Epidermal growth factor receptor abnormalities in lung cancer. Pathogenetic and clinical implications

Annals of Diagnostic Pathology

Volumn 10, Issue 5, 2006, Pages 306-315

  Prudkin, Ludmila ^a   Wistuba, Ignacio I ^a  

^a UNIVERSITY OF TEXAS MD ANDERSON CANCER CENTER   (United States)

Author keywords

Adenocarcinoma of the lung; Atypical adenomatous hyperplasia; EGFR; Gene amplification; Mutation; Normal epithelium

Indexed keywords

CETUXIMAB; EPIDERMAL GROWTH FACTOR RECEPTOR; ERLOTINIB; GEFITINIB; PROTEIN TYROSINE KINASE; PROTEIN TYROSINE KINASE INHIBITOR;

CARCINOGENESIS; CLINICAL FEATURE; CLINICAL TRIAL; EPIDERMAL GROWTH FACTOR RECEPTOR GENE; GENE AMPLIFICATION; GENE MUTATION; HISTOPATHOLOGY; HUMAN; IMMUNOHISTOCHEMISTRY; LUNG CARCINOMA; PREDICTION; PRIORITY JOURNAL; PROTEIN EXPRESSION; RECEPTOR GENE; REVIEW; SMOKING;

ADENOCARCINOMA; ENZYME INHIBITORS; FEMALE; GENE EXPRESSION REGULATION, NEOPLASTIC; HUMANS; LUNG NEOPLASMS; MALE; MUTATION; RECEPTOR, EPIDERMAL GROWTH FACTOR;

EID: 33748428638     PISSN: 10929134     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.anndiagpath.2006.06.011     Document Type: Review

References (87)

