Mechanistic evaluation of the novel HSP90 inhibitor NVP-AUY922 in adult and pediatric glioblastoma

Molecular Cancer Therapeutics

Volumn 9, Issue 5, 2010, Pages 1219-1233

  Gaspar, Nathalie ^a,b,c   Sharp, Swee Y ^a   Eccles, Suzanne A ^a   Gowan, Sharon ^a   Popov, Sergey ^b   Jones, Chris ^b   Pearson, Andrew ^b   Vassal, Gilles ^c   Workman, Paul ^a  

^a IMPERIAL CANCER RESEARCH FUND   (United Kingdom)

^b INSTITUTE OF CANCER RESEARCH   (United Kingdom)

^c INSTITUT GUSTAVE ROUSSY   (France)

Author keywords

[No Author keywords available]

Indexed keywords

17 DEMETHOXY 17 (2 DIMETHYLAMINOETHYLAMINO)GELDANAMYCIN; 2 (4 HYDROXYPHENYL) 4 MORPHOLINOPYRIDO[3',2':4,5]FURO[3,2 D]PYRIMIDINE; 3 (5 CHLORO 2,4 DIHYDROXYPHENYL) N ETHYL 4 (4 METHOXYPHENYL) 5 PYRAZOLECARBOXAMIDE; 5 (2,4 DIHYDROXY 5 ISOPROPYLPHENYL) 4 (4 MORPHOLINOMETHYLPHENYL) 3 ISOXAZOLECARBOXYLIC ACID ETHYLAMIDE; BIIB 021; CASPASE 3; CASPASE 7; CASPASE 8; CASPASE 9; CYCLIN D1; CYCLIN DEPENDENT KINASE 1; CYCLIN DEPENDENT KINASE 4; GLYCERALDEHYDE 3 PHOSPHATE DEHYDROGENASE; HEAT SHOCK PROTEIN 27; HEAT SHOCK PROTEIN 72; HEAT SHOCK PROTEIN 90; HEAT SHOCK PROTEIN 90 INHIBITOR; HEAT SHOCK PROTEIN 90ALPHA; HEAT SHOCK PROTEIN 90BETA; HYPOXIA INDUCIBLE FACTOR 1ALPHA; MITOGEN ACTIVATED PROTEIN KINASE; MITOGEN ACTIVATED PROTEIN KINASE 1; MITOGEN ACTIVATED PROTEIN KINASE 3; N (2,3 DIHYDROXYPROPOXY) 3,4 DIFLUORO 2 (2 FLUORO 4 IODOANILINO)BENZAMIDE; NICOTINAMIDE ADENINE DINUCLEOTIDE ADENOSINE DIPHOSPHATE RIBOSYLTRANSFERASE; PROTEIN KINASE B; RADICICOL; TANESPIMYCIN; UNCLASSIFIED DRUG; VER 50589;

ADULT; ANIMAL EXPERIMENT; ANIMAL MODEL; ANTIANGIOGENIC ACTIVITY; ANTINEOPLASTIC ACTIVITY; APOPTOSIS; ARTICLE; CANCER CELL CULTURE; CHILD; CONCENTRATION RESPONSE; CONTROLLED STUDY; CYTOSTASIS; DRUG EFFICACY; DRUG MECHANISM; DRUG POTENCY; ENZYME INHIBITION; ENZYME PHOSPHORYLATION; FEMALE; GLIOBLASTOMA; HUMAN; HUMAN CELL; IN VITRO STUDY; MAXIMUM TOLERATED DOSE; MOUSE; NONHUMAN; NUDE MOUSE; PRIORITY JOURNAL; PROGNOSIS; TUMOR REGRESSION; TUMOR XENOGRAFT;

ADULT; ANIMALS; ANTINEOPLASTIC AGENTS; BRAIN NEOPLASMS; CELL LINE, TUMOR; CHILD; DOSE-RESPONSE RELATIONSHIP, DRUG; FEMALE; GLIOBLASTOMA; HSP90 HEAT-SHOCK PROTEINS; HUMANS; ISOXAZOLES; MAXIMUM TOLERATED DOSE; MICE; MICE, NUDE; RESORCINOLS; TREATMENT OUTCOME; XENOGRAFT MODEL ANTITUMOR ASSAYS;

