Molecular pathways: Leveraging the BCL-2 interactome to kill cancer cells-mitochondrial outer membrane permeabilization and beyond

Clinical Cancer Research

Volumn 21, Issue 12, 2015, Pages 2671-2676

  Brahmbhatt, Hetal ^a,b   Oppermann, Sina ^b   Osterlund, Elizabeth J ^b,c   Leber, Brian ^a   Andrews, David W ^a,b,c  

^a MCMASTER UNIVERSITY   (Canada)

^b UNIVERSITY OF TORONTO   (Canada)

^c UNIVERSITY OF TORONTO   (Canada)

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; ANTISENSE OLIGONUCLEOTIDE; BECLIN 1; BIM PROTEIN; GOSSYPOL; MESSENGER RNA; NAVITOCLAX; OBATOCLAX; OBLIMERSEN; PROTEIN BAD; PROTEIN BAK; PROTEIN BAX; PROTEIN BCL 2; PROTEIN BCL XL; PROTEIN BID; PROTEIN IRE1; PROTEIN MCL 1; PROTEIN NOXA; PUMA PROTEIN; RAPAMYCIN; ROSCOVITINE; SORAFENIB; VENETOCLAX; CARRIER PROTEIN; PROTEIN BINDING;

ACUTE LYMPHOBLASTIC LEUKEMIA; APOPTOSIS; ARTICLE; AUTOPHAGY; BINDING AFFINITY; CANCER CELL LINE; CANCER CHEMOTHERAPY; CELL KILLING; CELL PROLIFERATION; CELL SPECIFICITY; CELL STRESS; CELL SURVIVAL; CELLULAR DISTRIBUTION; CHRONIC LYMPHATIC LEUKEMIA; CYTOTOXICITY; DOWN REGULATION; DRUG EFFICACY; DRUG POTENTIATION; DRUG RECEPTOR BINDING; DRUG SELECTIVITY; ENDOPLASMIC RETICULUM; ENZYME ACTIVATION; ENZYME INHIBITION; FEASIBILITY STUDY; FLUORESCENCE MICROSCOPY; FLUORESCENCE RESONANCE ENERGY TRANSFER; FLUORESCENT LIFETIME IMAGING MICROSCOPY; FORSTER RESONANCE ENERGY TRANSFER; HIGH THROUGHPUT SCREENING; HUMAN; HYDROPHOBICITY; IMAGE ANALYSIS; IN VITRO STUDY; IN VIVO STUDY; MELANOMA; MEMBRANE PERMEABILITY; MITOCHONDRIAL OUTER MEMBRANE PERMEABILIZATION; MITOCHONDRION; MOLECULARLY TARGETED THERAPY; MULTIPLE MYELOMA; NONHODGKIN LYMPHOMA; PHASE 1 CLINICAL TRIAL (TOPIC); PHASE 2 CLINICAL TRIAL (TOPIC); PHASE 3 CLINICAL TRIAL (TOPIC); PRESCRIPTION; PRIORITY JOURNAL; PROTEIN BINDING; PROTEIN DEGRADATION; PROTEIN EXPRESSION; PROTEIN PROTEIN INTERACTION; PROTEIN SYNTHESIS; QUANTITATIVE ANALYSIS; SIGNAL TRANSDUCTION; SMALL CELL LUNG CANCER; STEM CELL RESEARCH; UNFOLDED PROTEIN RESPONSE; ANIMAL; CELL MEMBRANE; CELL MEMBRANE PERMEABILITY; METABOLISM; MITOCHONDRIAL MEMBRANE; NEOPLASMS; TRANSLATIONAL RESEARCH;

ANIMALS; CARRIER PROTEINS; CELL MEMBRANE; CELL MEMBRANE PERMEABILITY; HUMANS; MITOCHONDRIA; MITOCHONDRIAL MEMBRANES; NEOPLASMS; PROTEIN BINDING; PROTO-ONCOGENE PROTEINS C-BCL-2; SIGNAL TRANSDUCTION; TRANSLATIONAL MEDICAL RESEARCH;

EID: 84942134819     PISSN: 10780432     EISSN: 15573265     Source Type: Journal    
DOI: 10.1158/1078-0432.CCR-14-0959     Document Type: Article

