The combined effect of acetylation and glycation on the chaperone and anti-apoptotic functions of human α-crystallin

Biochimica et Biophysica Acta - Molecular Basis of Disease

Volumn 1832, Issue 1, 2013, Pages 195-203

  Nahomi, Rooban B ^a   Oya Ito, Tomoko ^b   Nagaraj, Ram H ^a  

^a CASE WESTERN RESERVE UNIVERSITY SCHOOL OF MEDICINE   (United States)

^b KYOTO PREFECTURAL UNIVERSITY OF MEDICINE   (Japan)

Author keywords

Crystallin; Acetylation; Apoptosis; Chaperone; Glycation

Indexed keywords

ACETIC ANHYDRIDE; ADVANCED GLYCATION END PRODUCT; ALPHA B CYRSTALLIN; ALPHA CRYSTALLIN; ASCORBIC ACID; CASPASE 3; CRYSTALLIN; IMIDAZOLE DERIVATIVE; LYSINE; LYSINE DERIVATIVE; METHYLGLYOXAL; UNCLASSIFIED DRUG;

ACETYLATION; APOPTOSIS; ARTICLE; CONTROLLED STUDY; CROSS LINKING; ENZYME ACTIVITY; GLYCATION; HUMAN; HUMAN TISSUE; HYPERTHERMIA; IMMUNOPRECIPITATION; LENS; PRIORITY JOURNAL; PROTEIN FUNCTION; PROTEIN SYNTHESIS;

ACETYLATION; ALPHA-CRYSTALLIN A CHAIN; ALPHA-CRYSTALLIN B CHAIN; AMINO ACID MOTIFS; APOPTOSIS; GLYCOSYLATION; HUMANS; LENS, CRYSTALLINE; MOLECULAR CHAPERONES;

EID: 84868567139     PISSN: 09254439     EISSN: 1879260X     Source Type: Journal    
DOI: 10.1016/j.bbadis.2012.08.015     Document Type: Article

References (50)

