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[Cancer Research 59, 3374-3378, July 1, 1999]
© 1999 American Association for Cancer Research
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[Cancer Research 59, 3374-3378, July 15, 1999]
© 1999 American Association for Cancer Research

Advances in Brief

Blockade of the Vascular Endothelial Growth Factor Stress Response Increases the Antitumor Effects of Ionizing Radiation1

David H. Gorski, Michael A. Beckett, Nora T. Jaskowiak, Douglas P. Calvin, Helena J. Mauceri, Rabih M. Salloum, Saraswathy Seetharam, Ann Koons, Danielle M. Hari, Donald W. Kufe and Ralph R. Weichselbaum2

Departments of Radiation and Cellular Oncology [D. H. G., M. A. B., D. P. C., H. J. M., S. S., A. K., D. M. H., R. R. W.] and Surgery [N. T. J., R. M. S.], University of Chicago, Chicago, Illinois 60637, and Dana Farber Cancer Institute, Harvard Medical School, Boston, Massachusetts 02115 [D. W. K.]

The family of vascular endothelial growth factor (VEGF) proteins include potent and specific mitogens for vascular endothelial cells that function in the regulation of angiogenesis. Inhibition of VEGF-induced angiogenesis, either by neutralizing antibodies or a dominant-negative soluble receptor, blocks the growth of primary and metastatic experimental tumors. Here we report that VEGF expression is induced in Lewis lung carcinomas (LLCs) both in vitro and in vivo after exposure to ionizing radiation (IR) and in human tumor cell lines (Seg-1 esophageal adenocarcinoma, SQ20B squamous cell carcinoma, T98 and U87 glioblastomas, and U1 melanoma) in vitro. The biological significance of IR-induced VEGF production is supported by our finding that treatment of tumor-bearing mice (LLC, Seg-1, SQ20B, and U87) with a neutralizing antibody to VEGF-165 before irradiation is associated with a greater than additive antitumor effect. In vitro, the addition of VEGF decreases IR-induced killing of human umbilical vein endothelial cells, and the anti-VEGF treatment potentiates IR-induced lethality of human umbilical vein endothelial cells. Neither recombinant VEGF protein nor neutralizing antibody to VEGF affects the radiosensitivity of tumor cells. These findings support a model in which induction of VEGF by IR contributes to the protection of tumor blood vessels from radiation-mediated cytotoxicity and thereby to tumor radioresistance.




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Synchronous Coexpression of Epidermal Growth Factor Receptor and Cyclooxygenase-2 in Carcinomas of the Uterine Cervix: A Potential Predictor of Poor Survival
Clin. Cancer Res., February 15, 2004; 10(4): 1366 - 1374.
[Abstract] [Full Text] [PDF]

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L. W. Chan, M. A. Moses, E. Goley, M. Sproull, T. Muanza, C. N. Coleman, W. D. Figg, P. S. Albert, C. Menard, and K. Camphausen
Urinary VEGF and MMP Levels As Predictive Markers of 1-Year Progression-Free Survival in Cancer Patients Treated With Radiation Therapy: A Longitudinal Study of Protein Kinetics Throughout Tumor Progression and Therapy
J. Clin. Oncol., February 1, 2004; 22(3): 499 - 506.
[Abstract] [Full Text] [PDF]

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 ScienceHome page
R. Kolesnick and Z. Fuks
Response to Comments on "Tumor Response to Radiotherapy Regulated by Endothelial Cell Apoptosis"
Science, December 12, 2003; 302(5652): 1894e - 1894e.
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 JNCI J Natl Cancer InstHome page
H. Choy and L. Milas
Enhancing Radiotherapy With Cyclooxygenase-2 Enzyme Inhibitors: A Rational Advance?
J Natl Cancer Inst, October 1, 2003; 95(19): 1440 - 1452.
[Abstract] [Full Text] [PDF]

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F. Denis, S. Colas, L. Chami, P. Louisot, O. le Floch, F. Tranquart, and P. Bougnoux
Changes in Tumor Vascularization after Irradiation, Anthracyclin, or Antiangiogenic Treatment in Nitrosomethyl Ureas-Induced Rat Mammary Tumors
Clin. Cancer Res., October 1, 2003; 9(12): 4546 - 4552.
[Abstract] [Full Text] [PDF]

