Retinal vascular development and oxygen-induced retinopathy: A role for adenosine

Progress in Retinal and Eye Research

Volumn 22, Issue 1, 2003, Pages 95-111

  Lutty, Gerard A ^a   McLeod, D Scott ^a  

^a JOHNS HOPKINS UNIVERSITY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

5 AMINO 2 (2 FURYL) 7 (2 PHENYLETHYL)PYRAZOLO[4,3 E][1,2,4]TRIAZOLO[1,5 C]PYRIMIDINE; 5' NUCLEOTIDASE; 8 CYCLOPENTYLTHEOPHYLLINE; ADENOSINE; ADENOSINE A2A RECEPTOR; ADENOSINE RECEPTOR; ADENOSINE TRIPHOSPHATE; ALPHA TOCOPHEROL; ANTISENSE OLIGONUCLEOTIDE; N(G) NITROARGININE; NUCLEOSIDE; OXYGEN; VASCULOTROPIN; VASCULOTROPIN ANTIBODY;

AMBIENT AIR; ANGIOGENESIS; BLOOD VESSEL; BRAIN; BRAIN HEMORRHAGE; CATABOLISM; CELL PROLIFERATION; CLINICAL TRIAL; DISEASE COURSE; DISEASE MODEL; DOG; DRUG TARGETING; ENDOTHELIUM CELL; ENZYME ACTIVITY; EXPOSURE; EYE; HUMAN; HYPOXIA; ISCHEMIA; MUELLER CELL; NEOVASCULARIZATION (PATHOLOGY); NERVE GROWTH; NONHUMAN; OXYGEN CONSUMPTION; PERINATAL DEVELOPMENT; POSTNATAL DEVELOPMENT; PRIORITY JOURNAL; PROTEIN EXPRESSION; RETINA; RETINA BLOOD VESSEL; RETINA DEVELOPMENT; RETINOPATHY; RETROLENTAL FIBROPLASIA; REVIEW; STEM CELL;

ADENOSINE; ANIMALS; ANIMALS, NEWBORN; DISEASE MODELS, ANIMAL; DOGS; ENDOTHELIAL GROWTH FACTORS; HUMANS; INFANT, NEWBORN; INTERCELLULAR SIGNALING PEPTIDES AND PROTEINS; LYMPHOKINES; MICE; OXYGEN; RECEPTORS, PURINERGIC P1; RETINAL NEOVASCULARIZATION; RETINOPATHY OF PREMATURITY; VASCULAR ENDOTHELIAL GROWTH FACTOR A; VASCULAR ENDOTHELIAL GROWTH FACTORS;

EID: 0037280139     PISSN: 13509462     EISSN: None     Source Type: Journal    
DOI: 10.1016/S1350-9462(02)00058-7     Document Type: Review

References (136)

1. 3 receptors in rat brain. Mol. Pharmacol. 48:1995;1038-1045.
2. 1 adenosine receptor mediated Ins(1,4,5)P3 generation in allergic rabbitairway smooth muscle. Am. J. Physiol. 275:1998;L990-L997.
3. Afzal, A., Shaw, L.C., Caballero, S., Ellis, E.A., Grant, M. B., 2002. The development of hammerhead ribozymes that specifically cleave the A2B receptor mRNA. Invest. Ophthalmol. Vis. Sci. 43 (ARVO abstract #3711).
4. Aiello L.P., Pierce E.A., Foley E.D., Takagi H., Chen H., Riddle L., Ferrara N., King G.L., Smith L.E.H. Suppression of retinal neovascularization in vivo by inhibition of vascular endothelial growth factor (VEGF) using soluble VEGF-receptor chimeric proteins. Proc. Nat. Acad. Sci., USA. 92:1995;10457-10461.
5. Alon T., Hemo I., Itin A., Pe'er J., Stone J., Keshet E. Vascular endothelial growth factor acts as a survival factor for newly formed retinal vessels and has implications for retinopathy of pretmaturity. Nature Med. 1:1995;1024-1028.
