Network analysis identifies an HSP90-central hub susceptible in ovarian cancer

Clinical Cancer Research

Volumn 19, Issue 18, 2013, Pages 5053-5067

  Liu, Hanqing ^a   Xiao, Fang ^a   Serebriiskii, Ilya G ^a   O'Brien, Shane W ^a   Maglaty, Marisa A ^a   Astsaturov, Igor ^a   Litwin, Samuel ^a   Martin, Lainie P ^a   Proia, David A ^b   Golemis, Erica A ^a   Connolly, Denise C ^a  

^a FOX CHASE CANCER CENTER   (United States)

^b Synta Pharmaceuticals Corp   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ALISERTIB; ANTINEOPLASTIC AGENT; CISPLATIN; DASATINIB; ERLOTINIB; GANETESPIB; GSK 2334470; HEAT SHOCK PROTEIN 90; PACLITAXEL; RUXOLITINIB; SMALL INTERFERING RNA; UNCLASSIFIED DRUG;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ANTINEOPLASTIC ACTIVITY; APOPTOSIS; ARTICLE; CANCER INHIBITION; CELL CYCLE ARREST; CONCENTRATION RESPONSE; CONTROLLED STUDY; DATA MINING; DRUG POTENTIATION; FEMALE; GENE TARGETING; GROWTH INHIBITION; HUMAN; HUMAN CELL; HUMAN TISSUE; IN VITRO STUDY; IN VIVO STUDY; MOUSE; NONHUMAN; OVARY CARCINOMA; PHARMACODYNAMICS; PRIORITY JOURNAL; PROTEIN ANALYSIS; PROTEIN EXPRESSION; PROTEIN INDUCTION; SIGNAL TRANSDUCTION; TRANSGENIC MOUSE; TUMOR XENOGRAFT;

ANIMALS; ANTINEOPLASTIC AGENTS, PHYTOGENIC; APOPTOSIS; BLOTTING, WESTERN; CELL CYCLE; CELL PROLIFERATION; DRUG SYNERGISM; DRUG THERAPY, COMBINATION; FEMALE; FLOW CYTOMETRY; GENE REGULATORY NETWORKS; HSP90 HEAT-SHOCK PROTEINS; HUMANS; MICE; MICE, SCID; MICE, TRANSGENIC; OVARIAN NEOPLASMS; PACLITAXEL; PROTEIN ARRAY ANALYSIS; RNA, SMALL INTERFERING; TRIAZOLES; TUMOR CELLS, CULTURED; XENOGRAFT MODEL ANTITUMOR ASSAYS;

EID: 84884580988     PISSN: 10780432     EISSN: 15573265     Source Type: Journal    
DOI: 10.1158/1078-0432.CCR-13-1115     Document Type: Article

References (72)

