Non-enzymatic glycation of α-crystallin as an in vitro model for aging, diabetes and degenerative diseases

Amino Acids

Volumn 47, Issue 12, 2015, Pages 2601-2608

  Karumanchi, Devi Kalyan ^a   Karunaratne, Nuwan ^a   Lurio, Laurence ^a   Dillon, James P ^a   Gaillard, Elizabeth R ^a  

^a NORTHERN ILLINOIS UNIVERSITY   (United States)

Author keywords

Aging; Alpha crystallin; Cataract; Degenerative diseases; Diabetes; Lens; Presbyopia

Indexed keywords

ADVANCED GLYCATION END PRODUCT; ALPHA CRYSTALLIN; CHAPERONE; HEAT SHOCK PROTEIN; METHYLGLYOXAL; PROTEIN BINDING;

AGING; ANIMAL TISSUE; ARTICLE; CONTROLLED STUDY; DEGENERATIVE DISEASE; DIABETES MELLITUS; HYDROPHOBICITY; IN VITRO STUDY; NONHUMAN; PARTICLE SIZE; PRIORITY JOURNAL; PROTEIN AGGREGATION; PROTEIN DENATURATION; PROTEIN GLYCOSYLATION; PROTEIN MODIFICATION; STRUCTURE ANALYSIS; ANIMAL; APOPTOSIS; BOVINE; CATARACT; CHEMICAL PHENOMENA; CHEMISTRY; DISEASE MODEL; DRUG DEVELOPMENT; GLYCOLYSIS; GLYCOSYLATION; HUMAN; LENS; LIGHT; METABOLISM; PATHOLOGY; PRESBYOPIA; RADIATION SCATTERING; SIGNAL TRANSDUCTION; SPECTROFLUOROMETRY; TEMPERATURE;

AGING; ALPHA-CRYSTALLINS; ANIMALS; APOPTOSIS; CATARACT; CATTLE; DIABETES MELLITUS; DISEASE MODELS, ANIMAL; DRUG DISCOVERY; GLYCOLYSIS; GLYCOSYLATION; GLYCOSYLATION END PRODUCTS, ADVANCED; HEAT-SHOCK PROTEINS; HUMANS; HYDROPHOBIC AND HYDROPHILIC INTERACTIONS; LENS, CRYSTALLINE; LIGHT; MOLECULAR CHAPERONES; NEURODEGENERATIVE DISEASES; PRESBYOPIA; PROTEIN BINDING; PYRUVALDEHYDE; SCATTERING, RADIATION; SIGNAL TRANSDUCTION; SPECTROMETRY, FLUORESCENCE; TEMPERATURE;

EID: 84947021692     PISSN: 09394451     EISSN: 14382199     Source Type: Journal    
DOI: 10.1007/s00726-015-2052-8     Document Type: Article

References (90)

