Standardization of epidermal growth factor receptor (EGFR) measurement by quantitative immunofluorescence and impact on antibody-based mutation detection in non-small cell lung cancer

American Journal of Pathology

Volumn 179, Issue 2, 2011, Pages 580-589

  Dimou, Anastasios ^a   Agarwal, Seema ^a   Anagnostou, Valsamo ^a   Viray, Hollis ^a   Christensen, Stephen ^a   Gould Rothberg, Bonnie ^a   Zolota, Vassiliki ^c   Syrigos, Konstantinos ^b   Rimm, David L ^a  

^a YALE UNIVERSITY SCHOOL OF MEDICINE   (United States)

^b YALE CANCER CENTER   (United States)

^c UNIVERSITY HOSPITAL OF PATRAS   (Greece)

Author keywords

[No Author keywords available]

Indexed keywords

EPIDERMAL GROWTH FACTOR RECEPTOR;

ANTIBODY DETECTION; ARTICLE; CANCER SURVIVAL; CONTROLLED STUDY; DISEASE ASSOCIATION; DNA SEQUENCE; FALSE POSITIVE RESULT; FEMALE; GENE MUTATION; GENOTYPE; HISTOPATHOLOGY; HUMAN; HUMAN CELL; HUMAN TISSUE; IMMUNOFLUORESCENCE TEST; LUNG NON SMALL CELL CANCER; MAJOR CLINICAL STUDY; MALE; PRIORITY JOURNAL; PROGNOSIS; PROTEIN ANALYSIS; PROTEIN EXPRESSION; PROTEIN FUNCTION; QUANTITATIVE STUDY; REPRODUCIBILITY; SQUAMOUS CELL CARCINOMA;

ADULT; AGED; AGED, 80 AND OVER; BLOTTING, WESTERN; CARCINOMA, NON-SMALL-CELL LUNG; COHORT STUDIES; DNA MUTATIONAL ANALYSIS; FEMALE; GENE EXPRESSION REGULATION, NEOPLASTIC; GENOTYPE; HUMANS; LUNG NEOPLASMS; MALE; MICROSCOPY, FLUORESCENCE; MIDDLE AGED; MUTATION; PROGNOSIS; RECEPTOR, EPIDERMAL GROWTH FACTOR;

EID: 80052428201     PISSN: 00029440     EISSN: 15252191     Source Type: Journal    
DOI: 10.1016/j.ajpath.2011.04.031     Document Type: Article

References (42)

