Retinal gene expression and visually evoked behavior in diabetic Long Evans rats

Investigative Ophthalmology and Visual Science

Volumn 52, Issue 10, 2011, Pages 7654-7663

  Kirwin, Stefanie J ^a,b   Kanaly, Suzanne T ^a   Hansen, Candice R ^a   Cairns, Belinda J ^a,c   Ren, Meina ^a   Edelman, Jeffrey L ^a  

^a ALLERGAN INC   (United States)

^b EyeQConsulting Corp   (United States)

^c Takeda San Francisco Inc   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ALPHA LACTALBUM; CYTOCHROME P450; EYE PROTEIN; GLIAL FIBRILLARY ACIDIC PROTEIN; GLUTATHIONE TRANSFERASE ALPHA; HEAT SHOCK PROTEIN 22; INHIBITOR OF DIFFERENTIATION 3; INTEGRASE; INTEGRATOR COMPLEX SUBUNIT 10; LECITHIN RETINOL ACYLTRANSFERASE; MEMBRANE PROTEIN; MEMBRANE PROTEIN 27; PROTEIN RPE65; RADICAL S ADENOSYL METHIONINE DOMAIN CONTAINING 2; SOMATOMEDIN BINDING PROTEIN 3; STRATUM CORNEUM CHYMOTRYPTIC ENZYME; TRANSDUCIN; UNCLASSIFIED DRUG; CARRIER PROTEIN; G PROTEIN COUPLED RECEPTOR; RPE65 PROTEIN, RAT;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BLOOD RETINA BARRIER; CELL DEATH; CELL GROWTH; CELL INTERACTION; CELL MOTION; CELL PROLIFERATION; CONTROLLED STUDY; EVOKED VISUAL RESPONSE; EYE TRACKING; GENE EXPRESSION; HISTOPATHOLOGY; HYPERGLYCEMIA; IMMUNOHISTOCHEMISTRY; MALE; MICROARRAY ANALYSIS; NONHUMAN; PRIORITY JOURNAL; PROTEIN LOCALIZATION; RAT; REAL TIME POLYMERASE CHAIN REACTION; RETINA; SIGNAL TRANSDUCTION; STREPTOZOCIN DIABETES; VISUAL THRESHOLD; ANIMAL; DIABETIC RETINOPATHY; DNA MICROARRAY; EXPERIMENTAL DIABETES MELLITUS; GENE EXPRESSION PROFILING; GENE EXPRESSION REGULATION; GENETICS; LONG EVANS RAT; METABOLISM; OPTOKINETIC NYSTAGMUS; PATHOPHYSIOLOGY; PHYSIOLOGY; PIGMENT EPITHELIUM;

ANIMALS; BLOOD-RETINAL BARRIER; CARRIER PROTEINS; DIABETES MELLITUS, EXPERIMENTAL; DIABETIC RETINOPATHY; EVOKED POTENTIALS, VISUAL; EYE PROTEINS; GENE EXPRESSION PROFILING; GENE EXPRESSION REGULATION; IMMUNOHISTOCHEMISTRY; MALE; NYSTAGMUS, OPTOKINETIC; OLIGONUCLEOTIDE ARRAY SEQUENCE ANALYSIS; RATS; RATS, LONG-EVANS; REAL-TIME POLYMERASE CHAIN REACTION; RECEPTORS, G-PROTEIN-COUPLED; RETINAL PIGMENT EPITHELIUM;

EID: 84856373585     PISSN: 01460404     EISSN: 15525783     Source Type: Journal    
DOI: 10.1167/iovs.10-6609     Document Type: Article

References (99)

1. Congdon NG, Friedman DS, Lietman T. Important causes of visual impairment in the world today. JAMA. 2003;290:2057-2060.
2. Hardy KJ, Lipton J, Scase MO, Foster DH, Scarpello JH. Detection of colour vision abnormalities in uncomplicated type 1 diabetic patients with angiographically normal retinas. Br J Ophthalmol. 1992;76:461-464.
