Protective effects of carnosine on dehydroascorbate-induced structural alteration and opacity of lens crystallins: important implications of carnosine pleiotropic functions to combat cataractogenesis

References

• Ames, B. N., Shigenaga, M. K., & Hagen, T. M. (1993). Oxidants, antioxidants, and the degenerative diseases of aging. Proceedings of the National Academy of Sciences, 90, 7915–7922.10.1073/pnas.90.17.7915
   PubMed Web of Science ®Google Scholar
• Amin, S., Barnett, G. V., Pathak, J. A., Roberts, C. J., & Sarangapani, P. S. (2014). Protein aggregation, particle formation, characterization and rheology. Current Opinion in Colloid and Interface Science, 19, 438–449. doi:10.1016/j.cocis.2014.10.002
   Web of Science ®Google Scholar
• Andley, U. P. (2009). Effects of α-crystallin on lens cell function and cataract pathology. Current Molecular Medicine, 9, 887–892.10.2174/156652409789105598
   PubMed Web of Science ®Google Scholar
• Attanasio, F., Cataldo, S., Fisichella, S., Nicoletti, S., Nicoletti, V. G., Pignataro, B., Savarino, A., & Rizzarelli, E. (2009). Protective effects of L- and D-carnosine on α-crystallin amyloid fibril formation: Implications for cataract disease. Biochemistry, 48, 6522–6531. doi:10.1021/bi900343n
   PubMed Web of Science ®Google Scholar
• Babizhayev, M. A. (1989). Antioxidant activity of L-carnosine, a natural histidine-containing dipeptide in crystalline lens. Biochimica et Biophysica Acta (BBA) – Lipids and Lipid Metabolism, 1004, 363–371. doi:10.1016/0005-2760(89)90085-4
   PubMed Web of Science ®Google Scholar
• Ballinger, M. L., Thomas, M. C., Nigro, J., Ivey, M. E., Dilley, R. J., & Little, P. J. (2005). Glycated and carboxy-methylated proteins do not directly activate human vascular smooth muscle cells. Kidney International, 68, 2756–2765.10.1111/j.1523-1755.2005.00746.x
   PubMed Web of Science ®Google Scholar
• Bensch, K. G., Fleming, J. E., & Lohmann, W. (1985). The role of ascorbic acid in senile cataract. Proceedings of the National Academy of Sciences, 82, 7193–7196.10.1073/pnas.82.21.7193
   PubMed Web of Science ®Google Scholar
• Berlett, B. S., & Stadtman, E. R. (1997). Protein oxidation in aging, disease, and oxidative stress. Journal of Biological Chemistry, 272, 20313–20316. doi:10.1074/jbc.272.33.20313
   PubMed Web of Science ®Google Scholar
• Beswick, H. T., & Harding, J. J. (1987). Conformational changes induced in lens α-and γ-crystallins by modification with glucose 6-phosphate. Implications for cataract. Biochemical Journal, 246, 761–769. doi:10.1042/bj2460761
   PubMed Web of Science ®Google Scholar
• Bigley, R. H., & Stankova, L. (1974). Uptake and reduction of oxidized and reduced ascorbate by human leukocytes. Journal of Experimental Medicine, 139, 1084–1092. doi:10.1084/jem.139.5.1084
   PubMed Web of Science ®Google Scholar
• Bloemendal, H., de Jong, W., Jaenicke, R., Lubsen, N. H., Slingsby, C., & Tardieu, A. (2004). Ageing and vision: Structure, stability and function of lens crystallins. Progress in Biophysics and Molecular Biology, 86, 407–485. doi:10.1016/j.pbiomolbio.2003.11.012
   PubMed Web of Science ®Google Scholar
• Boldyrev, A. A. (1993). Does carnosine possess direct antioxidant activity? International Journal of Biochemistry, 25, 1101–1107. doi:10.1016/0020-711X(93)90587-5
   PubMedGoogle Scholar
• Boldyrev, A. A., Aldini, G., & Derave, W. (2013). Physiology and pathophysiology of carnosine. Physiological Reviews, 93, 1803–1845. doi:10.1152/physrev.00039.2012
   PubMed Web of Science ®Google Scholar
• Bradford, M. M. (1976). A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding. Analytical Biochemistry, 72, 248–254. doi:10.1016/0003-2697(76)90527-3
   PubMed Web of Science ®Google Scholar
• Bumagina, Z., Gurvits, B., Artemova, N., Muranov, K., & Kurganov, B. (2010). Paradoxical acceleration of dithiothreitol-induced aggregation of insulin in the presence of a chaperone. International Journal of Molecular Sciences, 11, 4556–4579. doi:10.3390/ijms11114556
   PubMed Web of Science ®Google Scholar
• Cheng, R., Feng, Q., Argirov, O. K., & Ortwerth, B. J. (2004). Structure elucidation of a novel yellow chromophore from human lens protein. Journal of Biological Chemistry, 279, 45441–45449.10.1074/jbc.M405664200
   PubMed Web of Science ®Google Scholar
• David, L. L., & Shearer, T. R. (1984). Calcium-activated proteolysis in the lens nucleus during selenite cataractogenesis. Investigative Ophthalmology and Visual Science, 25, 1275–1283.
