Digital PCR analysis of plasma cell-free DNA for non-invasive detection of drug resistance mechanisms in EGFR mutant NSCLC: Correlation with paired tumor samples

Oncotarget

Volumn 6, Issue 31, 2015, Pages 30850-30858

  Ishii, Hidenobu ^a   Azuma, Koichi ^a   Sakai, Kazuko ^b   Kawahara, Akihiko ^c   Yamada, Kazuhiko ^a   Tokito, Takaaki ^a   Okamoto, Isamu ^d   Nishio, Kazuto ^b   Hoshino, Tomoaki ^a  

^a KURUME UNIVERSITY SCHOOL OF MEDICINE   (Japan)

^b KINKI UNIVERSITY   (Japan)

^c KURUME UNIVERSITY HOSPITAL   (Japan)

^d KYUSHU UNIVERSITY HOSPITAL   (Japan)

Author keywords

Cell free DNA; Digital PCR; EGFR; Non small cell lung cancer; T790M mutation

Indexed keywords

CELL FREE DNA; DNA; EPIDERMAL GROWTH FACTOR RECEPTOR; EPIDERMAL GROWTH FACTOR RECEPTOR 2; EPIDERMAL GROWTH FACTOR RECEPTOR KINASE INHIBITOR; ERLOTINIB; GEFITINIB; SCATTER FACTOR RECEPTOR; UNCLASSIFIED DRUG; ANTINEOPLASTIC AGENT; EGFR PROTEIN, HUMAN; ERBB2 PROTEIN, HUMAN; MET PROTEIN, HUMAN; PROTEIN KINASE INHIBITOR; TUMOR MARKER;

ADULT; AGED; ARTICLE; CLINICAL ARTICLE; CONTROLLED STUDY; DIGITAL POLYMERASE CHAIN REACTION; EGFR GENE; FEMALE; GENE AMPLIFICATION; GENE DOSAGE; GENE MUTATION; HER2 GENE; HUMAN; HUMAN TISSUE; MALE; MET GENE; NON SMALL CELL LUNG CANCER; POLYMERASE CHAIN REACTION; RETROSPECTIVE STUDY; SENSITIVITY AND SPECIFICITY; ANTAGONISTS AND INHIBITORS; BLOOD; CARCINOMA, NON-SMALL-CELL LUNG; COPY NUMBER VARIATION; DRUG RESISTANCE; ENZYMOLOGY; EVALUATION STUDY; FEASIBILITY STUDY; GENETICS; LUNG NEOPLASMS; METABOLISM; MIDDLE AGED; MUTATION; PATHOLOGY; PREDICTIVE VALUE; PROCEDURES; REPRODUCIBILITY; TREATMENT OUTCOME; TUMOR RECURRENCE; VERY ELDERLY;

AGED; AGED, 80 AND OVER; ANTINEOPLASTIC AGENTS; BIOMARKERS, TUMOR; CARCINOMA, NON-SMALL-CELL LUNG; DNA COPY NUMBER VARIATIONS; DNA, NEOPLASM; DRUG RESISTANCE, NEOPLASM; FEASIBILITY STUDIES; FEMALE; GENE AMPLIFICATION; GENE DOSAGE; HUMANS; LUNG NEOPLASMS; MALE; MIDDLE AGED; MUTATION; NEOPLASM RECURRENCE, LOCAL; POLYMERASE CHAIN REACTION; PREDICTIVE VALUE OF TESTS; PROTEIN KINASE INHIBITORS; PROTO-ONCOGENE PROTEINS C-MET; RECEPTOR, EPIDERMAL GROWTH FACTOR; RECEPTOR, ERBB-2; REPRODUCIBILITY OF RESULTS; RETROSPECTIVE STUDIES; TREATMENT OUTCOME;

EID: 84945549891     PISSN: None     EISSN: 19492553     Source Type: Journal    
DOI: 10.18632/oncotarget.5068     Document Type: Article

References (44)

