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Current Protein & Peptide Science

Author(s): Yissell Borges-Rodríguez, Rodrigo Morales-Cueto* and Lina Rivillas-Acevedo*

DOI: 10.2174/1389203724666230106161436

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Effect of the Ultraviolet Radiation on the Lens

Page: [215 - 228] Pages: 14

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Abstract

The lens is a transparent, biconvex anatomical structure of the eyes responsible for light transmission and fine focusing on the retina. It is fundamentally constituted by water-soluble proteins called crystallins which are responsible for lens transparency due to their stable and highly organized disposition in the lens fiber cells. Some conformational changes and the subsequent aggregation of crystallins lead to loss of transparency in the lens and are the beginning of cataracts, which is the most frequent cause of reversible blindness in the world. Ultraviolet radiation is considered one of the risk factors for cataract development. The lens is exposed to radiation between 295 and 400 nm. This UV radiation may induce several processes that destroy the crystallins; the most significant is the oxidative stress due to increased free radicals formation. The oxidative stress is directly involved in modifications of the crystallin proteins leading to the formation of high molecular weight aggregates and then the subsequent opacification of the lens, known as cataracts. This review aims to summarize current knowledge about the damage of the lens proteins caused by ultraviolet radiation and its role in developing cataracts.

Keywords: Cataracts, crystallins, lens, ultraviolet radiation, free radicals, reactive oxygen species, membrane cation transport.

Graphical Abstract

[1]
Honrubia, F. General ophthalmology; General Ophthalmology, 2002.
[2]
Ortega, J.; Cortés, C.; Suárez, S. Postnatal development of porcine crystallin proteins; Universidad Complutense de Madrid, 2001.
[3]
Bassnett, S. Lens organelle degradation. Exp. Eye Res., 2002, 74(1), 1-6.
[http://dx.doi.org/10.1006/exer.2001.1111] [PMID: 11878813]
[4]
Bassnett, S. On the mechanism of organelle degradation in the vertebrate lens. Exp. Eye Res., 2009, 88(2), 133-139.
[http://dx.doi.org/10.1016/j.exer.2008.08.017] [PMID: 18840431]
[5]
Sánchez, A.; Sánchez, D. New contributions to the clinical-molecular correlation of senile catarats; Universidad de Salamanca, 2009.
[6]
Artigas, C. Effects of ultraviolet radiation on the spectral transmission of the lens of the common pig; Universidad Cardenal Herrera CEU, 2015, pp. 46-60.
[7]
Wistow, G. Domain structure and evolution in α-crystallins and small heat-shock proteins. FEBS Lett., 1985, 181(1), 1-6.
[http://dx.doi.org/10.1016/0014-5793(85)81102-9] [PMID: 3972098]
[8]
Grosas, A. Eye Lens Crystallins: Remarkable Long-Lived Proteins. In: Long-Lived Proteins in Human Aging and Disease; , 2021.
[9]
Siezen, R.I.; Hoenders, H.J. The Quaternary Structure of Bovine a-Crystallin Surface Probing by Limited Proteolysis in vitro. Eur. J. Biochem., 1979, 96(3), 431-440.
[http://dx.doi.org/10.1111/j.1432-1033.1979.tb13055.x]
[10]
Moran, S.D.; Zhang, T.O.; Decatur, S.M.; Zanni, M.T. Amyloid fiber formation in human γD-Crystallin induced by UV-B photodamage. Biochemistry, 2013, 52(36), 6169-6181.
[http://dx.doi.org/10.1021/bi4008353] [PMID: 23957864]
[11]
De Jong, WW.; Lubsen, NH.; Kraft, HJ. Molecular evolution of the eye lens. Retinal Eye Res., 1994, 0278-04327.
[12]
Zigler, J.S.; Rao, P.V. Enzyme/crystallins and extremely high pyridine nucleotide levels in the eye lens. In: FASEB; , 1991; pp. 223-225.
[13]
Taylor, A.; Davies, K.J.A. Protein oxidation and loss of protease activity may lead to cataract formation in the aged lens. Free Radic. Biol. Med., 1987, 3(6), 371-377.
[http://dx.doi.org/10.1016/0891-5849(87)90015-3] [PMID: 3322949]
[14]
Shiels, A. Molecular genetics of cataracts; Garner and Klintworth’s Pathobiology of Ocular Disease, 2008, pp. 713-732.
[15]
Department of Health and Human Serv Ces.Las Cataratas, Lo que usted debe saber; National Eye Institute, 2020.
[16]
World Health Organization Blindness and vision impairment; , 2021.
[17]
Fu, S.; Dean, R.; Southan, M.; Truscott, R. The hydroxyl radical in lens nuclear cataractogenesis. J. Biol. Chem., 1998, 273(44), 28603-28609.
[http://dx.doi.org/10.1074/jbc.273.44.28603] [PMID: 9786852]
[18]
Zhang, Z.; Smith, D.L.; Smith, J.B. Human β-crystallins modified by backbone cleavage, deamidation and oxidation are prone to associate. Exp. Eye Res., 2003, 77(3), 259-272.
