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[Cancer Research 61, 5090-5101, July 1, 2001]
© 2001 American Association for Cancer Research

Experimental Therapeutics

Acquired Resistance to the Antitumor Effect of Epidermal Growth Factor Receptor-blocking Antibodies in Vivo

A Role for Altered Tumor Angiogenesis1

Alicia Viloria-Petit, Tania Crombet, Serge Jothy, Daniel Hicklin, Peter Bohlen, Jean Marc Schlaeppi, Janusz Rak and Robert S. Kerbel2

Molecular and Cellular Biology Research [A. V-P., R. S. K.] and Department of Anatomic Pathology [S. J.], Sunnybrook and Women’s College Health Sciences Centre, Toronto, Ontario M4N 3M5, Canada; Clinical Immunology Division, Center of Molecular Immunology, Havana, Cuba [T. C.]; ImClone Systems, Inc., New York, New York [D. H., P. B.]; Core Technology Department, Novartis Pharmaceuticals, Novartis Limited, Basel, Switzerland [J. M. S.]; and Hamilton Civic Hospitals Research Centre, Ontario, Canada [J. R.]

Inhibitors of epidermal growth factor receptor (EGFR) signaling are among the novel drugs showing great promise for cancer treatment in the clinic. However, the possibility of acquired resistance to such drugs because of tumor cell genetic instabilities has not yet been explored. Here we report the experimental derivation and properties of such cell variants obtained from recurrent tumor xenografts of the human A431 squamous cell carcinoma, after two consecutive cycles of therapy with one of three different anti-EGFR monoclonal antibodies: mR3, hR3, or C225. Initial response to a 2-week period of treatment was generally total tumor regression and was not significantly different among the three antibody groups. However, tumors often reappeared at the site of inoculation, generally after prolonged latency periods, and most of the tumors became refractory to a second round of therapy. Cell lines established from such resistant tumors retained high EGFR expression, normal sensitivity to anti-EGFR antibody or ligand, and unaltered growth rate when compared with the parental line in vitro. In contrast, the A431 cell variants exhibited an accelerated growth rate and a significantly attenuated response to anti-EGFR antibodies in vivo relative to the parental line. Because of the reported suppressive effect of EGFR inhibitors on vascular endothelial growth factor (VEGF) expression, and the demonstrated role of VEGF in the angiogenesis and growth of A431 tumor xenografts, relative VEGF expression was examined. Five of six resistant variants expressed increased levels of VEGF, which paralleled an increase in both angiogenic potential in vitro and tumor angiogenesis in vivo. In addition, elevated expression of VEGF in variants of A431 cells obtained by gene transfection rendered the cells significantly resistant to anti-EGFR antibodies in vivo. Taken together, the results suggest that, at least in the A431 system, variants displaying acquired resistance to anti-EGFR antibodies can emerge in vivo and can do so, at least in part, by mechanisms involving the selection of tumor cell subpopulations with increased angiogenic potential.




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J. M.L. Ebos, J. Tran, Z. Master, D. Dumont, J. V. Melo, E. Buchdunger, and R. S. Kerbel
Imatinib Mesylate (STI-571) Reduces Bcr-Abl-Mediated Vascular Endothelial Growth Factor Secretion in Chronic Myelogenous Leukemia
Mol. Cancer Res., December 1, 2002; 1(2): 89 - 95.
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M. S. O'Reilly
Targeting Multiple Biological Pathways as a Strategy to Improve the Treatment of Cancer
Clin. Cancer Res., November 1, 2002; 8(11): 3309 - 3310.
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R. Fukuda, K. Hirota, F. Fan, Y. D. Jung, L. M. Ellis, and G. L. Semenza
Insulin-like Growth Factor 1 Induces Hypoxia-inducible Factor 1-mediated Vascular Endothelial Growth Factor Expression, Which is Dependent on MAP Kinase and Phosphatidylinositol 3-Kinase Signaling in Colon Cancer Cells
J. Biol. Chem., October 4, 2002; 277(41): 38205 - 38211.
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F. A. Scappaticci
Mechanisms and Future Directions for Angiogenesis-Based Cancer Therapies
J. Clin. Oncol., September 15, 2002; 20(18): 3906 - 3927.
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T. Karashima, P. Sweeney, J. W. Slaton, S. J. Kim, D. Kedar, J. I. Izawa, Z. Fan, C. Pettaway, D. J. Hicklin, T. Shuin, et al.
Inhibition of Angiogenesis by the Antiepidermal Growth Factor Receptor Antibody ImClone C225 in Androgen-independent Prostate Cancer Growing Orthotopically in Nude Mice
Clin. Cancer Res., May 1, 2002; 8(5): 1253 - 1264.
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R. S. Kerbel
Clinical Trials of Antiangiogenic Drugs: Opportunities, Problems, and Assessment of Initial Results
J. Clin. Oncol., September 15, 2001; 19(90001): 45s - 51.
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