1. A. Jemal, R. Siegel, J. Xu, and E. Ward Cancer Statistics, 2010 CA Cancer J Clin 60 2010 277 300
2. F.A. Shepherd, J. Rodrigues Pereira, T. Ciuleanu, E.H. Tan, V. Hirsh, S. Thongprasert, D. Campos, S. Maoleekoonpiroj, M. Smylie, R. Martins, M. van Kooten, M. Dediu, B. Findlay, D. Tu, D. Johnston, A. Bezjak, G. Clark, P. Santabarbara, and L. Seymour Erlotinib in previously treated non-small-cell lung cancer N Engl J Med 353 2005 123 132 (Pubitemid 41058344)
3. T.J. Lynch, D.W. Bell, R. Sordella, S. Gurubhagavatula, R.A. Okimoto, B.W. Brannigan, P.L. Harris, S.M. Haserlat, J.G. Supko, F.G. Haluska, D.N. Louis, D.C. Christiani, J. Settleman, and D.A. Haber Activating mutations in the epidermal growth factor receptor underlying responsiveness of non-small-cell lung cancer to gefitinib N Engl J Med 350 2004 2129 2139 (Pubitemid 38637993)
4. W. Pao, V. Miller, M. Zakowski, J. Doherty, K. Politi, I. Sarkaria, B. Singh, R. Heelan, V. Rusch, L. Fulton, E. Mardis, D. Kupfer, R. Wilson, M. Kris, and H. Varmus 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 2004 13306 13311 (Pubitemid 39209661)
5. P.A. Janne, J.A. Engelman, and B.E. Johnson Epidermal growth factor receptor mutations in non-small-cell lung cancer: implications for treatment and tumor biology J Clin Oncol 23 2005 3227 3234 (Pubitemid 46211347)
6. T. Kosaka, Y. Yatabe, H. Endoh, H. Kuwano, T. Takahashi, and T. Mitsudomi Mutations of the epidermal growth factor receptor gene in lung cancer: biological and clinical implications Cancer Res 64 2004 8919 8923 (Pubitemid 39665498)
7. G.J. Riely, K.A. Politi, V.A. Miller, and W. Pao Update on epidermal growth factor receptor mutations in nonsmall cell lung cancer Clin Cancer Res 12 2006 7232 7241 (Pubitemid 46095394)
8. T.S. Mok, Y.L. Wu, S. Thongprasert, C.H. Yang, D.T. Chu, N. Saijo, P. Sunpaweravong, B. Han, B. Margono, Y. Ichinose, Y. Nishiwaki, Y. Ohe, J.J. Yang, B. Chewaskulyong, H. Jiang, E.L. Duffield, C.L. Watkins, A.A. Armour, and M. Fukuoka Gefitinib or carboplatin-paclitaxel in pulmonary adenocarcinoma N Engl J Med 361 2009 947 957
9. J. Yu, S. Kane, J. Wu, E. Benedettini, D. Li, C. Reeves, G. Innocenti, R. Wetzel, K. Crosby, A. Becker, M. Ferrante, W.C. Cheung, X. Hong, L.R. Chirieac, L.M. Sholl, H. Haack, B.L. Smith, R.D. Polakiewicz, Y. Tan, T.L. Gu, M. Loda, X. Zhou, and M.J. Comb Mutation-specific antibodies for the detection of EGFR mutations in non-small-cell lung cancer Clinical Cancer Res 15 2009 3023 3028
10. M. Brevet, M. Arcila, and M. Ladanyi 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 2010 169 176
11. D. Veale, N. Kerr, G.J. Gibson, P.J. Kelly, and A.L. Harris The relationship of quantitative epidermal growth factor receptor expression in nonsmall cell lung cancer to long-term survival Br J Cancer 68 1993 162 165 (Pubitemid 23178571)
12. V.K. Anagnostou, A.W. Welsh, J.M. Giltnane, S. Siddiqui, C. Liceaga, M. Gustavson, K.N. Syrigos, J.L. Reiter, and D.L. Rimm Analytic variability in immunohistochemistry biomarker studies Cancer Epidemiol Biomarkers Prev 19 2010 982 991
13. D.C. Allred, J.M. Harvey, M. Berardo, and G.M. Clark Prognostic and predictive factors in breast cancer by immunohistochemical analysis Mod Pathol 11 1998 155 168 (Pubitemid 28144151)
14. A. Rhodes, B. Jasani, A.J. Balaton, D.M. Barnes, E. Anderson, L.G. Bobrow, and K.D. Miller Study of interlaboratory reliability and reproducibility of estrogen and progesterone receptor assays in Europe: documentation of poor reliability and identification of insufficient microwave antigen retrieval time as a major contributory element of unreliable assays Am J Clin Pathol 115 2001 44 58 (Pubitemid 33695090)
15. A. Rhodes, B. Jasani, A.J. Balaton, and K.D. Miller Immunohistochemical demonstration of oestrogen and progesterone receptors: correlation of standards achieved on in house tumours with that achieved on external quality assessment material in over 150 laboratories from 26 countries J Clin Pathol 53 2000 292 301 (Pubitemid 30180402)
