Understanding ischemic retinopathies: emerging concepts from oxygen-induced retinopathy (original) (raw)

References

1. Penn JS, Tolman BL, Lowery LA (1993) Variable oxygen exposure causes preretinal neovascularization in the newborn rat. Invest Ophthalmol Vis Sci 34:576–585
   PubMed CAS Google Scholar
2. Penn JS, Tolman BL, Henry MM (1994) Oxygen-induced retinopathy in the rat: relationship of retinal nonperfusion to subsequent neovascularization. Invest Ophthalmol Vis Sci 35:3429–3435
   PubMed CAS Google Scholar
3. 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
   PubMed CAS Google Scholar
4. Chan-Ling T, Tout S, Hollander H, Stone J (1992) Vascular changes and their mechanisms in the feline model of retinopathy of prematurity. Invest Ophthalmol Vis Sci 33:2128–2147
   PubMed CAS Google Scholar
5. McLeod DS, D’Anna SA, Lutty GA (1998) Clinical and histopathologic features of canine oxygen-induced proliferative retinopathy. Invest Ophthalmol Vis Sci 39:1918–1932
   PubMed CAS Google Scholar
6. Gyllensten LJ, Hellstrom BE (1954) Experimental approach to the pathogenesis of retrolental fibroplasia. I. Changes of the eye induced by exposure of newborn mice to concentrated oxygen. Acta Paediatr 43:131–148
   Article CAS Google Scholar
7. Alon T, Hemo I, Itin A, Pe’er J, Stone J, Keshet E (1995) Vascular endothelial growth factor acts as a survival factor for newly formed retinal vessels and has implications for retinopathy of prematurity. Nat Med 1:1024–1028
   Article PubMed CAS Google Scholar
8. Pierce EA, Foley ED, Smith LE (1996) Regulation of vascular endothelial growth factor by oxygen in a model of retinopathy of prematurity [erratum 1997, 115:427]. Arch Ophthalmol 114:1219–1228
   PubMed CAS Google Scholar
9. Stone J, Chan-Ling T, Pe’er J, Itin A, Gnessin H, Keshet E (1996) Roles of vascular endothelial growth factor and astrocyte degeneration in the genesis of retinopathy of prematurity. Invest Ophthalmol Vis Sci 37:290–299
   PubMed CAS Google Scholar
10. Simons BD, Flynn JT (1999) Retinopathy of prematurity and associated factors. Int Ophthalmol Clin 39:29–48
    Article PubMed CAS Google Scholar
11. Liu JP, Baker J, Perkins AS, Robertson EJ, Efstratiadis A (1993) Mice carrying null mutations of the genes encoding insulin-like growth factor I (IGF-1) and type 1 IGF receptor (IGF-1R). Cell 75:59–72
    PubMed CAS Google Scholar
12. Lassarre C, Hardouin S, Daffos F, Forestier F, Frankenne F, Binoux M (1991) Serum insulin-like growth factors and insulin-like growth factor binding proteins in the human fetus. Relationships with growth in normal subjects and in subjects with intrauterine growth retardation. Pediatr Res 29:219–225
    Article PubMed CAS Google Scholar
13. Reece EA, Wiznitzer A, Le E, Homko CJ, Behrman H, Spencer EM (1994) The relation between human fetal growth and fetal blood levels of insulin-like growth factors I and II, their binding proteins, and receptors. Obstet Gynecol 84:88–95
    PubMed CAS Google Scholar
14. Langford K, Nicolaides K, Miell JP (1998) Maternal and fetal insulin-like growth factors and their binding proteins in the second and third trimesters of human pregnancy. Hum Reprod 13:1389–1393
    Article PubMed CAS Google Scholar
15. Lineham JD, Smith RM, Dahlenburg GW, King RA, Haslam RR, Stuart MC, Faull L (1986) Circulating insulin-like growth factor I levels in newborn premature and full-term infants followed longitudinally. Early Hum Dev 13:37–46
    Article PubMed CAS Google Scholar