1. Jemal A., Siegel R., Ward E., et al. Cancer statistics, 2006. CA Cancer J Clin 56 2 (2006) 106-130
2. Minna J.D., and Gazdar A. Focus on lung cancer. Cancer Cell 1 (2002) 49-52
3. Brambilla E., Travis W.D., Colby T.V., Corrin B., and Shimosato Y. The new World Health Organization classification of lung tumours. Eur Respir J 18 6 (2001) 1059-1068
4. Wistuba I., and Gazdar A. Lung cancer prenoplasia. Annu Rev Pathol Mech Dis 1 (2005) 331-348
5. Kerr K.M. Pulmonary preinvasive neoplasia. J Clin Pathol 54 (2001) 257-271
6. Ebbert J.O., Yang P., Vachon C.M., et al. Lung cancer risk reduction after smoking cessation: observations from a prospective cohort of women. J Clin Oncol 21 5 (2003) 921-926
7. Tong L., Spitz M.R., Fueger J.J., and Amos C.A. Lung carcinoma in former smokers. Cancer 78 (1996) 1004-1010
8. Herbst R.S. Targeted therapy in non-small-cell lung cancer. Oncology (Williston Park) 16 9 Suppl 9 (2002) 19-24
9. Herbst R.S. Role of novel targeted therapies in the clinic. Br J Cancer 92 Suppl 1 (2005) S21-S27
10. Massarelli E., and Herbst R.S. Use of novel second-line targeted therapies in non-small cell lung cancer. Semin Oncol 33 1 Suppl 1 (2006) S9-S16
11. Paez J.G., Janne P.A., Lee J.C., et al. EGFR mutations in lung cancer: correlation with clinical response to gefitinib therapy. Science 304 5676 (2004) 1497-1500
12. Lynch T.J., Bell D.W., Sordella R., et al. Activating mutations in the epidermal growth factor receptor underlying responsiveness of non-small-cell lung cancer to gefitinib. N Engl J Med 350 21 (2004) 2129-2139
13. Huse M., and Kuriyan J. The conformational plasticity of protein kinases. Cell 109 3 (2002) 275-282
14. Robinson D.R., Wu Y.M., and Lin S.F. The protein tyrosine kinase family of the human genome. Oncogene 19 49 (2000) 5548-5557
15. Pisick E., Jagadeesh S., and Salgia R. Receptor tyrosine kinases and inhibitors in lung cancer. Sci World J 4 (2004) 589-604
16. Yarden Y., and Sliwkowski M.X. Untangling the ErbB signalling network. Nat Rev Mol Cell Biol 2 2 (2001) 127-137
17. Herbst R.S. Review of epidermal growth factor receptor biology. Int J Radiat Oncol Biol Phys 59 2 Suppl (2004) 21-26
18. Salomon D.S., Brandt R., Ciardiello F., and Normanno N. Epidermal growth factor-related peptides and their receptors in human malignancies. Crit Rev Oncol Hematol 19 3 (1995) 183-232
19. Jorissen R.N., Walker F., Pouliot N., Garrett T.P., Ward C.W., and Burgess A.W. Epidermal growth factor receptor: mechanisms of activation and signalling. Exp Cell Res 284 1 (2003) 31-53
20. Nicholson R.I., Gee J.M., and Harper M.E. EGFR and cancer prognosis. Eur J Cancer 37 Suppl 4 (2001) S9-S15
21. Scagliotti G.V., Selvaggi G., Novello S., and Hirsch F.R. The biology of epidermal growth factor receptor in lung cancer. Clin Cancer Res 10 12 Pt 2 (2004) 4227s-4232s
22. Franklin W.A., Veve R., Hirsch F.R., Helfrich B.A., and Bunn Jr. P.A. Epidermal growth factor receptor family in lung cancer and premalignancy. Semin Oncol 29 1 Suppl 4 (2002) 3-14
23. Hirsch F.R., Varella-Garcia M., Bunn Jr. P.A., et al. Epidermal growth factor receptor in non-small-cell lung carcinomas: correlation between gene copy number and protein expression and impact on prognosis. J Clin Oncol 21 20 (2003) 3798-3807
24. Meert A.P., Martin B., Delmotte P., et al. The role of EGF-R expression on patient survival in lung cancer: a systematic review with meta-analysis. Eur Respir J 20 4 (2002) 975-981
25. Rusch V., Baselga J., Cordon-Cardo C., et al. Differential expression of the epidermal growth factor receptor and its ligands in primary non-small cell lung cancers and adjacent benign lung. Cancer Res 53 10 Suppl (1993) 2379-2385
26. Suzuki S., Dobashi Y., Sakurai H., Nishikawa K., Hanawa M., and Ooi A. Protein overexpression and gene amplification of epidermal growth factor receptor in nonsmall cell lung carcinomas. An immunohistochemical and fluorescence in situ hybridization study. Cancer 103 6 (2005) 1265-1273
