The BH3-only mimetic ABT-737 synergizes the antineoplastic activity of proteasome inhibitors in lymphoid malignancies

Blood

Volumn 112, Issue 7, 2008, Pages 2906-2916

  Paoluzzi, Luca ^a   Gonen, Mithat ^b   Bhagat, Govind ^a,c   Furman, Richard R ^d   Gardner, Jeffrey R ^b   Scotto, Luigi ^a   Gueorguiev, Volodia D ^b   Heaney, Mark L ^b   Manova, Katia ^b   O'Connor, Owen A ^a,c  

^a Och Spine at New York Presbyterian Hospitals   (United States)

^b MEMORIAL SLOAN KETTERING CANCER CENTER   (United States)

^c New York Presbyterian Hospital ^*  (United States)

^d NEW YORK PRESBYTERIAN HOSPITAL   (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; BH3 PROTEIN; BORTEZOMIB; CARFILZOMIB; PROTEASOME INHIBITOR; PROTEIN BCL 2; PROTEIN BCL W; PROTEIN BCL XL; UNCLASSIFIED DRUG; ABT-737; ANTINEOPLASTIC AGENT; BIPHENYL DERIVATIVE; BORONIC ACID DERIVATIVE; ENZYME INHIBITOR; NITROPHENOL; PIPERAZINE DERIVATIVE; PROTEASOME; PYRAZINE DERIVATIVE; SULFONAMIDE;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; APOPTOSIS; ARTICLE; B CELL LYMPHOMA; CELL LEVEL; CHRONIC LYMPHATIC LEUKEMIA; CONTROLLED STUDY; CYTOTOXICITY; DRUG EFFICACY; DRUG INHIBITION; HUMAN; HUMAN CELL; IMMUNE DEFICIENCY; IN VIVO STUDY; LARGE CELL LYMPHOMA; MANTLE CELL LYMPHOMA; MEMBRANE DEPOLARIZATION; MITOCHONDRIAL MEMBRANE; MOUSE; NONHUMAN; PERIPHERAL BLOOD STEM CELL; PRIORITY JOURNAL; ANIMAL; B CELL LEUKEMIA; CELL DEATH; CONFOCAL MICROSCOPY; DONOR; DOSE RESPONSE; DRUG ANTAGONISM; DRUG EFFECT; DRUG POTENTIATION; DRUG RESISTANCE; DRUG SCREENING; ENZYMOLOGY; HEALTH; LYMPHOMA; METABOLISM; MITOCHONDRIAL MEMBRANE POTENTIAL; MOLECULAR MIMICRY; MONONUCLEAR CELL; PATHOLOGY; TUMOR CELL LINE;

ANIMALS; ANTINEOPLASTIC AGENTS; BIPHENYL COMPOUNDS; BORONIC ACIDS; CELL DEATH; CELL LINE, TUMOR; DOSE-RESPONSE RELATIONSHIP, DRUG; DRUG RESISTANCE, NEOPLASM; DRUG SYNERGISM; ENZYME INHIBITORS; HEALTH; HUMANS; LEUKEMIA, LYMPHOCYTIC, CHRONIC, B-CELL; LEUKOCYTES, MONONUCLEAR; LYMPHOMA; LYMPHOMA, LARGE B-CELL, DIFFUSE; LYMPHOMA, MANTLE-CELL; MEMBRANE POTENTIAL, MITOCHONDRIAL; MICE; MICROSCOPY, CONFOCAL; MOLECULAR MIMICRY; NITROPHENOLS; PIPERAZINES; PROTEASOME ENDOPEPTIDASE COMPLEX; PROTO-ONCOGENE PROTEINS C-BCL-2; PYRAZINES; SULFONAMIDES; TISSUE DONORS; XENOGRAFT MODEL ANTITUMOR ASSAYS;

EID: 53049106757     PISSN: 00064971     EISSN: 15280020     Source Type: Journal    
DOI: 10.1182/blood-2007-12-130781     Document Type: Article

References (50)

