EGFR mutations in lung cancer: From tissue testing to liquid biopsy

Future Oncology

Volumn 11, Issue 11, 2015, Pages 1611-1623

  Fenizia, Francesca ^a   De Luca, Antonella ^a   Pasquale, Raffaella ^a   Sacco, Alessandra ^a   Forgione, Laura ^a   Lambiase, Matilde ^a   Iannaccone, Alessia ^a   Chicchinelli, Nicoletta ^a   Franco, Renato ^a   Rossi, Antonio ^b   Morabito, Alessandro ^a   Rocco, Gaetano ^a   Piccirillo, Maria Carmela ^a   Normanno, Nicola ^a  

^a NATIONAL CANCER INSTITUTE   (Italy)

^b S G MOSCATI HOSPITAL   (Italy)

Author keywords

EGFR mutations; EGFR TKIs; liquid biopsy; mechanisms of resistance; non small cell lung carcinoma; targeted therapy

Indexed keywords

DNA; EPIDERMAL GROWTH FACTOR RECEPTOR; EPIDERMAL GROWTH FACTOR RECEPTOR KINASE INHIBITOR; ANTINEOPLASTIC AGENT; ERLOTINIB; GEFITINIB; PROTEIN KINASE INHIBITOR; QUINAZOLINE DERIVATIVE; TUMOR MARKER;

CANCER GENETICS; CANCER PATIENT; CANCER RESISTANCE; CIRCULATING TUMOR CELL; CYTOLOGY; GENE IDENTIFICATION; GENE MUTATION; GENOTYPE; HISTOLOGY; HUMAN; LIQUID BIOPSY; LUNG CANCER; MOLECULAR GENETICS; MOLECULARLY TARGETED THERAPY; MUTATIONAL ANALYSIS; NON SMALL CELL LUNG CANCER; OUTCOME ASSESSMENT; PERSONALIZED MEDICINE; PHASE 3 CLINICAL TRIAL (TOPIC); PRIORITY JOURNAL; RANDOMIZED CONTROLLED TRIAL (TOPIC); REVIEW; TUMOR BIOPSY; ANTAGONISTS AND INHIBITORS; BIOPSY; BLOOD; CARCINOMA, NON-SMALL-CELL LUNG; DRUG RESISTANCE; GENETICS; GENOTYPING TECHNIQUE; LUNG NEOPLASMS; MUTATION; PROCEDURES; TUMOR CELL CULTURE;

ANTINEOPLASTIC AGENTS; BIOMARKERS, TUMOR; BIOPSY; CARCINOMA, NON-SMALL-CELL LUNG; DNA, NEOPLASM; DRUG RESISTANCE, NEOPLASM; ERLOTINIB HYDROCHLORIDE; GENOTYPING TECHNIQUES; HUMANS; LUNG NEOPLASMS; MUTATION; PRECISION MEDICINE; PROTEIN KINASE INHIBITORS; QUINAZOLINES; RECEPTOR, EPIDERMAL GROWTH FACTOR; TUMOR CELLS, CULTURED;

EID: 84930607424     PISSN: 14796694     EISSN: 17448301     Source Type: Journal    
DOI: 10.2217/fon.15.23     Document Type: Review

References (75)