   PubMed Web of Science ®Google Scholar
• Du, J., Cullen, J. J., & Buettner, G. R. (2012). Ascorbic acid: Chemistry, biology and the treatment of cancer. Biochimica et Biophysica Acta (BBA) – Reviews on Cancer, 1826, 443–457. doi:10.1016/j.bbcan.2012.06.003
   PubMed Web of Science ®Google Scholar
• Fan, X., & Monnier, V. M. (2008). Nucleophilic compounds decrease advanced glycation end products (AGEs) from ascorbic acid in the hSVCT2 transgenic mouse model of lenticular aging. Investigative Opthalmology & Visual Science, 49, 4945. doi:10.1167/iovs.08-1813
   PubMed Web of Science ®Google Scholar
• Garland, D. L. (1991). Ascorbic acid and the eye. The American Journal of Clinical Nutrition, 54, 1198S–1202S
   Google Scholar
• Ghahramani, M., Yousefi, R., Khoshaman, K., & Alavianmehr, M. M. (2015). The impact of calcium ion on structure and aggregation propensity of peroxynitrite-modified lens crystallins: New insights into the pathogenesis of cataract disorders. Colloids and Surfaces B: Biointerfaces, 125, 170–180. doi:10.1016/j.colsurfb.2014.11.002
   PubMed Web of Science ®Google Scholar
• Ghosh, S., Pandey, N. K., Banerjee, P., Chaudhury, K., Nagy, N. V., & Dasgupta, S. (2015). Copper (II) directs formation of toxic amorphous aggregates resulting in inhibition of hen egg white lysozyme fibrillation under alkaline salt-mediated conditions. Journal of Biomolecular Structure and Dynamics, 33, 991–1007. doi:10.1080/07391102.2014.921864
   PubMed Web of Science ®Google Scholar
• Grünewald, R. A. (1993). Ascorbic acid in the brain. Brain Research Reviews, 18, 123–133. doi:10.1016/0165-0173(93)90010-W
   PubMedGoogle Scholar
• Hasan, A., Smith, J. B., Qin, W., & Smith, D. L. (1993). The reaction of bovine lens αA-crystallin with aspirin. Experimental Eye Research, 57, 29–35. doi:10.1006/exer.1993.1095
   PubMed Web of Science ®Google Scholar
• Hipkiss, A. R., Brownson, C., & Carrier, M. J. (2001). Carnosine, the anti-ageing, anti-oxidant dipeptide, may react with protein carbonyl groups. Mechanisms of Ageing and Development, 122, 1431–1445. doi:10.1016/S0047-6374(01)00272-X
   PubMed Web of Science ®Google Scholar
• Hipkiss, A. R., & Chana, H. (1998). Carnosine protects proteins against methylglyoxal-mediated modifications. Biochemical and Biophysical Research Communications, 248, 28–32. doi:10.1006/bbrc.1998.8806
   PubMed Web of Science ®Google Scholar
• Hipkiss, A. R., Preston, J. E., Himsworth, D. T. M., Worthington, V. C., Keown, M., Michaelis, J., … Abbott, N. (1998). Pluripotent protective effects of carnosine, a naturally occurring dipeptidea. Annals of the New York Academy of Sciences, 854, 37–53. doi:10.1111/j.1749-6632.1998.tb09890.x
   PubMed Web of Science ®Google Scholar
• Hobart, L. J., Seibel, I., Yeargans, G. S., & Seidler, N. W. (2004). Anti-crosslinking properties of carnosine: Significance of histidine. Life Sciences, 75, 1379–1389. doi:10.1016/j.lfs.2004.05.002
   PubMed Web of Science ®Google Scholar
• Hoefelschweiger, B. K., Duerkop, A., & Wolfbeis, O. S. (2005). Novel type of general protein assay using a chromogenic and fluorogenic amine-reactive probe. Analytical Biochemistry, 344, 122–129. doi:10.1016/j.ab.2005.06.030.
