AT1 receptor inhibition prevents astrocyte degeneration and restores vascular growth in oxygen-induced retinopathy

GLIA

Volumn 56, Issue 10, 2008, Pages 1076-1090

  Downie, Laura E ^a   Pianta, Michael J ^a   Vingrys, Algis J ^a   Wilkinson Berka, Jennifer L ^b   Fletcher, Erica L ^a  

^a UNIVERSITY OF MELBOURNE   (Australia)

^b MONASH UNIVERSITY   (Australia)

Author keywords

Angiotensin; Glia; Neovascularization; Renin angiotensin system; Retina; Retinopathy of prematurity

Indexed keywords

ANGIOTENSIN 1 RECEPTOR ANTAGONIST; CONNEXIN 26; DESMIN; GLIAL FIBRILLARY ACIDIC PROTEIN; NEUROGENIN 2; OXYGEN; PROTEIN S100B; VALSARTAN; ANGIOTENSIN 1 RECEPTOR; ANGIOTENSIN RECEPTOR ANTAGONIST; DRUG DERIVATIVE; TETRAZOLE DERIVATIVE; VALINE;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; ASTROCYTE; CELL COUNT; CELL DEGENERATION; CELL INTERACTION; CELL SURVIVAL; CONTROLLED STUDY; DRUG EFFICACY; DRUG MECHANISM; ENDOTHELIUM CELL; GLIA CELL; IMMUNOCYTOCHEMISTRY; IMMUNOREACTIVITY; MUELLER CELL; NEUROPROTECTION; NEWBORN; NONHUMAN; PERICYTE; PRIORITY JOURNAL; RAT; RETINA NEOVASCULARIZATION; RETINOPATHY; SUBRETINAL NEOVASCULARIZATION; ANGIOGENESIS; ANIMAL; CHEMICALLY INDUCED DISORDER; COMPARATIVE STUDY; DRUG EFFECT; GROWTH, DEVELOPMENT AND AGING; METABOLISM; PATHOLOGY; PHYSIOLOGY; RETINA BLOOD VESSEL; RETINA DEGENERATION; SPRAGUE DAWLEY RAT;

ANGIOTENSIN II TYPE 1 RECEPTOR BLOCKERS; ANIMALS; ANIMALS, NEWBORN; ASTROCYTES; NEOVASCULARIZATION, PHYSIOLOGIC; OXYGEN; RATS; RATS, SPRAGUE-DAWLEY; RECEPTOR, ANGIOTENSIN, TYPE 1; RETINAL DEGENERATION; RETINAL VESSELS; TETRAZOLES; VALINE;

EID: 51349130208     PISSN: 08941491     EISSN: 10981136     Source Type: Journal    
DOI: 10.1002/glia.20680     Document Type: Article

References (98)

