Alterations in the Noxa/Mcl-1 axis determine sensitivity of small cell lung cancer to the BH3 mimetic ABT-737

Molecular Cancer Therapeutics

Volumn 8, Issue 4, 2009, Pages 883-892

  Hauck, Paula ^a   Chao, Bo H ^a   Litz, Julie ^a   Krystal, Geoffrey W ^a,b  

^a VIRGINIA COMMONWEALTH UNIVERSITY SCHOOL OF MEDICINE   (United States)

^b VETERANS AFFAIRS MEDICAL CENTER   (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; BIM PROTEIN; PROTEIN BCL 2; PROTEIN MCL 1; PROTEIN NOXA; SMALL INTERFERING RNA; ABT-737; APOPTOSIS REGULATORY PROTEIN; BAX PROTEIN (53 86); BAX PROTEIN (53-86); BCL 2 LIKE PROTEIN 11; BCL-2-LIKE PROTEIN 11; BIPHENYL DERIVATIVE; MEMBRANE PROTEIN; MESSENGER RNA; MYELOID CELL LEUKEMIA SEQUENCE 1 PROTEIN; NITROPHENOL; ONCOPROTEIN; PEPTIDE FRAGMENT; PIPERAZINE DERIVATIVE; PMAIP1 PROTEIN, HUMAN; SULFONAMIDE;

APOPTOSIS; ARTICLE; CANCER CELL CULTURE; CONTROLLED STUDY; DRUG SENSITIVITY; GENE EXPRESSION; GENE EXPRESSION REGULATION; GENE OVEREXPRESSION; HUMAN; HUMAN CELL; LUNG SMALL CELL CANCER; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN PROTEIN INTERACTION; PROTEIN SECRETION; RNA INTERFERENCE; CELL PROLIFERATION; DRUG ANTAGONISM; DRUG EFFECT; DRUG RESISTANCE; GENETICS; IMMUNOPRECIPITATION; LUNG TUMOR; METABOLISM; MOLECULAR MIMICRY; PATHOLOGY; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; TUMOR CELL CULTURE; WESTERN BLOTTING;

APOPTOSIS; APOPTOSIS REGULATORY PROTEINS; BIPHENYL COMPOUNDS; BLOTTING, WESTERN; CELL PROLIFERATION; DRUG RESISTANCE, NEOPLASM; HUMANS; IMMUNOPRECIPITATION; LUNG NEOPLASMS; MEMBRANE PROTEINS; MOLECULAR MIMICRY; NITROPHENOLS; PEPTIDE FRAGMENTS; PIPERAZINES; PROTO-ONCOGENE PROTEINS; PROTO-ONCOGENE PROTEINS C-BCL-2; REVERSE TRANSCRIPTASE POLYMERASE CHAIN REACTION; RNA, MESSENGER; RNA, SMALL INTERFERING; SMALL CELL LUNG CARCINOMA; SULFONAMIDES; TUMOR CELLS, CULTURED;

EID: 66449130084     PISSN: 15357163     EISSN: None     Source Type: Journal    
DOI: 10.1158/1535-7163.MCT-08-1118     Document Type: Article

References (41)