1. Siegel R, Naishadham D, Jemal A. Cancer statics. CA Cancer J Clin. 2012; 62:10-29.
2. Mok TS, Wu YL, Thongprasert S, Yang CH, Chu DT, Saijo N, Sunpaweravong P, Han B, Margono B, Ichinose Y, Nishiwaki Y, Ohe Y, Yang JJ, et al. Gefitinib or carboplatin-paclitaxel in pulmonary adenocarcinoma. N Engl J Med. 2009; 361:947-957.
3. Maemondo M, Inoue A, Kobayashi K, Sugawara S, Oizumi S, Isobe H, Gemma A, Harada M, Yoshizawa H, Kinoshita I, Fujita Y, Okinaga S, Hirano H, et al. Gefitinib or chemotherapy for non-small-cell lung cancer with mutated EGFR. N Engl J Med. 2010; 362:2380-2388.
4. Mitsudomi T, Morita S, Yatabe Y, Negoro S, Okamoto I, Tsurutani J, Seto T, Satouchi M, Tada H, Hirashima T, Asami K, Katakami N, Takada M, et al. Gefitinib versus cisplatin plus docetaxel in patients with non-small-cell lung cancer harboring mutations of the epidermal growth factor receptor (WJTOG3405): an open label, randomized phase 3 trial. Lancet Oncol. 2010; 11:121-128.
5. Zhou C, Wu YL, Chen G, Feng J, Liu XQ, Wang C, Zhang S, Wang J, Zhou S, Ren S, Lu S, Zhang L, Hu C, et al. Erlotinib versus chemotherapy as first-line treatment for patients with advanced EGFR mutation-positive non-small-cell lung cancer (OPTIMAL, CTONG-0802): a multicenter, openlabel, randomized, phase 3 study. Lancet Oncol. 2011; 12:735-742.
6. Rosell R, Carcereny E, Gervais R, Vergnenegre A, Massuti B, Felip E, Palmero R, Garcia-Gomez R, Pallares C, Sanchez JM, Porta R, Cobo M, Garrido P, et al. Erlotinib versus chemotherapy as first-line treatment for patients with advanced EGFR mutation-positive non-smallcell lung cancer (EURTAC): a multicenter, open-label, randomized, phase 3 trial. Lancet Oncol. 2012; 13:239-246.
7. Sequist LV, Yang JC, Yamamoto N, O'Byrne K, Hirsh V, Mok T, Geater SL, Orlov S, Tsai CM, Boyer M, Su WC, Bennouna J, Kato T, et al. Phase III study of afatinib or cisplatin plus pemetrexed in patients with metastatic lung adenocarcinoma with EGFR mutations. J Clin Oncol. 2013; 31:3327-3334.
8. Sequist LV, Waltman BA, Dias-Santagata D, Digumarthy S, Turke AB, Fidias P, Bergethon K, Shaw AT, Gettinger S, Cosper AK, Akhavanfard S, Heist RS, Temel J, et al. Genotypic and histological evolution of lung cancers acquiring resistance to EGFR inhibitors. Sci Transl Med. 2011; 3:75ra26.
9. Engelman JA, Zejnuliahu K, Mitsudomi T, Song Y, Hyland C, Park JO, Lindeman N, Gale CM, Zhao X, Christensen J, Kosaka T, Holmes AJ, Rogers AM, et al. MET amplification leads to gefitinib resistance in lung cancer by activating ERBB3 signaling. Science. 2007; 316:1039-1043.
10. Takezawa K, Parazzoli V, Arcila ME, Nebhan CA, Song X, de Stanchina E, Ohashi K, Janjigian YY, Spitzler PJ, Melnick MA, Riely GJ, Kris MG, Miller VA, 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.
11. Cross DA, Ashton SE, Ghiorghiu S, Eberlein C, Nebhan CA, Spitzler PJ, Orme JP, Finlay MR, Ward RA, Mellor MJ, Hughes G, Rahi A, Jacobs VN, et al. AZD9291, an irreversible EGFR, TKI, overcomes T790M-mediated resistance to EGFR inhibitors in lung cancer. Cancer Discov. 2014; 4:1046-1061.
12. Steuer CE, Khuri FR, Ramalingam SS. The next generation of epidermal growth factor receptor tyrosine kinase inhibitors in the treatment of lung cancer. Cancer. 2015; 121:E1-6.
13. Janjigian YY, Smit EF, Groen HJ, Horn L, Gettinger S, Camidge DR, Riely GJ, Wang B, Fu Y, Chand VK, Miller VA, Pao W. Dual inhibition of EGFR with afatinib and cetuximab in kinase inhibitor-resistant EGFR-mutant lung cancer with and without T790M mutations. Cancer Discov. 2014; 4:1036-1045.
14. Sequist LV, Pawel JV, Garmey EG, Akerley WL, Brugger W, Ferrari D, Chen Y, Costa DB, Gerber DE, Orlov S, Ramlau R, Arthur S, Gorbachevsky I, et al. Randomized phase II study of erlotinib plus tivantinib versus erlotinib plus placebo in previously treated nonsmall-cell lung cancer. J Clin Oncol. 2011; 29:3307-3315.
