AUY922 effectively overcomes MET- And AXL-mediated resistance to EGFR-TKI in lung cancer cells

PLoS ONE

Volumn 10, Issue 3, 2015, Pages

  Choi, Yun Jung ^a   Kim, Seon Ye ^a   So, Kwang Sup ^a   Baek, In Jeoung ^a   Kim, Woo Sung ^a   Choi, Se Hoon ^a   Lee, Jae Cheol ^a   Bivona, Trever G ^b   Rho, Jin Kyung ^a   Choi, Chang Min ^a  

^a University of Ulsan College of Medicine   (South Korea)

^b UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

EPIDERMAL GROWTH FACTOR RECEPTOR; ERLOTINIB; GEFITINIB; GROWTH FACTOR RECEPTOR; LUMINESPIB; PROTEIN AXL; PROTEIN KINASE B; SCATTER FACTOR RECEPTOR; UNCLASSIFIED DRUG; 5-(2,4-DIHYDROXY-5-ISOPROPYLPHENYL)-4-(4-MORPHOLIN-4-YLMETHYLPHENYL)ISOXAZOLE-3-CARBOXYLIC ACID ETHYLAMIDE; AXL RECEPTOR TYROSINE KINASE; HEAT SHOCK PROTEIN 90; ISOXAZOLE DERIVATIVE; ONCOPROTEIN; PROTEIN TYROSINE KINASE; QUINAZOLINE DERIVATIVE; RESORCINOL DERIVATIVE;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ANTIPROLIFERATIVE ACTIVITY; ARTICLE; CELL DEATH; CELL MIGRATION; CONTROLLED STUDY; DRUG EFFICACY; DRUG RESISTANCE; EGFR GENE; ENZYME ACTIVATION; FEMALE; GENE DELETION; IN VIVO STUDY; LUNG CANCER; LUNG CANCER CELL LINE; MOUSE; NONHUMAN; RECEPTOR DOWN REGULATION; TUMOR GROWTH; TUMOR INVASION; TUMOR XENOGRAFT; ANIMAL; ANTAGONISTS AND INHIBITORS; CELL MOTION; CELL SURVIVAL; DRUG EFFECTS; DRUG SCREENING; GENETICS; HUMAN; LUNG TUMOR; SCID MOUSE; TUMOR CELL LINE;

ANIMALS; CELL LINE, TUMOR; CELL MOVEMENT; CELL SURVIVAL; DRUG RESISTANCE, NEOPLASM; ERLOTINIB HYDROCHLORIDE; FEMALE; HSP90 HEAT-SHOCK PROTEINS; HUMANS; ISOXAZOLES; LUNG NEOPLASMS; MICE, SCID; PROTO-ONCOGENE PROTEINS; PROTO-ONCOGENE PROTEINS C-MET; QUINAZOLINES; RECEPTOR PROTEIN-TYROSINE KINASES; RECEPTOR, EPIDERMAL GROWTH FACTOR; RESORCINOLS; XENOGRAFT MODEL ANTITUMOR ASSAYS;

EID: 84924956411     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0119832     Document Type: Article

References (39)

