Notch4 normalization reduces blood vessel size in arteriovenous malformations

Science Translational Medicine

Volumn 4, Issue 117, 2012, Pages

  Murphy, Patrick A ^a,c   Kim, Tyson N ^a   Lu, Gloria ^a   Bollen, Andrew W ^a   Schaffer, Chris B ^b   Wang, Rong A ^a  

^a UNIVERSITY OF CALIFORNIA   (United States)

^b Cornell University   (United States)

^c MASSACHUSETTS INSTITUTE OF TECHNOLOGY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

EPHRIN RECEPTOR B4; NOTCH4 RECEPTOR; NOTCH RECEPTOR; NOTCH4 PROTEIN, MOUSE; ONCOPROTEIN;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ARTERIOVENOUS MALFORMATION; ARTERIOVENOUS SHUNT; ARTERY BLOOD FLOW; ARTICLE; BLOOD FLOW VELOCITY; BLOOD VESSEL DIAMETER; CELL COUNT; CELL LOSS; CONTROLLED STUDY; ENDOTHELIUM CELL; FOUR DIMENSIONAL TWO PHOTON IMAGING; HYPOXEMIA; IMAGING; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; RECEPTOR UPREGULATION; SIGNAL TRANSDUCTION; TISSUE OXYGENATION; ANIMAL; ANOXIA; BIOLOGICAL MODEL; BIOSYNTHESIS; BLOOD VESSEL; BRAIN; CAPILLARY; CYTOLOGY; GENE EXPRESSION REGULATION; METABOLISM; PATHOLOGY; PHOTON; PHYSIOLOGY; TRANSGENIC MOUSE;

ANIMALS; ANOXIA; ARTERIOVENOUS MALFORMATIONS; BLOOD VESSELS; BRAIN; CAPILLARIES; ENDOTHELIAL CELLS; GENE EXPRESSION REGULATION; MICE; MICE, TRANSGENIC; MODELS, CARDIOVASCULAR; PHOTONS; PROTO-ONCOGENE PROTEINS; RECEPTOR, EPHB4; RECEPTORS, NOTCH; SIGNAL TRANSDUCTION;

EID: 84856077411     PISSN: 19466234     EISSN: 19466242     Source Type: Journal    
DOI: 10.1126/scitranslmed.3002670     Document Type: Article

References (35)

