Effcacy of the HSP90 inhibitor 17-AAG in human glioma cell lines and tumorigenic glioma stem cells

Neuro-Oncology

Volumn 11, Issue 2, 2009, Pages 109-121

  Sauvageot, Claire Marie Elisabeth ^a,b,d   Weatherbee, Jessica Leigh ^a   Kesari, Santosh ^b,d   Winters, Susan Elizabeth ^a   Barnes, Jessica ^a   Dellagatta, Jamie ^e   Ramakrishna, Naren Raj ^c,d   Stiles, Charles Dean ^a,d   Kung, Andrew Li Jen ^a,d   Kieran, Mark W ^a,d   Wen, Patrick Yung Chih ^a,b,d  

^a DANA FARBER CANCER INSTITUTE   (United States)

^b MASSACHUSETTS GENERAL HOSPITAL   (United States)

^c BRIGHAM AND WOMEN S HOSPITAL   (United States)

^d HARVARD MEDICAL SCHOOL   (United States)

^e NONE

Author keywords

17 AAG; Gliomas; Radiosensitizer; Stem cells

Indexed keywords

EPIDERMAL GROWTH FACTOR RECEPTOR; HEAT SHOCK PROTEIN 90; PHOSPHATIDYLINOSITOL 3,4,5 TRISPHOSPHATE 3 PHOSPHATASE; PROTEIN P53; TANESPIMYCIN; TEMOZOLOMIDE; 17-(ALLYLAMINO)-17-DEMETHOXYGELDANAMYCIN; ALKYLATING AGENT; BENZOQUINONE DERIVATIVE; DACARBAZINE; DRUG DERIVATIVE; EGFR PROTEIN, HUMAN; MACROCYCLIC LACTAM; PTEN PROTEIN, HUMAN;

ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; CANCER RADIOTHERAPY; CARCINOGENESIS; CONTROLLED STUDY; DRUG EFFICACY; DRUG INHIBITION; DRUG MECHANISM; DRUG POTENTIATION; ENZYME REGULATION; GLIOBLASTOMA; GLIOMA CELL; HUMAN; HUMAN CELL; IN VITRO STUDY; IN VIVO STUDY; MOUSE; NONHUMAN; PROTEIN DEGRADATION; SIGNAL TRANSDUCTION; TUMOR GROWTH; ANIMAL; BRAIN TUMOR; DRUG ANTAGONISM; DRUG COMBINATION; GENETICS; GLIOMA; METABOLISM; MOUSE MUTANT; NUDE MOUSE; PATHOLOGY; PHYSIOLOGY; RADIATION DOSE; STEM CELL; TUMOR CELL LINE; WESTERN BLOTTING;

ANIMALS; ANTINEOPLASTIC AGENTS, ALKYLATING; BENZOQUINONES; BLOTTING, WESTERN; BRAIN NEOPLASMS; CELL LINE, TUMOR; DACARBAZINE; DRUG THERAPY, COMBINATION; GLIOMA; HSP90 HEAT-SHOCK PROTEINS; HUMANS; LACTAMS, MACROCYCLIC; MICE; MICE, NUDE; MICE, SCID; PTEN PHOSPHOHYDROLASE; RADIATION TOLERANCE; RECEPTOR, EPIDERMAL GROWTH FACTOR; STEM CELLS; TUMOR SUPPRESSOR PROTEIN P53;

EID: 65949121610     PISSN: 15228517     EISSN: 15235866     Source Type: Journal    
DOI: 10.1215/15228517-2008-060     Document Type: Article

References (68)

