Epidermal growth factor receptor mutations, small-molecule kinase inhibitors, and non-small-cell lung cancer: Current knowledge and future directions

Journal of Clinical Oncology

Volumn 23, Issue 11, 2005, Pages 2556-2568

  Pao, William ^a   Miller, Vincent A ^a  

^a WEILL CORNELL MEDICAL COLLEGE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

EPIDERMAL GROWTH FACTOR RECEPTOR; ERLOTINIB; GEFITINIB; PHOSPHOTRANSFERASE INHIBITOR; PROTEIN KINASE INHIBITOR; QUINAZOLINE DERIVATIVE;

DRUG RESPONSE; DRUG TARGETING; GENE AMPLIFICATION; GENE MUTATION; HUMAN; HUMAN GENOME; INCIDENCE; NON SMALL CELL LUNG CANCER; PHASE 1 CLINICAL TRIAL (TOPIC); PHASE 2 CLINICAL TRIAL (TOPIC); PHYSICIAN; PRIORITY JOURNAL; REVIEW; CLINICAL TRIAL; DRUG ANTAGONISM; GENETICS; LUNG NON SMALL CELL CANCER; LUNG TUMOR; MUTATION; NUCLEOTIDE SEQUENCE; PATHOPHYSIOLOGY; PHYSIOLOGY; TREATMENT OUTCOME;

CARCINOMA, NON-SMALL-CELL LUNG; CLINICAL TRIALS; DNA MUTATIONAL ANALYSIS; GENE AMPLIFICATION; HUMANS; LUNG NEOPLASMS; MUTATION; PROTEIN KINASE INHIBITORS; QUINAZOLINES; RECEPTOR, EPIDERMAL GROWTH FACTOR; TREATMENT OUTCOME;

EID: 17844390172     PISSN: 0732183X     EISSN: 15277755     Source Type: Journal    
DOI: 10.1200/JCO.2005.07.799     Document Type: Review

References (104)

