Susceptibility of streptozotocin-induced diabetic rat retinal function and ocular blood flow to acute intraocular pressure challenge

Investigative Ophthalmology and Visual Science

Volumn 54, Issue 3, 2013, Pages 2133-2141

  Wong, Vickie H Y ^a   Vingrys, Algis J ^a   Jobling, Andrew I ^a   Bui, Bang V ^a  

^a UNIVERSITY OF MELBOURNE   (Australia)

Author keywords

[No Author keywords available]

Indexed keywords

ENDOTHELIAL NITRIC OXIDE SYNTHASE; NEURONAL NITRIC OXIDE SYNTHASE; STREPTOZOCIN;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; B WAVE; CONTROLLED STUDY; DIABETES MELLITUS; ELECTROPHYSIOLOGY; ELECTRORETINOGRAPHY; EVOKED RESPONSE; EYE BLOOD FLOW; INTRAOCULAR PRESSURE; LASER DOPPLER FLOWMETRY; MALE; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; REAL TIME POLYMERASE CHAIN REACTION; RETINA GANGLION CELL; SPECTROPHOTOMETRY; VISUAL SYSTEM FUNCTION;

ANIMALS; ANTIBIOTICS, ANTINEOPLASTIC; DIABETES MELLITUS, EXPERIMENTAL; DISEASE MODELS, ANIMAL; DISEASE SUSCEPTIBILITY; ELECTRORETINOGRAPHY; EYE; INTRAOCULAR PRESSURE; NITRIC OXIDE SYNTHASE; OCULAR HYPERTENSION; POLYMERASE CHAIN REACTION; RATS; RATS, LONG-EVANS; RETINA; RNA, MESSENGER; STREPTOZOCIN;

EID: 84875647810     PISSN: 01460404     EISSN: 15525783     Source Type: Journal    
DOI: 10.1167/iovs.13-11595     Document Type: Article

References (62)

