Acquired resistance of non-small cell lung cancer to epidermal growth factor receptor tyrosine kinase inhibitors

Respiratory Investigation

Volumn 52, Issue 2, 2014, Pages 82-91

  Nurwidya, Fariz ^a   Takahashi, Fumiyuki ^a   Murakami, Akiko ^a   Kobayashi, Isao ^a   Kato, Motoyasu ^a   Shukuya, Takehito ^a   Tajima, Ken ^a   Shimada, Naoko ^a   Takahashi, Kazuhisa ^a  

^a JUNTENDO UNIVERSITY GRADUATE SCHOOL OF MEDICINE   (Japan)

Author keywords

Acquired resistance; Epidermal growth factor receptor (EGFR); Non small cell lung cancer (NSCLC); Tyrosine kinase inhibitors

Indexed keywords

3 BROMO 5 TERT BUTYL 4 HYDROXYBENZYLIDENEMALONONITRILE; AEW 541; AFATINIB; ANTINEOPLASTIC AGENT; B RAF KINASE; BETA1 INTEGRIN; BMS 536924; BREAST CANCER RESISTANCE PROTEIN; CETUXIMAB; DACOMITINIB; EPIDERMAL GROWTH FACTOR RECEPTOR 2; EPIDERMAL GROWTH FACTOR RECEPTOR 3; EPIDERMAL GROWTH FACTOR RECEPTOR KINASE INHIBITOR; ERLOTINIB; GEFITINIB; GOLVATINIB; MEVINOLIN; MIDOSTAURIN; N (3 CHLOROPHENYL) 3 [3,5 DIMETHYL 4 (4 METHYL 1 PIPERAZINYLCARBONYL) 1H PYRROL 2 YLMETHYLENE] 2,3 DIHYDRO N METHYL 2 OXO 1H INDOLE 5 SULFONAMIDE; PHOSPHATIDYLINOSITOL 3,4,5 TRISPHOSPHATE 3 PHOSPHATASE; PROTEIN TYROSINE KINASE; SCATTER FACTOR; SCATTER FACTOR RECEPTOR; SGI 7079; SOMATOMEDIN C RECEPTOR; T 790M; TAK 701; UNCLASSIFIED DRUG; WZ 4002; YW 3276S2; EPIDERMAL GROWTH FACTOR RECEPTOR; PROTEIN KINASE INHIBITOR; PTEN PROTEIN, HUMAN; QUINAZOLINE DERIVATIVE; ADENOSINE TRIPHOSPHATE; CELL PROTEIN; EPITHELIAL MARKER PROTEIN 1; INDOLOCARBAZOLE;

ANGIOGENESIS; APOPTOSIS; BINDING AFFINITY; BINDING SITE; CANCER RECURRENCE; CANCER RESISTANCE; CELL MIGRATION; CELL PROLIFERATION; DOWN REGULATION; DRUG EFFICACY; DRUG POTENCY; DRUG SAFETY; EPITHELIAL MESENCHYMAL TRANSITION; ETHNICITY; GENE ACTIVATION; GENE AMPLIFICATION; GENE MUTATION; GENE OVEREXPRESSION; HUMAN; IN VITRO STUDY; IN VIVO STUDY; LUNG NON SMALL CELL CANCER; MOLECULAR DYNAMICS; POINT MUTATION; PROGRESSION FREE SURVIVAL; PROTEIN BINDING; PROTEIN EXPRESSION; PROTEIN PHOSPHORYLATION; QUALITY OF LIFE; REVIEW; SIGNAL TRANSDUCTION; ANTAGONISTS AND INHIBITORS; CARCINOMA, NON-SMALL-CELL LUNG; DRUG RESISTANCE; GENETICS; LUNG NEOPLASMS; MOLECULARLY TARGETED THERAPY; MUTATION; PATHOLOGY; ANTINEOPLASTIC ACTIVITY; BRAF GENE; CANCER CELL; CELL SURVIVAL; DRUG CYTOTOXICITY; DRUG MECHANISM; DRUG RESPONSE; DRUG TOLERABILITY; EGFR GENE; ENZYME INHIBITION; EXON; GENE; GENE DELETION; GENE EXPRESSION PROFILING; GENE FREQUENCY; GENOTYPE; GROWTH INHIBITION; HER2 GENE; MET GENE; MISSENSE MUTATION; NON SMALL CELL LUNG CANCER; ONCOGENE K RAS; PHASE 2 CLINICAL TRIAL (TOPIC); PHASE 3 CLINICAL TRIAL (TOPIC); RANDOMIZED CONTROLLED TRIAL (TOPIC); TREATMENT DURATION; TREATMENT OUTCOME;

