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Clinical Cancer Research Vol. 7, 2958-2970, October 2001
© 2001 American Association for Cancer Research

Review

A Novel Approach in the Treatment of Cancer: Targeting the Epidermal Growth Factor Receptor1

Fortunato Ciardiello2 and Giampaolo Tortora

Cattedra di Oncologia Medica, Dipartimento di Endocrinologia e Oncologia Molecolare e Clinica, Università di Napoli "Federico II," 80131 Napoli, Italy

The epidermal growth factor receptor (EGFR) autocrine pathway contributes to a number of processes important to cancer development and progression, including cell proliferation, apoptosis, angiogenesis, and metastatic spread. The critical role the EGFR plays in cancer has led to an extensive search for selective inhibitors of the EGFR signaling pathway. The results of a large body of preclinical studies and the early clinical trials thus far conducted suggest that targeting the EGFR could represent a significant contribution to cancer therapy. A variety of different approaches are currently being used to target the EGFR. The most promising strategies in clinical development include monoclonal antibodies to prevent ligand binding and small molecule inhibitors of the tyrosine kinase enzymatic activity to inhibit autophosphorylation and downstream intracellular signaling. At least five blocking monoclonal antibodies have been developed against the EGFR. Among these, IMC-225 is a chimeric human-mouse monoclonal IgG1 antibody that has been the first anti-EGFR targeted therapy to enter clinical evaluation in cancer patients in Phase II and III studies, alone or in combination with conventional therapies, such as radiotherapy and chemotherapy. A number of small molecule inhibitors of the EGFR tyrosine kinase enzymatic activity is also in development. OSI-774 and ZD1839 (Iressa) are currently in Phase II and III development, respectively. ZD1839, a p.o. active, selective quinazoline derivative has demonstrated promising in vitro and in vivo antitumor activity. Preliminary results from Phase I and II trials in patients with advanced disease demonstrate that ZD1839 and OSI-774 have an acceptable tolerability profile and promising clinical efficacy in patients with a variety of tumor types. This mini-review describes the EGFR inhibitors in clinical development.




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H E Jones, L Goddard, J M W Gee, S Hiscox, M Rubini, D Barrow, J M Knowlden, S Williams, A E Wakeling, and R I Nicholson
Insulin-like growth factor-I receptor signalling and acquired resistance to gefitinib (ZD1839; Iressa) in human breast and prostate cancer cells
Endocr. Relat. Cancer, December 1, 2004; 11(4): 793 - 814.
[Abstract] [Full Text] [PDF]

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 Clin. Cancer Res.Home page
L. H. Kalish, R. A. Kwong, I. E. Cole, R. M. Gallagher, R. L. Sutherland, and E. A. Musgrove
Deregulated Cyclin D1 Expression Is Associated with Decreased Efficacy of the Selective Epidermal Growth Factor Receptor Tyrosine Kinase Inhibitor Gefitinib in Head and Neck Squamous Cell Carcinoma Cell Lines
Clin. Cancer Res., November 15, 2004; 10(22): 7764 - 7774.
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 Cancer Res.Home page
O. G. Yigitbasi, M. N. Younes, D. Doan, S. A. Jasser, B. A. Schiff, C. D. Bucana, B. N. Bekele, I. J. Fidler, and J. N. Myers
Tumor Cell and Endothelial Cell Therapy of Oral Cancer by Dual Tyrosine Kinase Receptor Blockade
Cancer Res., November 1, 2004; 64(21): 7977 - 7984.
[Abstract] [Full Text] [PDF]

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 Clin. Cancer Res.Home page
B. Friedmann, M. Caplin, J. A. Hartley, and D. Hochhauser
Modulation of DNA Repair In vitro after Treatment with Chemotherapeutic Agents by the Epidermal Growth Factor Receptor Inhibitor Gefitinib (ZD1839)
Clin. Cancer Res., October 1, 2004; 10(19): 6476 - 6486.
[Abstract] [Full Text] [PDF]

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 JCOHome page
B. Van Den Bossche and C. Van de Wiele
Receptor Imaging in Oncology by Means of Nuclear Medicine: Current Status
J. Clin. Oncol., September 1, 2004; 22(17): 3593 - 3607.
[Abstract] [Full Text] [PDF]

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 Clin. Cancer Res.Home page
Z. Chen, X. Zhang, M. Li, Z. Wang, H. S. Wieand, J. R. Grandis, and D. M. Shin
Simultaneously Targeting Epidermal Growth Factor Receptor Tyrosine Kinase and Cyclooxygenase-2, an Efficient Approach to Inhibition of Squamous Cell Carcinoma of the Head and Neck
Clin. Cancer Res., September 1, 2004; 10(17): 5930 - 5939.
[Abstract] [Full Text] [PDF]