[http://dx.doi.org/10.1016/S0014-4835(03)00159-3] [PMID: 12907158]
[19]
Sharma, K.K.; Santhoshkumar, P. Lens aging: Effects of crystallins. Biochim. Biophys. Acta, Gen. Subj., 2009, 1790(10), 1095-1108.
[http://dx.doi.org/10.1016/j.bbagen.2009.05.008] [PMID: 19463898]
[20]
Rocha, M.A.; Sprague-Piercy, M.A.; Kwok, A.O.; Roskamp, K.W.; Martin, R.W. Chemical properties determine solubility and stability in βγ‐crystallins of the eye lens. ChemBioChem, 2021, 22(8), 1329-1346.
[http://dx.doi.org/10.1002/cbic.202000739] [PMID: 33569867]
[21]
Chiou, S.H.; Chylack, L.T., Jr; Tung, W.H.; Bunn, H.F. Nonenzymatic glycosylation of bovine lens crystallins. Effect of aging. J. Biol. Chem., 1981, 256(10), 5176-5180.
[http://dx.doi.org/10.1016/S0021-9258(19)69382-8] [PMID: 7228874]
[22]
Beswick, H.T.; Harding, J.J. Conformational changes induced in lens α- and γ-crystallins by modification with glucose 6-phosphate. Implications for cataract. Biochem. J., 1987, 246(3), 761-769.
[http://dx.doi.org/10.1042/bj2460761] [PMID: 3689329]
[23]
Fan, X.; Monnier, V.M. Protein posttranslational modification (PTM) by glycation: Role in lens aging and age-related cataractogenesis. Exp. Eye Res., 2021, 210, 108705.
[http://dx.doi.org/10.1016/j.exer.2021.108705] [PMID: 34297945]
[24]
Vetter, C.J.; Thorn, D.C.; Wheeler, S.G.; Mundorff, C.C.; Halverson, K.A.; Wales, T.E.; Shinde, U.P.; Engen, J.R.; David, L.L.; Carver, J.A.; Lampi, K.J. Cumulative deamidations of the major lens protein γS -crystallin increase its aggregation during unfolding and oxidation. Protein Sci., 2020, 29(9), 1945-1963.
[http://dx.doi.org/10.1002/pro.3915] [PMID: 32697405]
[25]
Robertson, L.J.G.; David, L.L.; Riviere, M.A.; Wilmarth, P.A.; Muir, M.S.; Morton, J.D. Susceptibility of ovine lens crystallins to proteolytic cleavage during formation of hereditary cataract. Invest. Ophthalmol. Vis. Sci., 2008, 49(3), 1016-1022.
[http://dx.doi.org/10.1167/iovs.07-0792] [PMID: 18326725]
[26]
Giblin, F.J.; Anderson, D.M.G.; Han, J.; Rose, K.L.; Wang, Z.; Schey, K.L. Acceleration of age-induced proteolysis in the guinea pig lens nucleus by in vivo exposure to hyperbaric oxygen: A mass spectrometry analysis. Exp. Eye Res., 2021, 210, 108697.
[http://dx.doi.org/10.1016/j.exer.2021.108697] [PMID: 34233175]
[27]
Wang, S.S.; Wen, W.S. Examining the influence of ultraviolet C irradiation on recombinant human γD-crystallin. Mol. Vis., 2010, 16, 2777-2790.
[PMID: 21197112]
[28]
Serebryany, E.; Takata, T.; Erickson, E.; Schafheimer, N.; Wang, Y.; King, J.A. Aggregation of Trp > Glu point mutants of human gamma-D crystallin provides a model for hereditary or UV-induced cataract. Protein Sci., 2016, 25(6), 1115-1128.
[http://dx.doi.org/10.1002/pro.2924] [PMID: 26991007]
[29]
Andley, U.P.; Clark, B.A. Generation of oxidants in the near-UV photooxidation of human lens alpha-crystallin. Invest. Ophthalmol. Vis. Sci., 1989, 30(4), 706-713.
[PMID: 2703311]
[30]
Balasubramanian, D.; Du, X.; Zigler, J.S., Jr The reaction of singlet oxygen with proteins, with special reference to crystallins. Photochem. Photobiol., 1990, 52(4), 761-768.
[http://dx.doi.org/10.1111/j.1751-1097.1990.tb08679.x] [PMID: 2089424]
[31]
Truscott, R.J.W. Age-related nuclear cataract—oxidation is the key. Exp. Eye Res., 2005, 80(5), 709-725.
[http://dx.doi.org/10.1016/j.exer.2004.12.007] [PMID: 15862178]
[32]
Santhoshkumar, P.; Udupa, P.; Murugesan, R.; Sharma, K.K. Significance of interactions of low molecular weight crystallin fragments in lens aging and cataract formation. J. Biol. Chem., 2008, 283(13), 8477-8485.