   PubMed Web of Science ®Google Scholar
• Hornig, D. (1975). Distribution of ascorbic acid, metabolites and analogues in man and animals. Annals of the New York Academy of Sciences, 258, 103–118. doi:10.1111/j.1749-6632.1975.tb29271.x
   PubMed Web of Science ®Google Scholar
• Huang, Y., & Wang, K. K. (2001). The calpain family and human disease. Trends in Molecular Medicine, 7, 355–362. doi:10.1016/S1471-4914(01)02049-4
   PubMed Web of Science ®Google Scholar
• Kelly, S. M., Jess, T. J., & Price, N. C. (2005). How to study proteins by circular dichroism. Biochimica et Biophysica Acta (BBA) – Proteins and Proteomics, 1751, 119–139. doi:10.1016/j.bbapap.2005.06.005
   PubMed Web of Science ®Google Scholar
• Khalili-Hezarjaribi, H., Yousefi, R., & Akbar Moosavi-Movahedi, A. (2012). Effect of temperature and ionic strength on structure and chaperone activity of glycated and non-glycated alpha-crystallins. Protein and Peptide Letters, 19, 450–457. doi:10.2174/09298661279978939610.2174/092986612799789396
   PubMed Web of Science ®Google Scholar
• Khazaei, S., Yousefi, R., & Alavian-Mehr, M. M. (2012). Aggregation and fibrillation of eye lens crystallins by homocysteinylation; implication in the eye pathological disorders. The Protein Journal, 31, 717–727. doi:10.1007/s10930-012-9451-4
   PubMed Web of Science ®Google Scholar
• Korla, K. (2015). Reactive oxygen species and energy machinery: An integrated dynamic model. Journal of Biomolecular Structure and Dynamics, 1–16. doi: 10.1080/07391102.2015.1086958
   Web of Science ®Google Scholar
• Kumar, A., Randhawa, V., Acharya, V., Singh, K., & Kumar, S. (2015). Amino acids flanking the central core of Cu, Zn superoxide dismutase are important in retaining enzyme activity after autoclaving. Journal of Biomolecular Structure and Dynamics, 38(3), 1–39. doi: 10.1080/07391102.2015.1049551
   Web of Science ®Google Scholar
• Kumar, P. A., Reddy, P. Y., Srinivas, P. N. B. S., & Reddy, G. B. (2009). Delay of diabetic cataract in rats by the antiglycating potential of cumin through modulation of α-crystallin chaperone activity. The Journal of Nutritional Biochemistry, 20, 553–562. doi:10.1016/j.jnutbio.2008.05.015
   PubMed Web of Science ®Google Scholar
• Liang, J. N., & Chakrabarti, B. (1982). Spectroscopic investigations of bovine lens crystallins. 1. Circular dichroism and intrinsic fluorescence. Biochemistry, 21, 1847–1852. doi:10.1021/bi00537a022
   PubMed Web of Science ®Google Scholar
• Lin, J. (1997). Pathophysiology of cataracts: Copper ion and peroxidation in diabetics. Japanese Journal of Ophthalmology, 41, 130–137. doi:10.1016/S0021-5155(97)00030-0
   PubMed Web of Science ®Google Scholar
• Lin, J. M., Hirano, K., Tsuchiya, H., & Tanaka, Y. (1994). Changes in copper ion levels in the lens and vitreous of diabetic patients. Folia Ophthalmologica Japonica, 45, 357–357.
