122
Views
81
CrossRef citations to date
0
Altmetric
Research Article

VEGF-A induced hyperpermeability of blood-retinal barrier endothelium in vivo is predominantly associated with pinocytotic vesicular transport and not with formation of fenestrations

, , , , , & show all
Pages 637-645 | Published online: 02 Jul 2009

Reference

  • Ferrara N, Davis-Smith T. The biology of vascular en-dothelial growth factor. Endocr Rev. 1997;18:4–25.
  • Leung DW, Cachinanes G, Kuang W-J, Goeddel DV, Ferrara N. Vascular endothelial growth factor is a se-creted angiogenic mitogen. Science. 1989;246:1309–1312.
  • Senger DR, Galli SJ, Dvorak AM, Perruzzi CA, Harvey VS, Dvorak HF. Tumor cells secrete a vascular perme-ability factor that promotes accumulation of ascites fluid. Science. 1983;219:983–985.
  • Schlingemann RO, van Hinsbergh VWM. Role of vas-cular permeability factor/vascular endothelial growth fac-tor in eye disease. Br J Ophthalmol. 1997;81:501–512.
  • Roberts WG, Palade G. Increased microvascular perme- ability and endothelial fenestration induced by vascular endothelial growth factor. J Cell Sci. 1985;108:2369–2379.
  • Dvorak AM, Kohn S, Morgan ES, Fox P, Nagy JA, Dvorak HF. The vesiculo-vacuolar Organelle (VV0); a distinct endothelial cell structure that provides a transcellular pathway for macrovascular extravasation. J Leukocyte Biol. 1996;59:100–115.
  • Feng D, Nagy JA, Hipp J, Dvorak HF, Dvorak AM. Vesiculo vacuolar organelles and the regulation of venule permeability to macromolecules by vascular permeabil-ity factor, histamine, and serotonin. J Exp Med. 1996;183: 1981–1986.
  • Collins PD, Connolly DT, Williams TJ. Characterization of the increase in vascular permeability induced by vas-cular permeability factor in vivo. Br J Pharmacol. 1993;109:195–199.
  • Feng Y, Venema VJ, Venema RC, Tsai N, Behzadian MA, Caldwell RB. VEGF-induced permeability increase is mediated by caveolae. Invest Ophthalmol Vis Sci. 1999;40:157–167.
  • Esser S, Wolburg K, Wolburg H, Breier G, Kurzchalia T, Risau W. Vascular endothelial growth factor induces endothelial fenestrations in vitro. J Cell Biol. 1998;20:947–959.
  • Wang W, Merrill MJ, Borchardt RT. Vascular endothe-lial growth factor affects permeability of brain microvessels in vitro. Am J Physiol. 1996;271:C1973–1980.
  • Bradbury MWB. The blood-brain barrier: transport across the cerebral endothelium. Circ Res. 1985;57:213–222.
  • Fride PM. Receptor mediated transport of peptides and proteins across the blood-brain barriers. In: WM Partridge, ed. The Blood-Brain Barrier. New York: Raven Press, Ltd.; 1993:229–247.
  • Raviola G. The structural basis of the blood-ocular bar-riers. Exp Eye Res. 1977;(suppl.):27–63.
  • Antonetti DE, Lieth E, Barber AJ, Gardner TW. Molecular mechanisms of vascular permeability in diabetic retino-pathy. Seminars in Ophthalmology. 1999;14:240–248.
  • Luna JD, Chan CC, Derevjanik NL, Mahlow J, Chiu C, Penk B, Tobe T, Campochiaro PA, Vinores SA. Blood-retinal barrier (BRB) breakdown in experimental autoim-mune uveoretinitis: comparison with vascular endothe-lial growth factor, tumor necrosis factor alpha, and interlukin-lbeta mediated breakdown. J Neurosci Res. 1997;49:268–280.
  • Ishibashi T, Inomata H. Ultrastructure of retinal vessels in diabetic patients. Br J Ophthalmol. 1993;77:574–578.
  • Wallow IHL, Engerman RL. Permeability and patency of retinal blood vessels in experimental diabetes. Invest Ophth. 1977;16:447–461.
  • Cunha-Vaz J, De Abreu JRF, Campos AJ, Figo GM. Early breakdown of the blood-retinal barrier in diabetes. Br J Ophthalmol. 1975;59:649–656.
  • Cunha-Vaz J. The blood-retinal barriers. Surv Ophthalmol.1979;23:279–296.
  • Senger DR, Brown LF, Claffey KP, Dvorak HF. Vas-cular permeability factor, tumor angiogenesis and stoma generation. Inv Metast. 1994;14:3853–3894.
  • Dvorak HF, Brown LF, Detmar M, Dvorak AM. Vascu-lar permeability factor/vascular endothelial growth fac-tor, microvascular hyperpermeability, and angiogenesis. Am J Pathol. 1995;146:1029–1039.
  • Plate KH, Breier G, Weich HA, Risau W. Vascular en-dothelial growth factor is a potential tumor angiogen-esis factor in human glioma in vivo. Nature. 1992;359: 845–848.