1. Augusteyn RC, Koretz JF (1987) A possible structure for α-crystallin. FEBS Lett 222:1-5
2. Bartling B, Hofmann H-S, Sohst A, Hatzky Y, Somoza V, Silber R-E, Simm A (2011) Prognostic potential and tumor growth-inhibiting effect of plasma advanced glycation end products in non-small cell lung carcinoma. Mol Med 17:980
3. Bento CF, Marques F, Fernandes R, Pereira P (2010) Methylglyoxal alters the function and stability of critical components of the protein quality control. PloS One 5:e13007
4. Borkman RF (1984) Cataracts and photochemical damage in the lens. In: Ciba foundation symposium 106-human cataract formation. Wiley Online Library, pp 88-109
5. Borkman RF, Lerman S (1978) Fluorescence spectra of tryptophan residues in human and bovine lens proteins. Exp Eye Res 26:705-713
6. Borkman RF, Dalrymple A, Lerman S (1977) Ultraviolet action spectrum for fluorogen production in the ocular lens. Photochem Photobiol 26:129-132
7. Borkman R, Tassin J, Lerman S (1980) Fluorescence lifetimes of ocular lens chromophores. Photochem Photobiol 31:519-521
8. Borkman RF, Tassin JD, Lerman S (1981) Fluorescence lifetimes of chromophores in intact human lenses and lens protection. Exp Eye Res 32:313-322
9. Borkman RF, Knight G, Obi B (1996) The molecular chaperone α-crystallin inhibits UV-induced protein aggregation. Exp Eye Res 62:141-148
10. Boyle D, Takemoto L (1994) Characterization of the α-γ and α-β complex: evidence for an in vivo functional role of α-crystallin as a molecular chaperone. Exp Eye Res 58:9-16
11. Cherian M, Abraham E (1995a) Decreased molecular chaperone property of α-crystallins due to posttranslational modifications. Biochem Biophys Res Commun 208:675-679
12. Cherian M, Abraham EC (1995b) Diabetes affects alpha-crystallin chaperone function. Biochem Biophys Res Commun 212:184-189. doi: 10.1006/bbrc.1995.1954
13. Craig EA, Weissman JS, Horwich AL (1994) Heat shock proteins and molecular chaperones: mediators of protein conformation and turnover in the cell. Cell 78:365-372
14. Das KP, Surewicz WK (1995) On the substrate specificity of alpha-crystallin as a molecular chaperone. Biochem J 311:367-370
15. Delaye M, Tardieu A (1983) Short-range order of crystallin proteins accounts for eye lens transparency. Nature 302:415-417
16. Dillon J (1991) New trends in photobiology: the photophysics and photobiology of the eye. J Photochem Photobiol B Biol 10:23-40
17. Dillon J, Atherton SJ (1990) Time resolved spectroscopic studies on the intact human lens. Photochem Photobiol 51:465-468
18. Dillon J, Wang RH, Atherton SJ (1990) Photochemical and photophysical studies on human lens constituents. Photochem Photobiol 52:849-854
19. Ervin LA, Dillon J, Gaillard ER (2001) Photochemically modified α-crystallin: a model system for aging in the primate lens. Photochem Photobiol 73:685-691
20. Finley EL, Busman M, Dillon J, Crouch RK, Schey KL (1997) Identification of photooxidation sites in bovine α-crystallin. Photochem Photobiol 66:635-641
21. Finley EL, Dillon J, Crouch RK, Schey KL (1998) Identification of tryptophan oxidation products in bovine α-crystallin. Protein Sci 7:2391-2397
22. Foffi G, Savin G, Bucciarelli S, Dorsaz N, Thurston GM, Stradner A, Schurtenberger P (2014) Hard sphere-like glass transition in eye lens α-crystallin solutions. Proc Natl Acad Sci 111:16748-16753
23. Fort PE, Lampi KJ (2011) New focus on alpha-crystallins in retinal neurodegenerative diseases. Exp Eye Res 92:98-103
24. Gaillard ER, Zheng L, Merriam JC, Dillon J (2000) Age-related changes in the absorption characteristics of the primate lens. Invest Ophthalmol Vis Sci 41:1454-1459
