Next-generation sequencing of lung cancer EGFR exons 18-21 allows effective molecular diagnosis of small routine samples (cytology and biopsy)

PLoS ONE

Volumn 8, Issue 12, 2013, Pages

  De Biase, Dario ^a   Visani, Michela ^a   Malapelle, Umberto ^b   Simonato, Francesca ^c   Cesari, Valentina ^a   Bellevicine, Claudio ^b   Pession, Annalisa ^a   Troncone, Giancarlo ^b   Fassina, Ambrogio ^c   Tallini, Giovanni ^a  

^a UNIVERSITY OF BOLOGNA   (Italy)

^b UNIVERSITY OF NAPLES FEDERICO II   (Italy)

^c UNIVERSITY OF PADOVA   (Italy)

Author keywords

[No Author keywords available]

Indexed keywords

EPIDERMAL GROWTH FACTOR RECEPTOR;

AGED; CARCINOMA, NON-SMALL-CELL LUNG; EXON; FEMALE; GENETICS; HIGH THROUGHPUT SEQUENCING; HUMAN; LUNG NEOPLASMS; MALE; MOLECULAR DIAGNOSIS; NUCLEOTIDE SEQUENCE; PATHOLOGY; PROCEDURES;

AGED; CARCINOMA, NON-SMALL-CELL LUNG; DNA MUTATIONAL ANALYSIS; EXONS; FEMALE; HIGH-THROUGHPUT NUCLEOTIDE SEQUENCING; HUMANS; LUNG NEOPLASMS; MALE; MOLECULAR DIAGNOSTIC TECHNIQUES; RECEPTOR, EPIDERMAL GROWTH FACTOR;

EID: 84893442971     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0083607     Document Type: Article

References (68)