1. Mendelsohn J, Baselga J: Status of epidermal growth factor receptor antagonists in the biology and treatment of cancer. J Clin Oncol 21:2787-2799, 2003
2. Manning G, Whyte DB, Martinez R, et al: The protein kinase complement of the human genome. Science 298:1912-1934, 2002
3. Citri A, Skaria KB, Yarden Y: The deaf and the dumb: The biology of ErbB-2 and ErbB-3. Exp Cell Res 284:54-65, 2003
4. Schlessinger J: Ligand-induced, receptor-mediated dimerization and activation of EGF receptor. Cell 110:669-672, 2002
5. Jorissen RN, Walker F, Pouliot N, et al: Epidermal growth factor receptor: Mechanisms of activation and signalling. Exp Cell Res 284:31-53, 2003
6. Yarden Y, Sliwkowski MX: Untangling the ErbB signalling network. Nat Rev Mol Cell Biol 2:127-137, 2001
7. Cohen S: Isolation of a mouse submaxillary gland protein accelerating incisor eruption and eyelid opening in the new born animal. J Biol Chem 237:1555-1562, 1962
8. Hunter T, Cooper JA: Epidermal growth factor induces rapid tyrosine phosphorylation of proteins in A431 human tumor cells. Cell 24:741-752, 1981
9. Anderson SM, Hayward WS, Neel BG, et al: Avian erythroblastosis virus produces two mRNA's. J Virol 36:676-683, 1980
10. Vennstrom B, Bishop JM: Isolation and characterization of chicken DNA homologous to the two putative oncogenes of avian erythroblastosis virus. Cell 28:135-143, 1982
11. Yamamoto T, Hihara H, Nishida T, et al: A new avian erythroblastosis virus, AEV-H, carries erbB gene responsible for the induction of both erythroblastosis and sarcomas. Cell 34:225-232, 1983
12. Downward J, Yarden Y, Mayes E, et al: Close similarity of epidermal growth factor receptor and v-erb-B oncogene protein sequences. Nature 307:521-527, 1984
13. Nicholson RI, Gee JM, Harper ME: EGFR and cancer prognosis. Eur J Cancer 37 (Suppl 4):S9-15, 2001
14. Gill GN, Kawamoto T, Cochet C, et al: Monoclonal anti-EGF receptor antibodies which are inhibitors of growth factor binding and antagonists of EGF-stimulated tyrosine protein kinase activity. J Biol Chem 259:7755-7760, 1984
15. Mendelsohn J: Targeting the epidermal growth factor receptor for cancer therapy. J Clin Oncol 20:1S-13S, 2002
16. Sandgren EP, Luetteke NC, Palmiter RD, et al: Overexpression of TGF alpha in transgenic mice: induction of epithelial hyperplasia, pancreatic metaplasia, and carcinoma of the breast. Cell 61:1121-1135, 1990
17. Xu YH, Richert N, Ito S, et al: Characterization of epidermal growth factor receptor gene expression in malignant and normal human cell lines. Proc Natl Acad Sci U S A 81:7308-7312, 1984
18. Di Fiore PP, Pierce JH, Fleming TP, et al: Overexpression of the human EGF receptor confers an EGF-dependent transformed phenotype to NIH 3T3 cells. Cell 51:1063-1070, 1987
19. Ekstrand AJ, Sugawa N, James CD, et al: Amplified and rearranged epidermal growth factor receptor genes in human glioblastomas reveal deletions of sequences encoding portions of the N- and/or C-terminal tails. Proc Natl Acad Sci U S A 89:4309-4313, 1992
20. Wong AJ, Ruppert JM, Bigner SH, et al: Structural alterations of the epidermal growth factor receptor gene in human gliomas. Proc Natl Acad Sci U S A 89:2965-2969, 1992
21. Kuan CT, Wikstrand CJ, Bigner DD: EGF mutant receptor vIII as a molecular target in cancer therapy. Endocr Relat Cancer 8:83-96, 2001
22. Okamoto I, Kenyon LC, Emlet DR, et al: Expression of constitutively activated EGFRvIII in non-small cell lung cancer. Cancer Sci 94:50-56, 2003
23. Garcia de Palazzo IE, Adams GP, Sundareshan P, et al: Expression of mutated epidermal growth factor receptor by non-small cell lung carcinomas. Cancer Res 53:3217-3220, 1993
24. Ward WH, Cook PN, Slater AM, et al: Epidermal growth factor receptor tyrosine kinase. Investigation of catalytic mechanism, structure-based searching and discovery of a potent inhibitor. Biochem Pharmacol 48:659-666, 1994
25. Merlino GT, Ishii S, Whang-Peng J, et al: Structure and localization of genes encoding aberrant and normal epidermal growth factor receptor RNAs from A431 human carcinoma cells. Mol Cell Biol 5:1722-1734, 1985
26. Merlino GT, Xu YH, Ishii S, et al: Amplification and enhanced expression of the epidermal growth factor receptor gene in A431 human carcinoma cells. Science 224:417-419, 1984
27. Ullrich A, Coussens L, Hayflick JS, et al: Human epidermal growth factor receptor cDNA sequence and aberrant expression of the amplified gene in A431 epidermoid carcinoma cells. Nature 309:418-425, 1984