References (60)

1. Hanahan D, Weinberg RA. The hallmarks of cancer. Cell 2000;100:57-70.
2. Kontos CK, Christodoulou MI, Scorilas A. Apoptosis-related BCL2-family members: key players in chemotherapy. Anticancer Agents Med Chem 2014;14:353-74.
3. Youle RJ, Strasser A. The BCL-2 protein family: opposing activities that mediate cell death. Nat Rev Mol Cell Biol 2008;9:47-59.
4. Leber B, Lin J, Andrews DW. Embedded together: the life and death consequences of interaction of the Bcl-2 family with membranes. Apopto-sis 2007;12:897-911.
5. Annis MG, Soucie EL, Dlugosz PJ, Cruz-Aguado JA, Penn LZ, Leber B, et al. BAX forms multispanning monomers that oligomerize to permeabilize membranes during apoptosis. EMBO J 2005;24:2096-103.
6. Dewson G, Kratina T, Sim HW, Puthalakath H, Adams JM, Colman PM, et al.Totrigger apoptosis, Bak exposes its BH3 domain and homodimerizes via BH3:groove interactions. Mol Cell 2008;30:369-80.
7. Willis SN, Chen L, Dewson G, Wei A, Naik E, Fletcher JI, et al. Proapoptotic Bak is sequestered by Mcl-1 and Bcl-xL, but not Bcl-2, until displaced by BH3-only proteins. Genes Dev 2005;19:1294-305.
8. Billen LP, Kokoski CL, Lovell JF, Leber B, Andrews DW. Bcl-XL inhibits membrane permeabilization by competing with BAX. PLoS Biol 2008; 6:e147.
9. Llambi F, Moldoveanu T, Tait SW, Bouchier-Hayes L, Temirov J, McCor-mick LL, et al. A unified model of mammalian BCL-2 protein family interactions at the mitochondria. Mol Cell 2011;44:517-31.
10. 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; 12:171-85.
11. Yamamoto H, Sawai H, Perucho M. Frameshift somatic mutations in gastrointestinal cancer of the microsatellite mutator phenotype. Cancer Res 1997;57:4420-6.
12. Beroukhim R, Mermel CH, Porter D, Wei G, Raychaudhuri S, Donovan J, et al. The landscape of somatic copy-number alteration across human cancers. Nature 2010;463:899-905.
13. Minn AJ, Rudin CM, Boise LH, Thompson CB. Expression of bcl-xL can confer a multidrug resistance phenotype. Blood 1995;86:1903-10.
14. Certo M, Del Gaizo Moore V, Nishino M, Wei G, Korsmeyer S, Armstrong SA, et al. Mitochondria primed by death signals determine cellular addiction to antiapoptotic BCL-2 family members. Cancer Cell 2006;9:351-65.
15. Gleave ME, Monia BP. Antisense therapy for cancer. Nat Rev Cancer 2005;5:468-79.
16. Petros AM, Olejniczak ET, Fesik SW. Structural biology of the Bcl-2 family of proteins. Biochim Biophys Acta 2004;1644:83-94.
17. Davids MS, Letai A. Targeting the B-cell lymphoma/leukemia 2 family in cancer. J Clin Oncol 2012;30:3127-35.
18. Billard C. BH3 mimetics: status of the field and new developments. Mol Cancer Ther 2013;12:1691-700.
19. Vogler M, Weber K, Dinsdale D, Schmitz I, Schulze-Osthoff K, Dyer MJ, et al. Different forms of cell death induced by putative BCL2 inhibitors. Cell Death Differ 2009;16:1030-9.
20. 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.
21. 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.
22. Ackler S, Mitten MJ, Chen J, Clarin J, Foster K, Jin S, et al. Navitoclax (ABT-263) and bendamustine +/-rituximab induce enhanced killing of non-Hodgkin's lymphoma tumours in vivo. Br J Pharmacol 2012; 167:881-91.
23. Lam LT, Zhang H, Chyla B. Biomarkers of therapeutic response to BCL2 antagonists in cancer. Mol Diagn Ther 2012;16:347-56.
