Green tea is neuroprotective in diabetic retinopathy

Investigative Ophthalmology and Visual Science

Volumn 54, Issue 2, 2013, Pages 1325-1336

  Silva, Kamila C ^a   Rosales, Mariana A B ^a   Hamassaki, Dania E ^b   Saito, Kelly C ^b   Faria, Aline M ^a   Ribeiro, Patrícia A O ^a   Lopes de Faria, José B ^a   Lopes de Faria, Jacqueline M ^a  

^a UNIVERSITY OF CAMPINAS   (Brazil)

^b UNIVERSITY OF SÃO PAULO   (Brazil)

Author keywords

[No Author keywords available]

Indexed keywords

CLAUDIN 1; CYCLIC GMP; GLIAL FIBRILLARY ACIDIC PROTEIN; GLUCOSE; GLUTAMATE AMMONIA LIGASE; GLUTAMATE RECEPTOR; GLUTAMATE TRANSPORTER; GLUTATHIONE; NITRIC OXIDE SYNTHASE; OCCLUDIN; REACTIVE OXYGEN METABOLITE;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; BLOOD RETINA BARRIER; COLORIMETRY; CONFOCAL LASER MICROSCOPY; CONTROLLED STUDY; DIABETIC RETINOPATHY; ELECTRORETINOGRAPHY; ENZYME LINKED IMMUNOSORBENT ASSAY; HUMAN; HUMAN CELL; IMMUNOFLUORESCENCE TEST; IMMUNOHISTOCHEMISTRY; MALE; MEMBRANE PERMEABILITY; MICROSCOPY; MUELLER CELL; NEUROPROTECTION; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; RAT; REAL TIME POLYMERASE CHAIN REACTION; TEA; WESTERN BLOTTING;

ANIMALS; ANTIOXIDANTS; DIABETES MELLITUS, EXPERIMENTAL; DIABETIC RETINOPATHY; ELECTRORETINOGRAPHY; MALE; OXIDATIVE STRESS; RATS; RATS, INBRED SHR; RATS, INBRED WKY; RETINA; TEA;

EID: 84874970238     PISSN: 01460404     EISSN: 15525783     Source Type: Journal    
DOI: 10.1167/iovs.12-10647     Document Type: Article

References (53)