1. Paz-Ares L, Soulieres D, Melezinek I, Moecks J, Keil L, Mok T, et al. Clinical outcomes in non-small-cell lung cancer patients with EGFR mutations: pooled analysis. J Cell Mol Med. 2010; 14: 51-69. doi: 10.1111/j.1582-4934.2009.00991.x PMID: 20015198
2. Perez-Soler R, Chachoua A, Hammond LA, Rowinsky EK, Huberman M, Karp D, et al. Determinants of tumor response and survival with erlotinib in patients with non-small-cell lung cancer. J Clin Oncol. 2004; 22: 3238-3247. PMID: 15310767
3. Kobayashi S, Boggon TJ, Dayaram T, Janne PA, Kocher O, Meyerson M, et al. EGFR mutation and resistance of non-small-cell lung cancer to gefitinib. N Engl J Med. 2005; 352: 786-792. PMID: 15728811
4. Pao W, Miller VA, Politi KA, Riely GJ, Somwar R, Zakowski M, et al. Acquired resistance of lung adenocarcinomas to gefitinib or erlotinib is associated with a second mutation in the EGFR kinase domain. PLoS Med. 2005; 2: e73. PMID: 15737014
5. Engelman JA, Zejnullahu K, Mitsudomi T, Song Y, Hyland C, Park JO, et al. MET amplification leads to gefitinib resistance in lung cancer by activating ERBB3 signaling. Science. 2007; 316: 1039-1043. PMID: 17463250
6. Zhang Z, Lee JC, Lin L, Olivas V, Au V, Laframboise T, et al. Activation of the AXL kinase causes resistance to EGFR-targeted therapy in lung cancer. Nat Genet. 2012; 44: 852-860. doi: 10.1038/ng.2330 PMID: 22751098
7. Bean J, Brennan C, Shih JY, Riely G, Viale A, Wang L, et al. MET amplification occurs with or without T790M mutations in EGFR mutant lung tumors with acquired resistance to gefitinib or erlotinib. Proc Natl Acad Sci U S A. 2007; 104: 20932-20937. PMID: 18093943
8. Sequist LV, Waltman BA, Dias-Santagata D, Digumarthy S, Turke AB, Fidias P, et al. Genotypic and histological evolution of lung cancers acquiring resistance to EGFR inhibitors. Sci Transl Med. 2011; 3: 75ra26. doi: 10.1126/scitranslmed.3002003 PMID: 21430269
9. Engelman JA, Zejnullahu K, Gale CM, Lifshits E, Gonzales AJ, Shimamura T, et al. PF00299804, an irreversible pan-ERBB inhibitor, is effective in lung cancer models with EGFR and ERBB2 mutations that are resistant to gefitinib. Cancer Res. 2007; 67: 11924-11932. PMID: 18089823
10. Robinson KW, Sandler AB. The role of MET receptor tyrosine kinase in non-small cell lung cancer and clinical development of targeted anti-MET agents. Oncologist. 2013; 18: 115-122. doi: 10.1634/theoncologist.2012-0262 PMID: 23345546
11. Postel-Vinay S, Ashworth A. AXL and acquired resistance to EGFR inhibitors. Nat Genet. 2012; 44: 835-836. doi: 10.1038/ng.2362 PMID: 22836088
12. Wandinger SK, Richter K, Buchner J. The Hsp90 chaperone machinery. J Biol Chem. 2008; 283: 18473-18477. doi: 10.1074/jbc.R800007200 PMID: 18442971
13. Trepel J, Mollapour M, Giaccone G, Neckers L. Targeting the dynamic HSP90 complex in cancer. Nat Rev Cancer. 2010; 10: 537-549. doi: 10.1038/nrc2887 PMID: 20651736
14. Kobayashi N, Toyooka S, Soh J, Yamamoto H, Dote H, Kawasaki K, et al. The anti-proliferative effect of heat shock protein 90 inhibitor, 17-DMAG, on non-small-cell lung cancers being resistant to EGFR tyrosine kinase inhibitor. Lung Cancer. 2012; 75: 161-166. doi: 10.1016/j.lungcan.2011.04.022 PMID: 21767894
