomas Express a Distinct Genetic Signature Affecting Lymphocyte Trafficking and Growth Regulation as Compared with Subpopulations of Normal Human B Cells. Cancer Res. 2002;62:4398-405.
6. Hofmann W-K, Vos de S, Tsukasaki K, Wachsman W, Pinkus GS, Said JW, Koeffler HP. Altered apoptosis pathways in mantle cell lymphoma detected by oligonucleotide microarray. Blood. 2001;98:787-794.
7. Deng J, Carlson N, Takeyama K, Dal Cin P, Shipp M, Letai A. BH3 profiling identifies three distinct classes of apoptotic blocks to predict response to ABT-737 and conventional chemotherapeutic agents. Cancer Cell. 2007;12:171-185.
8. Tse C, Shoemaker AR, Adickes J, Anderson MG, Chen J, Jin S, Johnson EF, Marsh KC, Mitten MJ, Nimmer P, Roberts L, Tahir SK, Xiao Y, Yang X, Zhang H, Fesik S, Rosenberg SH, Elmore SW. ABT-263: a potent and orally bioavailable Bcl-2 family inhibitor. Cancer Res. 2008;68:3421-3428.
9. Roberts AW, Seymour JF, Brown JR, Wierda WG, Kipps TJ, Khaw SL, Carney DA, He SZ, Huang DC, Xiong H, Cui Y, Busman TA, McKeegan EM, et al. Substantial susceptibility of chronic lymphocytic leukemia to BCL2 inhibition: results of a phase I study of navitoclax in patients with relapsed or refractory disease. J Clin Oncol. 2012;30:488-496.
10. Souers AJ, Leverson JD, Boghaert ER, Ackler SL, Catron ND, Chen J, Dayton BD, Ding H, Enschede SH, Fairbrother WJ, Huang DC, Hymowitz SG, et al. ABT-199, a potent and selective BCL-2 inhibitor, achieves antitumor activity while sparing platelets. Nat Med. 2013;19:202-8.
11. Davids MS, Letai A. ABT-199: Taking Dead Aim at BCL-2. Cancer Cell. 2013;23:139-141.
12. Burger JA, Ford RJ. The microenvironment in mantle cell lymphoma: cellular and molecular pathways and emerging targeted therapies. Semin Cancer Biol. 2011;21:308-312.
13. Kurtova AV, Tamayo AT, Ford RJ, Burger JA. Mantle cell lymphoma cells express high levels of CXCR4, CXCR5, and VLA-4 (CD49d): importance for interactions with the stromal microenvironment and specific targeting. Blood. 2009;113:4604-4613.
14. Tromp JM, Geest CR, Breij ECW, Elias JA, van Laar J, Luijks DM, Kater AP, Beaumont T, van Oers MH, Eldering E. Tipping the Noxa/Mcl-1 balance overcomes ABT-737 resistance in chronic lymphocytic leukemia. Clin Cancer Res. 2012;18:487-498.
15. Vogler M, Butterworth M, Majid A, Walewska RJ, Sun X-M, Dyer MJS, Cohen GM. Concurrent up-regulation of BCL-XL and BCL2A1 induces approximately 1000-fold resistance to ABT-737 in chronic lymphocytic leukemia. Blood. 2009;113:4403-4413.
16. Davids MS, Deng J, Wiestner A, Lannutti BJ, Wang L, Wu CJ, Wilson WH, Brown JR, Letai A. Decreased mitochondrial apoptotic priming underlies stroma-mediated treatment resistance in chronic lymphocytic leukemia. Blood. 2012;120:3501-3509.
17. Honigberg LA, Smith AM, Sirisawad M, Verner E, Loury D, Chang B, Li S, Pan Z, Thamm DH, Miller RA, Buggy JJ. The Bruton tyrosine kinase inhibitor PCI-32765 blocks B-cell activation and is efficacious in models of autoimmune disease and B-cell malignancy. Proc Natl Acad Sci U S A. 2010;107:13075-13080.
