Inhibition of vitreoretinal VEGF elevation and blood-retinal barrier breakdown in streptozotocin-induced diabetic rats by brimonidine

Investigative Ophthalmology and Visual Science

Volumn 51, Issue 2, 2010, Pages 1044-1051

  Kusari, Jyotirmoy ^a   Zhou, Sheila X ^a   Padillo, Edwin ^a   Clarke, Kenneth G ^a   Gil, Daniel W ^a  

^a ALLERGAN INC   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

BRIMONIDINE; GLUCOSE; GLUTAMIC ACID; VASCULOTROPIN; ALPHA ADRENERGIC RECEPTOR STIMULATING AGENT; QUINOXALINE DERIVATIVE; VASCULAR ENDOTHELIAL GROWTH FACTOR A, RAT; VASCULOTROPIN A;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BLOOD RETINA BARRIER; BODY WEIGHT; BROWN NORWAY RAT; CONTINUOUS INFUSION; CONTROLLED STUDY; DRUG MECHANISM; GLUCOSE BLOOD LEVEL; HYPERGLYCEMIA; LONG EVANS RAT; MALE; NONHUMAN; OSMOTIC MINIPUMP; PRIORITY JOURNAL; PROTEIN ANALYSIS; PROTEIN EXPRESSION; RAT; STREPTOZOCIN DIABETES; ANIMAL; CAPILLARY PERMEABILITY; DRUG EFFECT; EXPERIMENTAL DIABETES MELLITUS; INFUSION PUMP; METABOLISM; RETINA; VITREOUS BODY; WESTERN BLOTTING;

ADRENERGIC ALPHA-AGONISTS; ANIMALS; BLOOD GLUCOSE; BLOOD-RETINAL BARRIER; BLOTTING, WESTERN; CAPILLARY PERMEABILITY; DIABETES MELLITUS, EXPERIMENTAL; GLUTAMIC ACID; INFUSION PUMPS; MALE; QUINOXALINES; RATS; RATS, INBRED BN; RATS, LONG-EVANS; RETINA; VASCULAR ENDOTHELIAL GROWTH FACTOR A; VITREOUS BODY;

EID: 77449100906     PISSN: 01460404     EISSN: 15525783     Source Type: Journal    
DOI: 10.1167/iovs.08-3293     Document Type: Article

References (55)

