The vasoneuronal effects of AT1 receptor blockade in a rat model of retinopathy of prematurity

Investigative Ophthalmology and Visual Science

Volumn 55, Issue 6, 2014, Pages 3957-3970

  Hatzopoulos, Kate M ^a   Vessey, Kirstan A ^a   Wilkinson Berka, Jennifer L ^b   Fletcher, Erica L ^a  

^a UNIVERSITY OF MELBOURNE   (Australia)

^b MONASH UNIVERSITY   (Australia)

Author keywords

Electroretinogram; Hypoxia; Neovascularization; Oxygen induced retinopathy; Retinopathy of prematurity; Valsartan

Indexed keywords

ANGIOTENSIN 1 RECEPTOR; VALSARTAN; ANGIOTENSIN 1 RECEPTOR ANTAGONIST; DRUG DERIVATIVE; OXYGEN; TETRAZOLE DERIVATIVE; VALINE;

ANGIOGENESIS; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BLOOD VESSEL; BRAIN DYSFUNCTION; CELL ACTIVATION; CELL COUNT; CELL STRUCTURE; CONFOCAL MICROSCOPY; CONTROLLED STUDY; ELECTRORETINOGRAPHY; IMMUNOCYTOCHEMISTRY; IMMUNOHISTOCHEMISTRY; INFLAMMATION; MICROGLIA; NEWBORN; NONHUMAN; OSCILLATORY POTENTIAL; OXYGEN-INDUCED RETINOPATHY; PRIORITY JOURNAL; RAT; RECEPTOR BLOCKING; RETINA CONE; RETINA NEOVASCULARIZATION; RETINA ROD; RETROLENTAL FIBROPLASIA; VITREOUS BODY; ANIMAL; DISEASE MODEL; DRUG EFFECT; ELECTRORETINOGRAM; FEMALE; FLUORESCENT ANTIBODY TECHNIQUE; HYPOXIA; NEOVASCULARIZATION (PATHOLOGY); PATHOLOGY; PATHOPHYSIOLOGY; PHOTORECEPTOR CELL; PHOTOSTIMULATION; PHYSIOLOGY; RETINA BLOOD VESSEL; SPRAGUE DAWLEY RAT;

ELECTRORETINOGRAM; HYPOXIA; NEOVASCULARIZATION; OXYGEN-INDUCED RETINOPATHY; RETINOPATHY OF PREMATURITY; VALSARTAN;

ANGIOTENSIN II TYPE 1 RECEPTOR BLOCKERS; ANIMALS; ANIMALS, NEWBORN; DISEASE MODELS, ANIMAL; ELECTRORETINOGRAPHY; FEMALE; FLUORESCENT ANTIBODY TECHNIQUE, INDIRECT; MICROGLIA; MICROSCOPY, CONFOCAL; OXYGEN; PHOTIC STIMULATION; PHOTORECEPTOR CELLS, VERTEBRATE; RATS; RATS, SPRAGUE-DAWLEY; RECEPTOR, ANGIOTENSIN, TYPE 1; RETINAL NEOVASCULARIZATION; RETINAL VESSELS; RETINOPATHY OF PREMATURITY; TETRAZOLES; VALINE;

EID: 84903178860     PISSN: 01460404     EISSN: 15525783     Source Type: Journal    
DOI: 10.1167/iovs.13-13532     Document Type: Article

References (82)