25. Ganea E (2001) Chaperone-like activity of alpha-crystallin and other small heat shock proteins. Curr Protein Pept Sci 2:205-225
26. Gangadhariah MH, Wang B, Linetsky M, Henning C, Spanneberg R, Glomb MA, Nagaraj RH (2010) Hydroimidazolone modification of human αA-crystallin: effect on the chaperone function and protein refolding ability. Biochim Biophys Acta Mol Basis Dis 1802:432-441
27. Garland D, Russell P, Zigler JS Jr (1988) The oxidative modification of lens proteins. Oxygen radicals in biology and medicine. Springer, Berlin, pp 347-352
28. Groenen PJ, Merck KB, de Jong WW, Bloemendal H (1994) Structure and modifications of the junior chaperone alpha-crystallin. From lens transparency to molecular pathology. Eur J Biochem FEBS 225:1-19
29. Guo H (2008) Computational simulation studies of RPE65, alpha crystallin, and ABCR. Ph.D., Northern Illinois University
30. Hamann S, Métrailler S, Schorderet DF, Cottet S (2013) Analysis of the cytoprotective role of α-crystallins in cell survival and implication of the αA-crystallin C-terminal extension domain in preventing bax-induced apoptosis. PLoS One 8:e55372. doi: 10.1371/journal.pone.0055372
31. Heys KR, Friedrich MG, Truscott RJ (2007) Presbyopia and heat: changes associated with aging of the human lens suggest a functional role for the small heat shock protein, alpha-crystallin, in maintaining lens flexibility. Aging Cell 6:807-815. doi: 10.1111/j.1474-9726.2007.00342.x
32. Hoehenwarter W, Klose J, Jungblut PR (2006) Eye lens proteomics. Amino Acids 30:369-389
33. Hollar C, Parris N, Hsieh A, Cockley K (1995) Factors affecting the denaturation and aggregation of whey proteins in heated whey protein concentrate mixtures. J Dairy Sci 78:260-267
34. Hook DW, Harding JJ (1996) Alpha-crystallin acting as a molecular chaperone protects catalase against steroid-induced inactivation. FEBS Lett 382:281-284
35. Horwitz J (1992) Alpha-crystallin can function as a molecular chaperone. Proc Natl Acad Sci USA 89:10449-10453
36. Horwitz J (2003) Alpha-crystallin. Exp Eye Res 76:145-153
37. Jakob U, Gaestel M, Engel K, Buchner J (1993) Small heat shock proteins are molecular chaperones. J Biol Chem 268:1517-1520
38. Kannan R, Sreekumar PG, Hinton DR (2012) Novel roles for α-crystallins in retinal function and disease. Prog Retin Eye Res 31:576-604
39. Khanova HA et al (2005) Mechanism of chaperone-like activity. Suppression of thermal aggregation of βL-crystallin by α-crystallin. Biochemistry 44:15480-15487
40. Kielmas M, Kijewska M, Kluczyk A, Oficjalska J, Golebiewska B, Stefanowicz P, Szewczuk Z (2015) Comparison of modification sites in glycated crystallin in vitro and in vivo. Anal Bioanal Chem. doi: 10.1007/s00216-015-8487-7
41. Krishna Sharma K, Ortwerth B (1995) Effect of cross-linking on the chaperone-like function of alpha crystallin. Exp Eye Res 61:413-421
42. Kumar MS, Reddy PY, Kumar PA, Surolia I, Reddy GB (2004) Effect of dicarbonyl-induced browning on alpha-crystallin chaperone-like activity: physiological significance and caveats of in vitro aggregation assays. Biochem J 379:273-282. doi: 10.1042/bj20031633
43. Kumar PA, Kumar MS, Reddy GB (2007) Effect of glycation on alpha-crystallin structure and chaperone-like function. Biochem J 408:251-258. doi: 10.1042/bj20070989
44. Kurzel RB, Wolbarsht M, Yamanashi BS, Staton GW, Borkman RF (1973) Tryptophan excited states and cataracts in the human lens. Nature 241:132-133
45. Lakowicz J, Geddes C (1991) Topics in fluorescence spectrscopy. Plenum Press, New York
46. Lee J, Robinson GW (1985) Electron hydration dynamics using the 2-anilinonaphthalene precursor. J Am Chem Soc 107:6153-6156. doi: 10.1021/ja00308a001
