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Development, Vol 125, Issue 9 1591-1598, Copyright © 1998 by Company of Biologists
JOURNAL ARTICLES |
LE Benjamin, I Hemo and E Keshet
Department of Molecular Biology, Hebrew University-Hadassah Medical School, Jerusalem, Israel.
Little is known about how the initial endothelial plexus is remodelled into a mature and functioning vascular network. Studying postnatal remodelling of the retina vasculature, we show that a critical step in vascular maturation, namely pericyte recruitment, proceeds by outmigration of cells positive for (alpha)-smooth muscle actin from arterioles and that coverage of primary and smaller branches lags many days behind formation of the endothelial plexus. The transient existence of a pericyte-free endothelial plexus coincides temporally and spatially with the process of hyperoxia-induced vascular pruning, which is a mechanism for fine tuning of vascular density according to available oxygen. Acquisition of a pericyte coating marks the end of this plasticity window. To substantiate that association with pericytes stabilizes the vasculature, endothelial-pericyte associations were disrupted by intraocular injection of PDGF-BB. Ectopic PDGF-BB caused the detachment of PDGF-beta receptor-positive pericytes from newly coated vessels, presumably through interference with endogenous cues, but had no effect on mature vessels. Disruption of endothelial-pericyte associations resulted in excessive regression of vascular loops and abnormal remodelling. Conversely, intraocular injection of VEGF accelerated pericyte coverage of the preformed endothelial plexus, thereby revealing a novel function of this pleiotropic angiogenic growth factor. These findings also provide a cellular basis for clinical observations that vascular regression in premature neonates subjected to oxygen therapy [i.e. in retinopathy of prematurity] drops precipitously upon maturation of retina vessels and a mechanistic explanation to our previous findings that VEGF can rescue immature vessels from hyperoxia-induced regression.
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C. Colnot, L. de la Fuente, S. Huang, D. Hu, C. Lu, B. St-Jacques, and J. A. Helms Indian hedgehog synchronizes skeletal angiogenesis and perichondrial maturation with cartilage development Development, March 1, 2005; 132(5): 1057 - 1067. [Abstract] [Full Text] [PDF]
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M. Gallicchio, S. Mitola, D. Valdembri, R. Fantozzi, B. Varnum, G. C. Avanzi, and F. Bussolino Inhibition of vascular endothelial growth factor receptor 2-mediated endothelial cell activation by Axl tyrosine kinase receptor Blood, March 1, 2005; 105(5): 1970 - 1976. [Abstract] [Full Text] [PDF]
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J. E. Markkanen, T. T. Rissanen, A. Kivela, and S. Yla-Herttuala Growth factor-induced therapeutic angiogenesis and arteriogenesis in the heart-gene therapy Cardiovasc Res, February 15, 2005; 65(3): 656 - 664. [Abstract] [Full Text] [PDF]
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L. A. Wiley, G. R. Rupp, and J. J. Steinle Sympathetic Innervation Regulates Basement Membrane Thickening and Pericyte Number in Rat Retina Invest. Ophthalmol. Vis. Sci., February 1, 2005; 46(2): 744 - 748. [Abstract] [Full Text] [PDF]
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M. Berger, G. Bergers, B. Arnold, G. J. Hammerling, and R. Ganss Regulator of G-protein signaling-5 induction in pericytes coincides with active vessel remodeling during neovascularization Blood, February 1, 2005; 105(3): 1094 - 1101. [Abstract] [Full Text] [PDF]
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 T. Kitahara, K. Hiromura, H. Ikeuchi, S. Yamashita, S. Kobayashi, T. Kuroiwa, Y. Kaneko, K. Ueki, and Y. Nojima Mesangial cells stimulate differentiation of endothelial cells to form capillary-like networks in a three-dimensional culture system Nephrol. Dial. Transplant., January 1, 2005; 20(1): 42 - 49. [Abstract] [Full Text] [PDF]
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M. R. Machein, A. Knedla, R. Knoth, S. Wagner, E. Neuschl, and K. H. Plate Angiopoietin-1 Promotes Tumor Angiogenesis in a Rat Glioma Model Am. J. Pathol., November 1, 2004; 165(5): 1557 - 1570. [Abstract] [Full Text] [PDF]
