Targeting the B-cell lymphoma/leukemia 2 family in cancer

Journal of Clinical Oncology

Volumn 30, Issue 25, 2012, Pages 3127-3135

  Davids, Matthew S ^a   Letai, Anthony ^a  

^a DANA FARBER CANCER INSTITUTE   (United States)

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; ABT 199; BENDAMUSTINE; BIOLOGICAL MARKER; CARBOPLATIN; CYCLOPHOSPHAMIDE; DEXAMETHASONE; ETOPOSIDE; FLUDARABINE; NAVITOCLAX; OBATOCLAX; OBLIMERSEN; PROTEIN BCL 2; RITUXIMAB; UNCLASSIFIED DRUG;

ANEMIA; ARTICLE; BONE MARROW TOXICITY; CANCER CELL DESTRUCTION; CHRONIC LYMPHATIC LEUKEMIA; DIARRHEA; DRUG EFFECT; DRUG EFFICACY; DRUG MECHANISM; DRUG RESPONSE; DRUG TARGETING; FATIGUE; HUMAN; LUNG SMALL CELL CANCER; LYMPHOCYTOPENIA; MELANOMA; MULTIPLE MYELOMA; NAUSEA; NEOPLASM; NEUTROPENIA; NONHUMAN; PRIORITY JOURNAL; PROTEIN FUNCTION; PROTEIN PROTEIN INTERACTION; THROMBOCYTHEMIA; THROMBOCYTOPENIA;

ANILINE COMPOUNDS; ANIMALS; ANTINEOPLASTIC AGENTS; APOPTOSIS; BIPHENYL COMPOUNDS; DRUG RESISTANCE, NEOPLASM; HUMANS; MOLECULAR TARGETED THERAPY; NEOPLASMS; NITROPHENOLS; PIPERAZINES; PROTO-ONCOGENE PROTEINS C-BCL-2; PYRROLES; SULFONAMIDES; THIONUCLEOTIDES; TREATMENT OUTCOME;

EID: 84865736998     PISSN: 0732183X     EISSN: 15277755     Source Type: Journal    
DOI: 10.1200/JCO.2011.37.0981     Document Type: Article

References (72)