1. Siwak DR, Carey M, Hennessy BT, Nguyen CT, McGahren Murray MJ, Nolden L, et al. Targeting the epidermal growth factor receptor in epithelial ovarian cancer: current knowledge and future challenges. J Oncol 2010;2010:568938.
2. Behbakht K, Sill MW, Darcy KM, Rubin SC, Mannel RS, Waggoner S, et al. Phase II trial of themTORinhibitor, temsirolimus and evaluation of circulating tumor cells and tumor biomarkers in persistent and recurrent epithelial ovarian and primary peritoneal malignancies: a Gynecologic Oncology Group study. Gynecol Oncol 2011;123:19-26.
3. Bodnar L, Górnas M, Szczylik C. Sorafenib as a third line therapy in patients with epithelial ovarian cancer or primary peritoneal cancer: a phase II study. Gynecol Oncol 2011;123:33-6.
4. Garcia AA, Sill MW, Lankes HA, Godwin AK, Mannel RS, Armstrong DK, et al. A phase II evaluation of lapatinib in the treatment of persistent or recurrent epithelial ovarian or primary peritoneal carcinoma: a gynecologic oncology group study. Gynecol Oncol 2012;124:569-74.
5. Matei D, Sill MW, Lankes HA, De Geest K, Bristow RE, Mutch D, et al. Activity of sorafenib in recurrent ovarian cancer and primary peritoneal carcinomatosis: a Gynecologic Oncology Group Trial. J Clin Oncol 2011;29:69-75.
6. Noguera IR, Sun CC, Broaddus RR, Branham D, Levenback CF, Ramirez PT, et al. Phase II trial of imatinib mesylate in patients with recurrent platinum-and taxane-resistant low-grade serous carcinoma of the ovary, peritoneum, or fallopian tube. Gynecol Oncol 2012;125:640-5.
7. Schilder RJ, Brady WE, Lankes HA, Fiorica JV, Shahin MS, Zhou XC, et al. Phase II evaluation of dasatinib in the treatment of recurrent or persistent epithelial ovarian or primary peritoneal carcinoma: a Gynecologic Oncology Group study. Gynecol Oncol 2012;127:70-4.
8. Schilder RJ, Sill MW, Lee RB, Shaw TJ, Senterman MK, Klein-Szanto AJ, et al. Phase II evaluation of imatinib mesylate in the treatment of recurrent or persistent epithelial ovarian or primary peritoneal carcinoma: a Gynecologic Oncology Group study. J Clin Oncol 2008;26:3418-25.
9. Usha L, Sill MW, Darcy KM, Benbrook DM, Hurteau JA, Michelin DP, et al. A Gynecologic Oncology Group phase II trial of the protein kinase C-beta inhibitor, enzastaurin and evaluation of markers with potential predictive and prognostic value in persistent or recurrent epithelial ovarian and primary peritoneal malignancies. Gynecol Oncol 2011;121:455-61.
10. TCGA. Integrated genomic analyses of ovarian carcinoma. Nature 2011;474:609-15.
11. Astsaturov I, Ratushny V, Sukhanova A, Einarson MB, Bagnyukova T, Zhou Y, et al. Synthetic lethal screen of an EGFR-centered network to improve targeted therapies. Sci Signal 2010;3:ra67.
12. Neckers L, Workman P. Hsp90 molecular chaperone inhibitors: are we there yet? Clin Cancer Res 2012;18:64-76.
13. Workman P. Altered states: selectively drugging the Hsp90 cancer chaperone. Trends Mol Med 2004;10:47-51.
14. Kang MH, Reynolds CP, Houghton PJ, Alexander D, Morton CL, Kolb EA, et al. Initial testing (Stage 1) of AT13387, an HSP90 inhibitor, by the pediatric preclinical testing program. Pediatr Blood Cancer 2012;59:185-8.
15. Lock RB, Carol H, Maris JM, Kang MH, Reynolds CP, Kolb EA, et al. Initial testing (stage 1) of ganetespib, an Hsp90 inhibitor, by the pediatric preclinical testing program. Pediatr Blood Cancer 2013;60:E42-E5.
16. Shimamura T, Perera SA, Foley KP, Sang J, Rodig SJ, Inoue T, et al. Ganetespib (STA-9090), a nongeldanamycin HSP90 inhibitor, has potent antitumor activity in in vitro and in vivo models of non-small cell lung cancer. Clin Cancer Res 2012;18:4973-85.
17. Ying W, Du Z, Sun L, Foley KP, Proia DA, Blackman RK, et al. Ganetespib, a unique triazolone-containing Hsp90 inhibitor, exhibits potent antitumor activity and a superior safety profile for cancer therapy. Mol Cancer Ther 2012;11:475-84.
