Therapeutic interference with EphrinB2 signalling inhibits oxygen-induced angioproliferative retinopathy

Acta Ophthalmologica

Volumn 89, Issue 1, 2011, Pages 82-90

  Ehlken, Christoph ^a   Martin, Gottfried ^a   Lange, Clemens ^a   Gogaki, Eleni G ^a   Fiedler, Ulrike ^b   Schaffner, Florence ^b   Hansen, Lutz L ^a   Augustin, Hellmut G ^b   Agostini, Hansjürgen T ^a  

^a UNIVERSITY OF FREIBURG   (Germany)

^b TUMOR BIOLOGY CENTER   (Germany)

Author keywords

angiogenesis; molecular biology; retinal diseases; retinopathy of prematurity

Indexed keywords

EPHRIN B2; MESSENGER RNA; MONOMERIC EPHRIN B2; OXYGEN; UNCLASSIFIED DRUG; VASCULOTROPIN; VASCULOTROPIN RECEPTOR 1; VASCULOTROPIN RECEPTOR 2;

ANGIOGENESIS; ANGIOPROLIFERATIVE RETINOPATHY; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CONTROLLED STUDY; HYPOXIA; MOUSE; NONHUMAN; POLYMERASE CHAIN REACTION; PRIORITY JOURNAL; RETINOPATHY; SIGNAL TRANSDUCTION;

ANIMALS; ANIMALS, NEWBORN; DEXTRANS; DISEASE MODELS, ANIMAL; EPHRIN-B2; FLUORESCEIN-5-ISOTHIOCYANATE; HUMANS; INFANT, NEWBORN; INTRAVITREAL INJECTIONS; MICE; MICE, INBRED C57BL; OXYGEN; POLYMERASE CHAIN REACTION; RECEPTOR, EPHB4; RETINAL NEOVASCULARIZATION; RETINAL VESSELS; RETINOPATHY OF PREMATURITY; RNA, MESSENGER; SIGNAL TRANSDUCTION; VASCULAR ENDOTHELIAL GROWTH FACTOR A; VASCULAR ENDOTHELIAL GROWTH FACTOR RECEPTOR-1; VASCULAR ENDOTHELIAL GROWTH FACTOR RECEPTOR-2;

EID: 79551534506     PISSN: 1755375X     EISSN: 17553768     Source Type: Journal    
DOI: 10.1111/j.1755-3768.2009.01609.x     Document Type: Article

References (45)