28. Barker AJ, Gibson KH, Grundy W, et al: Studies leading to the identification of ZD1839 (IRESSA): An orally active, selective epidermal growth factor receptor tyrosine kinase inhibitor targeted to the treatment of cancer. Bioorg Med Chem Lett 11:1911-1914, 2001
29. Wakeling AE, Guy SP, Woodburn JR, et al: ZD1839 (Iressa): An orally active inhibitor of epidermal growth factor signaling with potential for cancer therapy. Cancer Res 62:5749-5754, 2002
30. Sirotnak FM: Studies with ZD1839 in preclinical models. Semin Oncol 30:12-20, 2003
31. Sirotnak FM, Zakowski MF, Miller VA, et al: Efficacy of cytotoxic agents against human tumor xenografts is markedly enhanced by coadministration of ZD1839 (Iressa), an inhibitor of EGFR tyrosine kinase. Clin Cancer Res 6:4885-4892, 2000
32. Ciardiello F, Caputo R, Bianco R, et al: Antitumor effect and potentiation of cytotoxic drugs activity in human cancer cells by ZD-1839 (Iressa), an epidermal growth factor receptor-selective tyrosine kinase inhibitor. Clin Cancer Res 6:2053-2063, 2000
33. She Y, Lee F, Chen J, et al: The epidermal growth factor receptor tyrosine kinase inhibitor ZD1839 selectively potentiates radiation response of human tumors in nude mice, with a marked improvement in therapeutic index. Clin Cancer Res 9:3773-3778, 2003
34. Williams KJ, Telfer BA, Stratford IJ, et al: ZD1839 ('Iressa'), a specific oral epidermal growth factor receptor-tyrosine kinase inhibitor, potentiates radiotherapy in a human colorectal cancer xenograft model. Br J Cancer 86:1157-1161, 2002
35. Nicholson RI, Hutcheson IR, Harper ME, et al: Modulation of epidermal growth factor receptor in endocrine-resistant, oestrogen receptor-positive breast cancer. Endocr Relat Cancer 8:175-182, 2001
36. Baselga J, Rischin D, Ranson M, et al: Phase I safety, pharmacokinetic, and pharmacodynamic trial of ZD1839, a selective oral epidermal growth factor receptor tyrosine kinase inhibitor, in patients with five selected solid tumor types. J Clin Oncol 20:4292-4302, 2002
37. Herbst RS, Maddox A-M, Rothenberg ML, et al: Selective oral epidermal growth factor receptor tyrosine kinase inhibitor ZD1839 is generally well-tolerated and has activity in non-small-cell lung cancer and other solid tumors: results of a phase I trial. J Clin Oncol 20:3815-3825, 2002
38. Ranson M, Hammond LA, Ferry D, et al: ZD1839, a selective oral epidermal growth factor receptor-tyrosine kinase inhibitor, is well tolerated and active in patients with solid, malignant tumors: Results of a phase I trial. J Clin Oncol 20:2240-2250, 2002
39. Nakagawa K, Tamura T, Negoro S, et al: Phase I pharmacokinetic trial of the selective oral epidermal growth factor receptor tyrosine kinase inhibitor gefitinib ('Iressa', ZD1839) in Japanese patients with solid malignant tumors. Ann Oncol 14:922-930, 2003
40. Kris M, Natale RB, Herbst R, et al: Efficacy of gefitinib, an inhibitor of the epidermal growth factor receptor tyrosine kinase, in symptomatic patients with non-small cell lung cancer. JAMA 290:2149-2158, 2003
41. 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. J Clin Oncol 21:2237-2246, 2003
42. Perez-Soler R, Chachoua A, Hammond LA, et al: Determinants of tumor response and survival with erlotinib in patients with non-small-cell lung cancer. J Clin Oncol 22:3238-3247, 2004
43. Kris M, Sandler A, Cespon M, et al: Cigarette smoking history predicts sensitivity to erlotinib (Tarceva): results of a phase II trial in patients with bronchioloalveolar cancer (BAC). Proc Am Soc Clin Oncol 22: 2004 (abstr 7062)
44. nd line chemotherapy. A National Cancer Institute of Canada Clinical Trials Group (NCIC CTG) trial. Proc Am Soc Clin Onc 22: 2004 (abstr 7022)
45. West H, Franklin WA, Gumerlock PH, et al: Gefitinib (ZD1839) therapy for advanced bronchioloalveolar lung cancer (BAC): Southwest Oncology Group (SWOG) Study S0126. Proc Am Soc Clin Oncol 22: 2004 (abstr 7014)
46. Herbst RS, Giaccone G, Schiller JH, et al: Gefitinib in combination with paclitaxel and carboplatin in advanced non-small-cell lung cancer: A phase III trial-INTACT 2. J Clin Oncol 22:785-794, 2004
47. Giaccone G, Herbst RS, 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 22:777-784, 2004
48. Ciardiello F, Tortora G: A novel approach in the treatment of cancer: Targeting the epidermal growth factor receptor. Clin Cancer Res 7:2958-2970, 2001
49. Moyer JD, Barbacci EG, Iwata KK, et al: Induction of apoptosis and cell cycle arrest by CP-358,774, an inhibitor of epidermal growth factor receptor tyrosine kinase. Cancer Res 57:4838-4848, 1997
