Inhibition of HSP90 with AUY922 induces synergy in HER2-amplified trastuzumab-resistant breast and gastric cancer

Molecular Cancer Therapeutics

Volumn 12, Issue 4, 2013, Pages 509-519

  Wainberg, Zev A ^a   Anghel, Adrian ^a   Rogers, Amy M ^a   Desai, Amrita J ^a   Kalous, Ondrej ^a   Conklin, Dylan ^a   Ayala, Raul ^a   O'Brien, Neil A ^a   Quadt, Cornelia ^b   Akimov, Mikhail ^b   Slamon, Dennis J ^a   Finn, Richard S ^a  

^a UNIVERSITY OF CALIFORNIA   (United States)

^b NOVARTIS PHARMA AG   (Switzerland)

Author keywords

[No Author keywords available]

Indexed keywords

5 (2,4 DIHYDROXY 5 ISOPROPYLPHENYL) 4 (4 MORPHOLINOMETHYLPHENYL) 3 ISOXAZOLECARBOXYLIC ACID ETHYLAMIDE; EPIDERMAL GROWTH FACTOR RECEPTOR 2; HEAT SHOCK PROTEIN 90; TRASTUZUMAB;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ANTIPROLIFERATIVE ACTIVITY; APOPTOSIS; ARTICLE; BREAST CANCER; CANCER CELL CULTURE; CANCER INHIBITION; CONTROLLED STUDY; DRUG EFFECT; DRUG EFFICACY; DRUG POTENTIATION; DRUG STRUCTURE; FEMALE; G2 PHASE CELL CYCLE CHECKPOINT; HUMAN; HUMAN CELL; MOUSE; NONHUMAN; PRIORITY JOURNAL; STOMACH CANCER; TUMOR XENOGRAFT; WESTERN BLOTTING;

ANIMALS; ANTIBODIES, MONOCLONAL, HUMANIZED; BREAST NEOPLASMS; CELL LINE, TUMOR; CELL PROLIFERATION; DRUG RESISTANCE, NEOPLASM; DRUG SYNERGISM; FEMALE; GENE AMPLIFICATION; HSP90 HEAT-SHOCK PROTEINS; HUMANS; INHIBITORY CONCENTRATION 50; ISOXAZOLES; MICE; RECEPTOR, ERBB-2; RESORCINOLS; SIGNAL TRANSDUCTION; STOMACH NEOPLASMS;

EID: 84876465085     PISSN: 15357163     EISSN: 15388514     Source Type: Journal    
DOI: 10.1158/1535-7163.MCT-12-0507     Document Type: Article

References (47)