1. Bloemendal H., de Jong W., Jaenicke R., Lubsen N.H., Slingsby C., Tardieu A. Ageing and vision: structure, stability and function of lens crystallins. Prog. Biophys. Mol. Biol. 2004, 86:407-485.
2. Andley U.P. The lens epithelium: focus on the expression and function of the alpha-crystallin chaperones. Int. J. Biochem. Cell Biol. 2008, 40:317-323.
3. Horwitz J. Alpha-crystallin can function as a molecular chaperone. Proc. Natl. Acad. Sci. U. S. A. 1992, 89:10449-10453.
4. Srinivasan A.N., Nagineni C.N., Bhat S.P. Alpha A-crystallin is expressed in non-ocular tissues. J. Biol. Chem. 1992, 267:23337-23341.
5. Bhat S.P., Nagineni C.N. Alpha B subunit of lens-specific protein alpha-crystallin is present in other ocular and non-ocular tissues. Biochem. Biophys. Res. Commun. 1989, 158:319-325.
6. Dubin R.A., Wawrousek E.F., Piatigorsky J. Expression of the murine alpha B-crystallin gene is not restricted to the lens. Mol. Cell. Biol. 1989, 9:1083-1091.
7. Horwitz J. Alpha-crystallin. Exp. Eye Res. 2003, 76:145-153.
8. Andley U.P. Crystallins in the eye: function and pathology. Prog. Retin. Eye Res. 2007, 26:78-98.
9. Pasupuleti N., Matsuyama S., Voss O., Doseff A.I., Song K., Danielpour D., Nagaraj R.H. The anti-apoptotic function of human alphaA-crystallin is directly related to its chaperone activity. Cell Death Dis. 2010, 1:e31.
10. Andley U.P. Effects of alpha-crystallin on lens cell function and cataract pathology. Curr. Mol. Med. 2009, 9:887-892.
11. Mao Y.W., Liu J.P., Xiang H., Li D.W. Human alphaA- and alphaB-crystallins bind to Bax and Bcl-X(S) to sequester their translocation during staurosporine-induced apoptosis. Cell Death Differ. 2004, 11:512-526.
12. Liu J.P., Schlosser R., Ma W.Y., Dong Z., Feng H., Lui L., Huang X.Q., Liu Y., Li D.W. Human alphaA- and alphaB-crystallins prevent UVA-induced apoptosis through regulation of PKCalpha, RAF/MEK/ERK and AKT signaling pathways. Exp. Eye Res. 2004, 79:393-403.
13. Sharma K.K., Santhoshkumar P. Lens aging: effects of crystallins. Biochim. Biophys. Acta 2009, 1790:1095-1108.
14. Harrington V., Srivastava O.P., Kirk M. Proteomic analysis of water insoluble proteins from normal and cataractous human lenses. Mol. Vis. 2007, 13:1680-1694.
15. Wilmarth P.A., Tanner S., Dasari S., Nagalla S.R., Riviere M.A., Bafna V., Pevzner P.A., David L.L. Age-related changes in human crystallins determined from comparative analysis of post-translational modifications in young and aged lens: does deamidation contribute to crystallin insolubility?. J. Proteome Res. 2006, 5:2554-2566.
16. Hains P.G., Truscott R.J. Post-translational modifications in the nuclear region of young, aged, and cataract human lenses. J. Proteome Res. 2007, 6:3935-3943.
17. Singh R., Barden A., Mori T., Beilin L. Advanced glycation end-products: a review. Diabetologia 2001, 44:129-146.
18. Nagaraj R.H., Shipanova I.N., Faust F.M. Protein cross-linking by the Maillard reaction. Isolation, characterization, and in vivo detection of a lysine-lysine cross-link derived from methylglyoxal. J. Biol. Chem. 1996, 271:19338-19345.
19. Wilmarth P.A., Taube J.R., Riviere M.A., Duncan M.K., David L.L. Proteomic and sequence analysis of chicken lens crystallin reveals alternate splicing and translational forms of bB2 and bA2 crystallins. Invest. Ophthalmol. Vis. Sci. 2004, 45:2705-2715.
20. Pal J.K., Bera S.K., Ghosh S.K. Acetylation of alpha-crystallin with N-acetylimidazole and its influence upon the native aggregate and subunit reassembly. Curr. Eye Res. 1999, 19:358-367.
21. Lin P.P., Barry R.C., Smith D.L., Smith J.B. In vivo acetylation identified at lysine 70 of human lens alphaA-crystallin. Protein Sci. 1998, 7:1451-1457.
22. Lapko V.N., Smith D.L., Smith J.B. In vivo carbamylation and acetylation of water-soluble human lens alphaB-crystallin lysine 92. Protein Sci. 2001, 10:1130-1136.
23. Shi Q., Yan H., Li M.Y., Harding J.J. Effect of a combination of carnosine and aspirin eye drops on streptozotocin - induced diabetic cataract in rats. Mol. Vis. 2009, 15:2129-2138.
24. Hasan A., Smith J.B., Qin W., Smith D.L. The reaction of bovine lens alpha A-crystallin with aspirin. Exp. Eye Res. 1993, 57:29-35.
25. Nagaraj R.H., Nahomi R.B., Shanthakumar S., Linetsky M., Padmanabha S., Pasupuleti N., Wang B., Santhoshkumar P., Panda A.K., Biswas A. Acetylation of alphaA-crystallin in the human lens: effects on structure and chaperone function. Biochim. Biophys. Acta 2012, 1822:120-129.
26. Ahmed N. Advanced glycation endproducts-role in pathology of diabetic complications. Diabetes Res. Clin. Pract. 2005, 67:3-21.
27. Beswick H.T., Harding J.J. Conformational changes induced in lens alpha- and gamma-crystallins by modification with glucose 6-phosphate. Implications for cataract. Biochem. J. 1987, 246:761-769.
