An integrated chemical biology approach identifies specific vulnerability of Ewing's sarcoma to combined inhibition of aurora kinases A and B

Molecular Cancer Therapeutics

Volumn 10, Issue 10, 2011, Pages 1846-1856

  Winter, Georg E ^a   Rix, Uwe ^a   Lissat, Andrej ^c   Stukalov, Alexey ^a   Müllner, Markus K ^a   Bennett, Keiryn L ^a   Colinge, Jacques ^a   Nijman, Sebastian M ^a   Kubicek, Stefan ^a   Kovar, Heinrich ^b   Kontny, Udo ^c   Superti Furga, Giulio ^a  

^a ERICH SCHMID INSTITUTE OF MATERIALS SCIENCE   (Austria)

^b ST ANNA CHILDREN S HOSPITAL   (Austria)

^c UNIVERSITY OF FREIBURG   (Germany)

Author keywords

[No Author keywords available]

Indexed keywords

AURORA A KINASE; AURORA B KINASE; DANUSERTIB; DOXORUBICIN; ETOPOSIDE; PROTEIN SERINE THREONINE KINASE; PROTEIN TYROSINE KINASE; TOZASERTIB;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; CONTROLLED STUDY; DRUG POTENTIATION; DRUG SENSITIVITY; EWING SARCOMA; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROTEIN DENATURATION; PROTEIN TARGETING; PROTEOMICS; RANDOMIZED CONTROLLED TRIAL;

ANIMALS; APOPTOSIS; BONE NEOPLASMS; CELL CYCLE; DOWN-REGULATION; DRUG SYNERGISM; GENE KNOCKDOWN TECHNIQUES; HUMANS; MICE; MICE, SCID; ONCOGENE PROTEINS, FUSION; PIPERAZINES; PROTEIN KINASE INHIBITORS; PROTEIN-SERINE-THREONINE KINASES; PROTO-ONCOGENE PROTEIN C-FLI-1; RANDOM ALLOCATION; RNA INTERFERENCE; RNA-BINDING PROTEIN EWS; SARCOMA, EWING; XENOGRAFT MODEL ANTITUMOR ASSAYS;

EID: 80054000380     PISSN: 15357163     EISSN: 15388514     Source Type: Journal    
DOI: 10.1158/1535-7163.MCT-11-0100     Document Type: Article

References (49)

