Aldose reductase inhibition prevents endotoxin-induced inflammatory responses in retinal microglia

Investigative Ophthalmology and Visual Science

Volumn 55, Issue 5, 2014, Pages 2853-2861

  Chang, Kun Che ^a,b   Ponder, Jessica ^b   LaBarbera, Daniel V ^b   Mark Petrash, J ^a,b  

^a UNIVERSITY OF COLORADO SCHOOL OF MEDICINE   (United States)

^b UNIVERSITY OF COLORADO   (United States)

Author keywords

Aldose reductase; Aldose reductase inhibitor; Inflammation; LPS; Migration; MMP 9; Retinal microglia; glucogallin

Indexed keywords

2 PHENYLINDOLE DERIVATIVE; 4', 6 DIAMIDINO 2 PHENYLINDOLE; ALDEHYDE REDUCTASE; ALDOSE REDUCTASE INHIBITOR; BETA ACTIN; BETA GLUCOGALLIN; EMBLICA OFFICINALIS EXTRACT; ENDOTOXIN; GELATIN; GELATINASE B; INTERLEUKIN 1BETA; LIPOCORTIN 5; LIPOPOLYSACCHARIDE; MATRIX METALLOPROTEINASE INHIBITOR; SMALL INTERFERING RNA; SORBINIL; TUMOR NECROSIS FACTOR ALPHA; UNCLASSIFIED DRUG;

ADULT; ANIMAL CELL; ANIMAL TISSUE; APOPTOSIS; ARTICLE; CELL COUNTING; CELL MIGRATION ASSAY; CONTROLLED STUDY; DIABETIC RETINOPATHY; DOWN REGULATION; ENZYME INHIBITION; ENZYME LINKED IMMUNOSORBENT ASSAY; FLUORESCENCE ACTIVATED CELL SORTING; GENE SILENCING; IMMUNOFLUORESCENCE TEST; INFLAMMATION; KNOCKOUT GENE; MACROPHAGE ACTIVATION; MICROGLIA; MOUSE; NONHUMAN; PIGMENT EPITHELIUM; PRIORITY JOURNAL; PROTEIN EXPRESSION; RETINA; RISK ASSESSMENT; WESTERN BLOTTING; ZYMOGRAPHY;

ALDOSE REDUCTASE; ALDOSE REDUCTASE INHIBITOR; INFLAMMATION; LPS; MIGRATION; MMP-9; RETINAL MICROGLIA; Β-GLUCOGALLIN;

ALDEHYDE REDUCTASE; ANALYSIS OF VARIANCE; ANIMALS; APOPTOSIS; BLOTTING, WESTERN; CELL MOVEMENT; CELLS, CULTURED; CYTOKINES; DISEASE MODELS, ANIMAL; ENDOTOXINS; ENZYME INHIBITORS; ENZYME-LINKED IMMUNOSORBENT ASSAY; IMIDAZOLIDINES; MACROPHAGES; MATRIX METALLOPROTEINASE 9; MICE; MICE, INBRED BALB C; MICROGLIA; RETINA; RETINAL DISEASES;

EID: 84899732600     PISSN: 01460404     EISSN: 15525783     Source Type: Journal    
DOI: 10.1167/iovs.13-13487     Document Type: Article

References (51)