18. Touzeau C, Dousset C, Bodet L, Gomez-Bougie P, Bonnaud S, Moreau A, Moreau P, Pellat-Deceunynk C, Amiot M, Le Gouill S. ABT-737 Induces Apoptosis in Mantle Cell Lymphoma Cells with a Bcl-2 high/Mcl-1low Profile and Synergizes with Other Antineoplastic Agents. Clin Cancer Res. 2011;17:5973-5981.
19. Coope HJ, Atkinson PG, Huhse B, Belich M, Janzen J, Holman MJ, Klaus GG, Johnston LH, Ley SC. CD40 regulates the processing of NF-kappaB2 p100 to p52. EMBO J. 2002;21:5375-5385.
20. Lee HH, Dadgostar H, Cheng Q, Shu J, Cheng G. NF-kappaB-mediated up-regulation of Bcl-x and Bfl-1/A1 is required for CD40 survival signaling in B lymphocytes. Proc Natl Acad Sci U S A. 1999;96:9136-9141.
21. Wang ML, Rule S, Martin P, Goy A, Auer R, Kahl BS, Jurczak W, Advani RH, Romaguera JE, Williams ME, Barrientos JC, Chmielowska E, Radford J, et al. Targeting BTK with ibrutinib in relapsed or refractory mantle-cell lymphoma. N Engl J Med. 2013;369:507-516.
22. Chang BY, Francesco M, De Rooij MFM, Magadala P, Steggerda SM, Huang MM, Kuil A, Herman SE, Chang S, Pals ST, Wilson W, Wiestner A, Spaargaren M, et al. Egress of CD19(+)CD5(+) cells into peripheral blood following treatment with the Bruton tyrosine kinase inhibitor ibrutinib in mantle cell lymphoma patients. Blood. 2013;122:2412-2424.
23. Ko TK, Chuah CT, Huang JW, Ng KP, Ong ST. The BCL2 inhibitor ABT-199 significantly enhances imatinib-induced cell death in chronic myeloid leukemia progenitors. Oncotarget. 2014;5:9033-9038.
24. Peirs S, Matthijssens F, Goossens S, Van de Walle I, Ruggero K, de Bock CE, Degryse S, Canté-Barrett K, Briot D, Clappier E, Lammens T, De Moerloose B, Benoit Y, et al. ABT-199 mediated inhibition of BCL-2 as a novel therapeutic strategy in T-cell acute lymphoblastic leukemia. Blood. 2014. pii: blood-2014-05-574566.
25. Fresquet V, Rieger M, Carolis C, García-Barchino MJ, Martinez-Climent JA. Acquired mutations in BCL2 family proteins conferring resistance to the BH3 mimetic ABT-199 in lymphoma. Blood. 2014 Jun 26;123:4111-9.
26. Hallaert DYH, Jaspers A, van Noesel CJ, van Oers MHJ, Kater AP, Eldering E. c-Abl kinase inhibitors overcome CD40-mediated drug resistance in CLL: implications for therapeutic targeting of chemoresistant niches. Blood. 2008;112:5141-5149.
27. Saba N, Wiestner A. Do mantle cell lymphomas have an "Achilles heel"? Curr Opin Hematol. 2014; 21:350-357.
28. Chiron D, Di Liberto M, Martin P, Huang X, Sharman J, Blecua P, Mathew S, Vijay P, Eng K, Ali S, Johnson A, Chang B, Ely S, et al. Cell-cycle reprogramming for PI3K inhibition overrides a relapse-specific C81S BTK mutation revealed by longitudinal functional genomics in mantle cell lymphoma. Cancer Discov. 2014;4:1022-1035.
29. Zhao X, Bodo J, Sun D, Durkin L, Lin J, Smith MR, Hsi ED. Combination of ibrutinib with ABT-199: synergistic effects on proliferation inhibition and apoptosis in mantle cell lymphoma cells through perturbation of BTK, AKT, and BCL2 pathways. Br J Haematol. 2014 doi: 10.1111/ bjh.13149.
30. Maïga S, Gomez-Bougie P, Bonnaud S, Gratas C, Moreau P, Le Gouill S, Pellat-Deceunynck C, Amiot M. Paradoxical effect of lenalidomide on cytokine/growth factor profiles in multiple myeloma. Br J Cancer. 2013;108:1801-1806.