1. Barber AJ. A new view of diabetic retinopathy: a neurodegenerative disease of the eye. Prog Neuropsychopharmacol Biol Psychiatry. 2003;27:283-290.
2. Tretiach M, Madigan MC, Wen L, Gillies MC. Effect of M̈uller cell co-culture on in vitro permeability of bovine retinal vascular endothelium in normoxic and hypoxic conditions. Neurosci Lett. 2005;378:160-165.
3. Bringmann A, Pannicke T, Grosche J, et al. M̈uller cells in the healthy and diseased retina. Prog Retin Eye Res. 2006;25:397-424.
4. Tout S, Chan-Ling T, Holl̈ander H, Stone J. The role of M̈uller cells in the formation of the blood-retinal barrier. Neuroscience. 1993;55:291-301.
5. Metea MR, Newman EA. Glial cells dilate and constrict blood vessels: a mechanism of neurovascular coupling. J Neurosci. 2006;26:2862-287.
6. Newman EA. Glial modulation of synaptic transmission in the retina. Glia. 2004;47:268-274.
7. Sucher NJ, Lipton SA, Dreyer EB. Molecular basis of glutamate toxicity in retinal ganglion cells. Vision Res. 1997;37:3483-3493.
8. Li Q, Puro DG. Diabetes-induced dysfunction of the glutamate transporter in retinal M̈uller cells. Invest Ophthalmol Vis Sci. 2002;43:3109-3116.
9. Lieth E, LaNoue KF, Antonetti DA, Ratz M. Diabetes reduces glutamate oxidation and glutamine synthesis in the retina. The Penn State Retina Research Group. Exp Eye Res. 2000;70:723-730.
10. Tanaka K, Watase K, Manabe T, et al. Epilepsy and exacerbation of brain injury in mice lacking the glutamate transporter GLT-1. Science. 1997;276:1699-1702.
11. Harada T, Harada C, Watanabe M, et al. Functions of the two glutamate transporters GLAST and GLT-1 in the retina. Proc Natl Acad Sci U S A. 1998;95:4663-4666.
12. Aoyama K, Suh SW, Hamby AM, et al. Neuronal glutathione deficiency and age-dependent neurodegeneration in the EAAC1 deficient mouse. Nat Neurosci. 2006;9:119-126.
13. Dringen R. Metabolism and functions of glutathione in brain. Prog Neurobiol. 2000;62:649-671.
14. Harada T, Harada C, Nakamura K, et al. The potential role of glutamate transporters in the pathogenesis of normal tension glaucoma. J Clin Invest. 2007;117:1763-1770.
15. Strauss O. The retinal pigment epithelium in visual function. Physiological Reviews. 2005;85:845-881.
16. Rothstein JD, Martin L, Levey AI, et al. Localization of neuronal and glial glutamate transporters. Neuron. 1994;13:713-725.
17. M̈aenp̈äa H, Gegelashvili G, T̈ahti H. Expression of glutamate transporter subtypes in cultured retinal pigment epithelial and retinoblastoma cells. Curr Eye Res. 2004;28:159-165.
18. Higdon JV, Frei B. Tea catechins and polyphenols: health effects, metabolism, and antioxidant functions. Crit Rev Food Sci Nutr. 2003;43:89-143.
19. Rice-Evans CA, Miller NJ, Bolwell PG, Bramley PM, Pridham JB. The relative antioxidant activities of plant-derived polyphenolic flavonoids. Free Radic Res. 1995;22:375-383.
20. Mustata GT, Rosca M, Biemel KM, et al. Paradoxical effects of green tea (Camellia sinensis) and antioxidant vitamins in diabetic rats: improved retinopathy and renal mitochondrial defects but deterioration of collagen matrix glycoxidation and cross-linking. Diabetes. 2005;54:517-526.
21. Kumar B, Gupta SK, Nag TC, Srivastava S, Saxena R. Green tea prevents hyperglycemia-induced retinal oxidative stress and inflammation in streptozotocin-induced diabetic rats. Ophthalmic Res. 2012;47:103-108.
22. Choi YB, Kim YI, Lee KS, Kim BS, Kim DJ. Protective effect of epigallocatechin gallate on brain damage after transient middle cerebral artery occlusion in rats. Brain Res. 2004;1019:47-54.
23. He Y, Cui J, Lee JC, et al. Prolonged exposure of cortical neurons to oligomeric amyloid-b impairs NMDA receptor function via NADPH oxidase-mediated ROS production: protective effect of green tea (-)-epigallocatechin-3-gallate. ASN Neuro. 2011;3:e00050.
24. Faria AM, Papadimitriou A, Silva KC, Lopes de Faria JM, Lopes de Faria JB. Uncoupling endothelial nitric oxide synthase is ameliorated by green tea in experimental diabetes mellitus by re-establishing BH4 levels. Diabetes. 2012;61:1838-1847.
25. Ribaldo PDB, Souza DS, Biswas SK, Block K, Lopes de Faria JM, Lopes de Faria JB. Green tea (Camellia sinensis) attenuates nephropathy by downregulating Nox4 NADPH oxidase in diabetic spontaneously hypertensive rats. J Nutr. 2009;139: 96-100.
26. Pinto CC, Silva KC, Biswas SK, Martins N, Lopes de Faria JB, Lopes de Faria JM. Arterial hypertension exacerbates oxidative stress in early diabetic retinopathy. Free Radic Res. 2007;41: 1151-1158.
27. Silva KC, Rosales MA, Biswas SK, Lopes de Faria JB, Lopes de Faria JM. Diabetic retinal neurodegeneration is associated with mitochondrial oxidative stress and is improved by an angiotensin receptor blocker in a model combining hypertension and diabetes. Diabetes. 2009;58:1382-1390.
28. Lopes de Faria JM, Silva KC, Boer PA, et al. A decrease in retinal progenitor cells is associated with early features of diabetic retinopathy in a model that combines diabetes and hypertension. Mol Vis. 2008;14:1680-1691.