1. Adams RH, &, Klein R, (2000): Eph receptors and ephrin ligands. Essential mediators of vascular development. Trends Cardiovasc Med 10: 183-188.
2. Adams RH, Wilkinson GA, Weiss C, Diella F, Gale NW, Deutsch U, Risau W, &, Klein R, (1999): Roles of ephrinB ligands and EphB receptors in cardiovascular development: demarcation of arterial/venous domains, vascular morphogenesis, and sprouting angiogenesis. Genes Dev 13: 295-306.
3. Agostini HT, Boden K, Unsold A, Martin G, Hansen L, Fiedler U, Esser N, &, Marme D, (2005): A single local injection of recombinant VEGF receptor 2 but not of Tie2 inhibits retinal neovascularization in the mouse. Curr Eye Res 30: 249-257.
4. Arvanitis D, &, Davy A, (2008): Eph/ephrin signaling: networks. Genes Dev 22: 416-429.
5. Augustin HG, &, Reiss Y, (2003): EphB receptors and ephrinB ligands: regulators of vascular assembly and homeostasis. Cell Tissue Res 314: 25-31.
6. Brantley-Sieders DM, &, Chen J, (2004): Eph receptor tyrosine kinases in angiogenesis: from development to disease. Angiogenesis 7: 17-28. (Pubitemid 39127767)
7. Butler SJ, &, Tear G, (2007): Getting axons onto the right path: the role of transcription factors in axon guidance. Development 134: 439-448.
8. Chen J, Hicks D, Brantley-Sieders D, Cheng N, McCollum GW, Qi-Werdich X, &, Penn J, (2006): Inhibition of retinal neovascularization by soluble EphA2 receptor. Exp Eye Res 82: 664-673.
9. Cheng N, Brantley DM, &, Chen J, (2002): The ephrins and Eph receptors in angiogenesis. Cytokine Growth Factor Rev 13: 75-85.
10. Claxton S, &, Fruttiger M, (2005): Oxygen modifies artery differentiation and network morphogenesis in the retinal vasculature. Dev Dyn 233: 822-828.
11. Dureau P, Bonnel S, Menasche M, Dufier JL, &, Abitbol M, (2001): Quantitative analysis of intravitreal injections in the rat. Curr Eye Res 22: 74-77.
12. Egea J, &, Klein R, (2007): Bidirectional Eph-ephrin signaling during axon guidance. Trends Cell Biol 17: 230-238.
13. Fuller T, Korff T, Kilian A, Dandekar G, &, Augustin HG, (2003): Forward EphB4 signaling in endothelial cells controls cellular repulsion and segregation from ephrinB2 positive cells. J Cell Sci 116: 2461-2470.
14. Gerety SS, Wang HU, Chen ZF, &, Anderson DJ, (1999): Symmetrical mutant phenotypes of the receptor EphB4 and its specific transmembrane ligand ephrin-B2 in cardiovascular development. Mol Cell 4: 403-414.
15. Hamada K, Oike Y, Ito Y, Maekawa H, Miyata K, Shimomura T, &, Suda T, (2003): Distinct roles of ephrin-B2 forward and EphB4 reverse signaling in endothelial cells. Arterioscler Thromb Vasc Biol 23: 190-197.
16. He S, Ding Y, Zhou J, et al. (2005): Soluble EphB4 regulates choroidal endothelial cell function and inhibits laser-induced choroidal neovascularization. Invest Ophthalmol Vis Sci 46: 4772-4779.
17. Heroult M, Schaffner F, &, Augustin HG, (2006): Eph receptor and ephrin ligand-mediated interactions during angiogenesis and tumor progression. Exp Cell Res 312: 642-650.
18. Higgins RD, Yu K, Sanders RJ, Nandgaonkar BN, Rotschild T, &, Rifkin DB, (1999): Diltiazem reduces retinal neovascularization in a mouse model of oxygen induced retinopathy. Curr Eye Res 18: 20-27.
19. Himanen JP, Saha N, &, Nikolov DB, (2007): Cell-cell signaling via Eph receptors and ephrins. Curr Opin Cell Biol 19: 534-542.
20. Kertesz N, Krasnoperov V, Reddy R, Leshanski L, Kumar SR, Zozulya S, &, Gill PS, (2006): The soluble extracellular domain of EphB4 (sEphB4) antagonizes EphB4-EphrinB2 interaction, modulates angiogenesis, and inhibits tumor growth. Blood 107: 2330-2338.
21. Kuijper S, Turner CJ, &, Adams RH, (2007): Regulation of angiogenesis by Eph-ephrin interactions. Trends Cardiovasc Med 17: 145-151.
22. Lackmann M, &, Boyd AW, (2008): Eph, a protein family coming of age: more confusion, insight, or complexity? Sci Signal 1: re2.
23. Lange C, Ehlken C, Martin G, Konzok K, Moscoso DP, Hansen LL, &, Agostini HT, (2007): Intravitreal injection of the heparin analog 5-amino-2-naphthalenesulfonate reduces retinal neovascularization in mice. Exp Eye Res 85: 323-327.
24. Lobe CG, Koop KE, Kreppner W, Lomeli H, Gertsenstein M, &, Nagy A, (1999): Z/AP, a double reporter for cre-mediated recombination. Dev Biol 208: 281-292.
