Development and pathology of the hyaloid, choroidal and retinal vasculature

International Journal of Developmental Biology

Volumn 48, Issue 8-9, 2004, Pages 1045-1058

  Saint Geniez, Magali ^b   D'Amore, Patricia A ^a  

^a SCHEPENS EYE RESEARCH INSTITUTE   (United States)

^b NONE

Author keywords

Angiogenesis; Diabetic retinopathy; Retinopathy of prematurity; Vascularization

Indexed keywords

FIBROBLAST GROWTH FACTOR; PLATELET DERIVED GROWTH FACTOR; VASCULOTROPIN;

ANGIOGENESIS; CELL INTERACTION; CHOROID DISEASE; CHOROID VASCULARIZATION; DIABETIC RETINOPATHY; EMBRYO DEVELOPMENT; EMBRYONIC STRUCTURES; EYE DEVELOPMENT; GLIA CELL; HUMAN; HYALOID; MOLECULAR BIOLOGY; NERVE CELL; NONHUMAN; PERSISTENT HYPERPLASTIC PRIMARY VITREOUS; PRIORITY JOURNAL; PROLIFERATIVE RETINOPATHY; RETINA BLOOD VESSEL; RETINA DISEASE; RETINA MACULA AGE RELATED DEGENERATION; RETINA NEUROEPITHELIAL LAYER; RETROLENTAL FIBROPLASIA; REVIEW; VASCULAR DISEASE; VASCULARIZATION;

ANIMALS; ARTERIES; CELL COMMUNICATION; CELL DIFFERENTIATION; CELL LINEAGE; CELL PROLIFERATION; CHOROID; DISEASE MODELS, ANIMAL; EMBRYONIC DEVELOPMENT; EYE; GENE EXPRESSION REGULATION, DEVELOPMENTAL; HUMANS; MACULAR DEGENERATION; MICE; MODELS, BIOLOGICAL; NEOVASCULARIZATION, PATHOLOGIC; NEOVASCULARIZATION, PHYSIOLOGIC; PHENOTYPE; PLATELET-DERIVED GROWTH FACTOR; RETINA; RETINAL NEOVASCULARIZATION; VASCULAR ENDOTHELIAL GROWTH FACTOR A;

MAMMALIA;

EID: 11144348973     PISSN: 02146282     EISSN: None     Source Type: Journal    
DOI: 10.1387/ijdb.041895ms     Document Type: Review

References (133)