ANTINEOPLASTIC AGENTS; CARCINOMA, NON-SMALL-CELL LUNG; DRUG RESISTANCE, NEOPLASM; EPITHELIAL-MESENCHYMAL TRANSITION; HEPATOCYTE GROWTH FACTOR; HUMANS; LUNG NEOPLASMS; MOLECULAR TARGETED THERAPY; MUTATION; PROTEIN KINASE INHIBITORS; PROTEIN-TYROSINE KINASES; PTEN PHOSPHOHYDROLASE; QUINAZOLINES; RECEPTOR, EPIDERMAL GROWTH FACTOR; SIGNAL TRANSDUCTION;

EID: 84896047823     PISSN: 22125345     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.resinv.2013.07.007     Document Type: Review

References (113)

1. Gschwind A, Fischer OM, Ullrich A. The discovery of receptor kinases: targets for cancer therapy. Nat Rev Cancer 2004, 4:361-370.
2. Cadena DL, Gill GN. Receptor tyrosine kinases. FASEB J 1992, 6:2332-2337.
3. Mitsudomi T, Yatabe Y. Mutations of the epidermal growth factor receptor gene and related genes as determinants of epidermal growth factor receptor tyrosine kinase inhibitors sensitivity in lung cancer. Cancer Sci 2007, 98:1817-1824.
4. Camp ER, Summy J, Bauer TW, et al. Molecular mechanisms of resistance to therapies targeting the epidermal growth factor receptor epidermal growth factor receptor. Clin Cancer Res 2005, 11:397-405.
5. Wilson KJ, Gilmore JL, Foley J, et al. Functional selectivity of EGF family peptide growth factors: implications for cancer. Pharmacol Ther 2009, 122:1-8.
6. Li Y, Macdonald-Obermann J, Westfall C, et al. Quantitation of the effect of ErbB2 on EGF receptor binding and dimerization. J Biol Chem 2012, 287:31116-31125.
7. Kumar A, Petri ET, Halmos B, et al. Structure and clinical relevance of the epidermal growth factor receptor in human cancer. J Clin Oncol 2008, 26:1742-1751.
8. Gridelli C, De Marinis F, Di Maio M, et al. Gefitinib as first-line treatment for patients with advanced non-small-cell lung cancer with activating epidermal growth factor receptor mutation: review of the evidence. Lung Cancer 2011, 71:249-257.
9. Sun S, Schiller JH, Gazdar AF. Lung cancer in never smokers-a different disease. Nat Rev Cancer 2007, 7:778-790.
10. Engelman JA, Cantley LC. The role of the ErbB family members in non-small cell lung cancers sensitive to epidermal growth factor receptor kinase inhibitors. Clin Cancer Res 2006, 12:4372s-4376s.
11. Fujimoto N, Wislez M, Zhang J, et al. High expression of ErbB family members and their ligands in lung adenocarcinomas that are sensitive to inhibition of epidermal growth factor receptor. Cancer Res 2005, 65:11478-11485.
12. Hynes NE, Lane HA. ERBB receptors and cancer: the complexity of targeted inhibitors. Nat Rev Cancer 2005, 5:341-354.
13. Sharma S V, Bell DW, Settleman J, et al. Epidermal growth factor receptor mutations in lung cancer. Nat Rev Cancer 2007, 7:169-181.
14. Nakamura Y, Sano K, Soda H, et al. Pharmacokinetics of gefitinib predicts antitumor activity in non-small cell lung cancer. J Thorac Oncol 2010, 5:1404-1409.
15. Mitsudomi T. Advances in target therapy for lung cancer. Jpn J Clin Oncol 2010, 40:101-106.
16. Yano S, Takeuchi S, Nakagawa T, et al. Ligand-triggered resistance to molecular targeted drugs in lung cancer: roles of HGF and EGFR ligands. Cancer Sci 2012, 103:1189-1194.
17. Sordella R, Bell DW, Haber DA, et al. Gefitinib-sensitizing EGFR mutations in lung cancer activate anti-apoptotic pathways. Science 2004, 305:1163-1167.
18. Miller VA, Kris MG, Shah N, et al. Bronchioloalveolar pathologic subtype and smoking history predict sensitivity to gefitinib in advanced non-small-cell lung cancer. J Clin Oncol 2004, 22:1103-1109.
19. Herbst RS, Heymach J V, Lippman SM. Lung cancer. N Engl J Med 2008, 359:1367-1380.