6. Andersen, C.C., Phelps, D.L., 2000. Peripheral retinal ablation for threshold retinopathy of prematurity in preterm infants. Cochrane Database System Rev. CD001693.
7. Ashton N., Ward B., Serpell G. Effect of oxygen on developing retinal vessels with particular reference to the problem of retrolental fibroplasia. Br. J. Ophthalmol. 38:1954;397-428.
8. Berne R., Knabb R., Ely S.W., Rubio R. Adenosine in the local regulation of blood flow. a brief overview Federation Proc. 42:1983;3136-3142.
9. 1 receptor-mediated inhibition of adenylate cyclase in rabbit retina. J. Neurosci. 7:1987;2522-2528.
10. Blazynski C., Perez M.-T.R. Neuroregulatory functions of adenosine in the retina. Prog. Retinal Res. 11:1992;293-332.
11. Blazynski C., Mosinger J.L., Cohen A.I. Comparison of adenosine uptake and endogenous adenosine-containing cells in mammalian retina. Vis. Neurosci. 2:1989;109-116.
12. Braas K.M., Zarbin M.A., Snyder S.H. Endogenous adenosine and adenosine receptors localized to ganglion cells of the retina. Proc. Nat. Acad. Sci., USA. 84:1987;3906.
13. Braun N., Brendel P., Zimmerman H. Distribution of 5′-nucleotidase in the developing mouse retina. Brain Res. 88:1995;79-86.
14. Braun N., Lenz C., Gillardon F., Zimmerman M., Zimmerman H. Focal cerebral ischemia enhances glial expression of ecto-5′-nucleotidase. Brain Res. 766:1997;213-226.
15. Breier G., Albrecht U., Sterrer S., Risau W. Expression of vascular endothelial growth factor during embryonic angiogenesis and endothelial cell differentiation. Development. 114:1992;521-532.
16. Brooks S.E., Gu X., Samuel S., Marcus D.M., Bartoli M., Huang P.L., Caldwell R.B. Reduced severity of oxygen-induced retinopathy in eNOS-deficient mice. Invest. Ophthalmol. Vis. Sci. 42:2001;222-228.
17. Chan-Ling T., Gock B., Stone J. The effect of oxygen on vasoformative cell division. Evidence that 'physiological hypoxia' is the stimulus for normal retinal vasculogenesis. Invest. Ophthalmol. Vis. Sci. 36:1995;1201-1214.
18. Chan-Ling T., Tout S., Holländer H., Stone J. Vascular changes and their mechanisms in the feline model of retinopathy of prematurity. Invest. Ophthalmol. Vis. Sci. 33(7):1992;2128-2147.
19. Chen Y.-F., Li P.-L., Zou A.-P. Oxidative stress enhances the production and actions of adenosine in the kidney. Am. J. Physiol. Regul. Integ. Comp. Physiol. 281:2001;R1808-R1816.
20. Cleaver O., Krieg P.A. VEGF mediates angioblast migration during development of the dorsal aorta in Xenopus. Development. 125:1998;3905-3914.
21. DeVries C., Escobeido J., Ueno H., Houck K., Ferrara N., Williams L.T. The fms-like tyrosine kinase, a receptor for vascular endothelial growth factor. Science. 255:1992;989-991.
22. Donahue M.L., Phelps D.L., Watkins R.H., LoMonaco M.B., Horowitz S. Retinal vascular endothelial growth factor (VEGF) mRNA expression is altered in relation to neovascularization in oxygen-induced retinopathy. Curr. Eye Res. 15:1996;175-184.
23. Dorey C.K., Aouididi S., Reynaud X., Dvorak H., Brown L.F. Correlation of vascular permeability factor/vascular endothelial growth factor with extraretinal neovascularization in rat. Arch. Ophthalmol. 114:1996;1210-1217.
24. Dubey R.K., Gillespie D.G., Jackson E.K. A(2B) adenosine receptors stimulate growth of porcine and rat arterial endothelial cells. Hypertension. 39(2 Pt 2):2002;530-535.
25. Dunwiddie T.V., Fredholme B. Adenosine neuromolulation. Jacobsen K.A., Jarvis M. Purinergic Approaches in Experimental Therapeutics. 1998;359-382 Wiley-Liss, New York.
