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[Cancer Research 64, 8919-8923, December 15, 2004]
© 2004 American Association for Cancer Research

Regular Articles

Mutations of the Epidermal Growth Factor Receptor Gene in Lung Cancer

Biological and Clinical Implications

Takayuki Kosaka1,3, Yasushi Yatabe2, Hideki Endoh1,3, Hiroyuki Kuwano3, Takashi Takahashi4 and Tetsuya Mitsudomi1,2

1 Departments of Thoracic Surgery and 2 Pathology and Molecular Diagnostics, Aichi Cancer Center Hospital, Nagoya, Japan; 3 Department of Surgery I, Gunma University School of Medicine, Gunma, Japan; and 4 Division of Molecular Oncology, Aichi Cancer Center Research Institute, Nagoya, Japan

Recently it has been reported that mutations in the tyrosine kinase domain of the epidermal growth factor receptor(EGFR) gene occur in a subset of patients with lung cancer showing a dramatic response to EGFR tyrosine kinase inhibitors. To gain further insights in the role of EGFR in lung carcinogenesis, we sequenced exons 18–21 of the tyrosine kinase domain using total RNA extracted from unselected 277 patients with lung cancer who underwent surgical resection and correlated the results with clinical and pathologic features. EGFR mutations were present in 111 patients (40%). Fifty-two were in-frame deletions around codons 746–750 in exon 19, 54 were point mutations including 49 at codon 858 in exon 21 and 4 at codon 719 in exon 18, and 5 were duplications/insertions mainly in exon 20. They were significantly more frequent in female (P < 0.001), adenocarcinomas (P = 0.0013), and in never-smokers (P < 0.001). Multivariate analysis suggested EGFR mutations were independently associated with adenocarcinoma histology (P = 0.0012) and smoking status (P < 0.001), but not with female gender (P = 0.9917). In adenocarcinomas, EGFR mutations were more frequent in well to moderately differentiated tumors (P < 0.001) but were independent of patient age, disease stages, or patient survival. KRAS and TP53 mutations were present in 13 and 41%, respectively. EGFR mutations never occurred in tumors with KRAS mutations, whereas EGFR mutations were independent of TP53 mutations. EGFR mutations define a distinct subset of pulmonary adenocarcinoma without KRAS mutations, which is not caused by tobacco carcinogens.




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A. Seow, D. P. Ng, S. Choo, P. Eng, W.-T. Poh, T. Ming, and Y.-T. Wang
Joint effect of asthma/atopy and an IL-6 gene polymorphism on lung cancer risk among lifetime non-smoking Chinese women
Carcinogenesis, June 1, 2006; 27(6): 1240 - 1244.
[Abstract] [Full Text] [PDF]

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 JCOHome page
J. Baselga
Is There a Role for the Irreversible Epidermal Growth Factor Receptor Inhibitor EKB-569 in the Treatment of Cancer? A Mutation-Driven Question
J. Clin. Oncol., May 20, 2006; 24(15): 2225 - 2226.
[Full Text] [PDF]

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 JCOHome page
E. Calvo and J. Baselga
Ethnic Differences in Response to Epidermal Growth Factor Receptor Tyrosine Kinase Inhibitors
J. Clin. Oncol., May 10, 2006; 24(14): 2158 - 2163.
[Abstract] [Full Text] [PDF]

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 Clin. Cancer Res.Home page
S.-W. Han, T.-Y. Kim, Y. K. Jeon, P. G. Hwang, S.-A. Im, K.-H. Lee, J. H. Kim, D.-W. Kim, D. S. Heo, N. K. Kim, et al.
Optimization of Patient Selection for Gefitinib in Non-Small Cell Lung Cancer by Combined Analysis of Epidermal Growth Factor Receptor Mutation, K-ras Mutation, and Akt Phosphorylation
Clin. Cancer Res., April 15, 2006; 12(8): 2538 - 2544.
[Abstract] [Full Text] [PDF]