16. Hellstrom A, Perruzzi C, Ju M, Engstrom E, Hard AL, Liu JL, Albertsson-Wikland K, Carlsson B, Niklasson A, Sjodell L, LeRoith D, Senger DR, Smith LE (2001) Low IGF-I suppresses VEGF-survival signaling in retinal endothelial cells: direct correlation with clinical retinopathy of prematurity. Proc Natl Acad Sci U S A 98:5804–5808
    Article PubMed CAS Google Scholar
17. Hellstrom A, Engstrom E, Hard AL, Albertsson-Wikland K, Carlsson B, Niklasson A, Lofqvist C, Svensson E, Holm S, Ewald U, Holmstrom G, Smith LE (2003) Postnatal serum insulin-like growth factor I deficiency is associated with retinopathy of prematurity and other complications of premature birth. Pediatrics 112:1016–1020
    Article PubMed Google Scholar
18. Lofqvist C, Andersson E, Sigurdsson J, Engstrom E, Hard AL, Niklasson A, Smith LE, Hellstrom A (2006) Longitudinal postnatal weight and insulin-like growth factor I measurements in the prediction of retinopathy of prematurity. Arch Ophthalmol 124:1711–1718
    Article PubMed Google Scholar
19. Smith LE, Kopchick JJ, Chen W, Knapp J, Kinose F, Daley D, Foley E, Smith RG, Schaeffer JM (1997) Essential role of growth hormone in ischemia-induced retinal neovascularization. Science 276:1706–1709
    Article PubMed CAS Google Scholar
20. Smith LE, Shen W, Perruzzi C, Soker S, Kinose F, Xu X, Robinson G, Driver S, Bischoff J, Zhang B, Schaeffer JM, Senger DR (1999) Regulation of vascular endothelial growth factor-dependent retinal neovascularization by insulin-like growth factor-1 receptor. Nat Med 5:1390–1395
    Article PubMed CAS Google Scholar
21. Frystyk J (2004) Free insulin-like growth factors–measurements and relationships to growth hormone secretion and glucose homeostasis. Growth Horm IGF Res 14:337–375
    Article PubMed CAS Google Scholar
22. Firth SM, Baxter RC (2002) Cellular actions of the insulin-like growth factor binding proteins. Endocr Rev 23:824–854
    Article PubMed CAS Google Scholar
23. Lofqvist C, Chen J, Connor KM, Smith AC, Aderman CM, Liu N, Pintar JE, Ludwig T, Hellstrom A, Smith LE (2007) IGFBP3 suppresses retinopathy through suppression of oxygen-induced vessel loss and promotion of vascular regrowth. Proc Natl Acad Sci U S A 104:10589–10594
    Article PubMed CAS Google Scholar
24. Chen J, Smith LE (2007) Retinopathy of prematurity. Angiogenesis 10:133–140
    Article PubMed Google Scholar
25. Jaquet K, Krause K, Tawakol-Khodai M, Geidel S, Kuck KH (2002) Erythropoietin and VEGF exhibit equal angiogenic potential. Microvasc Res 64:326–333
    Article PubMed CAS Google Scholar
26. Ribatti D, Presta M, Vacca A, Ria R, Giuliani R, Dell’Era P, Nico B, Roncali L, Dammacco F (1999) Human erythropoietin induces a pro-angiogenic phenotype in cultured endothelial cells and stimulates neovascularization in vivo. Blood 93:2627–2636
    PubMed CAS Google Scholar
27. Brines M, Cerami A (2005) Emerging biological roles for erythropoietin in the nervous system. Nat Rev Neurosci 6:484–494
    Article PubMed CAS Google Scholar
28. Chen J, Connor KM, Aderman CM, Smith LE (2008) Erythropoietin deficiency decreases vascular stability in mice. J Clin Invest 118:526–533
    PubMed CAS Google Scholar
29. Chen J, Connor KM, Aderman CM, Willett KL, Aspegren OP, Smith LE (2009) Erythropoietin siRNA suppresses retinal neovascularization in a mouse model of proliferative retinopathy. Invest Ophthalmol Vis Sci. doi:10.1167/iovs.1108-2521
    Google Scholar
30. Watanabe D, Suzuma K, Matsui S, Kurimoto M, Kiryu J, Kita M, Suzuma I, Ohashi H, Ojima T, Murakami T, Kobayashi T, Masuda S, Nagao M, Yoshimura N, Takagi H (2005) Erythropoietin as a retinal angiogenic factor in proliferative diabetic retinopathy. N Engl J Med 353:782–792
    Article PubMed CAS Google Scholar
