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Science 16 May 2003:
Vol. 300. no. 5622, pp. 1155 - 1159
DOI: 10.1126/science.1082504
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Reports

Tumor Response to Radiotherapy Regulated by Endothelial Cell Apoptosis

Monica Garcia-Barros,1 Francois Paris,1 Carlos Cordon-Cardo,2 David Lyden,3 Shahin Rafii,5 Adriana Haimovitz-Friedman,4 Zvi Fuks,4* Richard Kolesnick1*{dagger}

About 50% of cancer patients receive radiation therapy. Here we investigated the hypothesis that tumor response to radiation is determined not only by tumor cell phenotype but also by microvascular sensitivity. MCA/129 fibrosarcomas and B16F1 melanomas grown in apoptosis-resistant acid sphingomyelinase (asmase)–deficient or Bax-deficient mice displayed markedly reduced baseline microvascular endothelial apoptosis and grew 200 to 400% faster than tumors on wild-type microvasculature. Thus, endothelial apoptosis is a homeostatic factor regulating angiogenesis-dependent tumor growth. Moreover, these tumors exhibited reduced endothelial apoptosis upon irradiation and, unlike tumors in wild-type mice, they were resistant to single-dose radiation up to 20 grays (Gy). These studies indicate that microvascular damage regulates tumor cell response to radiation at the clinically relevant dose range.

1 Laboratory of Signal Transduction, Memorial Sloan-Kettering Cancer Center, 1275 York Avenue, New York, NY 10021, USA.
2 Department of Pathology, Memorial Sloan-Kettering Cancer Center, 1275 York Avenue, New York, NY 10021, USA.
3 Department of Pediatrics, Memorial Sloan-Kettering Cancer Center, 1275 York Avenue, New York, NY 10021, USA.
4 Department of Radiation Oncology, Memorial Sloan-Kettering Cancer Center, 1275 York Avenue, New York, NY 10021, USA.
5 Department of Hematology-Oncology, Cornell University Medical College, New York, NY 10021, USA.



* These authors contributed equally to this work.

{dagger} To whom correspondence should be addressed. E-mail: r-kolesnick{at}ski.mskcc.org

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Cancer Res. 64, 5398-5406
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A Specific Antagonist of the p110{delta} Catalytic Component of Phosphatidylinositol 3'-Kinase, IC486068, Enhances Radiation-Induced Tumor Vascular Destruction.
L. Geng, J. Tan, E. Himmelfarb, A. Schueneman, K. Niermann, A. Fu, K. Cuneo, E. A. Kesicki, J. Treiberg, J. S. Hayflick, et al. (2004)
Cancer Res. 64, 4893-4899
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TNFerade Biologic, an Adenovector With a Radiation-Inducible Promoter, Carrying the Human Tumor Necrosis Factor Alpha Gene: A Phase I Study in Patients With Solid Tumors.
N. Senzer, S. Mani, A. Rosemurgy, J. Nemunaitis, C. Cunningham, C. Guha, N. Bayol, M. Gillen, K. Chu, C. Rasmussen, et al. (2004)
J. Clin. Oncol. 22, 592-601
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STAT1 is overexpressed in tumors selected for radioresistance and confers protection from radiation in transduced sensitive cells.
N. N. Khodarev, M. Beckett, E. Labay, T. Darga, B. Roizman, and R. R. Weichselbaum (2004)
PNAS 101, 1714-1719
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Synergy between Celecoxib and Radiotherapy Results from Inhibition of Cyclooxygenase-2-Derived Prostaglandin E2, a Survival Factor for Tumor and Associated Vasculature.
T. W. Davis, J. M. O'Neal, M. D. Pagel, B. S. Zweifel, P. P. Mehta, D. M. Heuvelman, and J. L. Masferrer (2004)
Cancer Res. 64, 279-285
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Mdm2 in the Response to Radiation.
M. E. Perry (2004)
Mol. Cancer Res. 2, 9-19
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Comment on "Tumor Response to Radiotherapy Regulated by Endothelial Cell Apoptosis" (I).
H. D. Suit and H. Willers (2003)
Science 302, 1894c
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Comment on "Tumor Response to Radiotherapy Regulated by Endothelial Cell Apoptosis" (II).
M. Brown, R. Bristow, P. Glazer, R. Hill, W. McBride, G. McKenna, and R. Muschel (2003)
Science 302, 1894d
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Response to Comments on "Tumor Response to Radiotherapy Regulated by Endothelial Cell Apoptosis".
R. Kolesnick and Z. Fuks (2003)
Science 302, 1894e
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Overcoming the hypoxic barrier to radiation therapy with anaerobic bacteria.
C. Bettegowda, L. H. Dang, R. Abrams, D. L. Huso, L. Dillehay, I. Cheong, N. Agrawal, S. Borzillary, J. M. McCaffery, E. L. Watson, et al. (2003)
PNAS 100, 15083-15088
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Diagnosing Lynch syndrome: is the answer in the mouth?.
H K Roy and H T Lynch (2003)
Gut 52, 1665-1667
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The Cyclin-Dependent Kinase Inhibitor Flavopiridol Potentiates {gamma}-Irradiation-Induced Apoptosis in Colon and Gastric Cancer Cells.
C. Jung, M. Motwani, J. Kortmansky, F. M. Sirotnak, Y. She, M. Gonen, A. Haimovitz-Friedman, and G. K. Schwartz (2003)
Clin. Cancer Res. 9, 6052-6061
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Translating angiogenesis research into the clinic: the challenges ahead.
H G Augustin (2003)
Br. J. Radiol. 76, S3-S10
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Microvascular Function Regulates Intestinal Crypt Response to Radiation.
J. G. Maj, F. Paris, A. Haimovitz-Friedman, E. Venkatraman, R. Kolesnick, and Z. Fuks (2003)
Cancer Res. 63, 4338-4341
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