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 JCOHome page
D. Pham, M. G. Kris, G. J. Riely, I. S. Sarkaria, T. McDonough, S. Chuai, E. S. Venkatraman, V. A. Miller, M. Ladanyi, W. Pao, et al.
Use of Cigarette-Smoking History to Estimate the Likelihood of Mutations in Epidermal Growth Factor Receptor Gene Exons 19 and 21 in Lung Adenocarcinomas
J. Clin. Oncol., April 10, 2006; 24(11): 1700 - 1704.
[Abstract] [Full Text] [PDF]

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 JCOHome page
T. Takeuchi, S. Tomida, Y. Yatabe, T. Kosaka, H. Osada, K. Yanagisawa, T. Mitsudomi, and T. Takahashi
Expression Profile-Defined Classification of Lung Adenocarcinoma Shows Close Relationship With Underlying Major Genetic Changes and Clinicopathologic Behaviors
J. Clin. Oncol., April 10, 2006; 24(11): 1679 - 1688.
[Abstract] [Full Text] [PDF]

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 Neuro OncolHome page
S. Shimato, T. Mitsudomi, T. Kosaka, Y. Yatabe, T. Wakabayashi, M. Mizuno, N. Nakahara, H. Hatano, A. Natsume, D. Ishii, et al.
EGFR mutations in patients with brain metastases from lung cancer: Association with the efficacy of gefitinib
Neuro-oncol, April 1, 2006; 8(2): 137 - 144.
[Abstract] [Full Text] [PDF]

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 The OncologistHome page
D. S. Ettinger
Clinical Implications of EGFR Expression in the Development and Progression of Solid Tumors: Focus on Non-Small Cell Lung Cancer.
Oncologist, April 1, 2006; 11(4): 358 - 373.
[Abstract] [Full Text] [PDF]

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 Clin. Cancer Res.Home page
F. Leone, G. Cavalloni, Y. Pignochino, I. Sarotto, R. Ferraris, W. Piacibello, T. Venesio, L. Capussotti, M. Risio, and M. Aglietta
Somatic mutations of epidermal growth factor receptor in bile duct and gallbladder carcinoma.
Clin. Cancer Res., March 15, 2006; 12(6): 1680 - 1685.
[Abstract] [Full Text] [PDF]

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 JCOHome page
T. Takano, Y. Ohe, I. Sekine, H. Kunitoh, T. Yoshida, and T. Tamura
In Reply:
J. Clin. Oncol., March 1, 2006; 24(7): 1221 - 1221.
[Full Text] [PDF]

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 Clin. Cancer Res.Home page
I. Y. S. Tam, L. P. Chung, W. S. Suen, E. Wang, M. C.M. Wong, K. K. Ho, W. K. Lam, S. W. Chiu, L. Girard, J. D. Minna, et al.
Distinct Epidermal Growth Factor Receptor and KRAS Mutation Patterns in Non-Small Cell Lung Cancer Patients with Different Tobacco Exposure and Clinicopathologic Features
Clin. Cancer Res., March 1, 2006; 12(5): 1647 - 1653.
[Abstract] [Full Text] [PDF]

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 Cancer Res.Home page
S. Toyooka, M. Tokumo, H. Shigematsu, K. Matsuo, H. Asano, K. Tomii, S. Ichihara, M. Suzuki, M. Aoe, H. Date, et al.
Mutational and Epigenetic Evidence for Independent Pathways for Lung Adenocarcinomas Arising in Smokers and Never Smokers
Cancer Res., February 1, 2006; 66(3): 1371 - 1375.
[Abstract] [Full Text] [PDF]

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 Clin. Cancer Res.Home page
E. Conde, B. Angulo, M. Tang, M. Morente, J. Torres-Lanzas, A. Lopez-Encuentra, F. Lopez-Rios, and M. Sanchez-Cespedes
Molecular Context of the EGFR Mutations: Evidence for the Activation of mTOR/S6K Signaling
Clin. Cancer Res., February 1, 2006; 12(3): 710 - 717.
[Abstract] [Full Text] [PDF]