26. Dusseau J.W., Hutchins P.M. Hypoxia-induced angiogenesis in chick chorioallantoic membranes. a role for adenosine Respir. Physiol. 71:1988;33-44.
27. Dvorak H.F., Brown L.F., Detmar M., Dvorak A.M. Vascular permeability factor/vascular endothelial growth factor, microvascular hyperpermeability, and angiogenesis. Am. J. Pathol. 146(5):1995;1029-1039.
28. Feoktistov I., Goldstein A.E., Ryzhov S., Zeng D., Belardinelli L., Voyno-Yasenetskaya T., Biaggioni I. Differential expression of adenosine receptors in human endothelial cells. role of A2B receptors in angiogenic factor regulation Circ. Res. 90(5):2002;531-538.
29. Ferrara N., Henzel W.J. Pituitary follicular cells secrete a novel heparin-binding growth factor specific for vascular endothelial cells. Biochem. Biophys. Res. Commun. 161:1989;851-858.
30. Fischer S., Sharma H.S., Kaliczek G.F., Schaper W. Expression of vascular permeability factor/vascular endothelial growth factor in pig cerebral microvascular endothelial cells and its upregulation by adenosine. Mol. Brain Res. 28:1995;141-148.
31. Flamme I., Breier G., Risau W. Vascular endothelial growth factor (VEGF) and VEGF receptor 2 (flk-1) are expressed during vasculogenesis and vascular differentiation in the quail embryo. Dev. Biol. 169:1995;699-712.
32. Flower R.W., McLeod D.S., Lutty G.A., Goldberg B., Wajer S.D. Postnatal retinal vascular development of the puppy. Invest. Ophthal. Vis. Sci. 26:1985;957-968.
33. Forsythe J.A., Jiang B., Iyer N.V., Agani F., Leung S.W., Koos R.D., Semenza G.L. Activation of vascular endothelial growth factor gene transcription by hypoxia-inducible factor 1. Mol. Cell. Biol. 16:1996;4604-4613.
34. a-3. J. Biol. Chem. 266:1991;17778-17783.
35. Fruttiger M. Development of the mouse retinal vasculature. angiogenesis versus vasculogenesis Invest. Ophthalmol. Vis. Sci. 43:2002;522-527.
36. Gariano R.F., Iruela-Arispe M.L., Sage E.H., Hendrickson A.E. Immunohistochemical characterization of developing and mature primate retinal blood vessels. Invest. Ophthalmol. Vis. Sci. 37:1996;93-103.
37. Gariano R.F., Kalina R.E., Hendrickson A.E. Normal and pathological mechanisms in retinal vascular development. Surv. Ophthalmol. 40(6):1996;481-490.
38. Gariano R.F., Sage E.H., Kaplan H.J., Hendrickson A.E. Development of astrocytes and their relation to blood vessels in fetal monkey retina. Invest. Ophthalmol. Vis. Sci. 37(12):1996;2367-2375.
39. Ghiardi G.J., Gidday J.M., Roth S. The purine nucleoside adenosine in retinal uschemia-reperfusion injury. Vis. Res. 39:1999;2519-2535.
40. Gidday J.M., Park T.S. Adenosine-mediated autoregulation of retinal arteriolar tone in the piglet. Invest. Ophthalmol. Vis. Sci. 34:1993;2713-2719.
41. Gidday J.M., Park T.S. Microcirculatory responses to adenosine in the newborn pig. Pediatr. Res. 33:1993;620-627.
42. Gole G.A. Animal models of retinopathy of prematurity. Silverman W.A., Flynn J.T. Retinopathy of Prematurity. 1985;53-95 Blackwell Scientific Publications, Boston.
43. Grant M.B., Davis M.I., Caballero S., Feoktistov I., Biaggioni I., Belardinelli L. Proliferation, migration, and ERK activation in human retinal endothelial cells through A(2B) adenosine receptor stimulation. Invest. Ophthalmol. Vis. Sci. 42(9):2001;2068-2073.