[http://dx.doi.org/10.1074/jbc.M705876200] [PMID: 18227073]
[33]
Schafheimer, N.; Wang, Z.; Schey, K.; King, J. Tyrosine/cysteine cluster sensitizing human γD-crystallin to ultraviolet radiation-induced photoaggregation in vitro. Biochemistry, 2014, 53(6), 979-990.
[http://dx.doi.org/10.1021/bi401397g] [PMID: 24410332]
[34]
Cetinel, S.; Semenchenko, V.; Cho, J.Y.; Sharaf, M.G.; Damji, K.F.; Unsworth, L.D.; Montemagno, C. UV-B induced fibrillization of crystallin protein mixtures. PLoS One, 2017, 12(5), e0177991.
[http://dx.doi.org/10.1371/journal.pone.0177991]
[35]
Alperstein, A.M.; Ostrander, J.S.; Zhang, T.O.; Zanni, M.T. Amyloid found in human cataracts with two-dimensional infrared spectroscopy. Proc. Natl. Acad. Sci. USA, 2019, 116(14), 6602-6607.
[http://dx.doi.org/10.1073/pnas.1821534116] [PMID: 30894486]
[36]
Starr, C.; Evers, C.A. Starr, Lisa. Biology: concepts and applications. Thomson; Brooks/Cole, 2006.
[37]
Balasubramanian, D.; Balasubramanian, D. Ultraviolet radiation and cataract. J. Ocul. Pharmacol. Ther., 2000, 16(3), 285-297.
[http://dx.doi.org/10.1089/jop.2000.16.285] [PMID: 10872925]
[38]
González, R. Knowledge about the ocular damage caused by ultraviolet radiation in the student population of the departmental college of Cucaita, Boyacá. An education model for prevention. University of La Salle Science Unisalle, 2007.
[39]
Haag, R.; Sieber, N.; Heßling, M. Cataract development by exposure to ultraviolet and blue visible light in porcine lenses. Medicina , 2021, 57(6), 535.
[http://dx.doi.org/10.3390/medicina57060535]
[40]
Andrade, M.; Zaratti, F.; Forno, R. At Atmosphere. Pan American Health Organization, 2003, 79-81.
[41]
Lago, C.; Antoni, J.; Roda, M.; Carles, J.; Parra, O. Assessment of changes in ocular optical quality in patients with cataracts using the double-pass technique; Universitat Politécnica de Cayalunya, 2012.
[42]
Marín, D.O.; Marín, O. Corneal effects caused by ultraviolet radiation and air pollution; Universidad de La Salle, 2008.
[43]
Gozalo, P.D. Review of eye care for protection against ultraviolet radiation; Universidad de Valladolid, 2015.
[44]
Imbert, E.; Peña, T.; Martínez, E. Oxidative stress in ocular pathology. Electronic J. Porta. Medicos.com, 2012.
[45]
Kamari, F.; Hallaj, S.; Dorosti, F.; Alinezhad, F.; Taleschian-Tabrizi, N.; Farhadi, F. Phototoxicity of environmental radiations in human lens: revisiting the pathogenesis of UV-induced cataract. Graefe’s Archive for Clinical and Experimental Ophthalmology; Springer Verlag, 2019, Vol. 25, pp. 72065-72077.
[46]
Taylor, H. Ocular effects of UV-B exposure. Documenta Ophthalmologica, 1995, 88, 285-293.
[http://dx.doi.org/10.1007/BF01203682]
[47]
Ferrer, Y.; Gregorio, I. Oxidative stress: its impact on cataracts. Rev. Cuba. Farm., 2009, 43(3)
[48]
Modenese, A.; Gobba, F. Cataract frequency and subtypes involved in workers assessed for their solar radiation exposure: a systematic review. Acta Ophthalmol., 2018, 96(8), 779-788.
[http://dx.doi.org/10.1111/aos.13734]
[49]
Miric, D.J.; Kisic, B.B.; Zoric, L.D.; Mitic, R.V.; Miric, B.M.; Dragojevic, I.M. Xanthine oxidase and lens oxidative stress markers in diabetic and senile cataract patients. J. Diabetes Complications, 2013, 27(2), 171-176.
[http://dx.doi.org/10.1016/j.jdiacomp.2012.09.005] [PMID: 23142692]
[50]
Varma, S.D.; Hegde, K.; Henein, M. Oxidative damage to mouse lens in culture. Protective effect of pyruvate. Biochimica et Biophysica Acta (BBA) -. General Subjects, 2003, 1621(3), 246-252.
[http://dx.doi.org/10.1016/S0304-4165(03)00075-8]
[51]
Garner, W.H.; Garner, M.H.; Spector, A.H. 202-induced uncoupling of bovine lens Na+, K+-ATPase. Med. Sci., 1982, 80, 2044-2048.
[52]
Varma, S.D.; Kumar, S.; Richards, R.D. Light-induced damage to ocular lens cation pump: Prevention by vitamin C acid/superoxide/cataract). Proc. Natl. Sci. USA, 1979, 76(7), 3504-3506.
[53]
Taylor, H.R. Ultraviolet radiation and the eye: an epidemiologic study. Trans. Am. Ophthalmol. Soc., 1989, 87, 802-853.