1. ADAMIS, A.P., MILLER, J.W., BERNAL, M.-T., D'AMICO, D.J., FOLKMAN, J., YEO, T.-K. and YEO, K.-T. (1994). Increased vascular endothelial growth factor levels in the vitreous of eyes with proliferative diabetic retinopathy. Am. J. Ophthal. 118: 445-450.
2. ADAMIS, A.P., SHIMA, D.T., TOLENTINO, M.J., GRAGOUDAS, E.S., FERRARA, N., FOLKMAN, J., D'AMORE, P.A. and MILLER, J.W. (1996). Inhibition of VEGF prevents ocular neovascularization in a primate. Arch. Ophthalmol. 114: 66-71.
3. AIELLO, L.P., AVERY, R.L., ARRIGG, P.G., KEYT, B.A., H.D., J., SHAH, S.T., PASQUALE, L.R., THIEME, H., IWAMOTO, M.A., PARK, J.E., NGUYEN, H.V., AIELLO, L.M., FERRARA, N. and KING, G.L. (1994). Vascular endothelial growth factor in ocular fluid of patients with diabetic retinopathy and other ocular disorders. New Engl. J. Med. 331: 1480-1487.
4. AIELLO, L.P., PEIRCE, E.A., FOLEY, E.D., TAKAGI, H., CHEN, H., RIDDLE, L., FERRARA, N., KING, G.L. and SMITH, L.E.H. (1995). Suppression of retinal neovascularization in vivo by inhibition of vascular endothelial growth factor (VEGF) using soluble VEGF-receptor chimeric proteins. Proc. Natl. Acad. Sci. USA 92: 10457-10461.
5. ALON, T., HEMO, I., ITIN, A., PE'ER, J., STONE, J. and KESHET, S. (1995). Vascular endothelial growth factor acts as a survival factor for newly formed retinal vessels and has implications for retinopathy of prematurity. Nature Medicine 1: 1024-1028.
6. AMBATI, J., AMBATI, B., YOO, S., IANCHULEV, S. and ADAMIS, A. (2003). Age-related macular degeneration: etiology, pathogenesis, and therapeutic strategies. Surv Ophthalmol. 48: 257-293.
7. AMIN, R.H., FRANK, R.N., KENNEDY, A., ELIOTT, D., PUKLIN, J.E. and ABRAMS, G.W. (1997). Vascular endothelial growth factor is present in glial cells of the retina and optic nerve of human subjects with nonproliferative diabetic retinopathy. Invest Ophthalmol Vis Sci 38: 36-47.
8. ASH, J.D. and OVERBEEK, P.A. (2000). Lens-specific VEGF-A expression induces angioblast migration and proliferation and stimulates angiogenic remodeling. Dev Biol 223: 383-398.
9. BACIC, M., EDWARDS, N.A. and MERRILL, M.J. (1995). Differential expression of vascular endothelial growth factor (vascular permeability factor) forms in rat tissues. Growth Factors 12: 11-15.
10. BAFFI, J., BYRNES, G., CHAN, C.C. and CSAKY, K.G. (2000). Choroidal neovascularization in the rat induced by adenovirus mediated expression of vascular endothelial growth factor. Invest Ophthalmol Vis Sci 41: 3582-3589.
11. BENJAMIN, L.E., MEMO, I. and KESHET, E. (1998). A plasticity window for blood vessel remodelling is defined by pericyte coverage of the preformed endothelial network and is regulated by PDGF-B and VEGF. Development 125: 1591-1598.
12. BLAAUWGEERS, H.G., HOLTKAMP, G.M., RUTTEN, H., WITMER, A.N., KOOLWIJK, P., PARTANEN, T.A., ALITALO, K., KROON, M.E., KIJLSTRA, A., VAN HINSBERGH, V.W. and SCHLINGEMANN, R.O. (1999). Polarized vascular endothelial growth factor secretion by human retinal pigment epithelium and localization of vascular endothelial growth factor receptors on the inner choriocapillaris. Evidence for a trophic paracrine relation. Am J Pathol 155: 421-428.
13. BOTTINGER, E., LETTERIO, J. and ROBERTS, A. (1997). Biology of TGF-β in knockout and transgenic mouse models. Kid. Internat. 51: 1355-1360.
14. BROWNING, J., REICHELT, M.E., GOLE, G.A. and MASSA, H. (2001). Proximal arterial vasoconstriction precedes regression of the hyaloid vasculature. Curr Eye Res 22: 405-411.
15. CARMELIET, P., FERRIERA, V., BREIER, G., POLLEFEYT, S., KIECKENS, L., GERTSENSTEIN, M., FAHRIG, M., VANDENHOECK, A., HARPAL, K., EBERHARDT, C., DECLERCQ, C., PAWLING, J., MOONS, L., COLLEN, D., RISAU, W. and NAGY, A. (1996). Abnormal blood vessel development and lethality in embryos lacking a single VEGF allele. Nature 380: 435-439.
16. CHAN-LING, T., GOCK, B. and STONE, J. (1995). The effect of oxygen on vasoformative cell division. Evidence that 'physiologic hypoxia' is the stimulus for normal retinal vasculogenesis. Invest. Ophthalmol. Vis. Sci. 36: 1201-1214.
17. CHAN-LING, T., GOCK, B. and STONE, J. (1995). Supplemental oxygen therapy. Basis for noninvasive treatement of retinopathy of prematurity. Invest. Opthalmol. Vis. Sci. 36: 1215-1230.