1. Kempen JH, O'Colmain BJ, Leske MC, et al. and the Eye Diseases Prevalence Research Group. The prevalence of diabetic retinopathy among adults in the United States. Arch Ophthalmol. 2004; 122(4):552-563.
2. Ciulla TA, Amador AG, Zinman B. Diabetic retinopathy and diabetic macular edema: pathophysiology, screening, and novel therapies. Diabetes Care. 2003;26(9):2653-2664.
3. Barber AJ. A new view of diabetic retinopathy: a neurodegenerative disease of the eye. Prog Neuropsychopharmacol Biol Psychiatry. 2003;27(2):283-290.
4. Wolter JR. Diabetic retinopathy. Am J Ophthalmol. 1961;51:1123-1141.
5. Bloodworth JM Jr. Diabetic retinopathy. Diabetes. 1962;11:1-22.
6. Alder VA, Su EN, Yu DY, Cringle S, Yu P. Overview of studies on metabolic and vascular regulatory changes in early diabetic retinopathy (published correction Aust N Z J Ophthalmol. 1998; 26(3):267). Aust N Z J Ophthalmol. 1998;26(2):141-148.
7. Kern TS. Contributions of inflammatory processes to the development of the early stages of diabetic retinopathy. Exp Diabetes Res. 2007;2007:95103.
8. Joussen AM, Murata T, Tsujikawa A, Kirchhof B, Bursell SE, Adamis AP. Leukocyte-mediated endothelial cell injury and death in the diabetic retina. Am J Pathol. 2001;158(1):147-152.
9. Zhang SX, Ma JX, Sima J, et al. Genetic difference in susceptibility to the blood-retina barrier breakdown in diabetes and oxygeninduced retinopathy. Am J Pathol. 2005;166(1):313-321.
10. Kusari J, Zhou S, Padillo E, Clarke KG, Gil DW. Effect of memantine on neuroretinal function and retinal vascular changes of streptozotocin-induced diabetic rats. Invest Ophthalmol Vis Sci. 2007; 48(11):5152-5159.
11. Barber AJ, Lieth E, Khin SA, Antonetti DA, Buchanan AG, Gardner TW. Neural apoptosis in the retina during experimental and human diabetes: early onset and effect of insulin. J Clin Invest. 1998;102(4):783-791.
12. Shweiki D, Itin A, Soffer D, Keshet E. Vascular endothelial growth factor induced by hypoxia may mediate hypoxia-initiated angiogenesis. Nature. 1992;359(6398):843-845.
13. Senger DR, Galli SJ, Dvorak AM, Perruzzi CA, Harvey VS, Dvorak HF. Tumor cells secrete a vascular permeability factor that promotes accumulation of ascites fluid. Science. 1983;219(4587):983-985.
14. Ishida S, Usui T, Yamashiro K, et al. VEGF164 is proinflammatory in the diabetic retina. Invest Ophthalmol Vis Sci. 2003;44(5): 2155-2162.
15. Qaum T, Xu Q, Joussen AM, et al. VEGF-initiated blood-retinal barrier breakdown in early diabetes. Invest Ophthalmol Vis Sci. 2001;42(10):2408-2413.
16. Costa RA, Jorge R, Calucci D, Melo LA Jr., Cardillo JA, Scott IU. Intravitreal bevacizumab (Avastin) for central and hemicentral retinal vein occlusions: IBeVO study. Retina. 2007;27(2):141-149.
17. Obrosova IG, Minchenko AG, Vasupuram R, et al. Aldose reductase inhibitor fidarestat prevents retinal oxidative stress and vascular endothelial growth factor overexpression in streptozotocin-diabetic rats. Diabetes. 2003;52(3):864-871.
18. Funatsu H, Yamashita H, Ikeda T, Nakanishi Y, Kitano S, Hori S. Angiotensin II and vascular endothelial growth factor in the vitreous fluid of patients with diabetic macular edema and other retinal disorders. Am J Ophthalmol. 2002;133(4):537-543.
19. Hernández C, Burgos R, Cantón A, García-Arumí J, Segura RM, Simó R. Vitreous levels of vascular cell adhesion molecule and vascular endothelial growth factor in patients with proliferative diabetic retinopathy: a case-control study. Diabetes Care. 2001; 24(3):516-521.
20. Ambati J, Chalam KV, Chawla DK, et al. Elevated gamma-aminobutyric acid, glutamate, and vascular endothelial growth factor levels in the vitreous of patients with proliferative diabetic retinopathy. Arch Ophthalmol. 1997;115(9):1161-1166.
21. Kowluru RA, Engerman RL, Case GL, Kern TS. Retinal glutamate in diabetes and effect of antioxidants. Neurochem Int. 2001;38(5): 385-390.
22. Lieth E, Barber AJ, Xu B, et al. Glial reactivity and impaired glutamate metabolism in short-term experimental diabetic retinopathy. Penn State Retina Research Group. Diabetes. 1998;47(5): 815-820.
23. Li Q, Puro DG. Diabetes-induced dysfunction of the glutamate transporter in retinal Müller cells. Invest Ophthalmol Vis Sci. 2002;43(9):3109-3116.
24. Ng YK, Zeng XX, Ling EA. Expression of glutamate receptors and calcium-binding proteins in the retina of streptozotocin-induced diabetic rats. Brain Res. 2004;1018(1):66-72.
25. Baptiste DC, Hartwick AT, Jollimore CA, et al. Comparison of the neuroprotective effects of adrenoceptor drugs in retinal cell culture and intact retina. Invest Ophthalmol Vis Sci. 2002;43(8): 2666-2676.
26. Dong CJ, Guo Y, Agey P, Wheeler L, Hare WA. Alpha2 adrenergic modulation of NMDA receptor function as a major mechanism of retinal ganglion cell protection in experimental glaucoma and retinal excitotoxicity. Invest Ophthalmol Vis Sci. 2008;49(10): 4515-4522.
27. Metoki T, Ohguro H, Ohguro I, Mamiya K, Ito T, Nakazawa M. Study of effects of antiglaucoma eye drops on N-methyl-D-aspartateinduced retinal damage. Jpn J Ophthalmol. 2005;49(6):453-461.
28. 2-Adrenoceptor agonists inhibit vitreal glutamate and aspartate accumulation and preserve retinal function after transient ischemia. J Pharmacol Exp Ther. 2001;296(1):216-223.
