Antioxidant Status of Human Retinal Pigment Epithelium: A review
Keywords:
Reactive Oxygen Species, Oxidative Stress, Retinal Pigment Epithelium, Superoxide Dismutase, Catalase, Glutathione Peroxidase, Glutathione ReductaseAbstract
Reactive oxygen species (ROS) show both beneficial as well as harmful effects, especially when the level of ROS increased beyond the level of antioxidants it proved harmful to any living system. Oxidative stress (OS) is the imbalance of the level of antioxidants and ROS. The antioxidants are compounds that showed their presence by fighting against ROS. ROS damages various macromolecules such as protein, lipids, carbohydrates, and DNA. An antioxidant such as SOD, CAT, GSH-Px, and GR show their role by mitigating the harmful effects of ROS on the cellular macromolecules. Especially in the retina, the OS plays a vital role in the occurrence of retinopathies. Retinopathy is any impairment in the retina which leads to loss of visual acuity. The declined level of antioxidants leads to oculopathies such as diabetic retinopathy (DR), age-related macular degeneration (AMD), and other macular degenerative diseases. The retina is more susceptible to OS because of the presence of polyunsaturated fatty acid and photooxidative injury. AMD is the leading cause in the world but its occurrence due to OS is poorly understood. Additionally, it is found that the alteration of antioxidants in retinal pigment epithelial cells was observed in in vitro and in vivo conditions. There is a need to understand the underlying mechanism, either OS is responsible for retinopathies or the disease itself leads to stressful conditions in tissue or cells. In the current review article, we put an attempt to summarize the recent link between OS and retinopathies such as DR and AMD.
Keywords
Reactive Oxygen Species, Oxidative Stress, Retinal Pigment Epithelium, Superoxide Dismutase, Catalase, Glutathione Peroxidase, Glutathione Reductase
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Agarwal A, Afridi R, Hassan M, Sadiq MA, Sepah YJ, Do DV, Nguyen QD (2015) Novel Therapies in Development for Diabetic Macular Edema. Curr. Diab. Rep. https://doi.org/10.1007/s11892-015-0652-z
Ames BN, Gold LS (1991) Endogenous mutagens and the causes of aging and cancer, Mutation Research.
Angulo Daniela F (2015). Intracellular Redox Status and Cell Death Induced by H2O2 in a Human Retinal Epithelial Cell Line (ARPE-19). Am. J. Biosci. 3, 93. https://doi.org/10.11648/j.ajbio.20150303.15
Antunes, F., Cadenas, E., 2000. Estimation of H2O2 gradients across biomembranes. FEBS Lett. 475, 121–126. https://doi.org/10.1016/S0014-5793(00)01638-0
Bayir, H., 2005. Reactive oxygen species. Crit. Care Med. 33. https://doi.org/10.1097/01.CCM.0000186787.64500.12
Beatty, S., Koh, H.-H., Phil, M., Henson, D., Boulton, M., 2000. The role of oxidative stress in the pathogenesis of age-related macular degeneration. Surv. Ophthalmol. 45, 115–134. https://doi.org/10.1016/S0039-6257(00)00140-5
Bedard, K., Krause, K.H., 2007. The NOX family of ROS-generating NADPH oxidases: Physiology and pathophysiology. Physiol. Rev. https://doi.org/10.1152/physrev.00044.2005
Behndig, A., 2008. Corneal endothelial integrity in aging mice lacking superoxide dismutase-1 and/or superoxide dismutase-3. Mol. Vis. 14, 2025–2030.
Bird, A.C., Bressler, N.M., Bressler, S.B., Chisholm, I.H., Coscas, G., Davis, M.D., de Jong, P.T.V.M., Klaver, C.C.W., Klein, B.E.K., Klein, R., Mitchell, P., Sarks, J.P., Sarks, S.H., Soubrane, G., Taylor, H.R., Vingerling, J.R., 1995. An international classification and grading system for age-related maculopathy and age-related macular degeneration. Surv. Ophthalmol. 39, 367–374. https://doi.org/10.1016/S0039-6257(05)80092-X
Bok, D., 1993. The retinal pigment epithelium: a versatile partner in vision. J. Cell Sci. 1993, 189–195. https://doi.org/10.1097/HJH.0b013e3283546532
Cano, M., Thimmalappula, R., Fujihara, M., Nagai, N., Sporn, M., Wang, A.L., Neufeld, A.H., Biswal, S., Handa, J.T., 2010. Cigarette smoking, oxidative stress, the anti-oxidant response through Nrf2 signaling, and Age-related Macular Degeneration. Vision Res. 50, 652–664. https://doi.org/10.1016/j.visres.2009.08.018
Cano, M., Wang, L., Wan, J., Barnett, B.P., Ebrahimi, K., Qian, J., Handa, J.T., 2014. Oxidative Stress Induces Mitochondrial Dysfunction and a Protective Unfolded Protein Response in RPE cells. Free Radic. Biol. Med. 69, 1–14. https://doi.org/10.1038/jid.2014.371
Chance, B., Sies, H., Boveris, A., 1979. Hydroperoxide metabolism in mammalian organs. Physiol. Rev. 59, 527–605. https://doi.org/10.1152/physrev.1979.59.3.527
Chu, F.F., Esworthy, R.S., Doroshow, J.H., Doan, K., Liu, X.F., 1992. Expression of plasma glutathione peroxidase in human liver in addition to kidney, heart, lung, and breast in humans and rodents. Blood 79, 3233–3238. https://doi.org/10.1182/blood.v79.12.3233.bloodjournal79123233
Cohen, S.M., Olin, K.L., Feuer, W.J., Hjelmeland, L., Keen, C.L., Morse, L.S., 1994. Low glutathione reductase and peroxidase activity in age-related macular degeneration. Br. J. Ophthalmol. 78, 791–794. https://doi.org/10.1136/bjo.78.10.791
Costa, A., Scholer-Dahirel, A., Mechta-Grigoriou, F., 2014. The role of reactive oxygen species and metabolism on cancer cells and their microenvironment. Semin. Cancer Biol. https://doi.org/10.1016/j.semcancer.2013.12.007
Cui, Y., Xu, X., Bi, H., Zhu, Q., Wu, J., Xia, X., Qiushi Ren, Ho, P.C.P., 2006. Expression modification of uncoupling proteins and MnSOD in retinal endothelial cells and pericytes induced by high glucose: The role of reactive oxygen species in diabetic retinopathy. Exp. Eye Res. 83, 807–816. https://doi.org/10.1016/j.exer.2006.03.024
De Haan, J.B., Bladier, C., Griffiths, P., Kelner, M., O’Shea, R.D., Cheung, N.S., Bronson, R.T., Silvestro, M.J., Wild, S., Zheng, S.S., Beart, P.M., Hertzog, P.J., Kola, I., 1998. Mice with a homozygous null mutation for the most abundant glutathione peroxidase, Gpx1, show increased susceptibility to the oxidative stress- inducing agents paraquat and hydrogen peroxide. J. Biol. Chem. 273, 22528–22536. https://doi.org/10.1074/jbc.273.35.22528
De La Paz, M.A., Zhang, J., Fridovich, I., 1996. Antioxidant enzymes of the human retina: Effect of age on enzyme activity of macula and periphery. Curr. Eye Res. 15, 273–278. https://doi.org/10.3109/02713689609007621
Del Priore, L. V., Kuo, Y.H., Tezel, T.H., 2002. Age-related changes in human RPE cell density and apoptosis proportion in situ. Investig. Ophthalmol. Vis. Sci. 43, 3312–3318.