1. Bernstein M, Kovar H, Paulussen M, Randall RL, Schuck A, Teot LA, et al. Ewing's sarcoma family of tumors: current management. Oncologist 2006;11:503-19. (Pubitemid 43788277)
2. Grier HE, Krailo MD, Tarbell NJ, Link MP, Fryer CJ, Pritchard DJ, et al. Addition of ifosfamide and etoposide to standard chemotherapy for Ewing's sarcoma and primitive neuroectodermal tumor of bone. N Engl J Med 2003;348:694-701. (Pubitemid 36237038)
3. Linabery AM, Ross JA. Childhood and adolescent cancer survival in the US by race and ethnicity for the diagnostic period 1975-1999. Cancer 2008;113:2575-96.
4. Terrier P, Llombart-Bosch A, Contesso G. Small round blue cell tumors in bone: prognostic factors correlated to Ewing's sarcoma and neuroectodermal tumors. Semin Diagn Pathol 1996;13:250-7. (Pubitemid 26282691)
5. Delattre O, Zucman J, Plougastel B, Desmaze C, Melot T, Peter M, et al. Gene fusion with an ETS DNA-binding domain caused by chromosome translocation in human tumours. Nature 1992;359:162-5.
6. May WA, Lessnick SL, Braun BS, Klemsz M, Lewis BC, Lunsford LB, et al. The Ewing's sarcoma EWS/FLI-1 fusion gene encodes a more potent transcriptional activator and is a more powerful transforming gene than FLI-1. Mol Cell Biol 1993;13:7393-98. (Pubitemid 23354263)
7. Lessnick SL, Braun BS, Denny CT, May WA. Multiple domains mediate transformation by the Ewing's sarcoma EWS/FLI-1 fusion gene. Oncogene 1995;10:423-31.
8. Prieur A, Tirode F, Cohen P, Delattre OEWS/FLI-1 silencing and gene profiling of Ewing cells reveal downstream oncogenic pathways and a crucial role for repression of insulin-like growth factor binding protein 3. Mol Cell Biol 2004;24:7275-83. (Pubitemid 39014452)
9. Hahm KB. Repression of the gene encoding the TGF-beta type II receptor is a major target of the EWS-FLI1 oncoprotein. Nat Genet 1999;23:481.
10. Erkizan HV, Kong Y, Merchant M, Schlottmann S, Barber-Rotenberg JS, Yuan L, et al. A small molecule blocking oncogenic protein EWS-FLI1 interaction with RNA helicase A inhibits growth of Ewing's sarcoma. Nat Med 2009;15:750-6.
11. Scotlandi K, Benini S, Nanni P, Lollini PL, Nicoletti G, Landuzzi L, et al. Blockage of insulin-like growth factor-I receptor inhibits the growth of Ewing's sarcoma in athymic mice. Cancer Res 1998;58:4127-31. (Pubitemid 28440569)
12. Scotlandi K, Baldini N, Cerisano V, Manara MC, Benini S, Serra M, et al. CD99 engagement: an effective therapeutic strategy for Ewing tumors. Cancer Res 2000;60:5134-42.
13. Scotlandi K, Remondini D, Castellani G, Manara MC, Nardi F, Cantiani L, et al. Overcoming resistance to conventional drugs in Ewing sarcoma and identification of molecular predictors of outcome. J Clin Oncol 2009;27:2209-16.
14. Druker BJ, Tamura S, Buchdunger E, Ohno S, Segal GM, Fanning S, et al. Effects of a selective inhibitor of the Abl tyrosine kinase on the growth of Bcr-Abl-positive cells. Nat Med 1996;2:561-6.
15. Geyer CE, Forster J, Lindquist D, Chan S, Romieu CG, Pienkowski T, et al. Lapatinib plus capecitabine for HER2-positive advanced breast cancer. N Engl J Med 2006;355:2733-43. (Pubitemid 46021510)
16. Shepherd FA, Rodrigues Pereira J, Ciuleanu T, Tan EH, Hirsh V, Thongprasert S, et al. Erlotinib in previously treated non-small-cell lung cancer. N Engl J Med 2005;353:123-32. (Pubitemid 41058344)
17. Piccaluga PP, Paolini S, Martinelli G. Tyrosine kinase inhibitors for the treatment of Philadelphia chromosome-positive adult acute lymphoblastic leukemia. Cancer 2007;110:1178-86. (Pubitemid 47435586)
18. Hartwell LH, Szankasi P, Roberts CJ, Murray AW, Friend SH. Integrating genetic approaches into the discovery of anticancer drugs. Science 1997;278:1064-8. (Pubitemid 27517876)
19. Costanzo M, Baryshnikova A, Bellay J, Kim Y, Spear ED, Sevier CS, et al. The genetic landscape of a cell. Science 2010;327:425-31.
20. Barbie DA, Tamayo P, Boehm JS, Kim SY, Moody SE, Dunn IF, et al. Systematic RNA interference reveals that oncogenic KRAS-driven cancers require TBK1. Nature 2009;462:108-12.
21. Potratz JC, Saunders DN, Wai DH, Ng TL, McKinney SE, Carboni JM, et al. Synthetic lethality screens reveal RPS6 and MST1R as modifiers of insulin-like growth factor-1 receptor inhibitor activity in childhood sarcomas. Cancer Res 2010;70:8770-81.
22. Karaman MW, Herrgard S, Treiber DK, Gallant P, Atteridge CE, Campbell BT, et al. A quantitative analysis of kinase inhibitor selectivity. Nat Biotechnol 2008;26:127-32.
23. Huang SM, Mishina YM, Liu S, Cheung A, Stegmeier F, Michaud GA, et al. Tankyrase inhibition stabilizes axin and antagonizes Wnt signalling. Nature 2009;461:614-20.
24. Godl K, Gruss OJ, Eickhoff J, Wissing J, Blencke S, Weber M, et al. Proteomic characterization of the angiogenesis inhibitor SU6668 reveals multiple impacts on cellular kinase signaling. Cancer Res 2005;65:6919-26. (Pubitemid 41060731)