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 Clin. Cancer Res.Home page
G. J. Riely, W. Pao, D. Pham, A. R. Li, N. Rizvi, E. S. Venkatraman, M. F. Zakowski, M. G. Kris, M. Ladanyi, and V. A. Miller
Clinical Course of Patients with Non-Small Cell Lung Cancer and Epidermal Growth Factor Receptor Exon 19 and Exon 21 Mutations Treated with Gefitinib or Erlotinib
Clin. Cancer Res., February 1, 2006; 12(3): 839 - 844.
[Abstract] [Full Text] [PDF]

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 The Annals of PharmacotherapyHome page
D. A Frieze and J. S McCune
Current Status of Cetuximab for the Treatment of Patients with Solid Tumors
Ann. Pharmacother., February 1, 2006; 40(2): 241 - 250.
[Abstract] [Full Text] [PDF]

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 Clin. Cancer Res.Home page
H. Asano, S. Toyooka, M. Tokumo, K. Ichimura, K. Aoe, S. Ito, K. Tsukuda, M. Ouchida, M. Aoe, H. Katayama, et al.
Detection of EGFR Gene Mutation in Lung Cancer by Mutant-Enriched Polymerase Chain Reaction Assay
Clin. Cancer Res., January 1, 2006; 12(1): 43 - 48.
[Abstract] [Full Text] [PDF]

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 Clin. Cancer Res.Home page
J. W. Lee, Y. H. Soung, S. H. Seo, S. Y. Kim, C. H. Park, Y. P. Wang, K. Park, S. W. Nam, W. S. Park, S. H. Kim, et al.
Somatic Mutations of ERBB2 Kinase Domain in Gastric, Colorectal, and Breast Carcinomas
Clin. Cancer Res., January 1, 2006; 12(1): 57 - 61.
[Abstract] [Full Text] [PDF]

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 Cancer Res.Home page
N. Fujimoto, M. Wislez, J. Zhang, K. Iwanaga, J. Dackor, A. E. Hanna, S. Kalyankrishna, D. D. Cody, R. E. Price, M. Sato, et al.
High Expression of ErbB Family Members and Their Ligands in Lung Adenocarcinomas That Are Sensitive to Inhibition of Epidermal Growth Factor Receptor
Cancer Res., December 15, 2005; 65(24): 11478 - 11485.
[Abstract] [Full Text] [PDF]

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 Clin. Cancer Res.Home page
E. E.W. Cohen, M. W. Lingen, L. E. Martin, P. L. Harris, B. W. Brannigan, S. M. Haserlat, R. A. Okimoto, D. C. Sgroi, S. Dahiya, B. Muir, et al.
Response of Some Head and Neck Cancers to Epidermal Growth Factor Receptor Tyrosine Kinase Inhibitors May Be Linked to Mutation of ERBB2 rather than EGFR
Clin. Cancer Res., November 15, 2005; 11(22): 8105 - 8108.
[Abstract] [Full Text] [PDF]

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 JCOHome page
D. W. Bell, T. J. Lynch, S. M. Haserlat, P. L. Harris, R. A. Okimoto, B. W. Brannigan, D. C. Sgroi, B. Muir, M. J. Riemenschneider, R. B. Iacona, et al.
Epidermal Growth Factor Receptor Mutations and Gene Amplification in Non-Small-Cell Lung Cancer: Molecular Analysis of the IDEAL/INTACT Gefitinib Trials
J. Clin. Oncol., November 1, 2005; 23(31): 8081 - 8092.
[Abstract] [Full Text] [PDF]

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 JCOHome page
T. Takano, Y. Ohe, H. Sakamoto, K. Tsuta, Y. Matsuno, U. Tateishi, S. Yamamoto, H. Nokihara, N. Yamamoto, I. Sekine, et al.
Epidermal Growth Factor Receptor Gene Mutations and Increased Copy Numbers Predict Gefitinib Sensitivity in Patients With Recurrent Non-Small-Cell Lung Cancer
J. Clin. Oncol., October 1, 2005; 23(28): 6829 - 6837.
[Abstract] [Full Text] [PDF]