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 JNCI J Natl Cancer InstHome page
F. Cappuzzo, E. Magrini, G. L. Ceresoli, S. Bartolini, E. Rossi, V. Ludovini, V. Gregorc, C. Ligorio, A. Cancellieri, S. Damiani, et al.
Akt Phosphorylation and Gefitinib Efficacy in Patients With Advanced Non-Small-Cell Lung Cancer
J Natl Cancer Inst, August 4, 2004; 96(15): 1133 - 1141.
[Abstract] [Full Text] [PDF]

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 NEJMHome page
D. Cunningham, Y. Humblet, S. Siena, D. Khayat, H. Bleiberg, A. Santoro, D. Bets, M. Mueser, A. Harstrick, C. Verslype, et al.
Cetuximab Monotherapy and Cetuximab plus Irinotecan in Irinotecan-Refractory Metastatic Colorectal Cancer
N. Engl. J. Med., July 22, 2004; 351(4): 337 - 345.
[Abstract] [Full Text] [PDF]

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 Clin. Cancer Res.Home page
R. Bianco, R. Caputo, R. Caputo, V. Damiano, S. De Placido, C. Ficorella, S. Agrawal, A. R. Bianco, F. Ciardiello, and G. Tortora
Combined Targeting of Epidermal Growth Factor Receptor and MDM2 by Gefitinib and Antisense MDM2 Cooperatively Inhibit Hormone-Independent Prostate Cancer
Clin. Cancer Res., July 15, 2004; 10(14): 4858 - 4864.
[Abstract] [Full Text] [PDF]

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 J. Histochem. Cytochem.Home page
D. Atkins, K.-A. Reiffen, C. L. Tegtmeier, H. Winther, M. S. Bonato, and S. Storkel
Immunohistochemical Detection of EGFR in Paraffin-embedded Tumor Tissues: Variation in Staining Intensity Due to Choice of Fixative and Storage Time of Tissue Sections
J. Histochem. Cytochem., July 1, 2004; 52(7): 893 - 901.
[Abstract] [Full Text] [PDF]

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 Ann OncolHome page
L. Castillo, M. C. Etienne-Grimaldi, J. L. Fischel, P. Formento, N. Magne, and G. Milano
Pharmacological background of EGFR targeting
Ann. Onc., July 1, 2004; 15(7): 1007 - 1012.
[Abstract] [Full Text] [PDF]

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 Clin. Cancer Res.Home page
G. Giaccone
The Role of Gefitinib in Lung Cancer Treatment
Clin. Cancer Res., June 15, 2004; 10(12): 4233S - 4237S.
[Abstract] [Full Text] [PDF]

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 Cancer Res.Home page
S. K. Rabindran, C. M. Discafani, E. C. Rosfjord, M. Baxter, M. B. Floyd, J. Golas, W. A. Hallett, B. D. Johnson, R. Nilakantan, E. Overbeek, et al.
Antitumor Activity of HKI-272, an Orally Active, Irreversible Inhibitor of the HER-2 Tyrosine Kinase
Cancer Res., June 1, 2004; 64(11): 3958 - 3965.
[Abstract] [Full Text] [PDF]

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 J. Biol. Chem.Home page
T. Ahmad, G. Farnie, N. J. Bundred, and N. G. Anderson
The Mitogenic Action of Insulin-like Growth Factor I in Normal Human Mammary Epithelial Cells Requires the Epidermal Growth Factor Receptor Tyrosine Kinase
J. Biol. Chem., January 16, 2004; 279(3): 1713 - 1719.
[Abstract] [Full Text] [PDF]

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 Clin. Cancer Res.Home page
F. Ciardiello, R. Bianco, R. Caputo, R. Caputo, V. Damiano, T. Troiani, D. Melisi, F. De Vita, S. De Placido, A. R. Bianco, et al.
Antitumor Activity of ZD6474, a Vascular Endothelial Growth Factor Receptor Tyrosine Kinase Inhibitor, in Human Cancer Cells with Acquired Resistance to Antiepidermal Growth Factor Receptor Therapy
Clin. Cancer Res., January 15, 2004; 10(2): 784 - 793.
[Abstract] [Full Text] [PDF]

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 Ann OncolHome page
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. Onc., January 1, 2004; 15(1): 28 - 32.
[Abstract] [Full Text] [PDF]

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 GutHome page
J-L Yang, X-J Qu, P J Russell, and D Goldstein
Regulation of epidermal growth factor receptor in human colon cancer cell lines by interferon {alpha}
Gut, January 1, 2004; 53(1): 123 - 129.
[Abstract] [Full Text] [PDF]