Delcourt, C., Cristol, J.P., Léger, C.L., Descomps, B., Papoz, L., 1999. Associations of antioxidant enzymes with cataract and age-related macular degeneration: The POLA study. Ophthalmology 106, 215–222. https://doi.org/10.1016/S0161-6420(99)90059-3
Duh, E.J., Sun, J.K., Stitt, A.W., 2017. Diabetic retinopathy: current understanding, mechanisms, and treatment strategies. JCI insight 2, 1–13. https://doi.org/10.1172/jci.insight.93751
Fletcher, E., Phipps, J., Ward, M., Puthussery, T., Wilkinson-Berka, J., 2007. Neuronal and Glial Cell Abnormality as Predictors of Progression of Diabetic Retinopathy. Curr. Pharm. Des. 13, 2699–2712. https://doi.org/10.2174/138161207781662920
Fliesler, A.J., Anderson, R.E., 1983. Chemistry and metabolism of lipids in the vertebrate retina. Prog. Lipid Res. https://doi.org/10.1016/0163-7827(83)90004-8
Foyer, C.H., Noctor, G., 2005. Redox homeostasis and antioxidant signaling: A metabolic interface between stress perception and physiological responses. Plant Cell. https://doi.org/10.1105/tpc.105.033589
Frank, R.N., Amin, R.H., Puklin, J.E., 1999. Antioxidant enzymes in the macular retinal pigment epithelium of eyes with neovascular age-related macular degeneration. Am. J. Ophthalmol. 127, 694–709. https://doi.org/10.1016/S0002-9394(99)00032-X
Gille, J.J.P., Joenje, H., 1992. Cell culture models for oxidative stress: superoxide and hydrogen peroxide versus normobaric hyperoxia. Mutat. Res. DNAging 275, 405–414. https://doi.org/10.1016/0921-8734(92)90043-O
Glotin, A.L., Calipel, A., Brossas, J.Y., Faussat, A.M., Tréton, J., Mascarelli, F., 2006. Sustained versus transient ERK1/2 signaling underlies the anti- and proapoptotic effects of oxidative stress in human RPE cells. Investig. Ophthalmol. Vis. Sci. 47, 4614–4623. https://doi.org/10.1167/iovs.06-0297
Goldberg, J., Flowerdew, G., Smith, E., Brody, J.A., Tso, M.O.M., 1988. Factors associated with age-related macular degeneration: An ANALYSIS of DATA from THE fi1r8t NATIONAL health AND nutrition EXAMINATION survey. Am. J. Epidemiol. 128, 700–710. https://doi.org/10.1093/oxfordjournals.aje.a115023
Gracy, R.W., Talent, J.M., Kong, Y., Conrad, C.C., 1999. Reactive oxygen species: The unavoidable environmental insult?, in: Mutation Research - Fundamental and Molecular Mechanisms of Mutagenesis. pp. 17–22. https://doi.org/10.1016/S1383-5742(99)00027-7
Grassi, M.A., Tikhomirov, A., Ramalingam, S., Lee, K.E., Mohsen Hosseini, S., Klein, B.E.K., Klein, R., Lussier, Y.A., Cox, N.J., Nicolae, D.L., 2012. Replication analysis for severe diabetic retinopathy. Investig. Ophthalmol. Vis. Sci. 53, 2377–2381. https://doi.org/10.1167/iovs.11-8068
Gülden, M., Jess, A., Kammann, J., Maser, E., Seibert, H., 2010. Cytotoxic potency of H2O2 in cell cultures: Impact of cell concentration and exposure time. Free Radic. Biol. Med. 49, 1298–1305. https://doi.org/10.1016/j.freeradbiomed.2010.07.015
Guruvayoorappan, C., 2008. Antioxidant Potential Of Byesukar, A Polyherbal Formulation On Alloxan Induced Oxidative Stress In Rats. Malaysian J. Biochem. Mol. Biol. Volume 12.