27. Kawamoto T., Sato J.D., Le A., Polikoff J., Sato G.H., and Mendelsohn J. Growth stimulation of A431 cells by epidermal growth factor: identification of high-affinity receptors for epidermal growth factor by an anti-receptor monoclonal antibody. Proc Natl Acad Sci U S A 80 5 (1983) 1337-1341
28. Gill G.N., Kawamoto T., Cochet C., et al. Monoclonal anti-epidermal growth factor receptor antibodies which are inhibitors of epidermal growth factor binding and antagonists of epidermal growth factor binding and antagonists of epidermal growth factor-stimulated tyrosine protein kinase activity. J Biol Chem 259 12 (1984) 7755-7760
29. Mendelsohn J., and Baselga J. The EGF receptor family as targets for cancer therapy. Oncogene 19 56 (2000) 6550-6565
30. Mendelsohn J., and Baselga J. Status of epidermal growth factor receptor antagonists in the biology and treatment of cancer. J Clin Oncol 21 14 (2003) 2787-2799
31. FDA. Food and Drug Administration. In: www.fda.gov.
32. Shepherd F.A., Rodrigues Pereira J., Ciuleanu T., et al. Erlotinib in previously treated non-small-cell lung cancer. N Engl J Med 353 2 (2005) 123-132
33. Giaccone G., Herbst R.S., Manegold C., et al. Gefitinib in combination with gemcitabine and cisplatin in advanced non-small-cell lung cancer: a phase III trial-INTACT 1. J Clin Oncol 22 5 (2004) 777-784
34. Herbst R.S., Prager D., Hermann R., et al. TRIBUTE: a phase III trial of erlotinib hydrochloride (OSI-774) combined with carboplatin and paclitaxel chemotherapy in advanced non-small-cell lung cancer. J Clin Oncol 23 25 (2005) 5892-5899
35. Kris M.G., Natale R.B., Herbst R.S., et al. Efficacy of gefitinib, an inhibitor of the epidermal growth factor receptor tyrosine kinase, in symptomatic patients with non-small cell lung cancer: a randomized trial. JAMA 290 16 (2003) 2149-2158
36. Fukuoka M., Yano S., Giaccone G., et al. Multi-institutional randomized phase II trial of gefitinib for previously treated patients with advanced non-small-cell lung cancer (The IDEAL 1 Trial). [corrected]. J Clin Oncol 21 12 (2003) 2237-2246
37. Perez-Soler R., Chachoua A., Hammond L.A., et al. Determinants of tumor response and survival with erlotinib in patients with non-small-cell lung cancer. J Clin Oncol 22 16 (2004) 3238-3247
38. Miller V.A., Kris M.G., Shah N., et al. Bronchioloalveolar pathologic subtype and smoking history predict sensitivity to gefitinib in advanced non-small-cell lung cancer. J Clin Oncol 22 6 (2004) 1103-1109
39. Frederick L., Wang X.Y., Eley G., and James C.D. Diversity and frequency of epidermal growth factor receptor mutations in human glioblastomas. Cancer Res 60 5 (2000) 1383-1387
40. Shigematsu H., Lin L., Takahashi T., et al. Clinical and biological features associated with epidermal growth factor receptor gene mutations in lung cancers. J Natl Cancer Inst 97 5 (2005) 339-346
41. Yatabe Y., Kosaka T., Takahashi T., and Mitsudomi T. EGFR mutation is specific for terminal respiratory unit type adenocarcinoma. Am J Surg Pathol 29 5 (2005) 633-639
42. Huang S.F., Liu H.P., Li L.H., et al. 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 24 (2004) 8195-8203
43. Kosaka T., Yatabe Y., Endoh H., Kuwano H., Takahashi T., and Mitsudomi T. Mutations of the epidermal growth factor receptor gene in lung cancer: biological and clinical implications. Cancer Res 64 24 (2004) 8919-8923
44. Tokumo M., Toyooka S., Kiura K., et al. The relationship between epidermal growth factor receptor mutations and clinicopathologic features in non-small cell lung cancers. Clin Cancer Res 11 3 (2005) 1167-1173
45. Cappuzzo F., Hirsch F.R., Rossi E., et al. Epidermal growth factor receptor gene and protein and gefitinib sensitivity in non-small-cell lung cancer. J Natl Cancer Inst 97 9 (2005) 643-655
46. Sonobe M., Manabe T., Wada H., and Tanaka F. Mutations in the epidermal growth factor receptor gene are linked to smoking-independent, lung adenocarcinoma. Br J Cancer 93 3 (2005) 355-363