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P. Baluk, C. G. Lee, H. Link, E. Ator, A. Haskell, J. A. Elias, and D. M. McDonald Regulated Angiogenesis and Vascular Regression in Mice Overexpressing Vascular Endothelial Growth Factor in Airways Am. J. Pathol., October 1, 2004; 165(4): 1071 - 1085. [Abstract] [Full Text] [PDF]
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T. Chan-Ling, M. P. Page, T. Gardiner, L. Baxter, E. Rosinova, and S. Hughes Desmin Ensheathment Ratio as an Indicator of Vessel Stability: Evidence in Normal Development and in Retinopathy of Prematurity Am. J. Pathol., October 1, 2004; 165(4): 1301 - 1313. [Abstract] [Full Text] [PDF]
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J.-H. Paik, A. Skoura, S.-S. Chae, A. E. Cowan, D. K. Han, R. L. Proia, and T. Hla Sphingosine 1-phosphate receptor regulation of N-cadherin mediates vascular stabilization Genes & Dev., October 1, 2004; 18(19): 2392 - 2403. [Abstract] [Full Text] [PDF]
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S. Cui, A. Ross, N. Stallings, K. L. Parker, B. Capel, and S. E. Quaggin Disrupted gonadogenesis and male-to-female sex reversal in Pod1 knockout mice Development, August 15, 2004; 131(16): 4095 - 4105. [Abstract] [Full Text] [PDF]
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K. L. Christman, A. J. Vardanian, Q. Fang, R. E. Sievers, H. H. Fok, and R. J. Lee Injectable fibrin scaffold improves cell transplant survival, reduces infarct expansion, and induces neovasculature formation in ischemic myocardium J. Am. Coll. Cardiol., August 4, 2004; 44(3): 654 - 660. [Abstract] [Full Text] [PDF]
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 M. Dobaczewski, S. Akrivakis, K. Nasser, L. H. Michael, M. L. Entman, and N. G. Frangogiannis Vascular Mural Cells in Healing Canine Myocardial Infarcts J. Histochem. Cytochem., August 1, 2004; 52(8): 1019 - 1029. [Abstract] [Full Text] [PDF]
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S. Hughes and T. Chan-Ling Characterization of Smooth Muscle Cell and Pericyte Differentiation in the Rat Retina In Vivo Invest. Ophthalmol. Vis. Sci., August 1, 2004; 45(8): 2795 - 2806. [Abstract] [Full Text] [PDF]
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 J.-i. Fukushi, I. T. Makagiansar, and W. B. Stallcup NG2 Proteoglycan Promotes Endothelial Cell Motility and Angiogenesis via Engagement of Galectin-3 and {alpha}3{beta}1 Integrin Mol. Biol. Cell, August 1, 2004; 15(8): 3580 - 3590. [Abstract] [Full Text] [PDF]
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A. H. Shih, C. Dai, X. Hu, M. K. Rosenblum, J. A. Koutcher, and E. C. Holland Dose-Dependent Effects of Platelet-Derived Growth Factor-B on Glial Tumorigenesis Cancer Res., July 15, 2004; 64(14): 4783 - 4789. [Abstract] [Full Text] [PDF]
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A. V. Ohlmann, E. Adamek, A. Ohlmann, and E. Lutjen-Drecoll Norrie Gene Product Is Necessary for Regression of Hyaloid Vessels Invest. Ophthalmol. Vis. Sci., July 1, 2004; 45(7): 2384 - 2390. [Abstract] [Full Text] [PDF]
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 K. Tang, E. C. Breen, H.-P. Gerber, N. M. A. Ferrara, and P. D. Wagner Capillary regression in vascular endothelial growth factor-deficient skeletal muscle Physiol Genomics, June 17, 2004; 18(1): 63 - 69. [Abstract] [Full Text] [PDF]
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 O. Stoeltzing, M. F. McCarty, J. S. Wey, F. Fan, W. Liu, A. Belcheva, C. D. Bucana, G. L. Semenza, and L. M. Ellis Role of Hypoxia-Inducible Factor 1{alpha} in Gastric Cancer Cell Growth, Angiogenesis, and Vessel Maturation J Natl Cancer Inst, June 16, 2004; 96(12): 946 - 956. [Abstract] [Full Text] [PDF]
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 M. Ehrbar, V. G. Djonov, C. Schnell, S. A. Tschanz, G. Martiny-Baron, U. Schenk, J. Wood, P. H. Burri, J. A. Hubbell, and A. H. Zisch Cell-Demanded Liberation of VEGF121 From Fibrin Implants Induces Local and Controlled Blood Vessel Growth Circ. Res., April 30, 2004; 94(8): 1124 - 1132. [Abstract] [Full Text] [PDF]
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F. Baffert, G. Thurston, M. Rochon-Duck, T. Le, R. Brekken, and D. M. McDonald Age-Related Changes in Vascular Endothelial Growth Factor Dependency and Angiopoietin-1-Induced Plasticity of Adult Blood Vessels Circ. Res., April 16, 2004; 94(7): 984 - 992. [Abstract] [Full Text] [PDF]
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