47. Lee JS et al (2012) Expression of alpha B-crystallin overrides the anti-apoptotic activity of XIAP. Neurooncology 14:1332-1345. doi: 10.1093/neuonc/nos247
48. Lerman S, Borkman R (1978) Photochemistry and lens aging. Interdiscip Top Gerontol 13:154
49. Liang JJ, Liu BF (2006) Fluorescence resonance energy transfer study of subunit exchange in human lens crystallins and congenital cataract crystallin mutants. Protein Sci 15:1619-1627
50. Lindner AB, Demarez A (2009) Protein aggregation as a paradigm of aging. Biochi Biophys Acta 1790:980-996
51. Mandal K, Dillon J, Gaillard ER (2000) Heat and concentration effects on the small heat shock protein, alpha-crystallin. Photochem Photobiol 71:470-475
52. McDermott M, Chiesa R, Roberts JE, Dillon J (1991) Photooxidation of specific residues in alpha-crystallin polypeptides. Biochemistry 30:8653-8660
53. Meredith SC (2006) Protein denaturation and aggregation. Ann N Y Acad Sci 1066:181-221
54. Monnier VM (1989) Toward a Maillard reaction theory of aging. Prog Clin Biol Res 304:1-22
55. Monnier VM (1990) Nonenzymatic glycosylation, the Maillard reaction and the aging process. J Gerontol 45:B105-B111
56. Monnier VM, Cerami A (1982) Non-enzymatic glycosylation and browning of proteins in diabetes. Clin Endocrinol Metab 11:431-452
57. Monnier VM, Miyata S, Nagaraj RH, Sell DR (1993) Relevance of the early and advanced Maillard reaction in diabetic neuropathy. Diabet Med 10(Suppl 2):103s-106s
58. Monnier VM, Sell DR, Dai Z, Nemet I, Collard F, Zhang J (2008) The role of the amadori product in the complications of diabetes. Ann N Y Acad Sci 1126:81-88. doi: 10.1196/annals.1433.052
59. Moore JW (1961) Kinetics and mechanism. Wiley, New York
60. Mukhopadhyay S, Kar M, Das KP (2010) Effect of methylglyoxal modification of human alpha-crystallin on the structure, stability and chaperone function. Protein J 29:551-556. doi: 10.1007/s10930-010-9289-6
61. Nagaraj RH, Linetsky M, Stitt AW (2012) The pathogenic role of Maillard reaction in the aging eye. Amino Acids 42:1205-1220. doi: 10.1007/s00726-010-0778-x
62. Nahomi RB, Oya-Ito T, Nagaraj RH (2013) The combined effect of acetylation and glycation on the chaperone and anti-apoptotic functions of human alpha-crystallin. Biochim Biophys Acta 1832:195-203. doi: 10.1016/j.bbadis.2012.08.015
63. Nishio I, Weiss JN, Tanaka T, Clark JI, Giblin FJ, Reddy VN, Benedek GB (1984) In vivo observation of lens protein diffusivity in normal and X-irradiated rabbit lenses. Exp Eye Res 39:61-68
64. Njoroge FG, Monnier VM (1989) The chemistry of the Maillard reaction under physiological conditions: a review. Prog Clin Biol Res 304:85-107
65. Pasupuleti N, Matsuyama S, Voss O, Doseff AI, Song K, Danielpour D, Nagaraj RH (2010) The anti-apoptotic function of human [alpha]A-crystallin is directly related to its chaperone activity. Cell Death Dis 1:e31
66. Petta V, Pharmakakis N, Papatheodorou GN, Yannopoulos SN (2008) Dynamic light scattering study on phase separation of a protein-water mixture: application on cold cataract development in the ocular lens. Phys Rev E Stati Nonlin Soft Matter Phys 77:061904
67. Raman B, Rao CM (1994) Chaperone-like activity and quaternary structure of alpha-crystallin. J Biol Chem 269:27264-27268
68. Raman B, Ramakrishna T, Mohan Rao C (1995) Temperature dependent chaperone-like activity of alpha-crystallin. FEBS Lett 365:133-136
69. Rao PV, Horwitz J, Zigler J (1993) α-Crystallin, a molecular chaperone, forms a stable complex with carbonic anhydrase upon heat denaturation. Biochem Biophys Res Commun 190:786-793