1. Akula JD, Hansen RM, Martinez-Perez ME, Fulton AB. 2007. Rod photoreceptor function predicts blood vessel abnormality in retinopathy of prematurity. Invest Ophthalmol Vis Sci 48:4351-4359.
2. Asnaghi V, Gerhardinger C, Hoehn T, Adeboje A, Lorenzi M. 2003. A role for the polyol pathway in the early neuroretinal apoptosis and glial changes induced by diabetes in the rat. Diabetes 52:506-511.
3. Banin E, Dorrell MI, Aguilar E, Ritter MR, Aderman CM, Smith ACH, Friedlander J, Friedlander M. 2006. T2-TrpRS inhibits preretinal neovascularization and enhances physiological vascular regrowth in OIR as assessed by a new method of quantification. Invest Ophthalmol Vis Sci 47:2125-2134.
4. Benjamin LE, Hemo I, 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.
5. Berka JL, Stubbs AJ, Wang DZ, DiNicolantonio R, Alcorn D, Campbell DJ, Skinner SL. 1995. Renin-containing Müller cells of the retina display endocrine features. Invest Ophthalmol Vis Sci 36:1450-1458.
6. Bignami A, Dahl D. 1979. The radial glia of Müller in the rat retina and their response to injury. An immunofluorescence study with antibodies to the glial fibrillary acidic (GFA) protein. Exp Eye Res 28:63-69.
7. Bringmann A, Reichenbach A. 2001. Role of Müller cells in retinal degenerations. Front Biosci 6:E72-E92.
8. Bui B, Armitage JA, Tolcos M, Cooper ME, Vingrys AJ. 2003. ACE inhibition salvages the visual loss caused by diabetes. Diabetologia 46:401-408.
9. Calogero G, Ricci B. 1994. Experimental oxygen-induced retinal detachment in the newborn Wistar rat. Doc Ophthalmol 87:315-329.
10. Chan-Ling T. 1997. Glial, vascular and neuronal cytogenesis in whole-mounted cat retina. Microsc Res Tech 36:1-16.
11. Chan-Ling T, Gock B, Stone J. 1995. The effect of oxygen on vasoformative cell division. Evidence that 'physiological hypoxia' is the stimulus for normal retinal vasculogenesis. Invest Ophthalmol Vis Sci 36: 1201-1214.
12. Chan-Ling T, Page MP, Gardiner TA, Baxter L, Rosinova E, Hughes S. 2004. Desmin ensheathment ratio as an indicator of vessel stability: Evidence in normal development and in retinopathy of prematurity. Am J Pathol 165:1301-1313.
13. Chan-Ling T, Stone J. 1991. Factors determining the migration of astrocytes into the developing retina: Migration does not depend on intact axons or patent vessels. J Comp Neurol 303:375-386.
14. Chan-Ling T, Stone J. 1992. Degeneration of astrocytes in feline retinopathy of prematurity causes failure of the blood-retinal barrier. Invest Ophthalmol Vis Sci 33:2148-2159.
15. Chaturvedi N, Sjolie AK, Stephenson JM, Abrahamian H, Keipes M, Castellarin A, Rogulja-Pepeonik Z, Fuller JH. 1998. Effect of lisinopril on progression of retinopathy in normotensive people with type 1 diabetes. The EUCLID Study Group. EURODIAB controlled trial of lisinopril in insulin-dependent diabetes mellitus. Lancet 351:28-31.
16. Checchin D, Sennlaub MD, Levavasseur E, Leduc M, Chemtob S. 2006. Potential role of microglia in retinal blood vessel formation. Invest Ophthalmol Vis Sci 47:3595-3602.
17. Chen H, Weber AJ. 2002. Expression of glial fibrillary acidic protein and glutamine synthetase by Müller cells after optic nerve damage and intravitreal application of brain-derived neurotrophic factor. Glia 15:115-125.
18. Cho EYP, Choi HL, Chan FL. 2002. Expression pattern of Glycoconjugates in Rat Retina as Analysed by Lectin Histochemistry. J Histochem 34:589-600.
19. 2 receptors. Kidney Int 54:S95-S99.
20. Cogan DG, Toussaint D, Kuwabara T. 1961. Retinal vascular patterns. IV. Diabetic retinopathy. Arch Ophthalmol 66:366-378.