20. Kobayashi S, Boggon TJ, Dayaram T, et al. EGFR mutation and resistance of non-small-cell lung cancer to gefitinib. N Engl J Med 2005, 352:786-792.
21. Inoue A, Suzuki T, Fukuhara T, et al. Prospective phase II study of gefitinib for chemotherapy-naive patients with advanced non-small-cell lung cancer with epidermal growth factor receptor gene mutations. J Clin Oncol 2006, 24:3340-3346.
22. Shigematsu H, Gazdar AF. Somatic mutations of epidermal growth factor receptor signaling pathway in lung cancers. Int J Cancer 2006, 118:257-262.
23. Gazdar AF. Activating and resistance mutations of EGFR in non-small-cell lung cancer: role in clinical response to EGFR tyrosine kinase inhibitors. Oncogene 2009, 28:S24-S31.
24. Pao W, Miller VA, Politi KA, 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, 2:225-235.
25. Hirsch FR, Varella-Garcia M, Bunn PA, et al. Molecular predictors of outcome with gefitinib in a phase III placebo-controlled study in advanced non-small-cell lung cancer. J Clin Oncol 2006, 24:5034-5042.
26. Bell DW, Lynch TJ, Haserlat SM, et al. Epidermal growth factor receptor mutations and gene amplification in non-small-cell lung cancer: molecular analysis of the IDEAL/INTACT gefitinib trials. J Clin Oncol 2005, 23:8081-8092.
27. Fukuoka M, Yano S, Giaccone G, et al. Multi-institutional randomized phase II trial of gefitinib for previously treated patients with advanced non-small-cell lung cancer. J Clin Oncol 2003, 21:2237-2246.
28. Pao W, Wang TY, Riely GJ, et al. KRAS mutations and primary resistance of lung adenocarcinomas to gefitinib or erlotinib. PLoS Med 2005, 2:57-61.
29. Okamoto K, Okamoto I, Okamoto W, et al. Role of survivin in EGFR inhibitor-induced apoptosis in non-small cell lung cancers positive for EGFR mutations. Cancer Res 2010, 70:10402-10410.
30. Cappuzzo F, Varella-Garcia M, Shigematsu H, et al. Increased HER2 gene copy number is associated with response to gefitinib therapy in epidermal growth factor receptor-positive non-small-cell lung cancer patients. J Clin Oncol 2005, 23:5007-5018.
31. Oxnard GR, Janjigian YY, Arcila ME, et al. Maintained sensitivity to EGFR tyrosine kinase inhibitors in EGFR-mutant lung cancer recurring after adjuvant erlotinib or gefitinib. Clin Cancer Res 2011, 17:6322-6328.
32. Cappuzzo F, Jänne PA, Skokan M, et al. MET increased gene copy number and primary resistance to gefitinib therapy in non-small-cell lung cancer patients. Ann Oncol 2009, 20:298-304.
33. Jackman D, Pao W, Riely GJ, et al. Clinical definition of acquired resistance to epidermal growth factor receptor tyrosine kinase inhibitors in non-small cell lung cancer. J Clin Oncol 2010, 28:357-360.
34. Suda K, Murakami I, Katayama T, et al. Reciprocal and complementary role of MET amplification and EGFR T790M mutation in acquired resistance to kinase inhibitors in lung cancer. Clin Cancer Res 2010, 16:5489-5498.
35. Yun C-H, Mengwasser KE, Toms AV, et al. The T790M mutation in EGFR kinase causes drug resistance by increasing the affinity for ATP. Proc Natl Acad Sci USA 2008, 105:2070-2075.
36. Kwak EL, Sordella R, Bell DW, et al. Irreversible inhibitors of the EGF receptor may circumvent acquired resistance to gefitinib. Proc Natl Acad Sci USA 2005, 102:7665-7670.
37. Inukai M, Toyooka S, Ito S, et al. Presence of epidermal growth factor receptor gene T790M mutation as a minor clone in non-small cell lung cancer. Cancer Res 2006, 66:7854-7858.
38. Kubo T, Yamamoto H, Lockwood WW, et al. MET gene amplification or EGFR mutation activate MET in lung cancers untreated with EGFR tyrosine kinase inhibitors. Int J Cancer 2009, 124:1778-1784.