18. CHAN-LING, T., HALASZ, P. and STONE, J. (1990). Development of retinal vasculature in the cat: processes and mechanisms. Cur. Eye Res. 9: 459-478.
19. CHAN-LING, T., MCLEOD, D.S., HUGHES, S., BAXTER, L., CHU, Y., HASEGAWA, T. and LUTTY, G.A. (2004). Astrocyte-Endothelial Cell Relationships during Human Retinal Vascular Development. Invest Ophthalmol Vis Sci 45: 2020-2032.
20. CHANG, B., SMITH, R.S., PETERS, M., SAVINOVA, O.V., HAWES, N.L., ZABALETA, A., NUSINOWITZ, S., MARTIN, J.E., DAVISSON, M.L., CEPKO, C.L., HOGAN, B.L. and JOHN, S.W. (2001). Haploinsufficient Bmp4 ocular phenotypes include anterior segment dysgenesis with elevated intraocular pressure. BMC Genet 2: 18.
21. CHOW, J., OGUNSHOLA, O., FAN, S.Y., LI, Y., MENT, L.R. and MAORI, J.A. (2001). Astrocyte-derived VEGF mediates survival and tube stabilization of hypoxic brain microvasoular endothelial cells in vitro. Brain Res Dev Brain Res 130: 123-132.
22. COFFIN, J.D. and POOLE, T.J. (1988). Embryonic vascular development: immunohistochemical identification of the origin and subsequent morphogenesis of the major vessel primordia in quail embryo. Development 102: 1-14.
23. DARLAND, D.C. and D'AMORE, P.A. (2001). Cell-cell interactions in vascular development. Curr Top Dev Biol 52: 107-149.
24. DARLAND, D.C., MASSINGHAM, L.J., SMITH, S.R., PlEK, E., SAINT-GENIEZ, M. and D'AMORE, P.A. (2003). Pericyte production of cell-associated VEGF is differentiation-dependent and is associated with endothelial survival. Dev Biol 264: 275-288.
25. DAWSON, D.W., VOLPERT, O.V., GILLIS, P., CRAWFORD, S.E., XU, H., BENEDICT, W. and BOUCK, N.P. (1999). Pigment epithelium-derived factor: a potent inhibitor of angiogenesis. Science 285: 245-248.
26. DEL PRIORE, L.V., HORNBECK, R., KAPLAN, H.J., JONES, Z., VALENTINO, T.L., MOSINGER-OGILVIE, J. and SWINN, M. (1995). Debridement of the pig retinal pigment epithelium in vivo. Arch Ophthalmol 113: 939-944.
27. DOETSCHMAN, T.A., GOSSLER, A. and KEMLER, R. (1987). Blastocyst-derived embryonic stem cells as a model for embryogenesis. Future Aspects in Human In Vitro Fertilization. FEICHTINGEN, W. and KEMETER, P. Berlin, Springer-Verlag: 187-195.
28. DREHER, Z., ROBINSON, S.R. and DlSTLER, C. (1992). Muller cells in vascular and avascular retinae: a survey of seven mammals. J Comp Neurol 323: 59-80.
29. DUH, E.J., YANG, H.S., HALLER, J.A., DE JUAN, E., HUMAYUN, M.S., GEHLBACH, P., MELIA, M., PIERAMICI, D., HARLAN, J.B., CAMPOCHIARO, P.A., ZACK, D.J., OGATA, N., WADA, M., OTSUJI, T., JO, N., TOMBRAN-TINK, J., MATSUMURA, M., DAWSON, D.W., VOLPERT, O.V., GILLIS, P., CRAWFORD, S.E., XU, H., BENEDICT, W. and BOUCK, N.P. (2004). Vitreous levels of pigment epithelium-derived factor and vascular endothelial growth factor: implications for ocular angiogenesis. Am J Ophthalmol 137: 668-674.
30. DUMONT, D.J., GRADWOHL, G., FONG, G.-H., PURI, M.C., GERTSENSTEIN, M., AUERBACH, A. and BREITMAN, M.L. (1994). Dominant-negative and targeted null mutations in the endothelial receptor tyrosine kinase, tek, reveal a critical role in vasculogenesis of the embryo. Genes Dev. 8: 1897-1907.
31. ENGERMAN, R.L., PFAFFENBACH, D. and DAVIS, M.D. (1967). Cell turnover of capillaries. Lab. Invest. 17: 738-743.
32. ETCHEVERS, H.C., VINCENT, C., LE DOUARIN, N.M. and COULY, G.F. (2001). The cephalic neural crest provides pericytes and smooth muscle cells to all blood vessels of the face and forebrain. Development 128: 1059-1068.
33. FLOWER, R.W., MCLEOD, D.S., LUTTY, G.A., GOLDBERG, B. and WAJER, S.D. (1985). Postnatal retinal vascular development of the puppy. Invest Ophthalmol Vis Sci 26: 957-968.
34. FRANK, R.N. (2004). Diabetic retinopathy. N Engl J Med 350: 48-58.
35. FRANK, R.N., AMIN, R.H., ELIOTT, D., PUKLIN, J.E. and ABRAMS, G.W. (1996). Basic fibroblast growth factor and vascular endothelial growth factor are present in epiretinal and choroidal neovascular membranes. Am J Ophthalmol 122: 393-403.
36. FRUTTIGER, M. (2002). Development of the mouse retinal vasculature: angiogenesis versus vasculogenesis. Invest Ophthalmol Vis Sci 43: 522-527.
37. FRUTTIGER, M., CALVER, A.R., KRUGER, W.H., MUDHAR, H.S., MICHALOVICH, D., TAKAKURA, N., NISHIKAWA, S. and RICHARDSON, W.D. (1996). PDGF mediates a neuron-astrocyte interaction in the developing retina. Neuron 17:1117-1131.
