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[Cancer Research 61, 8887-8895, December 15, 2001]
© 2001 American Association for Cancer Research

Tumor Biology

Epidermal Growth Factor Receptor (HER1) Tyrosine Kinase Inhibitor ZD1839 (Iressa) Inhibits HER2/neu (erbB2)-overexpressing Breast Cancer Cells in Vitro and in Vivo1

Stacy L. Moulder2, F. Michael Yakes2, Senthil K. Muthuswamy3, Roberto Bianco, Jean F. Simpson and Carlos L. Arteaga4

Departments of Medicine [S. L. M., F. M. Y., R. B., C. L. A.], Cancer Biology [C. L. A.], Pathology [J. F. S.], and Vanderbilt-Ingram Cancer Center [C. L. A.], Vanderbilt University School of Medicine, Nashville, Tennessee 37232-6307, and Department of Cell Biology, Harvard Medical School, Boston, Massachusetts 02115 [S. K. M.]

Aberrrant signaling by the epidermal growth factor receptor [EGFR (HER1, erbB1)] and/or HER2/neu tyrosine kinases is present in a cohort of breast carcinomas. Because HER2 is constitutively phosphorylated in some breast tumors, we speculated that, in these cancers, transmodulation of HER2 may occur via EGFR signaling. To test this possibility, we examined the effect of EGFR-specific kinase inhibitors against the HER2-overexpressing human breast tumor lines BT-474, SKBR-3, MDA-361, and MDA-453. ZD1839 (Iressa) is an ATP-mimetic that inhibits the purified EGFR and HER2 kinases in vitro with an IC50 of 0.033 and >3.7 µM, respectively. The specificity of ZD1839 against EGFR was confirmed in Rat1 fibroblasts transfected with EGFR or HER2 chimeric receptors activated by synthetic ligands without the interference of endogenous receptors. Treatment of all breast cancer cell lines (except MDA-453) with 1 µM ZD1839 almost completely eliminated HER2 phosphorylation. In contrast, the incorporation of [{gamma}-32P]ATP in vitro onto HER2 receptors isolated from BT-474 cells was unaffected by 1 µM ZD1839. EGFR is expressed by BT-474, SKBR-3, and MDA-361 but not by MDA-453 cells, suggesting that ZD1839-mediated inhibition of the EGFR kinase explained the inhibition of HER2 phosphorylation in vivo. In SKBR-3 cells, ZD1839 exhibited a greater growth-inhibitory effect than Herceptin, a monoclonal antibody against the HER2 ectodomain. In both SKBR-3 and BT-474 cells, treatment with ZD1839 plus Herceptin induced a greater apoptotic effect than either inhibitor alone. Finally, ZD1839 completely prevented growth of BT-474 xenografts established in nude mice and enhanced the antitumor effect of Herceptin. These data imply that EGFR tyrosine kinase inhibitors will be effective against HER2-overexpressing breast tumor cells that also express EGFR and support their use in combination with HER2 antibodies, such as Herceptin, against mammary carcinomas with high levels of the HER2 proto-oncogene.




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Epidermal Growth Factor Receptor, Protein Kinase B/Akt, and Glioma Response to Erlotinib
J Natl Cancer Inst, June 15, 2005; 97(12): 880 - 887.
[Abstract] [Full Text] [PDF]