18. Whitehurst AW, Bodemann BO, Cardenas J, Ferguson D, Girard L, Peyton M, et al. Synthetic lethal screen identification of chemosensitizer loci in cancer cells. Nature 2007;446:815-9.
19. Smoot ME, Ono K, Ruscheinski J, Wang PL, Ideker T. Cytoscape 2.8: new features for data integration and network visualization. Bioinformatics 2011;27:431-2.
20. Jayapandian M, Chapman A, Tarcea VG, Yu C, Elkiss A, Ianni A, et al. Michigan Molecular Interactions (MiMI): putting the jigsaw puzzle together. Nucleic Acids Res 2007;35:D566-71.
21. Wishart DS, Knox C, Guo AC, Shrivastava S, Hassanali M, Stothard P, et al. DrugBank: a comprehensive resource for in silico drug discovery and exploration. Nucleic Acids Res 2006;34:D668-72.
22. Szklarczyk D, Franceschini A, Kuhn M, Simonovic M, Roth A, Minguez P, et al. The STRING database in 2011: functional interaction networks of proteins, globally integrated and scored. Nucleic Acids Res 2011;39:D561-8.
23. Taipale M, Jarosz DF, Lindquist S. HSP90 at the hub of protein homeostasis: emerging mechanistic insights. Nat Rev Mol Cell Biol 2010;11:515-28.
24. Echeverría PC, Bernthaler A, Dupuis P, Mayer B, Picard D. An interaction network predicted from public data as a discovery tool: application to the Hsp90 molecular chaperone machine. PLoSONE 2011;6:e26044.
25. Swift S, Lorens J, Achacoso P, Nolan GP. Rapid production of retroviruses for efficient gene delivery to mammalian cells using 293T cell-based systems. Curr Protoc Immunol 2001; Chapter 10:Unit 10.17C.
26. Chou TC, Talalay P. Quantitative analysis of dose-effect relationships: the combined effects of multiple drugs or enzyme inhibitors. Adv Enzyme Regul 1984;22:27-55.
27. Chou T-C, Talalay P. Analysis of combined drug effects: a new look at a very old problem. Trends Pharmacol Sci 1983;4:450-4.
28. Ferreira T, Rasband W. Image J user guide; 2012. Available from: http://imagej.nih.gov/ij/docs/guide
29. Connolly DC, Hensley HH. Xenograft and transgenic mouse models of epithelial ovarian cancer and non-invasive imaging modalities to monitor ovarian tumor growth in situ: applications in evaluating novel therapeutic agents. Curr Protoc Pharmacol 2009; Chapter 14:Unit 14.12.
30. Do TV, Xiao F, Bickel LE, Klein-Szanto AJ, Pathak HB, Hua X, et al. Aurora kinase A mediates epithelial ovarian cancer cell migration and adhesion. Oncogene. 2013 Jan 21. [Epub ahead of print].
31. Connolly DC, Bao R, Nikitin AY, Stephens KC, Poole TW, Hua X, et al. Female mice chimeric for expression of the SV40 TAg under control of the MISIIR promoter develop epithelial ovarian cancer. Cancer Res 2003;63:1389-97.
32. Connolly DC. Animal models of ovarian cancer. Cancer Treat Res 2009;149:353-91.
33. Hensley H, Quinn BA, Wolf RL, Litwin SL, Mabuchi S, Williams SJ, et al. Magnetic resonance imaging for detection and determination of tumor volume in a genetically engineered mouse model of ovarian cancer. Cancer Biol Ther 2007;6:1717-25.
34. Iadevaia S, Lu Y, Morales FC, Mills GB, Ram PT. Identification of optimal drug combinations targeting cellular networks: integrating phospho-proteomics and computational network analysis. Cancer Res 2010;70:6704-14.
35. Tibes R, Qiu Y, Lu Y, Hennessy B, Andreeff M, Mills GB, et al. Reverse phase protein array: validation of a novel proteomic technology and utility for analysis of primary leukemia specimens and hematopoietic stem cells. Mol Cancer Ther 2006;5:2512-21.
36. Bandyopadhyay S, Kelley R, Krogan NJ, Ideker T. Functional maps of protein complexes from quantitative genetic interaction data. PLoS Comput Biol 2008;4:e1000065.
37. Zhong W, Sternberg PW. Genome-wide prediction of C. elegans genetic interactions. Science 2006;311:1481-4.
