Effect of site-directed mutagenesis of methylglyoxal-modifiable arginine residues on the structure and chaperone function of human αA-crystallin

Biochemistry

Volumn 45, Issue 14, 2006, Pages 4569-4577

  Biswas, Ashis ^a   Miller, Antonia ^a   Oya Ito, Tomoko ^a   Santhoshkumar, Puttur ^c   Bhat, Manjunatha ^b   Nagaraj, Ram H ^a  

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

^b LERNER RESEARCH INSTITUTE   (United States)

^c UNIVERSITY OF MISSOURI   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

AGGLOMERATION; AMINO ACIDS; BIOASSAY; CHEMICAL MODIFICATION; CRYSTALLINE MATERIALS; METABOLISM;

ARGININE RESIDUES; CATARACT FORMATION; CHAPERONE FUNCTION; MALATE DEHYDROGENASE;

MUTAGENESIS;

ALPHA CRYSTALLIN; AMINO ACID; ARGININE; AROMATIC AMINO ACID; CHAPERONE; CITRATE SYNTHASE; GUANIDINE HYDROCHLORIDE; INSULIN; MALATE DEHYDROGENASE; METHYLGLYOXAL; MUTANT PROTEIN; PYRIMIDINE;

AGING; AMINO ACID SUBSTITUTION; ARTICLE; CATARACTOGENESIS; CIRCULAR DICHROISM; CONTROLLED STUDY; HUMAN; HYDROPHOBICITY; LENS; PRIORITY JOURNAL; PROTEIN AGGREGATION; PROTEIN FOLDING; PROTEIN FUNCTION; PROTEIN MODIFICATION; PROTEIN STRUCTURE; SITE DIRECTED MUTAGENESIS;

ALPHA-CRYSTALLIN A CHAIN; ARGININE; CARBONIC ANHYDRASES; CIRCULAR DICHROISM; HUMANS; MOLECULAR CHAPERONES; MUTAGENESIS, SITE-DIRECTED; PROTEIN STRUCTURE, SECONDARY; PYRUVALDEHYDE; SPECTROMETRY, FLUORESCENCE;

EID: 33645679798     PISSN: 00062960     EISSN: None     Source Type: Journal    
DOI: 10.1021/bi052574s     Document Type: Article

References (59)