25. Bantscheff M, Eberhard D, Abraham Y, Bastuck S, Boesche M, Hobson S, et al. Quantitative chemical proteomics reveals mechanisms of action of clinical ABL kinase inhibitors. Nat Biotechnol 2007;25:1035-44. (Pubitemid 47517638)
26. Rix U, Superti-Furga G. Target profiling of small molecules by chemical proteomics. Nat Chem Biol 2009;5:616-24.
27. Fernbach NV, Planyavsky M, Müller A, Breitwieser FP, Colinge J, Rix U, et al. Acid elution and one-dimensional shotgun analysis on an Orbitrap mass spectrometer: an application to drug affinity chromatography. J Proteome Res 2009;8:4753-65.
28. Borisy AA, Elliott PJ, Hurst NW, Lee MS, Lehar J, Price ER, et al. Systematic discovery of multicomponent therapeutics. Proc Natl Acad Sci U S A 2003;100:7977-82. (Pubitemid 36760080)
29. Harrington EA, Bebbington D, Moore J, Rasmussen RK, Ajose-Adeogun AO, Nakayama T, et al. VX-680, a potent and selective small-molecule inhibitor of the Aurora kinases, suppresses tumor growth in vivo. Nat Med 2004;10:262-7. (Pubitemid 38667616)
30. Carpinelli P, Ceruti R, Giorgini ML, Cappella P, Gianellini L, Croci V, et al. PHA-739358, a potent inhibitor of Aurora kinases with a selective target inhibition profile relevant to cancer. Mol Cancer Ther 2007;6:3158-68.
31. Modugno M, Casale E, Soncini C, Rosettani P, Colombo R, Lupi R, et al. Crystal structure of the T315I Abl mutant in complex with the Aurora kinases inhibitor PHA-739358. Cancer Res 2007;67:7987-90. (Pubitemid 47395130)
32. Carter TA, Wodicka LM, Shah NP, Velasco AM, Fabian MA, Treiber DK, et al. Inhibition of drug-resistant mutants of ABL, KIT, and EGF receptor kinases. Proc Natl Acad Sci U S A 2005;102:11011-6. (Pubitemid 41105984)
33. Rix U, Hantschel O, Dürnberger G, Remsing Rix LL, Planyavsky M, Fernbach NV, et al. Chemical proteomic profiles of the BCR-ABL inhibitors imatinib, nilotinib, and dasatinib reveal novel kinase and nonkinase targets. Blood 2007;110:4055-63. (Pubitemid 350248462)
34. Remsing Rix LL, Rix U, Colinge J, Hantschel O, Bennett KL, Stranzl T, et al. Global target profile of the kinase inhibitor bosutinib in primary chronic myeloid leukemia cells. Leukemia 2009;23:477-85.
35. Wakahara K, Ohno T, Kimura M, Masuda T, Nozawa S, Dohjima T, et al. EWS-Fli1 upregulates expression of the Aurora A and Aurora B kinases. Mol Cancer Res 2008;6:1937-45.
36. Embree LJ, Azuma M, Hickstein DD. Ewing sarcoma fusion protein EWSR1/FLI1 interacts with EWSR1 leading to mitotic defects in zebrafish embryos and human cell lines. Cancer Res 2009;69:4363-71.
37. Carrillo J, García-Aragoncillo E, Azorín D, Agra N, Sastre A, González-Mediero I, et al. Cholecystokinin downregulation by RNA interference impairs Ewing tumor growth. Clin Cancer Res 2007;13:2429-40. (Pubitemid 46698594)
38. Bliss CI. The toxicity of poisons applied jointly. Ann Appl Biol 1939;26:585-615.
39. Tirado OM, Mateo-Lozano S, Notario V. Roscovitine is an effective inducer of apoptosis of Ewing's sarcoma family tumor cells in vitro and in vivo. Cancer Res 2005;65:9320-7. (Pubitemid 41507999)
40. Hantschel O, Rix U, Schmidt U, Bürckstümmer T, Kneidinger M, Schütze G, et al. The Btk tyrosine kinase is a major target of the Bcr-Abl inhibitor dasatinib. Proc Natl Acad Sci U S A 2007;104:13283-8. (Pubitemid 47293937)
41. Li J, Rix U, Fang B, Bai Y, Edwards A, Colinge J, et al. A chemical and phosphoproteomic characterization of dasatinib action in lung cancer. Nat Chem Biol 2010;6:291-9.
42. Lehar J, Krueger A, Zimmermann G, Borisy A. High-order combination effects and biological robustness. Mol Syst Biol 2008;4:215.
43. Shor AC, Keschman EA, Lee FY, Muro-Cacho C, Letson GD, Trent JC, et al. Dasatinib inhibits migration and invasion in diverse human sarcoma cell lines and induces apoptosis in bone sarcoma cells dependent on SRC kinase for survival. Cancer Res 2007;67:2800-8. (Pubitemid 46548969)
44. Lens SM, Voest EE, Medema RH. Shared and separate functions of polo-like kinases and aurora kinases in cancer. Nat Rev Cancer 2010;10:825-41.
45. Lapenna S, Giordano A. Cell cycle kinases as therapeutic targets for cancer. Nat Rev Drug Discov 2009;8:547-66.
46. Marumoto T, Zhang D, Saya H. Aurora-A - a guardian of poles. Nat Rev Cancer 2005;5:42-50. (Pubitemid 40052324)
47. Dar AA, Goff LW, Majid S, Berlin J, El-Rifai WAurora kinase inhibitors-rising stars in cancer therapeutics? Mol Cancer Ther 2010;9:268-78.
48. El-Sheikh A, Fan R, Birks D, Donson A, Foreman NK, Vibhakar R, et al. Inhibition of Aurora Kinase A enhances chemosensitivity of medulloblastoma cell lines. Pediatr Blood Cancer 2010;55:35-41.
49. Maris JM, Morton CL, Gorlick R, Kolb EA, Lock R, Carol H, et al. Initial testing of the Aurora kinase A inhibitor MLN8237 by the Pediatric Preclinical Testing Program (PPTP). Pediatr Blood Cancer 2010;55:26-34.