21. Danielyan L, Lourhmati A, Verleysdonk S, Kabisch D, Proksch B, Thiess U, Umbreen S, Schmidt B, Gleiter CH. 2007. Angiotensin receptor type 1 blockade in astroglia decreases hypoxia-induced cell damage and TNFα release. Neurochem Res 32:1489-1498.
22. Danser AHJ, Derkx FHM, Admiraal PJJ, Deinum PT, de Jong VM, Schalekamp AH. 1994. Angiotensin levels in the eye. Invest Ophthalmol Vis Sci 35:1008-1018.
23. de Gasparo M, Catt KJ, Inagami T, Wright JW, Unger T. 2000. International union of pharmacology. XXIII. The angiotensin II receptors. Pharmacol Rev 52:415-472.
24. Dembinska O, Rojas LM, Chemtob S, Lachapelle P. 2002. Evidence for a brief period of enhanced oxygen susceptibility in the rat model of oxygen-induced retinopathy. Invest Ophthalmol Vis Sci 43:2481-2490.
25. Dembinska O, Rojas LM, Varma DR, Chemtob S, Lachapelle, P. 2001. Graded contribution of retinal maturation to the development of oxygen-induced retinopathy in rats. Invest Ophthalmol Vis Sci 42:1111-1118.
26. Dorrell MI, Aguilar E, Friedlander J. 2002. Retinal vascular development is mediated by endothelial filopodia, a preexisting astrocytic template and specific R-cadherin adhesion. Invest Ophthalmol Vis Sci 43:3500-3510.
27. Downie LE, Pianta MJ, Vingrys AJ, Wilkinson-Berka JL, Fletcher EL. 2007. Neuronal and glial cell changes are determined by retinal vascularization in retinopathy of prematurity. J Comp Neurol 504:404-417.
28. Eisenfeld AJ, Bunt-Milam AH, Sarthy PV. 1984. Müller cell expression of glial fibrillary acidic protein after genetic and experimental photo-receptor degeneration in the rat retina. Invest Ophthalmol Vis Sci 25:1321-1328.
29. Ferrari-Dileo G, Davis BE, Anderson DR. 1987. Angiotensin binding sites in bovine and human retinal blood vessels. Invest Ophthalmol Vis Sci 28:1747-1751.
30. Fletcher EL, Hack I, Brandstätter JH, Wässle H. 2000. Synaptic localization of NMDA receptor subunits in the rat retina. J Comp, Neurol 420:98-112.
31. Fogarty DJ, Sanchez-Gomez MV, Matute C. 2002. Multiple angiotensin receptor subtypes in normal and tumor astrocytes in vitro. Glia 39:304-313.
32. Fruttiger M, Calver AR, Richardson WD. 2000. Platelet-derived growth factor is constitutively secreted from neuronal cell bodies but not from axons. Curr Biol 10:1283-1286.
33. Fulton A, Reynaud X, Hansen R, Lemere CA, Parker C, Williams TP. 1999. Rod photoreceptors in infant rats with a history of oxygen exposure. Invest Ophthalmol Vis Sci 40:168-174.
34. Funatsu H, Yamashita H, Nakanishi Y, Hori S. 2002. Angiotensin II, vascular endothelial growth factor in the vitreous fluid of patients with proliferative diabetic retinopathy. Br J Ophthalmol 86: 311-315.
35. Gardiner TA, Gibson DS, de Gooyer T, de la Cruz VF, McDonald DM, Stitt AW. 2005. Inhibition of tumor necrosis factor-α improves physiological angiogenesis and reduces pathological neovascularization in ischemic retinopathy. Am J Pathol 166:637-644.
36. Graymore C. 1959. Metabolism of the developing retina. I. Aerobic and anaerobic glycolysis in the developing retina. Br J Ophthalmol 43:34-39.
37. Graymore C. 1960. Metabolism of the developing retina. III. Respiration in the developing rat retina and the effect on an inherited degeneration of the retinal neuro-epithelium. Br J Ophthalmol 44:363-369.
38. Gu X, Samuel S, El-shabrawey M, Caldwell RB, Bartoli M, Marcus DM, Brooks SE. 2002. Effects of sustained hyperoxia on revascularization in experimental retinopathy of prematurity. Invest Ophthalmol Vis Sci 43:496-502.
