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JNCI Journal of the National Cancer Institute 2005 97(5):339-346; doi:10.1093/jnci/dji055
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© 2005 Oxford University Press

ARTICLE

Clinical and Biological Features Associated With Epidermal Growth Factor Receptor Gene Mutations in Lung Cancers

Hisayuki Shigematsu, Li Lin, Takao Takahashi, Masaharu Nomura, Makoto Suzuki, Ignacio I. Wistuba, Kwun M. Fong, Huei Lee, Shinichi Toyooka, Nobuyoshi Shimizu, Takehiko Fujisawa, Ziding Feng, Jack A. Roth, Joachim Herz, John D. Minna, Adi F. Gazdar

Affiliations of authors: Hamon Center for Therapeutic Oncology Research (HS, TT, MN, JDM, AFG), Department of Molecular Genetics (JH), Department of Internal Medicine (JDM), Department of Pharmacology (JDM) and Department of Pathology (AFG), University of Texas Southwestern Medical Center, Dallas, TX; Cancer Prevention Research, Public Health Sciences, Fred Hutchinson Cancer Research Center, Seattle, WA (LL, ZF); Department of Thoracic Surgery, Graduate School of Medicine, Chiba University, Chiba, Japan (MS, TF); Department of Pathology (IIW) and Department of Thoracic and Cardiovascular Surgery (JAR), University of Texas, MD Anderson Cancer Center, Houston, TX; The Prince Charles Hospital, Brisbane, Australia (KMF); Institute of Medical and Molecular Toxicology, Chung Shan Medical University, Taichung, Taiwan (HL); Department of Cancer and Thoracic Surgery, Graduate School of Medicine and Dentistry, Okayama University, Okayama, Japan (HS, ST, NS)

Correspondence to: Adi F. Gazdar, MD, Hamon Center for Therapeutic Oncology Research, University of Texas Southwestern Medical Center, 6000 Harry Hines Boulevard, Dallas, TX 75390-8593 (e-mail: adi.gazdar{at}utsouthwestern.edu).

Background: Mutations in the tyrosine kinase (TK) domain of the epidermal growth factor receptor (EGFR) gene in lung cancers are associated with increased sensitivity of these cancers to drugs that inhibit EGFR kinase activity. However, the role of such mutations in the pathogenesis of lung cancers is unclear. Methods: We sequenced exons 18–21 of the EGFR TK domain from genomic DNA isolated from 617 non-small-cell lung cancers (NSCLCs) and 524 normal lung tissue samples from the same patients and 36 neuroendocrine lung tumors collected from patients in Japan, Taiwan, the United States, and Australia and from 243 other epithelial cancers. Mutation status was compared with clinicopathologic features and with the presence of mutations in KRAS, a gene in the EGFR signaling pathway that is also frequently mutated in lung cancers. All statistical tests were two sided. Results: We detected a total of 134 EGFR TK domain mutations in 130 (21%) of the 617 NSCLCs but not in any of the other carcinomas, nor in nonmalignant lung tissue from the same patients. In NSCLC patients, EGFR TK domain mutations were statistically significantly more frequent in never smokers than ever smokers (51% versus 10%), in adenocarcinomas versus cancer of other histologies (40% versus 3%), in patients of East Asian ethnicity versus other ethnicities (30% versus 8%), and in females versus males (42% versus 14%; all P < .001). EGFR TK domain mutation status was not associated with patient age at diagnosis, clinical stage, the presence of bronchioloalveolar histologic features, or overall survival. The EGFR TK domain mutations we detected were of three common types: in-frame deletions in exon 19, single missense mutations in exon 21, and in-frame duplications/insertions in exon 20. Rare missense mutations were also detected in exons 18, 20, and 21. KRAS gene mutations were present in 50 (8%) of the 617 NSCLCs but not in any tumors with an EGFR TK domain mutation. Conclusions: Mutations in either the EGFR TK domain or the KRAS gene can lead to lung cancer pathogenesis. EGFR TK domain mutations are the first molecular change known to occur specifically in never smokers.