38. FUKAI, N., EKLUND, L., MARNEROS, A.G., OH, S.P., KEENE, D.R., TAMARKIN, L., NIEMELA, M., ILVES, M., LI, E., PIHLAJANIEMI, T. and OLSEN, B.R. (2002). Lack of collagen XVIII/endostatin results in eye abnormalities. EMBO J 21: 1535-1544.
39. GALAMBOS, C., NG, Y.S., ALI, A., NOGUCHI, A., LOVEJOY, S., D'AMORE, P.A. and DEMELLO, D.E. (2002). Defective pulmonary development in the absence of heparin-binding vascular endothelial growth factor isoforms. Am J Respir Cell Mol Biol 27:194-203.
40. GALE, N.W., THURSTON, G., HACKETT, S.F., RENARD, R., WANG, Q., MCCLAIN, J., MARTIN, C., WITTE, C., WITTE, M.H., JACKSON, D., SURI, C., CAMPOCHIARO, P.A., WIEGAND, S.J. and YANCOPOULOS, G.D. (2002). Angiopoietin-2 is required for postnatal angiogenesis and lymphatic patterning, and only the latter role is rescued by Angiopoietin-1. Dev Cell 3: 411-423.
41. GAO, G., LI, Y., ZHANG, D., GEE, S., CROSSON, C. and MA, J. (2001). Unbalanced expression of VEGF and PEDF in ischemia-induced retinal neovascularization. FEBS Lett 489: 270-276.
42. GARRETT, K.L., SHEN, W.Y. and RAKOCZY, P.E. (2001). In vivo use of oligonucleotides to inhibit choroidal neovascularisation in the eye. J Gene Med 3: 373-383.
43. GERBER, H.-P., HILLAN, K.J., RYAN, A.M., KOWALSKI, J., KELLER, G.A., RANGELL, L., WRIGHT, B.D., RADTKE, F., AGUET, M. and FERRARA, N. (1999). VEGF is required for growth and survival in neonatal mice. Development 126: 1149-1159.
44. GOGAT, K., LE GAT, L., VAN DEN BERGHE, L., MARCHANT, D., KOBETZ, A., GADIN, S., GASSER, B., QUERE, I., ABITBOL, M. and MENASCHE, M. (2004). VEGF and KDR gene expression during human embryonic and fetal eye development. Invest Ophthalmol Vis Sci 45: 7-14.
45. GOLDBERG, M.F. (1997). Persistent fetal vasculature (PFV): an integrated interpretation of signs and symptoms associated with persistent hyperplastic primary vitreous (PHPV). LIV Edward Jackson Memorial Lecture. Am J Ophthalmol 124: 587-626.
46. GRANT, M.B., MAY, W.S., CABALLERO, S., BROWN, G.A., GUTHRIE, S.M., MAMES, R.N., BYRNE, B.J., VAUGHT, T., SPOERRI, P.E., PECK, A.B. and SCOTT, E.W. (2002). Adult hematopoietic stem cells provide functional hemangioblast activity during retinal neovascularization. Nat Med 8: 607-612.
47. GREEN, W.R. and ENGER, C. (1993). Age-related macular degeneration histopathologic studies. The 1992 Lorenz E. Zimmerman Lecture. Ophthalmology 100: 1519-1535.
48. HACKETT, S.F., WIEGAND, S., YANCOPOULOS, G. and CAMPOCHIARO, P.A. (2002). Angiopoietin-2 plays an important role in retinal angiogenesis. J Cell Prtysiol 192: 182-187.
49. HELLSTROM, M., KALEN, M., LINDAHL, P., ABRAMSSON, A. and BETSHOLTZ, C. (1999). Role of PDGF-B and PDGFR-β in recruitment of vascular smooth muscle cells and pericytes during embryonic blood vessel formation in the mouse. Development 126: 3047-3055.
50. HIRSCHI, K., ROHOVSKY, S.A. and D'AMORE, P.A. (1998). PDGF, TGF-β and heterotypic cell-cell interactions mediate the recruitment and differentiation of 10T1/2 cells to a smooth muscle cell fate. J Cell Biol 141: 805-814.
51. HIRSCHI, K.K., ROHOVSKY, S.A., BECK, L.H., SMITH, S.R. and D'AMORE, P.A. (1999). Endothelial cells modulate the proliferation of mural cell precursors via platelet-derived growth factor-BB and heterotypic cell contact. Circ. Res. 84: 298-305.
52. HOLEKAMP, N.M., BOUCK, N. and VOLPERT, O. (2002). Pigment epithelium-derived factor is deficient in the vitreous of patients with choroidal neovascularization due to age-related macular degeneration. Am J Ophthalmol 134: 220-227.
53. HONDA, M., SAKAMOTO, T., ISHIBASHI, T., INOMATA, H. and UENO, H. (2000). Experimental subretinal neovascularization is inhibited by adenovirus-mediated soluble VEGF/flt-1 receptor gene transfection: a role of VEGF and possible treatment for SRN in age-related macular degeneration. Gene Ther: 978-985.
54. HOUCK, K.A., LEUNG, D.W., ROWLAND, A.M., WINER, J. and FERRARA, N. (1992). Dual regulation of vascular endothelial growth factor bioavailability by genetic and proteolytic mechanisms. J. Biol. Chem. 257: 26031-26037.
55. HUGHES, S., YANG, H. and CHAN-LING, T. (2000). Vascularization of the human fetal retina: roles of vasculogenesis and angiogenesis. Invest Ophthalmol Vis Sci 41: 1217-1228.