1. McDonnell TJ, Korsmeyer SJ. Progression from lymphoid hyperplasia to high-grade malignant lymphoma in mice transgenic for the t(14; 18). Nature. 1991;349:254-256.
2. 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;275:1132-1136.
3. Korsmeyer SJ. BCL-2 gene family and the regulation of programmed cell death. Cancer Res. 1999;59(suppl 7);1693s-1700s.
4. Cory S, Huang DC. Adams JM. The Bcl-2 family: roles in cell survival and oncogenesis. Oncogene. 200322;8590-8607.
5. Yunis JJ, Frizzera G. Oken MM, McKenna J, Theologides A, Arnesen M. Multiple recurrent genomic defects in follicular lymphoma. A possible model for cancer. N Engl J Med. 1987;316: 79-84.
6. Yang E, Korsmeyer SJ. Molecular thanatopsis: a discourse on the BCL2 family and cell death. Blood. 1996;88:386-401.
7. Yang J, Liu X, Bhalla K, et al. Prevention of apoptosis by Bcl-2: release of cytochrome c from mitochondria blocked. Science. 1997;275:1129-1132.
8. Reed JC. Dysregulation of apoptosis in cancer. J Clin Oncol. 1999;17:2941-2953.
9. Wang JL, Liu D, Zhang ZJ, et al. Structure-based discovery of an organic compound that binds Bcl-2 protein and induces apoptosis of tumor cells. Proc Natl Acad Sci U S A. 2000;97:7124-7129.
10. Johnstone RW, Ruefli AA, Lowe SW. Apoptosis: a link between cancer genetics and chemotherapy. Cell. 2002;108:153-164.
11. Shangary S, Johnson DE. Peptides derived from BH3 domains of Bcl-2 family members: a comparative analysis of inhibition of Bcl-2, Bd-x(L) and Bax oligomerization, induction of cytochrome c release, and activation of cell death. Biochemistry. 2002;41:9485-9495.
12. Paoluzzi L, Gonen M, Gardner JR, et al. Targeting Bcl-2 family members with the BH3 mimetic AT-101 markedly enhances the therapeutic effects of chemotherapeutic agents in in vitro and in vivo models of B-cell lymphoma. Prepublished on February 21, 2008, as DOI 10.1182/blood-2007-12-129833. (Now available as Blood. 2008;111: 5350-5358.)
13. Oltersdorf T, Elmore SW, Shoemaker AR, et al. An inhibitor of Bcl-2 family proteins induces regression of solid tumors. Nature. 2005;435:677-681.
14. 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;10:389-399.
15. Richardson PG, Sonneveld P, Schuster MW, et al. Bortezomib or high-dose dexamethasone for relapsed multiple myeloma. N Engl J Med. 2005; 352:2487-2498.
16. O'Connor OA, Wright J, Moskowitz C, et al. Phase II clinical experience with the novel proteasome inhibitor bortezomib in patients with indolent non-Hodgkin's lymphoma and mantle cell lymphoma. J Clin Oncol. 2005;23:676-684.
17. Fisher RI, Bernstein SH, KahI BS, et al. Multicenter phase II study of bortezomib in patients with relapsed or refractory mantle cell lymphoma. J Clin Oncol. 2006;24:4867-4874.
18. Palombella VJ, RandoOJ, Goldberg AL, Maniatis T. The ubiquitin-proteasome pathway is required for processing the NF-kappa B1 precursor protein and the activation of NF-kappa B. Cell. 1994;78: 773-785.
19. Adams J. The proteasome: a suitable antineoplastic target. Nat Rev Cancer. 2004;4:349-360.
20. Paoluzzi L, O'Connor OA. Mechanistic rationale and clinical evidence for the efficacy of proteasome inhibitors against indolent and mantle cell lymphomas. BioDrugs. 2006;20:13-23.
21. Stapnes C, Doskeland AP, Hatfield K. et al. The proteasome inhibitors bortezomib and PR-171 have antiproliferative and proapoptotic effects on primary human acute myeloid leukaemia cells. Br J Haematol. 2007;136:814-828.
22. Demo SD, Kirk CJ, Aujay MA, et al. Antitumor activity of PR-171, a novel irreversible inhibitor of the proteasome. Cancer Res. 2007;67:6383-6391.
23. Kuhn DJ, Chen Q, Voorhees PM.et al. Potent activity of carfilzomib, a novel, irreversible inhibitor of the ubiquitin-proteasome pathway, against preclinical models of multiple myeloma. Blood. 2007;110:3281-3290.
24. q32) translocation from the ascites of a patient with diffuse large cell lymphoma. Leuk Lymphoma. 2001;40:419-423.
25. q32) translocation in an extranodal lymphoma. Blood. 2000;95:2930-2936.
26. Abe M, Nozawa Y, Wakasa H, Ohno H, Fukuhara S. Characterization and comparison of two newly established Epstein-Barr virus-negative lymphoma B-cell lines: surface markers, growth characteristics, cytogenetics, and transportability. Cancer. 1988;61:483-490.