1. Tsujimoto Y, Finger LR, Yunis J, et al: Cloning of the chromosome breakpoint of neoplastic B cells with the t(14;18) chromosome translocation. Science 226:1097-1099, 1984
2. Tsujimoto Y, Jaffe E, Cossman J, et al: Clustering of breakpoints on chromosome 11 in human B-cell neoplasms with the t(11;14) chromosome translocation. Nature 315:340-343, 1985
3. Bakhshi A, Jensen JP, Goldman P, et al: Cloning the chromosomal breakpoint of t(14;18) human lymphomas: Clustering around JH on chromosome 14 and near a transcriptional unit on 18. Cell 41:899-906, 1985
4. Cleary ML, Sklar J: Nucleotide sequence of a t(14;18) chromosomal breakpoint in follicular lymphoma and demonstration of a breakpoint-cluster region near a transcriptionally active locus on chromosome 18. Proc Natl Acad Sci U S A 82:7439-7443, 1985
5. Pegoraro L, Palumbo A, Erikson J, et al: A 14;18 and an 8;14 chromosome translocation in a cell line derived from an acute B-cell leukemia. Proc Natl Acad Sci U S A 81:7166-7170, 1984
6. McDonnell TJ, Deane N, Platt FM, et al: Bcl-2-immunoglobulin transgenic mice demonstrate extended B cell survival and follicular lymphoproliferation. Cell 57:79-88, 1989
7. Vaux DL, Cory S, Adams JM: Bcl-2 gene promotes haemopoietic cell survival and cooperates with c-myc to immortalize pre-B cells. Nature 335:440-442, 1988
8. Hockenbery D, Nuñez G, Milliman C, et al: Bcl-2 is an inner mitochondrial membrane protein that blocks programmed cell death. Nature 348:334-336, 1990
9. Boise LH, González-García M, Postema CE, et al: Bcl-x, a bcl-2-related gene that functions as a dominant regulator of apoptotic cell death. Cell 74:597-608, 1993
10. Gibson L, Holmgreen SP, Huang DC, et al: Bcl-w, a novel member of the bcl-2 family, promotes cell survival. Oncogene 13:665-675, 1996
11. Kozopas KM, Yang T, Buchan HL, et al: MCL1, a gene expressed in programmed myeloid cell differentiation, has sequence similarity to BCL2. Proc Natl Acad Sci U S A 90:3516-3520, 1993
12. Choi SS, Park IC, Yun JW, et al: A novel Bcl-2 related gene, Bfl-1, is overexpressed in stomach cancer and preferentially expressed in bone marrow. Oncogene 11:1693-1698, 1995
13. Oltvai ZN, Milliman CL, Korsmeyer SJ: Bcl-2 heterodimerizes in vivo with a conserved homolog, Bax, that accelerates programmed cell death. Cell 74:609-619, 1993
14. Del Gaizo Moore V, Schlis KD, Sallan SE, et al: BCL-2 dependence and ABT-737 sensitivity in acute lymphoblastic leukemia. Blood 111:2300-2309, 2008
15. Kuwana T, Mackey MR, Perkins G, et al: Bid, Bax, and lipids cooperate to form supramolecular openings in the outer mitochondrial membrane. Cell 111:331-342, 2002
16. Antonsson B, Montessuit S, Lauper S, et al: Bax oligomerization is required for channel-forming activity in liposomes and to trigger cytochrome c release from mitochondria. Biochem J 345:271-278, 2000
17. Korsmeyer SJ, Wei MC, Saito M, et al: Proapoptotic cascade activates BID, which oligomerizes BAK or BAX into pores that result in the release of cytochrome c. Cell Death Differ 7:1166-1173, 2000
18. Lindsten T, Ross AJ, King A, et al: The combined functions of proapoptotic Bcl-2 family members Bak and Bax are essential for normal development of multiple tissues. Mol Cell 6:1389-1399, 2000
19. Cartron PF, Gallenne T, Bougras G, et al: The first alpha helix of Bax plays a necessary role in its ligand-induced activation by the BH3-only proteins Bid and PUMA. Mol Cell 16:807-818, 2004
20. Wei MC, Lindsten T, Mootha VK, et al: TBID, a membrane-targeted death ligand, oligomerizes BAK to release cytochrome c. Genes Dev 14:2060-2071, 2000
21. Kuwana T, Bouchier-Hayes L, Chipuk JE, et al: BH3 domains of BH3-only proteins differentially regulate Bax-mediated mitochondrial membrane permeabilization both directly and indirectly. Mol Cell 17:525-535, 2005
22. Willis SN, Fletcher JI, Kaufmann T, et al: Apoptosis initiated when BH3 ligands engage multiple Bcl-2 homologs, not Bax or Bak. Science 315:856-859, 2007
23. Cheng EH, Levine B, Boise LH, et al: Bax-independent inhibition of apoptosis by Bcl-XL. Nature 379:554-556, 1996
24. Cheng EH, Wei MC, Weiler S, et al: BCL-2, BCL-X(L) sequester BH3 domain-only molecules preventing BAX- and BAK-mediated mitochondrial apoptosis. Mol Cell 8:705-711, 2001