1. Hellstrom A, Smith LE, Dammann O. Retinopathy of prematurity. Lancet. 2013;382:1445-1257.
2. Gilbert C, Fielder A, Gordillo L, et al. Characteristics of infants with severe retinopathy of prematurity in countries with low, moderate, and high levels of development: implications for screening programs. Pediatrics. 2005;115:e518-e525.
3. Austeng D, Kallen KB, Ewald UW, Jakobsson PG, Holmstrom GE. Incidence of retinopathy of prematurity in infants born before 27 weeks' gestation in Sweden. Arch Ophthalmol. 2009;127:1315-1319.
4. Fletcher EL, Downie LE, Hatzopoulos K, et al. The significance of neuronal and glial cell changes in the rat retina during oxygen-induced retinopathy. Doc Ophthalmol. 2010;120:67-86.
5. Connor KM, Krah NM, Dennison RJ, et al. Quantification of oxygen-induced retinopathy in the mouse: a model of vessel loss, vessel regrowth and pathological angiogenesis. Nat Protoc. 2009;4:1565-1573.
6. Stahl A, Connor KM, Sapieha P, et al. Computer-aided quantification of retinal neovascularization. Angiogenesis. 2009;12:297-301.
7. Fulton AB, Hansen RM, Moskowitz A, Akula JD. The neurovascular retina in retinopathy of prematurity. Prog Retin Eye Res. 2009;28:452-482.
8. Barnaby AM, Hansen RM, Moskowitz A, Fulton AB. Development of scotopic visual thresholds in retinopathy of prematurity. Invest Ophthalmol Vis Sci. 2007;48:4854-4860.
9. Fulton AB, Hansen RM. Photoreceptor function in infants and children with a history of mild retinopathy of prematurity. J Opt Soc Am A Opt Image Sci Vis. 1996;13:566-571.
10. Vessey KA, Wilkinson-Berka JL, Fletcher EL. Characterization of retinal function and glial cell response in a mouse model of oxygen-induced retinopathy. J Comp Neurol. 2011;519:506-527.
11. Downie LE, Pianta MJ, Vingrys AJ, Wilkinson-Berka JL, Fletcher EL. Neuronal and glial cell changes are determined by retinal vascularization in retinopathy of prematurity. J Comp Neurol. 2007;504:404-417.
12. Downie LE, Hatzopoulos KM, Pianta MJ, et al. Angiotensin type-1 receptor inhibition is neuroprotective to amacrine cells in a rat model of retinopathy of prematurity. J Comp Neurol. 2010;518:41-63.
13. Fletcher EL, Phipps JA, Ward MM, Vessey KA, Wilkinson-Berka JL. The renin-angiotensin system in retinal health and disease: Its influence on neurons, glia and the vasculature. Prog Retin Eye Res. 2010;29:284-311.
14. 1) and type 2 (AT2) receptors in the rat retina. Neuroscience. 2009;161:195-213.
15. Berka JL, Stubbs AJ, Wang DZ, et al. Renin-containing Muller cells of the retina display endocrine features. Invest Ophthalmol Vis Sci. 1995;36:1450-1458.
16. Yokota H, Nagaoka T, Mori F, et al. Prorenin levels in retinopathy of prematurity. Am J Ophthalmol. 2007;143: 531-533.
17. Moravski CJ, Kelly DJ, Cooper ME, et al. Retinal neovascularization is prevented by blockade of the renin-angiotensin system. Hypertension. 2000;36:1099-1104.
18. 1 receptor inhibition prevents astrocyte degeneration and restores vascular growth in oxygen-induced retinopathy. Glia. 2008;56:1076-1090.
19. Tadesse M, Yan Y, Yossuck P, Higgins RD. Captopril improves retinal neovascularization via endothelin-1. Invest Ophthalmol Vis Sci. 2001;42:1867-1872.
20. Deliyanti D, Miller AG, Tan G, Binger KJ, Samson AL, Wilkinson-Berka JL. Neovascularization is attenuated with aldosterone synthase inhibition in rats with retinopathy. Hypertension. 2012;59:607-613.