44. Grant M.B., Tarnuzzer R.W., Cabalerro S., Ozeck M.J., Davis M.I., Spoerri P.E., Feoktistov I., Biaggioni I., Shryock J.C., Belardinelli L. Adenosine receptor activation induces vascular endothelial growth factor in human endothelial cells. Circ. Res. 85:1999;699-706.
45. Hughes S., Yang H., Chan-Ling T. Vascularization of the human fetal retina. roles of vasculogenesis and angiogenesis Invest. Ophthalmol. Vis. Sci. 41:2000;1217-1228.
46. Jakeman L.B., Armanini M., Phillips H.S., Ferrara N. Developmental expression of binding sites and messenger ribonucleic acid for vascular endothelial growth factor suggests a role for this protein in vasculogenesis and angiogenesis. Endocrinology. 133:1993;848-859.
47. Kappel A., Ronicke V., Damert A., Flamme I., Risau W., Breier G. Identification of vascular endothelial growth factor (VEGF) receptor-2 (Flk-1) promoter/enhancer sequences sufficient for angioblast and endothelial cell-specific transcription in transgenic mice. Blood. 93:1999;4284-4292.
48. Keck P.J., Hauser S.D., Krivi G., Sanzo K., Warren T., Feder J., Connolly D.T. Vascular permeability factor/an endothelial cell mitogen related to PDGF. Science. 246:1989;1309-1312.
49. Kitakaze M., Hori M., Takashima S., Iwai K., Sato H., Inoue M., Kitabatake A., Kamada T. Superoxide dismutase enhances ischemia-induced reactive hyperemic flow and adenosine release in dogs. Circ. Res. 71:1992;558-566.
50. Kitakaze M., Hori M., Kamada T. Role of adenosine and its interaction with alpha adrenoceptor activity in ischaemic and reperfusion injury of the myocardium. Cardiovas. Res. 27:1993;18-27.
51. Kitakaze M., Hori M., Morioka T., Takashima S., Minamino T., Sato H., Inoue M., Kamada T. Attenuation of ecto-S'-nucleotidase activity and adenosine release in activated human polymorphonuclear leukocytes. Circ. Res. 73:1993;524-533.
52. Kliche S., Waltenburg J. VEGF receptor signaling and endothelial function. IUBMB Life. 52:2001;61-66.
53. Kreutzberg G.W., Hussain S.T. Cytochemical heterogeneity of the glial plasma membrane. 5′-nucleotidase in retinal müller cells J. Neurocytol. 11:1982;53-64.
54. Kroll J., Waltenberger J. A novel function of VEGF receptor-2 (KDR). rapid release of nitric oxide in response to VEGF-a stimulation in endothelial cells Biochem. Biophys. Res. Commun. 30:1999;636-639.
55. Larsen A.K., Osbourne N.N. Involvement of adenosine in retinal ischemia. Studies on rat. Invest. Ophthalmol. Vis. Sci. 37:1996;2603-2611.
56. Lewis C.D., Hourani S.M., Long C.J., Collis M.G. Characterization of adenosine receptors in the rat isolated aorta. Gen. Pharmacol. 25:1994;1381-1387.
57. Li B., Roth S. Retinal preconditioning in the rat. requirement for adenosine and repetitive induction Invest. Ophthalmol. Vis. Sci. 40:1999;1200-1216.
58. 2a receptors. Neurochem. Res. 25:2000;457-459.
59. Li B., Rosenbaum P.S., Jennings N.M., Maxwell K.A., Roth S. Differential roles of adenosine receptor subtypes in retinal ischemia-reperfusion injury in the rat. Exp. Eye Res. 68:1999;9-17.
60. ATP channel. Am. J. Physiol. 271:1996;H1769-H1777.
61. Linden J. Molecular approach to adensoine receptors. receptor-mediated mechanisms of tissue protection Ann. Rev. Pharmacol. Toxicol. 41:2001;775-787.
62. Lutty G.A., McLeod D.S. A new technique for visualization of the human retinal vasculature. Arch. Ophthalmol. 110:1992;267-276.