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 Molecular Cancer TherapeuticsHome page
D. C. Lev, M. Ruiz, L. Mills, E. C. McGary, J. E. Price, and M. Bar-Eli
Dacarbazine Causes Transcriptional Up-Regulation of Interleukin 8 and Vascular Endothelial Growth Factor in Melanoma Cells: A Possible Escape Mechanism from Chemotherapy
Mol. Cancer Ther., August 1, 2003; 2(8): 753 - 763.
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A. J. Schueneman, E. Himmelfarb, L. Geng, J. Tan, E. Donnelly, D. Mendel, G. McMahon, and D. E. Hallahan
SU11248 Maintenance Therapy Prevents Tumor Regrowth after Fractionated Irradiation of Murine Tumor Models
Cancer Res., July 15, 2003; 63(14): 4009 - 4016.
[Abstract] [Full Text] [PDF]

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 Cancer Res.Home page
E. K. Rofstad, K. Henriksen, K. Galappathi, and B. Mathiesen
Antiangiogenic Treatment with Thrombospondin-1 Enhances Primary Tumor Radiation Response and Prevents Growth of Dormant Pulmonary Micrometastases after Curative Radiation Therapy in Human Melanoma Xenografts
Cancer Res., July 15, 2003; 63(14): 4055 - 4061.
[Abstract] [Full Text] [PDF]

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B. B.Y. Ma, R. G. Bristow, J. Kim, and L. L. Siu
Combined-Modality Treatment of Solid Tumors Using Radiotherapy and Molecular Targeted Agents
J. Clin. Oncol., July 15, 2003; 21(14): 2760 - 2776.
[Abstract] [Full Text] [PDF]

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 Cancer Res.Home page
A. Abdollahi, K. E. Lipson, X. Han, R. Krempien, T. Trinh, K. J. Weber, P. Hahnfeldt, L. Hlatky, J. Debus, A. R. Howlett, et al.
SU5416 and SU6668 Attenuate the Angiogenic Effects of Radiation-induced Tumor Cell Growth Factor Production and Amplify the Direct Anti-endothelial Action of Radiation in Vitro
Cancer Res., July 1, 2003; 63(13): 3755 - 3763.
[Abstract] [Full Text] [PDF]

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 Arch Otolaryngol Head Neck SurgHome page
C. Cox, S. D. Merajver, S. Yoo, R. D. Dick, G. J. Brewer, J. S.-J. Lee, and T. N. Teknos
Inhibition of the Growth of Squamous Cell Carcinoma by Tetrathiomolybdate-Induced Copper Suppression in a Murine Model
Arch Otolaryngol Head Neck Surg, July 1, 2003; 129(7): 781 - 785.
[Abstract] [Full Text] [PDF]

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 Clin. Cancer Res.Home page
P. Wachsberger, R. Burd, and A. P. Dicker
Tumor Response to Ionizing Radiation Combined with Antiangiogenesis or Vascular Targeting Agents: Exploring Mechanisms of Interaction
Clin. Cancer Res., June 1, 2003; 9(6): 1957 - 1971.
[Abstract] [Full Text] [PDF]

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C. Roca, L. Primo, D. Valdembri, A. Cividalli, P. Declerck, P. Carmeliet, P. Gabriele, and F. Bussolino
Hyperthermia Inhibits Angiogenesis by a Plasminogen Activator Inhibitor 1-dependent Mechanism
Cancer Res., April 1, 2003; 63(7): 1500 - 1507.
[Abstract] [Full Text] [PDF]

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P. Sonveaux, A. Brouet, X. Havaux, V. Gregoire, C. Dessy, J.-L. Balligand, and O. Feron
Irradiation-induced Angiogenesis through the Up-Regulation of the Nitric Oxide Pathway: Implications for Tumor Radiotherapy
Cancer Res., March 1, 2003; 63(5): 1012 - 1019.
[Abstract] [Full Text] [PDF]

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D. H. Gorski, H. J. Mauceri, R. M. Salloum, A. Halpern, S. Seetharam, and R. R. Weichselbaum
Prolonged Treatment with Angiostatin Reduces Metastatic Burden during Radiation Therapy
Cancer Res., January 15, 2003; 63(2): 308 - 311.
[Abstract] [Full Text] [PDF]