Halliwell, B., 1991. Reactive oxygen species in living systems: Source, biochemistry, and role in human disease. Am. J. Med. 91. https://doi.org/10.1016/0002-9343(91)90279-7
Hamilton, C.A., Miller, W.H., Al-Benna, S., Brosnan, M.J., Drummond, R.D., McBride, M.W., Dominiczak, A.F., 2004. Strategies to reduce oxidative stress in cardiovascular disease. Clin. Sci. https://doi.org/10.1042/CS20030379
Hancock, J.T., Desikan, R., Neill, S.J., 2001. Role of reactive oxygen species in cell signalling pathways. Biochem. Soc. Trans. 29, 345–349. https://doi.org/10.1042/bst0290345
Haque, R., Chun, E., Howell, J.C., Sengupta, T., Chen, D., Kim, H., 2012. MicroRNA-30b-mediated regulation of catalase expression in human ARPE-19 cells. PLoS One 7. https://doi.org/10.1371/journal.pone.0042542
Hatem, E., Berthonaud, V., Dardalhon, M., Lagniel, G., Baudouin-Cornu, P., Huang, M.E., Labarre, J., Chédin, S., 2014. Glutathione is essential to preserve nuclear function and cell survival under oxidative stress. Free Radic. Biol. Med. 67, 103–114. https://doi.org/10.1016/j.freeradbiomed.2013.10.807
Held, P., 2012. An Introduction to Reactive Oxygen Species Measurement of ROS in Cells. BioTek Instr 1–14. https://doi.org/10.1017/CBO9781107415324.004
Helmut Sies, Berndt, C., Jones, D.P., 2017. Oxidative Stress. Annu. Rev. Biochem. 86. https://doi.org/10.1146/annurev-biochem-061516-045037
Herrmann, R.K., Robison, W.G., Bieri, J.G., 1984. Deficiencies of vitamins E and A in the rat: Lipofuscin accumulation in the choroid. Investig. Ophthalmol. Vis. Sci. 25, 429–433.
Honda, S., Hjelmeland, L.M., Handa, J.T., 2002. Senescence associated β galactosidase activity in human retinal pigment epithelial cells exposed to mildhyperoxia in vitro. Br. J. Ophthalmol. 86, 159–162. https://doi.org/10.1136/bjo.86.2.159
Huang, C.K., Lin, Y., Su, H., Ye, D., 2014. Forsythiaside Protects Against Hydrogen Peroxide-Induced Oxidative Stress and Apoptosis in PC12 Cell. Neurochem. Res. 40, 27–35. https://doi.org/10.1007/s11064-014-1461-5
Inumaru, J., Nagano, O., Takahashi, E., Ishimoto, T., Nakamura, S., Suzuki, Y., Niwa, S.I., Umezawa, K., Tanihara, H., Saya, H., 2009. Molecular mechanisms regulating dissociation of cell-cell junction of epithelial cells by oxidative stress. Genes to Cells 14, 703–716. https://doi.org/10.1111/j.1365-2443.2009.01303.x
Jager, R.D., Mieler, W.F., Miller, J.W., 2008. Age-related macular degeneration. N. Engl. J. Med. https://doi.org/10.1056/NEJMra0801537
Jain, M., Rivera, S., Monclus, E.A., Synenki, L., Zirk, A., Eisenbart, J., Feghali-Bostwick, C., Mutlu, G.M., Budinger, G.R.S., Chandel, N.S., 2013. Mitochondrial reactive oxygen species regulate transforming growth factor-β signaling. J. Biol. Chem. 288, 770–777. https://doi.org/10.1074/jbc.M112.431973
Jia, L., Dong, Y., Yang, H., Pan, X., Fan, R., Zhai, L., 2011. Serum superoxide dismutase and malondialdehyde levels in a group of Chinese patients with age-related macular degeneration. Aging Clin. Exp. Res. 23, 264–267. https://doi.org/10.1007/BF03324965
Jia, L., Liu, Z., Sun, L., Miller, S.S., Ames, B.N., Cotman, C.W., Liu, J., 2007. Acrolein, a toxicant in cigarette smoke, causes oxidative damage and mitochondrial dysfunction in RPE cells: Protection by (R)-α-lipoic acid. Investig. Ophthalmol. Vis. Sci. 48, 339–348. https://doi.org/10.1167/iovs.06-0248
Kalluri, R., 2009. EMT: When epithelial cells decide to become mesenchymal-like cells. J. Clin. Invest. https://doi.org/10.1172/JCI39675
Kamoshita, M., Toda, E., Osada, H., Narimatsu, T., Kobayashi, S., Tsubota, K., Ozawa, Y., 2016. Lutein acts via multiple antioxidant pathways in the photo-stressed retina. Sci. Rep. 6, 1–10. https://doi.org/10.1038/srep30226
Kayanoki, Y., Fujii, J., Islam, K.N., Suzuki, K., Kawata, S., Matsuzawa, Y., Taniguchi, N., 1996. The protective role of glutathione peroxidase in apoptosis induced by reactive oxygen species. J. Biochem. 119, 817–822. https://doi.org/10.1093/oxfordjournals.jbchem.a021313
Kelner, M.J., Bagnell, R.D., Uglik, S.F., Montoya, M.A., Mullenbach, G.T., 1995. Heterologous expression of selenium-dependent glutathione peroxidase affords cellular resistance to paraquat. Arch. Biochem. Biophys. 323, 40–46. https://doi.org/10.1006/abbi.1995.0007
Keys, S.A., Zimmerman, W.F., 1999. Antioxidant activity of retinol, glutathione, and taurine in bovine photoreceptor cell membranes. Exp. Eye Res. 68, 693–702. https://doi.org/10.1006/exer.1999.0657
Khandhadia, S., Cree, A., Lotery, A., 2014. Oxidative damage and macular degeneration, in: Systems Biology of Free Radicals and Antioxidants. pp. 3625–3653. https://doi.org/10.1007/978-3-642-30018-9_171
Kim, M.H., Chung, J., Yang, J. wook, Chung, S.M., Kwag, N.H., Yoo, J.S., 2003. Hydrogen peroxide-induced cell death in a human retinal pigment epithelial cell line, ARPE-19. Korean J. Ophthalmol. 17, 19–28. https://doi.org/10.3341/kjo.2003.17.1.19
Kim, Y.W., Byzova, T. V, 2014. Oxidative stress in angiogenesis and vascular disease. Blood. https://doi.org/10.1182/blood-2013-09-512749
Kliment, C.R., Suliman, H.B., Tobolewski, J.M., Reynolds, C.M., Day, B.J., Zhu, X., McTiernan, C.F., McGaffin, K.R., Piantadosi, C.A., Oury, T.D., 2009. Extracellular superoxide dismutase regulates cardiac function and fibrosis. J. Mol. Cell. Cardiol. 47, 730–742. https://doi.org/10.1016/j.yjmcc.2009.08.010
Kovacic, P., Radical, R.S.-C.M. and F., 2008, U., 2008. Unifying Mechanism for Eye Toxicity: Electron Transfer, Reactive Oxygen Species, Antioxidant Benefits, Cell Signaling and Cell Membranes. Cell Membr. Free Radic. Res. 1, 56–69.