[54]
Kinoshita, J.H. Mechanisms initiating cataract formation. Proctor Lecture. Invest. Ophthalmol., 1974, 13(10), 713-724.
[PMID: 4278188]
[55]
Roberts, JE Ocular phototoxicity. J. Photochem. Photobiol. Biol., 2001, 64(2-3), 136-143.
[56]
Chen, J.; Toptygin, D.; Brand, L.; King, J. Mechanism of the efficient tryptophan fluorescence quenching in human γD-crystallin studied by time-resolved fluorescence. Biochemistry, 2008, 47(40), 10705-10721.
[http://dx.doi.org/10.1021/bi800499k]
[57]
Pattison, D.I.; Rahmanto, A.S.; Davies, M.J. Photo-oxidation of proteins. In: Photochemical and Photobiological Sciences; Royal Society of Chemistry, 2012; 11, pp. 38-53.
[http://dx.doi.org/10.1039/c1pp05164d]
[58]
Chen, J.; Callis, P.R.; King, J. Mechanism of the very efficient quenching of tryptophan fluorescence in human γ D- and γ S-crystallins: the γ-crystallin fold may have evolved to protect tryptophan residues from ultraviolet photodamage. Biochemistry, 2009, 48(17), 3708-3716.
[http://dx.doi.org/10.1021/bi802177g] [PMID: 19358562]
[59]
Kanwar, R.; Balasubramanian, D. Structure and stability of the dityrosine-linked dimer of gammaB-crystallin. Exp. Eye Res., 1999, 68(6), 773-784.
[http://dx.doi.org/10.1006/exer.1999.0669] [PMID: 10375441]
[60]
Linetsky, M.; Ortwerth, B.J. Quantitation of the singlet oxygen produced by UVA irradiation of human lens proteins. Photochem. Photobiol., 1997, 65(3), 522-529.
[http://dx.doi.org/10.1111/j.1751-1097.1997.tb08598.x] [PMID: 9077138]
[61]
Andrade, G.; Alcántara, H.G.; González, M.; Silva, R.; Vilchis Landeros, L.H. Redox homeostasis. In: Mens. Bioquim; , 2020.
[62]
Castillo, M. in vitro and in vivo models of aging, oxidative stress and antioxidant protection. 2002.
[63]
Chaudhury, S.; Roy, P.; Dasgupta, S. Green tea flavanols protect human γB-crystallin from oxidative photodamage. Biochimie, 2017, 137, 46-55.
[http://dx.doi.org/10.1016/j.biochi.2017.02.016] [PMID: 28285129]
[64]
Finkel, T.; Holbrook, N.J. Oxidants, oxidative stress and the biology of ageing. Nature, 2000, 408(6809), 239-247.
[http://dx.doi.org/10.1038/35041687] [PMID: 11089981]
[65]
Guerra, J.I.E.; Guerra, J.I. Oxidative stress, diseases and antioxidant treatments. An. Med. Interna, 2001, 18(6), 326-335.
[66]
Satoh, K.; Takemura, Y.; Satoh, M.; Ozaki, K.; Kubota, S. Loss of FYCO1 leads to cataract formation. Sci. Rep., 2021, 11(1), 13771.
[http://dx.doi.org/10.1038/s41598-021-93110-1] [PMID: 34215815]
[67]
Naim, K.; Nair, S.T.; Yadav, P.; Shanavas, A.; Neelakandan, P.P. Supramolecular confinement within chitosan nanocomposites enhances singlet oxygen generation. ChemPlusChem, 2018, 83(5), 418-422.
[http://dx.doi.org/10.1002/cplu.201800041] [PMID: 31957367]
[68]
Zigman, S.; Yulo, T.; Griess, G.A. Inactivation of catalase by near ultraviolet light and tryptophan photoproducts. Mol. Cell. Biochem., 1976, 11(3), 149-154.
[http://dx.doi.org/10.1007/BF01744995]
[69]
Reddy, G.B. Seetharam, Bhat K. Protection against UVB inactivation (in vitro) of rat lens enzymes by natural antioxidants. Mol. Cell. Biochem., 1999.
[70]
Shibata, S.; Shibata, N.; Shibata, T.; Sasaki, H.; Singh, D.P.; Kubo, E. The role of Prdx6 in the protection of cells of the crystalline lens from oxidative stress induced by UV exposure. Jpn. J. Ophthalmol., 2016, 60(5), 408-418.
[http://dx.doi.org/10.1007/s10384-016-0461-1] [PMID: 27379999]
[71]
Wahlig, S.; Lovatt, M.; Mehta, J.S. Functional role of peroxiredoxin 6 in the eye. Free Radic. Biol. Med., 2018, 126, 210-220.
[http://dx.doi.org/10.1016/j.freeradbiomed.2018.08.017] [PMID: 30120980]
[72]
Hasanova, N.; Kubo, E.; Kumamoto, Y.; Takamura, Y.; Akagi, Y. Age-related cataracts and Prdx6: correlation between severity of lens opacity, age and the level of Prdx 6 expression. Br. J. Ophthalmol., 2009, 93(8), 1081-1084.