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 Neuro Oncol DukeHome page
S. Takano, K. Tsuboi, A. Matsumura, and T. Nose
Anti-vascular endothelial growth factor antibody and nimustine as combined therapy: Effects on tumor growth and angiogenesis in human glioblastoma xenografts
Neuro-oncol, January 1, 2003; 5(1): 1 - 7.
[Abstract] [PDF]

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 Cancer Res.Home page
J. S. Eshleman, B. L. Carlson, A. C. Mladek, B. D. Kastner, K. L. Shide, and J. N. Sarkaria
Inhibition of the Mammalian Target of Rapamycin Sensitizes U87 Xenografts to Fractionated Radiation Therapy
Cancer Res., December 15, 2002; 62(24): 7291 - 7297.
[Abstract] [Full Text] [PDF]

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H. F. Dvorak
Vascular Permeability Factor/Vascular Endothelial Growth Factor: A Critical Cytokine in Tumor Angiogenesis and a Potential Target for Diagnosis and Therapy
J. Clin. Oncol., November 1, 2002; 20(21): 4368 - 4380.
[Abstract] [Full Text] [PDF]

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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.
[Abstract] [Full Text] [PDF]

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 Cancer Res.Home page
E. Edwards, L. Geng, J. Tan, H. Onishko, E. Donnelly, and D. E. Hallahan
Phosphatidylinositol 3-Kinase/Akt Signaling in the Response of Vascular Endothelium to Ionizing Radiation
Cancer Res., August 15, 2002; 62(16): 4671 - 4677.
[Abstract] [Full Text] [PDF]

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P. A. Burke, S. J. DeNardo, L. A. Miers, K. R. Lamborn, S. Matzku, and G. L. DeNardo
Cilengitide Targeting of {alpha}v{beta}3 Integrin Receptor Synergizes with Radioimmunotherapy to Increase Efficacy and Apoptosis in Breast Cancer Xenografts
Cancer Res., August 1, 2002; 62(15): 4263 - 4272.
[Abstract] [Full Text] [PDF]

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 JCBHome page
J. E. Morgan, J. G. Gross, C. N. Pagel, J. R. Beauchamp, A. Fassati, A. J. Thrasher, J. P. Di Santo, I. B. Fisher, X. Shiwen, D. J. Abraham, et al.
Myogenic cell proliferation and generation of a reversible tumorigenic phenotype are triggered by preirradiation of the recipient site
J. Cell Biol., May 13, 2002; 157(4): 693 - 702.
[Abstract] [Full Text] [PDF]

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 Cancer Res.Home page
R. Ganss, E. Ryschich, E. Klar, B. Arnold, and G. J. Hammerling
Combination of T-Cell Therapy and Trigger of Inflammation Induces Remodeling of the Vasculature and Tumor Eradication
Cancer Res., March 1, 2002; 62(5): 1462 - 1470.
[Abstract] [Full Text] [PDF]

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R. J. Griffin, B. W. Williams, R. Wild, J. M. Cherrington, H. Park, and C. W. Song
Simultaneous Inhibition of the Receptor Kinase Activity of Vascular Endothelial, Fibroblast, and Platelet-derived Growth Factors Suppresses Tumor Growth and Enhances Tumor Radiation Response
Cancer Res., March 1, 2002; 62(6): 1702 - 1706.
[Abstract] [Full Text] [PDF]

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S. Franco, I. Segura, H. H. Riese, and M. A. Blasco
Decreased B16F10 Melanoma Growth and Impaired Vascularization in Telomerase-deficient Mice with Critically Short Telomeres
Cancer Res., January 1, 2002; 62(2): 552 - 559.
[Abstract] [Full Text] [PDF]

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M. I. Koukourakis, A. Giatromanolaki, E. Sivridis, K. Simopoulos, J. Pastorek, C. C. Wykoff, K. C. Gatter, and A. L. Harris
Hypoxia-regulated Carbonic Anhydrase-9 (CA9) Relates to Poor Vascularization and Resistance of Squamous Cell Head and Neck Cancer to Chemoradiotherapy
Clin. Cancer Res., November 1, 2001; 7(11): 3399 - 3403.
[Abstract] [Full Text] [PDF]