Kretzschmar, M., Müller, D., 1993. Aging, Training and Exercise: A Review of Effects on Plasma Glutathione and Lipid Peroxides. Sport. Med. Eval. Res. Exerc. Sci. Sport. Med. https://doi.org/10.2165/00007256-199315030-00005
Kumar, A., Pandey, R.K., Miller, L.J., Singh, P.K., Kanwar, M., 2013. Müller glia in retinal innate immunity: A perspective on their roles in endophthalmitis. Crit. Rev. Immunol. 33, 119–135. https://doi.org/10.1615/CritRevImmunol.2013006618
Lang, C.A., Naryshkin, S., Schneider, D.L., Mills, B.J., Lindeman, R.D., 1992. Low blood glutathione levels in healthy aging adults. J. Lab. Clin. Med. 120, 720–725. https://doi.org/10.5555/uri:pii:002221439290079Z
Lee, T.B., Moon, Y.S., Choi, C.H., 2012. Histone H4 deacetylation down-regulates catalase gene expression in doxorubicin-resistant AML subline. Cell Biol. Toxicol. 28, 11–18. https://doi.org/10.1007/s10565-011-9201-y
Lee, Y.S., Cheon, I.S., Kim, B.H., Kwon, M.J., Lee, H.W., Kim, T.Y., 2013. Loss of extracellular superoxide dismutase induces severe IL-23-mediated skin inflammation in mice. J. Invest. Dermatol. 133, 732–741. https://doi.org/10.1038/jid.2012.406
Li, W., Cao, L., Han, L., Xu, Q., Ma, Q., 2015. Superoxide dismutase promotes the epithelial-mesenchymal transition of pancreatic cancer cells via activation of the H2O2/ERK/NF-κB axis. Int. J. Oncol. 46, 2613–2620. https://doi.org/10.3892/ijo.2015.2938
Li, X., Cai, Y., Wang, Y.S., Shi, Y.Y., Hou, W., Xu, C.S., Wang, H.Y., Ye, Z., Yao, L.B., Zhang, J., 2012. Hyperglycaemia Exacerbates Choroidal Neovascularisation in Mice via the Oxidative Stress-Induced Activation of STAT3 Signalling in RPE Cells. PLoS One 7. https://doi.org/10.1371/journal.pone.0047600
Liles, M.R., Newsome, D.A., Oliver, P.D., 1991. Antioxidant Enzymes in the Aging Human Retinal Pigment Epithelium. Arch. Ophthalmol. 109, 1285–1288. https://doi.org/10.1001/archopht.1991.01080090111033
Liu, Y., Liu, M., Zhang, X., Chen, Q., Chen, H., Sun, L., Liu, G., 2016. Protective Effect of Fucoxanthin Isolated from Laminaria japonica against Visible Light-Induced Retinal Damage Both in Vitro and in Vivo. J. Agric. Food Chem. 64, 416–424. https://doi.org/10.1021/acs.jafc.5b05436
Liu, Z., Sun, L., Zhu, L., Jia, X., Li, X., Jia, H., Wang, Y., Weber, P., Long, J., Liu, J., 2007. Hydroxytyrosol protects retinal pigment epithelial cells from acrolein-induced oxidative stress and mitochondrial dysfunction. J. Neurochem. 103, 071019075320004-??? https://doi.org/10.1111/j.1471-4159.2007.04954.x
Lu, H., Hunt, D.M., Ganti, R., Davis, A., Dutt, K., Alam, J., Hunt, R.C., 2002. Metallothionein protects retinal pigment epithelial cells against apoptosis and oxidative stress. Exp. Eye Res. 74, 83–92. https://doi.org/10.1006/exer.2001.1101
Lu, L., Oveson, B.C., Jo, Y.J., Lauer, T.W., Usui, S., Komeima, K., Xie, B., Campochiaro, P.A., 2009. Increased expression of glutathione peroxidase 4 strongly protects retina from oxidative damage. Antioxidants Redox Signal. 11, 715–724. https://doi.org/10.1089/ars.2008.2171
Lubos, E., Loscalzo, J., Handy, D.E., 2011. Glutathione peroxidase-1 in health and disease: From molecular mechanisms to therapeutic opportunities. Antioxidants Redox Signal. https://doi.org/10.1089/ars.2010.3586
Maddipati, K.R., Marnett, L.J., 1987. Characerization of the major hydroperoxide-reducing activity of human plasma. Purification and properties of a selenium-dependent glutathione peroxidase. J. Biol. Chem. 262, 17398–17403. https://doi.org/10.1016/s0021-9258(18)45392-6
Makino, N., Mise, T., Sagara, J. ichi, 2008. Kinetics of hydrogen peroxide elimination by astrocytes and C6 glioma cells. Analysis based on a mathematical model. Biochim. Biophys. Acta - Gen. Subj. 1780, 927–936. https://doi.org/10.1016/j.bbagen.2008.03.010
Mateos, M. V, 2015. Inflammation and Oxidative Stress in Retinal Diseases: The Role of Intracellular Signaling in the Retinal Pigment Epithelium. Int. J. Ophthalmol. Clin. Res. 2. https://doi.org/10.23937/2378-346x/1410033
Meister, A., 1984. New aspects of glutathione biochemistry and transport: Selective alteration of glutathione metabolism. Fed. Proc.
