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[Cancer Research 60, 2926-2935, June 1, 2000]
© 2000 American Association for Cancer Research

Experimental Therapeutics

Blockade of the Epidermal Growth Factor Receptor Signaling by a Novel Tyrosine Kinase Inhibitor Leads to Apoptosis of Endothelial Cells and Therapy of Human Pancreatic Carcinoma1

Christiane J. Bruns, Carmen C. Solorzano, Matthew T. Harbison, Shutaro Ozawa, Rachel Tsan, Dominic Fan, James Abbruzzese, Peter Traxler, Elisabeth Buchdunger, Robert Radinsky and Isaiah J. Fidler2

Departments of Cancer Biology [C. J. B., C. C. S., M. T. H., S. O., R. T., D. F., R. R., I. J. F.] and Gastrointestinal Oncology and Digestive Diseases [J. A.], The University of Texas M. D. Anderson Cancer Center, Houston, Texas 77030, and Novartis Pharma, CH-4002 Basel, Switzerland [P. T., E. B.]

We determined whether down-regulation of the epidermal growth factor-receptor (EGF-R) signaling pathway by oral administration of a novel EGF-R tyrosine kinase inhibitor (PKI166) alone or in combination with gemcitabine (administered i.p.) can inhibit growth and metastasis of human pancreatic carcinoma cells implanted into the pancreas of nude mice. Therapy beginning 7 days after orthotopic injection of L3.6pl human pancreatic cancer cells reduced the volume of pancreatic tumors by 59% in mice treated with gemcitabine only, by 45% in those treated with PKI166 only, and by 85% in those given both drugs. The combination therapy also significantly inhibited lymph node and liver metastasis, which led to a significant increase in overall survival. EGF-R activation was significantly blocked by therapy with PKI166 and was associated with significant reduction in tumor cell production of VEGF and IL-8, which in turn correlated with a significant decrease in microvessel density and an increase in apoptotic endothelial cells. Collectively, our results demonstrate that oral administration of an EGF-R tyrosine kinase inhibitor decreased growth and metastasis of human pancreatic cancer growing orthotopically in nude mice and increased survival. The therapeutic effects were mediated in part by inhibition of tumor-induced angiogenesis attributable to a decrease in production of proangiogenic molecules by tumor cells and increased apoptosis of tumor-associated endothelial cells.




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F. C. Holsinger, D. D. Doan, S. A. Jasser, E. A. Swan, J. S. Greenberg, B. A. Schiff, B. N. Bekele, M. N. Younes, C. D. Bucana, I. J. Fidler, et al.
Epidermal Growth Factor Receptor Blockade Potentiates Apoptosis Mediated by Paclitaxel and Leads to Prolonged Survival in a Murine Model of Oral Cancer
Clin. Cancer Res., August 1, 2003; 9(8): 3183 - 3189.
[Abstract] [Full Text] [PDF]

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A. Garofalo, E. Naumova, L. Manenti, C. Ghilardi, G. Ghisleni, M. Caniatti, T. Colombo, J. M. Cherrington, E. Scanziani, M. I. Nicoletti, et al.
The Combination of the Tyrosine Kinase Receptor Inhibitor SU6668 with Paclitaxel Affects Ascites Formation and Tumor Spread in Ovarian Carcinoma Xenografts Growing Orthotopically
Clin. Cancer Res., August 1, 2003; 9(9): 3476 - 3485.
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J. Mendelsohn and J. Baselga
Status of Epidermal Growth Factor Receptor Antagonists in the Biology and Treatment of Cancer
J. Clin. Oncol., July 15, 2003; 21(14): 2787 - 2799.
[Abstract] [Full Text] [PDF]

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 Cancer Res.Home page
K. L. Weber, M. Doucet, J. E. Price, C. Baker, S. J. Kim, and I. J. Fidler
Blockade of Epidermal Growth Factor Receptor Signaling Leads to Inhibition of Renal Cell Carcinoma Growth in the Bone of Nude Mice
Cancer Res., June 1, 2003; 63(11): 2940 - 2947.
[Abstract] [Full Text] [PDF]

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C. C. Solorzano, R. Hwang, C. H. Baker, C. D. Bucana, P. W. Pisters, D. B. Evans, J. J. Killion, and I. J. Fidler
Administration of Optimal Biological Dose and Schedule of Interferon {alpha} Combined with Gemcitabine Induces Apoptosis in Tumor-associated Endothelial Cells and Reduces Growth of Human Pancreatic Carcinoma Implanted Orthotopically in Nude Mice
Clin. Cancer Res., May 1, 2003; 9(5): 1858 - 1867.
[Abstract] [Full Text] [PDF]