1. Aiello LP. Angiogenic pathways in diabetic retinopathy. N Engl J Med. 2005;353:839-841.
2. Barber AJ. A new view of diabetic retinopathy: a neurodegenerative disease of the eye. Prog Neuropsychopharmacol Biol Psychiatry. 2003;27:283-290.
3. Parisi V, Uccioli L. Visual electrophysiological responses in persons with type 1 diabetes. Diabetes Metab Res Rev. 2001; 17:12-18.
4. Holopigian K, Seiple W, Lorenzo M, Carr R. A comparison of photopic and scotopic electroretinographic changes in early diabetic retinopathy. Invest Ophthalmol Vis Sci. 1992;33: 2773-2780.
5. Bearse MA Jr, Adams AJ, Han Y, et al. A multifocal electroretinogram model predicting the development of diabetic retinopathy. Prog Retin Eye Res. 2006;25:425-448.
6. Harrison WW, Bearse MA Jr, Ng JS, et al. Multifocal electroretinograms predict onset of diabetic retinopathy in adult patients with diabetes. Invest Ophthalmol Vis Sci. 2011; 52:772-777.
7. Bursell SE, Clermont AC, Kinsley BT, Simonson DC, Aiello LM, Wolpert HA. Retinal blood flow changes in patients with insulin-dependent diabetes mellitus and no diabetic retinopathy. Invest Ophthalmol Vis Sci. 1996;37:886-897.
8. Burgansky-Eliash Z, Nelson DA, Bar-Tal OP, Lowenstein A, Grinvald A, Barak A. Reduced retinal blood flow velocity in diabetic retinopathy. Retina. 2010;30:765-773.
9. Lasta M, Pemp B, Schmidl D, et al. Neurovascular dysfunction precedes neural dysfunction in the retina of patients with type 1 diabetes. Invest Ophthalmol Vis Sci. 2013;54:842-847.
10. Cringle SJ, Yu DY, Alder VA, Su EN. Retinal blood flow by hydrogen clearance polarography in the streptozotocininduced diabetic rat. Invest Ophthalmol Vis Sci. 1993;34: 1716-1721.
11. Justesen BL, Mistry P, Chaturvedi N, et al. Retinal arterioles have impaired reactivity to hyperoxia in type 1 diabetes. Acta Ophthalmol. 2010;88:453-457.
12. Nguyen TT, Kawasaki R, Wang JJ, et al. Flicker light-induced retinal vasodilation in diabetes and diabetic retinopathy. Diabetes Care. 2009;32:2075-2080.
13. Mandecka A, Dawczynski J, Vilser W, et al. Abnormal retinal autoregulation is detected by provoked stimulation with flicker light in well-controlled patients with type 1 diabetes without retinopathy. Diabetes Res Clin Pract. 2009;86:51-55.
14. Kern TS, Tang J, Berkowitz BA. Validation of structural and functional lesions of diabetic retinopathy in mice. Mol Vis. 2010;16:2121-2131.
15. Quigley HA, Broman AT. The number of people with glaucoma worldwide in 2010 and 2020. Br J Ophthalmol. 2006;90:262-267.
16. Wong VH, Bui BV, Vingrys AJ. Clinical and experimental links between diabetes and glaucoma. Clin Exp Optom. 2011;94:4-23.
17. Kanamori A, Nakamura M, Mukuno H, Maeda H, Negi A. Diabetes has an additive effect on neural apoptosis in rat retina with chronically elevated intraocular pressure. Curr Eye Res. 2004;28:47-54.
18. Kohzaki K, Vingrys AJ, Armitage JA, Bui BV. Electroretinography in streptozotocin diabetic rats following acute intraocular pressure elevation. Graefes Arch Clin Exp Ophthalmol. 2012; 251:529-535.
19. Arango-Gonzalez B, Schatz A, Bolz S, et al. Effects of combined ketamine/xylazine anesthesia on light induced retinal degeneration in rats. PloS One. 2012;7:e35687.
20. Bui BV, Edmunds B, Cioffi GA, Fortune B. The gradient of retinal functional changes during acute intraocular pressure elevation. Invest Ophthalmol Vis Sci. 2005;46:202-213.
21. Hood DC, Birch DG. The A-wave of the human electroretinogram and rod receptor function. Invest Ophthalmol Vis Sci. 1990;31:2070-2081.
22. Stockton RA, Slaughter MM. B-wave of the electroretinogram. A reflection of ON bipolar cell activity. J Gen Physiol. 1989;93: 101-122.
23. Saszik SM, Robson JG, Frishman LJ. The scotopic threshold response of the dark-adapted electroretinogram of the mouse. J Physiol. 2002;543:899-916.
24. Bui BV, Fortune B. Ganglion cell contributions to the rat fullfield electroretinogram. J Physiol. 2004;555:153-173.
25. Frishman LJ, Sieving PA, Steinberg RH. Contributions to the electroretinogram of currents originating in proximal retina. Vis Neurosci. 1988;1:307-315.
26. Casson RJ, Chidlow G, Wood JP, Osborne NN. The effect of hyperglycemia on experimental retinal ischemia. Arch Ophthalmol. 2004;122:361-366.
27. He Z, Nguyen CT, Armitage JA, Vingrys AJ, Bui BV. Blood pressure modifies retinal susceptibility to intraocular pressure elevation. PloS One. 2012;7:e31104.
28. Chauhan BC, LeVatte TL, Jollimore CA, et al. Model of endothelin-1-induced chronic optic neuropathy in rat. Invest Ophthalmol Vis Sci. 2004;45:144-152.
29. Kiel JW, Shepherd AP. Autoregulation of choroidal blood flow in the rabbit. Invest Ophthalmol Vis Sci. 1992;33:2399-2410.
30. Riva CE, Cranstoun SD, Mann RM, Barnes GE. Local choroidal blood flow in the cat by laser Doppler flowmetry. Invest Ophthalmol Vis Sci. 1994;35:608-618.
31. Lamb TD, Pugh EN Jr. A quantitative account of the activation steps involved in phototransduction in amphibian photoreceptors. J Physiol. 1992;449:719-758.
32. Hood DC, Birch DG. A computational model of the amplitude and implicit time of the b-wave of the human ERG. Vis Neurosci. 1992;8:107-126.