38. Berns EM, Klijn JG, Henzen-Logmans SC, Rodenburg CJ, van der Burg ME, Foekens JA. Receptors for hormones and growth factors and (onco)-gene amplification in human ovarian cancer. Int J Cancer 1992;52:218-24.
39. Han LY, Landen CN, Trevino JG, Halder J, Lin YG, Kamat AA, et al. Antiangiogenic and antitumor effects of SRC inhibition in ovarian carcinoma. Cancer Res 2006;66:8633-9.
40. Henzen-Logmans SC, Fieret EJ, Berns EM, van der Burg ME, Klijn JG, Foekens JA. Ki-67 staining in benign, borderline, malignant primary and metastatic ovarian tumors: correlation with steroid receptors, epidermal-growth-factor receptor and cathepsin D. Int J Cancer 1994;57:468-72.
41. Huang M, Page C, Reynolds RK, Lin J. Constitutive activation of stat 3 oncogene product in human ovarian carcinoma cells. Gynecol Oncol 2000;79:67-73.
42. Ito K, Sasano H, Ozawa N, Sato S, Silverberg SG, Yajima A. Immunolocalization of epidermal growth factor receptor and c-erbB-2 oncogene product in human ovarian carcinoma. Int J Gynecol Pathol 1992;11:253-7.
43. Nilsson MB, Langley RR, Fidler IJ. Interleukin-6, secreted by human ovarian carcinoma cells, is a potent proangiogenic cytokine. Cancer Res 2005;65:10794-800.
44. Pengetnze Y, Steed M, Roby KF, Terranova PF, Taylor CC. Src tyrosine kinase promotes survival and resistance to chemotherapeutics in a mouse ovarian cancer cell line. Biochem Biophys Res Commun 2003;309:377-83.
45. Savarese TM, Campbell CL, McQuain C, Mitchell K, Guardiani R, Quesenberry PJ, et al. Coexpression of oncostatinM and its receptors and evidence for STAT3 activation in human ovarian carcinomas. Cytokine 2002;17:324-34.
46. Silver DL, Naora H, Liu J, Cheng W, Montell DJ. Activated signal transducer and activator of transcription (STAT) 3: localization in focal adhesions and function in ovarian cancer cell motility. Cancer Res 2004;64:3550-8.
47. van Dam PA, Vergote IB, Lowe DG, Watson JV, van Damme P, van der Auwera JC, et al. Expression of c-erbB-2, c-myc, and c-ras oncoproteins, insulin-like growth factor receptor I, and epidermal growth factor receptor in ovarian carcinoma. J Clin Pathol 1994;47:914-9.
48. Wang DP, Konishi I, Koshiyama M, Nanbu Y, Iwai T, Nonogaki H, et al. Immunohistochemical localization of c-erbB-2 protein and epidermal growth factor receptor in normal surface epithelium, surface inclusion cysts, and common epithelial tumours of the ovary. Virchows Arch A Pathol Anat Histopathol 1992;421:393-400.
49. Vidal CI, Mintz PJ, Lu K, Ellis LM, Manenti L, Giavazzi R, et al. An HSP90-mimic peptide revealed by fingerprinting the pool of antibodies from ovarian cancer patients. Oncogene 2004;23:8859-67.
50. Elstrand MB, Stavnes HT, Trope CG, Davidson B. Heat shock protein 90 is a putative therapeutic target in patients with recurrent advancedstage ovarian carcinoma with serous effusions. Hum Pathol 2012;43:529-35.
51. Bagatell R, Paine-Murrieta GD, Taylor CW, Pulcini EJ, Akinaga S, Benjamin IJ, et al. Induction of a heat shock factor 1-dependent stress response alters the cytotoxic activity of Hsp90-binding agents. Clin Cancer Res 2000;6:3312-8.
52. Gordon AN, Finkler N, Edwards RP, Garcia AA, Crozier M, Irwin DH, et al. Efficacy and safety of erlotinib HCl, an epidermal growth factor receptor (HER1/EGFR) tyrosine kinase inhibitor, in patients with advanced ovarian carcinoma: results from a phase II multicenter study. Int J Gynecol Cancer 2005;15:785-92.
53. Chou TC. Theoretical basis, experimental design, and computerized simulation of synergism and antagonism in drug combination studies. Pharmacol Rev 2006;58:621-81.
54. Bookman MA. First-line chemotherapy in epithelial ovarian cancer. Clin Obstet Gynecol 2012;55:96-113.
55. McGuire WP, Rowinsky EK, Rosenshein NB, Grumbine FC, Ettinger DS, Armstrong DK, et al. Taxol: a unique antineoplastic agent with significant activity in advanced ovarian epithelial neoplasms. Ann Intern Med 1989;111:273-9.