1. Lynch TJ, Bell DW, Sordella R, Gurubhagavatula S, Okimoto RA et al. (2004) Activating mutations in the epidermal growth factor receptor underlying responsiveness of non-small-cell lung cancer to gefitinib. N Engl J Med 350: 2129-2139. doi:10.1056/NEJMoa040938. PubMed: 15118073. (Pubitemid 38637993)
2. Paez JG, Jänne PA, Lee JC, Tracy S, Greulich H et al. (2004) EGFR mutations in lung cancer: correlation with clinical response to gefitinib therapy. Science 304: 1497-1500. doi:10.1126/science.1099314. PubMed: 15118125. (Pubitemid 38720929)
3. Fukuoka M, Wu YL, Thongprasert S, Sunpaweravong P, Leong SS et al. (2011) 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: 2866-2874. doi:10.1200/JCO.2010.33.4235. PubMed: 21670455.
4. Mitsudomi T, Morita S, Yatabe Y, Negoro S, Okamoto I et al. (2010) 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: 121-128. doi:10.1016/S1470-2045(09)70364-X. PubMed: 20022809.
5. Mok TS, Wu YL, Thongprasert S, Yang CH, Chu DT et al. (2009) Gefitinib or carboplatin-paclitaxel in pulmonary adenocarcinoma. N Engl J Med 361: 947-957. doi:10.1056/NEJMoa0810699. PubMed: 19692680.
6. Rosell R, Carcereny E, Gervais R, Vergnenegre A, Massuti B et al. (2012) Erlotinib versus standard chemotherapy as first-line treatment for European patients with advanced EGFR mutation-positive non-small-cell lung cancer (EURTAC): a multicentre, open-label, randomised phase 3 trial. Lancet Oncol 13: 239-246. doi:10.1016/S1470-2045(12)70227-9. PubMed: 22285168.
7. Zhou C, Wu YL, Chen G, Feng J, Liu XQ et al. (2011) Erlotinib versus chemotherapy as first-line treatment for patients with advanced EGFR mutation-positive non-small-cell lung cancer (OPTIMAL, CTONG-0802): a multicentre, open-label, randomised, phase 3 study. Lancet Oncol 12: 735-742. doi:10.1016/S1470-2045(11)70184-X. PubMed: 21783417.
8. Maemondo M, Inoue A, Kobayashi K, Sugawara S, Oizumi S et al. (2010) Gefitinib or chemotherapy for non-small-cell lung cancer with mutated EGFR. N Engl J Med 362: 2380-2388. doi:10.1056/NEJMoa0909530. PubMed: 20573926.
9. Yang JC, Schuler MH, Yamamoto N, O'Byrne KJ, et al. (2012) LUX-Lung 3: Afatinib versus pemetrexed/cisplatin as a first-line treatment in advanced lung cancer harbouring EGFR-activating mutations. J Clin Oncol 30S: LBA7500
10. Lindeman NI, Cagle PT, Beasley MB, Chitale DA, Dacic S et al. (2013) Molecular Testing Guideline for Selection of Lung Cancer Patients for EGFR and ALK Tyrosine Kinase Inhibitors: Guideline from the College of American Pathologists, International Association for the Study of Lung Cancer, and Association for Molecular. Pathology - Arch Pathol Lab Med: 828-860.
11. Pirker R, Herth FJ, Kerr KM, Filipits M, Taron M et al. (2010) Consensus for EGFR mutation testing in non-small cell lung cancer: results from a European workshop. J Thorac Oncol 5: 1706-1713. doi:10.1097/JTO.0b013e3181f1c8de. PubMed: 20871269.
12. Marks JL, Broderick S, Zhou Q, Chitale D, Li AR et al. (2008) Prognostic and therapeutic implications of EGFR and KRAS mutations in resected lung adenocarcinoma. J Thorac Oncol 3: 111-116. doi:10.1097/JTO.0b013e318160c607. PubMed: 18303429. (Pubitemid 351323183)
13. Eberhard DA, Johnson BE, Amler LC, Goddard AD, Heldens SL et al. (2005) Mutations in the epidermal growth factor receptor and in KRAS are predictive and prognostic indicators in patients with non-small-cell lung cancer treated with chemotherapy alone and in combination with erlotinib. J Clin Oncol 23: 5900-5909. doi:10.1200/JCO.2005.02.857. PubMed: 16043828.
14. Han SW, Kim TY, Hwang PG, Jeong S, Kim J et al. (2005) Predictive and prognostic impact of epidermal growth factor receptor mutation in non-small-cell lung cancer patients treated with gefitinib. J Clin Oncol 23: 2493-2501. doi:10.1200/JCO.2005.01.388. PubMed: 15710947. (Pubitemid 47050839)
