A comparison of EGFR mutation testing methods in lung carcinoma: Direct sequencing, real-time PCR and immunohistochemistry

PLoS ONE

Volumn 7, Issue 8, 2012, Pages

  Angulo, Bárbara ^a   Conde, Esther ^a   Suárez Gauthier, Ana ^a   Plaza, Carlos ^a   Martínez, Rebeca ^a   Redondo, Pilar ^a   Izquierdo, Elisa ^a   Rubio Viqueira, Belén ^a,b   Paz Ares, Luis ^c   Hidalgo, Manuel ^a,b   López Ríos, Fernando ^a  

^a UNIVERSIDAD SAN PABLO CEU   (Spain)

^b Centro Nacional de Investigaciones Oncológicas   (Spain)

^c HOSPITAL UNIVERSITARIO VIRGEN DEL ROCÍO   (Spain)

Author keywords

[No Author keywords available]

Indexed keywords

ACCURACY; ADULT; AGED; ANALYTIC METHOD; ARTICLE; DIRECT SEQUENCING; EGFR GENE; EXON; FEMALE; GENE DELETION; GENE EXPRESSION; GENE FREQUENCY; GENE MUTATION; HUMAN; HUMAN TISSUE; IMMUNOHISTOCHEMISTRY; INTERMETHOD COMPARISON; LIMIT OF DETECTION; LUNG CARCINOMA; MAJOR CLINICAL STUDY; MALE; MUTATIONAL ANALYSIS; ONCOGENE; POINT MUTATION; PREDICTIVE VALUE; REAL TIME POLYMERASE CHAIN REACTION; SENSITIVITY AND SPECIFICITY;

ADULT; AGED; AGED, 80 AND OVER; BASE SEQUENCE; DNA MUTATIONAL ANALYSIS; FEMALE; HUMANS; IMMUNOHISTOCHEMISTRY; LIMIT OF DETECTION; LUNG NEOPLASMS; MALE; MIDDLE AGED; REAL-TIME POLYMERASE CHAIN REACTION; RECEPTOR, EPIDERMAL GROWTH FACTOR;

EID: 84865432696     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0043842     Document Type: Article

References (54)