15. Sozzi G, Conte D, Leon M, Ciricione R, Roz L, Ratcliffe C, Roz E, Cirenei N, Bellomi M, Pelosi G, Pierotti MA, Pastorino U. Quantification of free circulating DNA as a diagnostic marker in lung cancer. J Clin Oncol. 2003; 21:3902-3908.
16. Kimura H, Suminoe M, Kasahara K, Sone T, Araya T, Tamori S, Koizumi F, Nishio K, Miyamoto K, Fujimura M, Nakao S. Evaluation of epidermal growth factor receptor mutation status in serum DNA as a predictor of response to gefitinib (IRESSA). Br J Cancer. 2007; 97:778-784.
17. Goto K, Ichinose Y, Ohe Y, Yamamoto N, Negoro S, Nishio K, Itoh Y, Jiang H, Duffield E, McCormack R, Saijo N, Mok T, Fukuoka M. 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. 2012; 7:115-121.
18. Kimura H, Kasahara K, Kawaishi M, Kunitoh H, Tamura T, Holloway B, Nishio K. Detection of epidermal growth factor receptor mutations in serum as a predictor of the response to gefitinib in patients with non-small-cell lung cancer. Clin Cancer Res. 2006; 12:3915-3921.
19. Kuang Y, Rogers A, Yeap BY, Wang L, Makrigiorgos M, Vetrand K, Thiede S, Distel RJ, Jänne PA. Noninvasive detection of EGFR T790M in gefitinib or erlotinib resistant non-small cell lung cancer. Clin Cancer Res. 2009; 15:2630-2636.
20. Bai H, Mao L, Wang HS, Zhao J, Yang L, An TT, Wang X, Duan CJ, Wu NM, Guo ZQ, Liu YX, Liu HN, Wang YY, Wang J. Epidermal growth factor receptor mutations in plasma DNA samples predict tumor response in Chinese patients with stages IIIB to IV non-small-cell lung cancer. J Clin Oncol. 2009; 27:2653-2659.
21. Brevet M, Johnson ML, Azzoli CG, Ladanyi M. Detection of EGFR mutations in plasma DNA from lung cancer patients by mass spectrometry genotyping is predictive of tumor EGFR status and response to EGFR inhibitor. Lung Cancer. 2011; 73:96-102.
22. Jiang B, Liu F, Yang L, Zhang W, Yuan H, Wang J, Huang G. Serum detection of epidermal growth factor receptor gene mutations using mutant-enriched sequencing in Chinese patients with advanced non-small cell lung cancer. J Int Med Res. 2011; 39:1392-1401.
23. Kim ST, Jung HY, Sung JS, Jo UH, Tanaka T, Hagiwara K, Park KH, Shin SW, Kim JS, Kim YH. Can serum be used for analyzing the EGFR mutation status in patients with advanced nonsmall cell lung cancer? Am J Clin Oncol. 2013; 36:57-63.
24. Yung TK, Chan KC, Mok TS, Tong J, To KF, Lo YM. Single-molecule detection of epidermal growth factor receptor mutations in plasma by microfluidics digital PCR in non-small cell lung cancer patients. Clin Cancer Res. 2009; 15:2076-2084.
25. Baker M. Digital PCR hits its stride. Nature Methods. 2012; 9:541-544.
26. Wang Z, Chen R, Wang S, Zhong J, Wu M, Zhao J, Duan J, Zhuo M, An T, Wang Y, Bai H, Wang J. Quantification and dynamic monitoring of EGFR T790M in plasma cell-free DNA by digital PCR for prognosis of EGFR-TKI treatment in advanced NSCLC. PLoS One. 2014; 9:e110780.
27. Goto K, Ichinose Y, Ohe Y, Yamamoto N, Negoro S, Nishio K, Itoh Y, Jiang H, Duffield E, McCormack R, Saijo N, Mok T, Fukuoka M. 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. 2012; 7:115-121.
28. Kuang Y, Rogers A, Yeap BY, Wang L, Makrigiorgos M, Vetrand K, Thiede S, Distel RJ, Jänne PA. Noninvasive detection of EGFR T790M in gefitinib or erlotinib resistant non-small cell lung cancer. Clin Cancer Res. 2009; 15:2630-2636.
29. Sakai K, Horiike A, Irwin DL, Kudo K, Fujita Y, Tanimoto A, Sakatani T, Saito R, Kaburaki K, Yanagitani N, Ohyanagi F, Nishio M, Nishio K. Detection of epidermal growth factor receptor T790M mutation in plasma DNA from patients refractory to epidermal growth factor receptor tyrosine kinase inhibitor. Cancer Sci. 2013; 104:1198-1204.