1. Cavenee WK, Furnari FB, Nagane M, et al. Diffusely infiltrating astro- cytomas. In: Kleihues P, Cavenee WK, eds. WHO Classification of Tumors: Pathology and Genetics of Tumours of the Nervous System. Lyon: IARC Press; 2000:10-21.
2. Stupp R, Mason WP, van den Bent MJ, et al. Radiotherapy plus con- comitant and adjuvant temozolomide for glioblastoma. N Engl J Med. 2005;352:987-996.
3. Galli R, Binda E, Orfanelli U, et al. Isolation and characterization of tumorigenic, stem-like neural precursors from human glioblastoma. Cancer Res. 2004;64:7011-7021.
4. Singh SK, Clarke ID, Terasaki M, et al. Identification of a cancer stem cell in human brain tumors. Cancer Res. 2003;63:5821-5828.
5. Singh SK, Hawkins C, Clarke ID, et al. Identification of human brain tumour initiating cells. Nature. 2004;432:396-401.
6. Yuan X, Curtin J, Xiong Y, et al. Isolation of cancer stem cells from adult glioblastoma multiforme. Oncogene. 2004;23:9392-9400.
7. Sauvageot CM, Kesari S, Stiles CD. Molecular pathogenesis of adult brain tumors and the role of stem cells. Neurol Clin. 2007;25:891-924.
8. Wang SI, Puc J, Li J, et al. Somatic mutations of PTEN in glioblastoma multiforme. Cancer Res. 1997;57:4183-4186.
9. Sansal I, Sellers WR. The biology and clinical relevance of the PTEN tumor suppressor pathway. J Clin Oncol. 2004;22:2954-2963.
10. Broderick DK, Di C, Parrett TJ, et al. Mutations of PIK3CA in anaplas- tic oligodendrogliomas, high-grade astrocytomas, and medulloblasto- mas. Cancer Res. 2004;64:5048-5050.
11. Samuels Y, Wang Z, Bardelli A, et al. High frequency of mutations of the PIK3CA gene in human cancers. Science. 2004;304:554.
12. Ekstrand AJ, James CD, Cavenee WK, et al. Genes for epidermal growth factor receptor, transforming growth factor alpha, and epi- dermal growth factor and their expression in human gliomas in vivo. Cancer Res. 1991;51:2164-2172.
13. Wong AJ, Bigner SH, Bigner DD, et al. Increased expression of the epidermal growth factor receptor gene in malignant gliomas is invari- ably associated with gene amplification. Proc Natl Acad Sci U S A. 1987;84:6899-6903.
14. Libermann TA, Nusbaum HR, Razon N, et al. Amplification, enhanced expression and possible rearrangement of EGF receptor gene in pri- mary human brain tumours of glial origin. Nature. 1985;313:144-147.
15. Libermann TA, Nusbaum HR, Razon N, et al. Amplification and over- expression of the EGF receptor gene in primary human glioblastomas. J Cell Sci. 1985;3(suppl):161-172.
16. Shinojima N, Tada K, Shiraishi S, et al. Prognostic value of epidermal growth factor receptor in patients with glioblastoma multiforme. Can- cer Res. 2003;63:6962-6970.
17. Steck PA, Lee P, Hung MC,Yung WK. Expression of an altered epider- mal growth factor receptor by human glioblastoma cells. Cancer Res. 1988;48:5433-5439.
18. Nishikawa R, Ji XD, Harmon RC, et al. A mutant epidermal growth factor receptor common in human glioma confers enhanced tumori- genicity. Proc Natl Acad Sci U S A. 1994;91:7727-7731.
19. Wong AJ, Ruppert JM, Bigner SH, et al. Structural alterations of the epidermal growth factor receptor gene in human gliomas. Proc Natl Acad Sci U S A. 1992;89:2965-2969.
20. Nagane M, Coufal F, Lin H, et al. A common mutant epidermal growth factor receptor confers enhanced tumorigenicity on human glioblas- toma cells by increasing proliferation and reducing apoptosis. Cancer Res. 1996;56:5079-5086.
21. Liu KJ, Chen CT, Hu WS, et al. Expression of cytoplasmic-domain substituted epidermal growth factor receptor inhibits tumorigenicity of EGFR-overexpressed human glioblastoma multiforme. Int J Oncol. 2004;24:581-590.
22. Lorimer IA, Lavictoire SJ. Activation of extracellular-regulated kinases by normal and mutant EGF receptors. Biochim Biophys Acta. 2001; 1538:1-9.
23. Wu CJ, Qian X, O'Rourke DM. Sustained mitogen-activated protein kinase activation is induced by transforming erbB receptor complexes. DNA Cell Biol. 1999;18:731-741.
24. Feldkamp MM, Lala P, Lau N, Roncari L, Guha A. Expression of acti- vated epidermal growth factor receptors, Ras-guanosine triphos- phate, and mitogen-activated protein kinase in human glioblastoma multiforme specimens. Neurosurgery. 1999;45:1442-1453.
25. Feldkamp MM, Lau N, Guha A. Signal transduction pathways and their relevance in human astrocytomas. J Neurooncol. 1997;35:223-248.