39. Xu L, Nilsson M, Saintigny P, et al. Epidermal growth factor receptor regulates MET levels and invasiveness through hypoxia-inducible factor-1alpha in non-small cell lung cancer cells. Oncogene 2010, 29:2616-2627.
40. Bean J, Brennan C, Shih J-Y, et al. MET amplification occurs with or without T790M mutations in EGFR mutant lung tumors with acquired resistance to gefitinib or erlotinib. Proc Nat Acad Sci USA 2007, 104:20932-20937.
41. Ma PC, Jagadeeswaran R, Jagadeesh S, et al. Functional expression and mutations of c-Met and its therapeutic inhibition with SU11274 and small interfering RNA in non-small cell lung cancer. Cancer Res 2005, 65:1479-1488.
42. Yano S, Wang W, Li Q, et al. Hepatocyte growth factor induces gefitinib resistance of lung adenocarcinoma with epidermal growth factor receptor-activating mutations. Cancer Res 2008, 68:9479-9487.
43. Turke AB, Zejnullahu K, Wu Y-L, et al. Preexistence and clonal selection of MET amplification in EGFR mutant NSCLC. Cancer Cell 2010, 17:77-88.
44. Ono M, Kuwano M. Molecular mechanisms of epidermal growth factor receptor (EGFR) activation and response to gefitinib and other EGFR-targeting drugs. Clin Cancer Res 2006, 12:7242-7251.
45. Baselga J, Swain SM. Novel anticancer targets: revisiting ERBB2 and discovering ERBB3. Nat Rev Cancer 2009, 9:463-475.
46. Erjala K, Sundvall M, Junttila TT, et al. Signaling via ErbB2 and ErbB3 associates with resistance and epidermal growth factor receptor (EGFR) amplification with sensitivity to EGFR inhibitor gefitinib in head and neck squamous cell carcinoma cells. Clin Cancer Res 2006, 12:4103-4111.
47. Engelman JA, Zejnullahu K, Mitsudomi T, et al. MET amplification leads to gefitinib resistance in lung cancer by activating ERBB3 signaling. Science 2007, 316:1039-1043.
48. Schoeberl B, Faber AC, Li D, et al. An ErbB3 antibody, MM-121, is active in cancers with ligand-dependent activation. Cancer Res 2010, 70:2485-2494.
49. Riedemann J, Macaulay VM. IGF1R signalling and its inhibition. Endocrine Related Cancer 2006, 13:S33-S43.
50. Xu Y, Liu H, Chen J, et al. Acquired resistance of lung adenocarcinoma to EGFR-tyrosine kinase inhibitors gefitinib and erlotinib. Cancer Bio Ther 2010, 9:572-582.
51. Hewish M, Chau I, Cunningham D. Insulin-like growth factor 1 receptor targeted therapeutics: novel compounds and novel treatment strategies for cancer medicine. Recent Patents Anti-cancer Drug Discover 2009, 4:54-72.
52. Guix M, Faber AC, Wang SE, et al. Acquired resistance to EGFR tyrosine kinase inhibitors in cancer cells is mediated by loss of IGF-binding proteins. J Clin Invest 2008, 118:23-26.
53. Qi HW, Shen Z, Fan LH. Combined inhibition of insulin-like growth factor-1 receptor enhances the effects of gefitinib in a human non-small cell lung cancer resistant cell line. Exp Ther Med 2011, 2:1091-1095.
54. Takezawa K, Pirazzoli V, Arcila ME, et al. HER2 amplification: a potential mechanism of acquired resistance to EGFR inhibition in EGFR-mutant lung cancers that lack the second-site EGFR T790M mutation. Cancer Discov 2012, 2:922-933.
55. Paik PK, Arcila ME, Fara M, et al. Clinical characteristics of patients with lung adenocarcinomas harboring BRAF mutations. J Clin Oncol 2011, 29:2046-2051.
56. Ohashi K, Sequist L V, Arcila ME, et al. Lung cancers with acquired resistance to EGFR inhibitors occasionally harbor BRAF gene mutations but lack mutations in KRAS, NRAS, or MEK1. Proc Nat Acad Sci USA 2012, 109:E2127-E2133.
57. Chow LML, Baker SJ. PTEN function in normal and neoplastic growth. Cancer Lett 2006, 241:184-196.