[http://dx.doi.org/10.1136/bjo.2008.152272] [PMID: 19429582]
[73]
Álvarez-Barrios, A.; Álvarez, L.; García, M.; Artime, E.; Pereiro, R.; González-Iglesias, H. Antioxidant defenses in the human eye: A focus on metallothioneins. Antioxidants, 2021, 10(1), 89.
[http://dx.doi.org/10.3390/antiox10010089] [PMID: 33440661]
[74]
Varma, S.D.; Kovtun, S.; Hegde, K.R. Role of ultraviolet irradiation and oxidative stress in cataract formation-medical prevention by nutritional antioxidants and metabolic agonists. Eye Contact Lens, 2011, 37(4), 233-245.
[http://dx.doi.org/10.1097/ICL.0b013e31821ec4f2] [PMID: 21670697]
[75]
Mills, I.A.; Flaugh, S.L.; Kosinski-Collins, M.S.; King, J.A. Folding and stability of the isolated Greek key domains of the long-lived human lens proteins γD-crystallin and γS-crystallin. Protein Sci., 2007, 16(11), 2427-2444.
[http://dx.doi.org/10.1110/ps.072970207] [PMID: 17905830]
[76]
Mizdrak, J.; Hains, P.G.; Truscott, R.J.W.; Jamie, J.F.; Davies, M.J. Tryptophan-derived ultraviolet filter compounds covalently bound to lens proteins are photosensitizers of oxidative damage. Free Radic. Biol. Med., 2008, 44(6), 1108-1119.
[http://dx.doi.org/10.1016/j.freeradbiomed.2007.12.003] [PMID: 18206985]
[77]
Varma, S.D.; Ramachandran, S.; Devamanoharan, P.S.; Morris, S.M.; Ali, A.H. Prevention of oxidative damage to rat lens by pyruvate in vitro: Possible attenuation in vivo. Curr. Eye Res., 1995, 14(8), 643-649.
[http://dx.doi.org/10.3109/02713689508998491] [PMID: 8529399]
[78]
Bent, D.; Hayon, E. Excited State Chemistry of Aromatic Amino Acids and Related Peptides. I. Tyrosine. J. Am. Chem. Soc., 1974, 97, 2599-2606.
[79]
Davies, M.J. Reactive species formed on proteins exposed to singlet oxygen. Photochem. Photobiol. Sci., 2004, 3(1), 17-25.
[http://dx.doi.org/10.1039/b307576c] [PMID: 14743273]
[80]
Fuentes-Lemus, E.; Hägglund, P.; López-Alarcón, C.; Davies, M.J. Oxidative crosslinking of peptides and proteins: mechanisms of formation, detection, characterization and quantification. Molecules, 2021, 27(1), 15.
[http://dx.doi.org/10.3390/molecules27010015] [PMID: 35011250]
[81]
van Kuijk, F.J. Effects of ultraviolet light on the eye: Role of protective glasses. Environ. Health Perspect., 1991, 96, 177-184.
[http://dx.doi.org/10.1289/ehp.9196177] [PMID: 1820264]
[82]
Jedziniak, J.; Arredondo, M.; Andley, U. Oxidative damage to human lens enzymes. Curr. Eye Res., 1987, 6(2), 345-350.
[http://dx.doi.org/10.3109/02713688709025186] [PMID: 3568748]
[83]
Dillon, J.; Spector, A.; Nakanishi, K. Identification of β carbolines isolated from fluorescent human lens proteins. Nature, 1976, 259(5542), 422-423.
[http://dx.doi.org/10.1038/259422a0] [PMID: 1250390]
[84]
Ambrogelly, A. The different colors of mabs in solution. Antibodies (Basel), 2021, 10(2), 21.
[http://dx.doi.org/10.3390/antib10020021] [PMID: 34073775]
[85]
Stadtman, E.R.; Levine, R.L. Free radical-mediated oxidation of free amino acids and amino acid residues in proteins. Amino Acids, 2003, 25(3-4), 207-218.
[http://dx.doi.org/10.1007/s00726-003-0011-2] [PMID: 14661084]
[86]
Quiney, C.; Finnegan, S.; Groeger, G.; Cotter, T.G. Protein oxidation. Protein Reviews, 2011, 13, 57-78.
[87]
Kim, H.J.; Ha, S.; Lee, H.Y.; Lee, K.J. ROSics: Chemistry and proteomics of cysteine modifications in redox biology. Mass Spectrom. Rev., 2015, 34(2), 184-208.
[http://dx.doi.org/10.1002/mas.21430] [PMID: 24916017]
[88]
Garzon, L. Eye, light, life and evolution. Arch. Med., 2009, 5(2), 5.
[89]
Yugay, M.T.; Pereira, P.C.; Leiria, F.; Mota, M.C. Oxidative damage to lens membranes induced by metal-catalyzed systems. Ophthalmic Res., 1996, 28(1), 92-96.