26. Hermanson M, Funa K, Hartman M, et al. Platelet-derived growth factor and its receptors in human glioma tissue: expression of messen- ger RNA and protein suggests the presence of autocrine and paracrine loops. Cancer Res. 1992;52:3213-3219.
27. Maxwell M, Naber SP, Wolfe HJ, et al. Coexpression of platelet- derived growth factor (PDGF) and PDGF-receptor genes by primary human astrocytomas may contribute to their development and main- tenance. J Clin Invest. 1990;86:131-140.
28. Westphal M, Ackermann E, Hoppe J, Herrmann HD. Receptors for platelet derived growth factor in human glioma cell lines and influence of suramin on cell proliferation. J Neurooncol. 1991;11:207-213.
29. Uhrbom L, Hesselager G, Nister M, Westermark B. Induction of brain tumors in mice using a recombinant platelet-derived growth factor B-chain retrovirus. Cancer Res. 1998;58:5275-5279.
30. Shamah SM, Stiles CD, Guha A. Dominant-negative mutants of platelet-derived growth factor revert the transformed phenotype of human astrocytoma cells. Mol Cell Biol. 1993;13:7203-7212.
31. Jensen RL. Growth factor-mediated angiogenesis in the malignant progression of glial tumors: a review. Surg Neurol. 1998;49:189-195.
32. Pratt WB, Toft DO. Regulation of signaling protein function and traf- ficking by the hsp90/hsp70-based chaperone machinery. Exp Biol Med (Maywood). 2003;228:111-133.
33. Burger AM, Fiebig HH, Stinson SF, Sausville EA. 17-(Allylamino)-17- demethoxygeldanamycin activity in human melanoma models. Anti- cancer Drugs. 2004;15:377-387.
34. Bagatell R, Khan O, Paine-Murrieta G, et al. Destabilization of steroid receptors by heat shock protein 90-binding drugs: a ligand-independent approach to hormonal therapy of breast cancer. Clin Cancer Res. 2001;7:2076-2084.
35. Nguyen DM, Desai S, Chen A, Weiser TS, Schrump DS. Modula- tion of metastasis phenotypes of non-small cell lung cancer cells by 17-allylamino 17-demethoxy geldanamycin. Ann Thorac Surg. 2000;70:1853-1860.
36. Nguyen DM, Lorang D, Chen GA, et al. Enhancement of paclitaxel- mediated cytotoxicity in lung cancer cells by 17-allylamino geldanamy- cin: in vitro and in vivo analysis. Ann Thorac Surg. 2001;72:371-378.
37. Nimmanapalli R, O'Bryan E, Bhalla K. Geldanamycin and its analogue 17-allylamino-17-demethoxygeldanamycin lowers Bcr-Abl levels and induces apoptosis and differentiation of Bcr-Abl-positive human leu- kemic blasts. Cancer Res. 2001;61:1799-1804.
38. Yang J, Yang JM, Iannone M et al. Disruption of the EF-2 kinase/Hsp90 protein complex: a possible mechanism to inhibit glioblastoma by geldanamycin. Cancer Res. 2001;61:4010-4016.
39. Braga-Basaria M, Hardy E, Gottfried R, et al. 17-Allylamino-17- demethoxygeldanamycin activity against thyroid cancer cell lines cor- relates with heat shock protein 90 levels. J Clin Endocrinol Metab. 2004;89:2982-2988.
40. Bisht KS, Bradbury CM, Mattson D, et al. Geldanamycin and 17-allylamino-17-demethoxygeldanamycin potentiate the in vitro and in vivo radiation response of cervical tumor cells via the heat shock protein 90-mediated intracellular signaling and cytotoxicity. Cancer Res. 2003;63:8984-8995.
41. Munster PN, Marchion DC, Basso AD, Rosen N. Degradation of HER2 by ansamycins induces growth arrest and apoptosis in cells with HER2 overexpression via a HER3, phosphatidylinositol 3-kinase-AKT-depen- dent pathway. Cancer Res. 2002;62:3132-3137.
42. Hostein I, Robertson D, DiStefano F, Workman P, Clarke PA. Inhibi- tion of signal transduction by the Hsp90 inhibitor 17-allylamino-17- demethoxygeldanamycin results in cytostasis and apoptosis. Cancer Res. 2001;61:4003-4009.
43. Solit DB, Zheng FF, Drobnjak M, et al. 17-Allylamino-17-demethox- ygeldanamycin induces the degradation of androgen receptor and HER-2/neu and inhibits the growth of prostate cancer xenografts. Clin Cancer Res. 2002;8:986-993.
44. Schulte TW, An WG, Neckers LM. Geldanamycin-induced destabiliza- tion of Raf-1 involves the proteasome. Biochem Biophys Res Com- mun. 1997;239:655-659.
45. An WG, Schulte TW, Neckers LM. The heat shock protein 90 antago- nist geldanamycin alters chaperone association with p210bcr-abl and v-src proteins before their degradation by the proteasome. Cell Growth Differ. 2000;11:355-360.