Miceli, M. V., Liles, M.R., Newsome, D.A., 1994. Evaluation of oxidative processes in human pigment epithelial cells associated with retinal outer segment phagocytosis. Exp. Cell Res. 214, 242–249. https://doi.org/10.1006/excr.1994.1254
Milton, R.C., Clemons, T.E., Klien, R., Seddon, J.M., Ferris, F.L., 2005. Risk factors for the incidence of advanced age-related macular degeneration in the Age-Related Eye Disease Study (AREDS): AREDS report no. 19. Ophthalmology 112, 533-539.e1. https://doi.org/10.1016/j.ophtha.2004.10.047
Mishima, K., Handa, J.T., Aotaki-Keen, A., Lutty, G.A., Morse, L.S., Hjelmeland, L.M., 1999. Senescence-associated β-galactosidase histochemistry for the primate eye. Investig. Ophthalmol. Vis. Sci. 40, 1590–1593.
Mitra, A.K., 2020. Antioxidants: A Masterpiece of Mother Nature to Prevent Illness. J. Chem. Rev. 2, 243–256. https://doi.org/10.33945/SAMI/JCR.2020.4.3
Miyamura, N., Ogawa, T., Boylan, S., Morse, L.S., Handa, J.T., Hjelmeland, L.M., 2004. Topographic and age-dependent expression of heme oxygenase-1 and catalase in the human retinal pigment epithelium. Investig. Ophthalmol. Vis. Sci. 45, 1562–1565. https://doi.org/10.1167/iovs.02-0761
Møller, I.M., Jensen, P.E., Hansson, A., 2007. Oxidative modifications to cellular components in plants. Annu. Rev. Plant Biol. https://doi.org/10.1146/annurev.arplant.58.032806.103946
Monaghan-Benson, E., Hartmann, J., Vendrov, A.E., Budd, S., Byfield, G., Parker, A., Ahmad, F., Huang, W., Runge, M., Burridge, K., Madamanchi, N., Hartnett, M.E., 2010. The role of vascular endothelial growth factor-induced activation of NADPH oxidase in choroidal endothelial cells and choroidal neovascularization. Am. J. Pathol. 177, 2091–2102. https://doi.org/10.2353/ajpath.2010.090878
Moron, M.S., Depierre, J.W., Mannervik, B., 1979. Levels of glutathione, glutathione reductase and glutathione S-transferase activities in rat lung and liver. BBA - Gen. Subj. 582, 67–78. https://doi.org/10.1016/0304-4165(79)90289-7
Mrowicka, M., Mrowicki, J., Szaflik, J.P., Szaflik, M., Ulinska, M., Szaflik, J., Majsterek, I., 2017. Analysis of antioxidative factors related to AMD risk development in the polish patients. Acta Ophthalmol. 95, 530–536. https://doi.org/10.1111/aos.13289
Mukherjee, P.K., Marcheselli, V.L., Serhan, C.N., Bazan, N.G., 2004. Neuroprotectin D1: A docosahexaenoic acid-derived docosatriene protects human retinal pigment epithelial cells from oxidative stress. Proc. Natl. Acad. Sci. U. S. A. 101, 8491–8496. https://doi.org/10.1073/pnas.0402531101
Mullarkey, C.J., Edelstein, D., Brownlee, M., 1990. Free radical generation by early glycation products: A mechanism for accelerated atherogenesis in diabetes. Biochem. Biophys. Res. Commun. 173, 932–939. https://doi.org/10.1016/S0006-291X(05)80875-7
Murphy, M.P., 2009. How mitochondria produce reactive oxygen species. Biochem. J. 417, 1–13. https://doi.org/10.1042/BJ20081386
Narimatsu, T., Negishi, K., Miyake, S., Hirasawa, M., Osada, H., Kurihara, T., Tsubota, K., Ozawa, Y., 2015. Blue light-induced inflammatory marker expression in the retinal pigment epithelium-choroid of mice and the protective effect of a yellow intraocular lens material invivo. Exp. Eye Res. 132, 48–51. https://doi.org/10.1016/j.exer.2015.01.003
Ni, T., Yang, W., Xing, Y., 2019. Protective effects of delphinidin against H2O2-induced oxidative injuries in human retinal pigment epithelial cells. Biosci. Rep. 39. https://doi.org/10.1042/BSR20190689
Nicolas, M.G., Fujiki, K., Murayama, K., Suzuki, M.T., Shindo, N., Hotta, Y., Iwata, F., Fujimura, T., Yoshikawa, Y., Cho, F., Kanai, A., 1996. Studies on the mechanism of early onset macular degeneration in cynomolgus monkeys. II. Suppression of metallothionein synthesis in the retina in oxidative stress. Exp. Eye Res. 62, 399–408. https://doi.org/10.1006/exer.1996.0045
Nita, M., Grzybowski, A., 2016. The Role of the Reactive Oxygen Species and Oxidative Stress in the Pathomechanism of the Age-Related Ocular Diseases and Other Pathologies of the Anterior and Posterior Eye Segments in Adults. Oxid. Med. Cell. Longev. https://doi.org/10.1155/2016/3164734
Novack, R.L., Stefánsson, E., 1990. Measurement of Retina and Optic Nerve Oxidative Metabolism in Vivo via Dual Wavelength Reflection Spectrophotometry of Cytochrome a, a 3, in: Noninvasive Diagnostic Techniques in Ophthalmology. Springer New York, pp. 499–509. https://doi.org/10.1007/978-1-4613-8896-8_25
Ohira, A., Tanito, M., Kaidzu, S., Kondo, T., 2003. Glutathione peroxidase induced in rat retinas to counteract photic injury. Investig. Ophthalmol. Vis. Sci. 44, 1230–1236. https://doi.org/10.1167/iovs.02-0191
Ozawa, Y., Sasaki, M., Takahashi, N., Kamoshita, M., Miyake, S., Tsubota, K., 2012. Neuroprotective effects of lutein in the retina. ingentaconnect.com 18, 51–56.