25. Maekawa H, Oike Y, Kanda S, Ito Y, Yamada Y, Kurihara H, Nagai R, &, Suda T, (2003): Ephrin-B2 induces migration of endothelial cells through the phosphatidylinositol-3 kinase pathway and promotes angiogenesis in adult vasculature. Arterioscler Thromb Vasc Biol 23: 2008-2014.
26. Maier P, Unsoeld AS, Junker B, Martin G, Drevs J, Hansen LL, &, Agostini HT, (2005): Intravitreal injection of specific receptor tyrosine kinase inhibitor PTK787/ZK222 584 improves ischemia-induced retinopathy in mice. Graefes Arch Clin Exp Ophthalmol 243: 593-600.
27. Martin G, Schlunck G, Hansen LL, &, Agostini HT, (2004): Differential expression of angioregulatory factors in normal and CNV-derived human retinal pigment epithelium. Graefes Arch Clin Exp Ophthalmol 242: 321-326.
28. Martiny-Baron G, Korff T, Schaffner F, Esser N, Eggstein S, Marme D, &, Augustin HG, (2004): Inhibition of tumor growth and angiogenesis by soluble EphB4. Neoplasia 6: 248-257.
29. Ozaki H, Yu AY, Della N, et al. (1999): Hypoxia inducible factor-1alpha is increased in ischemic retina: temporal and spatial correlation with VEGF expression. Invest Ophthalmol Vis Sci 40: 182-189.
30. Ozaki H, Seo MS, Ozaki K, et al. (2000): Blockade of vascular endothelial cell growth factor receptor signaling is sufficient to completely prevent retinal neovascularization. Am J Pathol 156: 697-707.
31. Pfaffl MW, Horgan GW, &, Dempfle L, (2002): Relative expression software tool (REST) for group-wise comparison and statistical analysis of relative expression results in real-time PCR. Nucleic Acids Res 30: e36.
32. Pierce EA, Foley ED, &, Smith LE, (1996): Regulation of vascular endothelial growth factor by oxygen in a model of retinopathy of prematurity. Arch Ophthalmol: 114: 1219-1228. [Published erratum appears in Arch Ophthalmol 1997; 115: 427.].
33. Ramakers C, Ruijter JM, Deprez RH, &, Moorman AF, (2003): Assumption-free analysis of quantitative real-time polymerase chain reaction (PCR) data. Neurosci Lett 339: 62-66.
34. Reber M, Hindges R, &, Lemke G, (2007): Eph receptors and ephrin ligands in axon guidance. Adv Exp Med Biol 621: 32-49.
35. Robinson GS, Ju M, Shih SC, Xu X, McMahon G, Caldwell RB, &, Smith LE, (2001): Nonvascular role for VEGF: VEGFR-1, 2 activity is critical for neural retinal development. FASEB J 15: 1215-1217.
36. Smith LE, Wesolowski E, McLellan A, Kostyk SK, D'Amato R, Sullivan R, &, D'Amore PA, (1994): Oxygen-induced retinopathy in the mouse. Invest Ophthalmol Vis Sci 35: 101-111.
37. Steinle JJ, Meininger CJ, Chowdhury U, Wu G, &, Granger HJ, (2003): Role of ephrin B2 in human retinal endothelial cell proliferation and migration. Cell Signal 15: 1011-1017.
38. Stitt AW, Graham D, &, Gardiner TA, (2004): Ocular wounding prevents pre-retinal neovascularization and upregulates PEDF expression in the inner retina. Mol Vis 10: 432-438.
39. Umeda N, Ozaki H, Hayashi H, &, Oshima K, (2004): Expression of ephrinB2 and its receptors on fibroproliferative membranes in ocular angiogenic diseases. Am J Ophthalmol 138: 270-279.
40. Unsoeld AS, Junker B, Mazitschek R, Martin G, Hansen LL, Giannis A, &, Agostini HT, (2004): Local injection of receptor tyrosine kinase inhibitor MAE 87 reduces retinal neovascularization in mice. Mol Vis 10: 468-475.
41. Wang HU, Chen ZF, &, Anderson DJ, (1998): Molecular distinction and angiogenic interaction between embryonic arteries and veins revealed by ephrin-B2 and its receptor Eph-B4. Cell 93: 661-664.
42. Yao YG, Yang HS, Cao Z, Danielsson J, &, Duh EJ, (2005): Upregulation of placental growth factor by vascular endothelial growth factor via a post-transcriptional mechanism. FEBS Lett 579: 1227-1234.
43. Yossuck P, Yan Y, Tadesse M, &, Higgins RD, (2000): Dexamethasone and critical effect of timing on retinopathy. Invest Ophthalmol Vis Sci 41: 3095-3099.
44. Zamora DO, Davies MH, Planck SR, Rosenbaum JT, &, Powers MR, (2005): Soluble forms of EphrinB2 and EphB4 reduce retinal neovascularization in a model of proliferative retinopathy. Invest Ophthalmol Vis Sci 46: 2175-2182.
45. Zhang J, &, Hughes S, (2006): Role of the ephrin and Eph receptor tyrosine kinase families in angiogenesis and development of the cardiovascular system. J Pathol 208: 453-461.