56. HUTCHINGS, H., MAITRE-BOUBE, M., TOMBRAN-TINK, J. and PLOUET, J. (2002). Pigment epithelium-derived factor exerts opposite effects on endothelial cells of different phenotypes. Biochem Biophys Res Commun 294: 764-769.
57. ISHIBASHI, T., HATA, Y., YOSHIKAWA, H., NAKAGAWA, K., SUEISHI, K. and INOMATA, H. (1997). Expression of vascular endothelial growth factor in experimental choroidal neovascularization. Graefes Arch Clin Exp Ophthalmol 235: 159-167.
58. ITO, M. and YOSHIOKA, M. (1999). Regression of the hyaloid vessels and pupillary membrane of the mouse. Anat Embryol 200: 403-411.
59. JANZER, R.C. and RAFF, M.C. (1987). Astrocytes induce blood-brain barrier properties in endothelial cells. Nature 325: 253-257.
60. KATO, M., PATEL, M.S., LEVASSEUR, R., LOBOV, I., CHANG, B.H., GLASS, D.A., 2ND, HARTMANN, C., LI, L., HWANG, T.H., BRAYTON, C.F., LANG, R.A., KARSENTY, G. and CHAN, L. (2002). Cbfa1-independent decrease in osteoblastproliferation, osteopenia, and persistent embryonic eye vascularization in mice deficient in Lrp5, a Wnt coreceptor. J Cell Biol 157: 303-314.
61. KEYT, B.A., BERLEAU, L.T., NGUYEN, H.V., CHEN, H., HEINSOHN, H., VANDLEN, R. and FERRARA, N. (1996). The carboxyl-terminal domain (111-165) of vascular endothelial growth factor is critical for its mitogenic potency. J. Biol. Chem. 271: 7788-7795.
62. KLIFFEN, M., SHARMA, H.S., MOOY, C.M., KERKVLIET, S. and DE JONG, P.T. (1997). Increased expression of angiogenic growth factors in age-related maculopathy. Br J Ophthalmol 81: 154-162.
63. KORTE, G.E., REPPUCCI, V. and HENKIND, P. (1984). RPE destruction causes choriocapillary atrophy. Invest Ophthalmol Vis Sci 25: 1135-1145.
64. KRZYSTOLIK, M.G., AFSHARI, M.A., ADAMIS, A.P., GAUDREAULT, J., GRAGOUDAS, E.S., MICHAUD, N.A., LI, W., CONNOLLY, E., O'NEILL, C.A. and MILLER, J.W. (2002). Prevention of experimental choroidal neovascularization with intravitreal anti-vascular endothelial growth factor antibody fragment. Arch Ophthalmol 120: 338-346.
65. KVANTA, A., ALGVERE, P.V., BERGLIN, L. and SEREGARD, S. (1996). Subfoveal fibrovascular membranes in age-related macular degeneration express vascular endothelial growth factor. Invest Ophthalmol Vis Sci 37: 1929-1934.
66. LANG, R., LUSTIG, M., FRANCOIS, F., SELLINGER, M. and PLESKEN, H. (1994). Apoptosis during macrophase-dependent ocular tissue remodelling. Development 120: 3395-3403.
67. LANG, R.A. and BISHOP, J.M. (1993). Macrophages are required for cell death and tissue remodeling in the developing mouse eye. Cell 74: 453-462.
68. LEONARD, D.S., SUGINO, I.K., ZHANG, X.G., NINOMIYA, Y., YAGI, F., TSUKAHARA, I., CASTELLARIN, A. and ZARBIN, M.A. (2003). Ultrastructural analysis of hydraulic and abrasive retinal pigment epithelial cell debridements. Exp Eye Res 76: 473-491.
69. LEUNG, D.W., CACHIANES, G., KUANG, W.-J., GOEDDEL, D.V. and FERRARA, N. (1989). Vascular endothelial growth factor is a secreted angiogenic mitogen. Science 246: 1306-1309.
70. LINDAHL, P., JOHANSSON, B.R., LEVEEN, P. and BETSHOLTZ, C. (1997). Pericyte loss and microaneurysm formation in PDGF-B-deficient mice. Science 277: 242-245.
71. LOPEZ, P.F., SIPPY, B.D., LAMBERT, H.M., THACH, A.B. and HINTON, D.R. (1996). Transdifferentiated retinal pigment epithelial cells are immunoreactive for vascular endothelial growth factor in surgically excised age-related macular degeneration-related choroidal neovascular membranes. Invest Ophthalmol Vis Sci 37: 855-868.
72. LORENZI, M. and GERHARDINGER, C. (2001). Early cellular and molecular changes induced by diabetes in the retina. Diabetologia 44: 791-804.
73. MAISONPIERRE, P.C., SURI, C., JONES, P.F., BARTUNKOVA, S., WIEGAND, S.J., RADZIEJEWSKI, C., COMPTON, D., MCCLAIN, J., ALDRICH, T.H., PAPADOPOULOS, N., DALY, T.J., DAVIS, S., SATO, T.N. and YANCOPOULOS, G.D. (1997). Angiopoietin-2, a natural anatognist for Tie2 that disrupts in vivo angiogenesis. Science 277: 55-60.
74. MALECAZE, F., CLAMENS, S., SIMORRE-PINATEL, V., MATHIS, A.,CHOLLET, P., FAVARD, P., BAYARD, F. and PLOUET, J. (1994). Detection of vascular endothelial growth factor messenger RNA and vascular endothelial growth factor-like activity in proliferative diabetic retinopathy. Lab. Sci. 112: 1476-1482.
75. MAXWELL, P.H. and RATCLIFFE, P.J. (2002). Oxygen sensors and angiogenesis. Semin Cell Dev Biol 13: 29-37.
