Resistance to HSP90 inhibition involving loss of MCL1 addiction

Oncogene

Volumn 35, Issue 12, 2016, Pages 1483-1492

  Busacca, S ^a   Law, E W P ^a   Powley, I R ^b   Proia, D A ^c   Sequeira, M ^c   Le Quesne, J ^a,b   Klabatsa, A ^d   Edwards, J M ^b   Matchett, K B ^e   Luo, J L ^a   Pringle, J H ^a   El Tanani, M ^f   MacFarlane, M ^b   Fennell, D A ^a  

^a UNIVERSITY OF LEICESTER   (United Kingdom)

^b MRC TOXICOLOGY UNIT   (United Kingdom)

^c Synta Pharmaceuticals Corp   (United States)

^d KING'S COLLEGE LONDON   (United Kingdom)

^e QUEEN'S UNIVERSITY BELFAST   (United Kingdom)

^f UNIVERSITY OF BRADFORD   (United Kingdom)

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; BIK PROTEIN; GANETESPIB; HEAT SHOCK PROTEIN 90; HEAT SHOCK PROTEIN 90 INHIBITOR; PROTEIN BCL 2; PROTEIN BID; PROTEIN MCL 1; PUMA PROTEIN; STAT5A PROTEIN; UNCLASSIFIED DRUG; MCL1 PROTEIN, HUMAN; PEPTIDOMIMETIC AGENT; STAT5 PROTEIN; STAT5A PROTEIN, HUMAN; TUMOR SUPPRESSOR PROTEIN;

ANIMAL CELL; ANIMAL MODEL; APOPTOSIS; ARTICLE; CANCER RESISTANCE; CELL SURVIVAL; CELL VIABILITY; CONTROLLED STUDY; FEMALE; GENE EXPRESSION; GENE LOSS; GENE REPRESSION; GROWTH INHIBITION; HUMAN; HUMAN CELL; IC50; IN VITRO STUDY; LETHALITY; MESOTHELIOMA; MOUSE; NONHUMAN; PHENOTYPE; PRIORITY JOURNAL; PROTEIN SYNTHESIS; TUMOR CELL LINE; TUMOR XENOGRAFT; ANTAGONISTS AND INHIBITORS; GENETICS;

CELL LINE, TUMOR; HSP90 HEAT-SHOCK PROTEINS; HUMANS; MYELOID CELL LEUKEMIA SEQUENCE 1 PROTEIN; PEPTIDOMIMETICS; STAT5 TRANSCRIPTION FACTOR; TUMOR SUPPRESSOR PROTEINS;

EID: 84932163545     PISSN: 09509232     EISSN: 14765594     Source Type: Journal    
DOI: 10.1038/onc.2015.213     Document Type: Article

References (51)

