Acquired mutations in BCL2 family proteins conferring resistance to the BH3 mimetic ABT-199 in lymphoma

Blood

Volumn 123, Issue 26, 2014, Pages 4111-4119

  Fresquet, Vicente ^a   Rieger, Melissa ^a   Carolis, Carlo ^b   García Barchino, Maria J ^a   Martinez Climent, Jose A ^a  

^a UNIVERSITY OF NAVARRA   (Spain)

^b UNIVERSITAT POMPEU FABRA   (Spain)

Author keywords

[No Author keywords available]

Indexed keywords

4 [4 (4' CHLORO 2 BIPHENYLYLMETHYL) 1 PIPERAZINYL] N [4 [3 DIMETHYLAMINO 1 (PHENYLTHIOMETHYL)PROPYLAMINO] 3 NITROBENZENESULFONYL]BENZAMIDE; CASPASE 3; CASPASE 9; CYTOCHROME C; MESSENGER RNA; PROTEIN BAX; PROTEIN BCL 2; PROTEIN MCL 1; VENETOCLAX;

ANIMAL CELL; ANIMAL EXPERIMENT; APOPTOSIS; ARTICLE; CANCER RESISTANCE; CELL VIABILITY; GENE EXPRESSION; GENE MUTATION; IMMUNOPRECIPITATION; IN VITRO STUDY; IN VIVO STUDY; LYMPHOMA; MISSENSE MUTATION; MITOCHONDRIAL MEMBRANE; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION;

AMINO ACID SUBSTITUTION; ANIMALS; ANTINEOPLASTIC AGENTS; APOPTOSIS; BCL-2-ASSOCIATED X PROTEIN; BICYCLO COMPOUNDS, HETEROCYCLIC; CELL LINE, TUMOR; DRUG RESISTANCE, NEOPLASM; HUMANS; LYMPHOMA; MICE; MICE, KNOCKOUT; MITOCHONDRIA; MUTATION, MISSENSE; SULFONAMIDES;

EID: 84903647814     PISSN: 00064971     EISSN: 15280020     Source Type: Journal    
DOI: 10.1182/blood-2014-03-560284     Document Type: Article

References (51)