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Correspondence about this Article

Re: Clinical and Biological Features Associated With Epidermal Growth Factor Receptor Gene Mutations in Lung Cancers
Jose R. Pardinas, Li Xiao, Jia Zhang, and Kai Li
J Natl Cancer Inst 2006 98: 362-363. [Extract] [Full Text] [PDF]

Editorial about this Article

EGFR Gene Mutations: A Call for Global x Global Views of Cancer
William R. Sellers and Matthew Meyerson
J Natl Cancer Inst 2005 97: 326-328. [Extract] [Full Text] [PDF]

Related Memo to the Media

Press Release: Study Examines Role of EGFR Gene Mutations in Lung Cancer Development
Sarah L. Zielinski
J Natl Cancer Inst 2005 97: 325. [Extract] [Full Text]



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Radiotherapy in Lung Adenocarcinoma with Brain Metastases: Effects of Activating Epidermal Growth Factor Receptor Mutations on Clinical Response
Clin. Cancer Res., January 1, 2008; 14(1): 162 - 168.
[Abstract] [Full Text] [PDF]

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 Clin. Cancer Res.Home page
S. Toyooka, K. Matsuo, H. Shigematsu, T. Kosaka, M. Tokumo, Y. Yatabe, S. Ichihara, M. Inukai, H. Suehisa, J. Soh, et al.
The Impact of Sex and Smoking Status on the Mutational Spectrum of Epidermal Growth Factor Receptor Gene in Non small Cell Lung Cancer
Clin. Cancer Res., October 1, 2007; 13(19): 5763 - 5768.
[Abstract] [Full Text] [PDF]

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 Molecular Cancer TherapeuticsHome page
J. F. Doody, Y. Wang, S. N. Patel, C. Joynes, S. P. Lee, J. Gerlak, R. L. Rolser, Y. Li, P. Steiner, R. Bassi, et al.
Inhibitory activity of cetuximab on epidermal growth factor receptor mutations in non small cell lung cancers
Mol. Cancer Ther., October 1, 2007; 6(10): 2642 - 2651.
[Abstract] [Full Text] [PDF]

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 JCOHome page
H. Suehisa, S. Toyooka, K. Hotta, A. Uchida, J. Soh, Y. Fujiwara, K. Matsuo, M. Ouchida, M. Takata, K. Kiura, et al.
Epidermal Growth Factor Receptor Mutation Status and Adjuvant Chemotherapy With Uracil-Tegafur for Adenocarcinoma of the Lung
J. Clin. Oncol., September 1, 2007; 25(25): 3952 - 3957.
[Abstract] [Full Text] [PDF]

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 Cancer Res.Home page
D. Padron, M. Sato, J. W. Shay, A. F. Gazdar, J. D. Minna, and M. G. Roth
Epidermal Growth Factor Receptors with Tyrosine Kinase Domain Mutations Exhibit Reduced Cbl Association, Poor Ubiquitylation, and Down-regulation but Are Efficiently Internalized
Cancer Res., August 15, 2007; 67(16): 7695 - 7702.
[Abstract] [Full Text] [PDF]

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 Cancer Res.Home page
A. Ogino, H. Kitao, S. Hirano, A. Uchida, M. Ishiai, T. Kozuki, N. Takigawa, M. Takata, K. Kiura, and M. Tanimoto
Emergence of Epidermal Growth Factor Receptor T790M Mutation during Chronic Exposure to Gefitinib in a Non Small Cell Lung Cancer Cell Line
Cancer Res., August 15, 2007; 67(16): 7807 - 7814.
[Abstract] [Full Text] [PDF]

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 JNCI J Natl Cancer InstHome page
M. Seike, N. Yanaihara, E. D. Bowman, K. A. Zanetti, A. Budhu, K. Kumamoto, L. E. Mechanic, S. Matsumoto, J. Yokota, T. Shibata, et al.
Use of a Cytokine Gene Expression Signature in Lung Adenocarcinoma and the Surrounding Tissue as a Prognostic Classifier
J Natl Cancer Inst, August 15, 2007; 99(16): 1257 - 1269.
[Abstract] [Full Text] [PDF]

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 Clin. Cancer Res.Home page
K.-K. Wong
HKI-272 in Non Small Cell Lung Cancer
Clin. Cancer Res., August 1, 2007; 13(15): 4593s - 4596s.
[Abstract] [Full Text] [PDF]

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 Clin. Cancer Res.Home page
P. D. Bonomi, L. Buckingham, and J. Coon
Selecting Patients for Treatment with Epidermal Growth Factor Tyrosine Kinase Inhibitors
Clin. Cancer Res., August 1, 2007; 13(15): 4606s - 4612s.
[Abstract] [Full Text] [PDF]