1. Trepel J, Mollapour M, Giaccone G, Neckers L. Targeting the dynamic HSP90 complex in cancer. Nat Rev Cancer 2010; 10: 537-549
2. Workman P, Al-Lazikani B. Drugging cancer genomes. Nat Rev Drug Discov 2013; 12: 889-890
3. Workman P, Al-Lazikani B, Clarke PA. Genome-based cancer therapeutics: targets, kinase drug resistance and future strategies for precision oncology. Curr Opin Pharmacol 2013; 13: 486-496
4. Moulick K, Ahn JH, Zong H, Rodina A, Cerchietti L, Gomes DaGama EM, et al. Affinity-based proteomics reveal cancer-specific networks coordinated by Hsp90. Nat Chem Biol 2011; 7: 818-826
5. Rutherford SL, Lindquist S. Hsp90 as a capacitor for morphological evolution. Nature 1998; 396: 336-342
6. Soda M, Choi YL, Enomoto M, Takada S, Yamashita Y, Ishikawa S, et al. Identification of the transforming EML4-ALK fusion gene in non-small-cell lung cancer. Nature 2007; 448: 561-566
7. Heuckmann JM, Balke-Want H, Malchers F, Peifer M, Sos ML, Koker M, et al. Differential protein stability and ALK inhibitor sensitivity of EML4-ALK fusion variants. Clin Cancer Res 2012; 18: 4682-4690
8. Richards MW, Law EW, Rennalls LP, Busacca S, O'Regan L, Fry AM, et al. Crystal structure of EML1 reveals the basis for Hsp90 dependence of oncogenic EML4-ALK by disruption of an atypical beta-propeller domain. Proc Natl Acad Sci USA 2014; 111: 5195-5200
9. Samant RS, Clarke PA, Workman P. E3 ubiquitin ligase Cullin-5 modulates multiple molecular and cellular responses to heat shock protein 90 inhibition in human cancer cells. Proc Natl Acad Sci USA 2014; 111: 6834-6839
10. McCollum AK, Teneyck CJ, Sauer BM, Toft DO, Erlichman C. Up-regulation of heat shock protein 27 induces resistance to 17-allylamino-demethoxygeldanamycin through a glutathione-mediated mechanism. Cancer Res 2006; 66: 10967-10975
11. Travers J, Sharp S, Workman P. HSP90 inhibition: two-pronged exploitation of cancer dependencies. Drug Discov Today 2012; 17: 242-252
12. Acquaviva J, He S, Zhang C, Jimenez JP, Nagai M, Sang J, et al. FGFR3 translocations in bladder cancer: differential sensitivity to HSP90 inhibition based on drug metabolism. Mol Cancer Res 2014; 12: 1042-1054
13. Landmann H, Proia DA, He S, Ogawa LS, Kramer F, Beissbarth T, et al. UDP glucuronosyltransferase 1 A expression levels determine the response of colorectal cancer cells to the heat shock protein 90 inhibitor ganetespib. Cell Death Dis 2014; 5: e1411
14. Garnett MJ, Edelman EJ, Heidorn SJ, Greenman CD, Dastur A, Lau KW, et al. Systematic identification of genomic markers of drug sensitivity in cancer cells. Nature 2012; 483: 570-575
15. Prodromou C, Nuttall JM, Millson SH, Roe SM, Sim TS, Tan D, et al. Structural basis of the radicicol resistance displayed by a fungal hsp90. ACS Chem Biol 2009; 4: 289-297
16. Altieri DC, Stein GS, Lian JB, Languino LR. TRAP-1 the mitochondrial Hsp90. Biochim Biophys Acta 2012; 1823: 767-773
17. Wei MC, Zong WX, Cheng EH, Lindsten T, Panoutsakopoulou V, Ross AJ, et al. Proapoptotic BAX and BAK: a requisite gateway to mitochondrial dysfunction and death. Science 2001; 292: 727-730
18. Green DR, Kroemer G. The pathophysiology of mitochondrial cell death. Science 2004; 305: 626-629
19. Korsmeyer SJ, Shutter JR, Veis DJ, Merry DE, Oltvai ZN. Bcl-2/Bax: a rheostat that regulates an anti-oxidant pathway and cell death. Semin Cancer Biol 1993; 4: 327-332
20. Danial NN, Korsmeyer SJ. Cell death: critical control points. Cell 2004; 116: 205-219
21. Kim H, Rafiuddin-Shah M, Tu HC, Jeffers JR, Zambetti GP, Hsieh JJ, et al. Hierarchical regulation of mitochondrion-dependent apoptosis by BCL-2 subfamilies. Nat Cell Biol 2006; 8: 1348-1358
22. Fu Y, Li J, Lee AS. GRP78/BiP inhibits endoplasmic reticulum BIK and protects human breast cancer cells against estrogen starvation-induced apoptosis. Cancer Res 2007; 67: 3734-3740
23. Upton JP, Austgen K, Nishino M, Coakley KM, Hagen A, Han D, et al. Caspase-2 cleavage of BID is a critical apoptotic signal downstream of endoplasmic reticulum stress. Mol Cell Biol 2008; 28: 3943-3951
24. Powers MV, Valenti M, Miranda S, Maloney A, Eccles SA, Thomas G, et al. Mode of cell death induced by the HSP90 inhibitor 17-AAG (tanespimycin) is dependent on the expression of pro-apoptotic BAX. Oncotarget 2013; 4: 1963-1975
25. Paul I, Savage KI, Blayney JK, Lamers E, Gately K, Kerr K, et al. PARP inhibition induces BAX/BAK-independent synthetic lethality of BRCA1-deficient non-small cell lung cancer. J Pathol 2011; 224: 564-574