31. Katsura Y, Okano T, Matsuno K, Osako M, Kure M, Watanabe T, Iwaki Y, Noritake M, Kosano H, Nishigori H, Matsuoka T (2005) Erythropoietin is highly elevated in vitreous fluid of patients with proliferative diabetic retinopathy. Diabetes Care 28:2252–2254
    Article PubMed CAS Google Scholar
32. Suk KK, Dunbar JA, Liu A, Daher NS, Leng CK, Leng JK, Lim P, Weller S, Fayard E (2008) Human recombinant erythropoietin and the incidence of retinopathy of prematurity: a multiple regression model. J AAPOS 12:233–238
    Article PubMed Google Scholar
33. Arjamaa O, Nikinmaa M (2006) Oxygen-dependent diseases in the retina: role of hypoxia-inducible factors. Exp Eye Res 83:473–483
    Article PubMed CAS Google Scholar
34. Sears JE, Hoppe G, Ebrahem Q, Anand-Apte B (2008) Prolyl hydroxylase inhibition during hyperoxia prevents oxygen-induced retinopathy. Proc Natl Acad Sci U S A 105:19898–19903
    Article PubMed Google Scholar
35. Morita M, Ohneda O, Yamashita T, Takahashi S, Suzuki N, Nakajima O, Kawauchi S, Ema M, Shibahara S, Udono T, Tomita K, Tamai M, Sogawa K, Yamamoto M, Fujii-Kuriyama Y (2003) HLF/HIF-2alpha is a key factor in retinopathy of prematurity in association with erythropoietin. EMBO J 22:1134–1146
    Article PubMed CAS Google Scholar
36. Dioum EM, Clarke SL, Ding K, Repa JJ, Garcia JA (2008) HIF-2alpha-haploinsufficient mice have blunted retinal neovascularization due to impaired expression of a proangiogenic gene battery. Invest Ophthalmol Vis Sci 49:2714–2720
    Article PubMed Google Scholar
37. Stone WL, Farnsworth CC, Dratz EA (1979) A reinvestigation of the fatty acid content of bovine, rat and frog retinal rod outer segments. Exp Eye Res 28:387–397
    Article PubMed CAS Google Scholar
38. Fliesler SJ, Anderson RE (1983) Chemistry and metabolism of lipids in the vertebrate retina. Prog Lipid Res 22:79–131
    Article PubMed CAS Google Scholar
39. SanGiovanni JP, Chew EY (2005) The role of omega-3 long-chain polyunsaturated fatty acids in health and disease of the retina. Prog Retin Eye Res 24:87–138
    Article PubMed CAS Google Scholar
40. Clandinin MT, Chappell JE, Leong S, Heim T, Swyer PR, Chance GW (1980) Intrauterine fatty acid accretion rates in human brain: implications for fatty acid requirements. Early Hum Dev 4:121–129
    Article PubMed CAS Google Scholar
41. Martinez M (1992) Tissue levels of polyunsaturated fatty acids during early human development. J Pediatr 120:S129–S138
    Article PubMed CAS Google Scholar
42. Krauss-Etschmann S, Shadid R, Campoy C, Hoster E, Demmelmair H, Jimenez M, Gil A, Rivero M, Veszpremi B, Decsi T, Koletzko BV (2007) Effects of fish-oil and folate supplementation of pregnant women on maternal and fetal plasma concentrations of docosahexaenoic acid and eicosapentaenoic acid: a European randomized multicenter trial. Am J Clin Nutr 85:1392–1400
    PubMed CAS Google Scholar
43. Uauy R, Peirano P, Hoffman D, Mena P, Birch D, Birch E (1996) Role of essential fatty acids in the function of the developing nervous system. Lipids 31:S167–S176
    Article PubMed CAS Google Scholar
44. Uauy R, Hoffman DR, Peirano P, Birch DG, Birch EE (2001) Essential fatty acids in visual and brain development. Lipids 36:885–895
    Article PubMed CAS Google Scholar
45. Connor KM, SanGiovanni JP, Lofqvist C, Aderman CM, Chen J, Higuchi A, Hong S, Pravda EA, Majchrzak S, Carper D, Hellstrom A, Kang JX, Chew EY, Salem N Jr, Serhan CN, Smith LE (2007) Increased dietary intake of omega-3-polyunsaturated fatty acids reduces pathological retinal angiogenesis. Nat Med 13:868–873
    Article PubMed CAS Google Scholar