70. Ray S, Dutta S, Halder J, Ray M (1994) Inhibition of electron flow through complex I of the mitochondrial respiratory chain of Ehrlich ascites carcinoma cells by methylglyoxal. Biochem J 303:69-72
71. Reddy VS, Reddy GB (2015) Emerging role for alphaB-crystallin as a therapeutic agent: pros and cons. Curr Mol Med 15:47-61
72. Regini J, Grossmann J, Burgio M, Malik N, Koretz J, Hodson S, Elliott G (2004) Structural changes in α-crystallin and whole eye lens during heating, observed by low-angle X-ray diffraction. J Mol Biol 336:1185-1194
73. Rekas A et al (2004) Interaction of the molecular chaperone αB-crystallin with α-synuclein: effects on amyloid fibril formation and chaperone activity. J Mol Biol 340:1167-1183
74. Roberts JE, Kinley JS, Young AR, Jenkins G, Atherton SJ, Dillon J (1991) In vivo and photophysical studies on photooxidative damage to lens proteins and their protection by radioprotectors. Photochem Photobiol 53:33-38
75. Rosca MG et al (2005) Glycation of mitochondrial proteins from diabetic rat kidney is associated with excess superoxide formation. Am J Physiol Renal Physiol 289:F420-F430
76. Simm A, Muller B, Nass N, Hofmann B, Bushnaq H, Silber RE, Bartling B (2015) Protein glycation - between tissue aging and protection. Exp Gerontol 68:71-75. doi: 10.1016/j.exger.2014.12.013
77. Sreelakshmi Y, Santhoshkumar P, Bhattacharyya J, Sharma KK (2004) αA-Crystallin interacting regions in the small heat shock protein, αB-crystallin. Biochemistry 43:15785-15795
78. Srinivas V, Raman B, Rao KS, Ramakrishna T, Rao CM (2003) Structural perturbation and enhancement of the chaperone-like activity of α-crystallin by arginine hydrochloride. Protein Sci 12:1262-1270
79. Srinivasan AN, Nagineni CN, Bhat SP (1992) Alpha A-crystallin is expressed in non-ocular tissues. J Biol Chem 267:23337-23341
80. Stevens VJ, Rouzer CA, Monnier VM, Cerami A (1978) Diabetic cataract formation: potential role of glycosylation of lens crystallins. Proc Natl Acad Sci USA 75:2918-2922
81. Strenk SA, Strenk LM, Koretz JF (2005) The mechanism of presbyopia. Progr Retin Eye Res 24:379-393. doi: 10.1016/j.preteyeres.2004.11.001
82. Takemoto L, Boyle D (1994) Molecular chaperone properties of the high molecular weight aggregate from aged lens. Curr Eye Res 13:35-44
83. Tanaka T, Ishimoto C (1977) In vivo observation of protein diffusivity in rabbit lenses. Invest Ophthalmol Vis Sci 16:135-140
84. Tardieu A (1998) Alpha-crystallin quaternary structure and interactive properties control eye lens transparency. Int J Biol Macromol 22:211-217
85. Turk Z, Nemet I, Varga-Defteardarovic L, Car N (2006) Elevated level of methylglyoxal during diabetic ketoacidosis and its recovery phase. Diabetes Metab 32:176-180
86. Van Kleef FS, De Jong WW, Hoenders HJ (1975) Stepwise degradations and deamidation of the eye lens protein alpha-crystallin in ageing. Nature 258:264-266
87. Van Montfort R, Slingsby C, Vierling E (2002) Structure and function of the small heat shock protein/alpha-crystallin family of molecular chaperones. Adv Protein Chem 59:105-156
88. Vanhoudt J, Abgar S, Aerts T, Clauwaert J (2000) Native quaternary structure of bovine alpha-crystallin. Biochemistry 39:4483-4492
89. Wang K, Spector A (1995) Alpha-crystallin can act as a chaperone under conditions of oxidative stress. Invest Ophthalmol Vis Sci 36:311-321
90. Wilker SC, Chellan P, Arnold BM, Nagaraj RH (2001) Chromatographic quantification of argpyrimidine, a methylglyoxal-derived product in tissue proteins: comparison with pentosidine. Anal Biochem 290:353-358. doi: 10.1006/abio.2001.4992