Ganetespib blocks HIF-1 activity and inhibits tumor growth, vascularization, stem cell maintenance, invasion, and metastasis in orthotopic mouse models of triple-negative breast cancer

Journal of Molecular Medicine

Volumn 92, Issue 2, 2014, Pages 151-164

  Xiang, Lisha ^a,b,d   Gilkes, Daniele M ^a,b   Chaturvedi, Pallavi ^a,b   Luo, Weibo ^a,c   Hu, Hongxia ^a,b   Takano, Naoharu ^a,b   Liang, Houjie ^d   Semenza, Gregg L ^a,b,c  

^a Institute for Cell Engineering   (United States)

^b JOHNS HOPKINS UNIVERSITY   (United States)

^c JOHNS HOPKINS UNIVERSITY SCHOOL OF MEDICINE   (United States)

^d THIRD MILITARY MEDICAL UNIVERSITY   (China)

Author keywords

Breast cancer metastasis; Cancer stem cell; Ganetespib; Hsp90 inhibitor; Hypoxia inducible factor 1

Indexed keywords

ANIMALS; CELL LINE, TUMOR; FEMALE; GENE EXPRESSION REGULATION, NEOPLASTIC; GLUCOSE TRANSPORTER TYPE 1; HSP90 HEAT-SHOCK PROTEINS; HUMANS; HYPOXIA-INDUCIBLE FACTOR 1; IMMUNOBLOTTING; IMMUNOHISTOCHEMISTRY; MICE; MICE, SCID; NEOPLASM INVASIVENESS; NEOPLASM METASTASIS; NEOPLASTIC STEM CELLS; NEOVASCULARIZATION, PATHOLOGIC; NEURAL CELL ADHESION MOLECULE L1; REVERSE TRANSCRIPTASE POLYMERASE CHAIN REACTION; TRIAZOLES; TRIPLE NEGATIVE BREAST NEOPLASMS; TUMOR BURDEN; VASCULAR ENDOTHELIAL GROWTH FACTOR A; XENOGRAFT MODEL ANTITUMOR ASSAYS;

EID: 84894058948     PISSN: 09462716     EISSN: 14321440     Source Type: Journal    
DOI: 10.1007/s00109-013-1102-5     Document Type: Article

References (39)