15. Shimamura T, Li D, Ji H, Haringsma HJ, Liniker E, Borgman CL, et al. Hsp90 inhibition suppresses mutant EGFR-T790M signaling and overcomes kinase inhibitor resistance. Cancer Res. 2008; 68: 5827-5838. doi: 10.1158/0008-5472.CAN-07-5428 PMID: 18632637
16. Shimamura T, Lowell AM, Engelman JA, Shapiro GI. Epidermal growth factor receptors harboring kinase domain mutations associate with the heat shock protein 90 chaperone and are destabilized following exposure to geldanamycins. Cancer Res. 2005; 65: 6401-6408. PMID: 16024644
17. Rho JK, Choi YJ, Kim SY, Kim TW, Choi EK, Yoon SJ, et al. MET and AXL inhibitor NPS-1034 exerts efficacy against lung cancer cells resistant to EGFR kinase inhibitors because of MET or AXL activation. Cancer Res. 2014; 74: 253-262. doi: 10.1158/0008-5472.CAN-13-1103 PMID: 24165158
18. Carmichael J, DeGraff WG, Gazdar AF, Minna JD, Mitchell JB. Evaluation of a tetrazolium-based semi-automated colorimetric assay: assessment of radiosensitivity. Cancer Res. 1987; 47: 943-946. PMID: 3802101
19. Kim HR, Kim WS, Choi YJ, Choi CM, Rho JK, Lee JCl. Epithelial-mesenchymal transition leads to crizotinib resistance in H2228 lung cancer cells with EML4-ALK translocation. Mol Oncol. 2013; 7: 1093-1102. doi: 10.1016/j.molonc.2013.08.001 PMID: 23993685
20. Whitesell L, Lin NU. HSP90 as a platform for the assembly of more effective cancer chemotherapy. Biochim Biophys Acta. 2012; 1823: 756-766. doi: 10.1016/j.bbamcr.2011.12.006 PMID: 22222203
21. Whitesell L, Lindquist SL. HSP90 and the chaperoning of cancer. Nat Rev Cancer. 2005; 5: 761-772. PMID: 16175177
22. Georgakis GV, Li Y, Rassidakis GZ, Martinez-Valdez H, Medeiros LJ, Younes A. Inhibition of heat shock protein 90 function by 17-allylamino-17-demethoxy-geldanamycin in Hodgkin's lymphoma cells down-regulates Akt kinase, dephosphorylates extracellular signal-regulated kinase, and induces cell cycle arrest and cell death. Clin Cancer Res. 2006; 12: 584-590. PMID: 16428504
23. Georgakis GV, Li Y, Younes A. The heat shock protein 90 inhibitor 17-AAG induces cell cycle arrest and apoptosis in mantle cell lymphoma cell lines by depleting cyclin D1, Akt, Bid and activating caspase 9. Br J Haematol. 2006; 135: 68-71. PMID: 16925576
24. Graham B, Curry J, Smyth T, Fazal L, Feltell R, Harada I, et al. The heat shock protein 90 inhibitor, AT13387, displays a long duration of action in vitro and in vivo in non-small cell lung cancer. Cancer Sci. 2012; 103: 522-527. doi: 10.1111/j.1349-7006.2011.02191.x PMID: 22181674
25. Lamottke B, Kaiser M, Mieth M, Heider U, Gao Z, Nikolova Z, et al. The novel, orally bioavailable HSP90 inhibitor NVP-HSP990 induces cell cycle arrest and apoptosis in multiple myeloma cells and acts synergistically with melphalan by increased cleavage of caspases. Eur J Haematol. 2012; 88: 406-415. doi: 10.1111/j.1600-0609.2012.01764.x PMID: 22309072
26. Okawa Y, Hideshima T, Steed P, Vallet S, Hall S, Huang K, et al. SNX-2112, a selective Hsp90 inhibitor, potently inhibits tumor cell growth, angiogenesis, and osteoclastogenesis in multiple myeloma and other hematologic tumors by abrogating signaling via Akt and ERK. Blood. 2009; 113: 846-855. doi: 10.1182/blood-2008-04-151928 PMID: 18948577