21. Sarlos S, Rizkalla B, Moravski CJ, Cao Z, Cooper ME, Wilkinson- Berka JL. Retinal angiogenesis is mediated by an interaction between the angiotensin type 2 receptor, VEGF, and angiopoietin. Am J Pathol. 2003;163:879-887.
22. Phipps JA, Wilkinson-Berka JL, Fletcher EL. Retinal dysfunction in diabetic ren-2 rats is ameliorated by treatment with valsartan but not atenolol. Invest Ophthalmol Vis Sci. 2007; 48:927-934.
23. Gao G, Li Y, Zhang D, Gee S, Crosson C, Ma J. Unbalanced expression of VEGF and PEDF in ischemia-induced retinal neovascularization. FEBS Lett. 2001;489:270-276.
24. Phipps JA, Fletcher EL, Vingrys AJ. Paired-flash identification of rod and cone dysfunction in the diabetic rat. Invest Ophthalmol Vis Sci. 2004;45:4592-4600.
25. Weymouth AE, Vingrys AJ. Rodent electroretinography: methods for extraction and interpretation of rod and cone responses. Prog Retin Eye Res. 2008;27:1-44.
26. Nixon PJ, Bui BV, Armitage JA, Vingrys AJ. The contribution of cone responses to rat electroretinograms. Clin Experiment Ophthalmol. 2001;29:193-196.
27. Vessey KA, Fletcher EL. Rod and cone pathway signalling is altered in the P2X7 receptor knock out mouse. PLoS One. 2012;7:e29990.
28. Lyubarsky AL, Pugh EN Jr. Recovery phase of the murine rod photoresponse reconstructed from electroretinographic recordings. J Neurosci. 1996;16:563-571.
29. Hood DC, Birch DG. A quantitative measure of the electrical activity of human rod photoreceptors using electroretinography. Vis Neurosci. 1990;5:379-387.
30. Szél A, Röhlich P. Two cone types of rat retina detected by antivisual pigment antibodies. Exp Eye Res. 1992;55:47-52.
31. Cho EY, Choi HL, Chan FL. Expression pattern of glycoconjugates in rat retina as analysed by lectin histochemistry. Histochem J. 2002;34:589-600.
32. Tyler NK, Burns MS. Comparison of lectin reactivity in the vessel beds of the rat eye. Curr Eye Res. 1991;10:801-810.
33. Lynch MA. The multifaceted profile of activated microglia. Mol Neurobiol. 2009;40:139-156.
34. Opie NL, Greferath U, Vessey KA, et al. Retinal prosthesis safety: alterations in microglia morphology due to thermal damage and retinal implant contact. Invest Ophthalmol Vis Sci. 2012;53:7802-7812.
35. Wilkinson-Berka JL, Heine R, Tan G, et al. RILLKKMPSV influences the vasculature, neurons and glia, and (pro)rennin receptor expression in the retina. Hypertension. 2010;55: 1454-1460.
36. Hanisch UK, Kettenmann H. Microglia: active sensor and versatile effector cells in the normal and pathologic brain. Nat Neurosci. 2007;10:1387-1394.
37. McCarthy CA, Widdop RE, Deliyanti D, Wilkinson-Berka JL. Brain and retinal microglia in health and disease: an unrecognized target of the renin-angiotensin system. Clin Exp Pharmacol Physiol. 2013;40:571-579.
38. Rivera JC, Sitaras N, Noueihed B, et al. Microglia and interleukin-1beta in ischemic retinopathy elicit microvascular degeneration through neuronal semaphorin-3A. Arterioscler Thromb Vasc Biol. 2013;33:1881-1891.
39. Lonchampt M, Pennel L, Duhault J. Hyperoxia/normoxiadriven retinal angiogenesis in mice: a role for angiotensin II. Invest Ophthalmol Vis Sci. 2001;42:429-432.
40. Wilkinson-Berka JL, Fletcher EL. Angiotensin and bradykinin: targets for the treatment of vascular and neuro-glial pathology in diabetic retinopathy. Curr Pharm Des. 2004;10:3313-3330.
41. Nagai N, Noda K, Urano T, et al. Selective suppression of pathologic, but not physiologic, retinal neovascularization by blocking the angiotensin II type 1 receptor. Invest Ophthalmol Vis Sci. 2005;46:1078-1084.