15. Huang SF, Liu HP, Li LH, Ku YC, Fu YN et al. (2004) High frequency of epidermal growth factor receptor mutations with complex patterns in non-small cell lung cancers related to gefitinib responsiveness in Taiwan. Clin Cancer Res 10: 8195-8203. doi:10.1158/1078-0432.CCR-04-1245. PubMed: 15623594.
16. Johnson BE, Jänne PA (2005) Epidermal growth factor receptor mutations in patients with non-small cell lung cancer. Cancer Res 65: 7525-7529. PubMed: 16140912. (Pubitemid 41297219)
17. Rosell R, Ichinose Y, Taron M, Sarries C, Queralt C et al. (2005) Mutations in the tyrosine kinase domain of the EGFR gene associated with gefitinib response in non-small-cell lung cancer. Lung Cancer 50: 25-33. doi:10.1016/j.lungcan.2005.05.017. PubMed: 16011858. (Pubitemid 41297466)
18. Sequist LV, von Pawel J, Garmey EG, Akerley WL, Brugger W et al. (2011) Randomized phase II study of erlotinib plus tivantinib versus erlotinib plus placebo in previously treated non-small-cell lung cancer. J Clin Oncol 29: 3307-3315. doi:10.1200/JCO.2010.34.0570. PubMed: 21768463.
19. Balak MN, Gong Y, Riely GJ, Somwar R, Li AR et al. (2006) Novel D761Y and common secondary T790M mutations in epidermal growth factor receptor-mutant lung adenocarcinomas with acquired resistance to kinase inhibitors. Clin Cancer Res 12: 6494-6501. doi:10.1158/1078-0432.CCR-06-1570. PubMed: 17085664. (Pubitemid 44799723)
20. Kosaka T, Yatabe Y, Endoh H, Yoshida K, Hida T et al. (2006) Analysis of epidermal growth factor receptor gene mutation in patients with non-small cell lung cancer and acquired resistance to gefitinib. Clin Cancer Res 12: 5764-5769. doi:10.1158/1078-0432.CCR-06-0714. PubMed: 17020982. (Pubitemid 44629607)
21. Pao W, Miller VA, Politi KA, Riely GJ, Somwar R et al. (2005) Acquired resistance of lung adenocarcinomas to gefitinib or erlotinib is associated with a second mutation in the EGFR kinase domain. PLoS Med 2: e73. doi:10.1371/journal.pmed.0020073. PubMed: 15737014.
22. Yang CH, Yu CJ, Shih JY, Chang YC, Hu FC et al. (2008) Specific EGFR mutations predict treatment outcome of stage IIIB/IV patients with chemotherapy-naive non-small-cell lung cancer receiving first-line gefitinib monotherapy. J Clin Oncol 26: 2745-2753. doi:10.1200/JCO.2007.15.6695. PubMed: 18509184.
23. Rosell R, Moran T, Queralt C, Porta R, Cardenal F et al. (2009) Screening for epidermal growth factor receptor mutations in lung cancer. N Engl J Med 361: 958-967. doi:10.1056/NEJMoa0904554. PubMed: 19692684.
24. Travis WD, Brambilla E, Müller-Hermelink HK, Harris CC (2004) WHO. Pathology and Genetics of Tumours of the Lung, Pleura,Thymus and Heart; W Tumours. Lyon, France: IARC.
25. Beau-Faller M, Degeorges A, Rolland E, Mounawar M, Antoine M et al. (2011) Cross-validation study for epidermal growth factor receptor and KRAS mutation detection in 74 blinded non-small cell lung carcinoma samples: a total of 5550 exons sequenced by 15 molecular French laboratories (evaluation of the EGFR mutation status for the administration of EGFR-TKIs in non-small cell lung carcinoma [ERMETIC] project - part 1). J Thorac Oncol 6: 1006-1015. doi:10.1097/JTO.0b013e318211dcee. PubMed: 21532509.
26. Aisner DL, Marshall CB (2012) Molecular pathology of non-small cell lung cancer: a practical guide. Am J Clin Pathol 138: 332-346. doi:10.1309/ AJCPFR12WJKCEEZZ. PubMed: 22912349.
27. John T, Liu G, Tsao MS (2009) Overview of molecular testing in non-small-cell lung cancer: mutational analysis, gene copy number, protein expression and other biomarkers of EGFR for the prediction of response to tyrosine kinase inhibitors. Oncogene 28 Suppl 1: S14-S23. doi:10.1038/onc.2009. 197. PubMed: 19680292.