63. Lutty G.A., Mathews M.K., Merges C., McLeod D.S. Adenosine stimulates canine retinal microvascular endothelial cell migration and tube formation. Curr. Eye Res. 17(6):1998;594-607.
64. Lutty G.A., Merges C., McLeod D.S. 5′ Nucleotidase and adenosine during retinal vasculogenesis and oxygen-induced retinopathy. Invest. Ophthalmol. Vis. Sci. 2000;41.
65. Lutty, G.A., McLeod, D.S., Hughes, S., Chu, Y., Baxter, L., Chan-Ling, T., 2002. Astrocyte-endothelial interactions during human retinal vasculogenesis. Invest. Ophthalmol. Vis. Sci. 43 (ARVO abstract #1934).
66. 2a receptors in human and porcine cardiovascular tissue. J. Pharmacol. Exp. Ther. 286:1998;1051-1057.
67. Maxwell P.H.R.P.J. Oxygen sensors and angiogenesis. Sem. Cell Dev. Biol. 13(1):2002;29-37.
68. McLeod D.S., Lutty G.A. High resolution histologic analysis of the human choroidal vasculature. Invest. Ophthalmol. Vis. Sci. 35:1994;3799-3811.
69. McLeod D.S., Lutty G.A. Menadione-dependent alpha glycerophosphate and succinate dehydrogenases in the developing canine retina. Curr. Eye Res. 14:1995;819-826.
70. McLeod D.S., Lutty G.A., Wajer S.D., Flower R.W. Visualization of a developing vasculature. Microvasc Res. 33(2):1987;257-269.
71. McLeod D.S., Brownstein R., Lutty G.A. Vaso-obliteration in the canine model of oxygen-induced retinopathy. Invest. Ophthalmol. Vis. Sci. 37:1996;300-311.
72. McLeod D.S., Crone S.N., Lutty G.A. Vasoproliferation in the neonatal dog model of oxygen-induced retinopathy. Invest. Ophthalmol. Vis. Sci. 37(7):1996;1322-1333.
73. McLeod D.S., D'Anna S.A., Lutty G.A. Clinical and histopathologic features of canine oxygen-induced proliferative retinopathy. Invest. Ophthalmol. Vis. Sci. 39(10):1998;1918-1932.
74. McLeod D.S., Taomoto M., Cao J., Zhu Z., Witte L., Lutty G.A. Localization of VEGF receptor-2 (KDR/FLK-1) and effects of blocking it in oxygen-induced retinopathy. Invest. Ophthalmol. Vis. Sci. 43:2002;474-482.
75. Meininger C.J., Schelling M.E., Granger H.J. Adenosine and hypoxia stimulate proliferation and migration of endothelial cells. Am. J. Physiol. 255:1988;H554-H562.
76. Michiels C., Minet E., Michel G., Mottet D., Piret J., Raes M. HIF-1 and AP-1 cooperate to increase gene expression in hypoxia. role of map kinases IUBMB Life. 52:2001;49-53.
77. Millauer B., Witzigmann-Voos S., Schnuerch H., Martinez R., Moeller N.P.H., Risau W., Ullrich A. High affinity VEGF binding and developmental expression suggest Flk-1 as a major regulator of vasculogenesis and angiogenesis. Cell. 72:1993;835-846.
78. Minet E., Arnould T., Michel G., Roland I., Mottet D., Raes M., Remade J., Michiels C. ERK activation upon hypoxia. involvement in HIF-1 activation FEBS Lett. 468:2000;53-58.
79. Mino R.P., Spoerri P.E., Caballero S., Player D., Belardinelli L., Biaggioni I., Grant M.B. Adenosine receptor antagonists and retinal neovascularization in vivo. Invest. Ophthalmol. Vis. Sci. 42(13):2001;3320-3324.
80. Moreau J.L., Huber G. Central adenosine A(2A) receptors. an overview Brain Res. Rev. 31:1999;65-82.
81. Morrison R.R., Talukder M.A., Ledent C., Mustafa S.J. Cardiac effects of adenosine in A(2A) receptor knockout hearts. uncovering A(2B) receptors Am. J. Physiol. Heart Circ. Physiol. 282(2):2002;H437-444.
