Shooting at survivors: Bcl-2 family members as drug targets for cancer

Biochimica et Biophysica Acta - Molecular Cell Research

Volumn 1644, Issue 2-3, 2004, Pages 251-260

  Juin, Philippe ^a   Geneste, Olivier ^b   Raimbaud, Eric ^b   Hickman, John A ^b  

^a UNIVERSITÉ DE NANTES   (France)

^b INSTITUT DE RECHERCHES INTERNATIONALES SERVIER   (France)

Author keywords

Bcl 2; Cancer; Target

Indexed keywords

PEPTIDE; PROTEIN BAX; PROTEIN BCL 2; PROTEIN BCL XL; RECOMBINANT PROTEIN;

APOPTOSIS; CANCER; CANCER SURVIVAL; CELL DEATH; CELL PROLIFERATION; DEREGULATION; DRUG TARGETING; ECONOMIC ASPECT; ENDOPLASMIC RETICULUM; GENE DELIVERY SYSTEM; GENE THERAPY; HUMAN; NONHUMAN; ONCOGENE C MYC; PATHOGENESIS; PHENOTYPE; PRIORITY JOURNAL; REVIEW; TUMOR GROWTH;

ANIMALS; APOPTOSIS; CELL DIVISION; HUMANS; MICE; NEOPLASMS; PROTO-ONCOGENE PROTEINS C-BCL-2;

EID: 1442335327     PISSN: 01674889     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.bbamcr.2003.10.010     Document Type: Review

References (82)