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 International Journal of ToxicologyHome page
H.-J. Haussmann
Smoking and Lung Cancer: Future Research Directions
International Journal of Toxicology, July 1, 2007; 26(4): 353 - 364.
[Abstract] [Full Text] [PDF]

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 J. Mol. Diagn.Home page
K. E. Finberg, L. V. Sequist, V. A. Joshi, A. Muzikansky, J. M. Miller, M. Han, J. Beheshti, L. R. Chirieac, E. J. Mark, and A. J. Iafrate
Mucinous Differentiation Correlates with Absence of EGFR Mutation and Presence of KRAS Mutation in Lung Adenocarcinomas with Bronchioloalveolar Features
J. Mol. Diagn., July 1, 2007; 9(3): 320 - 326.
[Abstract] [Full Text] [PDF]

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 The OncologistHome page
C. Gridelli, M. A. Bareschino, C. Schettino, A. Rossi, P. Maione, and F. Ciardiello
Erlotinib in Non-Small Cell Lung Cancer Treatment: Current Status and Future Development
Oncologist, July 1, 2007; 12(7): 840 - 849.
[Abstract] [Full Text] [PDF]

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 Cancer Res.Home page
M. Mounawar, A. Mukeria, F. Le Calvez, R. J. Hung, H. Renard, A. Cortot, C. Bollart, D. Zaridze, P. Brennan, P. Boffetta, et al.
Patterns of EGFR, HER2, TP53, and KRAS Mutations of p14arf Expression in Non-Small Cell Lung Cancers in Relation to Smoking History
Cancer Res., June 15, 2007; 67(12): 5667 - 5672.
[Abstract] [Full Text] [PDF]

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 Cancer Res.Home page
F. Yamasaki, M. J. Johansen, D. Zhang, S. Krishnamurthy, E. Felix, C. Bartholomeusz, R. J. Aguilar, K. Kurisu, G. B. Mills, G. N. Hortobagyi, et al.
Acquired Resistance to Erlotinib in A-431 Epidermoid Cancer Cells Requires Down-regulation of MMAC1/PTEN and Up-regulation of Phosphorylated Akt
Cancer Res., June 15, 2007; 67(12): 5779 - 5788.
[Abstract] [Full Text] [PDF]

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 Clin. Cancer Res.Home page
M. Wislez, M. Antoine, N. Rabbe, V. Gounant, V. Poulot, A. Lavole, J. Fleury-Feith, and J. Cadranel
Neutrophils Promote Aerogenous Spread of Lung Adenocarcinoma with Bronchioloalveolar Carcinoma Features
Clin. Cancer Res., June 15, 2007; 13(12): 3518 - 3527.
[Abstract] [Full Text] [PDF]

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 Clin. Cancer Res.Home page
J. Li, M. Zhao, P. He, M. Hidalgo, and S. D. Baker
Differential Metabolism of Gefitinib and Erlotinib by Human Cytochrome P450 Enzymes
Clin. Cancer Res., June 15, 2007; 13(12): 3731 - 3737.
[Abstract] [Full Text] [PDF]

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 JCOHome page
S. Temam, H. Kawaguchi, A. K. El-Naggar, J. Jelinek, H. Tang, D. D. Liu, W. Lang, J.-P. Issa, J. J. Lee, and L. Mao
Epidermal Growth Factor Receptor Copy Number Alterations Correlate With Poor Clinical Outcome in Patients With Head and Neck Squamous Cancer
J. Clin. Oncol., June 1, 2007; 25(16): 2164 - 2170.
[Abstract] [Full Text] [PDF]

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 JCOHome page
F. Cappuzzo, C. Ligorio, P. A. Janne, L. Toschi, E. Rossi, R. Trisolini, D. Paioli, A. J. Holmes, E. Magrini, G. Finocchiaro, et al.
Prospective Study of Gefitinib in Epidermal Growth Factor Receptor Fluorescence In Situ Hybridization-Positive/Phospho-Akt-Positive or Never Smoker Patients With Advanced Non-Small-Cell Lung Cancer: The ONCOBELL Trial
J. Clin. Oncol., June 1, 2007; 25(16): 2248 - 2255.
[Abstract] [Full Text] [PDF]

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 ChestHome page
A. Horiike, H. Kimura, K. Nishio, F. Ohyanagi, Y. Satoh, S. Okumura, Y. Ishikawa, K. Nakagawa, T. Horai, and M. Nishio
Detection of Epidermal Growth Factor Receptor Mutation in Transbronchial Needle Aspirates of Non-Small Cell Lung Cancer
Chest, June 1, 2007; 131(6): 1628 - 1634.
[Abstract] [Full Text] [PDF]