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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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S.-J. Kim, H. Uehara, T. Karashima, D. L. Shepherd, J. J. Killion, and I. J. Fidler
Blockade of Epidermal Growth Factor Receptor Signaling in Tumor Cells and Tumor-associated Endothelial Cells for Therapy of Androgen-independent Human Prostate Cancer Growing in the Bone of Nude Mice
Clin. Cancer Res., March 1, 2003; 9(3): 1200 - 1210.
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 Ann OncolHome page
K. D. Miller, C. J. Sweeney, and G. W. Sledge
The Snark is a Boojum: the continuing problem of drug resistance in the antiangiogenic era
Ann. Onc., January 1, 2003; 14(1): 20 - 28.
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 Mol Cancer ResHome page
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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 Molecular Cancer TherapeuticsHome page
S. T. Nawrocki, C. J. Bruns, M. T. Harbison, R. J. Bold, B. S. Gotsch, J. L. Abbruzzese, P. Elliott, J. Adams, and D. J. McConkey
Effects of the Proteasome Inhibitor PS-341 on Apoptosis and Angiogenesis in Orthotopic Human Pancreatic Tumor Xenografts
Mol. Cancer Ther., December 1, 2002; 1(14): 1243 - 1253.
[Abstract] [Full Text] [PDF]

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M. Li, C. Ye, C. Feng, F. Riedel, X. Liu, Q. Zeng, and J. R. Grandis
Enhanced Antiangiogenic Therapy of Squamous Cell Carcinoma by Combined Endostatin and Epidermal Growth Factor Receptor-Antisense Therapy
Clin. Cancer Res., November 1, 2002; 8(11): 3570 - 3578.
[Abstract] [Full Text] [PDF]

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D. Kedar, C. H. Baker, J. J. Killion, C. P. N. Dinney, and I. J. Fidler
Blockade of the Epidermal Growth Factor Receptor Signaling Inhibits Angiogenesis Leading to Regression of Human Renal Cell Carcinoma Growing Orthotopically in Nude Mice
Clin. Cancer Res., November 1, 2002; 8(11): 3592 - 3600.
[Abstract] [Full Text] [PDF]

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 Cancer Res.Home page
K. Matsuda, T. Idezawa, X. J. You, N. H. Kothari, H. Fan, and M. Korc
Multiple Mitogenic Pathways in Pancreatic Cancer Cells Are Blocked by a Truncated Epidermal Growth Factor Receptor
Cancer Res., October 1, 2002; 62(19): 5611 - 5617.
[Abstract] [Full Text] [PDF]

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 Molecular Cancer TherapeuticsHome page
V. M. Bondar, B. Sweeney-Gotsch, M. Andreeff, G. B. Mills, and D. J. McConkey
Inhibition of the Phosphatidylinositol 3'-Kinase-AKT Pathway Induces Apoptosis in Pancreatic Carcinoma Cells in Vitro and in Vivo
Mol. Cancer Ther., October 1, 2002; 1(12): 989 - 997.
[Abstract] [Full Text] [PDF]

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N. Reinmuth, W. Liu, F. Fan, Y. D. Jung, S. A. Ahmad, O. Stoeltzing, C. D. Bucana, R. Radinsky, and L. M. Ellis
Blockade of Insulin-like Growth Factor I Receptor Function Inhibits Growth and Angiogenesis of Colon Cancer
Clin. Cancer Res., October 1, 2002; 8(10): 3259 - 3269.
[Abstract] [Full Text] [PDF]

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 Cancer Res.Home page
I. K. Mellinghoff, C. Tran, and C. L. Sawyers
Growth Inhibitory Effects of the Dual ErbB1/ErbB2 Tyrosine Kinase Inhibitor PKI-166 on Human Prostate Cancer Xenografts
Cancer Res., September 15, 2002; 62(18): 5254 - 5259.
[Abstract] [Full Text] [PDF]

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 Am. J. Pathol.Home page
C. H. Baker, D. Kedar, M. F. McCarty, R. Tsan, K. L. Weber, C. D. Bucana, and I. J. Fidler
Blockade of Epidermal Growth Factor Receptor Signaling on Tumor Cells and Tumor-Associated Endothelial Cells for Therapy of Human Carcinomas
Am. J. Pathol., September 1, 2002; 161(3): 929 - 938.
[Abstract] [Full Text] [PDF]