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M. Milosevic, A. Fyles, D. Hedley, M. Pintilie, W. Levin, L. Manchul, and R. Hill
Interstitial Fluid Pressure Predicts Survival in Patients with Cervix Cancer Independent of Clinical Prognostic Factors and Tumor Oxygen Measurements
Cancer Res., September 1, 2001; 61(17): 6400 - 6405.
[Abstract] [Full Text] [PDF]

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Y. Chen, T. DeWeese, J. Dilley, Y. Zhang, Y. Li, N. Ramesh, J. Lee, R. Pennathur-Das, J. Radzyminski, J. Wypych, et al.
CV706, a Prostate Cancer-specific Adenovirus Variant, in Combination with Radiotherapy Produces Synergistic Antitumor Efficacy without Increasing Toxicity
Cancer Res., July 1, 2001; 61(14): 5453 - 5460.
[Abstract] [Full Text] [PDF]

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G. Kong, R. D. Braun, and M. W. Dewhirst
Characterization of the Effect of Hyperthermia on Nanoparticle Extravasation from Tumor Vasculature
Cancer Res., April 1, 2001; 61(7): 3027 - 3032.
[Abstract] [Full Text]

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 Cancer Res.Home page
K. Camphausen, M. A. Moses, W.-D. Beecken, M. K. Khan, J. Folkman, and M. S. O’Reilly
Radiation Therapy to a Primary Tumor Accelerates Metastatic Growth in Mice
Cancer Res., March 1, 2001; 61(5): 2207 - 2211.
[Abstract] [Full Text]

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 Cancer Res.Home page
L. Geng, E. Donnelly, G. McMahon, P. C. Lin, E. Sierra-Rivera, H. Oshinka, and D. E. Hallahan
Inhibition of Vascular Endothelial Growth Factor Receptor Signaling Leads to Reversal of Tumor Resistance to Radiotherapy
Cancer Res., March 1, 2001; 61(6): 2413 - 2419.
[Abstract] [Full Text]

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 Cancer Res.Home page
S. V. Kozin, Y. Boucher, D. J. Hicklin, P. Bohlen, R. K. Jain, and H. D. Suit
Vascular Endothelial Growth Factor Receptor-2-blocking Antibody Potentiates Radiation-induced Long-Term Control of Human Tumor Xenografts
Cancer Res., January 1, 2001; 61(1): 39 - 44.
[Abstract] [Full Text]

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C.-G. Lee, M. Heijn, E. di Tomaso, G. Griffon-Etienne, M. Ancukiewicz, C. Koike, K. R. Park, N. Ferrara, R. K. Jain, H. D. Suit, et al.
Anti-Vascular Endothelial Growth Factor Treatment Augments Tumor Radiation Response under Normoxic or Hypoxic Conditions
Cancer Res., October 1, 2000; 60(19): 5565 - 5570.
[Abstract] [Full Text]

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A. Ferrario, K. F. von Tiehl, N. Rucker, M. A. Schwarz, P. S. Gill, and C. J. Gomer
Antiangiogenic Treatment Enhances Photodynamic Therapy Responsiveness in a Mouse Mammary Carcinoma
Cancer Res., August 1, 2000; 60(15): 4066 - 4069.
[Abstract] [Full Text]

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N. Hansen-Algenstaedt, B. R. Stoll, T. P. Padera, D. E. J. G. J. Dolmans, D. J. Hicklin, D. Fukumura, and R. K. Jain
Tumor Oxygenation in Hormone-Dependent Tumors During Vascular Endothelial Growth Factor Receptor-2 Blockade, Hormone Ablation, and Chemotherapy
Cancer Res., August 1, 2000; 60(16): 4556 - 4560.
[Abstract] [Full Text]

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 Clin. Cancer Res.Home page
C. Li, S. Ke, Q.-P. Wu, W. Tansey, N. Hunter, L. M. Buchmiller, L. Milas, C. Charnsangavej, and S. Wallace
Tumor Irradiation Enhances the Tumor-specific Distribution of Poly(L-glutamic acid)-conjugated Paclitaxel and Its Antitumor Efficacy
Clin. Cancer Res., July 1, 2000; 6(7): 2829 - 2834.
[Abstract] [Full Text]


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