1. Spector, A., Li, L. K., Augusteyn, R. C., Schneider, A., and Freund, T. (1971) α-Crystallin. The isolation and characterization of distinct macromolecular fractions, Biochem. J. 124, 337-343.
2. Bloemendal, H. (1982) Lens proteins, CRC Crit. Rev. Biochem. 12, 1-38.
3. de Jong, W. W., Caspers, G. J., and Leunissen, J. A. (1998) Genealogy of the alpha-crystallin-small heat-shock protein superfamily, Int. J. Biol. Macromol. 22, 151-162.
4. de Jong, W. W., Leunissen, J. A., and Voorter, C. E. (1993) Evolution of the alpha-crystallin/small heat-shock protein family, Mol. Biol. Evol. 10, 103-126.
5. Kapphahn, R. J., Ethen, C. M., Peters, E. A., Higgins, L., and Ferrington, D. A. (2003) Modified alpha A crystallin in the retina: altered expression and truncation with aging, Biochemistry 42, 15310-15325.
6. Iwaki, T., Kume-Iwaki, A., and Goldman, J. E. (1990) Cellular distribution of alpha B-crystallin in non-lenticular tissues, J. Histochem. Cytochem. 38, 31-39.
7. van Boekel, M. A., Hoogakker, S. E., Harding, J. J., and de Jong, W. W. (1996) The influence of some post-translational modifications on the chaperone-like activity of alpha-crystallin, Ophthalmic Res. 28 (Suppl. 1), 32-38.
8. Horwitz, J. (1992) Alpha-crystallin can function as a molecular chaperone, Proc. Natl. Acad. Sci. U.S.A. 89, 10449-10453.
9. Horwitz, J. (2003) Alpha-crystallin, Exp. Eye Res. 76, 145-153.
10. Bloemendal, H., de Jong, W., Jaenicke, R., Lubsen, N. H., Slingsby, C., and Tardieu, A. (2004) Ageing and vision: structure, stability and function of lens crystalline, Prog. Biophys. Mol. Biol. 86, 407-485.
11. Fujii, N., Hiroki, K., Matsumoto, S., Masuda, K., Inoue, M., Tanaka, Y., Awakura, M., and Akaboshi, M. (2001) Correlation between the loss of the chaperone-like activity and the oxidation, isomerization and racemization of gamma-irradiated alpha-crystallin, Photochem. Photobiol. 74, 477-482.
12. Ito, H., Kamei, K., Iwamoto, I., Inaguma, Y., Nohara, D., and Kato, K. (2001) Phosphorylation-induced change of the oligomerization state of alpha B-crystallin, J. Biol. Chem. 276, 5346-5352.
13. Gupta, R., and Srivastava, O. P. (2004) Deamidation affects structural and functional properties of human alphaA-crystallin and its oligomerization with alphaB-crystallin, J. Biol. Chem. 279, 44258-44269.
14. Derham, B. K., and Harding, J. J. (1999) Alpha-crystallin as a molecular chaperone, Prog. Retinal Eye Res. 18, 463-509.
15. Cherian, M., and Abraham, E. C. (1995) Decreased molecular chaperone property of alpha-crystallins due to posttranslational modifications, Biochem. Biophys. Res. Commun. 208, 675-679.
16. Baynes, J. W. (2001) The role of AGEs in aging: causation or correlation, Exp. Gerontol. 36, 1527-1537.
17. Nagaraj, R. H., Sell, D. R., Prabhakaram, M., Ortwerth, B. J., and Monnier, V. M. (1991) High correlation between pentosidine protein crosslinks and pigmentation implicates ascorbate oxidation in human lens senescence and cataractogenesis, Proc. Natl. Acad. Sci. U.S.A. 88, 10257-10261.
18. Wilker, S. C., Chellan, P., Arnold, B. M., and Nagaraj, R. H. (2001) Chromatographic quantification of argpyrimidine, a methylglyoxal-derived product in tissue proteins: comparison with pentosidine, Anal. Biochem. 290, 353-358.
19. Lyons, T. J., Silvestri, G., Dunn, J. A., Dyer, D. G., and Baynes, J. W. (1991) Role of glycation in modification of lens crystalline in diabetic and nondiabetic senile cataracts, Diabetes 40, 1010-1015.
20. Wells-Knecht, K. J., Brinkmann, E., Wells-Knecht, M. C., Litchfield, J. E., Ahmed, M. U., Reddy, S., Zyzak, D. V., Thorpe, S. R., and Baynes, J. W. (1996) New biomarkers of Maillard reaction damage to proteins, Nephrol. Dial. Transplant. 11 (Suppl. 5), 41-47.
21. Thornalley, P. J. (1993) The glyoxalase system in health and disease, Mol. Aspects Med. 14, 287-371.
22. Haik, G. M., Jr., Lo, T. W., and Thornalley, P. J. (1994) Methylglyoxal concentration and glyoxalase activities in the human lens, Exp. Eye Res. 59, 497-500.