1. Jackman DM, Johnson BE. Small-cell lung cancer. Lancet 2005;366:1385-1396 (Pubitemid 41443406)
2. Wistuba II, Gazdar AF, Minna JD. Molecular genetics of small cell lung carcinoma. Semin Oncol 2001;28:3-13. (Pubitemid 32730372)
3. Meuwissen R, Linn SC, Linnoila RI, Zevenhoven J, Mooi WJ, Berns A. Induction of small cell lung cancer by somatic inactivation of both Trp53 and Rb1 in a conditional mouse model. Cancer Cell 2003;4:181-189 (Pubitemid 37163832)
4. Carraresi L, Martinelli R, Vannoni A, et al. Establishment and characterization of murine small cell lung carcinoma cell lines derived from HPV-16 E6/E7 transgenic mice. Cancer Lett 2006;231:65-73. (Pubitemid 41779454)
5. Calbó J, Meuwissen R, van Montfort E, van Tellingen O, Berns A. Genotype-phenotype relationships in a mouse model for human small-cell lung cancer. Cold Spring Harb Symp Quant Biol 2005;70:225-232 (Pubitemid 44124876)
6. Johnson BE, Ihde D, Makuch R, et al. myc family oncogene amplification in tumor cell lines established from small cell lung cancer patients and its relationship to clinical status and course. J Clin Invest 1987;79:1629-1634 (Pubitemid 17117266)
7. Takahashi T, Obata Y, Sekido Y, et al. Expression and amplification of myc gene family in small cell lung cancer and its relation to biological characteristics. Cancer Res 1989;49:2683-2688 (Pubitemid 19143399)
8. Packham G, Cleveland JL. c-Myc and apoptosis. Biochim Biophys Acta 1995;1242:11-28.
9. Krystal GW, Sulanke G, Litz J. Inhibition of phosphatidylinositol 3-kinase-Akt signaling blocks growth, promotes apoptosis, and enhances sensitivity of small cell lung cancer cells to chemotherapy. Mol Cancer Ther 2002;1:913-922
10. Ma PC, Tretiakova MS, Nallasura V, Jagadeeswaran R, Husain AN, Salgia R. Downstream signalling and specific inhibition of c-MET/HGF pathway in small cell lung cancer: implications for tumour invasion. Br J Cancer 2007;97:368-377 (Pubitemid 47196754)
11. Forgacs E, Biesterveld EJ, Sekido Y, et al. Mutation analysis of the PTEN/MMAC1 gene in lung cancer. Oncogene 1998;17:1557-1565 (Pubitemid 28472760)
12. Okudela K, Suzuki M, Kageyama S, et al. PIK3CA mutation and amplification in human lung cancer. Pathol Int 2007;57:664-671 (Pubitemid 47353042)
13. Ben-Ezra J, Kornstein M, Grimes M, Krystal G. Small cell carcinomas of the lung express the Bcl-2 protein. Am J Pathol 1994;145:1036-1040 (Pubitemid 24345651)
14. van Delft MF, Huang DC. How the Bcl-2 family of proteins interact to regulate apoptosis. Cell Res 2006;16:203-213 (Pubitemid 43247978)
15. Adams JM, Cory S. The Bcl-2 apoptotic switch in cancer development and therapy. Oncogene 2007;26:1324-1337 (Pubitemid 46328466)
16. Letai AG. Diagnosing and exploiting cancer's addiction to blocks in apoptosis. Nat Rev Cancer 2008;8:121-132
17. Willis SN, Adams JM. Life in the balance: how BH3-only proteins induce apoptosis. Curr Opin Cell Biol 2005;17:617-625 (Pubitemid 41540411)
18. Oltersdorf T, Elmore SW, Shoemaker AR, et al. An inhibitor of Bcl-2 family proteins induces regression of solid tumours. Nature 2005;435:677-681 (Pubitemid 40825512)
19. Tahir SK, Yang X, Anderson MG, et al. Influence of Bcl-2 family members on the cellular response of small-cell lung cancer cell lines to ABT-737. Cancer Res 2007;67:1176-1183 (Pubitemid 46270776)
20. Lin X, Morgan-Lappe S, Huang X, et al. 'Seed' analysis of off-target siRNAs reveals an essential role of Mcl-1 in resistance to the small-molecule Bcl-2/Bcl-XL inhibitor ABT-737. Oncogene 2007;26:3972-3979
21. Hann CL, Daniel VC, Sugar EA, et al. Therapeutic efficacy of ABT-737, a selective inhibitor of BCL-2, in small cell lung cancer. Cancer Res 2008;68:2321-2328