76. MCKELLER, R.N., FOWLER, J.L., CUNNINGHAM, J.J., WARNER, N., SMEYNE, R.J., ZINDY, F. and SKAPEK, S.X. (2002). The Art tumor suppressor gene promotes hyaloid vascular regression during mouse eye development. Proc Natl Acad Sci USA 99: 3848-3853.
77. MCLEOD, D.S., LUTTY, G.A., WAJER, S.D. and FLOWER, R.W. (1987). Visualization of a developing vasculature. Microvasc Res 33: 257-269.
78. MCLEOD, D.S., TAOMOTO, M., OTSUJI, T., GREEN, W.R., SUNNESS, J.S. and LUTTY, G.A. (2002). Quantifying changes in RPE and choroidal vasculature in eyes with age-related macular degeneration. Invest Ophthalmol Vis Sci 43:1986-1993.
79. MEESON, A., PALMER, M., CALFON, M. and LANG, R. (1996). A relationship between apoptosis and flow during programmed capillary regression is revealed by vital analysis. Development 122: 3929-3938.
80. MEESON, A.P., ARGILLA, M., KO, K., WITTE, L. and LANG, R.A. (1999). VEGF deprivation-induced apoptosis is acomponent of programmed capillary regression. Development 126: 1407-1415.
81. MICHAELSON, I.C., HERZ, N., LEWKOWITZ, E. and KERTESZ, D. (1954). Effect of increased oxygen on the development of the retinal vessels. Brit. J. Ophthal. 38: 577-587.
82. MILLER, H., MILLER, B. and RYAN, S.J. (1986). The role of retinal pigment epithelium in the involution of subretinal neovascularization. Invest Ophthalmol Vis Sci 27: 1644-1652.
83. MILLER, J.W., ADAMIS, A.P., SHIMA, D.T., D'AMORE, P.A., MOULTON, R.S., O'REILLY, M.S., FOLKMAN, J., DVORAK, H.F., BROWN, L.F., BERSE, B., YEO, T.-K. and YEO, K.-T. (1994). Vascular permeability factor/vascular endothelial cell growth factor is temporally and spatially correlated with ocular angiogenesis in a primate model. Am. J. Pathol. 145: 574-584.
84. MITCHELL, C.A., RISAU, W. and DREXLER, H.C. (1998). Regression of vessels in the tunica vasculosa lentis is initiated by coordinated endothelial apoptosis: a role for vascular endothelial growth factor as a survival factor for endothelium. Dev Dyn 213: 322-333.
85. MOORE, D.J., HUSSAIN, A.A. and MARSHALL, J. (1995). Age-related variation in the hydraulic conductivity of Bruch's membrane. Invest Ophthalmol Vis Sci 36: 1290-1297.
86. NAKAMURA, H. (1988). Electron microscopic study of the prenatal development of the thoracic aorta in the rat. Am. J. Anal 181: 406-418.
87. NG, Y.-S., ROHAN, R., SUNDAY, M., DEMELLO, D.E. and D'AMORE, P.A. (2001). Differential expression of VEGF isoforms in mouse during development and in the adult. Dev Dyn 220: 112-121.
88. NODEN, D.M. (1989). Embryonic origins and assembly of blood vessels. Am. Rev. Respir. Dis. 140: 1097-1103.
89. OGATA, N., MATSUSHIMA, M., TAKADA, Y., TOBE, T., TAKAHASHI, K., YI, X., YAMAMOTO, C., YAMADA, H. and UYAMA, M. (1996). Expression of basic fibroblast growth factor mRNA in developing choroidal neovascularization. Curr Eye Res 15: 1008-1018.
90. OGATA, N., WADA, M., OTSUJI, T., JO, N., TOMBRAN-TINK, J. and MATSUMURA, M. (2002). Expression of pigment epithelium-derived factor in normal adult rat eye and experimental choroidal neovascularization. Invest Ophthalmol Vis Sci 43: 1168-1175.
91. OTANI, A., KINDER, K., EWALT, K., OTERO, F.J., SCHIMMEL, P. and FRIEDLANDER, M. (2002). Bone marrow-derived stem cells target retinal astrocytes and can promote or inhibit retinal angiogenesis. Nat Med 8: 1004-1010.
92. OZAKI, H., HAYASHI, H., VINORES, S.A., MOROMIZATO, Y., CAMPOCHIARO, P. and OSHIMA, K. (1997). Intravitreal sustained release of VEGF causes retinal neovascularization in rabbits and breakdcwn of the blood-retinal barrier in rabbits and primates. Exp Eye Res 4: 505-517.
93. PARDANAUD, L., YASSINE, F. and DIETERLEN-LIEVRE, F. (1989). Relationship between vasculogenesis, angiogenesis and haemopoiesis during avian ontogeny. Development 105: 473-485.
94. PEROU, C., JEFFREY, S., VAN DE RUN, M., REES, C., EISEN, M., ROSS, D., PERGAMENSCHIKOV, A., WILLIAMS, C., ZHU, S., LEE, J., D.L., SHALON, D., BROWN, P. and BOTSTEIN, D. (1999). Distinctive gene expression patterns in human mammary epithelial cells and breast cancers. Proc Natl Acad Sci USA 96: 9212-9217.
95. PIERCE, E.A., AVERY, R.L., FOLEY, E.D., AIELLO, L.P. and SMITH, L.E.H. (1995). Vascular endothelial growth factor/vascular permeability factor expression in a mouse model of retinal neovascularization. Proc. Natl. Acad. Sci. USA 92: 905-909.