1. Cory S, Adams JM. The Bcl2 family: regulators of the cellular life-or-death switch. Nat Rev Cancer. 2002;2(9):647-656. (Pubitemid 37328916)
2. Labi V, Erlacher M, Kiessling S, Villunger A. BH3- only proteins in cell death initiation, malignant disease and anticancer therapy. Cell Death Differ. 2006;13(8):1325-1338. (Pubitemid 44057468)
3. Danial NN, Korsmeyer SJ. Cell death: critical control points. Cell. 2004;116(2):205-219. (Pubitemid 38167313)
4. Davids MS, Letai A. Targeting the B-cell lymphoma/leukemia 2 family in cancer. J Clin Oncol. 2012;30(25):3127-3135.
5. Vogler M, Dinsdale D, Dyer MJ, Cohen GM. Bcl-2 inhibitors: small molecules with a big impact on cancer therapy. Cell Death Differ. 2009;16(3): 360-367.
6. Lessene G, Czabotar PE, Colman PM. BCL-2 family antagonists for cancer therapy. Nat Rev Drug Discov. 2008;7(12):989-1000.
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(2):171-185. (Pubitemid 47199122)
8. Oltersdorf T, Elmore SW, Shoemaker AR, et al. An inhibitor of Bcl-2 family proteins induces regression of solid tumours. Nature. 2005; 435(7042):677-681. (Pubitemid 40825512)
9. Yecies D, Carlson NE, Deng J, Letai A. Acquired resistance to ABT-737 in lymphoma cells that up-regulate MCL-1 and BFL-1. Blood. 2010; 115(16):3304-3313.
10. Vogler M, Butterworth M, Majid A, et al. Concurrent up-regulation of BCL-XL and BCL2A1 induces approximately 1000-fold resistance to ABT-737 in chronic lymphocytic leukemia. Blood. 2009;113(18):4403-4413.
11. van Delft MF, Wei AH, Mason KD, et al. The BH3 mimetic ABT-737 targets selective Bcl-2 proteins and efficiently induces apoptosis via Bak/Bax if Mcl-1 is neutralized. Cancer Cell. 2006;10(5): 389-399. (Pubitemid 44711953)
12. Roberts AW, Seymour JF, Brown JR, 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(5): 488-496.
13. Tse C, Shoemaker AR, Adickes J, et al. ABT-263: a potent and orally bioavailable Bcl-2 family inhibitor. Cancer Res. 2008;68(9):3421-3428.
14. Gandhi L, Camidge DR, Ribeiro de Oliveira M, et al. Phase I study of Navitoclax (ABT-263), a novel Bcl-2 family inhibitor, in patients with small-cell lung cancer and other solid tumors. J Clin Oncol. 2011;29(7):909-916.
15. Souers AJ, Leverson JD, Boghaert ER, et al. ABT-199, a potent and selective BCL-2 inhibitor, achieves antitumor activity while sparing platelets. Nat Med. 2013;19(2):202-208.
16. Vandenberg CJ, Cory S. ABT-199, a new Bcl-2- specific BH3 mimetic, has in vivo efficacy against aggressive Myc-driven mouse lymphomas without provoking thrombocytopenia. Blood. 2013; 121(12):2285-2288.
17. Vaillant F, Merino D, Lee L, et al. Targeting BCL-2 with the BH3 mimetic ABT-199 in estrogen receptor-positive breast cancer. Cancer Cell. 2013;24(1):120-129.
18. Vogler M, Dinsdale D, Dyer MJ, Cohen GM. ABT-199 selectively inhibits BCL2 but not BCL2L1 and efficiently induces apoptosis of chronic lymphocytic leukaemic cells but not platelets. Br J Haematol. 2013;163(1):139-142.
19. Touzeau C, Dousset C, Le Gouill S, et al. The Bcl-2 specific BH3 mimetic ABT-199: a promising targeted therapy for t(11;14) multiple myeloma. Leukemia. 2014;28(1):210-212.
20. Anderson NM, Harrold I, Mansour MR, et al. BCL2-specific inhibitor ABT-199 synergizes strongly with cytarabine against the early immature LOUCY cell line but not moredifferentiated T-ALL cell lines [published online ahead of print Dec 17, 2013]. Leukemia.
21. Pan R, Hogdal LJ, Benito JM, et al. Selective BCL-2 inhibition by ABT-199 causes on target cell death in acute myeloid leukemia [published online ahead of print Dec 17, 2013]. Cancer Discov.
22. Niu X, Wang G, Wang Y, et al. Acute myeloid leukemia cells harboring MLL fusion genes or with the acute promyelocytic leukemia phenotype are sensitive to the Bcl-2-selective inhibitor ABT-199 [published online ahead of print Feb 17, 2014]. Leukemia.
23. Davids MS, Seymour JF, Gerecitano JF, et al. The single-agent Bcl-2 inhibitor ABT-199 (GDC-0199) in patients with relapsed/refractory (R/R) non-hodgkin lymphoma (NHL): responses observed in all mantle cell lymphoma (MCL) patients [abstract]. Blood. 2013;122(21). Abstract 1789.
24. Garraway LA, Jänne PA. Circumventing cancer drug resistance in the era of personalized medicine. Cancer Discov. 2012;2(3):214-226.
25. Montagut C, Dalmases A, Bellosillo B, et al. Identification of a mutation in the extracellular domain of the Epidermal Growth Factor Receptor conferring cetuximab resistance in colorectal cancer. Nat Med. 2012;18(2):221-223.
26. Shah NP, Nicoll JM, Nagar B, et al. Multiple BCRABL kinase domain mutations confer polyclonal resistance to the tyrosine kinase inhibitor imatinib (STI571) in chronic phase and blast crisis chronic myeloid leukemia. Cancer Cell. 2002;2(2): 117-125. (Pubitemid 41039112)