46. Penn JS, Tolman BL, Bullard LE (1997) Effect of a water-soluble vitamin E analog, trolox C, on retinal vascular development in an animal model of retinopathy of prematurity. Free Radic Biol Med 22:977–984
    Article PubMed CAS Google Scholar
47. Niesman MR, Johnson KA, Penn JS (1997) Therapeutic effect of liposomal superoxide dismutase in an animal model of retinopathy of prematurity. Neurochem Res 22:597–605
    Article PubMed CAS Google Scholar
48. Spierer A, Rabinowitz R, Pri-Chen S, Rosner M (2005) An increase in superoxide dismutase ameliorates oxygen-induced retinopathy in transgenic mice. Eye 19:86–91
    Article PubMed CAS Google Scholar
49. Ando A, Yang A, Mori K, Yamada H, Yamada E, Takahashi K, Saikia J, Kim M, Melia M, Fishman M, Huang P, Campochiaro PA (2002) Nitric oxide is proangiogenic in the retina and choroid. J Cell Physiol 191:116–124
    Article PubMed CAS Google Scholar
50. Beauchamp MH, Sennlaub F, Speranza G, Gobeil F Jr, Checchin D, Kermorvant-Duchemin E, Abran D, Hardy P, Lachapelle P, Varma DR, Chemtob S (2004) Redox-dependent effects of nitric oxide on microvascular integrity in oxygen-induced retinopathy. Free Radic Biol Med 37:1885–1894
    Article PubMed CAS Google Scholar
51. Beckman JS, Beckman TW, Chen J, Marshall PA, Freeman BA (1990) Apparent hydroxyl radical production by peroxynitrite: implications for endothelial injury from nitric oxide and superoxide. Proc Natl Acad Sci U S A 87:1620–1624
    Article PubMed CAS Google Scholar
52. Kirsch M, Korth HG, Sustmann R, de Groot H (2002) The pathobiochemistry of nitrogen dioxide. Biol Chem 383:389–399
    Article PubMed CAS Google Scholar
53. Gu X, El-Remessy AB, Brooks SE, Al-Shabrawey M, Tsai NT, Caldwell RB (2003) Hyperoxia induces retinal vascular endothelial cell apoptosis through formation of peroxynitrite. Am J Physiol Cell Physiol 285:C546–C554
    PubMed CAS Google Scholar
54. Holmes JM, Duffner LA, Kappil JC (1994) The effect of raised inspired carbon dioxide on developing rat retinal vasculature exposed to elevated oxygen. Curr Eye Res 13:779–782
    Article PubMed CAS Google Scholar
55. Holmes JM, Zhang S, Leske DA, Lanier WL (1997) The effect of carbon dioxide on oxygen-induced retinopathy in the neonatal rat. Curr Eye Res 16:725–732
    Article PubMed CAS Google Scholar
56. Checchin D, Hou X, Hardy P, Abran D, Najarian T, Beauchamp MH, Bernier SG, Gobeil F Jr, Quiniou C, Varma DR, Chemtob S (2002) PGE2-mediated eNOS induction in prolonged hypercapnia. Invest Ophthalmol Vis Sci 43:1558–1566
    PubMed Google Scholar
57. Checchin D, Sennlaub F, Sirinyan M, Brault S, Zhu T, Kermorvant-Duchemin E, Hardy P, Balazy M, Chemtob S (2006) Hypercapnia prevents neovascularization via nitrative stress. Free Radic Biol Med 40:543–553
    Article PubMed CAS Google Scholar
58. Brooks SE, Gu X, Samuel S, Marcus DM, Bartoli M, Huang PL, Caldwell RB (2001) Reduced severity of oxygen-induced retinopathy in eNOS-deficient mice. Invest Ophthalmol Vis Sci 42:222–228
    PubMed CAS Google Scholar
59. Balazy M, Poff CD (2004) Biological nitration of arachidonic acid. Curr Vasc Pharmacol 2:81–93
    Article PubMed CAS Google Scholar
60. Jiang H, Kruger N, Lahiri DR, Wang D, Vatele JM, Balazy M (1999) Nitrogen dioxide induces cis–trans-isomerization of arachidonic acid within cellular phospholipids. Detection of trans-arachidonic acids in vivo. J Biol Chem 274:16235–16241
    Article PubMed CAS Google Scholar
61. Zghibeh CM, Raj Gopal V, Poff CD, Falck JR, Balazy M (2004) Determination of trans-arachidonic acid isomers in human blood plasma. Anal Biochem 332:137–144
