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Science 4 July 1997:
Vol. 277. no. 5322, pp. 55 - 60
DOI: 10.1126/science.277.5322.55
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Research Articles

Angiopoietin-2, a Natural Antagonist for Tie2 That Disrupts in vivo Angiogenesis

Peter C. Maisonpierre, * Chitra Suri, * Pamela F. Jones, *dagger Sona Bartunkova, * Stanley J. Wiegand, Czeslaw Radziejewski, Debra Compton, Joyce McClain, Thomas H. Aldrich, Nick Papadopoulos, Thomas J. Daly, Samuel Davis, * Thomas N. Sato, * George D. Yancopoulos *ddagger

Angiogenesis is thought to depend on a precise balance of positive and negative regulation. Angiopoietin-1 (Ang1) is an angiogenic factor that signals through the endothelial cell-specific Tie2 receptor tyrosine kinase. Like vascular endothelial growth factor, Ang1 is essential for normal vascular development in the mouse. An Ang1 relative, termed angiopoietin-2 (Ang2), was identified by homology screening and shown to be a naturally occurring antagonist for Ang1 and Tie2. Transgenic overexpression of Ang2 disrupts blood vessel formation in the mouse embryo. In adult mice and humans, Ang2 is expressed only at sites of vascular remodeling. Natural antagonists for vertebrate receptor tyrosine kinases are atypical; thus, the discovery of a negative regulator acting on Tie2 emphasizes the need for exquisite regulation of this angiogenic receptor system.

P. C. Maisonpierre, C. Suri, P. F. Jones, S. J. Wiegand, C. Radziejewski, D. Compton, J. McClain, T. H. Aldrich, N. Papadopoulos, T. J. Daly, S. Davis, and G. D. Yancopoulos are at Regeneron Pharmaceuticals Inc., 777 Old Saw Mill River Road, Tarrytown, NY 10591, USA. S. Bartunkova and T. N. Sato are at Beth Israel-Deaconess Medical Center and Harvard Medical School, 330 Brookline Avenue, Boston, MA 02215, USA.
*   These authors contributed equally to this article.

dagger    Present address: Molecular Medicine, St. James University Hospital, Leeds LS9 7TS, UK.