30. Oxnard GR, Pawelets CP, Kuang Y, Mach SL, O'Connell A, Messineo MM, Luke JJ, Butaney M, Kirschmeier P, Jackman DM, Jänne PA. Noninvasive detection of response and resistance in EGFR-mutant lung cancer using quantitative next-generation genotyping of cell-free plasma DNA. Clin Cancer Res. 2014; 20:1698-1705.
31. Sorensen BS, Wu L, Wei W, Tsai J, Weber B, Nexo E, Meldgaard P. 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. 2014; 120:3896-3901.
32. Jänne PA, Yang JC, Kim DW, Planchard D, Ohe Y, Ramalingam SS, Ahn MJ, Kim SW, Su WC, Horn L, Haggstrom D, Felip E, Kim JH, et al. AZD9291 in EGFR inhibitor-resistant non-small-cell lung cancer. N Engl J Med. 2015; 372:1689-1699.
33. Park S, Holmes-Tisch AJ, Cho EY, Shim YM, Kim J, Kim HS, Lee J, Park YH, Ahn JS, Park K, Jänne PA, Ahn MJ. Discordance of molecular biomarkers associated with epidermal growth factor receptor pathway between primary tumors and lymph node metastasis in non-small cell lung cancer. J Thorac Oncol. 2009; 4:809-815.
34. Schmid K, Oehl N, Wrba F, Pirker R, Pirker C, Filipits M. EGFR/KRAS/BRAF mutations in primary lung adenocarcinomas and corresponding locoregional lymph node metastases. Clin Cancer Res. 2009; 15:4554-4560.
35. Shimizu K, Yukawa T, Hirami Y, Okita R, Saisho S, Maeda A, Yasuda K, Nakata M. Heterogeneity of the EGFR mutation status between the primary tumor and metastatic lymph node and the sensitivity to EGFR tyrosine kinase inhibitor in non-small cell lung cancer. Target Oncol. 2013; 8:237-42.
36. Taniguchi K, Okami J, Kodama K, Higashiyama M, Kato K. Intratumor heterogeneity of epidermal growth factor receptor mutations in lung cancer and its correlation to the response to gefitinib. Cancer Sci. 2008; 99:929-935.
37. Sakurada A, Lara-Guerra H, Liu N, Shepherd FA, Tsao MS. Tissue heterogeneity of EGFR mutation in lung adenocarcinoma. J Thorac Oncol. 2008; 3:527-529.
38. Graziano P, de Marinis F, Gori B, Gasbarra R, Migliorino R, De Santis S, Pelosi G, Leone A. EGFR-Driven Behavior and Intrapatient T790M Mutation Heterogeneity of NonSmall-Cell Carcinoma With Squamous Histology. J Clin Oncol. 2014; Apr 21. [Epub ahead of print].
39. Su KY, Chen HY, Li KC, Kuo ML, Yang JC, Chan WK, Ho BC, Chang GC, Shih JY, Yu SL, Yang PC. 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. 2012; 30:433-440.
40. Inukai M, Toyooka S, Ito S, Asano H, Ichihara S, Soh J, Suehisa H, Ouchida M, Aoe K, Aoe M, Kiura K, Shimizu N, Date H. 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.
41. Gevensleben H, Garcia-Murillas I, Graeser MK, Schiavon G, Osin P, Parton M, Smith IE, Ashworth A, Turner NC. Noninvasive detection of HER2 amplification with plasma DNA digital PCR. Clin Cancer Res. 2013; 19:3276-84.
42. Rothe F, Leas JF, Lambrechts D, Smeets D, Vincent D, Maetens M, Fumagalli D, Michiels S, Drisis S, Moerman C, Detiffe JP, Larsimont D, Awada A, et al. Plasma circulating tumor DNA as an alternative to metastatic biopsies for mutational analysis in breast cancer. Ann Oncol. 2014; 25:1959-1965.
43. Page K, Hava N, Ward B, Brown J, Guttery DS, Ruangpratheep C, Blighe K, Sharma A, Walker RA, Coombes RC, Shaw JA. Detection of HER2 amplification in circulating free DNA in patients with breast cancer. Br J Cancer. 2011; 104:1342-1348.
44. Wolff AC, Hammond ME, Hicks DG, Dowsett M, McShane LM, Allison KH, Allred DC, Bartlett JM, Bilous M, Fitzgibbons P, Hanna W, Jenkins RB, Mangu PB, et al. Recommendations for human epidermal growth factor receptor 2 testing in breast cancer: American Society of Clinical Oncology/College of American Pathologists clinical practice guideline update. J Clin Oncol. 2013; 31:3997-4013.