Finally, an apoptosis-targeting therapeutic for cancer

Cancer Research

Volumn 76, Issue 20, 2016, Pages 5914-5920

  Croce, Carlo M ^a   Reed, John C ^b,c  

^a OHIO STATE UNIVERSITY   (United States)

^b F HOFFMANN LA ROCHE LTD   (Switzerland)

^c ETH ZURICH   (Switzerland)

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; AZACITIDINE; BORTEZOMIB; CYCLOPHOSPHAMIDE; DECITABINE; FLUDARABINE; IDASANUTLIN; MESSENGER RNA; NAVITOCLAX; OBINUTUZUMAB; OBLIMERSEN; PROTEIN BCL 2; PROTEIN BCL XL; PROTEIN MCL 1; PROTEIN P53; RITUXIMAB; VENETOCLAX; ANTINEOPLASTIC AGENT; PROTEIN BCL X;

ACUTE MYELOBLASTIC LEUKEMIA; APOPTOSIS; BCL 2 GENE; CANCER RESISTANCE; CHROMOSOME 17P; CHROMOSOME DELETION; CHROMOSOME TRANSLOCATION 14; CHROMOSOME TRANSLOCATION 18; CHRONIC LYMPHATIC LEUKEMIA; DRUG TARGETING; GENE EXPRESSION; HEMATOLOGIC MALIGNANCY; HUMAN; LARGE CELL LYMPHOMA; LYMPHOCYTOPENIA; MANTLE CELL LYMPHOMA; MONOTHERAPY; MULTIPLE MYELOMA; NEUTROPENIA; NONHODGKIN LYMPHOMA; NONHUMAN; PRIORITY JOURNAL; PROGRESSION FREE SURVIVAL; REVIEW; STRUCTURE ACTIVITY RELATION; THROMBOCYTOPENIA; TUMOR LYSIS SYNDROME; WALDENSTROEM MACROGLOBULINEMIA; ANIMAL; ANTAGONISTS AND INHIBITORS; DRUG DESIGN; DRUG EFFECTS; LEUKEMIA, LYMPHOCYTIC, CHRONIC, B-CELL; NEOPLASMS; PHYSIOLOGY;

ANIMALS; ANTINEOPLASTIC AGENTS; APOPTOSIS; BCL-X PROTEIN; DRUG DESIGN; HUMANS; LEUKEMIA, LYMPHOCYTIC, CHRONIC, B-CELL; NEOPLASMS; PROTO-ONCOGENE PROTEINS C-BCL-2;

EID: 84991744708     PISSN: 00085472     EISSN: 15387445     Source Type: Journal    
DOI: 10.1158/0008-5472.CAN-16-1248     Document Type: Review

References (56)