82. Mustafa S.J., Abebe W. Coronary vasodilation by adenosine-receptor subtypes and mechanism of action. Drug Dev. Res. 39:1996;308-313.
83. Neufeld G., Cohen T., Gengrinovitch S., Poltorak Z. Vascular endothelial growth factor (VEGF) and its receptor. FASEB J. 13:1999;9-22.
84. Newby A.C., Sala G.B. A new procedure for haptenizing adenosine leading to a more specific radioimmunoassay method. Biochem. J. 208:1982;603-610.
85. Nilhausen K. The vasoformative tissue in foetal retina with particular reference to the histochemical demonstration of its alkaline phosphatase activity. Acta Opthalmol. 36:1958;65-70.
86. Olanrewaju H.A., Mustafa S.J. Adenosine A(2A) and A(2B) receptors mediated nitric oxide production in coronary artery endothelial cells. Gen. Pharmacol. 35(3):2000;171-177.
87. Olanrewaju H.A., Qin W., Feoktistov I., Scemama J.L., Mustafa S.J. Adenosine A(2A) and A(2B) receptors in cultured human and porcine coronary artery endothelial cells. Am. J. Physiol. Heart Circ. Physiol. 279(2):2000;H650-656.
88. Ostwald P., Park S.S., Toledando A.Y., Roth S. Adenosine receptor blockade and nitric oxide synthase inhibition in the retina. impact upon postischemic hyperemia and the electroretinogram Vis. Res. 37:1997;3453-3461.
89. Otsuji T., McLeod D.S., Hansen B., Lutty G.A. Immunohistochemical staining and morphometric analysis of the monkey choroidal vasculature. Exp. Eye Res. 75:2002;201-208.
90. Ozaki H., Seo M.S., Ozaki K., Yamada H., Yamada E., Okamoto N., Hofman F., Wood J.M., Campochiaro P.A. Blockade of vascular endothelial cell growth factor receptor signaling is sufficient to completely prevent retinal neovascularization. Am. J. Pathol. 156:2000;697-707.
91. Palmer E. The continuing threat of retinopathy of prematurity. Am. J. Ophthalmol. 122:1996;420-423.
92. Palmer T.M., Gettys T.W., Stiles G.L. Differential interaction with and regulation of multiple G-proteins by the rat A3 adenossne receptor. J. Biol. Chem. 270:1995;16895-16902.
93. Patz A. Oxygen studies in retrolental fibroplasia. IV clinical and experimental observations Am. J. Ophthalmol. 38:1954;291-307.
94. Patz A. The role of oxygen in retrolental fibroplasia. Trans. Am. Ophthal. Soc. 66:1968;940-985.
95. Penn J.S. Oxygen-induced retinopathy in the rat. possible contribution of peroxidation reactions Doc. Ophthalmol. 74:1990;179-186.
96. Penn J.S., Tolman B.L., Henry M.M. Oxygen-induced retinopathy in the rat. relationship of retinal nonperfusion to subsequent neovascularization Invest. Ophthalmol. Vis. Sci. 35:1994;3429-3435.
97. Phelps D.L. Current perspectives on vitamin E in infant nutrition. Am. J. Clin. Nutr. 46:1987;187-191.
98. Phelps D.L., Rosenbaum A.L., Isenberg S.J., Leake R.D., Dorey F.J. Tocopheral efficacy and safety for preventing retinopathy of prematurity. a randomized, controlled, double-masked trial Pediatrics. 79:1987;489-500.
99. Phillis J.W. Adenosine in the control of cerebral circulation. Cerebrovasc. Brain Metabolism Rev. 1:1989;26-54.
100. Pierce E.A., Avery R.L., Foley E.D., Aiello L.P., Smith L.E.H. Vascular endothelial growth factor/vascular permeability factor expression in a mouse model of retinal neovascularization. Proc. Nat. Acad. Sci., USA. 92:1995;905-909.
101. Poucher S.M., Keddie J.R., Brooks R., Shaw G.R., McKilIup D. Pharmacodynamics of ZM 241385, a potent A2a adenosine antagonist, after enteric administration in rat, cat and dog. J. Pharm. Pharmacol. 48:1996;601-606.