1. 2 histography. Antioxid Redox Signal 9:1221-1235
2. Semenza GL (2013) Cancer-stromal cell interactions mediated by hypoxia-inducible factors promote angiogenesis, lymphangiogenesis, and metastasis. Oncogene 32:4057-4063
3. Semenza GL (2013) HIF-1 mediates metabolic responses to intratumoral hypoxia and oncogenic mutations. J Clin Invest 123:3664-3671
4. Forsythe JA, Jiang BH, Iyer NV, Agani F, Leung SW, Koos RD, Semenza GL (1996) Activation of vascular endothelial growth factor gene transcription by hypoxia-inducible factor 1. Mol Cell Biol 16:4604-4613
5. Ceradini DJ, Kulkarni AR, Callaghan MJ, Tepper OM, Bastidas N, Kleinman ME, Capla JM, Galiano RD, Levine JP, Gurtner GC (2004) Progenitor cell trafficking is regulated by hypoxic gradients through HIF-1 induction of SDF-1. Nat Med 10:858-864
6. Chaturvedi P, Gilkes DM, Wong CC, Kshitiz LW, Zhang H, Wei H, Takano N, Schito L, Levchenko A et al (2013) Hypoxia-inducible factor-dependent breast cancer-mesenchymal stem cell bidirectional signaling promotes metastasis. J Clin Invest 123:189-205
7. Choi JY, Jang YS, Min SY, Song JY (2011) Overexpression of MMP-9 and HIF-1α in breast cancer cells under hypoxic conditions. J Breast Cancer 14:88-95
8. Gilkes DM, Chaturvedi P, Bajpai S, Wong CC, Wei H, Pitcairn S, Hubbi ME, Wirtz D, Semenza GL (2013) Collagen prolyl hydroxylases are essential for breast cancer metastasis. Cancer Res 73:3285-3296
9. Erler JT, Bennewith KL, Nicolau M, Dornhöfer N, Kong C, Le QT, Chi JT, Jeffrey SS, Giaccia AJ (2006) Lysyl oxidase is essential for hypoxia-induced metastasis. Nature 440:1222-1226
10. Wong CC, Gilkes DM, Zhang H, Chen J, Wei H, Chaturvedi P, Fraley SI, Wong CM, Khoo US, Ng IO et al (2011) Hypoxia-inducible factor 1 is a master regulator of breast cancer metastatic niche formation. Proc Natl Acad Sci U S A 108:16369-16374
11. Zhang H, Wong CC, Wei H, Gilkes DM, Korangath P, Chaturvedi P, Schito L, Chen J, Krishnamachary B, Winnard PT Jr et al (2012) HIF-1-dependent expression of angiopoietin-like 4 and L1CAM mediates vascular metastasis of hypoxic breast cancer cells to the lungs. Oncogene 31:1757-1770
12. Conley SJ, Gheordunescu E, Kakarala P, Newman B, Korkaya H, Heath AN, Clouthier SG, Wicha MS (2012) Antiangiogenic agents increase breast cancer stem cells via the generation of tumor hypoxia. Proc Natl Acad Sci U S A 109:2784-2789
13. Schwab LP, Peacock DL, Majumdar D, Ingels JF, Jensen LC, Smith KD, Cushing RC, Seagroves TN (2012) Hypoxia-inducible factor 1α promotes primary tumor growth and tumor-initiating cell activity in breast cancer. Breast Cancer Res 14:R6
14. 2 tension. Proc Natl Acad Sci U S A 92:5510-5514
15. Prabhakar NR, Semenza GL (2012) Adaptive and maladaptive cardiorespiratory responses to continuous and intermittent hypoxia mediated by hypoxia-inducible factors 1 and 2. Physiol Rev 92:967-1003
16. Minet E, Mottet D, Michel G, Roland I, Raes M, Remacle J, Michiels C (1999) Hypoxia-induced activation of HIF-1: role of HIF-1α-Hsp90 interaction. FEBS Lett 460:251-256
17. Isaacs JS, Jung YJ, Mimnaugh EG, Martinez A, Cuttitta F, Neckers LM (2002) Hsp90 regulates a von Hippel Lindau-independent hypoxia-inducible factor-1α-degradative pathway. J Biol Chem 277:29936-29944
18. Isaacs JS, Jung YJ, Neckers L (2004) Aryl hydrocarbon nuclear translocator (ARNT) promotes oxygen-independent stabilization of hypoxia-inducible factor-1α by modulating an Hsp90-dependent regulatory pathway. J Biol Chem 279:16128-16135
19. Katschinski DM, Schindler SG, Thomas T, Voss AK, Wenger RH (2004) Interaction of the PAS B domain with HSP90 accelerates hypoxia-inducible factor 1α stabilization. Cell Physiol Biochem 14:351-360
20. 2-independent and HSP90 inhibitor-induced degradation of HIF-1α. Mol Cell 25:207-217