50. Pao W, Miller VA, Kris MG: 'Targeting' the epidermal growth factor receptor tyrosine kinase with gefitinib (Iressa) in non-small cell lung cancer (NSCLC). Semin Cancer Biol 14:33-40, 2004
51. Hidalgo M, Siu LL, Nemunaitis J, et al: Phase I and pharmacologic study of OSI-774, an epidermal growth factor receptor tyrosine kinase inhibitor, in patients with advanced solid malignancies. J Clin Oncol 19:3267-3279, 2001
52. Gatzemeier U, Pluzanska A, Szczesna A, et al: Results of a phase III trial of erlotinib (OSI-774) combined with cisplatin and gemcitabine (GC) chemotherapy in advanced non-small cell lung cancer (NSCLC). Proc Am Soc Clin Onc 22:2004 (abstr 7010)
53. Herbst RS, Prager D, Hermann R, et al: TRIBUTE - A phase III trial of erlotinib HCl (OSI-774) combined with carboplatin and paclitaxel (CP) chemotherapy in advanced non-small cell lung cancer (NSCLC). Proc Am Soc Clin Onc 22:2004 (abstr 7011)
54. Moody SE, Sarkisian CJ, Hahn KT, et al: Conditional activation of Neu in the mammary epithelium of transgenic mice results in reversible pulmonary metastasis. Cancer Cell 2:451-461, 2002
55. Huettner CS, Zhang P, Van Etten RA, et al: Reversibility of acute B-cell leukaemia induced by BCR-ABL1. Nat Genet 24:57-60, 2000
56. Fisher GH, Wellen SL, Klimstra D, et al: Induction and apoptotic regression of lung adenocarcinomas by regulation of a K-Ras transgene in the presence and absence of tumor suppressor genes. Genes Dev 15:3249-3262, 2001
57. Felsher DW, Bishop JM: Reversible tumorigenesis by MYC in hematopoietic lineages. Mol Cell 4:199-207, 1999
58. Chin L, Tam A, Pomerantz J, et al: Essential role for oncogenic Ras in tumour maintenance. Nature 400:468-472, 1999
59. Weinstein I: Cancer. Addiction to oncogenes-The Achilles heal of cancer. Science 297:63-64, 2002
60. Druker B: STI571 (Gleevec) as a paradigm for cancer therapy. Trends Mol Med 8:S14-S18, 2002 (suppl 4)
61. Demetri GD: Targeting c-kit mutations in solid tumors: Scientific rationale and novel therapeutic options. Semin Oncol 28:19-26, 2001
62. Cools J, DeAngelo DJ, Gotlib J, et al: A tyrosine kinase created by fusion of the PDGFRA and FIP1L1 genes as a therapeutic target of imatinib in idiopathic hypereosinophilic syndrome. N Engl J Med 348:1201-1214, 2003
63. Lynch TJ, Bell DW, 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 350:2129-2139, 2004
64. Paez JG, Janne PA, Lee JC, et al: EGFR mutations in lung cancer: Correlation with clinical response to gefitinib therapy. Science 304:1497-1500, 2004
65. Bardelli A, Parsons DW, Silliman N, et al: Mutational analysis of the tyrosine kinome in colorectal cancers. Science 300:949, 2003
66. Kris MG, Natale RB, Herbst RS, 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 290:2149-2158, 2003
67. 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 101:13306-13311, 2004
68. Miller VA, Kris MG, Shah N, et al: Bronchioloalveolar pathologic subtype and smoking history predict sensitivity to gefitinib in advanced non-small-cell lung cancer. J Clin Oncol 22:1103-1109, 2004
69. Miller VA, Herbst R, Prager D, et al: Long survival of never smoking non-small cell lung cancer (NSCLC) patients treated with erlotinib HCl (OSI-774) and chemotherapy: Sub-group analysis of TRIBUTE. Proc Am Soc Clin Onc 22: 2004 (abstr 7061)
70. Perez-Soler R: The role of erlotinib (Tarceva, OSI 774) in the treatment of non-small cell lung cancer. Clin Cancer Res 10:4238s-4240s, 2004 (12 pt 2)
71. Parra HS, Cavina R, Latteri F, et al: Analysis of epidermal growth factor receptor expression as a predictive factor for response to gefitinib ('Iressa', ZD1839) in non-small-cell lung cancer. Br J Cancer 91:208-212, 2004
72. Sirotnak F, Zakowski M, Miller V, et al: Efficacy of cytotoxic agents against human tumor xenografts is markedly enhanced by co-administration of ZD1839 (Iressa), an inhibitor of EGFR tyrosine kinase. Clin Cancer Res 6:4885-4892, 2000
73. Erlotinib (Tarceva) package insert. Genentech, South San Francisco, CA and OSI Pharmaceuticals, Melville, NY.
74. Shigematsu H, Lin L, Takahashi T, et al: Clinical and biological features of epidermal growth factor receptor mutations in lung cancers. J Natl Cancer Inst: in press
75. Sordella R, Bell DW, Haber DA, et al: Gefitinib-sensitizing EGFR mutations in lung cancer activate anti-apoptotic pathways. Science 305:1163-1167, 2004