58. Yamamoto C, Basaki Y, Kawahara A, et al. Loss of PTEN expression by blocking nuclear translocation of EGR1 in gefitinib-resistant lung cancer cells harboring epidermal growth factor receptor-activating mutations. Cancer Res 2010, 70:8715-8725.
59. Wu Z, Gioeli D, Conaway M, et al. Restoration of PTEN expression alters the sensitivity of prostate cancer cells to EGFR inhibitors. Prostate 2008, 68:935-944.
60. Endoh H, Yatabe Y, Kosaka T, et al. PTEN and PIK3CA expression is associated with prolonged survival after gefitinib treatment in EGFR-mutated lung. J Thorac Oncol 2006, 1:629-634.
61. Frederick BA, Helfrich BA, Coldren CD, et al. Epithelial to mesenchymal transition predicts gefitinib resistance in cell lines of head and neck squamous cell carcinoma and non-small cell lung carcinoma. Mol Cancer Ther 2007, 6:1683-1691.
62. Witta SE, Gemmill RM, Hirsch FR, et al. Restoring E-cadherin expression increases sensitivity to epidermal growth factor receptor inhibitors in lung cancer cell lines. Cancer Res 2006, 66:944-950.
63. Barr S, Thomson S, Buck E, et al. Bypassing cellular EGF receptor dependence through epithelial-to-mesenchymal-like transitions. Clin Exp Metastasis 2008, 25:685-693.
64. Voulgari A, Pintzas A. Epithelial-mesenchymal transition in cancer metastasis: mechanisms, markers and strategies to overcome drug resistance in the clinic. Biochim Biophys Acta 2009, 1796:75-90.
65. Elkind NB, Szentpétery Z, Apáti A, et al. Multidrug transporter ABCG2 prevents tumor cell death induced by the epidermal growth factor receptor inhibitor Iressa (ZD1839, Gefitinib). Cancer Res 2005, 65:1770-1777.
66. Li J, Cusatis G, Brahmer J, et al. Association of variant ABCG2 and the pharmacokinetics of epidermal growth factor receptor tyrosine kinase inhibitors in cancer patients. Cancer Biol Ther 2007, 6:432-438.
67. Nakamura Y, Oka M, Soda H, et al. Gefitinib ("Iressa", ZD1839), an epidermal growth factor receptor tyrosine kinase inhibitor, reverses breast cancer resistance protein/ABCG2-mediated drug resistance. Cancer Res 2005, 65:1541-1546.
68. Lemos C, Kathmann I, Giovannetti E, et al. Impact of cellular folate status and epidermal growth factor receptor expression on BCRP/ABCG2-mediated resistance to gefitinib and erlotinib. Br J Cancer 2009, 100:1120-1127.
69. Usuda J, Ohira T, Suga Y, et al. Breast cancer resistance protein (BCRP) affected acquired resistance to gefitinib in a never-smoked female patient with advanced non-small cell lung cancer. Lung Cancer 2007, 58:296-299.
70. Gottschling S, Herpel E, Eberhardt WEE., et al. The gefitinib long-term responder (LTR)-a cancer stem-like cell story? Insights from molecular analyses of German long-term responders treated in the IRESSA expanded access program (EAP). Lung Cancer 2012, 77:183-191.
71. Eke I, Deuse Y, Hehlgans S, et al. β1 integrin/FAK/cortactin signaling is essential for human head and neck cancer resistance to radiotherapy. J Clin Invest 2012, 122:1529-1540.
72. Ju L, Zhou C, Li W, et al. Integrin beta1 over-expression associates with resistance to tyrosine kinase inhibitor gefitinib in non-small cell lung cancer. J Cell Biochem 2010, 111:1565-1574.
73. Morello V, Cabodi S, Sigismund S, et al. β1 integrin controls EGFR signaling and tumorigenic properties of lung cancer cells. Oncogene 2011, 30:4087-4096.
74. Jain A, Tindell CA, Laux I, et al. Epithelial membrane protein-1 is a biomarker of gefitinib resistance. Proc Natl Acad Sci USA 2005, 102:11858-11863.
75. Mink SR, Vashistha S, Zhang W. Cancer-associated fibroblasts derived from EGFR-TKI-resistant tumors reverse EGFR pathway inhibition by EGFR-TKIs. Mol Cancer Res 2010, 8:809-820.
76. Li Y, Ye X, Tan C, et al. Axl as a potential therapeutic target in cancer: role of Axl in tumor growth, metastasis and angiogenesis. Oncogene 2009, 28:3442-3455.