Panda-Jonas, S., Jonas, J.B., Jakobczyk-Zmija, M., 1996. Retinal pigment epithelial cell count, distribution, and correlations in normal human eyes. Am. J. Ophthalmol. 121, 181–189. https://doi.org/10.1016/S0002-9394(14)70583-5
Panieri, E., Gogvadze, V., Norberg, E., Venkatesh, R., Orrenius, S., Zhivotovsky, B., 2013. Reactive oxygen species generated in different compartments induce cell death, survival, or senescence. Free Radic. Biol. Med. 57, 176–187. https://doi.org/10.1016/j.freeradbiomed.2012.12.024
Pascolini, D., Mariotti, S.P., Pokharel, G.P., Pararajasegaram, R., Etya’ale, D., Négrel, A.D., Resnikoff, S., 2004. 2002 Global update of available data on visual impairment: A compilation of population-based prevalence studies. Ophthalmic Epidemiol. https://doi.org/10.1076/opep.11.2.67.28158
Plafker, S.M., O’Mealey, G.B., Szweda, L.I., 2012. Mechanisms for Countering Oxidative Stress and Damage in Retinal Pigment Epithelium, in: International Review of Cell and Molecular Biology. Elsevier Inc., pp. 135–177. https://doi.org/10.1016/B978-0-12-394309-5.00004-3
Plestina-Borjan, I., Katusic, D., Medvidovic-Grubisic, M., Supe-Domic, D., Bucan, K., Tandara, L., Rogosic, V., 2015. Association of age-related macular degeneration with erythrocyte antioxidant enzymes activity and serum total antioxidant status. Oxid. Med. Cell. Longev. 2015. https://doi.org/10.1155/2015/804054
Qin, S., Gerard A Rodrigues, 2008. Progress and perspectives on the role of RPE cell inflammatory responses in the development of age-related macular degeneration. J. Inflamm. Res. 49. https://doi.org/10.2147/jir.s4354
Ramachandran, S., Morris, S.M., Devamanoharan, P., Henein, M., Varma, S.D., 1991. Radio-isotopic determination of hydrogen peroxide in aqueous humor and urine. Exp. Eye Res. 53, 503–506. https://doi.org/10.1016/0014-4835(91)90167-D
Rex, T.S., Tsui, I., Hahn, P., Maguire, A.M., Duan, D., Bennett, J., Dunaief, J.L., 2004. Adenovirus-mediated delivery of catalase to retinal pigment epithelial cells protects neighboring photoreceptors from photo-oxidative stress. Hum. Gene Ther. 15, 960–967. https://doi.org/10.1089/hum.2004.15.960
Rizzolo, L.J., 2014. Barrier properties of cultured retinal pigment epithelium. Exp. Eye Res. https://doi.org/10.1016/j.exer.2013.12.018
Rosen, R.B., Hu, D.N., Chen, M., McCormick, S.A., Walsh, J., Roberts, J.E., 2012. Effects of melatonin and its receptor antagonist on retinal pigment epithelial cells against hydrogen peroxide damage. Mol.Vis. 18, 1640–1648.
Sajeeth, C.I., Manna, P.K., Manavalan, R., 2011. Antioxidant Activity of Polyherbal Formulation on Streptozotocin Induced Diabetes in Experimental Animals. Der Pharm. Sin. 2, 220–226.
Samiec, P.S., Drews-Botsch, C., Flagg, E.W., Kurtz, J.C., Sternberg, P., Reed, R.L., Jones, D.P., 1998. Glutathione in human plasma: Decline in association with aging, age- related macular degeneration, and diabetes. Free Radic. Biol. Med. 24, 699–704. https://doi.org/10.1016/S0891-5849(97)00286-4
Sasaki, M., Yuki, K., Kurihara, T., Miyake, S., Noda, K., Kobayashi, S., Ishida, S., Tsubota, K., Ozawa, Y., 2012. Biological role of lutein in the light-induced retinal degeneration. J. Nutr. Biochem. 23, 423–429. https://doi.org/10.1016/j.jnutbio.2011.01.006
Schieber, M., Chandel, N.S., 2014. ROS function in redox signaling and oxidative stress. Curr. Biol. 24, R453–R462. https://doi.org/10.1016/j.cub.2014.03.034
Seddon, J.M., Ajani, U.A., Sperduto, R.D., Hiller, R., Blair, N., Burton, T.C., Farber, M.D., Gragoudas, E.S., Haller, J., Miller, D.T., Yannuzzi, L.A., Willett, W., 1994. Dietary Carotenoids, Vitamins A, C, and E, and Advanced Age-Related Macular Degeneration. JAMA J. Am. Med. Assoc. 272, 1413–1420. https://doi.org/10.1001/jama.1994.03520180037032
Sen, C.K., Khanna, S., Gordillo, G., Bagchi, D., Bagchi, M., Roy, S., 2002. Oxygen, oxidants, and antioxidants in wound healing: An emerging paradigm, in: Annals of the New York Academy of Sciences. New York Academy of Sciences, pp. 239–249. https://doi.org/10.1111/j.1749-6632.2002.tb02920.x
Shen, X.L., Jia, L.H., Zhao, P., Fan, R., Pan, X.Y., Yang, H.M., Liu, L., 2012. Changes in blood oxidative and antioxidant parameters in a group of chinese patients with age-related macular degeneration. J. Nutr. Heal. Aging 16, 201–204. https://doi.org/10.1007/s12603-011-0350-8
Simon, H.U., Haj-Yehia, A., Levi-Schaffer, F., 2000. Role of reactive oxygen species (ROS) in apoptosis induction. Apoptosis 5, 415–418. https://doi.org/10.1023/A:1009616228304
Sindhi, V., Gupta, V., Sharma, K., Bhatnagar, S., Kumari, R., Dhaka, N., 2013. Potential applications of antioxidants – A review. J. Pharm. Res. 7, 828–835. https://doi.org/10.1016/j.jopr.2013.10.001
Sjølie, A.K., Klein, R., Porta, M., Orchard, T., Fuller, J., Parving, H.H., Bilous, R., Aldington, S., Chaturvedi, N., 2011. Retinal microaneurysm count predicts progression and regression of diabetic retinopathy. Post-hoc results from the DIRECT Programme. Diabet. Med. 28, 345–351. https://doi.org/10.1111/j.1464-5491.2010.03210.x
Smith, W., Assink, J., Klein, R., Mitchell, P., Klaver, C.C.W., Klein, B.E.K., Hofman, A., Jensen, S., Wang, J.J., De Jong, P.T.V.M., 2001. Risk factors for age-related macular degeneration: Pooled findings from three continents. Ophthalmology 108, 697–704. https://doi.org/10.1016/S0161-6420(00)00580-7
Spector, A., Ma, W., Wang, R.R., 1998. The aqueous humor is capable of generating and degrading H2O2. Investig. Ophthalmol. Vis. Sci. 39, 1188–1197.