3. Henson DB, North RV. Dark adaptation in diabetes mellitus. Br J Ophthalmol. 1979;63:539-541.
4. Shirao Y, Kawasaki K. Electrical responses from diabetic retina. Prog Ret Eye Res. 1998;17:59-76.
5. Holopigian K, Greenstein VC, Seiple W, Hood DC, Carr RE. Evidence for photoreceptor changes in patients with diabetic retinopathy. Invest Ophthalmol Vis Sci. 1997;38:2355-2365.
6. Bresnick GH, Palta M. Temporal aspects of the electroretinogram in diabetic retinopathy. Arch Ophthalmol. 1987;105:660-664.
7. 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.
8. Bresnick GH, Palta M. Oscillatory potential amplitudes: relation to severity of diabetic retinopathy. Arch Ophthalmol. 1987;105:929-933.
9. 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.
10. Hancock HA, Kraft TW. Oscillatory potential analysis and ERGs of normal and diabetic rats. Invest Ophthalmol Vis Sci. 2004;45: 1002-1008.
11. Kohzaki K, Vingrys AJ, Bui BV. Early inner retinal dysfunction in streptozotocin-induced diabetic rats. Invest Ophthalmol Vis Sci. 2008;49:3595-3604.
12. Shinoda K, Rejdak R, Schuettauf F, et al. Early electroretinographic features of streptozotocin-induced diabetic retinopathy. Clin Exp Ophthalmol. 2007;35:847-854.
13. Li Q, Zemel E, Miller B, Perlman I. Early retinal damage in experimental diabetes: electroretinographical and morphological observations. Exp Eye Res. 2002;74:615-625.
14. Puro DG. Diabetes-induced dysfunction of retinal Muller cells. Trans Am Ophthalmol Soc. 2002;100:339-352.
15. Lieth E, Barber AJ, Xu B, et al. Glial reactivity and impaired glutamate metabolism in short-term experimental diabetic retinopathy. Diabetes. 1998;47:815-820.
16. Lieth E, LaNoue KF, Antonetti DA, Ratz MJ, The Penn State Retina Research Group. Diabetes reduces glutamate oxidation and glutamine synthesis in the retina. Exp Eye Res. 2000;70:723-730.
17. Rungger-Brandle E, Dosso AA, Leuenberger PM. Glial reactivity, an early feature of diabetic retinopathy. Invest Ophthalmol Vis Sci. 2000;41:1971-1980.
18. Agardh E, Bruun A, Agardh C-D. Retinal glial cell immunoreactivity and neuronal cell changes in rats with STZ-induced diabetes. Curr Eye Res. 2001;23:276-284.
19. Barber AJ, Antonetti DA, Gardner TW. Altered expression of retinal occludin and glial fibrillary acidic protein in experimental diabetes. Invest Ophthalmol Vis Sci. 2000;41:3561-3568.
20. Maier R, Weger M, Haller-Schober EM, et al. Multiplex bead analysis of vitreous and serum concentrations of inflammatory and proangiogenic factors in diabetic patients. Mol Vis. 2008;14:637-643.
21. Hernández C, Segura RM, Fonollosa A, Carrasco E, Francisco G, Simó R. Interleukin-8, monocyte chemoattractant protein-1 and IL-10 in the vitreous fluid of patients with proliferative diabetic retinopathy. Diabet Med. 2005;22:719-722.
22. Murugeswari P, Shukla D, Rajendran A, Kim R, Namperumalsamy P, Muthukkaruppan V. Proinflammatory cytokines and angiogenic and anti-angiogenic factors in vitreous of patients with proliferative diabetic retinopathy and Eales' disease. Retina. 2008;28:817-824.
23. Abu El-Asrar AM, Struyf S, Kangave D, Geboes K, Van Damme J. Chemokines in proliferative diabetic retinopathy and proliferative vitreoretinopathy. Eur Cytokine Netw. 2006;17:155-165.