28. Eberhard DA, Giaccone G, Johnson BE (2008) Biomarkers of response to epidermal growth factor receptor inhibitors in Non-Small-Cell Lung Cancer Working Group: standardization for use in the clinical trial setting. J Clin Oncol 26: 983-994. doi:10.1200/JCO.2007.12.9858. PubMed: 18281673. (Pubitemid 351398092)
29. Arcila M, Lau C, Nafa K, Ladanyi M (2011) Detection of KRAS and BRAF mutations in colorectal carcinoma roles for high-sensitivity locked nucleic acid-PCR sequencing and broad-spectrum mass spectrometry genotyping. J Mol Diagn 13: 64-73. doi:10.1016/j.jmoldx.2010.11.005. PubMed: 21227396.
30. Ellison G, Zhu G, Moulis A, Dearden S, Speake G et al. (2013) EGFR mutation testing in lung cancer: a review of available methods and their use for analysis of tumour tissue and cytology samples. J Clin Pathol 66: 79-89. doi:10.1136/jclinpath-2012-201194. PubMed: 23172555.
31. Nomoto K, Tsuta K, Takano T, Fukui T, Yokozawa K et al. (2006) Detection of EGFR mutations in archived cytologic specimens of non-small cell lung cancer using high-resolution melting analysis. Am J Clin Pathol 126: 608-615. doi:10.1309/N5PQNGW2QKMX09X7. PubMed: 16938658. (Pubitemid 44498512)
32. Kawada I, Soejima K, Watanabe H, Nakachi I, Yasuda H et al. (2008) An alternative method for screening EGFR mutation using RFLP in non-small cell lung cancer patients. J Thorac Oncol 3: 1096-1103. doi:10.1097/JTO.0b013e318186fadd. PubMed: 18827604.
33. van Eijk R, Licht J, Schrumpf M, Talebian Yazdi M, Ruano D et al. (2011) Rapid KRAS, EGFR, BRAF and PIK3CA mutation analysis of fine needle aspirates from non-small-cell lung cancer using allele-specific qPCR. PLOS ONE 6: e17791. doi:10.1371/journal.pone.0017791. PubMed: 21408138.
34. Miyamae Y, Shimizu K, Mitani Y, Araki T, Kawai Y et al. (2010) Mutation detection of epidermal growth factor receptor and KRAS genes using the smart amplification process version 2 from formalin-fixed, paraffin-embedded lung cancer tissue. J Mol Diagn 12: 257-264. doi:10.2353/jmoldx.2010.090105. PubMed: 20093389.
35. Araki T, Shimizu K, Nakamura T, Baba M, Kawai Y et al. (2011) Clinical screening assay for EGFR exon 19 mutations using PNA-clamp smart amplification process version 2 in lung adenocarcinoma. Oncol Rep 26: 1213-1219. PubMed: 21769434.
36. Dufort S, Richard MJ, Lantuejoul S, de Fraipont F (2011) Pyrosequencing, a method approved to detect the two major EGFR mutations for anti EGFR therapy in NSCLC. J Exp Clin Cancer Res 30: 57. doi:10.1186/1756-9966-30-57. PubMed: 21575212.
37. Yu J, Kane S, Wu J, Benedettini E, Li D et al. (2009) Mutation-specific antibodies for the detection of EGFR mutations in non-small-cell lung cancer. Clin Cancer Res 15: 3023-3028. doi:10.1158/1078-0432.CCR-08-2739. PubMed: 19366827.
38. Kato Y, Peled N, Wynes MW, Yoshida K, Pardo M et al. (2010) Novel epidermal growth factor receptor mutation-specific antibodies for non-small cell lung cancer: immunohistochemistry as a possible screening method for epidermal growth factor receptor mutations. J Thorac Oncol 5: 1551-1558. doi:10.1097/JTO.0b013e3181e9da60. PubMed: 20697298.
39. Angulo B, Conde E, Suárez-Gauthier A, Plaza C, Martínez R et al. (2012) A comparison of EGFR mutation testing methods in lung carcinoma: direct sequencing, real-time PCR and immunohistochemistry. PLOS ONE 7: e43842. doi:10.1371/journal.pone.0043842. PubMed: 22952784.
40. Whitehall V, Tran K, Umapathy A, Grieu F, Hewitt C et al. (2009) A multicenter blinded study to evaluate KRAS mutation testing methodologies in the clinical setting. J Mol Diagn 11: 543-552. doi:10.2353/jmoldx.2009.090057. PubMed: 19815694.