23. Lo, T. W., Westwood, M. E., McLellan, A. C., Selwood, T., and Thornalley, P. J. (1994) Binding and modification of proteins by methylglyoxal under physiological conditions. A kinetic and mechanistic study with N alpha-acetylarginine, N alpha-acetylcysteine, and N alpha-acetyllysine, and bovine serum albumin, J. Biol. Chem. 269, 32299-32305.
24. Ahmed, N., Thornalley, P. J., Dawczynski, J., Franke, S., Strobel, J., Stein, G., and Haik, G. M. (2003) Methylglyoxal-derived hydroimidazolone advanced glycation end-products of human lens proteins, Invest. Ophthalmol. Visual Sci. 44, 5287-5292.
25. Thornalley, P. J., Battah, S., Ahmed, N., Karachalias, N., Agalou, S., Babaei-Jadidi, R., and Dawnay, A. (2003) Quantitative screening of advanced glycation endproducts in cellular and extracellular proteins by tandem mass spectrometry, Biochem. J. 375, 581-592.
26. Shipanova, I. N., Glomb, M. A., and Nagaraj, R. H. (1997) Protein modification by methylglyoxal: chemical nature and synthetic mechanism of a major fluorescent adduct, Arch. Biochem. Biophys. 344, 29-36.
27. Nagaraj, R. H., and Sady, C. (1996) The presence of a glucose-derived Maillard reaction product in the human lens, FEBS Lett. 382, 234-238.
28. Chellan, P., and Nagaraj, R. H. (1999) Protein crosslinking by the Maillard reaction: dicarbonyl-derived imidazolium crosslinks in aging and diabetes, Arch. Biochem. Biophys. 368, 98-104.
29. Ahmed, M. U., Brinkmann Frye, E., Degenhardt, T. P., Thorpe, S. R., and Baynes, J. W. (1997) N-epsilon-(carboxyethyl)lysine, a product of the chemical modification of proteins by methylglyoxal, increases with age in human lens proteins, Biochem. J. 324 (Part 2), 565-570.
30. Biemel, K. M., Friedl, D. A., and Lederer, M. O. (2002) Identification and quantification of major Maillard cross-links in human serum albumin and lens protein. Evidence for glucosepane as the dominant compound, J. Biol. Chem. 277, 24907-24915.
31. Padayatti, P. S., Ng, A. S., Uchida, K., Glomb, M. A., and Nagaraj, R. H. (2001) Argpyrimidine, a blue fluorophore in human lens proteins: high levels in brunescent cataractous lenses, Invest. Ophthalmol. Visual Sci. 42, 1299-1304.
32. Nagaraj, R. H., Oya-Ito, T., Padayatti, P. S., Kumar, R., Mehta, S., West, K., Levison, B., Sun, J., Crabb, J. W., and Padival, A. K. (2003) Enhancement of chaperone function of alpha-crystallin by methylglyoxal modification, Biochemistry 42, 10746-10755.
33. Kumar, L. V., Ramakrishna, T., and Rao, C. M. (1999) Structural and functional consequences of the mutation of a conserved arginine residue in alphaA and alphaB crystalline, J. Biol. Chem. 274, 24137-24141.
34. Sreelakshmi, Y., and Sharma, K. K. (2005) Recognition sequence 2 (residues 60-71) plays a role in oligomerization and exchange dynamics of alphaB-crystallin, Biochemistry 44, 12245-12252.
35. Provencher, S. W., and Glockner, J. (1981) Estimation of globular protein secondary structure from circular dichroism, Biochemistry 20, 33-37.
36. Bhattacharyya, J., and Das, K. P. (1998) Alpha-crystallin does not require temperature activation for its chaperone-like activity, Biochem. Mol. Biol. Int. 46, 249-258.
37. Santhoshkumar, P., and Sharma, K. K. (2001) Phe71 is essential for chaperone-like function in alpha A-crystallin, J. Biol. Chem. 276, 47094-47099.
38. Biswas, A., and Das, K. P. (2004) Role of ATP on the interaction of alpha-crystallin with its substrates and its implications for the molecular chaperone function, J. Biol. Chem. 279, 42648-42657.
39. Kumar, M. S., Reddy, P. Y., Kumar, P. A., Surolia, I., and Reddy, G. B. (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.
40. Pasta, S. Y., Raman, B., Ramakrishna, T., and Rao, Ch. M. (2003) Role of the conserved SRLFDQFFG region of alpha-crystallin, a small heat shock protein. Effect on oligomeric size, subunit exchange, and chaperone-like activity, J. Biol. Chem. 278, 51159-51166.