  • Aiello LP, Avery RL, Arrigg PG, et al. Vascular endot-helial growth factor in ocular fluid of patients with dia-betic retinopathy and other retinal disorders. N Eng J Med. 1994;331:1480–1487.
  • Ferrara N. Vascular endothelial growth factor. The trig-ger for neovascularization in the eye. Lab Invest. 1995;72:615–618.
  • Murata T, Nakagawa K, Khalil A, Ishibashi T, Inomata H, Sueishi K. The relation between expression of vas-cular endothelial growth factor and breakdown of the blood-retinal barrier in diabetic rat retinas. Lab Invest. 1996;74:819–825.
  • Miller JW, Adamis AP, Shima DT et al. Vascular en-dothelial growth factor/vascular permeability factor is temporally and spatially correlated with ocular angio-genesis in a primate model. Am J Pathol. 1994;145:574–584.
  • Aiello LP. Vascular endothelial growth factor and the eye: biochemical mechanisms of action and implications for novel therapies. Ophthalmic Res. 1997;29:354–362.
  • Tolentino MJ, Miller JW, Gragoudas ES, et al. Intravit-reous injections of vascular endothelial growth factor produce retinal ischemia and microangiopathy in an adult primate. Ophthalmology. 1996;103:1820–1828.
  • Connolly DT. Vascular permeability factor; a unique regulator of blood vessel function. J Cell Biochem. 1991;47:219–223.
  • Qu-H, Nagy, JA Senger, DR, Dvorak HF, Dvorak AM. Ultrastructural localization of vascular permeability factor / vascular endothelial growth factor (VPFNEGF) to the abluminal plasma membrane and vesiculovacuolar or-ganelles of tumor microvascular endothelium. J Histochem Cytochem. 1995;43:381–389.
  • Kohn S, Nagy JA, Dvorak HF, Dvorak AM. Pathways of macrovascular tracer transport across venules and small veins. Structural basis for the hyperpermeability of tu-mor blood vessels. Lab Invest. 1992;67:596–607.
  • Schnitzer JE, Oh P, Pinney E, Allard J. Filipin-sensitive caveolae-mediated transport in endothelium: reduced transcytosis, scavenger endocytosis, and capillary per-meability of select macromolecules. J Cell Biol. 1994;127:1217–1232.
  • Wagner RC, Cen SC. Transcapillary transport of solute by the endothelial vesicular system: evidence from thin serial section analysis. Microvasc Res. 1991;42:139–150
  • Schneeberger EE. Proteins and vesicular transport in capillary endothelium. Fed Proc. 1983;42:2419–2424.
  • Roberts WG, Delaat J, Nagane M, Huang S, Cavenee WK, Palade GE. Host microvasculature influence on tumor vascular morphology and endothelial gene expres-sion. Am J Pathol. 1998;153:1239–1248.
  • Risau W. Differentiation of endothelium. FASEB J. 1998;9:926–933.
  • Engler CB, Sander B, Larsen M, Dalgard P, Andersen HL. Fluorescein transport across the human blood-retina barrier in the direction vitreous to blood. Quantitative assessment in vivo. Acta Ophthalmol. 1994a;72:655–662.
  • Gardiner TA, Archer DB. Does unidurectional vesicular transport occur in retinal vessels? Br J Ophthalmol. 1986;70:249–254.
  • Raviola G, Butler JW. Unidirectional vesicular transport mechanism in retinal vessels. Invest Ophthalmol Vis Sci. 1983;24:1465–1474.
  • Engler CB, Sander B, Larsen M, Koefoed P, Parving HH, Andersen HL. Probenecid inhibition of the outward trans-port of fluorescein across the human blood-retina bar-rier. Acta Ophthalmol. 1994b;72:663–667.
  • Vinores SA, McGehee R, Lee A, Gadegbeku C, Campochiaro PA. Ultrastructural localization of blood-retinal barrier breakdown in diabetic and galactosemic rats. J Histochem Cytochem. 1990;38:1341–1352.

Reprints and Corporate Permissions

Please note: Selecting permissions does not provide access to the full text of the article, please see our help page How do I view content?

To request a reprint or corporate permissions for this article, please click on the relevant link below:

Academic Permissions

Please note: Selecting permissions does not provide access to the full text of the article, please see our help page How do I view content?

Obtain permissions instantly via Rightslink by clicking on the button below:

If you are unable to obtain permissions via Rightslink, please complete and submit this Permissions form. For more information, please visit our Permissions help page.