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 Clin. Cancer Res.Home page
E. Massarelli, M. Varella-Garcia, X. Tang, A. C. Xavier, N. C. Ozburn, D. D. Liu, B. N. Bekele, R. S. Herbst, and I. I. Wistuba
KRAS Mutation Is an Important Predictor of Resistance to Therapy with Epidermal Growth Factor Receptor Tyrosine Kinase Inhibitors in Non-Small-Cell Lung Cancer
Clin. Cancer Res., May 15, 2007; 13(10): 2890 - 2896.
[Abstract] [Full Text] [PDF]

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 Ann OncolHome page
F. Hirsch, M Varella-Garcia, F Cappuzzo, J McCoy, L Bemis, A. Xavier, R Dziadziuszko, P Gumerlock, K Chansky, H West, et al.
Combination of EGFR gene copy number and protein expression predicts outcome for advanced non-small-cell lung cancer patients treated with gefitinib
Ann. Onc., April 1, 2007; 18(4): 752 - 760.
[Abstract] [Full Text] [PDF]

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 J. Clin. Pathol.Home page
C.-K. Toh and W.-T. Lim
Lung cancer in never-smokers
J. Clin. Pathol., April 1, 2007; 60(4): 337 - 340.
[Full Text] [PDF]

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 JCOHome page
F. Leone, Y. Pignochino, G. Cavalloni, and M. Aglietta
Targeting of Epidermal Growth Factor Receptor in Patients Affected by Biliary Tract Carcinoma
J. Clin. Oncol., March 20, 2007; 25(9): 1145 - 1145.
[Full Text] [PDF]

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 JCOHome page
D. M. Jackman, B. Y. Yeap, N. I. Lindeman, P. Fidias, M. S. Rabin, J. Temel, A. T. Skarin, M. Meyerson, A. J. Holmes, A. M. Borras, et al.
Phase II Clinical Trial of Chemotherapy-Naive Patients >= 70 Years of Age Treated With Erlotinib for Advanced Non-Small-Cell Lung Cancer
J. Clin. Oncol., March 1, 2007; 25(7): 760 - 766.
[Abstract] [Full Text] [PDF]

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 Cancer Res.Home page
T. Okabe, I. Okamoto, K. Tamura, M. Terashima, T. Yoshida, T. Satoh, M. Takada, M. Fukuoka, and K. Nakagawa
Differential Constitutive Activation of the Epidermal Growth Factor Receptor in Non-Small Cell Lung Cancer Cells Bearing EGFR Gene Mutation and Amplification
Cancer Res., March 1, 2007; 67(5): 2046 - 2053.
[Abstract] [Full Text] [PDF]

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 J. Med. Genet.Home page
X. Zhang and A. Chang
Somatic mutations of the epidermal growth factor receptor and non-small-cell lung cancer
J. Med. Genet., March 1, 2007; 44(3): 166 - 172.
[Abstract] [Full Text] [PDF]

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 JCOHome page
J. Subramanian and R. Govindan
Lung Cancer in Never Smokers: A Review
J. Clin. Oncol., February 10, 2007; 25(5): 561 - 570.
[Abstract] [Full Text] [PDF]

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 JCOHome page
L. V. Sequist, D. W. Bell, T. J. Lynch, and D. A. Haber
Molecular Predictors of Response to Epidermal Growth Factor Receptor Antagonists in Non-Small-Cell Lung Cancer
J. Clin. Oncol., February 10, 2007; 25(5): 587 - 595.
[Abstract] [Full Text] [PDF]

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 The OncologistHome page
L. Toschi and F. Cappuzzo
Understanding the New Genetics of Responsiveness to Epidermal Growth Factor Receptor Tyrosine Kinase Inhibitors
Oncologist, February 1, 2007; 12(2): 211 - 220.
[Abstract] [Full Text] [PDF]

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 Proc Am Thorac SocHome page
A. C. Borczuk and C. A. Powell
Expression Profiling and Lung Cancer Development
Proceedings of the ATS, January 1, 2007; 4(1): 127 - 132.
[Abstract] [Full Text] [PDF]