1. Slamon DJ, Clark GM, Wong SG, Levin WJ, Ullrich A, McGuire WL. Human breast cancer: correlation of relapse and survival with amplification of the HER-2/neu oncogene. Science 1987;235:177-82. (Pubitemid 17231334)
2. Slamon DJ, Godolphin W, Jones LA, Holt JA, Wong SG, Keith DE, et al. Studies of the HER-2/neu proto-oncogene in human breast and ovarian cancer. Science 1989;244:707-12. (Pubitemid 19147683)
3. Gravalos C, Jimeno A. HER2 in gastric cancer: a new prognostic factor and a novel therapeutic target. Ann Oncol 2008;19:1523-9.
4. Yarden Y, Sliwkowski MX. Untangling the ErbB signalling network. Nat Rev Mol Cell Biol 2001;2:127-37. (Pubitemid 33674041)
5. Murphy CG, Modi S. HER2 breast cancer therapies: a review. Biologics 2009;3:289-301.
6. Montemurro F, Donadio M, Clavarezza M, Redana S, Jacomuzzi ME, Valabrega G, et al. Outcome of patients with HER2-positive advanced breast cancer progressing during trastuzumab-based therapy. Oncologist 2006;11:318-24.
7. Whitesell L, Lindquist SL. HSP90 and the chaperoning of cancer. Nat Rev Cancer 2005;5:761-72. (Pubitemid 41400776)
8. Travers J, Sharp S, Workman P. HSP90 inhibition: two-pronged exploitation of cancer dependencies. Drug Discov Today 2012;17:242-52.
9. Zuo DS, Dai J, Bo AH, Fan J, Xiao XY. Significance of expression of heat shock protein90alpha in human gastric cancer. World J Gastro-enterol 2003;9:2616-8. (Pubitemid 37461282)
10. Pick E, Kluger Y, Giltnane JM, Moeder C, Camp RL, Rimm DL, et al. High HSP90 expression is associated with decreased survival in breast cancer. Cancer Res 2007;67:2932-7. (Pubitemid 46724827)
11. Banerji U. Heat shock protein 90 as a drug target: some like it hot. Clin Cancer Res 2009;15:9-14.
12. Chavany C, Mimnaugh E, Miller P, Bitton R, Nguyen P, Trepel J, et al. p185erbB2 binds to GRP94 in vivo. Dissociation of the p185erbB2/GRP94 heterocomplex bybenzoquinone ansamycins precedes depletion of p185erbB2. J Biol Chem 1996;271:4974-7.
13. Eccles SA, Massey A, Raynaud FI, Sharp SY, Box G, Valenti M, et al. NVP-AUY922: a novel heat shock protein 90 inhibitor active against xenograft tumor growth, angiogenesis, and metastasis. Cancer Res 2008;68:2850-60. (Pubitemid 351556284)
14. Jensen MR, Schoepfer J, Radimerski T, Massey A, Guy CT, Brueggen J, et al. NVP-AUY922: a small molecule HSP90 inhibitor with potent antitumor activity in preclinical breast cancer models. Breast Cancer Res 2008;10:R33.
15. Samuel TA, Sessa C, Britten C, Milligan KS, Mita MM, Banerji U, et al. AUY922, a novel HSP90 inhibitor: final results of a first-in-human study in patients with advanced solid malignancies. J Clin Oncol 28:15s, 2010 (suppl; abstr 2528).
16. 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-pos-itive metastatic breast cancer progressing on trastuzumab. Clin Cancer Res 2011;17:5132-9.
17. Schroder CP, Pedersen JV, Chua S, Swanton C, Akimov M, Ide S, et al. Use of biomarkers and imaging to evaluate the treatment effect of AUY922, an HSP90 inhibitor, in patients with HER2 or ER meta-static breast cancer. J Clin Oncol 29: 2011 (suppl; abstr e11024).
18. Chandarlapaty S, Scaltriti M, Angelini P, Ye Q, Guzman M, Hudis CA, et al. Inhibitors of HSP90 block p95-HER2 signaling in trastuzumab-resistant tumors and suppress their growth. Oncogene 2010;29: 325-34.
19. Scaltriti M, Serra V, Normant E, Guzman M, Rodriguez O, Lim AR, et al. Antitumor activity of the Hsp90 inhibitor IPI-504 in HER2-positive trastuzumab-resistant breast cancer. Mol Cancer Ther 2011;10: 817-24.
20. Leow CC, Chesebrough J, Coffman KT, Fazenbaker CA, Gooya J, Weng D, et al. Antitumor efficacy of IPI-504, a selective heat shock protein 90 inhibitor against human epidermal growth factor receptor 2-positive human xenograft models as a single agent and in combination with trastuzumab or lapatinib. Mol Cancer Ther 2009;8:2131-41.
21. Konecny GE, Pegram MD, Venkatesan N, Finn R, Yang G, Rahmeh M, et al. Activity of the dual kinase inhibitor lapatinib (GW572016) against HER-2-overexpressing and trastuzumab-treated breast cancer cells. Cancer Res 2006;66:1630-9. (Pubitemid 43259947)
22. Baselga J. Targeting tyrosine kinases in cancer: the second wave. Science 2006;312:1175-8. (Pubitemid 43801135)
23. Xia W, Gerard CM, Liu L, Baudson NM, Ory TL, Spector NL. Combining lapatinib (GW572016), a small molecule inhibitor of ErbB1 and ErbB2 tyrosine kinases, with therapeutic anti-ErbB2 antibodies enhances apoptosis of ErbB2-overexpressing breast cancer cells. Oncogene 2005;24:6213-21. (Pubitemid 43080044)
24. Powers MV, Clarke PA, Workman P. Death by chaperone: HSP90, HSP70 or both? Cell Cycle 2009;8:518-26.
25. Finn RS, Dering J, Conklin D, Kalous O, Cohen DJ, Desai AJ, et al. PD 0332991, a selective cyclin D kinase 4/6 inhibitor, preferentially inhibits proliferation of luminal estrogen receptor-positive human breast cancer cell lines in vitro. Breast Cancer Res 2009;11:R77.