42. Wilkinson-Berka JL, Tan G, Binger KJ, et al. Aliskiren reduces vascular pathology in diabetic retinopathy and oxygeninduced retinopathy in the transgenic (mRen-2)27 rat. Diabetologia. 2011;54:2724-2735.
43. Sarlos S, Wilkinson-Berka JL. The renin-angiotensin system and the developing retinal vasculature. Invest Ophthalmol Vis Sci. 2005;46:1069-1077.
44. Ishida S, Usui T, Yamashiro K, et al. VEGF164 is proinflammatory in the diabetic retina. Invest Ophthalmol Vis Sci. 2003;44: 2155-2162.
45. Zhao L, Ma W, Fariss RN, Wong WT. Retinal vascular repair and neovascularization are not dependent on CX3CR1 signaling in a model of ischemic retinopathy. Exp Eye Res. 2009;88:1004-1013.
46. Checchin D, Sennlaub F, Levavasseur E, Leduc M, Chemtob S. Potential role of microglia in retinal blood vessel formation. Invest Ophthalmol Vis Sci. 2006;47:3595-3602.
47. Davies MH, Eubanks JP, Powers MR. Microglia and macrophages are increased in response to ischemia-induced retinopathy in the mouse retina. Mol Vis. 2006;12:467-477.
48. Davies MH, Stempel AJ, Powers MR. MCP-1 deficiency delays regression of pathologic retinal neovascularization in a model of ischemic retinopathy. Invest Ophthalmol Vis Sci. 2008;49: 4195-4202.
49. Biber K, Neumann H, Inoue K, Boddeke HW. Neuronal 'on' and 'off' signals control microglia. Trends Neurosci. 2007;30: 596-602.
50. Biber K, Sauter A, Brouwer N, Copray SC, Boddeke HW. Ischemia-induced neuronal expression of the microglia attracting chemokine secondary lymphoid-tissue chemokine (SLC). Glia. 2001;34:121-133.
51. de Cavanagh EM, Piotrkowski B, Fraga CG. Concerted action of the renin-angiotensin system, mitochondria, and antioxidant defenses in aging. Mol Aspects Med. 2004;25:27-36.
52. Han Y, Runge MS, Brasier AR. Angiotensin II induces interleukin-6 transcription in vascular smooth muscle cells through pleiotropic activation of nuclear factor-kappa B transcription factors. Circ Res. 1999;84:695-703.
53. Moeller I, Allen AM, Chai SY, Zhuo J, Mendelsohn FA. Bioactive angiotensin peptides. J Hum Hypertens. 1998;12:289-293.
54. Schiffrin EL. Vascular and cardiac benefits of angiotensin receptor blockers. Am J Med. 2002;113:409-418.
55. Fletcher EL, Phipps JA, Ward MM, Vessey KA, Wilkinson-Berka JL. The renin-angiotensin system in retinal health and disease: its influence on neurons, glia and the vasculature. Prog Retin Eye Res. 2010;29:284-311.
56. 1) signaling in astrocytes regulates synaptic degeneration-induced leukocyte entry to the central nervous system. Brain Behav Immun. 2010;25:897-904.
57. Miyoshi M, Miyano K, Moriyama N, Taniguchi M, Watanabe T. Angiotensin type 1 receptor antagonist inhibits lipopolysaccharide- induced stimulation of rat microglial cells by suppressing nuclear factor kappaB and activator protein-1 activation. Eur J Neurosci. 2008;27:343-351.
58. Nagai A, Nakagawa E, Hatori K, et al. Generation and characterization of immortalized human microglial cell lines: expression of cytokines and chemokines. Neurobiol Dis. 2001;8:1057-1068.
59. Pastore L, Tessitore A, Martinotti S, et al. Angiotensin II stimulates intercellular adhesion molecule-1 (ICAM-1) expression by human vascular endothelial cells and increases soluble ICAM-1 release in vivo. Circulation. 1999;100:1646-1652.
60. Suzuki Y, Ruiz-Ortega M, Lorenzo O, Ruperez M, Esteban V, Egido J. Inflammation and angiotensin II. Int J Biochem Cell Biol. 2003;35:881-900.
61. Satofuka S, Ichihara A, Nagai N, et al. Role of nonproteolytically activated prorenin in pathologic, but not physiologic, retinal neovascularization. Invest Ophthalmol Vis Sci. 2007; 48:422-429.