   Google Scholar
• Linetsky, M., Shipova, E., Cheng, R., & Ortwerth, B. J. (2008). Glycation by ascorbic acid oxidation products leads to the aggregation of lens proteins. Biochimica et Biophysica Acta (BBA) – Molecular Basis of Disease, 1782, 22–34 doi: 10.1016/j.bbadis.2007.10.003
   PubMed Web of Science ®Google Scholar
• Lou, M. F. (2003). Redox regulation in the lens. Progress in Retinal and Eye Research, 22, 657–682. doi:10.1016/S1350-9462(03)00050-8
   PubMed Web of Science ®Google Scholar
• Mason, C. V., & Hines, M. C. (1966). Alpha, beta, and gamma crystallins in the ocular lens of rabbits: Preparation and partial characterization. Investigative Ophthalmology and Visual Science, 5, 601–609.
   Google Scholar
• McNamara, M., & Augusteyn, R. C. (1984). The effects of hydrogen peroxide on lens proteins: A possible model for nuclear cataract. Experimental Eye Research, 38, 45–56. doi:10.1016/0014-4835(84)90137-4
   PubMed Web of Science ®Google Scholar
• Mikkelsen, R. B., & Wardman, P. (2003). Biological chemistry of reactive oxygen and nitrogen and radiation-induced signal transduction mechanisms. Oncogene, 22, 5734–5754. doi:10.1038/sj.onc.1206663
   PubMed Web of Science ®Google Scholar
• Miller, A. G., Meade, S. J., & Gerrard, J. A. (2003). New insights into protein crosslinking via the Maillard reaction: Structural requirements, the effect on enzyme function, and predicted efficacy of crosslinking inhibitors as anti-ageing therapeutics. Bioorganic and Medicinal Chemistry, 11, 843–852. doi:10.1016/S0968-0896(02)00565-5
   PubMed Web of Science ®Google Scholar
• Musci, G., & Berliner, L. J. (1985). Probing different conformational states of bovine alpha-lactalbumin: Fluorescence studies with 5, 5′-bis [8-anilino-1-naphthalenesulfonate]. Biochemistry, 24, 3852–3856. doi:10.1021/bi00336a006
   PubMed Web of Science ®Google Scholar
• Nagaraj, R. H., Sell, D. R., Prabhakaram, M., Ortwerth, B. J., & Monnier, V. M. (1991). High correlation between pentosidine protein crosslinks and pigmentation implicates ascorbate oxidation in human lens senescence and cataractogenesis. Proceedings of the National Academy of Sciences, 88, 10257–10261.10.1073/pnas.88.22.10257
   PubMed Web of Science ®Google Scholar
• Nagaraj, R. H., Shipanova, I. N., & Faust, F. M. (1996). Protein cross-linking by the maillard reaction: Isolation, characterization, and in vivo detection of a lysine-lysine cross-link derived from methylglyoxal. Journal of Biological Chemistry, 271, 19338–19345. doi:10.1074/jbc.271.32.19338
   PubMed Web of Science ®Google Scholar
• Nemet, I., & Monnier, V. M. (2011). Vitamin C degradation products and pathways in the human lens. Journal of Biological Chemistry, 286, 37128–37136. doi:10.1074/jbc.M111.245100
   PubMed Web of Science ®Google Scholar
• Ortwerth, B. J., Feather, M. S., & Olesen, P. R. (1988). The precipitation and cross-linking of lens crystallins by ascorbic acid. Experimental Eye Research, 47, 155–168. doi:10.1016/0014-4835(88)90032-2