39. Guenther E, Schmid S, Hewig B, Kohler K. 1996. Two-fold effect of angiotensin II on voltage-dependent calcium currents in rat retinal ganglion cells. Brain Res 718:112-116.
40. Hamada Y, Hamda M, Yonemoto H. 1984. Histopathlogical studies of demarcation line and avascular area in very low birth weight infants. Folia Ophthalmol Jpn 35:2414-2419.
41. Higgins RD, Yan Y, Geng Y, Sharma J, Barr SM. 2003. Captopril and vascular endothelial growth factor in a mouse model of retinopathy. Curr Eye Res 27:123-129.
42. Hirschi KK, Rohovsky SA, Beck LH, Smith SR, D'Amore PA. 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.
43. Hoffmann J, Alt A, Lin J, Lochnit G, Schubert U, Schleicher E, Chavakis T, Brownlee M, Van der Woude FJ, Preissner KT, Hammes HP. 2006. Tenilsetam prevents early diabetic retinopathy without correcting pericyte loss. Thromb Haemost 95:689-695.
44. Hollander H, Makarov F, Dreher Z, van Driel D, Chan-Ling T, Stone J. 1991. Structure of the macrogha of the retina: Sharing and division of labour between astrocytes and Milller cells. J Comp Neurol 313: 587-603.
45. Hughes S, Chan-Ling T. 2004. Characterization of smooth muscle cell and pericyte differentiation in the rat retina in vivo. Invest Ophthalmol Vis Sci 45:2795-2806.
46. Hughes S, Gardiner TA, Baxter L, Chan-Ling T. 2007. Changes in pericytes and smooth muscle cells in the kitten model of retinopathy of prematurity: Implications for plus disease. Invest Ophthalmol Vis Sci 48:1368-1379.
47. Janzer RC, Raff MC. 1987. Astrocytes induce blood-brain barrier properties in endothelial cells. Nature 325:253-257.
48. Kagiyama T, Kagiyama S, Phillips MI. 2003. Expression of angiotensin type 1 and 2 receptors in brain after transient middle cerebral artery occlusion in rats. Regal Pept 110:241-247.
49. Kligman D, Hilt DC. 1988. The S-100 protein family. Trends Biochem 13:437-443.
50. Kohler K, Jurlikes B, Guenther E, Zrenner E. 1997. Angiotensin II in the rabbit retina. Vis Neurosci 14:63-71.
51. Konopatskaya O, Churchill AJ, Harper SJ, Bates DO, Gardiner TA. 2006. VEGF165b, an endogenous C-terminal splice inhibits retinal neovascularization in mice. Mol Vis 12:626-632.
52. Lonchampt M, Pennel L, Duhault J. 2001. Hyperoxia/normoxia-driven retinal angiogenesis in mice: A role for angiotensin II. Invest Ophthalmol Vis Sci 42:429-432.
53. Lui K, Akula JD, Falk C, Hansen RM, Fulton A.B. 2006a. The retinal vasculature and function of the neural retina in a rat model of retinopathy of prematurity. Invest Ophthalmol Vis Sci 47:2639-2647.
54. Lai K, Akula JD, Hansen RM, Moskowitz A, Kleinman MS, Fulton AB. 2006b. Development of the electroretinographic oscillatory potentials in norinal and ROP rats. Invest Ophthalmol Vis Sci 47:5447-5452.
55. Madan A, Penn JS. 2003. Animal models of oxygen-induced retinopathy. From Biosci 8:1030-1043.
56. Matea MR, Newman E. 2006. Glial cells dilate and constrict blood vessels: A mechanism of neurovascular coupling. J Neurosci 26:2862-2870.
57. McLeod DS, D'Anna S, Lutty G. 1998. Clinical and histopathologic features of canine oxygen-induced proliferative retinopathy. Invest Ophthalmol Vis Sci 39:1918-1932.
58. Montiel-Herrera M, Miledi R, Garcia-Colunga J. 2006. Membrane currents elicited by angiotensin II in astrocytes from the rat corpus callosum. Glia 53:366-371.
59. Moravski CJ, Kelly DJ, Cooper ME, Gilbert RE, Bertram JF, Shahinfar S, Skinner SL, Wilkinson-Berka JL. 2000. Retinal neovascularization is prevented by blockade of the renin-angiotensin system. Hypertension 36:1099-1104.