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 JCOHome page
J. N. Rich, D. A. Reardon, T. Peery, J. M. Dowell, J. A. Quinn, K. L. Penne, C. J. Wikstrand, L. B. Van Duyn, J. E. Dancey, R. E. McLendon, et al.
Phase II Trial of Gefitinib in Recurrent Glioblastoma
J. Clin. Oncol., January 1, 2004; 22(1): 133 - 142.
[Abstract] [Full Text] [PDF]

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 Clin. Cancer Res.Home page
X.-H. Tang, B. Knudsen, D. Bemis, S. Tickoo, and L. J. Gudas
Oral Cavity and Esophageal Carcinogenesis Modeled in Carcinogen-Treated Mice
Clin. Cancer Res., January 1, 2004; 10(1): 301 - 313.
[Abstract] [Full Text] [PDF]

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 J Oncol Pharm PractHome page
S. R Shah, T. L Walsh, C. B Williams, and S. A Soefje
Gefitinib (ZD1839, Iressa(R)): a selective epidermal growth factor receptor-tyrosine kinase inhibitor
Journal of Oncology Pharmacy Practice, December 1, 2003; 9(4): 151 - 160.
[Abstract] [PDF]

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 Protein Eng Des SelHome page
M. Bach, P. Holig, E. Schlosser, T. Volkel, A. Graser, R. Muller, and R. E. Kontermann
Isolation from phage display libraries of lysine-deficient human epidermal growth factor variants for directional conjugation as targeting ligands
Protein Eng. Des. Sel., December 1, 2003; 16(12): 1107 - 1113.
[Abstract] [Full Text] [PDF]

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 Clin. Cancer Res.Home page
R. S. Herbst and P. A. Bunn Jr.
Targeting the Epidermal Growth Factor Receptor in Non-Small Cell Lung Cancer
Clin. Cancer Res., December 1, 2003; 9(16): 5813 - 5824.
[Abstract] [Full Text] [PDF]

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 The OncologistHome page
M. L. Janmaat and G. Giaccone
Small-Molecule Epidermal Growth Factor Receptor Tyrosine Kinase Inhibitors
Oncologist, December 1, 2003; 8(6): 576 - 586.
[Abstract] [Full Text] [PDF]

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 Cancer Res.Home page
T. M. Grana, C. I. Sartor, and A. D. Cox
Epidermal Growth Factor Receptor Autocrine Signaling in RIE-1 Cells Transformed by the Ras Oncogene Enhances Radiation Resistance
Cancer Res., November 15, 2003; 63(22): 7807 - 7814.
[Abstract] [Full Text] [PDF]

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 Clin. Cancer Res.Home page
O. Murillo, A. Arina, I. Tirapu, C. Alfaro, G. Mazzolini, B. Palencia, A. L.-D. De Cerio, J. Prieto, M. Bendandi, and I. Melero
Potentiation of Therapeutic Immune Responses against Malignancies with Monoclonal Antibodies
Clin. Cancer Res., November 15, 2003; 9(15): 5454 - 5464.
[Abstract] [Full Text] [PDF]

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 JCOHome page
F. R. Hirsch, M. Varella-Garcia, P. A. Bunn Jr, M. V. Di Maria, R. Veve, R. M. Bremnes, A. E. Baron, C. Zeng, and W. A. Franklin
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., October 15, 2003; 21(20): 3798 - 3807.
[Abstract] [Full Text] [PDF]

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 J. Biol. Chem.Home page
C. Buerger, K. Nagel-Wolfrum, C. Kunz, I. Wittig, K. Butz, F. Hoppe-Seyler, and B. Groner
Sequence-specific Peptide Aptamers, Interacting with the Intracellular Domain of the Epidermal Growth Factor Receptor, Interfere with Stat3 Activation and Inhibit the Growth of Tumor Cells
J. Biol. Chem., September 26, 2003; 278(39): 37610 - 37621.
[Abstract] [Full Text] [PDF]

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 Circ. Res.Home page
H. S. Shin, H. J. Lee, M. Nishida, M.-S. Lee, R. Tamura, S. Yamashita, Y. Matsuzawa, I.-K. Lee, and G. Y. Koh
Betacellulin and Amphiregulin Induce Upregulation of Cyclin D1 and DNA Synthesis Activity Through Differential Signaling Pathways in Vascular Smooth Muscle Cells
Circ. Res., August 22, 2003; 93(4): 302 - 310.
[Abstract] [Full Text] [PDF]

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 Cancer Res.Home page
H. Suzuki, K. Aoshiba, N. Yokohori, and A. Nagai
Epidermal Growth Factor Receptor Tyrosine Kinase Inhibition Augments a Murine Model of Pulmonary Fibrosis
Cancer Res., August 15, 2003; 63(16): 5054 - 5059.
[Abstract] [Full Text] [PDF]