22. 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 2006;10:375-388 (Pubitemid 44693472)
23. 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 (Pubitemid 44711953)
24. Olejniczak ET, Van Sant C, Anderson MG, et al. Integrative genomic analysis of small-cell lung carcinoma reveals correlates of sensitivity to bcl-2 antagonists and uncovers novel chromosomal gains. Mol Cancer Res 2007;5:331-339 (Pubitemid 46706995)
25. 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;12:171-185 (Pubitemid 47199122)
26. Wang S, Vrana JA, Bartimole TM, et al. Agents that down-regulate or inhibit protein kinase C circumvent resistance to 1-β-D- arabinofuranosylcytosine-induced apoptosis in human leukemia cells that overexpress Bcl-2. Mol Pharmacol 1997;52:1000-1009 (Pubitemid 28013718)
27. Carmichael J, DeGraff WG, Gazdar AF, Minna JD, Mitchell JB. Evaluation of a tetrazolium-based semiautomated colorimetric assay: assessment of chemosensitivity testing. Cancer Res 1987;47:936-942 (Pubitemid 17027905)
28. Czabotar PE, Lee EF, van Delft MF, et al. Structural insights into the degradation of Mcl-1 induced by BH3 domains. Proc Natl Acad Sci U S A 2007;104:6217-6222 (Pubitemid 47186075)
29. Willis SN, Chen L, Dewson G, 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;19:1294-1305 (Pubitemid 41003019)
30. Zangemeister-Wittke U, Schenker T, Luedke GH, Stahel RA. Synergistic cytotoxicity of bcl-2 antisense oligodeoxynucleotides and etoposide, doxorubicin and cisplatin on small-cell lung cancer cell lines. Br J Cancer 1998;78:1035-1042 (Pubitemid 28463979)
31. Sartorius UA, Krammer PH. Upregulation of Bcl-2 is involved in the mediation of chemotherapy resistance in human small cell lung cancer cell lines. Int J Cancer 2002;97:584-592 (Pubitemid 34087795)
32. Tse C, Shoemaker AR, Adickes J, et al. ABT-263: a potent and orally bioavailable Bcl-2 family inhibitor. Cancer Res 2008;68:3421-3428
33. Shoemaker AR, Mitten MJ, Adickes J, et al. Activity of the Bcl-2 family inhibitor ABT-263 in a panel of small cell lung cancer xenograft models. Clin Cancer Res 2008;14:3268-3277
34. Alves NL, Derks IA, Berk E, Spijker R, van Lier RA, Eldering E. The Noxa/Mcl-1 axis regulates susceptibility to apoptosis under glucose limitation in dividing T cells. Immunity 2006;24:703-716 (Pubitemid 43867360)
35. Gomez-Bougie P, Wuillème-Toumi S, Ménoret E, et al. Noxa up-regulation and Mcl-1 cleavage are associated to apoptosis induction by bortezomib in multiple myeloma. Cancer Res 2007;67:5418-5424 (Pubitemid 46997282)
36. Lee EF, Czabotar PE, van Delft MF, et al. A novel BH3 ligand that selectively targets Mcl-1 reveals that apoptosis can proceed without Mcl-1 degradation. J Cell Biol 2008;180:341-355
37. Gong Y, Somwar R, Politi K, et al. Induction of BIM is essential for apoptosis triggered by EGFR kinase inhibitors in mutant EGFR-dependent lung adenocarcinomas. PLoS Med 2007;4:e294. (Pubitemid 350035455)
38. Deng J, Shimamura T, Perera S, et al. Proapoptotic BH3-only BCL-2 family protein BIM connects death signaling from epidermal growth factor receptor inhibition to the mitochondrion. Cancer Res 2007;67:11867-11875
39. Cragg MS, Kuroda J, Puthalakath H, Huang DC, Strasser A. Gefitinib-induced killing of NSCLC cell lines expressing mutant EGFR requires BIM and can be enhanced by BH3 mimetics. PLoS Med 2007;4:1681-1689 (Pubitemid 350035457)
40. Chen S, Dai Y, Harada H, Dent P, Grant S. Mcl-1 down-regulation potentiates ABT-737 lethality by cooperatively inducing Bak activation and Bax translocation. Cancer Res 2007;67:782-791 (Pubitemid 46192219)
41. Morales AA, Gutman D, Lee KP, Boise LH. BH3-only proteins Noxa, Bmf, and Bim are necessary for arsenic trioxide-induced cell death in myeloma. Blood 2008;111:5152-5162