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 JCOHome page
B. E. Johnson and P. A. Janne
Selecting Patients for Epidermal Growth Factor Receptor Inhibitor Treatment: A FISH Story or a Tale of Mutations?
J. Clin. Oncol., October 1, 2005; 23(28): 6813 - 6816.
[Full Text] [PDF]

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 Clin. Cancer Res.Home page
Y. Tomizawa, H. Iijima, N. Sunaga, K. Sato, A. Takise, Y. Otani, S. Tanaka, T. Suga, R. Saito, T. Ishizuka, et al.
Clinicopathologic Significance of the Mutations of the Epidermal Growth Factor Receptor Gene in Patients with Non-Small Cell Lung Cancer
Clin. Cancer Res., October 1, 2005; 11(19): 6816 - 6822.
[Abstract] [Full Text] [PDF]

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 The OncologistHome page
M. G. Kris
How Today's Developments in the Treatment of Non-Small Cell Lung Cancer Will Change Tomorrow's Standards of Care
Oncologist, October 1, 2005; 10(suppl_2): 23 - 29.
[Abstract] [Full Text] [PDF]

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 Cancer Res.Home page
B. E. Johnson and P. A. Janne
Epidermal Growth Factor Receptor Mutations in Patients with Non-Small Cell Lung Cancer
Cancer Res., September 1, 2005; 65(17): 7525 - 7529.
[Abstract] [Full Text] [PDF]

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 Cancer Res.Home page
X. Tang, H. Shigematsu, B. N. Bekele, J. A. Roth, J. D. Minna, W. K. Hong, A. F. Gazdar, and I. I. Wistuba
EGFR Tyrosine Kinase Domain Mutations Are Detected in Histologically Normal Respiratory Epithelium in Lung Cancer Patients
Cancer Res., September 1, 2005; 65(17): 7568 - 7572.
[Abstract] [Full Text] [PDF]

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 Clin. Cancer Res.Home page
T. Shibata, S. Uryu, A. Kokubu, F. Hosoda, M. Ohki, T. Sakiyama, Y. Matsuno, R. Tsuchiya, Y. Kanai, T. Kondo, et al.
Genetic Classification of Lung Adenocarcinoma Based on Array-Based Comparative Genomic Hybridization Analysis: Its Association with Clinicopathologic Features
Clin. Cancer Res., September 1, 2005; 11(17): 6177 - 6185.
[Abstract] [Full Text] [PDF]

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 JCOHome page
A. P. Dicker and U. Rodeck
Predicting the Future From Trials of the Past: Epidermal Growth Factor Receptor Expression and Outcome of Fractionated Radiation Therapy Trials
J. Clin. Oncol., August 20, 2005; 23(24): 5437 - 5439.
[Full Text] [PDF]

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 JNCI J Natl Cancer InstHome page
T. Mukohara, J. A. Engelman, N. H. Hanna, B. Y. Yeap, S. Kobayashi, N. Lindeman, B. Halmos, J. Pearlberg, Z. Tsuchihashi, L. C. Cantley, et al.
Differential Effects of Gefitinib and Cetuximab on Non-small-cell Lung Cancers Bearing Epidermal Growth Factor Receptor Mutations
J Natl Cancer Inst, August 17, 2005; 97(16): 1185 - 1194.
[Abstract] [Full Text] [PDF]

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 Cancer Res.Home page
S. Kobayashi, H. Ji, Y. Yuza, M. Meyerson, K.-K. Wong, D. G. Tenen, and B. Halmos
An Alternative Inhibitor Overcomes Resistance Caused by a Mutation of the Epidermal Growth Factor Receptor
Cancer Res., August 15, 2005; 65(16): 7096 - 7101.
[Abstract] [Full Text] [PDF]

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 Cancer Res.Home page
Y. Nagai, H. Miyazawa, Huqun, T. Tanaka, K. Udagawa, M. Kato, S. Fukuyama, A. Yokote, K. Kobayashi, M. Kanazawa, 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., August 15, 2005; 65(16): 7276 - 7282.
[Abstract] [Full Text] [PDF]