1. M. C. Garzon, J. T. Huang, O. Enjolras, I. J. Frieden, Vascular malformations: Part I. J. Am. Acad. Dermatol. 56, 353-370 (2007).
2. R. M. Friedlander, Clinical practice. Arteriovenous malformations of the brain. N. Engl. J. Med. 356, 2704-2712 (2007).
3. C. Roca, R. H. Adams, Regulation of vascular morphogenesis by Notch signaling. Genes Dev. 21, 2511-2524 (2007).
4. H. U. Wang, Z. F. Chen, D. J. Anderson, Molecular distinction and angiogenic interaction between embryonic arteries and veins revealed by ephrin-B2 and its receptor Eph-B4. Cell 93, 741-753 (1998).
5. L. R. You, F. J. Lin, C. T. Lee, F. J. DeMayo, M. J. Tsai, S. Y. Tsai, Suppression of Notch signalling by the COUP-TFII transcription factor regulates vein identity. Nature 435, 98-104 (2005).
6. D. Shin, G. Garcia-Cardena, S. Hayashi, S. Gerety, T. Asahara, G. Stavrakis, J. Isner, J. Folkman, M. A. Gimbrone Jr., D. J. Anderson, Expression of ephrinB2 identifies a stable genetic difference between arterial and venous vascular smooth muscle as well as endothelial cells, and marks subsets of microvessels at sites of adult neovascularization. Dev. Biol. 230, 139-150 (2001).
7. R. Benedito, A. Duarte, Expression of Dll4 during mouse embryogenesis suggests multiple developmental roles. Gene Expr. Patterns 5, 750-755 (2005).
8. P. A. Murphy, G. Lu, S. Shiah, A. W. Bollen, R. A. Wang, Endothelial Notch signaling is upregulated in human brain arteriovenous malformations and a mouse model of the disease. Lab. Invest. 89, 971-982 (2009).
9. Q. ZhuGe, M. Zhong, W. Zheng, G. Y. Yang, X. Mao, L. Xie, G. Chen, Y. Chen, M. T. Lawton, W. L. Young, D. A. Greenberg, K. Jin, Notch-1 signalling is activated in brain arteriovenous malformations in humans. Brain 132, 3231-3241 (2009).
10. P. A. Murphy, M. T. Lam, X. Wu, T. N. Kim, S. M. Vartanian, A. W. Bollen, T. R. Carlson, R. A. Wang, Endothelial Notch4 signaling induces hallmarks of brain arteriovenous malformations in mice. Proc. Natl. Acad. Sci. U.S.A. 105, 10901-10906 (2008).
11. C. B. Schaffer, B. Friedman, N. Nishimura, L. F. Schroeder, P. S. Tsai, F. F. Ebner, P. D. Lyden, D. Kleinfeld, Two-photon imaging of cortical surface microvessels reveals a robust redistribution in blood flow after vascular occlusion. PLoS Biol. 4, e22 (2006).
12. T. R. Carlson, Y. Yan, X. Wu, M. T. Lam, G. L. Tang, L. J. Beverly, L. M. Messina, A. J. Capobianco, Z. Werb, R. Wang, Endothelial expression of constitutively active Notch4 elicits reversible arteriovenous malformations in adult mice. Proc. Natl. Acad. Sci. U.S.A. 102, 9884-9889 (2005).
13. M. Unekawa, M. Tomita, Y. Tomita, H. Toriumi, K. Miyaki, N. Suzuki, RBC velocities in single capillaries of mouse and rat brains are the same, despite 10-fold difference in body size. Brain Res. 1320, 69-73 (2010).
14. E. A. Jones, F. le Noble, A. Eichmann, What determines blood vessel structure? Genetic prespecification vs. hemodynamics. Physiology 21, 388-395 (2006).
15. E. Fuchs, The tortoise and the hair: Slow-cycling cells in the stem cell race. Cell 137, 811-819 (2009).
16. S. S. Gerety, H. U. Wang, Z. F. Chen, D. J. Anderson, Symmetrical mutant phenotypes of the receptor EphB4 and its specific transmembrane ligand ephrin-B2 in cardiovascular development. Mol. Cell 4, 403-414 (1999).
17. N. Kertesz, V. Krasnoperov, R. Reddy, L. Leshanski, S. R. Kumar, S. Zozulya, P. S. Gill, The soluble extracellular domain of EphB4 (sEphB4) antagonizes EphB4-EphrinB2 interaction, modulates angiogenesis, and inhibits tumor growth. Blood 107, 2330-2338 (2006).