1. Siegel R, Ma J, Zou Z, Jemal A. Cancer statistics, 2014. CA Cancer J. Clin. 64(1), 9-29 (2014).
2. Herbst RS, Heymach JV, Lippman SM. Lung cancer. N. Engl. J. Med. 359(13), 1367-1380 (2008).
3. Li T, Kung HJ, Mack PC, Gandara DR. Genotyping and genomic profiling of non-small-cell lung cancer: implications for current and future therapies. J. Clin. Oncol. 31(8), 1039-1049 (2013).
4. Weinstein IB. Cancer. Addiction to oncogenes - the Achilles heal of cancer. Science 297(5578), 63-64 (2002).
5. De Luca A, Normanno N. Predictive biomarkers to tyrosine kinase inhibitors for the epidermal growth factor receptor in non-small-cell lung cancer. Curr. Drug Targets 11(7), 851-864 (2010).
6. Normanno N, De Luca A, Bianco C et al. Epidermal growth factor receptor (EGFR) signaling in cancer. Gene 366(1), 2-16 (2006).
7. Lynch TJ, Bell DW, Sordella R et al. Activating mutations in the epidermal growth factor receptor underlying responsiveness of non-small-cell lung cancer to gefitinib. N. Engl. J. Med. 350(21), 2129-2139 (2004).
8. Linardou H, Dahabreh IJ, Kanaloupiti D et al. Assessment of somatic k-RAS mutations as a mechanism associated with resistance to EGFR-targeted agents. a systematic review and meta-analysis of studies in advanced non-small-cell lung cancer and metastatic colorectal cancer. Lancet Oncol. 9(10), 962-972 (2008).
9. Ohashi K, Maruvka YE, Michor F, Pao W. Epidermal growth factor receptor tyrosine kinase inhibitor-resistant disease. J. Clin. Oncol. 31(8), 1070-1080 (2013).
10. Paez JG, Janne PA, Lee JC et al. EGFR mutations in lung cancer. correlation with clinical response to gefitinib therapy. Science 304(5676), 1497-1500 (2004).
11. Rossi A, Pasquale R, Esposito C, Normanno N. Should epidermal growth factor receptor tyrosine kinase inhibitors be considered ideal drugs for the treatment of selected advanced non-small cell lung cancer patients? Cancer Treat. Rev. 39(5), 489-497 (2013).
12. Mok TS, Wu YL, Thongprasert S et al. Gefitinib or carboplatin-paclitaxel in pulmonary adenocarcinoma. N. Engl. J. Med. 361(10), 947-957 (2009).
13. Han JY, Park K, Kim SW et al. First-SIGNAL. first-line single-agent iressa versus gemcitabine and cisplatin trial in neversmokers with adenocarcinoma of the lung. J. Clin. Oncol. 30(10), 1122-1128 (2012).
14. Mitsudomi T, Morita S, Yatabe Y et al. Gefitinib versus cisplatin plus docetaxel in patients with non-small-cell lung cancer harbouring mutations of the epidermal growth factor receptor (WJTOG3405): an open label, randomised Phase 3 trial. Lancet Oncol. 11(2), 121-128 (2010).
15. Maemondo M, Inoue A, Kobayashi K et al. Gefitinib or chemotherapy for non-small-cell lung cancer with mutated EGFR. N. Engl. J. Med. 362(25), 2380-2388 (2010).
16. Zhou C, Wu YL, Chen G et al. Erlotinib versus chemotherapy as first-line treatment for patients with advanced EGFR mutationpositive non-small-cell lung cancer (OPTIMAL, CTONG-0802). a multicentre, open-label, randomised, Phase 3 study. Lancet Oncol. 12(8), 735-742 (2011).
17. Rosell R, Carcereny E, Gervais R et al. Erlotinib versus standard chemotherapy as first-line treatment for European patients with advanced EGFR mutation-positive non-smallcell lung cancer (EURTAC). a multicentre, open-label, randomised Phase 3 trial. Lancet Oncol. 13(3), 239-246 (2012).
18. Wu YL, Liam CK, Zhaou C et al. First-line erlotinib versus cisplatin/gemcitabine (GP) in patients with advanced EGFR mutationpositive non-small-lung cancer (NSCLC). interim analyses from the Phase 3, open-label, ENSURE study. J. Thorac. Oncol. 8(Suppl. 2), S603-S604 (2013) (Abstract P1.11.021).