   PubMed Web of Science ®Google Scholar
• Paoli, P., Sbrana, F., Tiribilli, B., Caselli, A., Pantera, B., Cirri, P., & Camici, G. (2010). Protein N-homocysteinylation induces the formation of toxic amyloid-like protofibrils. Journal of Molecular Biology, 400, 889–907. doi:10.1016/j.jmb.2010.05.039
   PubMed Web of Science ®Google Scholar
• Park, S., Yoon, J., Jang, S., Lee, K., & Shin, S. (2015). The role of the acidic domain of α-synuclein in amyloid fibril formation: a molecular dynamics study. Journal of Biomolecular Structure and Dynamics, 38(3), 1–8. doi: 10.1080/07391102.2015.1033016
   Web of Science ®Google Scholar
• Perry, R. E., Swamy, M. S., & Abraham, E. C. (1987). Progressive changes in lens crystallin glycation and high-molecular-weight aggregate formation leading to cataract development in streptozotocin-diabetic rats. Experimental Eye Research, 44, 269–282. doi:10.1016/S0014-4835(87)80011-8
   PubMed Web of Science ®Google Scholar
• Preston, J. E., Hipkiss, A. R., Himsworth, D. T., Romero, I. A., & Abbott, J. N. (1998). Toxic effects of β-amyloid (25–35) on immortalised rat brain endothelial cell: Protection by carnosine, homocarnosine and β-alanine. Neuroscience Letters, 242, 105–108. doi:10.1016/S0304-3940(98)00058-5
   PubMed Web of Science ®Google Scholar
• Qadeer, A., Zaman, M., & Khan, R. H. (2014). Inhibitory effect of post-micellar SDS concentration on thermal aggregation and activity of papain. Biochemistry (Moscow), 79, 785–796. doi:10.1134/S0006297914080069
   PubMed Web of Science ®Google Scholar
• Rácz, P., & Ördögh, M. (1977). Investigations on trace elements in normal and senile cataractous lenses. Albrecht von Graefes Archiv für Klinische und Experimentelle Ophthalmologie, 204, 67–72. doi:10.1007/BF02387418
   PubMedGoogle Scholar
• Raju, M., Santhoshkumar, P., Henzl, T. M., & Sharma, K. K. (2011). Identification and characterization of a copper-binding site in αA-crystallin. Free Radical Biology and Medicine, 50, 1429–1436. doi:10.1016/j.freeradbiomed.2011.01.036
   PubMed Web of Science ®Google Scholar
• Raman, B., Ramakrishna, T., & Rao, C. M. (1995). Rapid refolding studies on the chaperone-like α-crystallin effect of α-crystallin on refolding of β-and γ-crystallins. Journal of Biological Chemistry, 270, 19888–19892. doi:10.1074/jbc.270.34.19888
   PubMed Web of Science ®Google Scholar
• Robertson, L. J., David, L. L., Riviere, M. A., Wilmarth, P. A., Muir, M. S., & Morton, J. D. (2008). Susceptibility of ovine lens crystallins to proteolytic cleavage during formation of hereditary cataract. Investigative Opthalmology & Visual Science, 49, 1016–1022. doi:10.1167/iovs.07-0792
   PubMed Web of Science ®Google Scholar
• Sasaki, H., Giblin, F. J., Winkler, B. S., Chakrapani, B., Leverenz, V., & Shu, C. C. (1995). A protective role for glutathione-dependent reduction of dehydroascorbic acid in lens epithelium. Investigative Ophthalmology and Visual Science, 36, 1804–1817.