102. Provis J.M., Leech J., Diaz C., Penfold P.L., Stone J., Keshet E. Development of the human retinal vasculature. Cellular relations and VEGF expression Exp. Eye Res. 65:1997;555-568.
103. Quinn G.E., Johnson L., Otis C., Schaffer D.B., Bowen F.W. Incidence, severity and time course of ROP in a randomized clinical trial of vitamin E prophylaxis. Doc. Ophthamol. 74:1990;223-228.
104. Reynaud X., Dorey C.K. Extraretinal neovascularization induced by hypoxic episodes in the neonatal rat. Invest. Ophthalmol. Vis. Sci. 35:1994;3169-3177.
105. Rivkees S.A., Zhao Z., Porter G., Turner C. Influences of adenosine on the fetus and newborn. Mol. Genet. Metab. 74(1-2):2001;160-171.
106. Robinson G.S., Pierce E.A., Rook S.L., Foley E.D., Webb R., Smith L.E.H. Oligonucleotides inhibition retinal neovascularization in the murine model of proliferative retinopathy. Proc. Nat. Acad. Sci. 93:1996;4851-4856.
107. Robbins S.G., Veeraramani S.R., Penn J.S. Evidence for upregulation and redistribution of vascular endothelial growth factor (VEGF) receptors flt-1 and flk-1 in the oxygen-injured rat retina. Growth Factors. 16:1998;1-9.
108. Robinson G.S., Ju M., Shih S.C., Xu X., McMahon G., Caldwell R.B., Smith L.E. Nonvascular role for VEGF. VEGFR-1,2 activity is critical for neural retinal development FASEB J. 15:2001;1215-1217.
109. Roth S., Park S.S., Sikorski C.W., Osinski J., Chan R., Loomis K. Concentrations of adenosine and its metabolites in the rat retina/choroid during reperfusion after ischemia. Curr. Eye Res. 16:1997;875-885.
110. Roth S., Rosenbaum P.S., Osinski J., Park S.S., Toledano A.Y., Li B., Moshfeghi A.A. Ischemia induces significant changes in purine nucleoside concentration in the retina-choroid in rats. Exp. Eye Res. 65:1997;771-779.
111. Sandercoe T.M., Madigan M.C., Billson F.A., Penfold P.L., Provis J.M. Astrocyte proliferation during development of the human retinal vasculature. Exp. Eye Res. 69(5):1999;511-523.
112. Schopf G., Rumpold H., Muller M.M. Alterations of purine salvage pathways during differentiation of rat heart myoblasts toward myocytes. Biochim. Biophys. Acta. 884:1986;319-325.
113. Seetharam L., Gotoh N., Maru Y., Neufeld G., Yamaguchi S., Shibuya M. A unique signal transduction from FLT tyrosine kinase, a receptor for vascular endothelial growth factor VEGF. Oncogene. 10:1995;135-147.
114. Seo M.S., Kwak N., Ozaki H., Yamada H., Okamoto N., Yamada E., Fabbro D., Hofman F., Wood J.M., Campochiaro P.A. Dramatic inhibition of retinal and choroidal neovascularization by oral administration of a kinase inhibitor. Am. J. Pathol. 154:1999;1743-1753.
115. Serpell G. Polysaccharide granules in association with developing retinal vessels and with retrolental fibroplasia. Br. J. Ophthalmol. 38:1954;460-471.
116. Shalaby F., Roussant J., Yamaguchi T.P., Gersenstein M., Wu X.-F., Breltman M.L., Schuh A.C. Failure of blood island formation and vasculogenesis in Flk-1-deficient mice. Nature. 376:1995;62-66.
117. Shweiki D., Itin A., Soffer D., Keshet E. Vascular endothelial growth factor induced by hypoxia may mediate hypoxia-initiated angiogenesis. Nature. 359:1992;843-845.
118. Smith L.E.H., Wesolowski E., McLellan A., Kostyk S.K., D'Amato R.D., Sullivan R., D'Amore P.A. Oxygen-induced retinopathy in the mouse. Invest. Ophthalmol. Vis. Sci. 35(1):1994;101-111.
