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Science 18 June 1999:
Vol. 284. no. 5422, pp. 1994 - 1998
DOI: 10.1126/science.284.5422.1994
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Reports

Vessel Cooption, Regression, and Growth in Tumors Mediated by Angiopoietins and VEGF

J. Holash, 1 P. C. Maisonpierre, 1 D. Compton, 1 P. Boland, 1 C. R. Alexander, 1 D. Zagzag, 2 G. D. Yancopoulos, 1* S. J. Wiegand 1*

In contrast with the prevailing view that most tumors and metastases begin as avascular masses, evidence is presented here that a subset of tumors instead initially grows by coopting existing host vessels. This coopted host vasculature does not immediately undergo angiogenesis to support the tumor but instead regresses, leading to a secondarily avascular tumor and massive tumor cell loss. Ultimately, however, the remaining tumor is rescued by robust angiogenesis at the tumor margin. The expression patterns of the angiogenic antagonist angiopoietin-2 and of pro-angiogenic vascular endothelial growth factor (VEGF) suggest that these proteins may be critical regulators of this balance between vascular regression and growth.

1 Regeneron Pharmaceuticals, 777 Old Saw Mill River Road, Tarrytown, NY 10591, USA.
2 Microvascular and Molecular Neuro-Oncology Laboratory, Department of Pathology, Kaplan Cancer Center, New York University Medical Center, New York, NY 10016, USA.
*   To whom correspondence should be addressed. E-mail: gdy{at}regpha.com (G.D.Y.); stan.wiegand{at}regpha.com (S.J.W.)