56. Young RC, Von Hoff DD, Gormley P, Makuch R, Cassidy J, Howser D, et al. cis-Dichlorodiammineplatinum (II) for the treatment of advanced ovarian cancer. Cancer Treat Rep 1979;63:1539-44.
57. Modi S, Stopeck A, Linden H, Solit D, Chandarlapaty S, Rosen N, et al. HSP90 inhibition is effective in breast cancer: a phase II trial of tanespimycin (17-AAG) plus trastuzumab in patients with HER2-positive metastatic breast cancer progressing on trastuzumab. Clin Cancer Res 2011;17:5132-9.
58. Richardson PG, Chanan-Khan AA, Lonial S, Krishnan AY, Carroll MP, Alsina M, et al. Tanespimycin and bortezomib combination treatment in patients with relapsed or relapsed and refractory multiple myeloma: results of a phase 1/2 study. Br J Haematol 2011;153:729-40.
59. Sain N, Krishnan B, Ormerod MG, De Rienzo A, Liu WM, Kaye SB, et al. Potentiation of paclitaxel activity by the HSP90 inhibitor 17-allylamino-17- demethoxygeldanamycin in human ovarian carcinoma cell lines with high levels of activated AKT. Mol Cancer Ther 2006;5:1197-208.
60. Jiao Y, Ou W, Meng F, Zhou H, Wang A. Targeting HSP90 in ovarian cancers with multiple receptor tyrosine kinase coactivation. Mol Cancer 2011;10:125.
61. Banerji U, Walton M, Raynaud F, Grimshaw R, Kelland L, Valenti M, et al. Pharmacokinetic-pharmacodynamic relationships for the heat shock protein 90 molecular chaperone inhibitor 17-allylamino, 17-demethoxygeldanamycin in human ovarian cancer xenograft models. Clin Cancer Res 2005;11:7023-32.
62. Hendrickson AE, Oberg AL, Glaser G, Camoriano JK, Peethambaram PP, Colon-Otero G, et al. A phase II study of gemcitabine in combination with tanespimycin in advanced epithelial ovarian and primary peritoneal carcinoma. Gynecol Oncol 2012;124:210-5.
63. Jhaveri K, Miller K, Rosen L, Schneider B, Chap L, Hannah A, et al. A phase I dose-escalation trial of trastuzumab and alvespimycin hydrochloride (KOS-1022;17 DMAG) in the treatment of advanced solid tumors. Clin Cancer Res 2012;18:5090-8.
64. Taldone T, Sun W, Chiosis G. Discovery and development of heat shock protein 90 inhibitors. Bioorg Med Chem 2009;17:2225-35.
65. Proia DA, Foley KP, Korbut T, Sang J, Smith D, Bates RC, et al. Multifaceted intervention by the Hsp90 inhibitor ganetespib (STA-9090) in cancer cells with activated JAK/STAT signaling. PLoS ONE 2011;6:e18552.
66. Proia DA, Sang J, He S, Smith DL, Sequeira M, Zhang C, et al. Synergistic activity of the Hsp90 inhibitor ganetespib with taxanes in non-small cell lung cancer models. Invest New Drugs 2012;30:2201-9.
67. Sang J, Acquaviva J, Friedland JC, Smith DL, Sequeira M, Zhang C, et al. Targeted inhibition of the molecular chaperone Hsp90 overcomes ALK inhibitor resistance in non-small cell lung cancer. Cancer Discov 2013;3:430-43.
68. Wu X, Marmarelis ME, Hodi FS. Activity of the heat shock protein 90 inhibitor ganetespib in melanoma. PLoS ONE 2013;8:e56134.
69. Gritsko TM, Coppola D, Paciga JE, Yang L, Sun M, Shelley SA, et al. Activation and overexpression of centrosome kinase BTAK/Aurora-A in human ovarian cancer. Clin Cancer Res 2003;9:1420-6.
70. Hsu LC, Kapali M, DeLoia JA, Gallion HH. Centrosome abnormalities in ovarian cancer. Int J Cancer 2005;113:746-51.
71. Landen CN Jr, Lin YG, Immaneni A, Deavers MT, Merritt WM, Spannuth WA, et al. Overexpression of the centrosomal protein Aurora-A kinase is associated with poor prognosis in epithelial ovarian cancer patients. Clin Cancer Res 2007;13:4098-104.
72. Thigpen JT, Blessing JA, Ball H, Hummel SJ, Barrett RJ. Phase II trial of paclitaxel in patients with progressive ovarian carcinoma after platinumbased chemotherapy: a Gynecologic Oncology Group study. J Clin Oncol 1994;12:1748-53.