1. Joussen AM, Poulaki V, Le ML, et al. A central role for inflammation in the pathogenesis of diabetic retinopathy. FASEB J. 2004;18:1450-1452.
2. Schram MT, Chaturvedi N, Schalkwijk CG, Fuller JH, Stehouwer CD. Markers of inflammation are cross-sectionally associated with microvascular complications and cardiovascular disease in type 1 diabetes-the EURODIAB Prospective Complications Study. Diabetologia. 2005;48:370-378.
3. Demircan N, Safran BG, Soylu M, Ozcan AA, Sizmaz S. Determination of vitreous interleukin-1 (IL-1) and tumour necrosis factor (TNF) levels in proliferative diabetic retinopathy. Eye. (Lond). 2006;20:1366-1369.
4. Krady JK, Basu A, Allen CM, et al. Minocycline reduces proinflammatory cytokine expression, microglial activation, and caspase-3 activation in a rodent model of diabetic retinopathy. Diabetes. 2005;54:1559-1565.
5. Tang J, Kern TS. Inflammation in diabetic retinopathy. Prog Retin Eye Res. 2011;30:343-358.
6. Saren P, Welgus HG, Kovanen PT. TNF-alpha and IL-1beta selectively induce expression of 92-kDa gelatinase by human macrophages. J Immunol. 1996;157:4159-4165.
7. Marie O, Thillaye-Goldenberg B, Naud MC, de Kozak Y. Inhibition of endotoxin-induced uveitis and potentiation of local TNF-alpha and interleukin-6 mRNA expression by interleukin-13. Invest Ophthalmol Vis Sci. 1999;40:2275-2282.
8. Hume DA, Perry VH, Gordon S. Immunohistochemical localization of a macrophage-specific antigen in developing mouse retina: phagocytosis of dying neurons and differentiation of microglial cells to form a regular array in the plexiform layers. J Cell Biol. 1983;97:253-257.
9. Antonetti DA, Klein R, Gardner TW. Diabetic retinopathy. N Engl J Med. 2012;366:1227-1239.
10. Zeng HY, Green WR, Tso MO. Microglial activation in human diabetic retinopathy. Arch Ophthalmol. 2008;126:227-232.
11. Ibrahim AS, El-Remessy AB, Matragoon S, et al. Retinal microglial activation and inflammation induced by amadoriglycated albumin in a rat model of diabetes. Diabetes. 2011; 60:1122-1133.
12. Kezic JM, Chen X, Rakoczy EP, McMenamin PG. The effects of age and Cx3cr1 deficiency on retinal microglia in the Ins2(Akita) diabetic mouse. Invest Ophthalmol Vis Sci. 2013; 54:854-863.
13. Rungger-Brandle E, Dosso AA, Leuenberger PM. Glial reactivity, an early feature of diabetic retinopathy. Invest Ophthalmol Vis Sci. 2000;41:1971-1980.
14. Zeng XX, Ng YK, Ling EA. Neuronal and microglial response in the retina of streptozotocin-induced diabetic rats. Vis Neurosci. 2000;17:463-471.
15. Wang AL, Yuan M, Neufeld AH. Age-related changes in neuronal susceptibility to damage: comparison of the retinal ganglion cells of young and old mice before and after optic nerve crush. Ann N Y Acad Sci. 2007;1097:64-66.
16. Gardner TW, Antonetti DA, Barber AJ, LaNoue KF, Levison SW. Diabetic retinopathy: more than meets the eye. Surv Ophthalmol. 2002;47(suppl 2):S253-S262.
17. Guo C, Zhang Z, Zhang P, et al. Novel transgenic mouse models develop retinal changes associated with early diabetic retinopathy similar to those observed in rats with diabetes mellitus. Exp Eye Res. 2014;119:77-87.
18. 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;52:864-871.
19. Ramana KV, Tammali R, Reddy AB, Bhatnagar A, Srivastava SK. Aldose reductase-regulated tumor necrosis factor-alpha production is essential for high glucose-induced vascular smooth muscle cell growth. Endocrinology. 2007;148:4371-4384.
20. Petrash JM. All in the family: aldose reductase and closely related aldo-keto reductases. Cell Mol Life Sci. 2004;61:737-749.
21. Bhattacharya S, Manna P, Gachhui R, Sil PC. D-saccharic acid 1, 4-lactone protects diabetic rat kidney by ameliorating hyperglycemia-mediated oxidative stress and renal inflammatory cytokines via NF-kappaB and PKC signaling. Toxicol Appl Pharmacol. 2013;267:16-29.
22. Yadav UC, Srivastava SK, Ramana KV. Aldose reductase inhibition prevents endotoxin-induced uveitis in rats. Invest Ophthalmol Vis Sci. 2007;48:4634-4642.
23. Cheung AK, Fung MK, Lo AC, et al. Aldose reductase deficiency prevents diabetes-induced blood-retinal barrier breakdown, apoptosis, and glial reactivation in the retina of db/db mice. Diabetes. 2005;54:3119-3125.
24. Tang J, Du Y, Petrash JM, Sheibani N, Kern TS. Deletion of aldose reductase from mice inhibits diabetes-induced retinal capillary degeneration and superoxide generation. PLoS One. 2013;8:e62081.
25. Ho EC, Lam KS, Chen YS, et al. Aldose reductase-deficient mice are protected from delayed motor nerve conduction velocity, increased c-Jun NH2-terminal kinase activation, depletion of reduced glutathione, increased superoxide accumulation, and DNA damage. Diabetes. 2006;55:1946-1953.
26. Chang KC, Laffin B, Ponder J, et al. Beta-glucogallin reduces the expression of lipopolysaccharide-induced inflammatory markers by inhibition of aldose reductase in murine macrophages and ocular tissues. Chem Biol Interact. 2013;202:283-287.