EID: 77952219448     PISSN: 15357163     EISSN: None     Source Type: Journal    
DOI: 10.1158/1535-7163.MCT-09-0683     Document Type: Article

References (50)

1. Stupp R, Hegi ME, Mason WP, et al. Effects of radiotherapy with concomitant and adjuvant temozolomide versus radiotherapy alone on survival in glioblastoma in a randomised phase III study: 5-year analysis of the EORTC-NCIC trial. Lancet Oncol 2009;10: 459-466
2. Omuro AM, Faivre S, Raymond E. Lessons learned in the development of targeted therapy for malignant gliomas. Mol Cancer Ther 2007;6:1909-1919 (Pubitemid 47052481)
3. Workman P, Burrows F, Neckers L, Rosen N. Drugging the cancer chaperone HSP90: combinatorial therapeutic exploitation of oncogene addiction and tumor stress. Ann N Y Acad Sci 2007; 1113:202-216 (Pubitemid 350015011)
4. Banerji U, O'Donnell A, Scurr M, et al. Phase I pharmacokinetic and pharmacodynamic study of 17-allylamino, 17-demethoxygeldanamycin in patients with advanced malignancies. J Clin Oncol 2005; 23:4152-4161
5. Weigel BJ, Blaney SM, Reid JM, et al. A phase I study of 17-allylaminogeldanamycin in relapsed/refractory pediatric patients with solid tumors: a Children's Oncology Group study. Clin Cancer Res 2007; 13:1789-1793
6. Taldone T, Gozman A, Maharaj R, Chiosis G. Targeting Hsp90: small-molecule inhibitors and their clinical development. Curr Opin Pharmacol 2008;8:370-374
7. Yang J, Yang JM, Iannone M, Shih WJ, Lin Y, Hait WN. Disruption of the EF-2 kinase/Hsp90 protein complex: a possible mechanism to inhibit glioblastoma by geldanamycin. Cancer Res 2001;61: 4010-4016
8. Nomura M, Nomura N, Yamashita J. Geldanamycin-induced degradation of Chk1 is mediated by proteasome. Biochem Biophys Res Commun 2005;335:900-905
9. 2 arrest in U87MG glioblastoma cells through downregulation of Cdc2 and cyclin B1. Biochem Pharmacol 2007;73: 1528-1536
10. Zagzag D, Nomura M, Friedlander DR, et al. Geldanamycin inhibits migration of glioma cells in vitro: a potential role for hypoxia-inducible factor (HIF-1α) in glioma cell invasion. J Cell Physiol 2003; 196:394-402. (Pubitemid 36775888)
11. Nomura M, Nomura N, Newcomb EW, Lukyanov Y, Tamasdan C, Zagzag D. Geldanamycin induces mitotic catastrophe and subsequent apoptosis in human glioma cells. J Cell Physiol 2004;201: 374-384 (Pubitemid 39453123)
12. Sauvageot CM, Weatherbee JL, Kesari S, et al. Efficacy of the HSP90 inhibitor 17-AAG in human glioma cell lines and tumorigenic glioma stem cells. Neuro Oncol 2009;11:109-121
13. Flatten K, Dai NT, Vroman BT, et al. The role of checkpoint kinase 1 in sensitivity to topoisomerase I poisons. J Biol Chem 2005;280: 14349-14355 (Pubitemid 40517339)
14. Premkumar DR, Arnold B, Jane EP, Pollack IF. Synergistic interaction between 17-AAG and phosphatidylinositol 3-kinase inhibition in human malignant glioma cells. Mol Carcinog 2006;45:47-59. (Pubitemid 43122369)
15. Premkumar DR, Arnold B, Pollack IF. Cooperative inhibitory effect of ZD1839 (Iressa) in combination with 17-AAG on glioma cell growth. Mol Carcinog 2006;45:288-301. (Pubitemid 43749196)
16. Kelland LR, Sharp SY, Rogers PM, Myers TG, Workman P. DT-Diaphorase expression and tumor cell sensitivity to 17-allylamino, 17- demethoxygeldanamycin, an inhibitor of heat shock protein 90. J Natl Cancer Inst 1999;91:1940-1949