24. Wilson WH, O'Connor OA, Czuczman MS, LaCasce 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.
25. 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.
26. BCL-2 inhibitor yields high response in CLL and SLL. Cancer Discov 2014;4:OF5.
27. Liu Q, Leber B, Andrews DW. Interactions of pro-apoptotic BH3 proteins with anti-apoptotic Bcl-2 family proteins measured in live MCF-7 cells using FLIM FRET. Cell Cycle 2012;11:3536-42.
28. van Delft MF, Wei AH, Mason KD, Vandenberg CJ, Chen L, Czabotar PE, 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;10:389-99.
29. Wuilleme-Toumi S, Robillard N, Gomez P, Moreau P, Le Gouill S, Avet-Loiseau H, et al. Mcl-1 is overexpressed in multiple myeloma and associated with relapse and shorter survival. Leukemia 2005;19:1248-52.
30. Belmar J, Fesik SW. Small molecule Mcl-1 inhibitors for the treatment of cancer. Pharmacol Ther 2015;145C:76-84.
31. Friberg A, Vigil D, Zhao B, Daniels RN, Burke JP, Garcia-Barrantes PM, et al. Discovery of potent myeloid cell leukemia 1 (Mcl-1) inhibitors using fragment-based methods and structure-based design. J Med Chem 2013; 56:15-30.
32. Zhong Q, Gao W, Du F, Wang X. Mule/ARF-BP1, a BH3-only E3 ubiquitin ligase, catalyzes the polyubiquitination of Mcl-1 and regulates apoptosis. Cell 2005;121:1085-95.
33. Rahmani M, Davis EM, Bauer C, Dent P, Grant S. Apoptosis induced by the kinase inhibitor BAY 43-9006 in human leukemia cells involves down-regulation of Mcl-1 through inhibition of translation. J Biol Chem 2005; 280:35217-27.
34. Lacrima K, Valentini A, Lambertini C, Taborelli M, Rinaldi A, Zucca E, et al. In vitro activity of cyclin-dependent kinase inhibitor CYC202 (Seliciclib, R-roscovitine) in mantle cell lymphomas. Ann Oncol 2005; 16:1169-76.
35. Gavathiotis E, Suzuki M, Davis ML, Pitter K, Bird GH, Katz SG, et al. BAX activation is initiated at anovel interaction site. Nature2008;455:1076-81.
36. Gavathiotis E, Reyna DE, Bellairs JA, Leshchiner ES, Walensky LD. Direct and selective small-molecule activation of proapoptotic BAX. Nat Chem Biol 2012;8:639-45.
37. Xin M, Li R, Xie M, Park D, Owonikoko TK, Sica GL, et al. Small-molecule BAX agonists for cancer therapy. Nat Commun 2014;5:4935.
38. Wang M, Kaufman RJ. The impact of the endoplasmic reticulum protein-folding environment on cancer development. Nat Rev Cancer 2014;14: 581-97.
39. Mathai JP, Germain M, Shore GC. BH3-only BIK regulates BAX, BAK-dependent release of Ca2+ from endoplasmic reticulum stores and mito-chondrial apoptosis during stress-induced cell death. J Biol Chem 2005; 280:23829-36.
40. Chang NC, Nguyen M, Germain M, Shore GC. Antagonism of Beclin 1-dependent autophagy by BCL-2 at the endoplasmic reticulum requires NAF-1. EMBO J 2010;29:606-18.
41. Toton E, Lisiak N, Sawicka P, Rybczynska M. Beclin-1 and its role as a target for anticancer therapy. J Physiol Pharmacol 2014;65:459-67.
42. Vaillant F, Merino D, Lee L, Breslin K, Pal B, Ritchie ME, et al. Targeting BCL-2 with the BH3 mimetic ABT-199 in estrogen receptor-positive breast cancer. Cancer Cell 2013;24:120-9.
43. Rong YP, Bultynck G, Aromolaran AS, Zhong F, Parys JB, DeSmedt H, et al. The BH4 domain of Bcl-2 inhibits ER calcium release and apoptosis by binding the regulatory and coupling domain of the IP3 receptor. Proc Natl Acad Sci U S A 2009;106:14397-402.