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 Cancer Res.Home page
S.-M. Huang, J. Li, E. A. Armstrong, and P. M. Harari
Modulation of Radiation Response and Tumor-induced Angiogenesis after Epidermal Growth Factor Receptor Inhibition by ZD1839 (Iressa)
Cancer Res., August 1, 2002; 62(15): 4300 - 4306.
[Abstract] [Full Text] [PDF]

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 Arch Otolaryngol Head Neck SurgHome page
J. N. Myers, F. C. Holsinger, B. N. Bekele, E. Li, S. A. Jasser, J. J. Killion, and I. J. Fidler
Targeted Molecular Therapy for Oral Cancer With Epidermal Growth Factor Receptor Blockade: A Preliminary Report
Arch Otolaryngol Head Neck Surg, August 1, 2002; 128(8): 875 - 879.
[Abstract] [Full Text] [PDF]

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 Molecular Cancer TherapeuticsHome page
S. S. W. Ng, M.-S. Tsao, T. Nicklee, and D. W. Hedley
Effects of the Epidermal Growth Factor Receptor Inhibitor OSI-774, Tarceva, on Downstream Signaling Pathways and Apoptosis in Human Pancreatic Adenocarcinoma
Mol. Cancer Ther., August 1, 2002; 1(10): 777 - 783.
[Abstract] [Full Text] [PDF]

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V. Kaushal, M. Kohli, M. Zangari, L. Fink, P. Mehta, B. Kuenen, and G. Giaccone
Endothelial Dysfunction in Antiangiogenesis-Associated Thrombosis
J. Clin. Oncol., July 1, 2002; 20(13): 3042 - 3043.
[Full Text] [PDF]

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S. Tedjarati, C. H. Baker, S. Apte, S. Huang, J. K. Wolf, J. J. Killion, and I. J. Fidler
Synergistic Therapy of Human Ovarian Carcinoma Implanted Orthotopically in Nude Mice by Optimal Biological Dose of Pegylated Interferon {alpha} Combined with Paclitaxel
Clin. Cancer Res., July 1, 2002; 8(7): 2413 - 2422.
[Abstract] [Full Text] [PDF]

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A. B. Motoyama, N. E. Hynes, and H. A. Lane
The Efficacy of ErbB Receptor-targeted Anticancer Therapeutics Is Influenced by the Availability of Epidermal Growth Factor-related Peptides
Cancer Res., June 1, 2002; 62(11): 3151 - 3158.
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 Molecular Cancer TherapeuticsHome page
D. Fan, S. Yano, H. Shinohara, C. Solorzano, M. Van Arsdall, C. D. Bucana, S. Pathak, E. Kruzel, R. S. Herbst, A. Onn, et al.
Targeted Therapy against Human Lung Cancer in Nude Mice by High-Affinity Recombinant Antimesothelin Single-Chain Fv Immunotoxin
Mol. Cancer Ther., June 1, 2002; 1(8): 595 - 600.
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 Cancer Res.Home page
A. Hirata, S.-i. Ogawa, T. Kometani, T. Kuwano, S. Naito, M. Kuwano, and M. Ono
ZD1839 (Iressa) Induces Antiangiogenic Effects through Inhibition of Epidermal Growth Factor Receptor Tyrosine Kinase
Cancer Res., May 1, 2002; 62(9): 2554 - 2560.
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 Molecular Cancer TherapeuticsHome page
S.-M. Huang, J. Li, and P. M. Harari
Molecular Inhibition of Angiogenesis and Metastatic Potential in Human Squamous Cell Carcinomas after Epidermal Growth Factor Receptor Blockade
Mol. Cancer Ther., May 1, 2002; 1(7): 507 - 514.
[Abstract] [Full Text] [PDF]

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 Cancer Res.Home page
C. H. Baker, C. C. Solorzano, and I. J. Fidler
Blockade of Vascular Endothelial Growth Factor Receptor and Epidermal Growth Factor Receptor Signaling for Therapy of Metastatic Human Pancreatic Cancer
Cancer Res., April 1, 2002; 62(7): 1996 - 2003.
[Abstract] [Full Text] [PDF]