1. Abdel-Rahman W.M., Katsura K., Rens W., Gorman P.A., Sheer D., Bicknell D., Bodmer W.F., Arends M.J., Wyllie A.H., Edwards P.A. Spectral karyotyping suggests additional subsets of colorectal cancers characterized by pattern of chromosome rearrangement. Proc. Natl. Acad. Sci. U. S. A. 98:2001;2538-2543.
2. Boland C.R., Ricciardiello L. How many mutations does it take to make a tumor? Proc. Natl. Acad. Sci. U. S. A. 96:1999;14675-14677.
3. Stoler D.L., Chen N., Basik M., Kahlenberg M.S., Rodriguez-Bigas M.A., Petrelli N.J., Anderson G.R. The onset and extent of genomic instability in sporadic colorectal tumor progression. Proc. Natl. Acad. Sci. U. S. A. 96:1999;15121-15126.
4. Loeb L.A., Loeb K.R., Anderson J.P. Multiple mutations and cancer. Proc. Natl. Acad. Sci. U. S. A. 100:2003;776-781.
5. Lazebnik Y. Can a biologist fix a radio? - Or, what I learned while studying apoptosis. Cancer Cells. 2:2002;179-182.
6. Evan G.I., Vousden K.H. Proliferation, cell cycle and apoptosis in cancer. Nature. 411:2001;342-348.
7. Gatenby R.A., Maini P.K. Mathematical oncology: cancer summed up. Nature. 421:2003;321.
8. Reddy A., Kaelin W.G. Jr. Using cancer genetics to guide the selection of anticancer drug targets. Curr. Opin. Pharmacol. 4:2002;366-373.
9. Renan M.J. How many mutations are required for tumorigenesis? Implications from human cancer data. Mol. Carcinog. 7:1993;139-146.
10. Marx J. Debate surges over the origins of genomic defects in cancer. Science. 297:2002;544-546.
11. Pelengaris S., Khan M., Evan G.I. Suppression of Myc-induced apoptosis in beta cells exposes multiple oncogenic properties of Myc and triggers carcinogenic progression. Cell. 109:2002;321-334.
12. Hickman J.A. Apoptosis and tumourogenesis. Curr. Opin. Genet. Dev. 12:2002;67-72.
13. Chin L., DePinho R.A. Flipping the oncogene switch: illumination of tumor maintenance and regression. Trends Genet. 16:2000;147-150.
14. Evan G.I., Littlewood T. A matter of life and cell death. Science. 281:1998;1317-1322.
15. Hanahan D., Weinberg R.A. The hallmarks of cancer. Cell. 100:2000;57-70.
16. Dive C., Hickman J.A. Drug-target interactions: only the first step in the ommitment to a programmed cell death? Br. J. Cancer. 64:1991;192-196.
17. Schmitt C.A., Lowe S.W. Apoptosis and therapy. J. Pathol. 187:1999;127-137.
18. Adams J.M., Cory S. The Bcl-2 protein family: arbiters of cell survival. Science. 281:1998;1322-1326.
19. Kuwana T., Mackey M.R., Perkins G., Ellisman M.H., Latterich M., Schneiter R., Green D.R., Newmeyer D.D. Bid, Bax, and lipids cooperate to form supramolecular openings in the outer mitochondrial membrane. Cell. 111:2002;331-342.
20. Martinou J.C., Desagher S., Antonsson B. Cytochrome c release from mitochondria: all or nothing. Nat. Cell Biol. 2:2000;E41-E43.
21. Scorrano L., Oakes S.A., Opferman J.T., Cheng E.H., Sorcinelli M.D., Pozzan T., Korsmeyer S.J. BAX and BAK regulation of endoplasmic reticulum Ca2+: a control point for apoptosis. Science. 300:2003;135-139.
22. Oltvai Z., Milliman C., Korsmeyer S. Bcl-2 heterodimerizes in vivo with a conserved homolog, Bax, that accelerates programed cell death. Cell. 74:1993;609-619.
23. Oakes S.A., Opferman J.T., Pozzan T., Korsmeyer S., Scorrano L. Regulation of endoplasmic reticulum Ca(2+) dynamics by proapoptotic BCL-2 family members. Biochem. Pharmacol. 66:2003;1335-1340.
24. Degterev A., Boyce M., Yuan J. The channel of death. J. Cell Biol. 155:2001;695-698.
25. Kelekar A., Thompson C. Bcl-2 family proteins: the role of the BH3 domain in apoptosis. Trends Cell Biol. 8:1998;324-330.
26. Wei M.C., Zong W.X., Cheng E.H., Lindsten T., Panoutsakopoulou V., Ross A.J., Roth K.A., MacGregor G.R., Thompson C.B., Korsmeyer S.J. Proapoptotic BAX and BAK: a requisite gateway to mitochondrial dysfunction and death. Science. 292:2001;727-730.