46. Whitesell L, Mimnaugh EG, De Costa B, Myers CE, Neckers LM. Inhibition of heat shock protein HSP90-pp60v-src heteroprotein complex formation by benzoquinone ansamycins: essential role for stress proteins in oncogenic transformation. Proc Natl Acad Sci U S A. 1994;91:8324-8328.
47. Miller P, DiOrio C, Moyer M, et al. Depletion of the erbB-2 gene prod- uct p185 by benzoquinoid ansamycins. Cancer Res. 1994;54:2724-2730.
48. Mimnaugh EG, Chavany C, Neckers L. Polyubiquitination and pro- teasomal degradation of the p185c-erbB-2 receptor protein-tyrosine kinase induced by geldanamycin. J Biol Chem. 1996;271:22796-22801.
49. Schulte TW, Blagosklonny MV, Ingui C, Neckers L. Disruption of the Raf-1-Hsp90 molecular complex results in destabilization of Raf-1 and loss of Raf-1-Ras association. J Biol Chem. 1995;270:24585-24588.
50. Kamal A, Thao L, Sensintaffar J, et al. A high-affinity conformation of Hsp90 confers tumour selectivity on Hsp90 inhibitors. Nature. 2003;425:407-410.
51. Workman P. Auditing the pharmacological accounts for Hsp90 molecular chaperone inhibitors: unfolding the relationship between pharmacokinetics and pharmacodynamics. Mol Cancer Ther. 2003;2:131-138.
52. Xu L, Eiseman JL, Egorin MJ, D'Argenio DZ. Physiologically-based phar- macokinetics and molecular pharmacodynamics of 17-(allylamino)-17- demethoxygeldanamycin and its active metabolite in tumor-bearing mice. J Pharmacokinet Pharmacodyn. 2003;30:185-219.
53. Stommel JM, Kimmelman AC, Ying H, et al. Coactivation of receptor tyrosine kinases affects the response of tumor cells to targeted thera- pies. Science. 2007;318:287-290.
54. Rubin JB, Kung AL, Klein RS, et al. A small-molecule antagonist of CXCR4 inhibits intracranial growth of primary brain tumors. Proc Natl Acad Sci U S A. 2003;100:13513-13518.
55. Bachoo RM, Maher EA, Ligon KL, et al. Epidermal growth factor receptor and Ink4a/Arf: convergent mechanisms governing terminal differentiation and transformation along the neural stem cell to astro- cyte axis. Cancer Cell. 2002;1:269-277.
56. Reynolds BA, Weiss S. Generation of neurons and astrocytes from iso- lated cells of the adult mammalian central nervous system. Science. 1992;255:1707-1710.
57. Ligon KL, Huillard E, Mehta S, et al. Olig2-regulated lineage-restricted pathway controls replication competence in neural stem cells and malignant glioma. Neuron. 2007;53:503-517.
58. Newcomb EW, Lukyanov Y, Schnee T, et al. The geldanamycin analogue 17-allylamino-17-demethoxygeldanamycin inhibits the growth of GL261 glioma cells in vitro and in vivo. Anticancer Drugs. 2007;18:875-882.
59. 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.
60. Russell JS, Burgan W, Oswald KA, Camphausen K, Tofilon PJ. Enhanced cell killing induced by the combination of radiation and the heat shock protein 90 inhibitor 17-allylamino-17-demethoxygeldana- mycin: a multitarget approach to radiosensitization. Clin Cancer Res. 2003;9:3749-3755.
61. Ishii N, Maier D, Merlo A, et al. Frequent co-alterations of TP53, p16/CDKN2A, p14ARF, PTEN tumor suppressor genes in human glioma cell lines. Brain Pathol. 1999;9:469-479.
62. Kesari S, Ramakrishna N, Sauvageot C, Stiles CD, Wen PY. Targeted molecular therapy of malignant gliomas. Curr Neurol Neurosci Rep. 2005;5:186-197.
63. Dote H, Burgan WE, Camphausen K, Tofilon PJ. Inhibition of hsp90 compromises the DNA damage response to radiation. Cancer Res. 2006;66:9211-9220.
64. Kao GD, Jiang Z, Fernandes AM, Gupta AK, Maity A. Inhibition of phosphatidylinositol-3-OH kinase/Akt signaling impairs DNA repair in glioblastoma cells following ionizing radiation. J Biol Chem. 2007;282:21206-21212.
65. Pirollo KF, Hao Z, Rait A, Ho CW, Chang EH. Evidence support- ing a signal transduction pathway leading to the radiation-resistant phenotype in human tumor cells. Biochem Biophys Res Commun. 1997;230:196-201.
66. Friedman HS, Kerby T, Calvert H. Temozolomide and treatment of malignant glioma. Clin Cancer Res. 2000;6:2585-2597.
67. Kokkinakis DM, Bocangel DB, Schold SC, Moschel RC, Pegg AE. Thresholds of O6-alkylguanine-DNA alkyltransferase which confer significant resistance of human glial tumor xenografts to treatment with 1,3-bis(2-chloroethyl)-1- nitrosourea or temozolomide. Clin Can- cer Res. 2001;7:421-428.
68. Hegi ME, Diserens AC, Gorlia T, et al. MGMT gene silencing and benefit from temozolomide in glioblastoma. N Engl J Med. 2005; 352:997-1003.