24. Tashimo A, Mitamura Y, Nagai S, et al. Aqueous levels of macrophage migration inhibitory factor and monocyte chemotactic protein-1 in patients with diabetic retinopathy. Diabet Med. 2004;21: 1292-1297.
25. Gerhardinger C, Costa MB, Coulombe MC, Toth I, Hoehn T, Grosu P. Expression of acute-phase response proteins in retinal Muller cells in diabetes. Invest Ophthalmol Vis Sci. 2005;46:349-357.
26. 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. 2008;1.
27. Kirwin SJ, Kanaly ST, Linke NA, Edelman JL. Strain-dependent increases in retinal inflammatory proteins and photoreceptor FGF-2 expression in streptozotocin-induced diabetic rats. Invest Ophthalmol Vis Sci. 2009;50:5396-5404.
28. Oshitari T, Roy S. Diabetes: a potential enhancer of retinal injury in rat retinas. Neurosci Lett. 2005;390:25-30.
29. Gastinger MJ, Singh RS, Barber AJ. Loss of cholinergic and dopaminergic amacrine cells in streptozotocin-diabetic rat and Ins2Akita-diabetic mouse retinas. Invest Ophthalmol Vis Sci. 2006;47:3143-3150.
30. Martin PM, Roon P, Van Ells TK, Ganapathy V, Smith SB. Death of retinal neurons in streptozotocin-induced diabetic mice. Invest Ophthalmol Vis Sci. 2004;45:3330-3336.
31. Park S-H, Park J-W, Park S-J, et al. Apoptotic death of photoreceptors in the streptozotocin-induced diabetic rat retina. Diabetologia. 2003;V46:1260-1268.
32. Asnaghi V, Gerhardinger C, Hoehn T, Adeboje A, Lorenzi M. A role for the polyol pathway in the early neuroretinal apoptosis and glial changes induced by diabetes in the rat. Diabetes 2003;506-511.
33. 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.
34. Phipps JA, Yee P, Fletcher EL, Vingrys AJ. Rod photoreceptor dysfunction in diabetes: activation, deactivation, and dark adaptation. Invest Ophthalmol Vis Sci. 2006;47:3187-3194.
35. Ostroy SE, Frede SM, Wagner EF, Gaitatzes CG, Janle EM. Decreased rhodopsin regeneration in diabetic mouse eyes. Invest Ophthalmol Vis Sci. 1994;35:3905-3909.
36. Tuitoek PJ, Ziari S, Tsin AT, Rajotte RV, Suh M, Basu TK. Streptozotocin-induced diabetes in rats is associated with impaired metabolic availability of vitamin A (retinol). Br J Nutr. 1996;75:615-622.
37. Thompson DA, Gal A. Vitamin A metabolism in the retinal pigment epithelium: genes, mutations, and diseases. Prog Ret Eye Res. 2003;22:683-703.
38. Strauss O. The retinal pigment epithelium in visual function. Physiol Rev. 2005;85:845-881.
39. Barry RJ, Canada FJ, Rando RR. Solubilization and partial purification of retinyl ester synthetase and retinoid isomerase from bovine ocular pigment epithelium. J Biol Chem. 1989;264:9231-9238.
40. Jahng WJ, David C, Nesnas N, Nakanishi K, Rando RR. A cleavable affinity biotinylating agent reveals a retinoid binding role for RPE65. Biochemistry. 2003;42:6159-6168.
41. Simon A, Hellman U, Wernstedt C, Eriksson U. The retinal pigment epithelial-specific 11-cis retinol dehydrogenase belongs to the family of short chain alcohol dehydrogenases. J Biol Chem. 1995;270: 1107-1112.
42. Hao W, Fong HKW. The endogenous chromophore of retinal G protein-coupled receptor opsin from the pigment epithelium. J Biol Chem. 1999;274:6085-6090.
43. Muniz A, Villazana-Espinoza ET, Hatch AL, Trevino SG, Allen DM, Tsin ATC. A novel cone visual cycle in the cone-dominated retina. Exp Eye Res. 2007;85:175-184.