19. Sequist LV, Yang JC, Yamamoto N et al. Phase III study of afatinib or cisplatin plus pemetrexed in patients with metastatic lung adenocarcinoma with EGFR mutations. J. Clin. Oncol. 31(27), 3327-3334 (2013).
20. Wu YL, Zhou C, Hu CP et al. Afatinib versus cisplatin plus gemcitabine for first-line treatment of Asian patients with advanced non-small-cell lung cancer harbouring EGFR mutations (LUX-Lung 6). an open-label, randomised Phase 3 trial. Lancet Oncol. 15(2), 213-222 (2014).
21. Yang J, Sequist Lv, Schuler Mh et al. Overall survival in patients with advanced NSCLC harboring common (Del19/L858R) EGFR mutations: analysis of two large, open-label Phase III studies of afatinib vs chemotherapy, LUX-Lung 3 and LUX-Lung 6. J. Clin. Oncol. 32(Suppl. 5), Abstract 8004 (2014).
22. Wannesson L, Viteri S, Costa C, Karachaliou N, Molina-Vila MA, Rosell R. Signaling pathways modulating dependence of lung cancer on mutant epidermal growth factor receptor and mechanisms of intrinsic and acquired resistance to tyrosine kinase inhibitors. Curr. Pharm. Des. 20(24), 3883-3893 (2014).
23. Rosell R, Moran T, Queralt C et al. Screening for epidermal growth factor receptor mutations in lung cancer. N. Engl. J. Med. 361(10), 958-967 (2009).
24. Fukuoka M, Wu YL, Thongprasert S et al. Biomarker analyses and final overall survival results from a Phase III, randomized, open-label, first-line study of gefitinib versus carboplatin/paclitaxel in clinically selected patients with advanced non-small-cell lung cancer in Asia (IPASS). J. Clin. Oncol. 29(21), 2866-2874 (2011).
25. Bai H, Wang Z, Wang Y et al. Detection and clinical significance of intratumoral EGFR mutational heterogeneity in Chinese patients with advanced non-small cell lung cancer. PLoS ONE 8(2), e54170 (2013).
26. Yatabe Y, Matsuo K, Mitsudomi T. Heterogeneous distribution of EGFR mutations is extremely rare in lung adenocarcinoma. J. Clin. Oncol. 29(22), 2972-2977 (2011).
27. Govindan R, Ding L, Griffith M et al. Genomic landscape of non-small cell lung cancer in smokers and never-smokers. Cell 150(6), 1121-1134 (2012).
28. Chen Z, Fillmore CM, Hammerman PS, Kim CF, Wong KK. Non-small-cell lung cancers: a heterogeneous set of diseases. Nat. Rev. Cancer 14(8), 535-546 (2014).
29. Zhou Q, Zhang XC, Chen ZH et al. Relative abundance of EGFR mutations predicts benefit from gefitinib treatment for advanced non-small-cell lung cancer. J. Clin. Oncol. 29(24), 3316-3321 (2011).
30. Ono A, Kenmotsu H, Watanabe M et al. Mutant allele frequency predicts the efficacy of EGFR-TKIs in lung adenocarcinoma harboring the L858R mutation. Ann. Oncol. 25(10), 1948-1953 (2014).
31. Yuan S, Yu SL, Chen HY et al. Clustered genomic alterations in chromosome 7p dictate outcomes and targeted treatment responses of lung adenocarcinoma with EGFR-activating mutations. J. Clin. Oncol. 29(25), 3435-3442 (2011).
32. Bivona TG, Hieronymus H, Parker J et al. FAS and NF-kappaB signalling modulate dependence of lung cancers on mutant EGFR. Nature 471(7339), 523-526 (2011).
33. Rosell R, Molina MA, Costa C et al. Pretreatment EGFR T790M mutation and BRCA1 mRNA expression in erlotinib-treated advanced non-small-cell lung cancer patients with EGFR mutations. Clin. Cancer Res. 17(5), 1160-1168 (2011).
34. Kobayashi S, Boggon TJ, Dayaram T et al. EGFR mutation and resistance of non-smallcell lung cancer to gefitinib. N. Engl. J. Med. 352(8), 786-792 (2005).
35. 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. 2(3), e73 (2005).
36. Yun CH, 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 105(6), 2070-2075 (2008).
37. Sequist LV, Waltman BA, Dias-Santagata D et al. Genotypic and histological evolution of lung cancers acquiring resistance to EGFR inhibitors. Sci. Transl. Med. 3(75), 75ra26 (2011).