26. Walensky LD, Pitter K, Morash J, Oh KJ, Barbuto S, Fisher J, et al. A stapled BID BH3 helix directly binds and activates BAX. Mol Cell 2006; 24: 199-210
27. Paraiso KH, Haarberg HE, Wood E, Rebecca VW, Chen YA, Xiang Y, et al. The HSP90 inhibitor XL888 overcomes BRAF inhibitor resistance mediated through diverse mechanisms. Clin Cancer Res 2012; 18: 2502-2514
28. Geserick P, Wang J, Feoktistova M, Leverkus M. The ratio of Mcl-1 and Noxa determines ABT737 resistance in squamous cell carcinoma of the skin. Cell Death Dis 2014; 5: e1412
29. Hanahan D, Weinberg RA. Hallmarks of cancer: the next generation. Cell 2011; 144: 646-674
30. 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 discussion 90
31. Costa DB, Halmos B, Kumar A, Schumer ST, Huberman MS, Boggon TJ, et al. BIM mediates EGFR tyrosine kinase inhibitor-induced apoptosis in lung cancers with oncogenic EGFR mutations. PLoS Med 2007; 4: 1669-1679 discussion 80
32. Gong Y, Somwar R, Politi K, Balak M, Chmielecki J, Jiang X, et al. Induction of BIM is essential for apoptosis triggered by EGFR kinase inhibitors in mutant EGFRdependent lung adenocarcinomas. PLoS Med 2007; 4: e294
33. Nakano K, Vousden KH. PUMA a novel proapoptotic gene, is induced by p53. Mol Cell 2001; 7: 683-694
34. McDonnell JM, Fushman D, Milliman CL, Korsmeyer SJ, Cowburn D. Solution structure of the proapoptotic molecule BID: a structural basis for apoptotic agonists and antagonists. Cell 1999; 96: 625-634
35. 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
36. Akgul C, Turner PC, White MR, Edwards SW. Functional analysis of the human MCL-1 gene. Cell Mol Life Sci 2000; 57: 684-691
37. Akgul C. Mcl-1 is a potential therapeutic target in multiple types of cancer. Cell Mol Life Sci 2009; 66: 1326-1336
38. Fritsch RM, Schneider G, Saur D, Scheibel M, Schmid RM. Translational repression of MCL-1 couples stress-induced eIF2 alpha phosphorylation to mitochondrial apoptosis initiation. J Biol Chem 2007; 282: 22551-22562
39. Mills JR, Hippo Y, Robert F, Chen SM, Malina A, Lin CJ, et al. mTORC1 promotes survival through translational control of Mcl-1. Proc Natl Acad Sci USA 2008; 105: 10853-10858
40. Sathe P, Delconte RB, Souza-Fonseca-Guimaraes F, Seillet C, Chopin M, Vandenberg CJ, et al. Innate immunodeficiency following genetic ablation of Mcl1 in natural killer cells. Nat Commun 2014; 5: 4539
41. Kotha A, Sekharam M, Cilenti L, Siddiquee K, Khaled A, Zervos AS, et al. Resveratrol inhibits Src and Stat3 signaling and induces the apoptosis of malignant cells containing activated Stat3 protein. Mol Cancer Ther2006; 5: 621-629
42. Nam S, Williams A, Vultur A, List A, Bhalla K, Smith D, et al. Dasatinib (BMS-354825) inhibits Stat5 signaling associated with apoptosis in chronic myelogenous leukemia cells. Mol Cancer Ther 2007; 6: 1400-1405
43. 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: 677-681
44. Pillai RN, Ramalingam SS. Heat shock protein 90 inhibitors in non-small-cell lung cancer. Curr Opin Oncol 2014; 26: 159-164
45. Paul I, Chacko AD, Stasik I, Busacca S, Crawford N, McCoy F, et al. Acquired differential regulation of caspase-8 in cisplatin-resistant non-small-cell lung cancer. Cell Death Dis 2012; 3: e449
46. Busacca S, Sheaff M, Arthur K, Gray SG, O'Byrne KJ, Richard DJ, et al. BRCA1 is an essential mediator of vinorelbine-induced apoptosis in mesothelioma. J Pathol 2012; 227: 200-208
47. Ricci MS, Kim SH, Ogi K, Plastaras JP, Ling J, Wang W, et al. Reduction of TRAILinduced Mcl-1 and cIAP2 by c-Myc or sorafenib sensitizes resistant human cancer cells to TRAIL-induced death. Cancer Cell 2007; 12: 66-80
48. Messeguer X, Escudero R, Farre D, Nunez O, Martinez J, Alba MM. PROMO: detection of known transcription regulatory elements using species-tailored searches. Bioinformatics 2002; 18: 333-334
49. Twiddy D, Naik S, Mistry R, Edwards J, Walker RA, Cohen GM, et al. A TRAIL-R1-specific ligand in combination with doxorubicin selectively targets primary breast tumour cells for apoptosis. Breast Cancer Res 2010, p 58
50. Shah OJ, Lin X, Li L, Huang X, Li J, Anderson MG, et al. Bcl-XL represents a druggable molecular vulnerability during aurora B inhibitor-mediated polyploidization. Proc Natl Acad Sci USA 2010; 107: 12634-12639
51. Sun XM, Bratton SB, Butterworth M, MacFarlane M, Bcl-2 Cohen GM. and Bcl-xL inhibit CD95-mediated apoptosis by preventing mitochondrial release of Smac/DIABLO and subsequent inactivation of X-linked inhibitor-of-apoptosis protein. J Biol Chem 2002; 277: 11345-11351