29. Chaturvedi N, Porta M, Klein R, et al. Effect of candesartan on prevention (DIRECT-Prevent 1) and progression (DIRECTProtect 1) of retinopathy in type 1 diabetes: randomised, placebo-controlled trials. Lancet. 2008;372:1394-1402.
30. Sjølie AK, Klein R, Porta M, et al. Effect of candesartan on progression and regression of retinopathy in type 2 diabetes (DIRECT-Protect 2): a randomised placebo-controlled trial. Lancet. 2008;372:1385-1393.
31. Mosmann T. Rapid colorimetric assay for cellular growth and survival: application to proliferation and cytotoxicity assays. J Immunol Meth. 1983;65:55-63.
32. Hicks D, Courtois Y. The growth and behaviour of rat retinal M̈uller cells in vitro. An improved method for isolation and culture. Exp Eye Res. 1990;51:119-129.
33. Bradford MM. A rapid and sensitive method for the quantification of microgram quantities of protein utilizing the principle of protein dye binding. Anal Biochem. 1976;72: 248-254.
34. Leal EC, Manivannan A, Hosoya K, et al. Inducible nitric oxide synthase isoform is a key mediator of leukostasis and bloodretinal barrier breakdown in diabetic retinopathy. Invest Ophthalmol Vis Sci. 2007;48:5257-5265.
35. Bui BV, Armitage JA, Tolcos M, Cooper ME, Vingrys AJ. ACE inhibition salvages the visual loss caused by diabetes. Diabetologia. 2003;46:401-408.
36. Ribeiro PA, Sbragia L, Gilioli R, Langone F, Conte FF, Lopes-Cendes I. Expression profile of Lgi1 gene in mouse brain during development. J Mol Neurosci. 2008;35:323-329.
37. Zeng K, Xu H, Chen K, et al. Effects of taurine on glutamate uptake and degradation in M̈uller cells under diabetic conditions via antioxidant mechanism. Mol Cell Neurosci. 2010;45:192-199.
38. Rameau GA, Chiu LY, Ziff EB. Bidirectional regulation of neuronal nitric-oxide synthase phosphorylation at serine 847 by the N-methyl-D-aspartate receptor. J Biol Chem. 2004;279: 14307-14314.
39. Bucolo C, Ward KW, Mazzon E, Cuzzocrea S, Drago F. Protective effects of a coumarin derivative in diabetic rats. Invest Ophthalmol Vis Sci. 2009;50:3846-3852.
40. Thibeault S, Rautureau Y, Oubaha M, et al. S-nitrosylation of bcatenin by eNOS-derived NO promotes VEGF-induced endothelial cell permeability. Mol Cell. 2010;39:468-476.
41. Dimmeler S, Fleming I, Fisslthaler B, Hermann C, Busse R, Zeiher AM. Activation of nitric oxide synthase in endothelial cells by Akt-dependent phosphorylation. Nature. 1999;399: 601-605.
42. Blanes MG, Oubaha M, Rautureau Y, Gratton JP. Phosphorylation of tyrosine 801 of vascular endothelial growth factor receptor-2 is necessary for Akt-dependent endothelial nitricoxide synthase activation and nitric oxide release from endothelial cells. J Biol Chem. 2007;282:10660-10699.
43. Freireich EJ, Gehan EA, Rall DP, Schmidt LH, Skipper HE. Quantitative comparison of toxicity of anticancer agents in mouse, rat, dog, monkey and man. Cancer Chemother Rep. 1966;50:219-244.
44. Suzuma I, Hata Y, Clermont A, et al. Cyclic stretch and hypertension induce retinal expression of vascular endothelial growth factor and vascular endothelial growth factor receptor-2: potential mechanisms for exacerbation of diabetic retinopathy by hypertension. Diabetes. 2001;50:444-454.
45. Suzuma I, Suzuma K, Ueki K, et al. Stretch-induced retinal vascular endothelial growth factor expression is mediated by phosphatidylinositol 3-kinase and protein kinase C (PKC)-zeta but not by stretch-induced ERK1/2, Akt, Ras, or classical/novel PKC pathways. J Biol Chem. 2002;277:1047-1057.
46. Hollmann M, Heinemann S. Cloned glutamate receptors. Annu Rev Neurosci. 1994;17:31-108.
47. Waldman SA, Murad F. Cyclic GMP synthesis and function. Pharmacol Rev. 1987;39:163-196.
48. Ciani E, Virgili M, Contestabile A. Akt pathway mediates a cGMP-dependent survival role of nitric oxide in cerebellar granule neurones. J Neurochem. 2002;81:218-228.
49. Zhang B, Rusciano D, Osborne NN. Orally administered epigallocatechin gallate attenuates retinal neuronal death in vivo and light-induced apoptosis in vitro. Brain Res. 2008; 1198:141-152.
50. Siu AW, Lau MK, Cheng JS, et al. Glutamate-induced retinal lipid and protein damage: the protective effects of catechin. Neurosci Lett. 2008;432:193-197.
51. Villarroel M, Garci{dotless}á-Rami{dotless}́rez M, Corraliza L, Hernández C, Siḿo R. Effects of high glucose concentration on the barrier function and the expression of tight junction proteins in human retinal pigment epithelial cells. Exp Eye Res. 2009;89: 913-920.
52. Lee MJ, Maliakal P, Chen L, et al. Pharmacokinetics of tea catechins after ingestion of green tea and (-)-epigallocatechin-3-gallate by humans: formation of different metabolites and individual variability. Cancer Epidemiol Biomarkers Prev. 2002;11:1025-1032.
53. Renouf M, Guy P, Marmet C, et al. Plasma appearance and correlation between coffee and green tea metabolites in human subjects. Br J Nutr. 2010;104:1635-1640