77. Linger R, Cohen R, Cummings C, et al. Mer or Axl receptor tyrosine kinase inhibition promotes apoptosis, blocks growth and enhances chemosensitivity of human non-small cell lung cancer. Oncogene 2013, 32:3420-3431.
78. Zhang Z, Lee JC, Lin L, et al. Activation of the AXL kinase causes resistance to EGFR-targeted therapy in lung cancer. Nat Genet 2012, 44:852-860.
79. Byers LA, Diao L, Wang J, et al. An epithelial-mesenchymal transition (EMT) gene signature predicts resistance to EGFR and PI3K inhibitors and identifies Axl as a therapeutic target for overcoming EGFR inhibitor resistance. Clin Cancer Res 2012, 19:279-290.
80. Sequist LV, Waltman BA, Dias-Santagata D, et al. Genotypic and histological evolution of lung cancers acquiring resistance to EGFR inhibitors. Sci Transl Med 2011, 3:75ra26.
81. Yu HA, Arcila ME, Rekhtman N, et al. Analysis of tumor specimens at the time of acquired resistance to EGFR-TKI therapy in 155 patients with EGFR-Mutant lung cancers. Clin Cancer Res 2013, 19:2240-2247.
82. Popat S, Wotherspoon A, Nutting C., et al. Transformation to high grade neuroendocrine carcinoma as an acquired drug resistance mechanism in EGFR-mutant lung adenocarcinoma. Lung Cancer 2013, 80:1-4.
83. Pao W, Chmielecki J. Rational, biologically based treatment of EGFR-mutant non-small-cell lung cancer. Nat Rev Cancer 2010, 10:760-774.
84. Hammerman PS, Jänne PA, Johnson BE. Resistance to epidermal growth factor receptor tyrosine kinase inhibitors in non-small cell lung cancer. Clin Cancer Res 2009, 15:7502-7509.
85. Engelman JA, Jänne PA. Mechanisms of acquired resistance to epidermal growth factor receptor tyrosine kinase inhibitors in non-small cell lung cancer. Clin Cancer Res 2008, 14:2895-2899.
86. Yu Z, Boggon TJ, Kobayashi S, et al. Resistance to an irreversible epidermal growth factor receptor (EGFR) inhibitor in EGFR-mutant lung cancer reveals novel treatment strategies. Cancer Res 2007, 67:10417-10427.
87. Kim Y, Ko J, Cui Z, et al. The EGFR T790M mutation in acquired resistance to an irreversible second-generation EGFR inhibitor. Mol Cancer Ther 2012, 11:784-791.
88. Regales L, Gong Y, Shen R, et al. Dual targeting of EGFR can overcome a major drug resistance mutation in mouse models of EGFR mutant lung cancer. J Clin Invest 2009, 119:3000-3010.
89. Miller VA, Hirsh V, Cadranel J, et al. Afatinib versus placebo for patients with advanced, metastatic non-small-cell lung cancer after failure of erlotinib, gefitinib, or both, and one or two lines of chemotherapy (LUX-Lung 1): a phase 2b/3 randomised trial. Lancet Oncol 2012, 13:528-538.
90. Hirsh V, Cadranel J, Cong XJ, et al. Symptom and quality of life benefit of afatinib in advanced non-small-cell lung cancer patients previously treated with erlotinib or gefitinib: results of a randomized phase IIb/III trial (LUX-Lung 1). J Thorac Oncol 2013, 8:229-237.
91. Wu J, Yang C, Hsu Y, et al. Use of cetuximab after failure of gefitinib in patients with advanced non-small-cell lung cancer. Clin Lung Cancer 2010, 11:257-263.
92. Lee H-J, Schaefer G, Heffron TP, et al. Noncovalent wild-type-sparing inhibitors of EGFR T790M. Cancer Discov 2013, 3:168-181.
93. Engelman JA, Zejnullahu K, Gale C-M, 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.
94. Gonzales AJ, Hook KE, Althaus IW, et al. Antitumor activity and pharmacokinetic properties of PF-00299804, a second-generation irreversible pan-erbB receptor tyrosine kinase inhibitor. Mol Cancer Ther 2008, 7:1880-1889.