1. Hanahan D, Weinberg RA. Hallmarks of cancer: the next generation. Cell 2011;144:646-74.
2. Tsujimoto Y, Finger LR, Yunis J, Nowell PC, Croce CM. Cloning of the chromosome breakpoint of neoplastic B cells with the t(14;18) chromosome translocation. Science 1984;226:1097-9.
3. Tsujimoto Y, Cossman J, Jaffe E, Croce C. Involvement of the Bcl-2 gene in human follicular lymphoma. Science 1985;228:1440-3.
4. Tsujimoto Y, Croce C. Analysis of the structure, transcripts, and protein products of Bcl-2, the gene involved in human follicular lymphoma. Proc Natl Acad Sci USA 1986;83:5214-8.
5. Hanada M, Delia D, Aiello A, Stadtmauer E, Reed J. Bcl-2 gene hypomethylation and high-level expression in B-cell chronic lymphocytic leukemia. Blood 1993;82:1820-8.
6. Adachi M, Cossman J, Longo D, Croce CM, Tsujimoto Y. Variant translocation of the bcl-2 gene to immunoglobulin lambda light chain gene in chronic lymphocytic leukemia. Proc Natl Acad Sci U S A 1989; 86:2771-4.
7. McDonnell TJ, Nunez G, Platt FM, Hockenberry D, London L, McKearn JP, et al. Deregulated Bcl-2-immunoglobulin transgene expands a resting but responsive immunoglobulin M and D-expressing B-cell population. Mol Cell Biol 1990;10:1901-7.
8. Reed JC, Cuddy M, Slabiak T, Croce CM, Nowell PC. Oncogenic potential of bcl-2 demonstrated by gene transfer. Nature 1988;336:259-61.
9. Vaux DL, Cory S, Adams JM. Bcl-2 gene promotes haemopoietic cell survival and cooperates with c-myc to immortalize pre-B cells. Nature 1988;335:440-2.
10. Miyashita T, Reed JC. Bcl-2 gene transfer increases relative resistance of S49.1 and WEHI7.2 lymphoid cells to cell death and DNA fragmentation induced by glucocorticoids and multiple chemotherapeutic drugs. Cancer Res 1992;52:5407-1
11. Campos L, Roualult J-P, Sabido O, Oriol P, Roubi N, Vasselon C, et al. High expression of Bcl-2 protein in acute myeloid leukemia cells is associated with poor response to chemotherapy. Blood 1993;81: 3091-6.
12. Kitada S, Takayama S, De Riel K, Tanaka S, Reed JC. Reversal of chemoresistance of lymphoma cells by antisense-mediated reduction of Bcl-2 gene expression. Antisense Res Dev 1994;4:71-9.
13. Gascoyne RD, Adomat SA, Krajewski S, Krajewska M, Horsman DE, Tolcher AW, et al. Prognostic significance of Bcl-2 protein expression and Bcl-2 gene rearrangement in diffuse aggressive Non-Hodgkin's lymphoma. Blood 1997;90:244-51.
14. Tsujimoto Y, Ikegaki N, Croce CM. Characterization of the protein product of Bcl-2, the gene involved in human follicular lymphoma. Oncogene 1987;2:3-7.
15. Hockenbery DM, Nunez G, Milliman C, Schreiber RD, Korsmeyer SJ. Bcl-2 is an innermitochondrial membrane protein that blocks programmed cell death. Nature 1990;348:334-6.
16. Newmeyer D, Farschon DM, Reed JC. Cell-free apoptosis in Xenopus egg extracts: inhibition by Bcl-2 and requirement for an organelle fraction enriched in mitochondria. Cell 1994;79:353-64.
17. Kluck RM, Bossy-Wetzel E, Green DR, Newmeyer DD. The release of cytochrome c from mitochondria: a primary site for Bcl-2 regulation of apoptosis. Science 1997;275:1132-6.
18. Liu X, Kim CN, Yang J, Jemmerson R, Wang X. Induction of apoptotic program in cell-free extracts: requirement for dATP and Cytochrome c. Cell 1996;86:147-57.
19. Reed JC, Stein C, Subasinghe C, Haldar S, Croce CM, Yum S, et al. Antisense-mediated inhibition of BCL2 proto-oncogene expression and leukemic cell growth and survival: comparisons of phosphodiester and phosphorothioate oligodeoxynucleotides. Cancer Res 1990;50: 6565-70.
20. O'Brien S, Moore JO, Boyd TE, Haldar S, Croce CM, Yum S, et al. Randomized phase III trial of fludarabine plus cyclophosphamide with or without oblimersen sodium (Bcl-2 antisense) in patients with relapsed or refractory chronic lymphocytic leukemia. J Clin Oncol 2007; 25:1114-20.