44. Kumar S, Alibhai D, Margineanu A, Laine R, Kennedy G, McGinty J, et al. FLIM FRET technologyfor drugdiscovery: automatedmultiwell-plate highcontent analysis, multiplexed readouts and application in situ. Chem-physchem 2011;12:609-26.
45. Crystal AS, Shaw AT, Sequist LV, Friboulet L, Niederst MJ, Lockerman EL, et al. Patient-derived models of acquired resistance can identify effective drug combinations for cancer. Science 2014;346:1480-6.
46. Shen M, Zhang Y, Saba N, Austin CP, Wiestner A, Auld DS. Identification of therapeutic candidates for chronic lymphocytic leukemia from a library of approved drugs. PLoS ONE 2013;8:e75252.
47. Mhaidat NM, Zhang XD, Jiang CC, Hersey P. Docetaxel-induced apo-ptosis of human melanoma is mediated by activation of c-Jun NH2-terminal kinase and inhibited by the mitogen-activated protein kinase extracellular signal-regulated kinase 1/2 pathway. Clin Cancer Res 2007; 13:1308-14.
48. Kutuk O, Arisan ED, Tezil T, Shoshan MC, Basaga H. Cisplatin overcomes Bcl-2-mediated resistance to apoptosis via preferential engagement of Bak: critical role of Noxa-mediated lipid peroxidation. Carcinogenesis 2009; 30:1517-27.
49. Jiang M, Wei Q, Wang J, Du Q, Yu J, Zhang L, et al. Regulation of PUMAalpha by p53 in cisplatin-induced renal cell apoptosis. Oncogene 2006; 25:4056-66.
50. Floros KV, Talieri M, Scorilas A. Topotecan and methotrexate alter expression of the apoptosis-related genes BCL2, FAS and BCL2L12 in leukemic HL-60 cells. Biol Chem 2006;387:1629-33.
51. Sawada M, Nakashima S, Banno Y, Yamakawa H, Hayashi K, Takenaka K, et al. Ordering of ceramide formation, caspase activation, and BAX/Bcl-2 expression during etoposide-induced apoptosis in C6 glioma cells. Cell Death Differ 2000;7:761-72.
52. Malugin A, Kopeckova P, Kopecek J. HPMA copolymer-bound doxorubicin induces apoptosis in ovarian carcinoma cells by the disruption of mito-chondrial function. Mol Pharm 2006;3:351-61.
53. Cheng H, Hong B, Zhou L, Allen JE, Tai G, Humphreys R, et al. Mitomycin C potentiates TRAIL-induced apoptosis through p53-independent upregula-tion of death receptors: evidence for the role of c-Jun N-terminal kinase activation. Cell Cycle 2012;11:3312-23.
54. Hou Y, Wang HQ, Ba Y. Effects of CDC7 gene silencing and Rituximab on apoptosis in diffuse large B cell lymphoma cells. J Cancer Res Clin Oncol 2012;138:2027-34.
55. Lopez-Fauqued M, Gil R, Grueso J, Hernandez-Losa J, Pujol A, Moline T, et al. The dual PI3K/mTOR inhibitor PI-103 promotes immunosuppres-sion, in vivo tumor growth and increases survival of sorafenib-treated melanoma cells. Int J Cancer 2010;126:1549-61.
56. Galmiche A, Ezzoukhry Z, Francois C, Louandre C, Sabbagh C, Nguyen-Khac E, et al. BAD, a proapoptotic member of the BCL2 family, is a potential therapeutic target in hepatocellular carcinoma. Mol Cancer Res 2010;8: 1116-25.
57. Fennell DA, Chacko A, Mutti L. BCL-2 family regulation by the 20S proteasome inhibitor bortezomib. Oncogene 2008;27:1189-97.
58. Oblimersen: Augmerosen, BCL-2 antisense oligonucleotide-Genta, G 3139, GC 3139, oblimersen sodium. Drugs R D 2007;8:321-34.
59. Zhai D, Jin C, Satterthwait AC, Reed JC. Comparison of chemical inhibitors of antiapoptotic Bcl-2-family proteins. Cell Death Differ 2006;13:1419-21.
60. 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.