44. Wang J-S, Kefalov VJ. The cone-specific visual cycle. Prog Ret Eye Res. 2011;30:115-128.
45. Joussen AM, Huang S, Poulaki V, et al. In vivo retinal gene expression in early diabetes. Invest Ophthalmol Vis Sci. 2001;42:3047-3057.
46. Ramsey DJ, Ripps H, Qian H. An electrophysiological study of retinal function in the diabetic female rat. Invest Ophthalmol Vis Sci. 2006;47:5116-5124.
47. Ramsey DJ, Ripps H, Qian H. Streptozotocin-induced diabetes modulates GABA receptor activity of rat retinal neurons. Exp Eye Res. 2007;85:413-422.
48. Oku H, Kodama T, Sakagami K, Puro DG. Diabetes-induced disruption of gap junction pathways within the retinal microvasculature. Invest Ophthalmol Vis Sci. 2001;42:1915-1920.
49. Gustavsson C, Agardh CD, Hagert P, Agardh E. Inflammatory markers in nondiabetic and diabetic rat retinas exposed to ischemia followed by reperfusion. Retina. 2008;28:645-652.
50. Agardh C-D, Agardh E, Qian Y, Hultberg B. Glutathione levels are reduced in diabetic rat retina but are not influenced by ischemia followed by recirculation. Metabolism. 1998;47:269-272.
51. Kirwin SJ, Dowdell KC, Hindinger C, et al. Altered neuroantigenspecific cytokine secretion in a Th2 environment reduces experimental autoimmune encephalomyelitis. J Neuroimmunol. 2006;178:30-39.
52. Douglas RM, Alam NM, Silver BD, McGill TJ, Tschetter WW, Prusky GT. Independent visual threshold measurements in the two eyes of freely moving rats and mice using a virtual-reality optokinetic system. Vis Neurosci. 2005;22:677-684.
53. Altimus CM, Guler AD, Alam NM, et al. Rod photoreceptors drive circadian photoentrainment across a wide range of light intensities. Nat Neurosci. 2010;13:1107-1112.
54. Casson RJ, Chidlow G, Wood JPM, Vidal-Sanz M, Osborne NN. The effect of retinal ganglion cell injury on light-induced photoreceptor degeneration. Invest Ophthalmol Vis Sci. 2004;45:685-693.
55. Nir I, Agarwal N, Papermaster DS. Opsin gene expression during early and late phases of retinal degeneration in rds mice. Exp Eye Res. 1990;51:257-267.
56. Gardner TW, Antonetti DA, Barber AJ, LaNoue KF, Levison SW. Diabetic retinopathy: more than meets the eye. Surv Ophthalmol. 2002;47:S253-S262.
57. Mizutani M, Gerhardinger C, Lorenzi M. Muller cell changes in human diabetic retinopathy. Diabetes. 1998;47:445-449.
58. Qiu A, Jansen M, Sakaris A, et al. Identification of an intestinal folate transporter and the molecular basis for hereditary folate malabsorption. Cell. 2006;127:917-928.
59. Sofer Y, Harel L, Sharkia M, Amir J, Schoenfeld T, Straussberg R. Neurological manifestations of folate transport defect: case report and review of the literature. J Child Neurol. 2007;22:783-786.
60. Umapathy NS, Gnana-Prakasam JP, Martin PM, et al. Cloning and functional characterization of the proton-coupled electrogenic folate transporter and analysis of its expression in retinal cell types. Invest Ophthalmol Vis Sci. 2007;48:5299-5305.
61. Wice BM, Bernal-Mizrachi E, Permutt MA. Glucose and other insulin secretagogues induce, rather than inhibit, expression of Id-1 and Id-3 in pancreatic islet beta cells. Diabetologia. 2001;44:453-463.
62. Rivieccio MA, Suh H-S, Zhao Y, et al. TLR3 ligation activates an antiviral response in human fetal astrocytes: a role for Viperin/ cig5. J Immunol. 2006;177:4735-4741.