27. Ramana KV, Fadl AA, Tammali R, Reddy AB, Chopra AK, Srivastava SK. Aldose reductase mediates the lipopolysaccharide-induced release of inflammatory mediators in RAW264.7 murine macrophages. J Biol Chem. 2006;281:33019-33029.
28. Ramana KV, Srivastava SK. Mediation of aldose reductase in lipopolysaccharide-induced inflammatory signals in mouse peritoneal macrophages. Cytokine. 2006;36:115-122.
29. Ramana KV, Reddy AB, Tammali R, Srivastava SK. Aldose reductase mediates endotoxin-induced production of nitric oxide and cytotoxicity in murine macrophages. Free Radic Biol Med. 2007;42:1290-1302.
30. Puppala M, Ponder J, Suryanarayana P, Reddy GB, Petrash JM, LaBarbera DV. The isolation and characterization of betaglucogallin as a novel aldose reductase inhibitor from Emblica officinalis. PLoS One. 2012;7:e31399.
31. Ma W, Zhao L, Fontainhas AM, Fariss RN, Wong WT. Microglia in the mouse retina alter the structure and function of retinal pigmented epithelial cells: a potential cellular interaction relevant to AMD. PLoS One. 2009;4:e7945.
32. Huang SP, Palla S, Ruzycki P, et al. Aldo-keto reductases in the eye. J Ophthalmol. 2010;2010:521204.
33. Chang KC, Lo CW, Fan TC, et al. TNF-alpha mediates eosinophil cationic protein-induced apoptosis in BEAS-2B cells. BMC Cell Biol. 2010;11:6.
34. El-Remessy AB, Tang Y, Zhu G, et al. Neuroprotective effects of cannabidiol in endotoxin-induced uveitis: critical role of p38 MAPK activation. Mol Vis. 2008;14:2190-2203.
35. Tajima T, Murata T, Aritake K, et al. Lipopolysaccharide induces macrophage migration via prostaglandin D(2) and prostaglandin E(2). J Pharmacol Exp Ther. 2008;326:493-501.
36. Pladzyk A, Reddy AB, Yadav UC, Tammali R, Ramana KV, Srivastava SK. Inhibition of aldose reductase prevents lipopolysaccharide-induced inflammatory response in human lens epithelial cells. Invest Ophthalmol Vis Sci. 2006;47:5395-5403.
37. Reddy AB, Ramana KV, Srivastava S, Bhatnagar A, Srivastava SK. Aldose reductase regulates high glucose-induced ectodomain shedding of tumor necrosis factor (TNF)-alpha via protein kinase C-delta and TNF-alpha converting enzyme in vascular smooth muscle cells. Endocrinology. 2009;150:63-74.
38. Rogove AD, Tsirka SE. Neurotoxic responses by microglia elicited by excitotoxic injury in the mouse hippocampus. Curr Biol. 1998;8:19-25.
39. Medana IM, Chan-Ling T, Hunt NH. Redistribution and degeneration of retinal astrocytes in experimental murine cerebral malaria: relationship to disruption of the blood-retinal barrier. Glia. 1996;16:51-64.
40. Faghiri Z, Bazan NG. PI3K/Akt and mTOR/p70S6K pathways mediate neuroprotectin D1-induced retinal pigment epithelial cell survival during oxidative stress-induced apoptosis. Exp Eye Res. 2010;90:718-725.
41. Gupta N, Brown KE, Milam AH. Activated microglia in human retinitis pigmentosa, late-onset retinal degeneration, and agerelated macular degeneration. Exp Eye Res. 2003;76:463-471.
42. Roque RS, Rosales AA, Jingjing L, Agarwal N, Al-Ubaidi MR. Retina-derived microglial cells induce photoreceptor cell death in vitro. Brain Res. 1999;836:110-119.
43. Harada T, Harada C, Kohsaka S, et al. Microglia-Müller glia cell interactions control neurotrophic factor production during light-induced retinal degeneration. J Neurosci. 2002;22:9228-9236.
44. Bosco A, Inman DM, Steele MR, et al. Reduced retina microglial activation and improved optic nerve integrity with minocycline treatment in the DBA/2J mouse model of glaucoma. Invest Ophthalmol Vis Sci. 2008;49:1437-1446.
45. Bousquet E, Zhao M, Ly A, et al. The aldosterone-mineralocorticoid receptor pathway exerts anti-inflammatory effects in endotoxin-induced uveitis. PLoS One. 2012;7:e49036.
46. Xu YF, Fu LL, Jiang CH, Qin YW, Ni YQ, Fan JW. Naloxone inhibition of lipopolysaccharide-induced activation of retinal microglia is partly mediated via the p38 mitogen activated protein kinase signalling pathway. J Int Med Res. 2012;40: 1438-1448.
47. Baker D, Butler D, Scallon BJ, O'Neill JK, Turk JL, Feldmann M. Control of established experimental allergic encephalomyelitis by inhibition of tumor necrosis factor (TNF) activity within the central nervous system using monoclonal antibodies and TNF receptor-immunoglobulin fusion proteins. Eur J Immunol. 1994;24:2040-2048.
48. Nelimarkka LO, Nikkari ST, Ravanti LS, Kahari VM, Jarvelainen HT. Collagenase-1, stromelysin-1 and 92 kDa gelatinase are associated with tumor necrosis factor-alpha induced morphological change of human endothelial cells in vitro. Matrix Biol. 1998;17:293-304.
49. Gong Y, Hart E, Shchurin A, Hoover-Plow J. Inflammatory macrophage migration requires MMP-9 activation by plasminogen in mice. J Clin Invest. 2008;118:3012-3024.
50. Lorenzi M. The polyol pathway as a mechanism for diabetic retinopathy: attractive, elusive, and resilient. Exp Diabetes Res. 2007;2007:61038.
51. Li L, Chang KC, Zhou Y, et al. Design of an amide N-glycoside derivative of beta-glucogallin: a stable, potent, and specific inhibitor of aldose reductase. J Med Chem. 2014;57:71-77.