96. PROVIS, J.M., LEECH, J., DIAZ, C.M., PENFOLD, P.L., STONE, J. and KESHET, E. (1997). Development of the human retinal vasculature: cellular relations and VEGF expression. Exp Eye Res 65: 555-568.
97. PROVIS, J.M., SANDERCOE, T. and HENDRICKSON, A.E. (2000). Astrocytes and blood vessels define the foveal rim during primate retinal development. Invest Ophthalmol Vis Sci 41: 2827-2836.
98. RAFII, S. and LYDEN, D. (2003). Therapeutic stem and progenitor cell transplantation for organ vascularization and regeneration. War Med 9: 702-712.
99. RAFII, S., MEEUS, S., DIAS, S., HATTORI, K., HEISSIG, B., SHMELKOV, S., RAFII, D. and LYDEN, D. (2002). Contribution of marrow-derived progenitors to vascular and cardiac regeneration. Semin Cell Dev Biol 13: 61-67.
100. RAMRATTAN, R.S., VAN DER SCHAFT, T.L., MOOY, C.M., DE BRUIJN, W.C., MULDER, P.G. and DE JONG, P.T. (1994). Morphometric analysis of Bruch's membrane, the choriocapillaris, and the choroid in aging. Invest Ophthalmol Vis Sci 35: 2857-2864.
101. RENNO, R.Z., YOUSSRI, A.I., MICHAUD, N., GRAGOUDAS, E.S. and MILLER, J.W. (2002). Expression of pigment epithelium-derived factor in experimental choroidal neovascularization. Invest Ophthalmol Vis Sci 43: 1574-1580.
102. ROBERTS, W.G. and PALADE, G.E. (1995). Increased microvascular permeability and endothelial fenestration induced by vascular endothelial growth factor. J. Cell Sci. 108: 2369-2379.
103. ROUSSEAU, B., LARRIEU-LAHARGUE, F., BIKFALVI, A. and JAVERZAT, S. (2003). Involvement of fibroblast growth factors in choroidal angiogenesis and retinal vascularization. Exp Eye Res 77: 147-156.
104. SAKAMOTO, T., SAKAMOTO, H., MURPHY, T.L., SPEE, C., SORIANO, D., ISHIBASHI, T., HINTON, D.R. and RYAN, S.J. (1995). Vessel formation by choroidal endothelial cells in vitro is modulated by retinal pigment epithelial cells. Arch Ophthalmol 113: 512-520.
105. SARKS, J.P., SARKS, S.H. and KILLINGSWORTH, M.C. (1988). Evolution of geographic atrophy of the retinal pigment epithelium. Eye 2 (Pt 5): 552-577.
106. SARKS, S.H. (1976). Ageing and degeneration in the macular region: a clinico-pathological study. Br J Ophthalmol 60: 324-341.
107. SCHWESINGER, C., YEE, C., ROHAN, R.M., JOUSSEN, A.M., FERNANDEZ, A., MEYER, T.N., POULAKI, V., MA, J.J., REDMOND, T.M., LIU, S., ADAMIS, A.P. and D'AMATO, R.J. (2001). Intrachoroidal neovascularization in transgenic mice overexpressing vascular endothelial growth factor in the retinal pigment epithelium. Am. J. Pathol. 158: 1161-1172.
108. SELLHEYER, K. and SPITZNAS, M. (1987). Ultrastructure of the human posterior tunica vasculosa lentis during early gestation. Graefes Arch Clin Exp Ophthalmol 225: 377-383.
109. SENGER, D.R., GALLI, S.J., DVORAK, A.M., PERUZZI, C.A., HARVEY, V.S. and DVORAK, H.F. (1983). Tumor cells secrete a vascular permeability factor that promotes accumulation of ascites fluid. Science 219: 983-985.
110. SHEN, W.Y., YU, M.J., BARRY, C.J., CONSTABLE, I.J. and RAKOCZY, P.E. (1998). Expression of cell adhesion molecules and vascular endothelial growth factor in experimental choroidal neovascularisation in the rat. Br J Ophthalmol 82: 1063-1071.
111. SHIMA, D.T., GOUGOS, A., MILLER, J.W., TOLENTINO, M., ROBINSON, G., ADAMIS, A.P. and D'AMORE, P.A. (1996). Cloning and mRNA expression of vascular endothelial growth factor in ischemic retinas of Macaca fasicularis. Invest. Ophthalmol. Vis. Sci. 37: 1334-1347.
112. SHIMA, D.T., KUROKI, M., DEUTSCH, U., NG, Y.-S., ADAMIS, A.P. and D'AMORE, P.A. (1996). The mouse gene for vascular endothelial growth factor. Genomic structure, definition of the transcriptional unit and characterization of transcriptional and post-transcriptional regulatory sequences. J. Biol. Chem. 271: 3877-3883.
113. SHUI, Y.B., WANG, X., HU, J.S., WANG, S.P., GARCIA, C.M., POTTS, J.D., SHARMA, Y. and BEEBE, D.C. (2003). Vascular endothelial growth factor expression and signaling in the lens. Invest Ophthalmol Vis Sci 44: 3911-3919.
114. SMITH, L.E.H., WESLOWSKI, E., MCLELLAN, A., KOSTYK, S.K., D'AMATO, R., SULLIVAN, R. and D'AMORE, P.A. (1994). Oxygen-induced retinopathy in the mouse. Invest. Ophthalmol. Vis. Sci. 35: 101-111.
115. SOKER, S., FIDDER, H., NEUFELD, G. and KLAGSBRUN, M. (1996). Characterization of novel vascular endothelial growth factor (VEGF) receptors on tumor cells that bind VEGF165 via its exon 7-encoded domain. J. Biol. Chem. 271: 5761-5767.