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 Endocr Relat CancerHome page
N Normanno, A De Luca, D Aldinucci, M R Maiello, M Mancino, A D'Antonio, R De Filippi, and A Pinto
Gefitinib inhibits the ability of human bone marrow stromal cells to induce osteoclast differentiation: implications for the pathogenesis and treatment of bone metastasis
Endocr. Relat. Cancer, June 1, 2005; 12(2): 471 - 482.
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 Mol. Cell. Biol.Home page
S. E. Wang, F. Y. Wu, I. Shin, S. Qu, and C. L. Arteaga
Transforming Growth Factor {beta} (TGF-{beta})-Smad Target Gene Protein Tyrosine Phosphatase Receptor Type Kappa Is Required for TGF-{beta} Function
Mol. Cell. Biol., June 1, 2005; 25(11): 4703 - 4715.
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 Cancer Res.Home page
A. Hirata, F. Hosoi, M. Miyagawa, S.-i. Ueda, S. Naito, T. Fujii, M. Kuwano, and M. Ono
HER2 Overexpression Increases Sensitivity to Gefitinib, an Epidermal Growth Factor Receptor Tyrosine Kinase Inhibitor, through Inhibition of HER2/HER3 Heterodimer Formation in Lung Cancer Cells
Cancer Res., May 15, 2005; 65(10): 4253 - 4260.
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 Clin. Cancer Res.Home page
K. D. Miller, J. M. Trigo, C. Wheeler, A. Barge, J. Rowbottom, G. Sledge, and J. Baselga
A Multicenter Phase II Trial of ZD6474, a Vascular Endothelial Growth Factor Receptor-2 and Epidermal Growth Factor Receptor Tyrosine Kinase Inhibitor, in Patients with Previously Treated Metastatic Breast Cancer
Clin. Cancer Res., May 1, 2005; 11(9): 3369 - 3376.
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 JCOHome page
J. Baselga and C. L. Arteaga
Critical Update and Emerging Trends in Epidermal Growth Factor Receptor Targeting in Cancer
J. Clin. Oncol., April 10, 2005; 23(11): 2445 - 2459.
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 Cancer Res.Home page
I. Shin, J. Edl, S. Biswas, P. C. Lin, R. Mernaugh, and C. L. Arteaga
Proapoptotic Activity of Cell-Permeable Anti-Akt Single-Chain Antibodies
Cancer Res., April 1, 2005; 65(7): 2815 - 2824.
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 JCOHome page
C. J. Fabian and B. F. Kimler
Selective Estrogen-Receptor Modulators for Primary Prevention of Breast Cancer
J. Clin. Oncol., March 10, 2005; 23(8): 1644 - 1655.
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 Proc. Natl. Acad. Sci. USAHome page
J. A. Engelman, P. A. Janne, C. Mermel, J. Pearlberg, T. Mukohara, C. Fleet, K. Cichowski, B. E. Johnson, and L. C. Cantley
ErbB-3 mediates phosphoinositide 3-kinase activity in gefitinib-sensitive non-small cell lung cancer cell lines
PNAS, March 8, 2005; 102(10): 3788 - 3793.
[Abstract] [Full Text] [PDF]

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 Clin. Cancer Res.Home page
D. B. Solit, Y. She, J. Lobo, M. G. Kris, H. I. Scher, N. Rosen, and F. M. Sirotnak
Pulsatile Administration of the Epidermal Growth Factor Receptor Inhibitor Gefitinib Is Significantly More Effective than Continuous Dosing for Sensitizing Tumors to Paclitaxel
Clin. Cancer Res., March 1, 2005; 11(5): 1983 - 1989.
[Abstract] [Full Text] [PDF]

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 JCOHome page
M. P. DiGiovanna, D. F. Stern, S. M. Edgerton, S. G. Whalen, D. Moore II, and A. D. Thor
Relationship of Epidermal Growth Factor Receptor Expression to ErbB-2 Signaling Activity and Prognosis in Breast Cancer Patients
J. Clin. Oncol., February 20, 2005; 23(6): 1152 - 1160.
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 Clin. Cancer Res.Home page
C. Tuccillo, M. Romano, T. Troiani, E. Martinelli, F. Morgillo, F. De Vita, R. Bianco, G. Fontanini, R. A. Bianco, G. Tortora, et al.
Antitumor Activity of ZD6474, a Vascular Endothelial Growth Factor-2 and Epidermal Growth Factor Receptor Small Molecule Tyrosine Kinase Inhibitor, in Combination with SC-236, a Cyclooxygenase-2 Inhibitor
Clin. Cancer Res., February 1, 2005; 11(3): 1268 - 1276.
[Abstract] [Full Text] [PDF]

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 Clin. Cancer Res.Home page
S. R. Johnston
Combinations of Endocrine and Biological Agents: Present Status of Therapeutic and Presurgical Investigations
Clin. Cancer Res., January 15, 2005; 11(2): 889s - 899s.
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 Cancer Res.Home page
M. L. Reyzer, R. L. Caldwell, T. C. Dugger, J. T. Forbes, C. A. Ritter, M. Guix, C. L. Arteaga, and R. M. Caprioli
Early Changes in Protein Expression Detected by Mass Spectrometry Predict Tumor Response to Molecular Therapeutics
Cancer Res., December 15, 2004; 64(24): 9093 - 9100.
[Abstract] [Full Text] [PDF]

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 Endocr Relat CancerHome page
P M Harari
Epidermal growth factor receptor inhibition strategies in oncology
Endocr. Relat. Cancer, December 1, 2004; 11(4): 689 - 708.
[Abstract] [Full Text] [PDF]

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 Clin. Cancer Res.Home page
M. Milella, D. Trisciuoglio, T. Bruno, L. Ciuffreda, M. Mottolese, A. Cianciulli, F. Cognetti, U. Zangemeister-Wittke, D. Del Bufalo, and G. Zupi
Trastuzumab Down-Regulates Bcl-2 Expression and Potentiates Apoptosis Induction by Bcl-2/Bcl-XL Bispecific Antisense Oligonucleotides in HER-2Gene-Amplified Breast Cancer Cells
Clin. Cancer Res., November 15, 2004; 10(22): 7747 - 7756.
[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.
[Abstract] [Full Text] [PDF]