63. Olofsson PS, Jatta K, Wagsater D, et al. The antiviral cytomegalovirus inducible gene 5/Viperin is expressed in atherosclerosis and regulated by proinflammatory agents. Arterioscler Thromb Vasc Biol. 2005;25:e113-e116.
64. Baillat D, Hakimi M-A, Näär AM, Shilatifard A, Cooch N, Shiekhattar R. Integrator, a multiprotein mediator of small nuclear RNA processing, associates with the C-terminal repeat of RNA polymerase II. Cell. 2005;123:265-276.
65. Quraishe S, Asuni A, Boelens WC, O'Connor V, Wyttenbach A. Expression of the small heat shock protein family in the mouse CNS: differential anatomical and biochemical compartmentalization. Neuroscience. 2008;153:483-491.
66. Chowdary TK, Raman B, Ramakrishna T, Rao CM. Mammalian Hsp22 is a heat-inducible small heat-shock protein with chaperone-like activity. Biochem J. 2004;381:379-387.
67. Carra S, Brunsting JF, Lambert H, Landry J, Kampinga HH. HspB8 participates in protein quality control by a non-chaperone-like mechanism that requires eIF2+ phosphorylation. J Biol Chem. 2009;284:5523-5532.
68. Stefani M, Dobson CM. Protein aggregation and aggregate toxicity: new insights into protein folding, misfolding diseases and biological evolution. J Mol Med. 2003;81:678-699.
69. Yang Y, Sharma R, Zimniak P, Awasthi YC. Role of α class glutathione S-transferases as antioxidant enzymes in rodent tissues. Toxicol Appl Pharmacol. 2002;182:105-115.
70. Du Y, Miller CM, Kern TS. Hyperglycemia increases mitochondrial superoxide in retina and retinal cells. Free Radic Biol Med. 2003;35:1491-1499.
71. Obrosova IG, Fathallah L, Greene DA. Early changes in lipid peroxidation and antioxidative defense in diabetic rat retina: effect of α-lipoic acid. Eur J Pharmacol. 2000;398:139-146.
72. Malakauskas SM, Quan H, Fields TA, et al. Aminoaciduria and altered renal expression of luminal amino acid transporters in mice lacking novel gene collectrin. Am J Physiol Renal Physiol. 2007;292:F533-F544.
73. Yang C-T, Hindes AE, Hultman KA, Johnson SL. Mutations in gfpt1 and skiv2l2 cause distinct stage-specific defects in larval melanocyte regeneration in Zebrafish. PLoS Genet. 2007;3:e88.
74. Matsubara T, Kim HJ, Miyata M, Shimada M, Nagata K, Yamazoe Y. Isolation and characterization of a new major intestinal CYP3A form, CYP3A62, in the rat. Pharmacol Exp Ther. 2004;309:1282-1290.
75. Maag RS, Mancini M, Rosen A, Machamer CE. Caspase-resistant Golgin-160 disrupts apoptosis induced by secretory pathway stress and ligation of death receptors. Mol Biol Cell. 2005;16:3019-3027.
76. Permyakov EA, Berliner LJ. A-lactalbumin: structure and function. FEBS Lett. 2000;473:269-274.
77. Spoerri PE, Caballero S, Wilson SH, Shaw LC, Grant MB. Expression of IGFBP-3 by human retinal endothelial cell cultures: IGFBP-3 involvement in growth inhibition and apoptosis. Invest Ophthalmol Vis Sci. 2003;44:365-369.
78. van Eenennaam H, Pruijn GJ, van Venrooij WJ. hPop4: a new protein subunit of the human RNase MRP and RNase P ribonucleoprotein complexes. Nucleic Acids Res. 1999;27:2465-2472.
79. Kowluru RA, Abbas SN. Diabetes-induced mitochondrial dysfunction in the retina. Invest Ophthalmol Vis Sci. 2003;44:5327-5334.
80. Ramani VC, Haun RS. The extracellular matrix protein fibronectin is a substrate for kallikrein 7. Biochem Biophys Res Commun. 2008;369:1169-1173.