41. Wyatt, P. J. (1993) Light scattering and the absolute characterization of macromolecules, Anal. Chim. Acta 272, 1-40.
42. Pasta, S. Y., Raman, B., Ramakrishna, T., and Rao, Ch. M. (2004) The IXI/V motif in the C-terminal extension of alpha-crystallins: alternative interactions and oligomeric assemblies, Mol. Vision 10, 655-662.
43. Liao, J. H., Lee, J. S., and Chiou, S. H. (2002) Distinct roles of alphaA- and alphaB-crystallins under thermal and UV stresses, Biochem. Biophys. Res. Commun. 295, 854-861.
44. Bera, S., Thampi, P., Cho, W. J., and Abraham, E. C. (2002) A positive charge preservation at position 116 of alpha A-crystallin is critical for its structural and functional integrity, Biochemistry 41, 12421-12426.
45. Bova, M. P., Yaron, O., Huang, Q., Ding, L., Haley, D. A., Stewart, P. L., and Horwitz, J. (1999) Mutation R120G in alphaB-crystallin, which is linked to a desmin-related myopathy, results in an irregular structure and defective chaperone-like function, Proc. Natl. Acad. Sci. U.S.A. 96, 6137-6142.
46. Sun, T. X., Das, B. K., and Liang, J. J. (1997) Conformational and functional differences between recombinant human lens alphaA- and alphaB-crystallin, J. Biol. Chem. 272, 6220-6225.
47. Reddy, G. B., Das, K. P., Petrash, J. M., and Surewicz, W. K. (2000) Temperature-dependent chaperone activity and structural properties of human alphaA- and alphaB-crystallins, J. Biol. Chem. 275, 4565-4570.
48. Das, K. P., and Surewicz, W. K. (1995) Temperature-induced exposure of hydrophobic surfaces and its effect on the chaperone activity of alpha-crystallin, FEBS Lett. 369, 321-325.
49. Saha, S., and Das, K. P. (2004) Relationship between chaperone activity and oligomeric size of recombinant human alphaA- and alphaB-crystallin: a tryptic digestion study, Proteins 57, 610-617.
50. Raman, B., Ramakrishna, T., and Rao, C. M. (1995) Temperature-dependent chaperone-like activity of alpha-crystallin, FEBS Lett. 365, 133-136.
51. Bhattacharyya, J., Srinivas, V., and Sharma, K. K. (2002) Evaluation of hydrophobicity versus chaperonelike activity of bovine alphaA- and alphaB-crystallin, J. Protein Chem. 21, 65-71.
52. Kumar, M. S., Kapoor, M., Sinha, S., and Reddy, G. B. (2005) Insights into hydrophobicity and the chaperone-like function of alphaA- and alphaB-crystallins: an isothermal titration calorimetric study, J. Biol. Chem. 280, 21726-21730.
53. McClure, W. O., and Edelman, G. M. (1966) Fluorescent probes for conformational states of proteins. I. Mechanism of fluorescence of 2-p-toluidinylnaphthalene-6-sulfonate, a hydrophobic probe, Biochemistry 5, 1908-1919.
54. Shroff, N. P., Bera, S., Cherian-Shaw, M., and Abraham, E. C. (2001) Substituted hydrophobic and hydrophilic residues at methionine-68 influence the chaperone-like function of alphaB-crystallin, Mol. Cell. Biochem. 220, 127-133.
55. Rawat, U., and Rao, M. (1998) Interactions of chaperone alpha-crystallin with the molten globule state of xylose reductase. Implications for reconstitution of the active enzyme, J. Biol. Chem. 273, 9415-9423.
56. Wang, K., and Spector, A. (1994) The chaperone activity of bovine alpha crystallin. Interaction with other lens crystalline in native and denatured states, J. Biol. Chem. 269, 13601-13608.
57. Wang, K., and Spector, A. (2000) Alpha-crystallin prevents irreversible protein denaturation and acts cooperatively with other heat-shock proteins to renature the stabilized partially denatured protein in an ATP-dependent manner, Eur. J. Biochem. 267, 4705-4712.
58. Muchowski, P. J., and Clark, J. I. (1998) ATP-enhanced molecular chaperone functions of the small heat shock protein human alphaB crystallin, Proc. Natl. Acad. Sci. U.S.A. 95, 1004-1009.
59. Clark, J. I., Estrada, M. R., and Ghosh, J. G. (2004) Interaction sites in human alphaB-crystallin mediate multiple functions, Invest. Ophthalmol. Visual Sci. 45, E-abstract 3976.