47. Sasaki H., Endo K., Konishi A., et al. EGFR mutation status in Japanese lung cancer patients: genotyping analysis using LightCycler. Clin Cancer Res 11 8 (2005) 2924-2929
48. Yang S.H., Mechanic L.E., Yang P., et al. Mutations in the tyrosine kinase domain of the epidermal growth factor receptor in non-small cell lung cancer. Clin Cancer Res 11 6 (2005) 2106-2110
49. Mu X.L., Li L.Y., Zhang X.T., et al. Gefitinib-sensitive mutations of the epidermal growth factor receptor tyrosine kinase domain in Chinese patients with non-small cell lung cancer. Clin Cancer Res 11 12 (2005) 4289-4294
50. Tsao M.S., Sakurada A., Cutz J.C., et al. Erlotinib in lung cancer-molecular and clinical predictors of outcome. N Engl J Med 353 2 (2005) 133-144
51. Mitsudomi T., Kosaka T., Endoh H., et al. Mutations of the epidermal growth factor receptor gene predict prolonged survival after gefitinib treatment in patients with non-small-cell lung cancer with postoperative recurrence. J Clin Oncol 23 11 (2005) 2513-2520
52. Shigematsu H., and Gazdar A.F. Somatic mutations of epidermal growth factor receptor signaling pathway in lung cancers. Int J Cancer 118 2 (2006) 257-262
53. Pao W., and Miller V.A. Epidermal growth factor receptor mutations, small-molecule kinase inhibitors, and non-small-cell lung cancer: current knowledge and future directions. J Clin Oncol 23 11 (2005) 2556-2568
54. Dowell J.E. Epidermal growth factor receptor mutations in non-small cell lung cancer: a basic science discovery with immediate clinical impact. Am J Med Sci 331 3 (2006) 139-149
55. Johnson B.E., and Janne P.A. Epidermal growth factor receptor mutations in patients with non-small cell lung cancer. Cancer Res 65 17 (2005) 7525-7529
56. Gazdar A.F., Shigematsu H., Herz J., and Minna J.D. Mutations and addiction to EGFR: the Achilles 'heal' of lung cancers?. Trends Mol Med 10 10 (2004) 481-486
57. Sordella R., Bell D.W., Haber D.A., and Settleman J. Gefitinib-sensitizing EGFR mutations in lung cancer activate anti-apoptotic pathways. Science 305 5687 (2004) 1163-1167
58. Tam I.Y., Chung L.P., Suen W.S., 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 12 5 (2006) 1647-1653
59. Toyooka S., Tokumo M., Shigematsu H., et al. Mutational and epigenetic evidence for independent pathways for lung adenocarcinomas arising in smokers and never smokers. Cancer Res 66 3 (2006) 1371-1375
60. Tsao A.S., Tang X., Sabloff B., et al. Clinical-pathological characteristics of the EGFR gene mutation in non-small cell lung cancer. J Thoracic Oncol 1 (2006) 231-239
61. Toyooka S., Yatabe Y., Tokumo M., et al. Mutations of epidermal growth factor receptor and K-ras genes in adenosquamous carcinoma of the lung. Int J Cancer 118 6 (2006) 1588-1590
62. Pao W., Miller V., Zakowski M., et al. 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 U S A 101 36 (2004) 13306-13311
63. Travis W.D., Garg K., Franklin W.A., et al. Evolving concepts in the pathology and computed tomography imaging of lung adenocarcinoma and bronchioloalveolar carcinoma. J Clin Oncol 23 14 (2005) 3279-3287
64. Travis W.D., Brambilla E., Muller-Hermelink H.K., and Harris C.C. Tumours of the lung. In: Travis W.D., Brambilla E., Muller-Hermelink H.K., and Harris C.C. (Eds). Pathology and genetics: tumours of the lung, pleura, thymus and heart (2004), IARC Press, Lyon 9-124
65. Riely G.J., Pao W., Pham D., et al. 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 12 31 (2006) 839-844
66. Tidow N., Boecker A., Schmidt H., et al. Distinct amplification of an untranslated regulatory sequence in the egfr gene contributes to early steps in breast cancer development. Cancer Res 63 6 (2003) 1172-1178
67. Gebhardt F., Zanker K.S., and Brandt B. Modulation of epidermal growth factor receptor gene transcription by a polymorphic dinucleotide repeat in intron 1. J Biol Chem 274 19 (1999) 13176-13180