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 Clin. Cancer Res.Home page
M. Taron, Y. Ichinose, R. Rosell, T. Mok, B. Massuti, L. Zamora, J. L. Mate, C. Manegold, M. Ono, C. Queralt, et al.
Activating Mutations in the Tyrosine Kinase Domain of the Epidermal Growth Factor Receptor Are Associated with Improved Survival in Gefitinib-Treated Chemorefractory Lung Adenocarcinomas
Clin. Cancer Res., August 15, 2005; 11(16): 5878 - 5885.
[Abstract] [Full Text] [PDF]

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 J. Mol. Diagn.Home page
Q. Pan, W. Pao, and M. Ladanyi
Rapid Polymerase Chain Reaction-Based Detection of Epidermal Growth Factor Receptor Gene Mutations in Lung Adenocarcinomas
J. Mol. Diagn., August 1, 2005; 7(3): 396 - 403.
[Abstract] [Full Text] [PDF]

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 Clin. Cancer Res.Home page
R. J. Schilder, M. W. Sill, X. Chen, K. M. Darcy, S. L. Decesare, G. Lewandowski, R. B. Lee, C. A. Arciero, H. Wu, and A. K. Godwin
Phase II Study of Gefitinib in Patients with Relapsed or Persistent Ovarian or Primary Peritoneal Carcinoma and Evaluation of Epidermal Growth Factor Receptor Mutations and Immunohistochemical Expression: A Gynecologic Oncology Group Study
Clin. Cancer Res., August 1, 2005; 11(15): 5539 - 5548.
[Abstract] [Full Text] [PDF]

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 The OncologistHome page
R. L. Comis
The Current Situation: Erlotinib (Tarceva(R)) and Gefitinib (Iressa(R)) in Non-Small Cell Lung Cancer
Oncologist, August 1, 2005; 10(7): 467 - 470.
[Full Text] [PDF]

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 NEJMHome page
M. S. Tsao, A. Sakurada, J.-C. Cutz, C.-Q. Zhu, S. Kamel-Reid, J. Squire, I. Lorimer, T. Zhang, N. Liu, M. Daneshmand, et al.
Erlotinib in Lung Cancer -- Molecular and Clinical Predictors of Outcome
N. Engl. J. Med., July 14, 2005; 353(2): 133 - 144.
[Abstract] [Full Text] [PDF]

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 Clin. Cancer Res.Home page
X. L. Mu, L. Y. Li, X. T. Zhang, M. Z. Wang, R. E. Feng, Q. C. Cui, H. S. Zhou, and B. Q. Guo
Gefitinib-Sensitive Mutations of the Epidermal Growth Factor Receptor Tyrosine Kinase Domain in Chinese Patients with Non-Small Cell Lung Cancer
Clin. Cancer Res., June 15, 2005; 11(12): 4289 - 4294.
[Abstract] [Full Text] [PDF]

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 NEJMHome page
S. Toyooka, K. Kiura, T. Mitsudomi, S. Kobayashi, D. G. Tenen, and B. Halmos
EGFR Mutation and Response of Lung Cancer to Gefitinib
N. Engl. J. Med., May 19, 2005; 352(20): 2136 - 2136.
[Full Text] [PDF]

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 Clin. Cancer Res.Home page
T.-Y. Chou, C.-H. Chiu, L.-H. Li, C.-Y. Hsiao, C.-Y. Tzen, K.-T. Chang, Y.-M. Chen, R.-P. Perng, S.-F. Tsai, and C.-M. Tsai
Mutation in the Tyrosine Kinase Domain of Epidermal Growth Factor Receptor Is a Predictive and Prognostic Factor for Gefitinib Treatment in Patients with Non-Small Cell Lung Cancer
Clin. Cancer Res., May 15, 2005; 11(10): 3750 - 3757.
[Abstract] [Full Text] [PDF]

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 JCOHome page
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., May 10, 2005; 23(14): 3227 - 3234.
[Abstract] [Full Text] [PDF]


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