29. Mayor-Torroglosa S, De la Villa P, Rodríguez ME, et al. Ischemia results 3 months later in altered ERG, degeneration of inner layers, and deafferented tectum: neuroprotection with brimonidine. Invest Ophthalmol Vis Sci. 2005;46(10):3825-3835.
30. Vidal-Sanz M, Lafuente MP, Mayor S, de Imperial JM, Villegas-Pérez MP. Retinal ganglion cell death induced by retinal ischemia. neuroprotective effects of two alpha-2 agonists. Surv Ophthalmol. 2001;45(suppl 3):S261-S277.
31. Radius RL, Anderson DR. Distribution of albumin in the normal monkey eye as revealed by Evans blue fluorescence microscopy. Invest Ophthalmol Vis Sci. 1980;19(3):238-243.
32. Gao G, Li Y, Fant J, Crosson CE, Becerra SP, Ma JX. Difference in ischemic regulation of vascular endothelial growth factor and pigment epithelium-derived factor in Brown Norway and Sprague Dawley rats contributing to different susceptibilities to retinal neovascularization. Diabetes. 2002;51(4):1218-1225.
33. Bates DO, Lodwick D, Williams B. Vascular endothelial growth factor and microvascular permeability. Microcirculation. 1999;6: 83-96.
34. Ferris FL 3rd, Patz A. Macular edema. A complication of diabetic retinopathy. Surv Ophthalmol. 1984;28(suppl):452-461.
35. Murata T, Nakagawa K, Khalil A, Ishibashi T, Inomata H, Sueishi K. The relation between expression of vascular endothelial growth factor and breakdown of the blood-retinal barrier in diabetic rat retinas. Lab Invest. 1996;74(4):819-825.
36. Aiello LP, Avery RL, Arrigg PG, et al. Vascular endothelial growth factor in ocular fluid of patients with diabetic retinopathy and other retinal disorders. N Engl J Med. 1994;331(22):1480-1487.
37. Hammes HP, Lin J, Bretzel RG, Brownlee M, Breier G. Upregulation of the vascular endothelial growth factor/vascular endothelial growth factor receptor system in experimental background diabetic retinopathy of the rat. Diabetes. 1998;47(3):401-406.
38. Funatsu H, Yamashita H. Pathophysiology of diabetic retinopathy. Drug News Perspect. 2002;15(10):633-639.
39. Rosa RH Jr., Hein TW, Yuan Z, et al. Brimonidine evokes heterogeneous vasomotor response of retinal arterioles: diminished nitric oxide-mediated vasodilation when size goes small. Am J Physiol Heart Circ Physiol. 2006;291(1):H231-H238.
40. Lagrèze WA, Knörle R, Bach M, Feuerstein TJ. Memantine is neuroprotective in a rat model of pressure-induced retinal ischemia. Invest Ophthalmol Vis Sci. 1998;39(6):1063-1066.
41. Wang K, Wang Y, Gao L, Li X, Li M, Guo J. Dexamethasone inhibits leukocyte accumulation and vascular permeability in retina of streptozotocin-induced diabetic rats via reducing vascular endothelial growth factor and intercellular adhesion molecule-1 expression. Biol Pharm Bull. 2008;31(8):1541-1546.
42. Gerhardinger C, Costa MB, Coulombe MC, Toth I, Hoehn T, Grosu P. Expression of acute-phase response proteins in retinal Müller cells in diabetes. Invest Ophthalmol Vis Sci. 2005;46(1):349-357.
43. Brucklacher RM, Patel KM, VanGuilder HD, et al. Whole genome assessment of the retinal response to diabetes reveals a progressive neurovascular inflammatory response. BMC Med Genomics. 200813;1:26.
44. Chung HK, Choi SM, Ahn BO, Kwak HH, Kim JH, Kim WB. Efficacy of troxerutin on streptozotocin-induced rat model in the early stage of diabetic retinopathy. Arzneimittelforschung. 2005; 55(10):573-580.
45. Liu W, Yuen EY, Allen PB, Feng J, Greengard P, Yan Z. Adrenergic modulation of NMDA receptors in prefrontal cortex is differentially regulated by RGS proteins and spinophilin. Proc Natl Acad Sci U S A. 2006;103(48):18338-18343.
46. Zhang J, Diamond JS. Distinct perisynaptic and synaptic localization of NMDA and AMPA receptors on ganglion cells in rat retina. J Comp Neurol. 2006;498(6):810-820.
47. Taylor S, Srinivasan B, Wordinger RJ, Roque RS. Glutamate stimulates neurotrophin expression in cultured Müller cells. Brain Res Mol Brain Res. 2003;111(1-2):189-197.
48. Kalapesi FB, Coroneo MT, Hill MA. Human ganglion cells express the alpha-2 adrenergic receptor: relevance to neuroprotection. Br J Ophthalmol. 2005;89(6):758-763.
49. Gao H, Qiao X, Gao R, Mieler WF, McPherson AR, Holz ER. Intravitreal triamcinolone does not alter basal vascular endothelial growth factor mRNA expression in rat retina. Vision Res. 2004; 44(4):349-356.
50. Zhang SX, Wang JJ, Gao G, Parke K, Ma JX. Pigment epitheliumderived factor downregulates vascular endothelial growth factor (VEGF) expression and inhibits VEGF-VEGF receptor 2 binding in diabetic retinopathy. J Mol Endocrinol. 2006;37(1):1-12.
51. Jonas JB. Intravitreal triamcinolone acetonide for treatment of intraocular oedematous and neovascular diseases. Acta Ophthalmol Scand. 2005;83(6):645-663.
52. Zhang X, Bao S, Lai D, Rapkins RW, Gillies MC. Intravitreal triamcinolone acetonide inhibits breakdown of the blood-retinal barrier through differential regulation of VEGF-A and its receptors in early diabetic rat retinas. Diabetes. 2008;57(4):1026-1033.
53. Cantor LB. Brimonidine in the treatment of glaucoma and ocular hypertension. Ther Clin Risk Manag. 2006;2(4):337-346.
54. Wheeler L, WoldeMussie E, Lai R. Role of alpha-2 agonists in neuroprotection. Surv Ophthalmol. 2003;48(suppl 1):S47-S51.
55. Mondal LK, Baidya KP, Bhattacharya B, Chatterjee PR, Bhaduri G. The efficacy of topical administration of BRI to reduce ischaemia in the very early stage of diabetic retinopathy in good controlled type-2 diabetes mellitus. J Indian Med Assoc. 2004;102(12):724-725, 729.