18. E. L. Rolett, A. Azzawi, K. J. Liu, M. N. Yongbi, H. M. Swartz, J. F. Dunn, Critical oxygen tension in rat brain: A combined 31P-NMR and EPR oximetry study. Am. J. Physiol. Regul. Integr. Comp. Physiol. 279, R9-R16 (2000).
19. Y. H. Kim, H. Hu, S. Guevara-Gallardo, M. T. Lam, S. Y. Fong, R. A. Wang, Artery and vein size is balanced by Notch and ephrin B2/EphB4 during angiogenesis. Development 135, 3755-3764 (2008).
20. K. Red-Horse, H. Ueno, I. L. Weissman, M. A. Krasnow, Coronary arteries form by developmental reprogramming of venous cells. Nature 464, 549-553 (2010).
21. M. E. Pitulescu, R. H. Adams, Eph/ephrin molecules-A hub for signaling and endocytosis. Genes Dev. 24, 2480-2492 (2010).
22. R. K. Jain, Normalization of tumor vasculature: An emerging concept in antiangiogenic therapy. Science 307, 58-62 (2005).
23. F. Baffert, T. Le, B. Sennino, G. Thurston, C. J. Kuo, D. Hu-Lowe, D. M. McDonald, Cellular changes in normal blood capillaries undergoing regression after inhibition of VEGF signaling. Am. J. Physiol. Heart Circ. Physiol. 290, H547-H559 (2006).
24. I. B. Lobov, S. Rao, T. J. Carroll, J. E. Vallance, M. Ito, J. K. Ondr, S. Kurup, D. A. Glass, M. S. Patel, W. Shu, E. E. Morrisey, A. P. McMahon, G. Karsenty, R. A. Lang, WNT7b mediates macrophage-induced programmed cell death in patterning of the vasculature. Nature 437, 417-421 (2005).
25. A. Meeson, M. Palmer, M. Calfon, R. Lang, A relationship between apoptosis and flow during programmed capillary regression is revealed by vital analysis. Development 122, 3929-3938 (1996).
26. D. Miniati, E. B. Jelin, J. Ng, J. Wu, T. R. Carlson, X. Wu, M. R. Looney, R. A. Wang, Constitutively active endothelial Notch4 causes lung arteriovenous shunts in mice. Am. J. Physiol. Lung Cell. Mol. Physiol. 298, L169-L177 (2010).
27. A. Davy, J. O. Bush, P. Soriano, Inhibition of gap junction communication at ectopic Eph/ephrin boundaries underlies craniofrontonasal syndrome. PLoS Biol. 4, e315 (2006).
28. M. D. Muzumdar, B. Tasic, K. Miyamichi, L. Li, L. Luo, A global double-fluorescent Cre reporter mouse. Genesis 45, 593-605 (2007).
29. T. Tumbar, G. Guasch, V. Greco, C. Blanpain, W. E. Lowry, M. Rendl, E. Fuchs, Defining the epithelial stem cell niche in skin. Science 303, 359-363 (2004).
30. N. Takamoto, L. R. You, K. Moses, C. Chiang, W. E. Zimmer, R. J. Schwartz, F. J. DeMayo, M. J. Tsai, S. Y. Tsai, COUP-TFII is essential for radial and anteroposterior patterning of the stomach. Development 132, 2179-2189 (2005).
31. A. Holtmaat, T. Bonhoeffer, D. K. Chow, J. Chuckowree, V. De Paola, S. B. Hofer, M. Hübener, T. Keck, G. Knott, W. C. Lee, R. Mostany, T. D. Mrsic-Flogel, E. Nedivi, C. Portera-Cailliau, K. Svoboda, J. T. Trachtenberg, L. Wilbrecht, Long-term, high-resolution imaging in the mouse neocortex through a chronic cranial window. Nat. Protoc. 4, 1128-1144 (2009).
32. C. Portera-Cailliau, R. M. Weimer, V. De Paola, P. Caroni, K. Svoboda, Diverse modes of axon elaboration in the developing neocortex. PLoS Biol. 3, e272 (2005).
33. S. Hornig, C. Biskup, A. Gräfe, J. Wotschadlo, T. Liebert, G. J. Mohr, T. Heinze, Biocompatible fluorescent nanoparticles for pH-sensoring. Soft Matter 4, 1169-1172 (2008).
34. R. Braren, H. Hu, Y. H. Kim, H. E. Beggs, L. F. Reichardt, R. Wang, Endothelial FAK is essential for vascular network stability, cell survival, and lamellipodial formation. J. Cell Biol.172, 151-162 (2006).
35. B. Carpenter, Y. Lin, S. Stoll, R. L. Raffai, R. McCuskey, R. Wang, VEGF is crucial for the hepatic vascular development required for lipoprotein uptake. Development 132, 3293-3303 (2005).