38. Ercan D, Xu C, Yanagita M et al. Reactivation of ERK signaling causes resistance to EGFR kinase inhibitors. Cancer Discov. 2(10), 934-947 (2012).
39. 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 EGFRT790M mutation. Cancer Discov. 2(10), 922-933 (2012).
40. Zhang Z, Lee JC, Lin L et al. Activation of the AXL kinase causes resistance to EGFR-targeted therapy in lung cancer. Nat. Genet. 44(8), 852-860 (2012).
41. 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. 19(8), 2240-2247 (2013).
42. Godin-Heymann N, Bryant I, Rivera MN et al. Oncogenic activity of epidermal growth factor receptor kinase mutant alleles is enhanced by the T790M drug resistance mutation. Cancer Res 67(15), 7319-7326 (2007).
43. Maheswaran S, Sequist LV, Nagrath S et al. Detection of mutations in EGFR in circulating lung-cancer cells. N. Engl. J. Med. 359(4), 366-377 (2008).
44. Costa C, Molina MA, Drozdowskyj A et al. The impact of EGFR T790M mutations and BIM mRNA expression on outcome in patients with EGFR-mutant NSCLC treated with erlotinib or chemotherapy in the randomized Phase III EURTAC trial. Clin. Cancer Res. 20(7), 2001-2010 (2014).
45. Su KY, Chen HY, Li KC et al. Pretreatment epidermal growth factor receptor (EGFR) T790M mutation predicts shorter EGFR tyrosine kinase inhibitor response duration in patients with non-small-cell lung cancer. J. Clin. Oncol. 30(4), 433-440 (2012).
46. Yu HA, Arcila ME, Hellmann MD, Kris MG, Ladanyi M, Riely GJ. Poor response to erlotinib in patients with tumors containing baseline EGFR T790M mutations found by routine clinical molecular testing. Ann. On-col. 25(2), 423-428 (2014).
47. Morabito A, Costanzo R, Rachiglio AM et al. Activity of gefitinib in a non-small-cell lung cancer patient with both activating and resistance EGFR mutations. J. Thorac. Oncol. 8(7), e59-60 (2013).
48. Engelman JA, Zejnullahu K, Mitsudomi T et al. MET amplification leads to gefitinib resistance in lung cancer by activating ERBB3 signaling. Science 316(5827), 1039-1043 (2007).
49. Turke AB, Zejnullahu K, Wu YL et al. Preexistence and clonal selection of MET amplification in EGFR mutant NSCLC. Cancer Cell 17(1), 77-88 (2010).
50. Ohashi K, Sequist LV, 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. Natl Acad. Sci. USA 109(31), E2127-E2133 (2012).
51. Marchetti A, Normanno N, Pinto C et al. Recommendations for mutational analysis of EGFR in lung carcinoma. Pathologica 102(3), 119-126 (2010).
52. Sequist LV, Heist RS, Shaw AT et al. Implementing multiplexed genotyping of non-small-cell lung cancers into routine clinical practice. Ann. Oncol. 22(12), 2616-2624 (2011).
53. Diaz LA Jr, Bardelli A. Liquid biopsies: genotyping circulating tumor DNA. J. Clin. Oncol. 32(6), 579-586 (2014).
54. Murtaza M, Dawson SJ, Tsui DW et al. Non-invasive analysis of acquired resistance to cancer therapy by sequencing of plasma DNA. Nature 497(7447), 108-112 (2013).
55. Goto K, Ichinose Y, Ohe Y et al. Epidermal growth factor receptor mutation status in circulating free DNA in serum. from IPASS, a Phase III study of gefitinib or carboplatin/ paclitaxel in non-small cell lung cancer. J. Thorac. Oncol. 7(1), 115-121 (2012).
56. Morabito A, Sandomenico C, Costanzo R et al. Positron emission tomography and circulating tumor cells to monitor a dramatic response to gefitinib. J. Thorac. Oncol. 7(11), e27-28 (2012).
57. Stroun M, Maurice P, Vasioukhin V et al. The origin and mechanism of circulating DNA. Ann. NY Acad. Sci. 906, 161-168 (2000).
58. Newman AM, Bratman SV, To J et al. An ultrasensitive method for quantitating circulating tumor DNA with broad patient coverage. Nat. Med. 20(5), 548-554 (2014).