[http://dx.doi.org/10.1159/000267979]
[90]
Davies, M.J. Singlet oxygen-mediated damage to proteins and its consequences. Biochem. Biophys. Res. Commun., 2003, 305(3), 761-770.
[http://dx.doi.org/10.1016/S0006-291X(03)00817-9] [PMID: 12763058]
[91]
Alcock, L.J.; Perkins, M.V.; Chalker, J.M. Chemical methods for mapping cysteine oxidation. Chem. Soc. Rev., 2018, 47(1), 231-268.
[http://dx.doi.org/10.1039/C7CS00607A]
[92]
Mamoun, A. Biological Functions of Proteins; Santa Cruz Biotechnology, 2014.
[93]
van Bergen, L.A.H.; Roos, G.; De Proft, F. From thiol to sulfonic acid: modeling the oxidation pathway of protein thiols by hydrogen peroxide. J. Phys. Chem. A, 2014, 118(31), 6078-6084.
[http://dx.doi.org/10.1021/jp5018339] [PMID: 25036614]
[94]
Garland, D. Role of site-specific, metal-catalyzed oxidation in lens aging and cataract: A hypothesis. Exp. Eye Res., 1990, 50(6), 677-682.
[http://dx.doi.org/10.1016/0014-4835(90)90113-9] [PMID: 2197108]
[95]
Garland, D.; Russell, P.; Zigler, S. The Oxidative Modification of Lens Proteins. Oxygen Rad. Biol. Med., 1988, 347-352.
[96]
Carney Almroth, B. Oxidative damage in fish used as biomarkers in field and laboratory studies; University of Gothenburg, 2008.
[97]
Garland, D.; Zigler, J.S., Jr; Kinoshita, J. Structural changes in bovine lens crystallins induced by ascorbate, metal, and oxygen. Arch. Biochem. Biophys., 1986, 251(2), 771-776.
[http://dx.doi.org/10.1016/0003-9861(86)90389-9] [PMID: 3800399]
[98]
Davies, M.J.; Dean, R.T. Radical-mediated protein oxidation: From chemistry to medicine, 1st ed; Oxford University Press, 1997, p. 465.
[99]
Shacter, E. Quantification and significance of protein oxidation in biological samples. Drug Metab. Rev., 2000, 32(3-4), 307-326.
[http://dx.doi.org/10.1081/DMR-100102336] [PMID: 11139131]
[100]
Dean, R.T.; Fu, S.; Stocker, R.; Davies, M.J. Biochemistry and pathology of radical-mediated protein oxidation. Biochem. J., 1997, 324(1), 1-18.
[http://dx.doi.org/10.1042/bj3240001] [PMID: 9164834]
[101]
Wolff, S.P.; Gamer, A.; Dean, R.T. Free radicals, lipids and protein degradation. Trends Biochem. Sci., 1986, 11(1), 27-31.
[http://dx.doi.org/10.1016/0968-0004(86)90228-8]
[102]
Davies, K.J. Protein damage and degradation by oxygen radicals. I. general aspects. J. Biol. Chem., 1987, 262(20), 9895-9901.
[http://dx.doi.org/10.1016/S0021-9258(18)48018-0] [PMID: 3036875]
[103]
Plowman, J.E.; Deb-Choudhury, S.; Grosvenor, A.J.; Dyer, J.M. Protein oxidation: identification and utilisation of molecular markers to differentiate singlet oxygen and hydroxyl radical-mediated oxidative pathways. Photochem. Photobiol. Sci., 2013, 12(11), 1960-1967.
[http://dx.doi.org/10.1039/c3pp50182e] [PMID: 24057301]
[104]
Bartesaghi, S.; Radi, R. Fundamentals on the biochemistry of peroxynitrite and protein tyrosine nitration. Redox Biol., 2018, 14, 618-625.
[http://dx.doi.org/10.1016/j.redox.2017.09.009] [PMID: 29154193]
[105]
Poole, L.B. The basics of thiols and cysteines in redox biology and chemistry. Free Radic. Biol. Med., 2015, 80, 148-157.
[http://dx.doi.org/10.1016/j.freeradbiomed.2014.11.013] [PMID: 25433365]
[106]
Hawkins, C.L.; Davies, M.J. Detection, identification, and quantification of oxidative protein modifications. J. Biol. Chem., 2019, 294(51), 19683-19708.
[http://dx.doi.org/10.1074/jbc.REV119.006217] [PMID: 31672919]
[107]
Truscott, R.J.W.; Augusteyn, R.C. The state of sulphydryl groups in normal and cataractous human lenses. Exp. Eye Res., 1977, 25(2), 139-148.
[http://dx.doi.org/10.1016/0014-4835(77)90126-9] [PMID: 913506]
[108]
Lou, MF. Redox regulation in the lens. Prog. Retinal Eye Res., 2003, 22(5), 657-682.