68. Ahrendt S.A., Decker P.A., Alawi E.A., et al. Cigarette smoking is strongly associated with mutation of the K-ras gene in patients with primary adenocarcinoma of the lung. Cancer 92 6 (2001) 1525-1530
69. Keohavong P., Mady H.H., Gao W.M., Siegfried J.M., Luketich J.D., and Melhem M.F. Topographic analysis of K-ras mutations in histologically normal lung tissues and tumours of lung cancer patients. Br J Cancer 85 2 (2001) 235-241
70. Westra W.H., Slebos R.J., Offerhaus G.J., et al. K-ras oncogene activation in lung adenocarcinomas from former smokers. Evidence that K-ras mutations are an early and irreversible event in the development of adenocarcinoma of the lung. Cancer 72 2 (1993) 432-438
71. Pao W., Wang T.Y., Riely G.J., et al. KRAS mutations and primary resistance of lung adenocarcinomas to gefitinib or erlotinib. PLoS Med 2 1 (2005) e17
72. Tomizawa Y., Iijima H., Sunaga N., 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 11 19 Pt 1 (2005) 6816-6822
73. Han S.W., Kim T.Y., Hwang P.G., et al. Predictive and prognostic impact of epidermal growth factor receptor mutation in non-small-cell lung cancer patients treated with gefitinib. J Clin Oncol 23 11 (2005) 2493-2501
74. Taron M., Ichinose Y., Rosell R., 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 11 16 (2005) 5878-5885
75. Takano T., Ohe Y., Sakamoto H., 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 23 28 (2005) 6829-6837
76. Hirsch F.R., Varella-Garcia M., McCoy J., et al. Increased epidermal growth factor receptor gene copy number detected by fluorescence in situ hybridization associates with increased sensitivity to gefitinib in patients with bronchioloalveolar carcinoma subtypes: a Southwest Oncology Group Study. J Clin Oncol 23 28 (2005) 6838-6845
77. Sequist L.V., Haber D.A., and Lynch T.J. Epidermal growth factor receptor mutations in non-small cell lung cancer: predicting clinical response to kinase inhibitors. Clin Cancer Res 11 16 (2005) 5668-5670
78. Amann J., Kalyankrishna S., Massion P.P., et al. Aberrant epidermal growth factor receptor signaling and enhanced sensitivity to EGFR inhibitors in lung cancer. Cancer Res 65 1 (2005) 226-235
79. Tracy S., Mukohara T., Hansen M., Meyerson M., Johnson B.E., and Janne P.A. Gefitinib induces apoptosis in the EGFRL858R non-small-cell lung cancer cell line H3255. Cancer Res 64 20 (2004) 7241-7244
80. Janne P.A., Borras A.M., Kuang Y., et al. A rapid and sensitive enzymatic method for epidermal growth factor receptor mutation screening. Clin Cancer Res 12 3 Pt 1 (2006) 751-758
81. Eberhard D.A., Johnson B.E., Amler L.C., et al. 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 25 (2005) 5900-5909
82. Pao W., Miller V.A., Venkatraman E., and Kris M.G. Predicting sensitivity of non-small-cell lung cancer to gefitinib: is there a role for P-Akt?. J Natl Cancer Inst 96 15 (2004) 1117-1119
83. Pao W., Miller V.A., Politi K.A., et al. Acquired resistance of lung adenocarcinomas to gefitinib or erlotinib is associated with a second mutation in the EGFR kinase domain. PLoS Med 2 3 (2005) e73
84. Kobayashi S., Boggon T.J., Dayaram T., et al. EGFR mutation and resistance of non-small-cell lung cancer to gefitinib. N Engl J Med 352 8 (2005) 786-792
85. Marchetti A., Martella C., Felicioni L., et al. EGFR mutations in non-small-cell lung cancer: analysis of a large series of cases and development of a rapid and sensitive method for diagnostic screening with potential implications on pharmacologic treatment. J Clin Oncol 23 4 (2005) 857-865
86. Soung Y.H., Lee J.W., Kim S.Y., et al. Mutational analysis of EGFR and K-RAS genes in lung adenocarcinomas. Virchows Arch 446 5 (2005) 483-488
87. Sugio K., Uramoto H., Ono K., et al. Mutations within the tyrosine kinase domain of EGFR gene specifically occur in lung adenocarcinoma patients with a low exposure of tobacco smoking. Br J Cancer 94 6 (2006) 896-903