76. Travis WD, Colby TV, Corrin B, et al: Histological typing of lung and pleural tumors (ed 3rd), Berlin, Springer Verlag, 1999
77. Ebright MI, Zakowski MF, Martin J, et al: Clinical pattern and pathologic stage but not histologic features predict outcome for bronchioloalveolar carcinoma. Ann Thorac Surg 74:1640-1646, 2002
78. Lee JW, Soung YH, Kim SY, et al: Absence of EGFR mutation in the kinase domain in common human cancers besides non-small cell lung cancer. Int J Cancer 113:510-511, 2004
79. Soulieres D, Senzer NN, Vokes EE, et al: Multicenter phase II study of erlotinib, an oral epidermal growth factor receptor tyrosine kinase inhibitor, in patients with recurrent or metastatic squamous cell cancer of the head and neck. J Clin Oncol 22:77-85, 2004
80. Raizer JJ, Abrey LE, Wen P, et al: A phase II trial of erlotinib (OSI-774) in patients with recurrent malignant gliomas not on EIAEDs. Proc Am Soc Clin Oncol 22: 2004 (abstr 1502)
81. Honegger AM, Dull TJ, Felder S, et al: Point mutation at the ATP binding site of EGF receptor abolishes protein-tyrosine kinase activity and alters cellular routing. Cell 51:199-209, 1987
82. Huse M, Kuriyan J: The conformational plasticity of protein kinases. Cell 109:275-282, 2002
83. Gazdar A, Shigematsu H, Herz J, et al: Mutations and addiction to EGFR: The Achilles 'heal' of lung cancers? Trends Mol Med 10:481-486, 2004
84. Tracy S, Mukohara T, Hansen M, et al: Gefitinib induces apoptosis in the EGFRL858R non-small cell lung cancer cell line H3255. Cancer Res 64:7241-7244, 2004
85. Hirsch FR, Varella-Garcia M, Bunn PA, Jr., 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 21:3798-3807, 2003
86. Ko YC, Cheng LS, Lee CH, et al: Chinese food cooking and lung cancer in women non-smokers. Am J Epidemiol 151:140-147, 2000
87. Cheng Y, Chiou H, Sheu G, et al: The association of human papillomavirus 16/18 infection with lung cancer among nonsmoking Taiwanese women. Cancer Res 61:2799-2803, 2001
88. Stephens P, Hunter C, Bignell G, et al: Lung cancer: Intragenic ERBB2 kinase mutations in tumours. Nature 431:525-526, 2004
89. Rodenhuis S, Slebos RJC, Boot AJM, et al: Incidence and possible clinical significance of K-ras oncogene activation in adenocarcinoma of the human lung. Cancer Res 48:5738-5741, 1988
90. Suzuki Y, Orita M, Shiraishi M, et al: Detection of ras gene mutations in human lung cancers by single-strand conformation polymorphism analysis of polymerase chain reaction products. Oncogene 5:1037-1043, 1990
91. Rodenhuis S, Slebos RJ: The ras oncogenes in human lung cancer. Am Rev Respir Dis 142:S27-S30, 1990 (6 pt 2)
92. Ahrendt SA, Decker PA, Alawi EA, et al: Cigarette smoking is strongly associated with mutation of the K-ras gene in patients with primary adenocarcinoma of the lung. Cancer 92:1525-1530, 2001
93. Pao W, Wang TY, Riely GJ, et al: KRAS mutations and primary resistance of lung adenocarcinomas to gefitinib or erlotinib. PLoS Med 2:e17, 2005
94. Davies H, Bignell G, Cox C, et al: Mutations of the BRAF gene in human cancer. Nature 417:949-954, 2002
95. Brose MS, Volpe P, Feldman M, et al: BRAF and RAS mutations in human lung cancer and melanoma. Cancer Res 62:6997-7000, 2002
96. Naoki K, Chen TH, Richards WG, et al: Missense mutations of the BRAF gene in human lung adenocarcinoma. Cancer Res 62:7001-7003, 2002
97. Samuels Y, Wang Z, Bardelli A, et al: High frequency of mutations of the PIK3CA gene in human cancers. Science 304:554, 2004
98. Cappuzzo F, Magrini E, Ceresoli GL, et al: Akt phosphorylation and gefitinib efficacy in patients with advanced non-small-cell lung cancer. J Natl Cancer Inst 96:1133-1141, 2004
99. Pao W, Miller VA, Venkatraman E, et al: Predicting sensitivity of non-small-cell lung cancer to gefitinib: is there a role for P-Akt? J Natl Cancer Inst 96:1117-1119, 2004
100. O'Hare T, Pollock R, Stoffregen EP, et al: Inhibition of wild-type and mutant Bcr-Abl by AP23464, a potent ATP-based oncogenic protein kinase inhibitor: Implications for CML. Blood 104:2532-2539, 2004
101. Shah NP, Tran C, Lee FY, et al: Overriding imatinib resistance with a novel ABL kinase inhibitor. Science 305:399-401, 2004
102. Gorre ME, Sawyers CL: Molecular mechanisms of resistance to STI571 in chronic myeloid leukemia. Curr Opin Hematol 9:303-307, 2002
103. Sanchez-Cespedes M, Ahrendt SA, Piantadosi S, et al: Chromosomal alterations in lung adenocarcinoma from smokers and non-smokers. Cancer Res 61:1309-1313, 2001
104. Sekido Y, Fong KM, Minna JD: Molecular genetics of lung cancer. Annu Rev Med 54:73-87, 2003