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 Cancer Res.Home page
E. G. Barbacci, L. R. Pustilnik, A. M. K. Rossi, E. Emerson, P. E. Miller, B. P. Boscoe, E. D. Cox, K. K. Iwata, J. P. Jani, K. Provoncha, et al.
The Biological and Biochemical Effects of CP-654577, a Selective erbB2 Kinase Inhibitor, on Human Breast Cancer Cells
Cancer Res., August 1, 2003; 63(15): 4450 - 4459.
[Abstract] [Full Text] [PDF]

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 Am. J. Pathol.Home page
F. Mascia, V. Mariani, G. Girolomoni, and S. Pastore
Blockade of the EGF Receptor Induces a Deranged Chemokine Expression in Keratinocytes Leading to Enhanced Skin Inflammation
Am. J. Pathol., July 1, 2003; 163(1): 303 - 312.
[Abstract] [Full Text] [PDF]

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 JNCI J Natl Cancer InstHome page
V. Grunwald and M. Hidalgo
Developing Inhibitors of the Epidermal Growth Factor Receptor for Cancer Treatment
J Natl Cancer Inst, June 18, 2003; 95(12): 851 - 867.
[Abstract] [Full Text] [PDF]

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 Molecular Cancer TherapeuticsHome page
M. Matsuo, H. Sakurai, and I. Saiki
ZD1839, a Selective Epidermal Growth Factor Receptor Tyrosine Kinase Inhibitor, Shows Antimetastatic Activity Using a Hepatocellular Carcinoma Model
Mol. Cancer Ther., June 1, 2003; 2(6): 557 - 561.
[Abstract] [Full Text] [PDF]

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 Clin. Cancer Res.Home page
M. L. Janmaat, F. A. E. Kruyt, J. A. Rodriguez, and G. Giaccone
Response to Epidermal Growth Factor Receptor Inhibitors in Non-Small Cell Lung Cancer Cells: Limited Antiproliferative Effects and Absence of Apoptosis Associated with Persistent Activity of Extracellular Signal-regulated Kinase or Akt Kinase Pathways
Clin. Cancer Res., June 1, 2003; 9(6): 2316 - 2326.
[Abstract] [Full Text] [PDF]

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 Cancer Res.Home page
L. Rosano, F. Spinella, D. Salani, V. Di Castro, A. Venuti, M. R. Nicotra, P. G. Natali, and A. Bagnato
Therapeutic Targeting of the Endothelin A Receptor in Human Ovarian Carcinoma
Cancer Res., May 15, 2003; 63(10): 2447 - 2453.
[Abstract] [Full Text] [PDF]

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 JCOHome page
E. E. W. Cohen, F. Rosen, W. M. Stadler, W. Recant, K. Stenson, D. Huo, and E. E. Vokes
Phase II Trial of ZD1839 in Recurrent or Metastatic Squamous Cell Carcinoma of the Head and Neck
J. Clin. Oncol., May 15, 2003; 21(10): 1980 - 1987.
[Abstract] [Full Text] [PDF]

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 Clin. Cancer Res.Home page
F. Ciardiello, R. Caputo, V. Damiano, R. Caputo, T. Troiani, D. Vitagliano, F. Carlomagno, B. M. Veneziani, G. Fontanini, A. R. Bianco, et al.
Antitumor Effects of ZD6474, a Small Molecule Vascular Endothelial Growth Factor Receptor Tyrosine Kinase Inhibitor, with Additional Activity against Epidermal Growth Factor Receptor Tyrosine Kinase
Clin. Cancer Res., April 1, 2003; 9(4): 1546 - 1556.
[Abstract] [Full Text] [PDF]

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 Clin. Cancer Res.Home page
G. Tortora, R. Caputo, V. Damiano, D. Melisi, R. Bianco, G. Fontanini, B. M. Veneziani, S. De Placido, A. R. Bianco, and F. Ciardiello
Combination of a Selective Cyclooxygenase-2 Inhibitor with Epidermal Growth Factor Receptor Tyrosine Kinase Inhibitor ZD1839 and Protein Kinase A Antisense Causes Cooperative Antitumor and Antiangiogenic Effect
Clin. Cancer Res., April 1, 2003; 9(4): 1566 - 1572.
[Abstract] [Full Text] [PDF]

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 Pharmacol. Rev.Home page
R. Danesi, F. De Braud, S. Fogli, T. M. De Pas, A. Di Paolo, G. Curigliano, and M. Del Tacca
Pharmacogenetics of Anticancer Drug Sensitivity in Non-Small Cell Lung Cancer
Pharmacol. Rev., March 1, 2003; 55(1): 57 - 103.
[Abstract] [Full Text] [PDF]


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