119. Sobrevia L., Yudilevich D.L., Mann G.E. Activation of A2-purinoceptors by adenosine stimulates L-arginine transport (system y+) and nitric oxide synthesis in fetal human endothelial cells. J. Physiol. 499:1997;135-140.
120. 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., D'Amore P.A. Arteriolar and venular patterning in retinas of mice selectively expressing VEGF isoforms. J. Clin. Invest. 109(3):2002;327-336.
121. 2 receptor. FEBS Lett. 331:1993;96-100.
122. Stone J., Itin A., Alon T., Pe'er J., Gnessin H., Chan-Ling T., Keshet E. Development of retinal vasculature is mediated by hypoxia-induced vascular endothelial growth factor (VEGF) expression by neuroglia. J. Neurosci. 15:1995;4738-4747.
123. Stone J., Chan-Ling T., Pe'er J., Itin A., Gnessin H., Keshet E. Roles of vascular endothelial growth factor and astrocyte degeneration in the genesis of retinopathy of prematurity. Invest. Ophthalmol. Vis. Sci. 37:1996;290-299.
124. Suzuma K., Takagi H., Otani A., Suzuma I., Honda Y. Increased expression of KDR/Flk-1 (VEGFR-2) in murine model of ischemia-induced retinal neovascularization. Microvasc. Res. 56:1998;183-191.
125. Tabrizchi R., Bedi S. Pharmacology of adenosine receptors in the vasculature. Pharmacol Ther. 91(2):2001;133-147.
126. Takagi H., King G.L., Ferrara N., Aiello L.P. Hypoxia regulates vascular endothelial growth factor receptor KDR/Flk gene expression through adenosine A2 receptors in retinal capillary endothelial cells. Invest. Ophthalmol. Vis. Sci. 37:1996;1311-1321.
127. Takagi H., King G.L., Robinson G.S., Ferrara N., Aiello L.P. Adenosine mediates hypoxic induction of vascular endothelial growth factor in retinal pericytes and endothelial cells. Invest. Ophthalmol. Vis. Sci. 37:1996;2165-2176.
128. Taomoto M., McLeod D.S., Merges C., Lutty G.A. Localization of adenosine A2a receptor in retinal development and oxygen-induced retinopathy. Invest. Ophthalmol. Vis. Sci. 41(1):2000;230-243.
129. Teuscher E., Weidlich V. Adenosine nucleotides, adenosine and adenine as angiogenesis factors. Biomed. Biochim. Acta. 44:1985;493-495.
130. Unemori E.N., Ferrara N., Bauer E.A., Amento E.P. Vascular endothelial growth factor induces interstitial collagenase expression in human endothelial cells. J. Cell Physiol. 153:1992;557-562.
131. Van Waarde A., Stromski M.E., Thulin G., Guadio K.M., Kashgarian M., Shulman R.G., Siegel N.J. Protection of the kidney against ischemic injury by inhibition of 5′-nucleotidase. Am. J. Physiol. 256:1989;F298-F305.
132. Waltenberger J., Claesson-Welsh L., Siegbahn A., Shibuya M., Heldin C.-H. Different signal transduction properties of KDR and FLT1, two receptors for vascular endothelial growth factor. J. Bio. Chem. 269:1994;26988-26995.
133. Winn H., Morii S., Berne R. The role of adenosine in autoregulation of cerebral blood flow. Ann. Biomed. Eng. 13:1985;321-328.
134. Yang X., Cepko C.L. Flk-1, a receptor for vascular endothelial growth factor (VEGF), is expressed by retinal progenitor cells. J. Neurosci. 16:1996;6089-6099.
135. 3-subtype receptor is highly expressed in rat smooth muscle cells. Its role in attenuating adensoine-induced increase in camp Microvasc. Res. 54:1997;243-252.
136. Zhao Z., Makaritsis K., Francis C.E., Gavris H., Ravid K. A role for the A3 adenosine receptor in determining tissue levels of cAMP and blood pressure. Studies in knockout mice Biochem. Biophys. Acta. 1500:2000;280-290.