28. Ahmed M.U., Brinkmann Frye E., Degenhardt T.P., Thorpe S.R., Baynes J.W. N-epsilon-(carboxyethyl)lysine, a product of the chemical modification of proteins by methylglyoxal, increases with age in human lens proteins. Biochem. J. 1997, 324(Pt 2):565-570.
29. Hains P.G., Truscott R.J. Proteomic analysis of the oxidation of cysteine residues in human age-related nuclear cataract lenses. Biochim. Biophys. Acta 2008, 1784:1959-1964.
30. Derham B.K., Harding J.J. Effects of modifications of alpha-crystallin on its chaperone and other properties. Biochem. J. 2002, 364:711-717.
31. Kumar M.S., Reddy P.Y., Kumar P.A., Surolia I., Reddy G.B. Effect of dicarbonyl-induced browning on alpha-crystallin chaperone-like activity: physiological significance and caveats of in vitro aggregation assays. Biochem. J. 2004, 379:273-282.
32. Ortwerth B.J., Feather M.S., Olesen P.R. The precipitation and cross-linking of lens crystallins by ascorbic acid. Exp. Eye Res. 1988, 47:155-168.
33. Fan X., Reneker L.W., Obrenovich M.E., Strauch C., Cheng R., Jarvis S.M., Ortwerth B.J., Monnier V.M. Vitamin C mediates chemical aging of lens crystallins by the Maillard reaction in a humanized mouse model. Proc. Natl. Acad. Sci. U. S. A. 2006, 103:16912-16917.
34. Fan X., Monnier V.M. Inhibition of crystallin ascorbylation by nucleophilic compounds in the hSVCT2 mouse model of lenticular aging. Invest. Ophthalmol. Vis. Sci. 2008, 49:4945-4952.
35. Nagaraj R.H., Linetsky M., Stitt A.W. The pathogenic role of Maillard reaction in the aging eye. Amino Acids 2012, 42:1205-1220.
36. Pirie A. Color and solubility of the proteins of human cataracts. Investig. Ophthalmol. 1968, 7:634-650.
37. Puttaiah S., Biswas A., Staniszewska M., Nagaraj R.H. Methylglyoxal inhibits glycation-mediated loss in chaperone function and synthesis of pentosidine in alpha-crystallin. Exp. Eye Res. 2007, 84:914-921.
38. Grandhee S.K., Monnier V.M. Mechanism of formation of the Maillard protein cross-link pentosidine. Glucose, fructose, and ascorbate as pentosidine precursors. J. Biol. Chem. 1991, 266:11649-11653.
39. Nagaraj R.H., Biswas A., Miller A., Oya-Ito T., Bhat M. The other side of the Maillard reaction. Ann. N. Y. Acad. Sci. 2008, 1126:107-112.
40. Swamy M.S., Abraham E.C. Inhibition of lens crystallin glycation and high molecular weight aggregate formation by aspirin in vitro and in vivo. Investig. Ophthalmol. Vis. Sci. 1989, 30:1120-1126.
41. Stevens A. The effectiveness of putative anti-cataract agents in the prevention of protein glycation. J. Am. Optom. Assoc. 1995, 66:744-749.
42. Henning C., Smuda M., Girndt M., Ulrich C., Glomb M.A. Molecular basis of maillard amide-advanced glycation end product (AGE) formation in vivo. J. Biol. Chem. 2011, 286:44350-44356.
43. Nagaraj R.H., Sell D.R., Prabhakaram M., Ortwerth B.J., Monnier V.M. High correlation between pentosidine protein crosslinks and pigmentation implicates ascorbate oxidation in human lens senescence and cataractogenesis. Proc. Natl. Acad. Sci. U. S. A. 1991, 88:10257-10261.
44. Linetsky M., Shipova E., Cheng R., Ortwerth B.J. Glycation by ascorbic acid oxidation products leads to the aggregation of lens proteins. Biochim. Biophys. Acta 2008, 1782:22-34.
45. Ortwerth B.J., Speaker J.A., Prabhakaram M., Lopez M.G., Li E.Y., Feather M.S. Ascorbic acid glycation: the reaction of L-threose in lens tissue. Exp. Eye Res. 1994, 58:665-674.
46. Cheng R., Lin B., Lee K.W., Ortwerth B.J. Similarity of the yellow chromophores isolated from human cataracts with those from ascorbic acid-modified calf lens proteins: evidence for ascorbic acid glycation during cataract formation. Biochim. Biophys. Acta 2001, 1537:14-26.
47. Mailankot M., Padmanabha S., Pasupuleti N., Major D., Howell S., Nagaraj R.H. Glyoxalase I activity and immunoreactivity in the aging human lens. Biogerontology 2009, 10:711-720.
48. Nagaraj R.H., Oya-Ito T., Padayatti P.S., Kumar R., Mehta S., West K., Levison B., Sun J., Crabb J.W., Padival A.K. Enhancement of chaperone function of alpha-crystallin by methylglyoxal modification. Biochemistry 2003, 42:10746-10755.
49. Biswas A., Miller A., Oya-Ito T., Santhoshkumar P., Bhat M., Nagaraj R.H. Effect of site-directed mutagenesis of methylglyoxal-modifiable arginine residues on the structure and chaperone function of human alphaA-crystallin. Biochemistry 2006, 45:4569-4577.
50. Nagaraj R.H., Panda A.K., Shanthakumar S., Santhoshkumar P., Pasupuleti N., Wang B., Biswas A. Hydroimidazolone modification of the conserved Arg12 in small heat shock proteins: studies on the structure and chaperone function using mutant mimics. PLoS One 2012, 7:e30257.