Subrizi, A., Toropainen, E., Ramsay, E., Airaksinen, A.J., Kaarniranta, K., Urtti, A., 2015. Oxidative stress protection by exogenous delivery of rhhsp70 chaperone to the retinal pigment epithelium (RPE), a possible therapeutic strategy against RPE degeneration. Pharm. Res. 32, 211–221. https://doi.org/10.1007/s11095-014-1456-6
Sui, G.Y., Liu, G.C., Liu, G.Y., Gao, Y.Y., Deng, Y., Wang, W.Y., Tong, S.H., Wang, L., 2013. Is sunlight exposure a risk factor for age-related macular degeneration? A systematic review and meta-analysis. Br. J. Ophthalmol. https://doi.org/10.1136/bjophthalmol-2012-302281
Sundelin, S.P., Nilsson, S.E.G., Brunk, U.T., 2001. Lipofuscin-formation in cultured retinal pigment epithelial cells is related to their melanin content. Free Radic. Biol. Med. 30, 74–81. https://doi.org/10.1016/S0891-5849(00)00444-5
Tabatabaie, T., Floyd, R.A., 1994. Susceptibility of glutathione peroxidase and glutathione reductase to oxidative damage and the protective effect of spin trapping agents. Arch. Biochem. Biophys. 314, 112–119. https://doi.org/10.1006/abbi.1994.1418
Taguchi, H., Takanashi, T., Hashizoe, M., Ogura, Y., Honda, Y., 1996. In vivo quantitation of peroxides in the vitreous humor after panretinal laser photocoagulation. Investig. Ophthalmol. Vis. Sci. 37.
Tang, J., Kern, T.S., 2011. Inflammation in diabetic retinopathy. Prog. Retin. Eye Res. https://doi.org/10.1016/j.preteyeres.2011.05.002
Tate, D.J., Miceli, M. V., Newsome, D.A., 1999. Zinc protects against oxidative damage in cultured human retinal pigment epithelial cells. Free Radic. Biol. Med. 26, 704–713. https://doi.org/10.1016/S0891-5849(98)00253-6
Tate, T.Dm.Mn., 1995. Phagocytosis and H2O2 induce catalase and metallothionein gene expression in human retinal pigment epithelial cells. Investig. Ophthalmol. Vis. Sci. 36, 1271–1279.
Taylor, H.R., West, S., Muñoz, B., Rosenthal, F.S., Bressler, S.B., Bressler, N.M., 1992. The Long-term Effects of Visible Light on the Eye. Arch. Ophthalmol. 110, 99–104. https://doi.org/10.1001/archopht.1992.01080130101035.