95. Ercan D, Zejnullahu K, Yonesaka K, et al. Amplification of EGFR T790M causes resistance to an irreversible EGFR inhibitor. Oncogene 2010, 29:2346-2356.
96. Zhou W, Ercan D, Chen L, et al. Novel mutant-selective EGFR kinase inhibitors against EGFR T790M. Nature 2009, 462:1070-1074.
97. Nakagawa T, Takeuchi S, Yamada T, et al. Combined therapy with mutant-selective EGFR inhibitor and Met kinase inhibitor for overcoming erlotinib resistance in EGFR-mutant lung cancer. Mol Cancer Ther 2012, 11:2149-2157.
98. Karamouzis MV, Konstantinopoulos PA, Papavassiliou AG. Targeting MET as a strategy to overcome crosstalk-related resistance to EGFR inhibitors. Lancet Oncol 2009, 10:709-717.
99. Comoglio PM, Giordano S, Trusolino L. Drug development of MET inhibitors: targeting oncogene addiction and expedience. Nature Rev Drug Discov 2008, 7:504-516.
100. Tang Z, Du R, Jiang S, et al. Dual MET-EGFR combinatorial inhibition against T790M-EGFR-mediated erlotinib-resistant lung cancer. British J Cancer 2008, 99:911-922.
101. Takeuchi S, Wang W, Li Q, et al. Dual inhibition of Met kinase and angiogenesis to overcome HGF-induced EGFR-TKI resistance in EGFR mutant lung cancer. Am J Pathol 2012, 181:1034-1043.
102. Wang W, Li Q, Takeuchi S, et al. Met kinase inhibitor E7050 reverses three different mechanisms of hepatocyte growth factor-induced tyrosine kinase inhibitor resistance in EGFR mutant lung cancer. Clin Cancer Res 2012, 18:1663-1671.
103. Choi YJ, Rho JK, Jeon B, et al. Combined inhibition of IGFR enhances the effects of gefitinib in H1650: a lung cancer cell line with EGFR mutation and primary resistance to EGFR-TK inhibitors. Cancer Chemother Pharmacol 2010, 66:381-388.
104. Jones HE, Goddard L, Gee JMW, et al. Insulin-like growth factor-I receptor signalling and acquired resistance to gefitinib (ZD1839; Iressa) in human breast and prostate cancer cells. Endocrine-Related Cancer 2004, 11:793-814.
105. Camirand A, Zakikhani M, Young F, et al. Inhibition of insulin-like growth factor-1 receptor signaling enhances growth-inhibitory and proapoptotic effects of gefitinib (Iressa) in human breast cancer cells. Breast Cancer Res 2005, 7:R570-R579.
106. Hurbin A, Wislez M, Busser B, et al. Insulin-like growth factor-1 receptor inhibition overcomes gefitinib resistance in mucinous lung adenocarcinoma. J Pathol 2011, 225:83-95.
107. Sharma S V, Lee DY, Li B, et al. A chromatin-mediated reversible drug-tolerant state in cancer cell subpopulations. Cell 2010, 141:69-80.
108. Cortot AB, Repellin CE, Shimamura T, et al. Resistance to irreversible EGF receptor tyrosine kinase inhibitors through a multistep mechanism involving the IGF1R pathway. Cancer Res 2013, 73:834-843.
109. Moreira-Leite FF, Harrison LR, Mironov A, et al. Inducible EGFR T790M-mediated gefitinib resistance in non-small cell lung cancer cells does not modulate sensitivity to PI103 provoked autophagy. J Thorac Oncol 2010, 5:765-777.
110. Okamoto W, Okamoto I, Tanaka K, et al. TAK-701, a humanized monoclonal antibody to hepatocyte growth factor, reverses gefitinib resistance induced by tumor-derived HGF in non-small cell lung cancer with an EGFR mutation. Mol Cancer Ther 2010, 9:2785-2792.
111. Ye X, Li Y, Stawicki S, et al. An anti-Axl monoclonal antibody attenuates xenograft tumor growth and enhances the effect of multiple anticancer therapies. Oncogene 2010, 29:5254-5264.
112. Park IH, Kim JY, Jung JI, et al. Lovastatin overcomes gefitinib resistance in human non-small cell lung cancer cells with K-Ras mutations. Investig New Drugs 2010, 28:791-799.
113. Zhang Z, Stiegler AL, Boggon TJ, et al. EGFR-mutated lung cancer: a paradigm of molecular oncology. Oncotarget 2010, 1:497-514.