27. Zong W.X., Lindsten T., Ross A.J., MacGregor G.R., Thompson C.B. BH3-only proteins that bind pro-survival Bcl-2 family members fail to induce apoptosis in the absence of Bax and Bak. Genes Dev. 15:2001;1481-1486.
28. Cheng E.H., Wei M.C., Weiler S., Flavell R.A., Mak T.W., Lindsten T., Korsmeyer S.J. BCL-2, BCL-X(L) sequester BH3 domain-only molecules preventing BAX- and BAK-mediated mitochondrial apoptosis. Mol. Cell. 8:2001;705-711.
29. Rampino N., Yamamoto H., Ionov Y., Li Y., Sawai H., Reed J.C., Perucho M. Somatic frameshift mutations in the BAX gene in colon cancers of the microsatellite mutator phenotype. Science. 275:1997;967-969.
30. Meijerink J.P., Mensink E.J., Wang K., Sedlak T.W., Sloetjes A.W., de Witte T., Waksman G., Korsmeyer S.J. Hematopoietic malignancies demonstrate loss-of-function mutations of BAX. Blood. 91:1998;2991-2997.
31. Cartron P.F., Oliver L., Martin S., Moreau C., LeCabellec M.T., Jezequel P., Meflah K., Vallette F.M. The expression of a new variant of the pro-apoptotic molecule Bax, Baxpsi, is correlated with an increased survival of glioblastoma multiforme patients. Hum. Mol. Genet. 11:2002;675-687.
32. Juin P., Hueber A.O., Littlewood T., Evan G. c-Myc-induced sensitization to apoptosis is mediated through cytochrome c release. Genes Dev. 13:1999;1367-1381.
33. Soucie E.L., Annis M.G., Sedivy J., Filmus J., Leber B., Andrews D.W., Penn L.Z. Myc potentiates apoptosis by stimulating Bax activity at the mitochondria. Mol. Cell. Biol. 21:2001;4725-4736.
34. Eischen C.M., Woo D., Roussel M.F., Cleveland J.L. Apoptosis triggered by Myc-induced suppression of Bcl-X(L) or Bcl-2 is bypassed during lymphomagenesis. Mol. Cell. Biol. 21:2001;5063-5070.
35. Fulda S., Wick W., Weller M., Debatin K.M. Smac agonists sensitize for Apo2L/TRAIL-or anticancer drug-induced apoptosis and induce regression of malignant glioma in vivo. Nat. Med. 8:2002;808-815.
36. Kagawa S., Pearson S.A., Ji L., Xu K., McDonnell T.J., Swisher S.G., Roth J.A., Fang B. A binary adenoviral vector system for expressing high levels of the proapoptotic gene bax. Gene Ther. 7:2000;75-79.
37. Tsuruta Y., Mandai M., Konishi I., Kuroda H., Kusakari T., Yura Y., Hamid A.A., Tamura I., Kariya M., Fujii S. Combination effect of adenovirus-mediated pro-apoptotic bax gene transfer with cisplatin or paclitaxel treatment in ovarian cancer cell lines. Eur. J. Cancer. 37:2001;531-541.
38. Gu J., Kagawa S., Takakura M., Kyo S., Inoue M., Roth J.A., Fang B. Tumor-specific transgene expression from the human telomerase reverse transcriptase promoter enables targeting of the therapeutic effects of the Bax gene to cancers. Cancer Res. 60:2000;5359-5364.
39. Jansen B., Zangemeister-Wittke U. Antisense therapy for cancer-the time of truth. Lancet Oncol. 3:2002;672-683.
40. Derenne S., Monia B., Dean N.M., Taylor J.K., Rapp M.J., Harousseau J.L., Bataille R., Amiot M. Antisense strategy shows that Mcl-1 rather than Bcl-2 or Bcl-x(L) is an essential survival protein of human myeloma cells. Blood. 100:2002;194-199.
41. Taylor J.K., Zhang Q.Q., Wyatt J.R., Dean N.M. Induction of endogenous Bcl-xS through the control of Bcl-x pre-mRNA splicing by antisense oligonucleotides. Nat. Biotechnol. 17:1999;1097-1100.
42. Zangemeister-Wittke U., Leech S.H., Olie R.A., Simoes-Wust A.P., Gautschi O., Luedke G.H., Natt F., Haner R., Martin P., Hall J.et al. A novel bispecific antisense oligonucleotide inhibiting both bcl-2 and bcl-xL expression efficiently induces apoptosis in tumor cells. Clin. Cancer Res. 6:2000;2547-2555.
43. Huang D.C., O'Reilly L.A., Strasser A., Cory S. The anti-apoptosis function of Bcl-2 can be genetically separated from its inhibitory effect on cell cycle entry. EMBO J. 16:1997;4628-4638.
44. Janumyan Y.M., Sansam C.G., Chattopadhyay A., Cheng N., Soucie E.L., Penn L.Z., Andrews D., Knudson C.M., Yang E. Bcl-x(L)/Bcl-2 coordinately regulates apoptosis, cell cycle arrest and cell cycle entry. EMBO J. 22:2003;5459-5470.