21. Cimmino A, Calin GA, Fabbri M, Iorio MV, Ferracin M, Shimizu M, et al. miR-15 and miR-16 induce apoptosis by targeting BCL2. Proc Nat Acad Sci USA 2005;102:13944-9.
22. Oltvai Z, Milliman C, Korsmeyer S. Bcl-2 heterodimerizes in vivo with a conserved homolog, Bax, that accelerates programmed cell death. CELL 1993;74:609-19.
23. Wang K, Yin W-M, Chao DT, Milliman CL, Korsmeyer SJ. BID: a novel BH3 domain-only death agonist. Gene Dev 1996;10:2859-69.
24. Zha H, Aime-Sempe C, Sato T, Reed JC. Pro-apoptotic protein Bax heterodimerizes with Bcl-2 and homodimerizes with Bax via a novel domain (BH3) distinct from BH1 and BH2. J Biol Chem 1996;271: 7440-4.
25. Chang BS, Minn AJ, Muchmore SW, Fesik SW, Thompson CB. Identification of a novel regulatory domain in Bcl-xL and Bcl-2. EMBO J 1997; 16:968-77.
26. Cosulich S, Worrall V, Hedge P, Green S, Clarke P. Regulation of apoptosis by BH3 domains in a cell-free system. Curr Biol 1997;7: 913-20.
27. Muchmore SW, Sattler M, Liang H, Meadows RP, Harlan JE, Yoon HS, et al. X-ray and NMR structure of human Bcl-XL, an inhibitor of programmed cell death. Nature 1996;381:335-41.
28. Sattler M, Liang H, Nettesheim D, Meadows RP, Harlan JE, Eberstadt M, et al. Structure of Bcl-xL-Bak peptide complex: recognition between regulators of apoptosis. Science 1997;275:983-6.
29. Petros AM, Medek A, Nettesheim DG, Kim DH, Yoon HS, Swift K, et al. Solution structure of the antiapoptotic protein Bcl-2. ProcNatl Acad Sci USA 2001;98:3012-7.
30. Nguyen M, Marcellus RC, Roulston A, Watson M, Serfass L, Murthy Madiraju SR, 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 2007;104:19512-7.
31. Hajduk PJ, Gerfin T, Boehlen JM, Haberli M, Marek D, Fesik SW. Highthroughput nuclear magnetic resonance-based screening. J Med Chem 1999;42:2315-57.
32. Shuker SB, Hajduk PJ, Meadows RP, Fesik SW. Discovering high-affinity ligands for proteins: SAR by NMR. Science 1996;274:1531-4.
33. Oltersdorf T, Elmore SW, Shoemaker AR, Armstrong RC, Augeri DJ, Belli BA, et al. An inhibitor of Bcl-2 family proteins induces regression of solid tumours. Nature 2005;435:677-81.
34. Tse C, Shoemaker AR, Adickes J, Anderson MG, Chen J, Jin S, et al. ABT-263: a potent and orally bioavailable Bcl-2 family inhibitor. Cancer Res 2008;68:3421-8.
35. Wilson WH, O'Connor OA, Czuczman MS, La Casce AS, Gerecitano JF, Leonard JP, 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 2010;11:1149-59.
36. Kipps TJ, Eradat H, Grosicki S, Catalano J, Cosolo W, Dyagil IS, et al. A phase 2 study of the BH3 mimetic BCL2 inhibitor navitoclax (ABT-263) with or without rituximab, in previously untreated B-cell chronic lymphocytic leukemia. Leuk Lymphoma 2015;56:2826-33.
37. Roberts AW, Seymour JF, Brown JR, Wierda WG, Kipps TJ, Khaw SL, 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;30:488-96.
38. Gandhi L, Camidge DR, Ribeiro de Oliveira M, Bonomi P, Gandara D, Khaira D, 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;29:909-16.
39. Rudin CM, Hann CL, Garon EB, Ribeiro de Oliveira M, Bonomi PD, et al. Phase II study of single-agent navitoclax (ABT-263) and biomarker correlates in patients with relapsed small cell lung cancer. Clin Cancer Res 2012;18:3163-9.
40. Mason KD, Carpinelli MR, Fletcher JI, Collinge JE, Hilton AA, Ellis S, et al. Programmed anuclear cell death delimits platelet life span. Cell 2007; 128:1173-86.
41. Souers AJ, Leverson JD, Boghaert ER, Ackler SL, Catron ND, Chen J, et al. ABT-199, a potent and selective BCL-2 inhibitor, achieves antitumor activity while sparing platelets. Nat Med 2013;19:202-8.