16. G. Selvaggi, S. Novello, V. Torri, E. Leonardo, P. De Giuli, P. Borasio, C. Mossetti, F. Ardissone, P. Lausi, and G.V. Scagliotti Epidermal growth factor receptor overexpression correlates with a poor prognosis in completely resected non-small-cell lung cancer Ann Oncol 15 2004 28 32 (Pubitemid 38139599)
17. A.P. Meert, B. Martin, P. Delmotte, T. Berghmans, J.J. Lafitte, C. Mascaux, M. Paesmans, E. Steels, J.M. Verdebout, and J.P. Sculier The role of EGF-R expression on patient survival in lung cancer: a systematic review with meta-analysis Eur Respir J 20 2002 975 981 (Pubitemid 35175137)
18. U. Pastorino, S. Andreola, E. Tagliabue, F. Pezzella, M. Incarbone, G. Sozzi, M. Buyse, S. Menard, M. Pierotti, and F. Rilke Immunocytochemical markers in stage I lung cancer: relevance to prognosis J Clin Oncol 15 1997 2858 2865 (Pubitemid 27330013)
19. P. Ceppi, M. Volante, S. Novello, I. Rapa, K.D. Danenberg, P.V. Danenberg, A. Cambieri, G. Selvaggi, S. Saviozzi, R. Calogero, M. Papotti, and G.V. Scagliotti ERCC1 and RRM1 gene expressions but not EGFR are predictive of shorter survival in advanced non-small-cell lung cancer treated with cisplatin and gemcitabine Ann Oncol 17 2006 1818 1825 (Pubitemid 44884058)
20. P. Pfeiffer, P.P. Clausen, K. Andersen, and C. Rose Lack of prognostic significance of epidermal growth factor receptor and the oncoprotein p185HER-2 in patients with systemically untreated non-small-cell lung cancer: an immunohistochemical study on cryosections Br J Cancer 74 1996 86 91 (Pubitemid 26231983)
21. V. Rusch, D. Klimstra, E. Venkatraman, P.W. Pisters, J. Langenfeld, and E. Dmitrovsky Overexpression of the epidermal growth factor receptor and its ligand transforming growth factor alpha is frequent in resectable nonsmall cell lung cancer but does not predict tumor progression Clin Cancer Res 3 1997 515 522 (Pubitemid 27211827)
22. M. Dolled-Filhart, A. McCabe, J. Giltnane, M. Cregger, R.L. Camp, and D.L. Rimm Quantitative in situ analysis of beta-catenin expression in breast cancer shows decreased expression is associated with poor outcome Cancer Res 66 2006 5487 5494 (Pubitemid 43844977)
23. R.L. Camp, G.G. Chung, and D.L. Rimm Automated subcellular localization and quantification of protein expression in tissue microarrays Nat Med 8 2002 1323 1327 (Pubitemid 35373567)
24. A. Fassina, A. Gazziero, D. Zardo, M. Corradin, E. Aldighieri, and G.P. Rossi Detection of EGFR and KRAS mutations on trans-thoracic needle aspiration of lung nodules by high resolution melting analysis J Clin Pathol 62 2009 1096 1102
25. K. Schmid, N. Oehl, F. Wrba, R. Pirker, C. Pirker, and M. Filipits EGFR/KRAS/BRAF mutations in primary lung adenocarcinomas and corresponding locoregional lymph node metastases Clin Cancer Res 15 2009 4554 4560
26. F. Oshita, S. Matsukuma, M. Yoshihara, Y. Sakuma, N. Ohgane, Y. Kameda, H. Saito, K. Yamada, E. Tsuchiya, and Y. Miyagi 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 2006 1070 1075 (Pubitemid 44606834)
27. D.A. Eberhard, B.E. Johnson, L.C. Amler, A.D. Goddard, S.L. Heldens, R.S. Herbst, W.L. Ince, P.A. Janne, T. Januario, D.H. Johnson, P. Klein, V.A. Miller, M.A. Ostland, D.A. Ramies, D. Sebisanovic, J.A. Stinson, Y.R. Zhang, S. Seshagiri, and K.J. Hillan 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 2005 5900 5909
28. R. Rosell, T. Moran, C. Queralt, R. Porta, F. Cardenal, C. Camps, M. Majem, G. Lopez-Vivanco, D. Isla, M. Provencio, A. Insa, B. Massuti, J.L. Gonzalez-Larriba, L. Paz-Ares, I. Bover, R. Garcia-Campelo, M.A. Moreno, S. Catot, C. Rolfo, N. Reguart, R. Palmero, J.M. Sanchez, R. Bastus, C. Mayo, J. Bertran-Alamillo, M.A. Molina, J.J. Sanchez, and M. Taron Screening for epidermal growth factor receptor mutations in lung cancer N Engl J Med 361 2009 958 967
29. F.R. Hirsch, M. Varella-Garcia, J.R. Bunn PA, W.A. Franklin, R. Dziadziuszko, N. Thatcher, A. Chang, P. Parikh, J.R. Pereira, T. Ciuleanu, J. von Pawel, C. Watkins, A. Flannery, G. Ellison, E. Donald, L. Knight, D. Parums, N. Botwood, and B. Holloway Molecular predictors of outcome with gefitinib in a phase III placebo-controlled study in advanced non-small-cell lung cancer J Clin Oncol 24 2006 5034 5042 (Pubitemid 46631407)