60. Murphy TJ, Alexandrer RW, Griendling KK, Runge MS, Bernstein KE. 1991. Isolation of a cDNA encoding the vascular type-1 angiotensin II receptor. Nature 351:233-236.
61. Nadal JA, Scicli GM, Carbini LA, Scicli AG. 2002. Angiotensin II stimulates migration of retinal microvascular pericytes: Involvement of TGF-β and PDGF-BB. Am J Physiol 282:11739-11748.
62. Nagai N, Noda K, Urano T, Kubota K, Shinoda H, Koto T, Shinoda K, Inoue M, Shiomi T, Ikeda E, Tsubota K, Suds, T, Oike Y, Ishida S. 2005. Selective suppression of pathologic, but not physiologic, retinal neovascularization by blocking the angiotensin II type-1 receptor. Invest Ophthalmol Vis Sci 46:1078-1084.
63. Nakase T, Sohl G, Theis M, Willecke K, Naus CC. 2004. Increased apoptosis and inflammation after focal brain ischemia in mice lacking connexin43 in astrocytes. Am J Pathol 164:2067-2075.
64. Novartis. 2006. Diovan/valsartan. New Jersey: East Hanover. pp 1-17.
65. Orlidge A, DAmore PA. 1987. Inhibition of capillary endothelial cell growth by pericytes and smooth muscle cells. J Cell Biol 105:1455-1462.
66. Otani A, Takagi H, Suzuma K, Honda Y. 1998. Angiotensin II potentiates endothelial growth factor-induced angiogenic activity in retinal microcapillary endothelial cells. Circ Res 82:619-628.
67. Penn JS, Thum LA, Rhem MN, Dell SJ. 1988. Effects of oxygen rearing on the electroretinogram and GFA-protein in the rat. Invest Ophthalmol Vis Sci 29:1623-1630.
68. Perio C, Rodriguez-Lopez AM, Angulo J, Regadera J, Maria J, Sanchez-Ferrer CF, Lopez-Novoa JM. 1998. Endogenous angiotensin II, cell hypertrophy in vascular smooth muscle cultures from hypertensive Ren-2 transgenic rats. Cell Physiol Biochem 8:106-116.
69. Riepe R, Norenburg M. 1977. Müller cell localisation of glutamine synthetase in rat retina. Nature 268:645-655.
70. Ritter MR, Banin E, Moreno SK, Aguilar E, Dorrell MI, Friedlander M. 2006. Myeloid progenitors differentiate into microglia and promote vascular repair in a model of ischemic retinopathy. J Clin Invest 116:3266-3276.
71. Sarlos S, Rizkalla B, Moravski CJ, Cao Z, Cooper ME, Wilkinson-Berka J. 2003. Retinal angiogenesis is mediated by an interaction between the angiotensin type-2 receptor, VEGF, and angiopoietin. Am J Pathol 163:879-887.
72. Sarlos S, Wilkinson-Berka JL. 2005. The renin-angiotensin system and the developing retinal vasculature. Invest Ophthalmol Vis Sci 46: 1069-1077.
73. Sasaki K, Yamano Y, Bardhan S, Iwai N, Murray JJ, Hasegawa M, Matsuda Y, Inagami T. 1991. Cloning and expression of a complementary DNA encoding a bovine adrenal angiotensin II type-1 receptor. Nature 351:230-233.
74. Sato T, Niwa M, Himeno A, Tsutumi K, Amemiya T. 1993. Quantitative receptor autoradiographic analysis for angiotensin II receptors in bovine retinal microvessels: Quantitation with radioluminography. Cell Mol Neurobiol 13:233-245.
75. Schnitzer J. 1988. Astrocytes in the guinea pig, horse, and monkey retina: Their occurrence coincides with the presence of blood vessels. Glia 1:74-89.
76. Stone J, Chan-Ling T, Pe'er J, Ito M, 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.
77. Stone J, Dreher Z. 1987. Relationships between astrocytes, ganglion cells and vasculature of the retina. J Comp Neurol 255:35-49.
78. Stone J, Itin A, Alon T, Pe'er J, Gnessin H, Chan-Ling T, Keshet E. 1995. Development of retinal vasculature is mediated by hypoxia-induced vascular endothelial growth factor (VEGF) expression by neuroglia. J Neurosci 15(7, Part 1):4738-4747.