ddagger    To whom correspondence should be addressed. E-mail: gdy{at}regpha.com

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Invest. Ophthalmol. Vis. Sci. 48, 1368-1379
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In Vivo Actions of Angiopoietins on Quiescent and Remodeling Blood and Lymphatic Vessels in Mouse Airways and Skin.
K. Eun Kim, C.-H. Cho, H.-Z. Kim, P. Baluk, D. M. McDonald, and G. Young Koh (2007)
Arterioscler Thromb Vasc Biol 27, 564-570
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Human Epidermal Growth Factor Receptor 2 Regulates Angiopoietin-2 Expression in Breast Cancer via AKT and Mitogen-Activated Protein Kinase Pathways.
G. Niu and W. B. Carter (2007)
Cancer Res. 67, 1487-1493
   Abstract »    Full Text »    PDF »
The Molecular Control of Corpus Luteum Formation, Function, and Regression.
C. Stocco, C. Telleria, and G. Gibori (2007)
Endocr. Rev. 28, 117-149
   Abstract »    Full Text »    PDF »
Expression of the Receptor Tyrosine Kinase Tie2 in Neoplastic Glial Cells Is Associated with Integrin {beta}1-Dependent Adhesion to the Extracellular Matrix.
O.-H. Lee, J. Xu, J. Fueyo, G. N. Fuller, K. D. Aldape, M. M. Alonso, Y. Piao, T.-J. Liu, F. F. Lang, B. N. Bekele, et al. (2006)
Mol. Cancer Res. 4, 915-926
   Abstract »    Full Text »    PDF »
Interaction between Tie receptors modulates angiogenic activity of angiopoietin2 in endothelial progenitor cells.
K. L. Kim, I.-S. Shin, J.-M. Kim, J.-H. Choi, J. Byun, E.-S. Jeon, W. Suh, and D.-K. Kim (2006)
Cardiovasc Res 72, 394-402
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Extracellular Matrix-Bound Angiopoietin-Like 4 Inhibits Endothelial Cell Adhesion, Migration, and Sprouting and Alters Actin Cytoskeleton.
A. Cazes, A. Galaup, C. Chomel, M. Bignon, N. Brechot, S. Le Jan, H. Weber, P. Corvol, L. Muller, S. Germain, et al. (2006)
Circ. Res. 99, 1207-1215
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Pathological but Not Physiological Retinal Neovascularization Is Altered in TNF-Rp55-Receptor-Deficient Mice.
N. Kociok, S. Radetzky, T. U. Krohne, C. Gavranic, and A. M. Joussen (2006)
Invest. Ophthalmol. Vis. Sci. 47, 5057-5065
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Angiopoietin-2 functions as an autocrine protective factor in stressed endothelial cells.
C. Daly, E. Pasnikowski, E. Burova, V. Wong, T. H. Aldrich, J. Griffiths, E. Ioffe, T. J. Daly, J. P. Fandl, N. Papadopoulos, et al. (2006)
PNAS 103, 15491-15496
   Abstract »    Full Text »    PDF »
Review of the Pericyte during Angiogenesis and its Role in Cancer and Diabetic Retinopathy.
A. P. Hall (2006)
Toxicol Pathol 34, 763-775
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Antiangiogenic therapy in human gastrointestinal malignancies..
J Heidemann, D G Binion, W Domschke, and T Kucharzik (2006)
Gut 55, 1497-1511
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Emerging roles of the Angiopoietin-Tie and the ephrin-Eph systems as regulators of cell trafficking.
D. Pfaff, U. Fiedler, and H. G. Augustin (2006)
J. Leukoc. Biol. 80, 719-726
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Hepatitis B Virus Promotes Angiopoietin-2 Expression in Liver Tissue: Role of HBV X Protein.
P. Sanz-Cameno, S. Martin-Vilchez, E. Lara-Pezzi, M. J. Borque, J. Salmeron, P. Munoz de Rueda, J. A. Solis, M. Lopez-Cabrera, and R. Moreno-Otero (2006)
Am. J. Pathol. 169, 1215-1222
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Signaling and regulation of endothelial cell survival by angiopoietin-2.
R. Harfouche and S. N. A. Hussain (2006)
Am J Physiol Heart Circ Physiol 291, H1635-H1645
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Structure of the Extracellular Domain of Tie Receptor Tyrosine Kinases and Localization of the Angiopoietin-binding Epitope.
P. R. Macdonald, P. Progias, B. Ciani, S. Patel, U. Mayer, M. O. Steinmetz, and R. A. Kammerer (2006)
J. Biol. Chem. 281, 28408-28414
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Angiopoietin-2 Overexpression in Morris Hepatoma Results in Increased Tumor Perfusion and Induction of Critical Angiogenesis-Promoting Genes.
P. Kunz, J. Hoffend, A. Altmann, A. Dimitrakopoulou-Strauss, D. Koczan, M. Eisenhut, G. A. Bonaterra, T. J. Dengler, W. Mier, U. Haberkorn, et al. (2006)
J. Nucl. Med. 47, 1515-1524
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Expression of angiogenic growth factors by uterine natural killer cells during early pregnancy.
G. E. Lash, B. Schiessl, M. Kirkley, B. A. Innes, A. Cooper, R. F. Searle, S. C. Robson, and J. N. Bulmer (2006)
J. Leukoc. Biol. 80, 572-580
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Activation of Tie2 by angiopoietin-1 and angiopoietin-2 results in their release and receptor internalization.
E. Bogdanovic, V. P. K. H. Nguyen, and D. J. Dumont (2006)
J. Cell Sci. 119, 3551-3560
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