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 Cancer Res.Home page
S. Tracy, T. Mukohara, M. Hansen, M. Meyerson, B. E. Johnson, and P. A. Janne
Gefitinib Induces Apoptosis in the EGFRL858R Non-Small-Cell Lung Cancer Cell Line H3255
Cancer Res., October 15, 2004; 64(20): 7241 - 7244.
[Abstract] [Full Text] [PDF]

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 Molecular Cancer TherapeuticsHome page
C. D. Britten
Targeting ErbB receptor signaling: A pan-ErbB approach to cancer
Mol. Cancer Ther., October 1, 2004; 3(10): 1335 - 1342.
[Abstract] [Full Text] [PDF]

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 Clin. Cancer Res.Home page
P. Matar, F. Rojo, R. Cassia, G. Moreno-Bueno, S. Di Cosimo, J. Tabernero, M. Guzman, S. Rodriguez, J. Arribas, J. Palacios, et al.
Combined Epidermal Growth Factor Receptor Targeting with the Tyrosine Kinase Inhibitor Gefitinib (ZD1839) and the Monoclonal Antibody Cetuximab (IMC-C225): Superiority Over Single-Agent Receptor Targeting
Clin. Cancer Res., October 1, 2004; 10(19): 6487 - 6501.
[Abstract] [Full Text] [PDF]

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 JCOHome page
A. R. Tan, X. Yang, S. M. Hewitt, A. Berman, E. R. Lepper, A. Sparreboom, A. L. Parr, W. D. Figg, C. Chow, S. M. Steinberg, et al.
Evaluation of Biologic End Points and Pharmacokinetics in Patients With Metastatic Breast Cancer After Treatment With Erlotinib, an Epidermal Growth Factor Receptor Tyrosine Kinase Inhibitor
J. Clin. Oncol., August 1, 2004; 22(15): 3080 - 3090.
[Abstract] [Full Text] [PDF]

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 Cancer Res.Home page
S. Huang, E. A. Armstrong, S. Benavente, P. Chinnaiyan, and P. M. Harari
Dual-Agent Molecular Targeting of the Epidermal Growth Factor Receptor (EGFR): Combining Anti-EGFR Antibody with Tyrosine Kinase Inhibitor
Cancer Res., August 1, 2004; 64(15): 5355 - 5362.
[Abstract] [Full Text] [PDF]

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 Annals of Clinical & Laboratory ScienceHome page
R. E. Brown, M. Lun, J. W. Prichard, T. M. Blasick, and P. L. Zhang
Morphoproteomic and Pharmacoproteomic Correlates in Hormone-Receptor-Negative Breast Carcinoma Cell Lines
Ann. Clin. Lab. Sci., July 1, 2004; 34(3): 251 - 262.
[Abstract] [Full Text] [PDF]

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 J. Biol. Chem.Home page
Y. Ueda, S. Wang, N. Dumont, J. Y. Yi, Y. Koh, and C. L. Arteaga
Overexpression of HER2 (erbB2) in Human Breast Epithelial Cells Unmasks Transforming Growth Factor {beta}-induced Cell Motility
J. Biol. Chem., June 4, 2004; 279(23): 24505 - 24513.
[Abstract] [Full Text] [PDF]

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 The OncologistHome page
H. A. Burris III
Dual Kinase Inhibition in the Treatment of Breast Cancer: Initial Experience with the EGFR/ErbB-2 Inhibitor Lapatinib
Oncologist, June 3, 2004; 9(suppl_3): 10 - 15.
[Abstract] [Full Text] [PDF]

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 The OncologistHome page
K. D. Miller
The Role of ErbB Inhibitors in Trastuzumab Resistance
Oncologist, June 3, 2004; 9(suppl_3): 16 - 19.
[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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 JCOHome page
N. Normanno, M. Di Maio, F. Perrone, and M. Campiglio
Molecular Markers to Predict Response to Gefitinib: EGFR, ErbB-2, or More?
J. Clin. Oncol., May 15, 2004; 22(10): 2035 - 2036.
[Full Text] [PDF]