17. Gaspar N, Sharp SY, Pacey S, et al. Acquired resistance to 17-allylamino-17-demethoxygeldanamycin (17-AAG, tanespimycin) in glioblastoma cells. Cancer Res 2009;69:1966-1975.
18. Cheung KM, Matthews TP, James K, et al. The identification, synthesis, protein crystal structure and in vitro biochemical evaluation of a new 3,4-diarylpyrazole class of Hsp90 inhibitors. Bioorg Med Chem Lett 2005;15:3338-3343
19. Dymock BW, Barril X, Brough PA, et al. Novel, potent small-molecule inhibitors of the molecular chaperone Hsp90 discovered through structure-based design. J Med Chem 2005;48:4212-4215
20. Brough PA, Aherne W, Barril X, et al. 4,5-Diarylisoxazole Hsp90 chaperone inhibitors: potential therapeutic agents for the treatment of cancer. J Med Chem 2008;51:196-218.
21. Sharp SY, Prodromou C, Boxall K, et al. Inhibition of the heat shock protein 90 molecular chaperone in vitro and in vivo by novel, synthetic, potent resorcinylic pyrazole/isoxazole amide analogues. Mol Cancer Ther 2007;6:1198-1211
22. Eccles SA, Massey A, Raynaud FI, et al. NVP-AUY922: a novel heat shock protein 90 inhibitor active against xenograft tumor growth, angiogenesis, and metastasis. Cancer Res 2008;68: 2850-2860
23. Chou TC. Theoretical basis, experimental design, and computerized simulation of synergism and antagonism in drug combination studies. Pharmacol Rev 2006;58:621-681
24. Workman P, Twentyman P, Balkwill F, et al. United Kingdom Co-ordinating Committee on Cancer Research (UKCCCR) Guidelines for the Welfare of Animals in Experimental Neoplasia (Second Edition). Br J Cancer 1998;77:1-10.
25. Geoerger B, Gaspar N, Opolon P, et al. EGFR tyrosine kinase inhibition radiosensitizes and induces apoptosis in malignant glioma and childhood ependymoma xenografts. Int J Cancer 2008;123: 209-216 (Pubitemid 351705211)
26. Gowan SM, Hardcastle A, Hallsworth AE, et al. Application of meso scale technology for the measurement of phosphoproteins in human tumor xenografts. Assay Drug Dev Technol 2007;5:391-401. (Pubitemid 47067884)
27. Sanderson S, Valenti M, Gowan S, et al. Benzoquinone ansamycin heat shock protein 90 inhibitors modulate multiple functions required for tumor angiogenesis. Mol Cancer Ther 2006;5:522-532
28. Bax DA, Little SE, Gaspar N, et al. Molecular and phenotypic characterisation of paediatric glioma cell lines as models for preclinical drug development. PLoS ONE 2009;4:e5209.
29. Douglas M, Lim AR, Porter JR, et al. The antiproliferative activity of the heat shock protein 90 inhibitor IPI-504 is not dependent on NAD (P)H:quinone oxidoreductase 1 activity in vivo. Mol Cancer Ther 2009;8:3369-3378
30. Hostein I, Robertson D, DiStefano F, Workman P, Clarke PA. Inhibition of signal transduction by the Hsp90 inhibitor 17-allylamino-17- demethoxygeldanamycin results in cytostasis and apoptosis. Cancer Res 2001;61:4003-4009 (Pubitemid 32720963)
31. Banerji U, de Bono J, Judson I, Kaye S, Workman P. Biomarkers in early clinical trials: the committed and the skeptics. Clin Cancer Res 2008;14:2512; author reply 3-4.
32. Maloney A, Clarke PA, Naaby-Hansen S, et al. Gene and protein expression profiling of human ovarian cancer cells treated with the heat shock protein 90 inhibitor 17-allylamino-17-demethoxygeldanamycin. Cancer Res 2007;67:3239-3253
33. Citri A, Kochupurakkal BS, Yarden Y. The achilles heel of ErbB-2/ HER2: regulation by the Hsp90 chaperone machine and potential for pharmacological intervention. Cell Cycle 2004;3:51-60. (Pubitemid 40268587)