42. Konopleva M, Contractor R, Tsao T, Samudio I, Ruvolo PP, Kitada S, et al. Mechanisms of apoptosis sensitivity and resistance to the BH3 mimetic ABT-737 in acute myeloid leukemia. Cancer Cell 2006;10:375-88.
43. Vogler M, Butterworth M, Majid A, Walewska RJ, Sun XM, Dyer MJ, et al. Concurrent up-regulation of BCL-XL and BCL2A1 induces approximately 1000-fold resistance to ABT-737 in chronic lymphocytic leukemia. Blood 2009;113:4403-13.
44. Davids MS, Seymour JF, Gerecitano JF, Kahl BS, Pagel JM, Wierda WG, et al. Phase I study of ABT-199 (GDC-0199) in patients with relapsed/refractory non-Hodgkin lymphoma: responses observed in diffuse large B-cell (DLBCL) and follicular lymphoma (FL) at higher cohort doses. Clin Adv Hematol Oncol 2014;12:18-9.
45. Roberts AW, Davids MS, Pagel JM, Kahl BS, Puvvada SD, Gerecitano JF, et al. Targeting BCL2 with venetoclax in relapsed chronic lymphocytic leukemia. N Engl J Med 2016;374:311-22.
46. Seymour JF. Reduction of tumor lysis syndrome (Tls) risk in chronic lymphocytic leukemia (Cll) patients treated with Abt-199 (Gdc-0199): results of modifications to dosing schedule and Tls prophylaxis. Haematologica 2014;99:321.
47. Miyashita T, Reed JC. Tumor suppressor p53 is a direct transcriptional activator of human BAX gene. Cell 1995;80:293-9.
48. Yu J, Wang Z, Kinzler KW, Vogelstein B, Zhang L. PUMA mediates the apoptotic response to p53 in colorectal cancer cells. Proc Natl Acad Sci USA 2003;100:1931-6.
49. Sax JK, Fei P, Murphy ME, Bernhard E, Korsmeyer SJ, El-Deiry WS. BID regulation by p53 contributes to chemosensitivity. Nat Cell Biol 2002;4:842-9.
50. Giles A, Salles MD, Boyd TE, Morschhauser F, Wendtner C-M, Hallek M, et al. Updated Safety and Preliminary Efficacy Data from a phase 1b study combining venetoclax (GDC-0199, ABT-199)with bendamustine/rituximab in patients with relapsed/refractory or previously untrated chronic lymphocitic leukemia. American Society of Hematology 57th Annual Meeting and Exposition, Orlando, FL, December 5-8, 2015, Abstract #829. https://ash. confex.com/ash/2015/webprogramscheduler/Paper78695.html.
51. Byrd JC, Kitada S, Flinn IW, Aron JL, Pearson M, Lucas D, et al. The mechanism of tumor cell clearance by rituximab in vivo in patients with B-cell chronic lymphocytic leukemia: evidence of caspase activation and apoptosis induction. Blood 2002;99:1038-43.
52. Konopleva M, Pollyea DA, Potluri J, Chyla B, Hogdal L, Busman T, et al. A phase 2 study of ABT-199 (GDC-0199) in patients with acute myelogenous leukemia (AML). American Society of Hematology 56th Annual Meeting & Exposition, San Francisco, CA, December 6-9, 2014, Abstract #118.
53. Di Nardo C, Pollyea D, Pratz K, Thirman MJ, Letai A, Frattini M, et al. A phase 1bstudy of venetoclax (ABT-199/GDC-0199) in combinationwith decitabine or azacitidine in treatment-naive patients with acute myelogenous leukemia who are ≥ to 65 years and not eligible for standard induction therapy. American Society of Hematology 57th Annual Meeting & Exposition, Orlando, FL, December 5-8, 2015, Abstract #327.
54. Kojima K, Konopleva M, Samudio IJ, Ruvolo V, Andreeff M. MDM2 antagonists induce p53-dependent apoptosis in AML: implications for leukemia therapy. Blood 2005;106:3150-9.
55. Reis B, Jukofsky L, Chen G, Martinelli G, Zhong H, So WV, et al. Acute myeloid leukemia patient clinical response to idasanutlin (RG7388) is associated with pre-treatment MDM2 protein expression in leukemic blasts. Haematologica 2016;101:e185-8.
56. Moreau P, Chanan-Khan A, Roberts AW, Agarwal AB, Facon T, Kumar S, et al. Safety and efficacy of venetoclax (ABT-199/GDC-0199) in combination with bortezomib and dexamethasone in relapsed/refractory multiple myeloma: phase 1b results. Blood 2015;126: 3038.