21. Cleator S, Heller W, Coombes RC (2007) Triple-negative breast cancer: therapeutic options. Lancet Oncol 8:235-244
22. Caldas-Lopes E, Cerchietti L, Ahn JH, Clement CC, Robles AI, Rodina A, Moulick K, Taldone T, Gozman A, Guo Y et al (2009) Hsp90 inhibitor PU-H71, a multimodal inhibitor of malignancy, induces complete responses in triple-negative breast cancer models. Proc Natl Acad Sci U S A 106:8368-8373
23. Mehta PP, Whalen P, Baxi SM, Kung PP, Yamazaki S, Yin M (2011) Effective targeting of triple-negative breast cancer cells by PF-4942847, a novel oral inhibitor of Hsp90. Clin Cancer Res 17:5432-5442
24. Friedland JC, Smith DL, Sang J, Acquaviva J, He S, Zhang C, Proia DA (2013) Targeted inhibition of Hsp90 by ganetespib is effective across a broad spectrum of breast cancer subtypes. Invest New Drugs 2013 May 18 [Epub ahead of print]
25. Ying W, Du Z, Sun L, Foley KP, Proia DA, Blackman RK, Zhou D, Inoue T, Tatsuta N, Sang J et al (2012) Ganetespib, a unique triazolone-containing Hsp90 inhibitor, exhibits potent antitumor activity and a superior safety profile for cancer therapy. Mol Cancer Ther 11:475-484
26. Shimamura T, Perera SA, Foley KP, Sang J, Rodig SJ, Inoue T, Chen L, Li D, Carretero J, Li Y et al (2012) 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 18:4973-4985
27. Schito L, Rey S, Tafani M, Zhang H, Wong CC, Russo A, Russo MA, Semenza GL (2012) Hypoxia-inducible factor 1-dependent expression of platelet-derived growth factor B promotes lymphatic metastasis of hypoxic breast cancer cells. Proc Natl Acad Sci U S A 109:E2707-E2716
28. Lee K, Zhang H, Qian DZ, Rey S, Liu JO, Semenza GL (2009) Acriflavine inhibits HIF-1 dimerization, tumor growth, and vascularization. Proc Natl Acad Sci U S A 106:17910-17915
29. Krishnamachary B, Semenza GL (2007) Analysis of hypoxia-inducible factor 1α expression and its effects on invasion and metastasis. Methods Enzymol 435:347-354
30. Ruifrok AC, Johnston DA (2001) Quantification of histochemical staining by color deconvolution. Anal Quant Cytol Histol 23:291-299
31. Cailleau R, Young R, Olive M, Reeves WJ Jr (1974) Breast tumor cell lines from pleural effusions. J Natl Cancer Inst 53:661-674
32. Chambers AF (2009) MDA-MB-435 and M14 cell lines: identical but not M14 melanoma? Cancer Res 69:5292-5293
33. Charafe-Jauffret E, Ginestier C, Iovino F, Wicinski J, Cervera N, Finetti P, Hur MH, Diebel ME, Monville F, Dutcher J et al (2009) Breast cancer cell lines contain functional cancer stem cells with metastatic capacity and a distinct molecular signature. Cancer Res 69:1302-1313
34. Ginestier C, Hur MH, Charafe-Jauffret E, Monville F, Dutcher J, Brown M, Jacquemier J, Viens P, Kleer CG, Liu S et al (2007) ALDH1 is a marker of normal and malignant human mammary stem cells and a predictor of poor clinical outcome. Cell Stem Cell 1:555-567
35. Marcato P, Dean CA, Giacomantonio CA, Lee PW (2011) Aldehyde dehydrogenase: its role as a cancer stem cell marker comes down to the specific isoform. Cell Cycle 10:1378-1384
36. Ganji PN, Park W, Wen J, Mahaseth H, Landry J, Farris AB, Willingham F, Sullivan PS, Proia DA, El-Hariry I et al (2013) Antiangiogenic effects of ganetespib in colorectal cancer mediated through inhibition of HIF-1α and STAT-3. Angiogenesis 16:903-917
37. Bhola NE, Balko JM, Dugger TC, Kuba MG, Sanchez V, Sanders M, Stanford J, Cook RS, Arteaga CL (2013) TGF-β inhibition enhances chemotherapy action against triple-negative breast cancer. J Clin Invest 123:1348-1358
38. The Cancer Genome Atlas Network (2012) Comprehensive molecular portraits of human breast tumors. Nature 490:61-70
39. Semenza GL (2010) Defining the role of hypoxia-inducible factor 1 in cancer biology and therapeutics. Oncogene 29:625-634