45. Konopleva M., Tari A.M., Estrov Z., Harris D., Xie Z., Zhao S., Lopez-Berestein G., Andreeff M. Liposomal Bcl-2 antisense oligonucleotides enhance proliferation, sensitize acute myeloid leukemia to cytosine-arabinoside, and induce apoptosis independent of other antiapoptotic proteins. Blood. 97:2000;578-579.
46. Gutierrez-Puente Y., Zapata-Benavides P., Tari A.M., Lopez-Berestein G. Bcl-2-related antisense therapy. Semin. Oncol. 3:2002;71-76.
47. Sattler M., Liang H., Nettesheim D., Meadows R.P., Harlan J.E., Eberstadt M., Yoon H.S., Shuker S.B., Chang B.S., Minn A.J.et al. Structure of Bcl-xL-Bak peptide complex: recognition between regulators of apoptosis. Science. 275:1997;983-986.
48. Petros A.M., Medek A., Nettesheim D.G., Kim D.H., Yoon H.S., Swift K., Matayoshi E.D., Oltersdorf T., Fesik S.W. Solution structure of the antiapoptotic protein bcl-2. Proc. Natl. Acad. Sci. U. S. A. 98:2001;3012-3017.
49. Wang J.L., Zhang Z.J., Choksi S., Shan S., Lu Z., Croce C.M., Alnemri E.S., Korngold R., Huang Z. Cell permeable Bcl-2 binding peptides: a chemical approach to apoptosis induction in tumor cells. Cancer Res. 60:2000;1498-1502.
50. Holinger E.P., Chittenden T., Lutz R.J. Bak BH3 peptides antagonize Bcl-xL function and induce apoptosis through cytochrome c-independent activation of caspases. J. Biol. Chem. 274:1999;13298-13304.
51. Juin P., Hunt A., Littlewood T., Griffiths B., Brown L., Korsmeyer S., Evan G. c-Myc functionnally cooperates with Bax to induce apoptosis. Mol. Cell. Biol. 22:2002;6158-6169.
52. Finnegan N.M., Curtin J.F., Prevost G., Morgan B., Cotter T.G. Induction of apoptosis in prostate carcinoma cells by BH3 peptides which inhibit Bak/ Bcl-2 interactions. Br. J. Cancer. 85:2001;115-121.
53. Jiang M., Milner J. Bcl-2 constitutively suppresses p53-dependent apoptosis in colorectal cancer cells. Genes Dev. 17(7):2003;832-837.
54. Baell J.B., Huang D.C.S. Prospects for targeting Bcl-2 family of proteins to develop novel cytotoxic drugs. Biochem. Pharmacol. 64:2002;851-863.
55. O'Neill J.W., Hockenbery D.M. Bcl-2-related proteins as drug targets. Curr. Med. Chem. 10:2003;1553-1562.
56. Rutledge S.E., Chin J.W., Schepartz A. A view to kill: ligands for Bcl-2 family proteins. Curr. Opin. Chem. Biol. 6:2003;479-485.
57. Wang J.L., Liu D., Zhang Z.J., Shan S., Han X., Srinivasula S.M., Croce C.M., Alnemri E.S., Huang Z. 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. 97:2000;7124-7129.
58. Enyedy I.J., Ling Y., Nacro K., Tomita Y., Wu X., Cao Y., Guo R., Li B., Zhu X., Huang Y.et al. Discovery of small-molecule inhibitors of Bcl-2 through structure-based computer screening. J. Med. Chem. 44:2001;4313-4324.
59. Lickliter J.D., Wood N.J., Johnson L., McHugh G., Tan J., Wood F., Cox J., Wickham N.W. HA14-1 selectively induces apoptosis in Bcl-2-overexpressing leukemia/lymphoma cells, and enhances cytarabine-induced cell death. Leukemia. 17:2003;2074-2080.
60. Chen J., Freeman A., Liu J., Dai Q., Lee R.M. The apoptotic effect of HA14-1, a Bcl-2-interacting small molecular compound, requires Bax translocation and is enhanced by PK11195. Mol. Cancer Ther. 12:2002;961-967.
61. Degterev A., Lugovskoy A., Cardone M., Mulley B., Wagner G., Mitchison T., Yuan J. Identification of small-molecule inhibitors of interaction between the BH3 domain and Bcl-xL. Nat. Cell Biol. 3:2001;173-182.
62. Lugovskoy A.A., Degterev A.I., Fahmy A.F., Zhou P., Gross J.D., Yuan J., Wagner G. A novel approach for characterizing protein ligand complexes: molecular basis for specificity of small-molecule Bcl-2 inhibitors. J. Am. Chem. Soc. 124:2002;1234-1240.
63. Kitada S., Leone M., Sareth S., Zhai D., Reed J.C., Pellecchia M. Discovery, characterization, and structure-activity relationships studies of proapoptotic polyphenols targeting B-cell lymphocyte/leukemia-2 proteins. J. Med. Chem. 46:2003;4259-4264.