    Article PubMed CAS Google Scholar
62. Balazy M (2000) Trans-arachidonic acids: new mediators of inflammation. J Physiol Pharmacol 51:597–607
    PubMed CAS Google Scholar
63. Landry DW, Oliver JA (2001) The pathogenesis of vasodilatory shock. N Engl J Med 345:588–595
    Article PubMed CAS Google Scholar
64. Vincent JL, Zhang H, Szabo C, Preiser JC (2000) Effects of nitric oxide in septic shock. Am J Respir Crit Care Med 161:1781–1785
    PubMed CAS Google Scholar
65. Kermorvant-Duchemin E, Sennlaub F, Sirinyan M, Brault S, Andelfinger G, Kooli A, Germain S, Ong H, d’Orleans-Juste P, Gobeil F Jr, Zhu T, Boisvert C, Hardy P, Jain K, Falck JR, Balazy M, Chemtob S (2005) Trans-arachidonic acids generated during nitrative stress induce a thrombospondin-1-dependent microvascular degeneration. Nat Med 11:1339–1345
    Article PubMed CAS Google Scholar
66. Dawson DW, Pearce SF, Zhong R, Silverstein RL, Frazier WA, Bouck NP (1997) CD36 mediates the in vitro inhibitory effects of thrombospondin-1 on endothelial cells. J Cell Biol 138:707–717
    Article PubMed CAS Google Scholar
67. Jimenez B, Volpert OV, Crawford SE, Febbraio M, Silverstein RL, Bouck N (2000) Signals leading to apoptosis-dependent inhibition of neovascularization by thrombospondin-1. Nat Med 6:41–48
    Article PubMed CAS Google Scholar
68. Wang S, Wu Z, Sorenson CM, Lawler J, Sheibani N (2003) Thrombospondin-1-deficient mice exhibit increased vascular density during retinal vascular development and are less sensitive to hyperoxia-mediated vessel obliteration. Dev Dyn 228:630–642
    Article PubMed CAS Google Scholar
69. Cai W, Rook SL, Jiang ZY, Takahara N, Aiello LP (2000) Mechanisms of hepatocyte growth factor-induced retinal endothelial cell migration and growth. Invest Ophthalmol Vis Sci 41:1885–1893
    PubMed CAS Google Scholar
70. D’Amore PA (1994) Mechanisms of retinal and choroidal neovascularization. Invest Ophthalmol Vis Sci 35:3974–3979
    PubMed Google Scholar
71. Enge M, Bjarnegard M, Gerhardt H, Gustafsson E, Kalen M, Asker N, Hammes HP, Shani M, Fassler R, Betsholtz C (2002) Endothelium-specific platelet-derived growth factor-B ablation mimics diabetic retinopathy. EMBO J 21:4307–4316
    Article PubMed CAS Google Scholar
72. Gariano RF, Gardner TW (2005) Retinal angiogenesis in development and disease. Nature 438:960–966
    Article PubMed CAS Google Scholar
73. Lee MS, Moon EJ, Lee SW, Kim MS, Kim KW, Kim YJ (2001) Angiogenic activity of pyruvic acid in in vivo and in vitro angiogenesis models. Cancer Res 61:3290–3293
    PubMed CAS Google Scholar
74. Murray B, Wilson DJ (2001) A study of metabolites as intermediate effectors in angiogenesis. Angiogenesis 4:71–77
    Article PubMed CAS Google Scholar
75. Neuman RE, Mc CT (1958) Growth-promoting properties of pyruvate oxal-acetate, and alpha-ketoglutarate for isolated Walker carcinosarcoma 256 cells. Proc Soc Exp Biol Med 98:303–306
    PubMed CAS Google Scholar
76. He W, Miao FJ, Lin DC, Schwandner RT, Wang Z, Gao J, Chen JL, Tian H, Ling L (2004) Citric acid cycle intermediates as ligands for orphan G-protein-coupled receptors. Nature 429:188–193
    Article PubMed CAS Google Scholar
77. Sapieha P, Sirinyan M, Hamel D, Zaniolo K, Joyal JS, Cho JH, Honore JC, Kermorvant-Duchemin E, Varma DR, Tremblay S, Leduc M, Rihakova L, Hardy P, Klein WH, Mu X, Mamer O, Lachapelle P, Di Polo A, Beausejour C, Andelfinger G, Mitchell G, Sennlaub F, Chemtob S (2008) The succinate receptor GPR91 in neurons has a major role in retinal angiogenesis. Nat Med 14:1067–1076
    Article PubMed CAS Google Scholar

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