[http://dx.doi.org/10.1016/S1350-9462(03)00050-8]
[109]
Serebryany, E.; Yu, S.; Trauger, S.A.; Budnik, B.; Shakhnovich, E.I. Dynamic disulfide exchange in a crystallin protein in the human eye lens promotes cataract-associated aggregation. J. Biol. Chem., 2018, 293(46), 17997-18009.
[http://dx.doi.org/10.1074/jbc.RA118.004551] [PMID: 30242128]
[110]
Truscott, R.J.W.; Mizdrak, J.; Friedrich, M.G.; Hooi, M.Y.; Lyons, B.; Jamie, J.F.; Davies, M.J.; Wilmarth, P.A.; David, L.L. Is protein methylation in the human lens a result of non-enzymatic methylation by S-adenosylmethionine? Exp. Eye Res., 2012, 99, 48-54.
[http://dx.doi.org/10.1016/j.exer.2012.04.002] [PMID: 22542751]
[111]
Kuck, F.R.; Nabiev, I.R.; Yu, G. Surface-enhanced Raman spectra of eye lens pigments. Appl. Spect., 1990, 44(4), 571-575.
[112]
Das, B.K.; Sun, T.X.; Akhtar, N.J.; Chylack, L.T., Jr; Liang, J.J. Fluorescence and immunochemical studies of advanced glycation-related lens pigments. Invest. Ophthalmol. Vis. Sci., 1998, 39(11), 2058-2066.
[PMID: 9761284]
[113]
Zingler, S. Aging of protein molecules: lens crystallins as a model system. Trends Biochem. Sci., 1981, 6, 133-136.
[114]
Andley, U.P.; Mathur, S.; Griest, T.A. Cloning, Expression, and Chaperone-like Activity of Human αA-Crystallin. J. Biol. Chem., 1996, 270(50), 31973-31980.
[115]
Ortwerth, B.J.; Feather, M.S.; Olesen, P. The precipitation and cross-linking of lens crystallins by ascorbic acid. Exp. Eye Res., 1988, 47(1), 155-168.
[116]
Ranjan, M.; Beedu, S.R. Spectroscopic and biochemical correlations during the course of human lens aging. BMC Ophthalmol., 2006, 6(1), 10.
[http://dx.doi.org/10.1186/1471-2415-6-10] [PMID: 16519820]
[117]
Mucke, H.A.M.; Mucke, P.; Mucke, E. Pharmacological therapies for cataract and refractive errors: landscaping niches of ocular drug patenting. Pharm. Pat. Anal., 2012, 1(2), 165-175.
[http://dx.doi.org/10.4155/ppa.12.23] [PMID: 24236781]
[118]
Heruye, S.H.; Maffofou Nkenyi, L.N.; Singh, N.U.; Yalzadeh, D.; Ngele, K.K.; Njie-Mbye, Y.F.; Ohia, S.E.; Opere, C.A. Current trends in the pharmacotherapy of cataracts. Pharmaceuticals (Basel), 2020, 13(1), 15.
[http://dx.doi.org/10.3390/ph13010015] [PMID: 31963166]
[119]
Guo, S.P.; Chang, H.C.; Lu, L.S.; Liu, D.Z.; Wang, T.J. Activation of kelch-like ECH-associated protein 1/nuclear factor erythroid 2-related factor 2/antioxidant response element pathway by curcumin enhances the anti-oxidative capacity of corneal endothelial cells. Biomed. Pharmacother., 2021, 141, 111834.
[http://dx.doi.org/10.1016/j.biopha.2021.111834] [PMID: 34153850]
[120]
Fernandez, M.; Afshari, N. Nutrition and the prevention of cataracts. Curr. Opin. Ophthalmol., 2018, 19(1), 66-70.
[PMID: 18090901]
[121]
Ruiss, M.; Findl, O.; Kronschlager, M. The human lens: An antioxidant-dependent tissue revealed by the role of caffeine. Ageing Res. Rev., 2022, 79, 101664.
[122]
Feng, W.; Yang, X.; Feng, M.; Pan, H.; Liu, J.; Hu, Y.; Wang, S.; Zhang, D.; Ma, F.; Mao, Y. Alginate oligosaccharide prevents against D-galactose-mediated Cataract in C57BL/6J mice via regulating oxidative stress and antioxidant system. Curr. Eye Res., 2021, 46(6), 802-810.
[http://dx.doi.org/10.1080/02713683.2020.1842456]
[123]
Tanito, M. Reported evidence of vitamin E protection against cataract and glaucoma. Free Radic. Biol. Med., 2021, 177, 100-119.
[http://dx.doi.org/10.1016/j.freeradbiomed.2021.10.027] [PMID: 34695546]
[124]
Braakhuis, A.J.; Donaldson, C.I.; Lim, J.C.; Donaldson, P.J. Nutritional strategies to prevent lens cataract: Current status and future strategies. Nutrients, 2019, 11(5), 1186.
[http://dx.doi.org/10.3390/nu11051186] [PMID: 31137834]
[125]
Lim, J.C.; Caballero Arredondo, M.; Braakhuis, A.J.; Donaldson, P.J. Vitamin C and the lens: New insights into delaying the onset of cataract. Nutrients, 2020, 12(10), 3142.