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 nonsmall-cell lung cancer to gefitinib. N Engl J Med 350: 2129-2139.
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.
3. Pao W, Miller V, Zakowski M, Doherty J, Politi K, et al. (2003) EGF receptor gene mutations are common in lung cancers from "never smokers" and are associated with sensitivity of tumors to gefitinib and erlotinib. Proc Natl Acad Sci USA 101: 13306-13311.
4. Pan Q, Pao W, Ladanyi M, (2005) Rapid polymerase chain reaction-based detection of epidermal growth factor receptor gene mutations in lung adenocarcinomas. J Mol Diagn 7: 396-403.
5. 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.
6. Asano H, Toyooka S, Tokumo M, Ichimura K, Aoe K, et al. (2006) Detection of EGFR gene mutation in lung cancer by mutant-enriched polymerase chain reaction assay. Clin Cancer Res 12: 43-48.
7. Li J, Wang L, Mamon H, Kulke MH, Berbeco R, et al. (2008) Replacing PCR with COLD-PCR enriches variant DNA sequences and redefines the sensitivity of genetic testing. Nat Med 14: 579-584.
8. Endo K, Konishi A, Sasaki H, Takada M, Tanaka H, et al. (2005) Epidermal growth factor receptor gene mutation in non-small cell lung cancer using highly sensitive and fast TaqMan PCR assay. Lung Cancer 50: 375-384.
9. Zhou C, Ni J, Zhao Y, Su B, (2006) Rapid detection of epidermal growth factor receptor mutations in non-small cell lung cancer using real-time polymerase chain reaction with TaqMan-MGB probes. Cancer J 12: 33-39.
10. Kimura H, Fujiwara Y, Sone T, Kunitoh H, Tamura T, et al. (2006) High sensitivity detection of epidermal growth factor receptor mutations in the pleural effusion of non-small cell lung cancer patients. Cancer Sci 97: 642-648.
11. 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.
12. Brevet M, Arcila M, Ladanyi M, (2010) Assessment of EGFR mutation status in lung adenocarcinoma by immunohistochemistry using antibodies specific to the two major forms of mutant EGFR. J Mol Diagn 12: 169-176.
13. Kawahara A, Yamamoto C, Nakashima K, Azuma K, Hattori S, et al. (2010) Molecular diagnosis of activating EGFR mutations in non-small cell lung cancer using mutation specific antibodies for immunohistochemical analysis. Clin Cancer Res 16: 3163-3170.
14. Benedettini E, Sholl LM, Peyton M, Reilly J, Ware C, et al. (2010) Met Activation in Non-Small Cell Lung Cancer Is Associated with de Novo Resistance to EGFR Inhibitors and the Development of Brain Metastasis. Am J Pathol 177: 415-423.
15. 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.
16. Kitamura A, Hosoda W, Sasaki E, Mitsudomi T, Yatabe Y, (2010) Immunohistochemical detection of EGFR mutation using mutation-specific antibodies in lung cancer. Clin Cancer Res 16: 3349-3355.
17. Simonetti S, Molina MA, Queralt C, de Aguirre I, Mayo C, et al. (2010) Detection of EGFR mutations with mutation-specific antibodies in stage IV non-small-cell lung cancer. J Transl Med 8: 135.
18. Ilie MI, Hofman V, Bonnetaud C, Havet K, Lespinet-Fabre V, et al. (2010) Usefulness of tissue microarrays for assessment of protein expression, gene copy number and mutational status of EGFR in lung adenocarcinoma. Virchows Arch 457: 483-495.
19. Kozu Y, Tsuta K, Kohno T, Sekine I, Yoshida A, et al. (2011) The usefulness of mutation-specific antibodies in detecting epidermal growth factor receptor mutations and in predicting response to tyrosine kinase inhibitor therapy in lung adenocarcinoma. Lung Cancer 73: 45-50.
20. Zhou Q, Zhang XC, Chen ZH, Yin XL, Yang JJ, et al. (2011) Relative abundance of EGFR mutations predicts benefit from gefitinib treatment for advanced non-small-cell lung cancer. J Clin Oncol 29: 3316-3321.
21. Azuma K, Okamoto I, Kawahara A, Taira T, Nakashima K, et al. (2012) Association of the expression of mutant epidermal growth factor receptor protein as determined with mutation-specific antibodies in non-small cell lung cancer with progression-free survival after gefitinib treatment. J Thorac Oncol 7: 122-127.
22. 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.
23. Conde E, Angulo B, Tang M, Morente M, Torres-Lanzas J, et al. (2006) Molecular context of the epidermal growth factor receptor mutations: evidence for the activation of mTOR/S6K signaling. Clin Cancer Res 12: 710-717.
24. Clayton SJ, Scott FM, Walker J, Callaghan K, Haque K, et al. (2000) K-ras point mutation detection in lung cancer: comparison of two approaches to somatic mutation detection using ARMS allele-specific amplification. Clin Chem 46: 1929-1938.