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Hypoxia and the hypoxia-inducible-factor pathway in glioma growth and angiogenesis.
B. Kaur, F. W. Khwaja, E. A. Severson, S. L. Matheny, D. J. Brat, and E. G. Van Meir (2005)
Neuro-oncol 7, 134-153
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Survival After Pathological Stage IA Nonsmall Cell Lung Cancer: Tumor Size Matters.
O. Birim, A. P. Kappetein, J. J.M. Takkenberg, R. J. van Klaveren, and A. J.J.C. Bogers (2005)
Ann. Thorac. Surg. 79, 1137-1141
   Abstract »    Full Text »    PDF »
Angiogenesis: a curse or cure?.
K Gupta and J Zhang (2005)
Postgrad. Med. J. 81, 236-242
   Abstract »    Full Text »    PDF »
Angiopoietin-1 Promotes Cardiac and Skeletal Myocyte Survival Through Integrins.
S. M. Dallabrida, N. Ismail, J. R. Oberle, B. E. Himes, and M. A. Rupnick (2005)
Circ. Res. 96, e8-e24
   Abstract »    Full Text »    PDF »
Analysis of Concerted Expression of Angiogenic Growth Factors in Acute Myeloid Leukemia: Expression of Angiopoietin-2 Represents an Independent Prognostic Factor for Overall Survival.
S. Loges, G. Heil, M. Bruweleit, V. Schoder, M. Butzal, U. Fischer, U. M. Gehling, G. Schuch, D. K. Hossfeld, and W. Fiedler (2005)
J. Clin. Oncol. 23, 1109-1117
   Abstract »    Full Text »    PDF »
PTEN and Hypoxia Regulate Tissue Factor Expression and Plasma Coagulation by Glioblastoma.
Y. Rong, D. E. Post, R. O. Pieper, D. L. Durden, E. G. Van Meir, and D. J. Brat (2005)
Cancer Res. 65, 1406-1413
   Abstract »    Full Text »    PDF »
The Tie-2 ligand Angiopoietin-2 destabilizes quiescent endothelium through an internal autocrine loop mechanism.
M. Scharpfenecker, U. Fiedler, Y. Reiss, and H. G. Augustin (2005)
J. Cell Sci. 118, 771-780
   Abstract »    Full Text »    PDF »
The pathophysiologic role of VEGF in hematologic malignancies: therapeutic implications.
K. Podar and K. C. Anderson (2005)
Blood 105, 1383-1395
   Abstract »    Full Text »    PDF »
Vascularization of Melanoma by Mobilization and Remodeling of Preexisting Latent Vessels to Patency.
W. Lu and A. J. Schroit (2005)
Cancer Res. 65, 913-918
   Abstract »    Full Text »    PDF »
Accessing key steps of human tumor progression in vivo by using an avian embryo model.
M. Hagedorn, S. Javerzat, D. Gilges, A. Meyre, B. de Lafarge, A. Eichmann, and A. Bikfalvi (2005)
PNAS 102, 1643-1648
   Abstract »    Full Text »    PDF »
VEGF Trap as a Novel Antiangiogenic Treatment Currently in Clinical Trials for Cancer and Eye Diseases, and VelociGene(R)- based Discovery of the Next Generation of Angiogenesis Targets.
J.S. RUDGE, G. THURSTON, S. DAVIS, N. PAPADOPOULOS, N. GALE, S.J. WIEGAND, and G.D. YANCOPOULOS (2005)
Cold Spring Harb Symp Quant Biol 70, 411-418
   Abstract »    PDF »
Plasma vascular endothelial growth factor, angiopoietin-2, and soluble angiopoietin receptor tie-2 in diabetic retinopathy: effects of laser photocoagulation and angiotensin receptor blockade.
P L Lip, S Chatterjee, G J Caine, M Hope-Ross, J Gibson, A D Blann, and G Y H Lip (2004)
Br J Ophthalmol 88, 1543-1546
   Abstract »    Full Text »    PDF »
Tumor-Associated Endothelial Cells with Cytogenetic Abnormalities.
K. Hida, Y. Hida, D. N. Amin, A. F. Flint, D. Panigrahy, C. C. Morton, and M. Klagsbrun (2004)
Cancer Res. 64, 8249-8255
   Abstract »    Full Text »    PDF »
Haploinsufficiency of delta-like 4 ligand results in embryonic lethality due to major defects in arterial and vascular development.
N. W. Gale, M. G. Dominguez, I. Noguera, L. Pan, V. Hughes, D. M. Valenzuela, A. J. Murphy, N. C. Adams, H. C. Lin, J. Holash, et al. (2004)
PNAS 101, 15949-15954
   Abstract »    Full Text »    PDF »
Characterization of a First-Pass Gradient-Echo Spin-Echo Method to Predict Brain Tumor Grade and Angiogenesis.
K. M. Schmainda, S. D. Rand, A. M. Joseph, R. Lund, B. D. Ward, A. P. Pathak, J. L. Ulmer, M. A. Baddrudoja, and H. G. J. Krouwer (2004)
AJNR Am. J. Neuroradiol. 25, 1524-1532
   Abstract »    Full Text »    PDF »
Expression of Angiopoietin-2 in Endothelial Cells Is Controlled by Positive and Negative Regulatory Promoter Elements.
A. Hegen, S. Koidl, K. Weindel, D. Marme, H. G. Augustin, and U. Fiedler (2004)
Arterioscler Thromb Vasc Biol 24, 1803-1809
   Abstract »    Full Text »    PDF »
Expression of angiopoietins in renal epithelial and clear cell carcinoma cells: regulation by hypoxia and participation in angiogenesis.
M. Yamakawa, L. X. Liu, A. J. Belanger, T. Date, T. Kuriyama, M. A. Goldberg, S. H. Cheng, R. J. Gregory, and C. Jiang (2004)
Am J Physiol Renal Physiol 287, F649-F657
   Abstract »    Full Text »    PDF »
Angiopoietin-3 Is Tethered on the Cell Surface via Heparan Sulfate Proteoglycans.
Y. Xu, Y.-j. Liu, and Q. Yu (2004)
J. Biol. Chem. 279, 41179-41188
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Genetically tagging endothelial cells in vivo: bone marrow-derived cells do not contribute to tumor endothelium.
J. R. Gothert, S. E. Gustin, J. A. M. van Eekelen, U. Schmidt, M. A. Hall, S. M. Jane, A. R. Green, B. Gottgens, D. J. Izon, and C. G. Begley (2004)
Blood 104, 1769-1777
   Abstract »    Full Text »    PDF »
Cannabinoids Inhibit the Vascular Endothelial Growth Factor Pathway in Gliomas.
C. Blazquez, L. Gonzalez-Feria, L. Alvarez, A. Haro, M. L. Casanova, and M. Guzman (2004)
Cancer Res. 64, 5617-5623
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Structural and functional adaptation to hypoxia in the rat brain.
J. C. LaManna, J. C. Chavez, and P. Pichiule (2004)
J. Exp. Biol. 207, 3163-3169
   Abstract »    Full Text »    PDF »
Vascular Gene Expression in Nonneoplastic and Malignant Brain.
S. L. Madden, B. P. Cook, M. Nacht, W. D. Weber, M. R. Callahan, Y. Jiang, M. R. Dufault, X. Zhang, W. Zhang, J. Walter-Yohrling, et al. (2004)
Am. J. Pathol. 165, 601-608
   Abstract »    Full Text »    PDF »
Vascular Endothelial Growth Factor as a Target for Anticancer Therapy.
N. Ferrara (2004)
Oncologist 9, 2-10
   Abstract »    Full Text »    PDF »


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