33. Maloney LT. Confidence intervals for the parameters of psychometric functions. Percept Psychophys. 1990;47:127-134.
34. Foster DH, Bischof WF. Bootstrap variance estimators for the parameters of small-sample sensory-performance functions. Biol Cybern. 1987;57:341-347.
35. Bui BV, Weisinger HS, Sinclair AJ, Vingrys AJ. Comparison of guinea pig electroretinograms measured with bipolar corneal and unipolar intravitreal electrodes. Doc Ophthalmol. 1998; 95:15-34.
36. Klein R, Klein BE, Moss SE, Cruickshanks KJ. The Wisconsin Epidemiologic Study of Diabetic Retinopathy: XVII. The 14-year incidence and progression of diabetic retinopathy and associated risk factors in type 1 diabetes. Ophthalmology. 1998;105:1801-1815.
37. Giove TJ, Deshpande MM, Gagen CS, Eldred WD. Increased neuronal nitric oxide synthase activity in retinal neurons in early diabetic retinopathy. Mol Vis. 2009;15:2249-2258.
38. Goto R, Doi M, Ma N, Semba R, Uji Y. Contribution of nitric oxide-producing cells in normal and diabetic rat retina. Jpn J Ophthalmol. 2005;49:363-370.
39. Li Q, Verma A, Han PY, et al. Diabetic eNOS-knockout mice develop accelerated retinopathy. Invest Ophthalmol Vis Sci. 2010;51:5240-5246.
40. Abu El-Asrar AM, Meersschaert A, Dralands L, Missotten L, Geboes K. Inducible nitric oxide synthase and vascular endothelial growth factor are colocalized in the retinas of human subjects with diabetes. Eye (Lond). 2004;18:306-313.
41. Kohzaki K, Vingrys AJ, Bui BV. Early inner retinal dysfunction in streptozotocin-induced diabetic rats. Invest Ophthalmol Vis Sci. 2008;49:3595-3604.
42. Wong VH, Vingrys AJ, Bui BV. Glial and neuronal dysfunction in streptozotocin-induced diabetic rats. J Ocul Biol Dis Infor. 2011;4:42-50.
43. Ly A, Yee P, Vessey KA, Phipps JA, Jobling AI, Fletcher EL. Early inner retinal astrocyte dysfunction during diabetes and development of hypoxia, retinal stress, and neuronal functional loss. Invest Ophthalmol Vis Sci. 2011;52:9316-9326.
44. Bui BV, Kalloniatis M, Vingrys AJ. The contribution of glycolytic and oxidative pathways to retinal photoreceptor function. Invest Ophthalmol Vis Sci. 2003;44:2708-2715.
45. Sinclair SH, Grunwald JE, Riva CE, Braunstein SN, Nichols CW, Schwartz SS. Retinal vascular autoregulation in diabetes mellitus. Ophthalmology. 1982;89:748-750.
46. Lecleire-Collet A, Audo I, Aout M, et al. Evaluation of retinal function and flicker light-induced retinal vascular response in normotensive patients with diabetes without retinopathy. Invest Ophthalmol Vis Sci. 2011;52:2861-2867.
47. Fletcher EL, Phipps JA, Wilkinson-Berka JL. Dysfunction of retinal neurons and glia during diabetes. Clin Exp Optom. 2005;88:132-145.
48. Hammes HP. Pericytes and the pathogenesis of diabetic retinopathy. Horm Metab Res. 2005;37:39-43.
49. Zheng L, Du Y, Miller C, et al. Critical role of inducible nitric oxide synthase in degeneration of retinal capillaries in mice with streptozotocin-induced diabetes. Diabetologia. 2007;50: 1987-1996.
50. Sobrevia L, Mann GE. Dysfunction of the endothelial nitric oxide signalling pathway in diabetes and hyperglycaemia. Exp Physiol. 1997;82:423-452.
51. Joussen AM, Poulaki V, Qin W, et al. Retinal vascular endothelial growth factor induces intercellular adhesion molecule-1 and endothelial nitric oxide synthase expression and initiates early diabetic retinal leukocyte adhesion in vivo. Am J Pathol. 2002;160:501-509.
52. Takeda M, Mori F, Yoshida A, et al. Constitutive nitric oxide synthase is associated with retinal vascular permeability in early diabetic rats. Diabetologia. 2001;44:1043-1050.
53. Williamson JR, Chang K, Frangos M, et al. Hyperglycemic pseudohypoxia and diabetic complications. Diabetes. 1993; 42:801-813.
54. Berkowitz BA, Luan H, Gupta RR, et al. Regulation of the early subnormal retinal oxygenation response in experimental diabetes by inducible nitric oxide synthase. Diabetes. 2004; 53:173-178.
55. Nakamura M, Kanamori A, Negi A. Diabetes mellitus as a risk factor for glaucomatous optic neuropathy. Ophthalmologica. 2005;219:1-10.
56. 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;102:783-791.
57. Bui BV, Loeliger M, Thomas M, et al. Investigating structural and biochemical correlates of ganglion cell dysfunction in streptozotocin-induced diabetic rats. Exp Eye Res. 2009;88: 1076-1083.
58. Sharma R, Buras E, Terashima T, et al. Hyperglycemia induces oxidative stress and impairs axonal transport rates in mice. PloS One. 2010;5:e13463.
59. Berkowitz BA, Gradianu M, Bissig D, Kern TS, Roberts R. Retinal ion regulation in a mouse model of diabetic retinopathy: natural history and the effect of Cu/Zn superoxide dismutase overexpression. Invest Ophthalmol Vis Sci. 2009;50:2351-2358.
60. Kaur C, Sivakumar V, Foulds WS. Early response of neurons and glial cells to hypoxia in the retina. Invest Ophthalmol Vis Sci. 2006;47:1126-1141.
61. Kim WT, Suh ES. Retinal protective effects of resveratrol via modulation of nitric oxide synthase on oxygen-induced retinopathy. Korean J Ophthalmol. 2010;24:108-118.
62. Ward MM, Jobling AI, Kalloniatis M, Fletcher EL. Glutamate uptake in retinal glial cells during diabetes. Diabetologia. 2005;48:351-360.