81. Roy S, Cagliero E, Lorenzi M. Fibronectin overexpression in retinal microvessels of patients with diabetes. Invest Ophthalmol Vis Sci. 1996;37:258-266.
82. Das SR, Bhardwaj N, Kjeldbye H, Gouras P. Muller cells of chicken retina synthesize 11-cis-retinol. Biochem J. 1992;285:907-913.
83. Goldstein EB. Cone pigment regeneration in the isolated frog retina. Vision Res. 1970;10:1065-1068.
84. Muniz A, Betts BS, Trevino AR, et al. Evidence for two retinoid cycles in the cone-dominated chicken eye. Biochemistry. 2009;48: 6854-6863.
85. Wang J-S, Kefalov VJ. An alternative pathway mediates the mouse and human cone visual cycle. Curr Biol. 2009;19:1665-1669.
86. Batten ML, Imanishi Y, Maeda T, et al. Lecithin-retinol acyltransferase is essential for accumulation of all-trans-retinyl esters in the eye and in the liver. J Biol Chem. 2004;279:10422-10432.
87. Bunt-Milam AH, Saari JC. Immunocytochemical localization of two retinoid-binding proteins in vertebrate retina. J Cell Biol. 1983;97: 703-712.
88. Bok D, Ong DE, Chytil F. Immunocytochemical localization of cellular retinol binding protein in the rat retina. Invest Ophthalmol Vis Sci. 1984;25:877-883.
89. Pandey S, Blanks JC, Spee C, Jiang M, Fong HKW. Cytoplasmic retinal localization of an evolutionary homolog of the visual pigments. Exp Eye Res. 1994;58:605-614.
90. Znoiko SL, Crouch RK, Moiseyev G, Ma J-X. Identification of the RPE65 protein in mammalian cone photoreceptors. Invest Ophthalmol Vis Sci. 2002;43:1604-1609.
91. Mata NL, Radu RA, Clemmons RS, Travis GH. Isomerization and oxidation of vitamin A in cone-dominant retinas: a novel pathway for visual-pigment regeneration in daylight. Neuron. 2002;36:69-80.
92. Naggar H, Ola MS, Moore P, et al. Downregulation of reducedfolate transporter by glucose in cultured RPE cells and in RPE of diabetic mice. Invest Ophthalmol Vis Sci. 2002;43:556-563.
93. Decanini A, Karunadharma P, Nordgaard C, Feng X, Olsen T, Ferrington D. Human retinal pigment epithelium proteome changes in early diabetes. Diabetologia. 2008;51:1051-1061.
94. McGill TJ, Prusky GT, Douglas RM, et al. Intraocular CNTF reduces vision in normal rats in a dose-dependent manner. Invest Ophthalmol Vis Sci. 2007;48:5756-5766.
95. Aizu Y, Oyanagi K, Hu J, Nakagawa H. Degeneration of retinal neuronal processes and pigment epithelium in the early stage of the streptozotocin-diabetic rats. Neuropathology. 2002;22:161-170.
96. Hardy KJ, Fisher C, Heath P, Foster DH, Scarpello JH. Comparison of colour discrimination and electroretinography in evaluation of visual pathway dysfunction in aretinopathic IDDM patients. Br J Ophthalmol. 1995;79:35-37.
97. Aizu Y, Katayama H, Takahama S, Hu J, Nakagawa H, Oyanagi K. Topical instillation of ciliary neurotrophic factor inhibits retinal degeneration in streptozotocin-induced diabetic rats. Neuroreport. 2003;14:2067-2071.
98. Cukiernik M, Hileeto D, Evans T, Mukherjee S, Downey D, Chakrabarti S. Vascular endothelial growth factor in diabetes induced early retinal abnormalities. Diabet Res Clin Pract. 2004;65: 197-208.
99. Zhang SX, Ma J-X, Sima J, et al. Genetic difference in susceptibility to the blood-retina barrier breakdown in diabetes and oxygeninduced retinopathy. Am J Pathol. 2005;166:313-321.