27. Jackson N, Lowe J, Ball J, Bromidge E, Ling NR. Two new 1gA1-kappa plasma cell leukaemia cell lines (JJN-1 & JJN-2) which proliferate in response to B cell stimulatory factor 2. Clin Exp Immunol. 1989;75:93-99.
28. Jaffa ES, Harris NL, Stein H, Vardiman JW. World Health Organization Classification of Tumours: Pathology and Genetics of Tumours of Hematopoietic and Lymphoid Tissues. Lyon, France: IARC Press; 2001.
29. O'Connor OA, Smith EA, Toner LE, et al. The combination of the proteasome inhibitor bortezomib and the bcl-2 antisense molecule oblimersen sensitizes human B-cell lymphomas to cyclophosphamide. Clin Cancer Res. 2006;12: 2902-2911.
30. Boffa DJ, Waka J, Thomas D, et al. Measurement of apoptosis of intact human islets by confocal optical sectioning and stereologic analysis of YO-PRO-1-stained islets. Transplantation. 2005;79: 842-845.
31. Hockberg Y, Tamhane AC. Multiple Comparison Procedures. Wiley: New York, NY; 1987;1-450.
32. xL. Nat Cell Biol. 2001;3:173-182.
33. Klasa RJ, Bally MB, Ng R, Goldie JH, Gascoyne RD, Wong FM. Eradication of human non-Hodgkin's lymphoma in SCID mice by BCL-2 antisense oligonucleotides combined with low-dose cyclophosphamide. Clin Cancer Res. 2000;6: 2492-2500.
34. Smith MR, Jin F, Joshi I. Enhanced efficacy of therapy with antisense BCL-2 oligonucleotides plus anti-CD20 monoclonal antibody in scid mouse/human lymphoma xenografts. Mol Cancer Ther. 2004;3:1693-1699.
35. Kitada S, Leone M, Sareth S, et al. Discovery, characterization, and structure-activity relationships studies of proapoptotic polyphenols targeting B-cell Iymphocyte/leukemia-2 proteins. J Med Chem. 2003;46:4259-4264.
36. Letai A, Bassik MC, Walensky LD, Sorcinelli MD, Weiler S, Korsmeyer SJ. Distinct BH3 domains either sensitize or activate mitochondrial apoptosis, serving as prototype cancer therapeutics. Cancer Cell. 2002;2:183-192.
37. Danial NN, Korsmeyer SJ. Cell death: critical control points. Cell. 2004;116:205-219.
38. 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. 2005;17:525-535.
39. Walensky LD, Pitter K, Morash J, et al. Astapled BID BH3 helix directly binds and activates BAX. Mol Cell. 2006;24:199-210.
40. Certo M, Moore Vdel G. Nishino M, et al. Mitochondria primed by death signals determine cellular addiction to antiapoptotic BCL-2 family members. Cancer Cell. 2006;9:351-365.
41. 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. 2005;17:393-403.
42. L. but not Bcl-2. until displaced by BH3-only proteins. Genes Dev. 2005;19:1294-1305.
43. Oh KJ, Barbuto S, Pitter K, Morash J, Walensky LD, Korsmeyer SJ. A membrane-targeted BID BCL-2 homology 3 peptide is sufficient for high potency activation of BAX in vitro. J Biol Chem. 2006;281:36999-37008.
44. ShoemakerAR, Oleksijew A, Bauch J, et al. A small-molecule inhibitor of Bcl-XL potentiates the activity of cytotoxic drugs in vitro and in vivo. Cancer Res. 2006;66:8731-8739.
45. Chauhan D, Velankar M. Brahmandam M, et al. A novel Bcl-2/Bcl-X(L)/Bcl-w inhibitor ABT-737 as therapy in multiple myeloma. Oncogene. 2007; 26:2374-2380.
46. Trudel S, Stewart AK, Li Z, et al. The Bcl-2 family protein inhibitor, ABT-737, has substantial antimyeloma activity and shows synergistic effect with dexamethasone and melphalan. Clin Cancer Res. 2007;13(pt 1):621-629.
47. Kline MP, Rajkumar SV, Timm MM. et al. ABT-737, an inhibitor of Bcl-2 family proteins, is a potent inducer of apoptosis in multiple myeloma cells. Leukemia. 2007;21:1549-1560.
48. Pérez-Galán P, Roue G, Villamor N, Campo E, Colomer D. The BH3-mimetic GX15-070 synergizes with bortezomib in mantle cell lymphoma by enhancing Noxa-mediated activation of Bak. Blood. 2007;109:4441-4449.
49. Beg AA, Baltimore D. An essential role for NF-kappaB in preventing TNF-alpha-induced cell death. Science. 1996;274:782-784.
50. Pérez-Galán P, Roue G, Villamor N, Montserrat E, Campo E, Colomer D. The proteasome inhibitor bortezomib induces apoptosis in mantle-cell lymphoma through generation of ROS and Noxa activation independent of p53 status. Blood. 2006;107:257-264.