26. O'Brien NA, Browne BC, Chow L, Wang Y, Ginther C, Arboleda J, et al. Activated phosphoinositide 3-kinase/AKT signaling confers resistance to trastuzumab but not lapatinib. Mol Cancer Ther 2010;9:1489-502.
27. Samuels Y, Wang Z, Bardelli A, Silliman N, Ptak J, Szabo S, et al. High frequencyofmutations of the PIK3CA genein humancancers. Science 2004;304:554. (Pubitemid 38541907)
28. Minaguchi T, Yoshikawa H, Oda K, Ishino T, Yasugi T, Onda T, et al. PTEN mutation located only outside exons 5, 6, and 7 is an independent predictor of favorable survival in endometrial carcinomas. Clini Cancer Res 2001;7:2636-42. (Pubitemid 32911365)
29. Chou TC. Preclinical versus clinical drug combination studies. Leuk Lymphoma 2008;49:2059-80.
30. Koopman G, Reutelingsperger CP, Kuijten GA, Keehnen RM, Pals ST, van Oers MH. Annexin V for flow cytometric detection of phosphati-dylserine expression on B cells undergoing apoptosis. Blood 1994;84:1415-20. (Pubitemid 24273007)
31. Martin SJ, Reutelingsperger CP, McGahon AJ, Rader JA, van Schie RC, LaFace DM, et al. Early redistribution of plasma membrane phosphatidylserine is a general feature of apoptosis regardless of the initiating stimulus: inhibition byoverexpressionof Bcl-2and Abl. J Exp Med 1995;182:1545-56.
32. Wainberg ZA, Anghel A, Desai AJ, Ayala R, Luo T, Safran B, et al. Lapatinib, a dual EGFR and HER2 kinase inhibitor, selectively inhibits HER2-amplified human gastric cancer cells and is synergistic with trastuzumab in vitro and in vivo. Clin Cancer Res 2010;16:1509-19.
33. Pegram MD, Konecny GE, O'Callaghan C, Beryt M, Pietras R, Slamon DJ. Rational combinations of trastuzumab with chemotherapeutic drugs used in the treatment of breast cancer. J Natl Cancer Inst 2004;96:739-49. (Pubitemid 38771819)
34. Kim YS, Alarcon SV, Lee S, Lee MJ, Giaccone G, Neckers L, et al. Update on Hsp90 inhibitors in clinical trial. Curr Top Med Chem 2009;9:1479-92.
35. Roe SM, Prodromou C, O'Brien R, Ladbury JE, Piper PW, Pearl LH. Structural basisfor inhibition oftheHsp90 molecular chaperone by the antitumor antibiotics radicicol and geldanamycin. J Med Chem 1999;42:260-6. (Pubitemid 29069861)
36. Mimnaugh EG, Chavany C, Neckers L. Polyubiquitination and protea-somal degradation of the p185c-erbB-2 receptor protein-tyrosine kinase induced by geldanamycin. J Biol Chem 1996;271:22796-801. (Pubitemid 26304727)
37. Schneider C, Sepp-Lorenzino L, Nimmesgern E, Ouerfelli O, Danishefsky S, Rosen N, et al. Pharmacologic shifting of a balance between protein refolding and degradation mediated by Hsp90. Proc Natl Acad Sci U S A 1996;93:14536-41. (Pubitemid 26419002)
38. Neckers L, Workman P. Hsp90 molecular chaperone inhibitors: are we there yet? Clin Cancer Res 2012;18:64-76.
39. Sharp SY, Boxall K, Rowlands M, Prodromou C, Roe SM, Maloney A, et al. In vitro biological characterization of a novel, synthetic diaryl pyrazole resorcinol class of heat shock protein 90 inhibitors. Cancer Res 2007;67:2206-16. (Pubitemid 46424240)
40. 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;1113:202-16. (Pubitemid 350015011)
41. Garrett JT, Arteaga CL. Resistance to HER2-directed antibodies and tyrosine kinase inhibitors: mechanisms and clinical implications. Cancer Biol Ther 2011;11:793-800.
42. Baselga J, Bradbury I, Eidtmann H, Di Cosimo S, de Azambuja E, Aura C, et al. Lapatinib with trastuzumab for HER2-positive early breast cancer (NeoALTTO): a randomised, open-label, multicentre, phase 3 trial. Lancet 2012;379:633-40.
43. Baselga J, Cortes J, Kim S-B, Im S-A, Hegg R, Im Y-H, et al. Pertu-zumab plus trastuzumab plus docetaxel for metastatic breast cancer. N Engl J Med 2012;366:109-19.
44. Lee KH, Lee JH, Han SW, Im SA, Kim TY, Oh DY, et al. Antitumor activity of NVP-AUY922, a novel heat shock protein 90 inhibitor, in human gastric cancer cells is mediated through proteasomal degradation of client proteins. Cancer Sci 2011;102:1388-95.
45. Modi S, Stopeck AT, Gordon MS, Mendelson D, Solit DB, Bagatell R, et al. Combination of trastuzumab and tanespimycin (17-AAG, KOS-953) is safe and active in trastuzumab-refractory HER-2 overexpres-sing breast cancer: a phase I dose-escalation study. J Clin Oncol 2007;25:5410-7. (Pubitemid 350232217)
46. Nahta R, Yuan LX, Zhang B, Kobayashi R, Esteva FJ. Insulin-like growth factor-I receptor/human epidermal growth factor receptor 2 heterodimerization contributes to trastuzumab resistance of breast cancer cells. Cancer Res 2005;65:11118-28. (Pubitemid 41713383)
47. Huang X, Gao L, Wang S, McManaman JL, Thor AD, Yang X, et al. Heterotrimerization of the growth factor receptors erbB2, erbB3, and insulin-like growth factor-i receptor in breast cancer cells resistant to herceptin. Cancer Res 2010;70:1204-14.