41. Angulo B, García-García E, Martínez R, Suárez-Gauthier A, Conde E et al. (2010) A commercial real-time PCR kit provides greater sensitivity than direct sequencing to detect KRAS mutations: a morphology-based approach in colorectal carcinoma. J Mol Diagn 12: 292-299. doi:10.2353/jmoldx.2010.090139. PubMed: 20203003.
42. Metzker ML (2010) Sequencing technologies - the next generation. Nat Rev Genet 11: 31-46. doi:10.1038/nrg2626. PubMed: 19997069.
43. Meyerson M, Gabriel S, Getz G (2010) Advances in understanding cancer genomes through second-generation sequencing. Nat Rev Genet 11: 685-696. doi:10.1038/nrg2841. PubMed: 20847746.
44. Malapelle U, Bellevicine C, De Luca C, Salatiello M, De Stefano A et al. (2013) EGFR mutations detected on cytology samples by a centralized laboratory reliably predict response to gefitinib in non-small cell lung carcinoma patients. Cancer Cytopathol, 121: 552-60. PubMed: 23780873.
45. Fassina A, Gazziero A, Zardo D, Corradin M, Aldighieri E et al. (2009) Detection of EGFR and KRAS mutations on trans-thoracic needle aspiration of lung nodules by high resolution melting analysis. J Clin Pathol 62: 1096-1102. doi:10.1136/jcp.2009.067587. PubMed: 19640859.
46. Morandi L, de Biase D, Visani M, Cesari V, De Maglio G et al. (2012) Allele specific locked nucleic acid quantitative PCR (ASLNAqPCR): an accurate and cost-effective assay to diagnose and quantify KRAS and BRAF mutation. PLOS ONE 7: e36084. doi:10.1371/journal.pone.0036084. PubMed: 22558339.
47. Patel RK, Jain M (2012) NGS QC Toolkit: a toolkit for quality control of next generation sequencing data. PLOS ONE 7: e30619. doi:10.1371/journal.pone. 0030619. PubMed: 22312429.
48. Campbell PJ, Pleasance ED, Stephens PJ, Dicks E, Rance R et al. (2008) Subclonal phylogenetic structures in cancer revealed by ultradeep sequencing. Proc Natl Acad Sci U S A 105: 13081-13086. doi:10.1073/pnas.0801523105. PubMed: 18723673.
49. Williams C, Pontén F, Moberg C, Söderkvist P, Uhlén M et al. (1999) A high frequency of sequence alterations is due to formalin fixation of archival specimens. Am J Pathol 155: 1467-1471. doi:10.1016/S0002- 9440(10)65461-2. PubMed: 10550302.
50. Hadd AG, Houghton J, Choudhary A, Sah S, Chen L et al. (2013) Targeted, high-depth, next-generation sequencing of cancer genes in formalin-fixed, paraffin-embedded and fine-needle aspiration tumor specimens. J Mol Diagn 15: 234-247. doi:10.1016/j.jmoldx.2012.11.006. PubMed: 23321017.
51. Chin EL, da Silva C, Hegde M (2013) Assessment of clinical analytical sensitivity and specificity of next-generation sequencing for detection of simple and complex mutations. BMC Genet 14: 6. doi:10.1186/1471-2164-14-S3-S6. PubMed: 23418865.
52. Rosell R, Molina MA, Serrano MJ (2012) EGFR mutations in circulating tumour DNA. Lancet Oncol 13: 971-973. doi:10.1016/S1470-2045(12)70369-8. PubMed: 23026821.
53. Tuononen K, Mäki-Nevala S, Sarhadi VK, Wirtanen A, Rönty M et al. (2013) Comparison of targeted next-generation sequencing (NGS) and real-time PCR in the detection of EGFR, KRAS, and BRAF mutations on formalin-fixed, paraffin-embedded tumor material of non-small cell lung carcinoma-superiority of NGS. Genes Chromosomes Cancer 52: 503-511. doi:10.1002/gcc.22047. PubMed: 23362162.
54. Moskalev EA, Stöhr R, Rieker R, Hebele S, Fuchs F et al. (2013) Increased detection rates of EGFR and KRAS mutations in NSCLC specimens with low tumour cell content by 454 deep sequencing. Virchows Arch 462: 409-419. doi:10.1007/s00428-013-1376-6. PubMed: 23468066.
55. Buttitta F, Felicioni L, Del Grammastro M, Filice G, Di Lorito A et al. (2013) Effective Assessment of egfr Mutation Status in Bronchoalveolar Lavage and Pleural Fluids by Next-Generation Sequencing. Clin Cancer Res 19: 691-698. doi:10.1158/1078-0432.CCR-12-1958. PubMed: 23243218.