64. Chan S.L., Lee M.C., Tan K.O., Yang L.K., Lee A.S., Flotow H., Fu N.Y., Butler M.S., Soejarto D.D., Buss A.D., Yu V.C. Identification of chelerythrine as an inhibitor of BclXL function. J. Biol. Chem. 278:2003;20453-20456.
65. Tzung S.P., Kim K.M., Basanez G., Giedt C.D., Simon J., Zimmerberg J., Zhang K.Y., Hockenbery D.M. Antimycin A mimics a cell-death-inducing Bcl-2 homology domain 3. Nat. Cell Biol. 3:2001;183-191.
66. Kim K.M., Giedt C.D., Basanez G., O'Neill J.W., Hill J.J., Han Y.H., Tzung S.P., Zimmerberg J., Hockenbery D.M., Zhang K.Y. Biophysical characterization of recombinant human Bcl-2 and its interactions with an inhibitory ligand, antimycin A. Biochemistry. 40:2001;4911-4922.
67. Kutzki O., Park H.S., Ernst J.T., Orner B.P., Yin H., Hamilton A.D. Development of a potent Bcl-x(L) antagonist based on alpha-helix mimicry. J. Am. Chem. Soc. 124:2002;11838-11839.
68. Wolter K.G., Hsu Y.T., Smith C.L., Nechushtan A., Xi X.G., Youle R.J. Movement of Bax from the cytosol to mitochondria during apoptosis. J. Cell Biol. 139:1997;1281-1292.
69. Letai A., Bassik M., Walensky L., Sorcinelli M., Weiler S., Korsmeyer S. Distinct BH3 domains either sensitize or activate mitochondrial apoptosis serving as prototype cancer therapeutics. Cancer Cells. 2:2002;183-192.
70. Degterev A., Lugovskoy A., Cardone M., Mulley B., Wagner G., Mitchison T., Yuan J. Identification of small-molecule inhibitors of interaction between the BH3 domain and Bcl-xL. Nat. Cell Biol. 3:2001;173-182.
71. Moreau C., Cartron P.F., Hunt A., Meflah K., Green D., Evan G., Vallette F.M., Juin P. BH3 peptides promote cell death by antagonizing anti-apoptotic Bcl-2 family members. J. Biol. Chem. 278:2003;19426-19435.
72. Cheng E.H., Kirsch D.G., Clem R.J., Ravi R., Kastan M.B., Bedi A., Ueno K., Hardwick J.M. Conversion of Bcl-2 to a Bax-like death effector by caspases. Science. 278:1997;1966-1968.
73. Clem R.J., Cheng E.H., Karp C.L., Kirsch D.G., Ueno K., Takahashi A., Kastan M.B., Griffin D.E., Earnshaw W.C., Veliuona M.A., Hardwick J.M. Modulation of cell death by Bcl-XL through caspase interaction. Proc. Natl. Acad. Sci. U. S. A. 95:1998;554-559.
74. Makin G.W., Corfe B.M., Griffiths G.J., Thistlethwaite A., Hickman J.A., Dive C. Damage-induced Bax N-terminal change, translocation to mitochondria and formation of Bax dimers/complexes occur regardless of cell fate. EMBO J. 20:2001;6306-6315.
75. Scorrano L., Korsmeyer S. Mechanisms of cytochrome c release by proapoptotic BCL-2 family members. Biochem. Biophys. Res. Commun. 304(3):2003;437-444.
76. Cartron P.F., Juin P., Oliver L., Martin S., Meflah K., Vallette F.M. A non-redundant role for Bax and Bak in Bid-mediated apoptosis. Mol. Cell. Biol. 23:2003;4701-4712.
77. Frank S., Gaume B., Bergmann-Leitner E.S., Leitner W.W., Robert E.G., Catez F., Smith C.L., Youle R.J. The role of dynamin-related protein 1, a mediator of mitochondrial fission, in apoptosis. Dev. Cell. 1:2001;515-525.
78. Lassus P., Opitz-Araya X., Lazebnik Y. Requirement for caspase-2 in stress-induced apoptosis before mitochondrial permeabilization. Science. 297:2002;1352-1354.
79. Marsden V.S., O'Connor L., O'Reilly L.A., Silke J., Metcalf D., Ekert P.G., Huang D.C., Cecconi F., Kuida K., Tomaselli K.J.et al. Apoptosis initiated by Bcl-2-regulated caspase activation independently of the cytochrome c/Apaf-1/caspase-9 apoptosome. Nature. 419:2002;634-637.
80. Chai J., Du C., Wu J.W., Kyin S., Wang X., Shi Y. Structural and biochemical basis of apoptotic activation by Smac/DIABLO. Nature. 406:2000;855-862.
81. Reed J.C. Bcl-2 family proteins. Oncogene. 17:1998;3225-3236.
82. Jonas E.A., Hoit D., Hickman J.A., Brandt T.A., Polster B.M., Fannjiang Y., McCarthy E., Montanez M.K., Hardwick J.M., Kaczmarek L.K. Modulation of synaptic transmission by the BCL-2 family protein BCL-xL. J. Neurosci. 23:2003;8423-8431.