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J. Albanell, F. Rojo, S. Averbuch, A. Feyereislova, J. M. Mascaro, R. Herbst, P. LoRusso, D. Rischin, S. Sauleda, J. Gee, et al.
Pharmacodynamic Studies of the Epidermal Growth Factor Receptor Inhibitor ZD1839 in Skin From Cancer Patients: Histopathologic and Molecular Consequences of Receptor Inhibition
J. Clin. Oncol., January 1, 2002; 20(1): 110 - 124.
[Abstract] [Full Text] [PDF]

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 Cancer Res.Home page
D. Tomioka, N. Maehara, K. Kuba, K. Mizumoto, M. Tanaka, K. Matsumoto, and T. Nakamura
Inhibition of Growth, Invasion, and Metastasis of Human Pancreatic Carcinoma Cells by NK4 in an Orthotopic Mouse Model
Cancer Res., October 1, 2001; 61(20): 7518 - 7524.
[Abstract] [Full Text] [PDF]

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 Clin. Cancer Res.Home page
F. Ciardiello and G. Tortora
A Novel Approach in the Treatment of Cancer: Targeting the Epidermal Growth Factor Receptor
Clin. Cancer Res., October 1, 2001; 7(10): 2958 - 2970.
[Abstract] [Full Text] [PDF]

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C. L. Arteaga
The Epidermal Growth Factor Receptor: From Mutant Oncogene in Nonhuman Cancers to Therapeutic Target in Human Neoplasia
J. Clin. Oncol., September 15, 2001; 19(90001): 32s - 40.
[Abstract] [Full Text] [PDF]

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 Cancer Res.Home page
N. Akakura, M. Kobayashi, I. Horiuchi, A. Suzuki, J. Wang, J. Chen, H. Niizeki, K.-i. Kawamura, M. Hosokawa, and M. Asaka
Constitutive Expression of Hypoxia-inducible Factor-1{alpha} Renders Pancreatic Cancer Cells Resistant to Apoptosis Induced by Hypoxia and Nutrient Deprivation
Cancer Res., September 1, 2001; 61(17): 6548 - 6554.
[Abstract] [Full Text] [PDF]

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 Clin. Cancer Res.Home page
C. C. Solorzano, C. H. Baker, R. Tsan, P. Traxler, P. Cohen, E. Buchdunger, J. J. Killion, and I. J. Fidler
Optimization for the Blockade of Epidermal Growth Factor Receptor Signaling for Therapy of Human Pancreatic Carcinoma
Clin. Cancer Res., August 1, 2001; 7(8): 2563 - 2572.
[Abstract] [Full Text] [PDF]

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A. Viloria-Petit, T. Crombet, S. Jothy, D. Hicklin, P. Bohlen, J. M. Schlaeppi, J. Rak, and R. S. Kerbel
Acquired Resistance to the Antitumor Effect of Epidermal Growth Factor Receptor-blocking Antibodies in Vivo: A Role for Altered Tumor Angiogenesis
Cancer Res., July 1, 2001; 61(13): 5090 - 5101.
[Abstract] [Full Text] [PDF]

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 Clin. Cancer Res.Home page
J. S. Wolf, Z. Chen, G. Dong, J. B. Sunwoo, C. C. Bancroft, D. E. Capo, N. T. Yeh, N. Mukaida, and C. V. Waes
IL (Interleukin)-1{{alpha}} Promotes Nuclear Factor-{{kappa}}B and AP-1-induced IL-8 Expression, Cell Survival, and Proliferation in Head and Neck Squamous Cell Carcinomas
Clin. Cancer Res., June 1, 2001; 7(6): 1812 - 1820.
[Abstract] [Full Text] [PDF]

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 Clin. Cancer Res.Home page
F. Ciardiello, R. Caputo, R. Bianco, V. Damiano, G. Fontanini, S. Cuccato, S. De Placido, A. R. Bianco, and G. Tortora
Inhibition of Growth Factor Production and Angiogenesis in Human Cancer Cells by ZD1839 (Iressa), a Selective Epidermal Growth Factor Receptor Tyrosine Kinase Inhibitor
Clin. Cancer Res., May 1, 2001; 7(5): 1459 - 1465.
[Abstract] [Full Text]

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 Circ. Res.Home page
S. Dimmeler and A. M. Zeiher
Endothelial Cell Apoptosis in Angiogenesis and Vessel Regression
Circ. Res., September 15, 2000; 87(6): 434 - 439.
[Abstract] [Full Text] [PDF]


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