25. Letai A, Bassik MC, Walensky LD, et al: Distinct BH3 domains either sensitize or activate mitochondrial apoptosis, serving as prototype cancer therapeutics. Cancer Cell 2:183-192, 2002
26. Zhai D, Jin C, Satterthwait AC, et al: Comparison of chemical inhibitors of antiapoptotic Bcl-2-family proteins. Cell Death Differ 13:1419-1421, 2006
27. Lopes de Menezes DE, Hudon N, McIntosh N, et al: Molecular and pharmacokinetic properties associated with the therapeutics of bcl-2 antisense oligonucleotide G3139 combined with free and liposomal doxorubicin. Clin Cancer Res 6:2891-2902, 2000
28. Cotter FE, Waters J, Cunningham D: Human Bcl-2 antisense therapy for lymphomas. Biochim Biochim Biophys Acta 1489:97-106, 1999
29. O'Brien SM, Cunningham CC, Golenkov AK, et al: Phase I to II multicenter study of oblimersen sodium, a Bcl-2 antisense oligonucleotide, in patients with advanced chronic lymphocytic leukemia. J Clin Oncol 23:7697-7702, 2005
30. Badros AZ, Goloubeva O, Rapoport AP, et al: Phase II study of G3139, a Bcl-2 antisense oligonucleotide, in combination with dexamethasone and thalidomide in relapsed multiple myeloma patients. J Clin Oncol 23:4089-4099, 2005
31. Bedikian AY, Millward M, Pehamberger H, et al: Bcl-2 antisense (oblimersen sodium) plus dacarbazine in patients with advanced melanoma: The Oblimersen Melanoma Study Group. J Clin Oncol 24:4738-4745, 2006
32. Chanan-Khan AA, Niesvizky R, Hohl RJ, et al: Phase III randomised study of dexamethasone with or without oblimersen sodium for patients with advanced multiple myeloma. Leuk Lymphoma 50: 559-565, 2009
33. O'Brien S, Moore JO, Boyd TE, et al: 5-year survival in patients with relapsed or refractory chronic lymphocytic leukemia in a randomized, phase III trial of fludarabine plus cyclophosphamide with or without oblimersen. J Clin Oncol 27:5208-5212, 2009
34. Benimetskaya L, Miller P, Benimetsky S, et al: Inhibition of potentially anti-apoptotic proteins by antisense protein kinase C-alpha (Isis 3521) and antisense bcl-2 (G3139) phosphorothioate oligodeoxynucleotides: Relationship to the decreased viability of T24 bladder and PC3 prostate cancer cells. Mol Pharmacol 60:1296-1307, 2001
35. Dai G, Chan KK, Liu S, et al: Cellular uptake and intracellular levels of the bcl-2 antisense g3139 in cultured cells and treated patients with acute myeloid leukemia. Clin Cancer Res 11:2998-3008, 2005
36. 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 U S A 104:19512-19517, 2007
37. Konopleva M, Watt J, Contractor R, et al: Mechanisms of antileukemic activity of the novel Bcl-2 homology domain-3 mimetic GX15-070 (obatoclax). Cancer Res 68:3413-3420, 2008
38. Schimmer AD, O'Brien S, Kantarjian H, et al: A phase I study of the pan bcl-2 family inhibitor obatoclax mesylate in patients with advanced hematologic malignancies. Clin Cancer Res 14:8295-8301, 2008
39. Brown JR, Tesar B, Werner L, et al: Obatoclax in combination with fludarabine and rituximab (FR) is well-tolerated and shows promising clinical activity in relapsed CLL/SLL. Presented at the 53rd Annual Meeting of the American Society of Hematology, San Diego, CA, December 10-13, 2011
40. Paik PK, Rudin CM, Brown A, et al: A phase I study of obatoclax mesylate, a Bcl-2 antagonist, plus topotecan in solid tumor malignancies. Cancer Chemother Pharmacol 66:1079-1085, 2010
41. Langer CJ, Albert P, Kovacs P, et al: A randomized phase II study of carboplatin (C) and etoposide (E) with or without pan-BCL-2 antagonist obatoclax (Ob) in extensive-stage small cell lung cancer (ES-SCLC). J Clin Oncol 29:453s, 2011 (suppl 15; abstr 7001)
42. Oltersdorf T, Elmore SW, Shoemaker AR, et al: An inhibitor of Bcl-2 family proteins induces regression of solid tumours. Nature 435:677-681, 2005
43. Certo M, Del Gaizo Moore V, Nishino M, et al: Mitochondria primed by death signals determine cellular addiction to antiapoptotic BCL-2 family members. Cancer Cell 9:351-365, 2006
44. Chen L, Willis SN, Wei A, et al: Differential targeting of prosurvival Bcl-2 proteins by their BH3- only ligands allows complementary apoptotic function. Mol Cell 17:393-403, 2005
45. Tse C, Shoemaker AR, Adickes J, et al: ABT-263: a potent and orally bioavailable Bcl-2 family inhibitor. Cancer Res 68:3421-3428, 2008
46. Vogler M, Weber K, Dinsdale D, et al: Different forms of cell death induced by putative BCL2 inhibitors. Cell Death Differ 16:1030-1039, 2009