Tokarz, P., Kaarniranta, K., Blasiak, J., 2013. Role of antioxidant enzymes and small molecular weight antioxidants in the pathogenesis of age-related macular degeneration (AMD). Biogerontology. https://doi.org/10.1007/s10522-013-9463-2
Tosi, G.M., Marigliani, D., Romeo, N., Toti, P., 2014. Disease Pathways in Proliferative Vitreoretinopathy: An Ongoing Challenge. J. Cell. Physiol. 229, 1577–1583. https://doi.org/10.1002/jcp.24606
Trakkides, T.O., Schäfer, N., Reichenthaler, M., Kühn, K., Enzmann, V., Pauly, D., 2019. Oxidative stress in retinal pigment epithelial cells increased endogenous complement-dependent inflammatory and angiogenic responses - Independent from exogenous complement sources. bioRxiv 722470. https://doi.org/10.1101/722470
Ueta, T., Inoue, T., Furukawa, T., Tamaki, Y., Nakagawa, Y., Imai, H., Yanagi, Y., 2012. Glutathione peroxidase 4 is required for maturation of photoreceptor cells. J. Biol. Chem. 287, 7675–7682. https://doi.org/10.1074/jbc.M111.335174
Ulańczyk, Z., Grabowicz, A., Cecerska-Heryć, E., Śleboda-Taront, D., Krytkowska, E., Mozolewska-Piotrowska, K., Safranow, K., Kawa, M.P., Dołęgowska, B., Machalińska, A., 2020. Dietary and lifestyle factors modulate the activity of the endogenous antioxidant system in patients with age-related macular degeneration: Correlations with disease severity. Antioxidants 9, 1–19. https://doi.org/10.3390/antiox9100954
Umazume, K., Tsukahara, R., Liu, L., Fernandez De Castro, J.P., McDonald, K., Kaplan, H.J., Tamiya, S., 2014. Role of retinal pigment epithelial cell β-catenin signaling in experimental proliferative vitreoretinopathy. Am. J. Pathol. 184, 1419–1428. https://doi.org/10.1016/j.ajpath.2014.01.022
Ung et al., 2017, 2017. Oxidative stress and reactive oxygen species: a review of their role in ocular disease. Clin. Sci. 131, 2865–2883. https://doi.org/10.1042/CS20171246
Valko, M., Rhodes, C.J., Moncol, J., Izakovic, M., Mazur, M., 2006. Free radicals, metals and antioxidants in oxidative stress-induced cancer. Chem. Biol. Interact. https://doi.org/10.1016/j.cbi.2005.12.009
Venza, I., Visalli, M., Cucinotta, M., Teti, D., Venza, M., 2012. Association between oxidative stress and macromolecular damage in elderly patients with age-related macular degeneration. Aging Clin. Exp. Res. 24, 21–27. https://doi.org/10.3275/7659
Voloboueva, L.A., Liu, J., Suh, J.H., Ames, B.N., Miller, S.S., 2005. (R)-α-lipoic acid protects retinal pigment epithelial cells from oxidative damage. Investig. Ophthalmol. Vis. Sci. 46, 4302–4310. https://doi.org/10.1167/iovs.04-1098
Wang, P., Zhou, S., Xu, L., Lu, Y., Yuan, X., Zhang, H., Li, R., Fang, J., Liu, P., 2013. Hydrogen peroxide-mediated oxidative stress and collagen synthesis in cardiac fibroblasts: Blockade by tanshinone IIA. J. Ethnopharmacol. 145, 152–161. https://doi.org/10.1016/j.jep.2012.10.044.
Weydert, C.J., Cullen, J.J., 2010. Measurement of superoxide dismutase, catalase and glutathione peroxidase in cultured cells and tissue. Nat. Protoc. 5, 51–66. https://doi.org/10.1038/nprot.2009.197
Wolf, S., 2008. Current status of anti-vascular endothelial growth factor therapy in Europe. Jpn. J. Ophthalmol. https://doi.org/10.1007/s10384-008-0580-4
Yamashita, H., Horie, K., Yamamoto, T., Nagano, T., Hirano, T., 1992. Light-induced retinal damage in mice: Hydrogen peroxide production and superoxide dismutase activity in retina. Retina 12, 59–66. https://doi.org/10.1097/00006982-199212010-00012
Yang, I.H., Lee, J.J., Wu, P.C., Kuo, H.K., Kuo, Y.H., Huang, H.M., 2020. Oxidative stress enhanced the transforming growth factor-β2-induced epithelial-mesenchymal transition through chemokine ligand 1 on ARPE-19 cell. Sci. Rep. 10, 1–10. https://doi.org/10.1038/s41598-020-60785-x
Yang, P., Peairs, J.J., Tano, R., Jaffe, G.J., 2006. Oxidant-mediated Akt activation in human RPE cells. Investig. Ophthalmol. Vis. Sci. 47, 4598–4606. https://doi.org/10.1167/iovs.06-0140
Yang, X., Chung, J.Y., Rai, U., Esumi, N., 2018. Cadherins in the retinal pigment epithelium (RPE) revisited: P-cadherin is the highly dominant cadherin expressed in human and mouse RPE in vivo. PLoS One 13, 1–20. https://doi.org/10.1371/journal.pone.0191279
Yau, J.W.Y., Rogers, S.L., Kawasaki, R., Lamoureux, E.L., Kowalski, J.W., Bek, T., Chen, S.J., Dekker, J.M., Fletcher, A., Grauslund, J., Haffner, S., Hamman, R.F., Ikram, M.K., Kayama, T., Klein, B.E.K., Klein, R., Krishnaiah, S., Mayurasakorn, K., O’Hare, J.P., Orchard, T.J., Porta, M., Rema, M., Roy, M.S., Sharma, T., Shaw, J., Taylor, H., Tielsch, J.M., Varma, R., Wang, J.J., Wang, N., West, S., Zu, L., Yasuda, M., Zhang, X., Mitchell, P., Wong, T.Y., 2012. Global prevalence and major risk factors of diabetic retinopathy. Diabetes Care 35, 556–564. https://doi.org/10.2337/dc11-1909
Young, I.S., Woodside, J. V, 2001. Antioxidants in health and disease. J. Clin. Pathol. https://doi.org/10.1136/jcp.54.3.176
Yu, A.L., Fuchshofer, R., Kook, D., Kampik, A., Bloemendal, H., Welge-Lüssen, U., 2009. Subtoxic oxidative stress induces senescence in retinal pigment epithelial cells via TGF-β release. Investig. Ophthalmol. Vis. Sci. 50, 926–935. https://doi.org/10.1167/iovs.07-1003
Zhang, X.Y., Ng, T.K., Brelén, M.E., Wu, D., Wang, J.X., Chan, K.P., Yung, J.S.Y., Cao, D., Wang, Y., Zhang, S., Chan, S.O., Pang, C.P., 2016. Continuous exposure to non-lethal doses of sodium iodate induces retinal pigment epithelial cell dysfunction. Sci. Rep. 6, 1–13. https://doi.org/10.1038/srep37279
Zhao, H., Wang, R., Ye, M., Zhang, L., 2019. Genipin protects against H 2 O 2 -induced oxidative damage in retinal pigment epithelial cells by promoting Nrf2 signaling. Int. J. Mol. Med. 43, 936–944. https://doi.org/10.3892/ijmm.2018.4027.
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