79. Strettoi E, Porciatti V, Falsini B, Pignatelli V, Rossi C. 2002. Morphological and functional abnormalities in the inner retina of the rd/ rd mouse. J Neurosci 22:5492-5504.
80. Sumners C, Tang W, Paulding W, Raizada MK. 1994. Peptide receptors in astroglia: Focus on angiotensin II, atrial natriuretic peptide. Glia 11:110-116.
81. Sumners C, Tang W, Zelezna B, Raizada MK. 1991. Angiotensin II receptor subtypes are coupled with distinct signal-transduction mechanisms in neurons and astrocytes from rat brain. Proc Natl Acad Sci USA 88:7567-7571.
82. Tadesse M, Yan Y, Yossuck P, Higgins RD. 2001. Captopril improves retinal neovascularization via endothelin-1. Invest Ophthalmol Vis Sci 42:1867-1872.
83. Takuma K, Baba A, Matsuda T. 2004. Astrocyte apoptosis: Implications for neuroprotection. Prog Neurobiol 72:111-127.
84. Tao-Cheng J-H, Nagy Z, Brightman MW. 1987. Tight junctions of the brain endotheliurn in vitro are enhanced by astroglia. J Neurosci 7:3293-3299.
85. Tyler NK, Burns MS. 1991. Comparison of lectin reactivity in the vessel beds of the rat eye. Curr Eye Res 10:801-810.
86. Verbeek MM, Otte-Holler I, Wesseling P, Ruiter DJ, de Waal RM. 1994. Induction of α-smooth muscle actin expression in cultured human brain pericytes by transforming growth factor-β 1. Am J Pathol 144:372-382.
87. Wagner J, Danser AHJ, Derkx FHM, de Jong TV, Paul M, Mullins JJ, Schalekamp MA, Ganten D. 1996. Demonstration of renin mRNA, angiotensinogen mRNA, and angiotensin converting enzyme mRNA expression in the human eye: Evidence for an intraocular renin-angiotensin system. Br J Ophthalmol 80:159-163.
88. Wattanabe T, Raff MC. 1988. Retinal astrocytes are immigrants from the optic nerve. Nature 332:834-837.
89. Weidman TA, Kuwabara T. 1968. Postnatal development of the rat retina. Arch Ophthalmol 79:471-484.
90. Werdich XQ, Penn JS. 2006. Specific involvement of SRC family kinase activation in the pathogenesis of retinal neovascularization. Invest Ophthalmol Vis Sci 47:5047-5056.
91. Wheeler-Schilling TH, Kohler K, Sautter M, Guenther E. 1999. Angiotensin II receptor subtype gene expression and cellular localization in the retina and non-neuronal ocular tissues of the rat. Eur J Neurosci 11:3387-3394.
92. Wilkinson-Berka J, Babic S, de Gooyer T, Stitt AW, Jaworski K, Ong LGT, Kelly D, Gilbert R. 2004. Inhibition of platelet-derived growth factor promotes pericyte loss and angiogenesis in ischemic retinopathy. Am J Pathol 164:1263-1273.
93. Wilkinson-Berka JL, Fletcher EL. 2004. Angiotensin and bradykinin: Targets for the treatment of vascular and neuro-glial pathology in diabetic retinopathy. Curr Pharm Des 10:3313-3330.
94. Yamada H, Yamada E, Ando A, Seo MS, Esumi N, Okamoto N, Vinores M, LaRochelle W, Zack DJ, Campochiaro PA. 2000. Platelet-derived growth factor-A-induced retinal gliosis protects against ischemic retinopathy. Am J Pathol 156:477-487.
95. Yasuhara T, Shingo T, Date I. 2004. The potential role of vascular endothelial growth factor in the central nervous system. Rev Neurosci 15:293-307.
96. Zahs KR, Kofuji P, Meier C, Dermietzel R. 2003. Connexin immuno-reactivity in glial cells of the rat retina. J Comp Neurol 455:531-546.
97. Zhang Y, Porat RM, Alon T, Keshet E, Stone J. 1999. Tissue oxygen levels control astrocyte movement and differentiation in developing retina. Dev Brain Res 118:135-145.
98. Zhang Y, Stone J. 1997. Role of astrocytes in the control of developing retinal vessels. Invest Ophthalmol Vis Sci 38:1653-1666.