30. A.S. Tsao, X.M. Tang, B. Sabloff, L. Xiao, H. Shigematsu, J. Roth, M. Spitz, W.K. Hong, A. Gazdar, and I. Wistuba Clinicopathologic characteristics of the EGFR gene mutation in nonsmall cell lung cancer J Thorac Oncol 1 2006 231 239 (Pubitemid 47181440)
31. H. Shigematsu, L. Lin, T. Takahashi, M. Nomura, M. Suzuki, I.I. Wistuba, K.M. Fong, H. Lee, S. Toyooka, N. Shimizu, T. Fujisawa, Z. Feng, J.A. Roth, J. Herz, J.D. Minna, and A.F. Gazdar Clinical and biological features associated with epidermal growth factor receptor gene mutations in lung cancers J Natl Cancer Inst 97 2005 339 346 (Pubitemid 40425952)
32. T. Kawaguchi, A. Matsumura, S. Fukai, A. Tamura, R. Saito, J.A. Zell, Y. Maruyama, A. Ziogas, M. Kawahara, and S.H. Ignatius Ou Japanese ethnicity compared with Caucasian ethnicity and never-smoking status are independent favorable prognostic factors for overall survival in nonsmall cell lung cancer: a collaborative epidemiologic study of the National Hospital Organization Study Group for Lung Cancer (NHSGLC) in Japan and a Southern California Regional Cancer Registry databases J Thorac Oncol 5 2010 1001 1010
33. R. van Puijenbroek, L. Bosquee, A.P. Meert, D. Schallier, J.C. Goeminne, G. Tits, P. Collard, K. Nackaerts, J.L. Canon, F. Duplaquet, D. Galdermans, P. Germonpre, M.A. Azerad, G. Vandenhoven, J. De Greve, and J. Vansteenkiste Gefitinib monotherapy in advanced nonsmall cell lung cancer: a large Western community implementation study Eur Respir J 29 2007 128 133 (Pubitemid 46092008)
34. F. Pinter, J. Papay, A. Almasi, Z. Sapi, E. Szabo, M. Kanya, A. Tamasi, B. Jori, E. Varkondi, J. Moldvay, K. Szondy, G. Keri, M. Dominici, P. Conte, S. Eckhardt, L. Kopper, R. Schwab, and I. Petak Epidermal growth factor receptor (EGFR) high gene copy number and activating mutations in lung adenocarcinomas are not consistently accompanied by positivity for EGFR protein by standard immunohistochemistry J Mol Diagn 10 2008 160 168 (Pubitemid 351428398)
35. Z. Liang, J. Zhang, X. Zeng, J. Gao, S. Wu, and T. Liu Relationship between EGFR expression, copy number and mutation in lung adenocarcinomas BMC Cancer 10 2010 376
36. A. McCabe, M. Dolled-Filhart, R.L. Camp, and D.L. Rimm Automated quantitative analysis (AQUA) of in situ protein expression, antibody concentration, and prognosis J Natl Cancer Inst 97 2005 1808 1815 (Pubitemid 43033901)
37. Y. Kato, N. Peled, M.W. Wynes, K. Yoshida, M. Pardo, C. Mascaux, T. Ohira, M. Tsuboi, J. Matsubayashi, T. Nagao, N. Ikeda, and F.R. Hirsch Novel epidermal growth factor receptor mutation-specific antibodies for nonsmall cell lung cancer: immunohistochemistry as a possible screening method for epidermal growth factor receptor mutations J Thorac Oncol 5 2010 1551 1558
38. A. Kawahara, C. Yamamoto, K. Nakashima, K. Azuma, S. Hattori, M. Kashihara, H. Aizawa, Y. Basaki, M. Kuwano, M. Kage, T. Mitsudomi, and M. Ono Molecular diagnosis of activating EGFR mutations in nonsmall cell lung cancer using mutation-specific antibodies for immunohistochemical analysis Clin Cancer Res 16 2010 3163 3170
39. A. Kitamura, W. Hosoda, E. Sasaki, T. Mitsudomi, and Y. Yatabe Immunohistochemical detection of EGFR mutation using mutation-specific antibodies in lung cancer Clin Cancer Res 16 2010 3349 3355
40. T. John, G. Liu, and M.S. Tsao 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 2009 S14 S23
41. C. Willmore-Payne, J.A. Holden, C.T. Wittwer, and L.J. Layfield The use of EGFR exon 19 and 21 unlabeled DNA probes to screen for activating mutations in nonsmall cell lung cancer J Biomol Tech 19 2008 217 224
42. V. Cohen, J.S. Agulnik, C. Ang, G. Kasymjanova, G. Batist, D. Small, G. Brandao, G. Chong, and W.H. Miller Jr Epidermal growth factor receptor mutations detected by denaturing high-performance liquid chromatography in nonsmall cell lung cancer: impact on response to therapy with epidermal growth factor receptor-tyrosine kinase inhibitors Cancer 116 2010 4309 4317