34. Koga F, Xu W, Karpova TS, McNally JG, Baron R, Neckers L. Hsp90 inhibition transiently activates Src kinase and promotes Src-dependent Akt and Erk activation. Proc Natl Acad Sci U S A 2006;103:11318-11322 (Pubitemid 44156515)
35. Guillard S, Clarke PA, Te Poele R, et al. Molecular pharmacology of phosphatidylinositol 3-kinase inhibition in human glioma. Cell Cycle 2009;8:443-453
36. Birchmeier C, Birchmeier W, Gherardi E, Vande Woude GF. Met, metastasis, motility and more. Nat Rev Mol Cell Biol 2003;4:915-925
37. Broniscer A, Gajjar A. Supratentorial high-grade astrocytoma and diffuse brainstem glioma: two challenges for the pediatric oncologist. Oncologist 2004;9:197-206. (Pubitemid 38452119)
38. Faury D, Nantel A, Dunn SE, et al. Molecular profiling identifies prognostic subgroups of pediatric glioblastoma and shows increased YB-1 expression in tumors. J Clin Oncol 2007;25:1196-1208
39. Uhrbom L, Dai C, Celestino JC, RosenblumMK, Fuller GN, Holland EC. Ink4a-Arf loss cooperates with KRas activation in astrocytes and neural progenitors to generate glioblastomas of various morphologies depending on activated Akt. Cancer Res 2002;62:5551-5558
40. Lyustikman Y, Momota H, Pao W, Holland EC. Constitutive activation of Raf-1 induces glioma formation in mice. Neoplasia 2008;10: 501-510 (Pubitemid 351657392)
41. Stuhmer T, Zollinger A, Siegmund D, et al. Signalling profile and anti-tumour activity of the novel Hsp90 inhibitor NVP-AUY922 in multiple myeloma. Leukemia 2008;22:1604-1612
42. Stommel JM, Kimmelman AC, Ying H, et al. Coactivation of receptor tyrosine kinases affects the response of tumor cells to targeted therapies. Science 2007;318:287-290
43. Chakravarti A, Loeffler JS, Dyson NJ. Insulin-like growth factor receptor I mediates resistance to anti-epidermal growth factor receptor therapy in primary human glioblastoma cells through continued activation of phosphoinositide 3-kinase signaling. Cancer Res 2002;62:200-207 (Pubitemid 34074005)
44. Mellinghoff IK, Wang MY, Vivanco I, et al. Molecular determinants of the response of glioblastomas to EGFR kinase inhibitors. N Engl J Med 2005;353:2012-2024
45. Pore N, Liu S, Haas-Kogan DA, O'Rourke DM, Maity A. PTEN mutation and epidermal growth factor receptor activation regulate vascular endothelial growth factor (VEGF) mRNA expression in human glioblastoma cells by transactivating the proximal VEGF promoter. Cancer Res 2003;63:236-241 (Pubitemid 36070445)
46. Hendriksen EM, Span PN, Schuuring J, et al. Angiogenesis, hypoxia and VEGF expression during tumour growth in a human xenograft tumour model. Microvasc Res 2009;77:96-103.
47. Bardos JI, Ashcroft M. Hypoxia-inducible factor-1 and oncogenic signalling. Bioessays 2004;26:262-269
48. Xie Q, Gao CF, Shinomiya N, et al. Geldanamycins exquisitely inhibit HGF/SF-mediated tumor cell invasion. Oncogene 2005;24: 3697-3707 (Pubitemid 40826869)
49. Lefranc F, Brotchi J, Kiss R. Possible future issues in the treatment of glioblastomas: special emphasis on cell migration and the resistance of migrating glioblastoma cells to apoptosis. J Clin Oncol 2005;23: 2411-2422 (Pubitemid 46218735)
50. Bao R, Lai CJ, Qu H, et al. CUDC-305, a novel synthetic HSP90 inhibitor with unique pharmacologic properties for cancer therapy. Clin Cancer Res 2009;15:4046-4057