[http://dx.doi.org/10.3390/nu12103142] [PMID: 33066702]
[126]
Zhang, X.; Peng, L.; Dai, Y.; Xie, Q.; Wu, P.; Chen, M.; Liu, C. Anti-cataract effects of coconut water in vivo and in vitro. Biomed. Pharmacother., 2021, 143, 112032.
[http://dx.doi.org/10.1016/j.biopha.2021.112032]
[127]
Upaphong, P.; Thonusin, C.; Choovuthayakorn, J.; Chattipakorn, N.; Chattipakorn, S.C. The possible positive mechanisms of pirenoxine in cataract formation. Int. J. Mol. Sci., 2022, 23(16), 9431.
[http://dx.doi.org/10.3390/ijms23169431] [PMID: 36012695]
[128]
Zhao, L.; Chen, X.; Zhu, J.; Xi, Y.; Yang, X.; Hu, L.; Ouyang, H.; Patel, S.; Jin, X.; Lin, D.; Wu, F.; Flagg, K.; Li, G.; Cao, G.; Lin, Y.; Chen, D.; Wen, C.; Chung, C.; Wang, Y.; Qiu, A.; Yeh, E.; Wang, W.; Hu, W.; Grob, S.; Abagyan, R.; Su, Z.; Tondro, H.; Zhao, X.; Luo, H.; Hou, R.; Perry, J.; Gao, W.; Kozao, I.; Granet, D.; Li, Y.; Sun, X.; Wang, J.; Zhang, L.; Liu, Y.; Yan, Y.; Zhang, K. Lanosterol reverses protein aggregation in cataracts. Nature, 2015, 523(7562), 607-611.
[129]
Kang, H.; Yang, Z.; Zhou, R. Lanosterol disrupts aggregation of human γd-crystallin by binding to the hydrophobic dimerization interface. J. Am. Chem. Soc., 2018, 140(27), 8479-8486.
[http://dx.doi.org/10.1021/jacs.8b03065]
[130]
Anbaraki, A.; Khoshaman, K.; Ghasemi, Y.; Yousefi, R. Preventive role of lens antioxidant defense mechanism against riboflavin-mediated sunlight damaging of lens crystallins. Int. J. Biol. Macromol., 2016, 91, 895-904.
[http://dx.doi.org/10.1016/j.ijbiomac.2016.06.047] [PMID: 27316765]
[131]
Shang, F.; Lu, M.; Dudek, E.; Reddan, J.; Taylor, A. Vitamin C and vitamin E restore the resistance of GSH-depleted lens cells to H2O2. Free Radic. Biol. Med., 2003, 34(5), 521-530.
[http://dx.doi.org/10.1016/S0891-5849(02)01304-7] [PMID: 12614841]
[132]
Gao, S.; Qin, T.; Liu, Z.; Caceres, M.A.; Ronchi, C.F.; Chen, C.Y.; Yeum, K.J.; Taylor, A.; Blumberg, J.B.; Liu, Y.; Shang, F. Lutein and zeaxanthin supplementation reduces H2O2-induced oxidative damage in human lens epithelial cells. Mol. Vis., 2011, 17, 3180-3190.
[PMID: 22194644]
[133]
Rathore, M.; Gupta, V. Protective effect of amino acids on eye lenses against oxidative stress induced by hydrogen peroxide. Asian J. Pharm. Clin. Res., 2010, 3(3), 166-169.
[134]
Dolar-Szczasny, J.; Flieger, J.; Kowalska, B.; Majerek, D.; Tatarczak-Michalewska, M.; Zakrocka, I.; Załuska, W.; Rejdak, R. Hemodialysis effect on the composition of the eye fluid of cataract patients. J. Clin. Med., 2021, 10(23), 5485.
[http://dx.doi.org/10.3390/jcm10235485] [PMID: 34884186]
[135]
Barman, S.; Srinivasan, K. Zinc supplementation ameliorates diabetic cataract through modulation of crystallin proteins and polyol pathway in experimental rats. Biol. Trace Elem. Res., 2019, 187(1), 212-223.
[http://dx.doi.org/10.1007/s12011-018-1373-3] [PMID: 29756175]
[136]
Williams, R.J.; Spencer, J.P.E.; Rice-Evans, C. Flavonoids: antioxidants or signalling molecules? Free Radic. Biol. Med., 2004, 36(7), 838-849.
[http://dx.doi.org/10.1016/j.freeradbiomed.2004.01.001] [PMID: 15019969]
[137]
Anwar, F.; Latif, S.; Ashraf, M.; Gilani, A.H. Moringa oleifera: a food plant with multiple medicinal uses. Phytother. Res., 2007, 21(1), 17-25.
[http://dx.doi.org/10.1002/ptr.2023] [PMID: 17089328]
[138]
Pathak, N.; Pant, N.; Singh, J.; Agrawal, S. Antioxidant activity of Trigonella foenum graecum L. using various in vitro models. Int. J. Herb. Med., 2014.