59. Bettegowda C, Sausen M, Leary RJ et al. Detection of circulating tumor DNA in early- and late-stage human malignancies. Sci. Transl. Med. 6(224), 224ra224 (2014).
60. Diehl F, Li M, Dressman D et al. Detection and quantification of mutations in the plasma of patients with colorectal tumors. Proc. Natl Acad. Sci. USA 102(45), 16368-16373 (2005).
61. Forshew T, Murtaza M, Parkinson C et al. Noninvasive identification and monitoring of cancer mutations by targeted deep sequencing of plasma DNA. Sci. Transl. Med. 4(136), 136ra168 (2012).
62. Luke JJ, Oxnard GR, Paweletz CP et al. Realizing the potential of plasma genotyping in an age of genotype-directed therapies. J. Natl Cancer Inst. 106(8), (2014).
63. Luo J, Shen L, Zheng D. Diagnostic value of circulating free DNA for the detection of EGFR mutation status in NSCLC: a systematic review and meta-analysis. Sci. Rep. 4, 6269 (2014).
64. Takano T, Ohe Y, Tsuta K et al. Epidermal growth factor receptor mutation detection using high-resolution melting analysis predicts outcomes in patients with advanced non small cell lung cancer treated with gefitinib. Clin. Cancer Res. 13(18 Pt 1), 5385-5390 (2007).
65. Nagai Y, Miyazawa H, Huqun et al. Genetic heterogeneity of the epidermal growth factor receptor in non-small cell lung cancer cell lines revealed by a rapid and sensitive detection system, the peptide nucleic acid-locked nucleic acid PCR clamp. Cancer Res. 65(16), 7276-7282 (2005).
66. Zhao X, Han RB, Zhao J et al. Comparison of epidermal growth factor receptor mutation statuses in tissue and plasma in stage I-IV non-small cell lung cancer patients. Respiration 85(2), 119-125 (2013).
67. Douillard JY, Ostoros G, Cobo M et al. First-line gefitinib in Caucasian EGFR mutation-positive NSCLC patients: a Phase-IV, open-label, single-arm study. Br. J. Cancer 110(1), 55-62 (2014).
68. Douillard JY, Ostoros G, Cobo M et al. Gefitinib treatment in EGFR mutated caucasian NSCLC. circulating-free tumor DNA as a surrogate for determination of EGFR status. J. Thorac. Oncol. 9(9), 1345-1353 (2014).
69. Nakamura T, Sueoka-Aragane N, Iwanaga K et al. A noninvasive system for monitoring resistance to epidermal growth factor receptor tyrosine kinase inhibitors with plasma DNA. J. Thorac. Oncol. 6(10), 1639-1648 (2011).
70. Taniguchi K, Uchida J, Nishino K et al. Quantitative detection of EGFR mutations in circulating tumor DNA derived from lung adenocarcinomas. Clin. Cancer Res. 17(24), 7808-7815 (2011).
71. Oxnard GR, Paweletz CP, Kuang Y et al. Noninvasive detection of response and resistance in EGFR-mutant lung cancer using quantitative next-generation genotyping of cell-free plasma DNA. Clin. Cancer Res. 20(6), 1698-1705 (2014).
72. Sorensen BS, Wu L, Wei W et al. Monitoring of epidermal growth factor receptor tyrosine kinase inhibitor-sensitizing and resistance mutations in the plasma DNA of patients with advanced non-small cell lung cancer during treatment with erlotinib. Cancer 120(24), 3896-3901 (2014).
73. Janne PA, Suresh SR, Yang JCH et al. Clinical activity of the mutant-selective EGFR inhibitor AZD9291 in patients (pts) with EGFR inhibitor-resistant non-small cell lung cancer (NSCLC). J. Clin. Oncol. 32(Suppl. 5), Abstract 8009 (2014).
74. Sequist L, Soria JC, Gadgeel SM et al. First-in-human evaluation of CO-1686, an irreversible, highly selective tyrosine kinase inhibitor of mutations of EGFR (activating and T790M). J. Clin. Oncol. 32(Suppl. 5), Abstract 8010 (2014).
75. Cortot AB, Janne PA. Molecular mechanisms of resistance in epidermal growth factor receptor-mutant lung adenocarcinomas. Eur. Respir. Rev. 23(133), 356-366 (2014).