62. Satofuka S, Ichihara A, Nagai N, et al. Suppression of ocular inflammation in endotoxin-induced uveitis by inhibiting nonproteolytic activation of prorenin. Invest Ophthalmol Vis Sci. 2006;47:2686-2692.
63. Wilkinson-Berka JL, Campbell DJ. (Pro)renin receptor: a treatment target for diabetic retinopathy? Diabetes. 2009;58: 1485-1487.
64. Fulton AB, Hansen RM, Petersen RA, Vanderveen DK. The rod photoreceptors in retinopathy of prematurity: an electroretinographic study. Arch Ophthalmol. 2001;119:499-505.
65. Fulton AB, Hansen RM, Westall CA. Development of ERG responses: the ISCEV rod, maximal and cone responses in normal subjects. Doc Ophthalmol. 2003;107:235-241.
66. Dembinska O, Rojas LM, Chemtob S, Lachapelle P. Evidence for a brief period of enhanced oxygen susceptibility in the rat model of oxygen-induced retinopathy. Invest Ophthalmol Vis Sci. 2002;43:2481-2490.
67. Fulton AB, Dodge J, Hansen RM, Williams TP. The rhodopsin content of human eyes. Invest Ophthalmol Vis Sci. 1999;40: 1878-1883.
68. Cringle SJ, Yu DY. Oxygen supply and consumption in the retina: implications for studies of retinopathy of prematurity. Doc Ophthalmol. 2010;120:99-109.
69. Cringle SJ, Yu DY, Yu PK, Su EN. Intraretinal oxygen consumption in the rat in vivo. Invest Ophthalmol Vis Sci. 2002;43:1922-1927.
70. Shao Z, Dorfman AL, Seshadri S, et al. Choroidal involution is a key component of oxygen-induced retinopathy. Invest Ophthalmol Vis Sci. 2011;52:6238-6248.
71. Lachapelle P, Dembinska O, Rojas LM, Benoit J, Almazan G, Chemtob S. Persistent functional and structural retinal anomalies in newborn rats exposed to hyperoxia. Can J Physiol Pharmacol. 1999;77:48-55.
72. Reynaud X, Dorey CK. Extraretinal neovascularization induced by hypoxic episodes in the neonatal rat. Invest Ophthalmol Vis Sci. 1994;35:3169-3177.
73. Wachtmeister L. Oscillatory potentials in the retina: what do they reveal. Prog Retin Eye Res. 1998;17:485-521.
74. Dijk F, Kamphuis W. An immunocytochemical study on specific amacrine cell subpopulations in the rat retina after ischemia. Brain Res. 2004;1026:205-217.
75. Osborne NN, Casson RJ, Wood JP, Chidlow G, Graham M, Melena J. Retinal ischemia: mechanisms of damage and potential therapeutic strategies. Prog Retin Eye Res. 2004; 23:91-147.
76. Bloomfield SA, Dacheux RF. Rod vision: pathways and processing in the mammalian retina. Prog Retin Eye Res. 2001;20:351-384.
77. Akula JD, Hansen RM, Martinez-Perez ME, Fulton AB. Rod photoreceptor function predicts blood vessel abnormality in retinopathy of prematurity. Invest Ophthalmol Vis Sci. 2007; 48:4351-4359.
78. Akula JD, Mocko JA, Moskowitz A, Hansen RM, Fulton AB. The oscillatory potentials of the dark-adapted electroretinogram in retinopathy of prematurity. Invest Ophthalmol Vis Sci. 2007; 48:5788-5797.
79. Hansen RM, Fulton AB. Rod-mediated increment threshold functions in infants. Invest Ophthalmol Vis Sci. 2000;41: 4347-4352.
80. Reisner DS, Hansen RM, Findl O, Petersen RA, Fulton AB. Darkadapted thresholds in children with histories of mild retinopathy of prematurity. Invest Ophthalmol Vis Sci. 1997; 38:1175-1183.
81. 1R and AT2R signaling in retinal inflammation. Invest Ophthalmol Vis Sci. 2006;47:5545-5552.
82. Clermont A, Bursell SE, Feener EP. Role of the angiotensin II type 1 receptor in the pathogenesis of diabetic retinopathy: effects of blood pressure control and beyond. J Hypertens Suppl. 2006;24:S73-S80.