27. Li Y, Ye X, Tan C, Hongo JA, Zha J, Liu J, et al. Axl as a potential therapeutic target in cancer: role of Axl in tumor growth, metastasis and angiogenesis. Oncogene. 2009; 28: 3442-3455. doi: 10.1038/onc.2009.212 PMID: 19633687
28. Webb CP, Taylor GA, Jeffers M, Fiscella M, Oskarsson M, Resau JH, et al. Evidence for a role of Met-HGF/SF during Ras-mediated tumorigenesis/metastasis. Oncogene. 1998; 17: 2019-2025. PMID: 9798673
29. Zhang YX, Knyazev PG, Cheburkin YV, Sharma K, Knyazev YP, Orfi L, et al. AXL is a potential target for therapeutic intervention in breast cancer progression. Cancer Res. 2008; 68: 1905-1915. doi: 10.1158/0008-5472.CAN-07-2661 PMID: 18339872
30. Bao R, Lai CJ, Qu H, Wang D, Yin L, Zifcak B, et al. CUDC-305, a novel synthetic HSP90 inhibitor with unique pharmacologic properties for cancer therapy. Clin Cancer Res. 2009; 15: 4046-4057. doi: 10.1158/1078-0432.CCR-09-0152 PMID: 19509149
31. Rice JW, Veal JM, Barabasz A, Foley B, Fadden P, Scott A, et al. Targeting of multiple signaling pathways by the Hsp90 inhibitor SNX-2112 in EGFR resistance models as a single agent or in combination with erlotinib. Oncol Res. 2009; 18: 229-242. PMID: 20225761
32. Ueno T, Tsukuda K, Toyooka S, Ando M, Takaoka M, Soh J, et al. Strong anti-tumor effect of NVPAUY922, a novel Hsp90 inhibitor, on non-small cell lung cancer. Lung Cancer. 2012; 76: 26-31. doi: 10.1016/j.lungcan.2011.09.011 PMID: 21996088
33. Koizumi H, Yamada T, Takeuchi S, Nakagawa T, Kita K, Nakamura T, et al. Hsp90 inhibition overcomes HGF-triggering resistance to EGFR-TKIs in EGFR-mutant lung cancer by decreasing client protein expression and angiogenesis. J Thorac Oncol. 2012; 7: 1078-1085. doi: 10.1097/JTO.0b013e3182519a2c PMID: 22592212
34. Xu L, Kikuchi E, Xu C, Ebi H, Ercan D, Cheng KA, et al. Combined EGFR/MET or EGFR/HSP90 inhibition is effective in the treatment of lung cancers codriven by mutant EGFR containing T790M and MET. Cancer Res. 2012; 72: 3302-3311. doi: 10.1158/0008-5472.CAN-11-3720 PMID: 22552292
35. Krishnamoorthy GP, Guida T, Alfano L, Avilla E, Santoro M, Carlomagno F, et al. Molecular mechanism of 17-allylamino-17-demethoxygeldanamycin (17-AAG)-induced AXL receptor tyrosine kinase degradation. J Biol Chem. 2013; 288: 17481-17494. doi: 10.1074/jbc.M112.439422 PMID: 23629654
36. Grugan KD, Miller CG, Yao Y, Michaylira CZ, Ohashi S, Klein-Szanto AJ, et al. Fibroblast-secreted hepatocyte growth factor plays a functional role in esophageal squamous cell carcinoma invasion. Proc Natl Acad Sci U S A. 2010; 107: 11026-11031. doi: 10.1073/pnas.0914295107 PMID: 20534479
37. Masuya D, Huang C, Liu D, Nakashima T, Kameyama K, Haba R, et al. The tumour-stromal interaction between intratumoral c-Met and stromal hepatocyte growth factor associated with tumour growth and prognosis in non-small-cell lung cancer patients. Br J Cancer. 2004; 90: 1555-1562. PMID: 15083185
38. Birchmeier C, Birchmeier W, Gherardi E, Vande Woude GF. Met, metastasis, motility and more. Nat Rev Mol Cell Biol. 2003; 4: 915-925. PMID: 14685170
39. Wu W, Bi C, Credille KM, Manro JR, Peek VL, Donoho GP, et al. Inhibition of tumor growth and metastasis in non-small cell lung cancer by LY2801653, an inhibitor of several oncokinases, including MET. Clin Cancer Res. 2013; 19: 5699-5710. doi: 10.1158/1078-0432.CCR-13-1758 PMID: 23989980