   PubMed Web of Science ®Google Scholar
• Seidler, N. W., Yeargans, G. S., & Morgan, T. G. (2004). Carnosine disaggregates glycated α-crystallin: an in vitro study. Archives of Biochemistry and Biophysics, 427, 110–115. doi:10.1016/j.abb.2004.04.024
   PubMed Web of Science ®Google Scholar
• Simpson, G. L., & Ortwerth, B. J. (2000). The non-oxidative degradation of ascorbic acid at physiological conditions. Biochimica et Biophysica Acta (BBA)-Molecular Basis of Disease, 1501, 12–24. doi:10.1016/S0925-4439(00)00009-0
   PubMed Web of Science ®Google Scholar
• Sinclair, A. J., Girling, A. J., Gray, L., Le Guen, C., Lunec, J., & Barnett, A. H. (1991). Disturbed handling of ascorbic acid in diabetic patients with and without microangiopathy during high dose ascorbate supplementation. Diabetologia, 34, 171–175. doi:10.1007/BF00418271
   PubMed Web of Science ®Google Scholar
• Slingsby, C., & Clout, N. J. (1999). Structure of the crystallins. Eye, 13, 395–402. doi:10.1038/eye.1999.113
   Google Scholar
• Smuda, M., & Glomb, M. A. (2013). Titelbild: Maillard degradation pathways of Vitamin C (Angew. Chem. 18/2013). Angewandte Chemie, 125, 4795–4795. doi:10.1002/ange.201302392
   Google Scholar
• Tessier, F., Obrenovich, M., & Monnier, V. M. (1999). Structure and mechanism of formation of human lens fluorophore LM-1: Relationship to vesperlysine A and the advanced Maillard reaction in aging, diabetes, and cataractogenesis. Journal of Biological Chemistry, 274, 20796–20804. doi:10.1074/jbc.274.30.20796
   PubMed Web of Science ®Google Scholar
• Varma, S. D., & Richards, R. D. (1988). Ascorbic acid and the eye lens. Ophthalmic Research, 20, 164–173. doi:10.1159/000266579
   PubMed Web of Science ®Google Scholar
• Viteri, G., Carrard, G., Birlouez-Aragón, I., Silva, E., & Friguet, B. (2004). Age-dependent protein modifications and declining proteasome activity in the human lens. Archives of Biochemistry and Biophysics, 427, 197–203. doi:10.1016/j.abb.2004.05.006
   PubMed Web of Science ®Google Scholar
• Wang, K., & Spector, A. (1994). The chaperone activity of bovine alpha crystallin. Interaction with other lens crystallins in native and denatured states. Journal of Biological Chemistry, 269, 13601–13608.
   PubMed Web of Science ®Google Scholar
• Weber, K., & Osborn, M. (1969). The reliability of molecular weight determinations by dodecyl sulfate-polyacrylamide gel electrophoresis. Journal of Biological Chemistry, 244, 4406–4412.
   PubMed Web of Science ®Google Scholar
• Winkler, B. S. (1987). In vitro oxidation of ascorbic acid and its prevention by GSH. Biochimica et Biophysica Acta (BBA)-General Subjects, 925, 258–264. doi: 10.1016/0304-4165(87)90190-5
   PubMed Web of Science ®Google Scholar
• Yan, H., & Harding, J. J. (2005). Carnosine protects against the inactivation of esterase induced by glycation and a steroid. Biochimica et Biophysica Acta (BBA) – Molecular Basis of Disease, 1741, 120–126. doi: 10.1016/j.bbadis.2004.11.008
   PubMed Web of Science ®Google Scholar
• Yokoyama, T., Sasaki, H., Giblin, F. J., & Reddy, V. N. (1994). A physiological level of ascorbate inhibits galactose cataract in guinea pigs by decreasing polyol accumulation in the lens epithelium: A dehydroascorbate-linked mechanism. Experimental Eye Research, 58, 207–218. doi:10.1006/exer.1994.1009
   PubMed Web of Science ®Google Scholar
• Yousefi, R., & Jalili, S. (2011). The synergistic chaperoning operation in a Bi-chaperone system consisting of alpha-crystallin and beta-casein: Bovine pancreatic insulin as the target protein. Colloids and Surfaces B: Biointerfaces, 88, 497–504. doi:10.1016/j.colsurfb.2011.07.040
   PubMed Web of Science ®Google Scholar
• Yousefi, R., Khazaei, S., & Movahedi, A. A. M. (2013). Effect of homocysteinylation on structure, chaperone activity and fibrillation propensity of lens alpha-crystallin. Protein and Peptide Letters, 20, 932–941.10.2174/0929866511320080011
   PubMed Web of Science ®Google Scholar
• Zhou, C., Qi, W., Lewis, E. N., & Carpenter, J. F. (2015). Concomitant Raman spectroscopy and dynamic light scattering for characterization of therapeutic proteins at high concentrations. Analytical Biochemistry, 472, 7–20. doi:10.1016/j.ab.2014.11.016
   PubMed Web of Science ®Google Scholar