25. Thelwell N, Millington S, Solinas A, Booth J, Brown T, (2000) Mode of action and application of Scorpion primers to mutation detection. Nucleic Acids Res 28: 3752-3761.
26. Whitcombe D, Theaker J, Guy SP, Brown T, Little S, (1999) Detection of PCR products using self-probing amplicons and fluorescence. Nature Biotechnol 17: 804-807.
27. Hirsch FR, Wynes MW, Gandara DR, Bunn PA Jr, (2010) The tissue is the issue: personalized medicine for non-small cell lung cancer. Clin Cancer Res 16: 4909-4911.
28. Mok TS, (2011) Personalized medicine in lung cancer: what we need to know. Nat Rev Clin Oncol 8: 661-668.
29. Janku F, Garrido-Laguna I, Petruzelka LB, Stewart DJ, Kurzrock R, (2011) Novel therapeutic targets in non-small cell lung cancer. J Thorac Oncol 6: 1601-1612.
30. Pao W, Girard N, (2011) New driver mutations in non-small-cell lung cancer. Lancet Oncol 12: 175-180.
31. Pao W, Ladanyi M, (2007) Epidermal growth factor receptor mutation testing in lung cancer: searching for the ideal method. Clin Cancer Res 13: 4954-4955.
32. Willmore-Payne C, Holden JA, Layfield LJ, (2006) Detection of epidermal growth factor receptor and human epidermal growth factor receptor 2 activating mutations in lung adenocarcinoma by high-resolution melting amplicon analysis: correlation with gene copy number, protein expression, and hormone receptor expression. Hum Pathol 37: 755-763.
33. Angulo B, Conde E, Martínez R, Rubio-Viqueira B, López-Ríos F, (2011) Analytic performance of a novel real-time PCR method for the detection of mutations in EGFR in formalin-fixed paraffin-embedded tissue (FFPET) samples of lung cancer. J Thorac Oncol 6: S1061.
34. 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.
35. 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.
36. 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.
37. Sharma SV, Bell DW, Settleman J, Harber DA, (2007) Epidermal growth factor receptor mutations in lung cancer. Nat Rev Cancer 7: 169-181.
38. 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.
39. 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.
40. 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.
41. Marchetti A, Felicioni L, Buttitta F, (2006) Assessing EGFR mutations. N Engl J Med 354: 526-528.
42. Ellison G, Donald E, McWalter G, Knight L, Fletcher L, et al. (2010) A comparison of ARMS and DNA sequencing for mutation analysis in clinical biopsy samples. J Exp Clin Cancer Res 29: 132.
43. 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.
44. Zhu CQ, da Cunha Santos G, Ding K, Sakurada A, Cutz JC, et al. (2008) Role of KRAS and EGFR as biomarkers of response to erlotinib in National Cancer Institute of Canada Clinical Trials Group Study BR.21. J Clin Oncol 26: 4268-4275.
45. Salto-Tellez M, Tsao MS, Shih JY, Thongprasert S, Lu S, et al. (2011) Clinical and testing protocols for the analysis of epidermal growth factor receptor mutations in East Asian patients with non-small cell lung cancer: a combined clinical-molecular pathological approach. J Thorac Oncol 6: 1663-1669.
46. Jänne PA, Borras AM, Kuang Y, Rogers AM, Joshi VA, et al. (2006) A rapid and sensitive enzymatic method for epidermal growth factor receptor mutation screening. Clin Cancer Res 12: 751-758.
47. 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.
48. 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.
49. Dacic S, (2011) Lung carcinoma morphology or mutational profile: that is the question. Arch Pathol Lab Med 135: 1242-1243.
50. Conde E, Angulo B, Redondo P, Toldos O, García-García E, et al. (2010) The use of P63 immunohistochemistry for the identification of squamous cell carcinoma of the lung. PLoS One 5: e12209.
51. Chen ZY, Zhong WZ, Zhang XC, Su J, Yang XN, et al. (2012) EGFR Mutation Heterogeneity and the Mixed Response to EGFR Tyrosine Kinase Inhibitors of Lung Adenocarcinomas. Oncologist 17: 978-985.
52. Bai H, Wang Z, Chen K, Zhao J, Lee JJ, et al. (2012) Influence of Chemotherapy on EGFR Mutation Status Among Patients With Non-Small-Cell Lung Cancer. J Clin Oncol Jul 23 [Epub ahead of print].
53. Yasuda H, Kobayashi S, Costa DB, (2012) EGFR exon 20 insertion mutations in non-small-cell lung cancer: preclinical data and clinical implications. Lancet Oncol 13: e23-31.
54. De Pas T, Toffalorio F, Manzotti M, Fumagalli C, Spitaleri G, et al. (2011) Activity of epidermal growth factor receptor-tyrosine kinase inhibitors in patients with non-small cell lung cancer harboring rare epidermal growth factor receptor mutations. J Thorac Oncol 6: 1895-1901.