27. Beltran E, Fresquet V, Martinez-Useros J, et al. A cyclin-D1 interaction with BAX underlies its oncogenic role and potential as a therapeutic target in mantle cell lymphoma. Proc Natl Acad Sci USA. 2011;108(30):12461-12466.
28. Richter-Larrea JA, Robles EF, Fresquet V, et al. Reversion of epigenetically mediated BIM silencing overcomes chemoresistance in Burkitt lymphoma. Blood. 2010;116(14):2531-2542.
29. Petros AM, Medek A, Nettesheim DG, et al. Solution structure of the antiapoptotic protein bcl-2. Proc Natl Acad Sci USA. 2001;98(6): 3012-3017. (Pubitemid 32220791)
30. Sagardoy A, Martinez-Ferrandis JI, Roa S, et al. Downregulation of FOXP1 is required during germinal center B-cell function. Blood. 2013; 121(21):4311-4320.
31. Jerabek-Willemsen M, Wienken CJ, Braun D, Baaske P, Duhr S. Molecular interaction studies using microscale thermophoresis. Assay Drug Dev Technol. 2011;9(4):342-353.
32. Seidel SA, Dijkman PM, Lea WA, et al. Microscale thermophoresis quantifies biomolecular interactions under previously challenging conditions. Methods. 2013;59(3):301-315.
33. Vicente-Dueñas C, Fontán L, Gonzalez-Herrero I, et al. Expression of MALT1 oncogene in hematopoietic stem/progenitor cells recapitulates the pathogenesis of human lymphoma in mice. Proc Natl Acad Sci USA. 2012;109(26): 10534-10539.
34. Schindelin J, Arganda-Carreras I, Frise E, et al. Fiji: an open-source platform for biological-image analysis. Nat Methods. 2012;9(7):676-682.
35. Nechushtan A, Smith CL, Hsu YT, Youle RJ. Conformation of the Bax C-terminus regulates subcellular location and cell death. EMBO J. 1999;18(9):2330-2341. (Pubitemid 29213267)
36. Wolter KG, Hsu YT, Smith CL, Nechushtan A, Xi XG, Youle RJ. Movement of Bax from the cytosol to mitochondria during apoptosis. J Cell Biol. 1997;139(5):1281-1292. (Pubitemid 27523214)
37. Zhou H, Hou Q, Hansen JL, Hsu YT. Complete activation of Bax by a single site mutation. Oncogene. 2007;26(50):7092-7102. (Pubitemid 350059677)
38. Lohr JG, Stojanov P, Lawrence MS, et al. Discovery and prioritization of somatic mutations in diffuse large B-cell lymphoma (DLBCL) by whole-exome sequencing. Proc Natl Acad Sci USA. 2012;109(10):3879-3884.
39. Schuetz JM, Johnson NA, Morin RD, et al. BCL2 mutations in diffuse large B-cell lymphoma. Leukemia. 2012;26(6):1383-1390.
40. Rampino N, Yamamoto H, Ionov Y, et al. Somatic frameshift mutations in the BAX gene in colon cancers of the microsatellite mutator phenotype. Science. 1997;275(5302):967-969. (Pubitemid 27087710)
41. Ionov Y, Yamamoto H, Krajewski S, Reed JC, Perucho M. Mutational inactivation of the proapoptotic gene BAX confers selective advantage during tumor clonal evolution. Proc Natl Acad Sci USA. 2000;97(20):10872-10877.
42. Brimmell M, Mendiola R, Mangion J, Packham G. BAX frameshift mutations in cell lines derived from human haemopoietic malignancies are associated with resistance to apoptosis and microsatellite instability. Oncogene. 1998;16(14):1803-1812. (Pubitemid 28197400)
43. Meijerink JP, Mensink EJ, Wang K, et al. Hematopoietic malignancies demonstrate loss-of-function mutations of BAX. Blood. 1998;91(8):2991-2997. (Pubitemid 28227551)
44. Poulikakos PI, Persaud Y, Janakiraman M, et al. RAF inhibitor resistance is mediated by dimerization of aberrantly spliced BRAF(V600E). Nature. 2011;480(7377):387-390.
45. Knoechel B, Roderick JE, Williamson KE, et al. An epigenetic mechanism of resistance to targeted therapy in T cell acute lymphoblastic leukemia. Nat Genet. 2014;46(4):364-370.
46. Konopleva M, Contractor R, Tsao T, et al. Mechanisms of apoptosis sensitivity and resistance to the BH3 mimetic ABT-737 in acute myeloid leukemia. Cancer Cell. 2006;10(5): 375-388. (Pubitemid 44693472)
47. Mazumder S, Choudhary GS, Al-Harbi S, Almasan A. Mcl-1 Phosphorylation defines ABT-737 resistance that can be overcome by increased NOXA expression in leukemic B cells. Cancer Res. 2012;72(12):3069-3079.
48. Touzeau C, Dousset C, Bodet L, et al. ABT-737 induces apoptosis in mantle cell lymphoma cells with a Bcl-2high/Mcl-1low profile and synergizes with other antineoplastic agents. Clin Cancer Res. 2011;17(18): 5973-5981.
49. Letai AG. Diagnosing and exploiting cancer's addiction to blocks in apoptosis. Nat Rev Cancer. 2008;8(2):121-132. (Pubitemid 351161322)
50. Nguyen M, Marcellus RC, Roulston A, et al. Small molecule obatoclax (GX15-070) antagonizes MCL-1 and overcomes MCL-1- mediated resistance to apoptosis. Proc Natl Acad Sci USA. 2007;104(49):19512-19517.
51. BCL-2 inhibitor yields high response in CLL and SLL. Cancer Discov. 2014;4(2):OF5.