47. Del Gaizo Moore V, Brown JR, Certo M, et al: Chronic lymphocytic leukemia requires BCL2 to sequester prodeath BIM, explaining sensitivity to BCL2 antagonist ABT-737. J Clin Invest 117:112-121, 2007
48. 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 10:389-399, 2006
49. Deng J, Carlson N, Takeyama K, et al: BH3 profiling identifies three distinct classes of apoptotic blocks to predict response to ABT-737 and conventional chemotherapeutic agents. Cancer Cell 12:171-185, 2007
50. Zhang H, Nimmer PM, Tahir SK, et al: Bcl-2 family proteins are essential for platelet survival. Cell Death Differ 14:943-951, 2007
51. Vogler M, Hamali HA, Sun XM, et al: BCL2/BCL-X(L) inhibition induces apoptosis, disrupts cellular calcium homeostasis, and prevents platelet activation. Blood 117:7145-7154, 2011
52. Schoenwaelder SM, Jarman KE, Gardiner EE, et al: Bcl-xL-inhibitory BH3 mimetics can induce a transient thrombocytopathy that undermines the hemostatic function of platelets. Blood 118:1663-1674, 2011
53. 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 30:488-496, 2012
54. Mason KD, Carpinelli MR, Fletcher JI, et al: Programmed anuclear cell death delimits platelet life span. Cell 128:1173-1186, 2007
55. Wilson WH, O'Connor OA, Czuczman MS, et al: Navitoclax, a targeted high-affinity inhibitor of BCL-2, in lymphoid malignancies: A phase 1 dose-escalation study of safety, pharmacokinetics, pharmacodynamics, and antitumour activity. Lancet Oncol 11:1149-1159, 2010
56. 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 29:909-916, 2011
57. Kipps TJ, Swinnen LJ, Wierda WG, et al: Navitoclax (ABT-263) plus fludarabine/cyclophosphamide/rituximab (FCR) or bendaymustine/rituximab (BR): A phase I study in patients with relapsed/refractory CLL. Presented at the 53rd Annual Meeting of the American Society of Hematology, San Diego, CA, December 10-13, 2011
58. 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 10:375-388, 2006
59. 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 113:4403-4413, 2009
60. Yecies D, Carlson NE, Deng J, et al: Acquired resistance to ABT-737 in lymphoma cells that upregulate MCL-1 and BFL-1. Blood 115:3304-3313, 2010
61. Al-Harbi S, Hill BT, Mazumder S, et al: An antiapoptotic BCL-2 family expression index predicts the response of chronic lymphocytic leukemia to ABT-737. Blood 118:3579-3590, 2011
62. Tromp JM, Geest CR, Breij EC, et al: Tipping the Noxa/Mcl-1 balance overcomes ABT-737 resistance in chronic lymphocytic leukemia. Clin Cancer Res 18:487-498, 2012
63. Skipper HE, Perry S: Kinetics of normal and leukemic leukocyte populations and relevance to chemotherapy. Cancer Res 30:1883-1897, 1970
64. Messmer BT, Messmer D, Allen SL, et al: In vivo measurements document the dynamic cellular kinetics of chronic lymphocytic leukemia B cells. J Clin Invest 115:755-764, 2005
65. Weinstein GD, McCullough JL, Ross P: Cell proliferation in normal epidermis. J Invest Dermatol 82:623-628, 1984
66. Holdaway KM, Finlay GJ, Baguley BC: Relationship of cell cycle parameters to in vitro and in vivo chemosensitivity for a series of Lewis lung carcinoma lines. Eur J Cancer 28A:1427-1431, 1992
67. Petru E, Sevin BU, Haas J, et al: A correlation of cell cycle perturbations with chemosensitivity in human ovarian cancer cells exposed to cytotoxic drugs in vitro. Gynecol Oncol 58:48-57, 1995
68. Hochhauser D: Modulation of chemosensitivity through altered expression of cell cycle regulatory genes in cancer. Anticancer Drugs 8:903-910, 1997
69. Ni Chonghaile T, Sarosiek KA, Vo TT, et al: Pretreatment mitochondrial priming correlates with clinical response to cytotoxic chemotherapy. Science 334:1129-1133, 2011
70. Ryan JA, Brunelle JK, Letai A: Heightened mitochondrial priming is the basis for apoptotic hypersensitivity of CD4+ CD8+ thymocytes. Proc Natl Acad Sci U S A 107:12895-12900, 2010
71. Dawson SJ, Makretsov N, Blows FM, et al: BCL2 in breast cancer: A favourable prognostic marker across molecular subtypes and independent of adjuvant therapy received. Br J Cancer 103:668-675, 2010
72. Hamilton A, Piccart M: The contribution of molecular markers to the prediction of response in the treatment of breast cancer: A review of the literature on HER-2, p53 and BCL-2. Ann Oncol11: 647-663, 2000