56. Marchetti A, Del Grammastro M, Filice G, Felicioni L, Rossi G et al. (2012) Complex mutations & subpopulations of deletions at exon 19 of EGFR in NSCLC revealed by next generation sequencing: potential clinical implications. PLOS ONE 7: e42164. doi:10.1371/journal.pone.0042164. PubMed: 22848739.
57. Querings S, Altmüller J, Ansén S, Zander T, Seidel D et al. (2011) Benchmarking of mutation diagnostics in clinical lung cancer specimens. PLOS ONE 6: e19601. doi:10.1371/journal.pone.0019601. PubMed: 21573178.
58. Oshita F, Matsukuma S, Yoshihara M, Sakuma Y, Ohgane N et al. (2006) Novel heteroduplex method using small cytology specimens with a remarkably high success rate for analysing EGFR gene mutations with a significant correlation to gefitinib efficacy in non-small-cell lung cancer. Br J Cancer 95: 1070-1075. doi:10.1038/sj.bjc.6603396. PubMed: 17047654. (Pubitemid 44606834)
59. Lozano MD, Zulueta JJ, Echeveste JI, Gúrpide A, Seijo LM et al. (2011) Assessment of epidermal growth factor receptor and K-ras mutation status in cytological stained smears of non-small cell lung cancer patients: correlation with clinical outcomes. Oncologist 16: 877-885. doi:10.1634/ theoncologist.2010-0155. PubMed: 21572125.
60. Rekhtman N, Brandt SM, Sigel CS, Friedlander MA, Riely GJ et al. (2011) Suitability of thoracic cytology for new therapeutic paradigms in non-small cell lung carcinoma: high accuracy of tumor subtyping and feasibility of EGFR and KRAS molecular testing. J Thorac Oncol 6: 451-458. doi:10.1097/JTO. 0b013e31820517a3. PubMed: 21266922.
61. da Cunha Santos G, Saieg MA, Geddie W, Leighl N (2011) EGFR gene status in cytological samples of nonsmall cell lung carcinoma: controversies and opportunities. Cancer Cytopathol 119: 80-91. doi:10.1002/cncy.20150. PubMed: 21400669.
62. Na II, Kang HJ, Cho SY, Koh JS, Lee JK et al. (2007) EGFR mutations and human papillomavirus in squamous cell carcinoma of tongue and tonsil. Eur J Cancer 43: 520-526. doi:10.1016/j.ejca.2006.09.025. PubMed: 17224267. (Pubitemid 46177596)
63. Na II, Rho JK, Choi YJ, Kim CH, Park JH et al. (2007) The survival outcomes of patients with resected non-small cell lung cancer differ according to EGFR mutations and the P21 expression. Lung Cancer 57: 96-102. doi:10.1016/j.lungcan.2007.01.027. PubMed: 17337084. (Pubitemid 46843338)
64. Kotoula V, Sozopoulos E, Litsiou H, Fanourakis G, Koletsa T et al. (2009) Mutational analysis of the BRAF, RAS and EGFR genes in human adrenocortical carcinomas. Endocr Relat Cancer 16: 565-572. doi:10.1677/ERC-08-0101. PubMed: 19190079.
65. Metzger B, Chambeau L, Begon DY, Faber C, Kayser J et al. (2011) The human epidermal growth factor receptor (EGFR) gene in European patients with advanced colorectal cancer harbors infrequent mutations in its tyrosine kinase domain. BMC Med Genet 12: 144. doi:10.1186/1471-2350-12-144. PubMed: 22026926.
66. Chang YL, Wu CT, Shih JY, Lee YC (2011) Unique p53 and epidermal growth factor receptor gene mutation status in 46 pulmonary lymphoepithelioma-like carcinomas. Cancer Sci 102: 282-287. doi:10.1111/j.1349-7006.2010.01768.x. PubMed: 21070477.
67. Akbari M, Hansen MD, Halgunset J, Skorpen F, Krokan HE (2005) Low copy number DNA template can render polymerase chain reaction error prone in a sequence-dependent manner. J Mol Diagn 7: 36-39. doi:10.1016/S1525-1578(10) 60006-2. PubMed: 15681472. (Pubitemid 40310163)
68. Altimari A, de Biase D, De Maglio G, Gruppioni E, Capizzi E et al. (2013) 454 next generation-sequencing outperforms allele-specific PCR, Sanger sequencing, and pyrosequencing for routine KRAS mutation analysis of formalin-fixed, paraffin-embedded samples. OncoTargets and Therapy 6: 1057-1064. PubMed: 23950653.