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 Ann OncolHome page
N van Zandwijk, A Mathy, L Boerrigter, H Ruijter, I Tielen, D de Jong, P Baas, S Burgers, and P Nederlof
EGFR and KRAS mutations as criteria for treatment with tyrosine kinase inhibitors: retro- and prospective observations in non-small-cell lung cancer
Ann. Onc., January 1, 2007; 18(1): 99 - 103.
[Abstract] [Full Text] [PDF]

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 Clin. Cancer Res.Home page
Y.-L. Chang, C.-T. Wu, S.-C. Lin, C.-F. Hsiao, Y.-S. Jou, and Y.-C. Lee
Clonality and Prognostic Implications of p53 and Epidermal Growth Factor Receptor Somatic Aberrations in Multiple Primary Lung Cancers
Clin. Cancer Res., January 1, 2007; 13(1): 52 - 58.
[Abstract] [Full Text] [PDF]

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 Molecular Cancer TherapeuticsHome page
T. Fukazawa, Y. Maeda, M. L. Durbin, T. Nakai, J. Matsuoka, H. Tanaka, Y. Naomoto, and N. Tanaka
Pulmonary adenocarcinoma-targeted gene therapy by a cancer- and tissue-specific promoter system
Mol. Cancer Ther., January 1, 2007; 6(1): 244 - 252.
[Abstract] [Full Text] [PDF]

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 Am. J. Pathol.Home page
J. Zhang, S. Kalyankrishna, M. Wislez, N. Thilaganathan, B. Saigal, W. Wei, L. Ma, I. I. Wistuba, F. M. Johnson, and J. M. Kurie
Src-Family Kinases Are Activated in Non-Small Cell Lung Cancer and Promote the Survival of Epidermal Growth Factor Receptor-Dependent Cell Lines
Am. J. Pathol., January 1, 2007; 170(1): 366 - 376.
[Abstract] [Full Text] [PDF]

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 Clin. Chem.Home page
T. M. Chin, D. Anuar, R. Soo, M. Salto-Tellez, W. Q. Li, B. Ahmad, S. C. Lee, B. C. Goh, K. Kawakami, A. Segal, et al.
Detection of Epidermal Growth Factor Receptor Variations by Partially Denaturing HPLC
Clin. Chem., January 1, 2007; 53(1): 62 - 70.
[Abstract] [Full Text] [PDF]

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 The OncologistHome page
L. V. Sequist, V. A. Joshi, P. A. Janne, A. Muzikansky, P. Fidias, M. Meyerson, D. A. Haber, R. Kucherlapati, B. E. Johnson, and T. J. Lynch
Response to treatment and survival of patients with non-small cell lung cancer undergoing somatic EGFR mutation testing.
Oncologist, January 1, 2007; 12(1): 90 - 98.
[Abstract] [Full Text] [PDF]

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 J. Biol. Chem.Home page
M. Perez-Torres, M. Guix, A. Gonzalez, and C. L. Arteaga
Epidermal Growth Factor Receptor (EGFR) Antibody Down-regulates Mutant Receptors and Inhibits Tumors Expressing EGFR Mutations
J. Biol. Chem., December 29, 2006; 281(52): 40183 - 40192.
[Abstract] [Full Text] [PDF]

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 Clin. Cancer Res.Home page
R. Rosell, M. Taron, N. Reguart, D. Isla, and T. Moran
Epidermal Growth Factor Receptor Activation: How Exon 19 and 21 Mutations Changed Our Understanding of the Pathway
Clin. Cancer Res., December 15, 2006; 12(24): 7222 - 7231.
[Abstract] [Full Text] [PDF]

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 Clin. Cancer Res.Home page
G. J. Riely, K. A. Politi, V. A. Miller, and W. Pao
Update on Epidermal Growth Factor Receptor Mutations in Non-Small Cell Lung Cancer
Clin. Cancer Res., December 15, 2006; 12(24): 7232 - 7241.
[Abstract] [Full Text] [PDF]

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 Cancer Res.Home page
S. Kobayashi, T. Shimamura, S. Monti, U. Steidl, C. J. Hetherington, A. M. Lowell, T. Golub, M. Meyerson, D. G. Tenen, G. I. Shapiro, et al.
Transcriptional Profiling Identifies Cyclin D1 as a Critical Downstream Effector of Mutant Epidermal Growth Factor Receptor Signaling
Cancer Res., December 1, 2006; 66(23): 11389 - 11398.
[Abstract] [Full Text] [PDF]


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