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 Molecular Cancer TherapeuticsHome page
M. Ono, A. Hirata, T. Kometani, M. Miyagawa, S.-i. Ueda, H. Kinoshita, T. Fujii, and M. Kuwano
Sensitivity to gefitinib (Iressa, ZD1839) in non-small cell lung cancer cell lines correlates with dependence on the epidermal growth factor (EGF) receptor/extracellular signal-regulated kinase 1/2 and EGF receptor/Akt pathway for proliferation
Mol. Cancer Ther., April 1, 2004; 3(4): 465 - 472.
[Abstract] [Full Text] [PDF]

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 Clin. Cancer Res.Home page
C. Warburton, W. H. Dragowska, K. Gelmon, S. Chia, H. Yan, D. Masin, T. Denyssevych, A. E. Wallis, and M. B. Bally
Treatment of HER-2/neu Overexpressing Breast Cancer Xenograft Models with Trastuzumab (Herceptin) and Gefitinib (ZD1839): Drug Combination Effects on Tumor Growth, HER-2/neu and Epidermal Growth Factor Receptor Expression, and Viable Hypoxic Cell Fraction
Clin. Cancer Res., April 1, 2004; 10(7): 2512 - 2524.
[Abstract] [Full Text] [PDF]

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 J. Biol. Chem.Home page
G. Yang, K. Q. Cai, J. A. Thompson-Lanza, R. C. Bast Jr., and J. Liu
Inhibition of Breast and Ovarian Tumor Growth through Multiple Signaling Pathways by Using Retrovirus-mediated Small Interfering RNA against Her-2/neu Gene Expression
J. Biol. Chem., February 6, 2004; 279(6): 4339 - 4345.
[Abstract] [Full Text] [PDF]

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 Cancer Res.Home page
S. D. Pack, O. M. Alper, K. Stromberg, M. Augustus, M. Ozdemirli, A. M. Miermont, G. Klus, M. Rusin, R. Slack, N. F. Hacker, et al.
Simultaneous Suppression of Epidermal Growth Factor Receptor and c-erbB-2 Reverses Aneuploidy and Malignant Phenotype of a Human Ovarian Carcinoma Cell Line
Cancer Res., February 1, 2004; 64(3): 789 - 794.
[Abstract] [Full Text] [PDF]

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 The OncologistHome page
R. Perez-Soler
HER1/EGFR Targeting: Refining the Strategy
Oncologist, February 1, 2004; 9(1): 58 - 67.
[Abstract] [Full Text] [PDF]

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 Clin. Cancer Res.Home page
Z. Yang, R. Bagheri-Yarmand, R.-A. Wang, L. Adam, V. V. Papadimitrakopoulou, G. L. Clayman, A. El-Naggar, R. Lotan, C. J. Barnes, W. K. Hong, et al.
The Epidermal Growth Factor Receptor Tyrosine Kinase Inhibitor ZD1839 (Iressa) Suppresses c-Src and Pak1 Pathways and Invasiveness of Human Cancer Cells
Clin. Cancer Res., January 15, 2004; 10(2): 658 - 667.
[Abstract] [Full Text] [PDF]

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 Clin. Cancer Res.Home page
M. K. Nyati, D. Maheshwari, S. Hanasoge, A. Sreekumar, S. D. Rynkiewicz, A. M. Chinnaiyan, W. R. Leopold, S. P. Ethier, and T. S. Lawrence
Radiosensitization by Pan ErbB Inhibitor CI-1033 in Vitro and in Vivo
Clin. Cancer Res., January 15, 2004; 10(2): 691 - 700.
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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.
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 Clin. Cancer Res.Home page
M. Sumitomo, T. Asano, J. Asakuma, T. Asano, A. Horiguchi, and M. Hayakawa
ZD1839 Modulates Paclitaxel Response in Renal Cancer by Blocking Paclitaxel-Induced Activation of the Epidermal Growth Factor Receptor-Extracellular Signal-Regulated Kinase Pathway
Clin. Cancer Res., January 15, 2004; 10(2): 794 - 801.
[Abstract] [Full Text] [PDF]

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 JNCI J Natl Cancer InstHome page
G. E. Konecny, C. A. Wilson, and D. J. Slamon
Is There a Role for Epidermal Growth Factor Receptor Inhibitors in Breast Cancer Prevention?
J Natl Cancer Inst, December 17, 2003; 95(24): 1813 - 1815.
[Full Text] [PDF]

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 JNCI J Natl Cancer InstHome page
C. Lu, C. Speers, Y. Zhang, X. Xu, J. Hill, E. Steinbis, J. Celestino, Q. Shen, H. Kim, S. Hilsenbeck, et al.
Effect of Epidermal Growth Factor Receptor Inhibitor on Development of Estrogen Receptor-Negative Mammary Tumors
J Natl Cancer Inst, December 17, 2003; 95(24): 1825 - 1833.
[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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