116. SPILSBURY, K., GARRETT, K.L., SHEN, W.Y., CONSTABLE, I.J. and RAKOCZY, P.E. (2000). Overexpression of vascular endothelial growth factor (VEGF) in the retinal pigment epithelium leads to the development of choroidal neovascularization. Am. J. Pathol. 157: 135-144.
117. STALMANS, I., NG, Y.S., ROHAN, R., FRUTTIGER, M., BOUCHE, A., YUCE, A., FUJISAWA, H., HERMANS, B., SHANI, M., JANSEN, S., HICKLIN, D., ANDERSON, D.J., GARDINER, T., HAMMES, H.P., MOONS, L., DEWERCHIN, M., COLLEN, D., CARMELIET, P. and D'AMORE, P.A. (2002). Arteriolar and venular patterning in retinas of mice selectively expressing VEGF isoforms. J Clin Invest 109: 327-336.
118. STONE, J., CHAN-LING, T., J., P.E., ITIN, A., GNESSIN, H. and KESHET, E. (1996). Roles of vascular endothelial growth factor and astrocyte degeneration in the genesis of retinopathy of prematurity. Invest. Ophthal. Vis. Sci. 37: 290-299.
119. STONE, J., ITIN, A., ALON, T., PE'ER, J., GNESSIN, H., CHAN-LING, T. and KESHET, E. (1995). Development of retinal vasculature is mediated by hypoxia-induced vascular endothelial growth factor (VEGF) expression by neuroglia. J. Neurosci. 15: 4738-4747.
120. SURI, C., JONES, P.F., PATAN, S., BARTUNKOVA, S., MAISONPIERRE, P.C., DAVIS, S., SATO, T.N. and YANCOPOULOS, G.D. (1996). Requisite role of angiopoietin-1, a ligand for the TIE2 receptor, during embryonic angiogenesis. Cell 87: 1171-1180.
121. TAKAHASHI, T., NAKAMURA, T., HAYASHI, A., KAMEI, M., NAKABAYASHI, M., OKADA, A.A., TOMITA, N., KANEDA, Y. and TANO, Y. (2000). Inhibition of experimental choroidal neovascularization by overexpression of tissue inhibitor of metalloproteinases-3 in retinal pigment epithelium cells. Am J Ophthalmol 130: 774-781.
122. TISCHER, E., MITCHELL, R., HARTMAN, T., SILVA, M., GOSPODAROWICZ, D., FIDDES, J.C. and ABRAHAM, J.A. (1991). The human gene for vascular endothelial growth factor. Multiple proteins are encoded through alternative exon splicing. J. Biol. Chem. 266: 11947-11954.
123. TOBE, T., ORTEGA, S., LUNA, J.D., OZAKI, H., OKAMOTO, N., DEREVJANIK, N.L., VINORES, S.A., BASILICO, C. and CAMPOCHIARO, P.A. (1998). Targeted disruption of the FGF2 gene does not prevent choroidal neovascularization in a murine model. Am. J. Pathol. 153: 1641-1646.
124. TORCZYNSKI, E. (1982). Choroid and suprachoroid. Ocular anatomy, embryology and teratology. FA, J. Philadelphia, Harper & Row: 553-585.
125. TOUT, S., CHAN-LING, T., HOLLANDER, H. and STONE, J. (1993). The role of Muller cells in the formation of the blood-retinal barrier. Neuroscience 55: 291-301.
126. VIRDI, P.S. and HAYREH, S.S. (1982). Ocular neovascularization with retinal vascular occlusion I. Association with experimental retinal vein occlusion. Arch. Ophthalmol. 100: 331-341.
127. WANG, F., RENDAHL, K.G., MANNING, W.C., QUIROZ, D., COYNE, M. and MILLER, S.S. (2003). AAV-mediated expression of vascular endothelial growth factor induces choroidal neovascularization in rat. Invest Ophthalmol Vis Sci 44: 781-790.
128. XU, Q., WANG, Y., DABDOUB, A., SMALLWOOD, P.M., WILLIAMS, J., WOODS, C., KELLEY, M.W., JIANG, L., TASMAN, W., ZHANG, K. and NATHANS, J. (2004). Vascular development in the retina and inner ear: control by Norrin and Frizzled-4, a high-affinity ligand-receptor pair. Cell 116: 883-895.
129. YAMADA, H., YAMADA, E., KWAK, N., ANDO, A., SUZUKI, A., ESUMI, N., ZACK, D.J. and CAMPOCHIARO, P.A. (2000). Cell injury unmasks a latent proangiogenic phenotype in mice with increased expression of FGF2 in the retina. J Cell Physiol 185: 135-142.
130. YI, X., MAI, L.C., UYAMA, M. and YEW, D.T. (1998). Time-course expression of vascular endothelial growth factor as related to the development of the retinochoroidal vasculature in rats. Exp Brain Res 118: 155-160.
131. YOUNG, R.W. (1987). Pathophysiology of age-related macular degeneration. Surv Ophthalmol 31: 291-306.
132. ZHAO, S. and OVERBEEK, P.A. (2001). Regulation of choroid development by the retinal pigment epithelium. Mol Vis 7: 277-282.
133. ZHU, W.H., GUO, X., VILLASCHI, S. and FRANCESCO NICOSIA, R. (2000). Regulation of vascular growth and regression by matrix metalloproteinases in the rat aorta model of angiogenesis. Laboratory Investigation 80: 545-555.