Inhibition of unfolding and aggregation of lens protein human gamma D crystallin by sodium citrate

Experimental Eye Research

Volumn 93, Issue 4, 2011, Pages 371-381

  Goulet, Daniel R ^a   Knee, Kelly M ^a   King, Jonathan A ^a  

^a MASSACHUSETTS INSTITUTE OF TECHNOLOGY   (United States)

Author keywords

Aggregation; Citrate; Crystallin; Protein folding; Stability

Indexed keywords

CITRATE SODIUM; HUMAN GAMMA DEXTRO CRYSTALLIN; LENS PROTEIN; UNCLASSIFIED DRUG;

AMINO TERMINAL SEQUENCE; ARTICLE; BINDING KINETICS; CARBOXY TERMINAL SEQUENCE; HUMAN; MOLECULAR DYNAMICS; PRIORITY JOURNAL; PROTEIN AGGREGATION; PROTEIN REFOLDING; PROTEIN UNFOLDING; TURBIDITY;

CATARACT; CITRATES; GAMMA-CRYSTALLINS; HUMANS; LENS, CRYSTALLINE; PROTEIN DENATURATION; PROTEIN FOLDING; PROTEIN UNFOLDING; SPECTROMETRY, FLUORESCENCE;

EID: 80055059979     PISSN: 00144835     EISSN: 10960007     Source Type: Journal    
DOI: 10.1016/j.exer.2011.04.011     Document Type: Article

References (78)

1. Abraham A.G., Condon N.G., West Gower E. The new epidemiology of cataract. Ophthalmology Clinics of North America 2006, 19:415-425.
2. Acosta-Sampson L., King J. Partially folded aggregation intermediates of human gammaD-, gammaC-, and gammaS-crystallin are recognized and bound by human alphaB-crystallin chaperone. Journal of Molecular Biology 2010, 401:134-152.
3. Aravind P., Mishra A., Suman S.K., Jobby M.K., Sankaranarayanan R., Sharma Y. Betagamma-Crystallin superfamily contains a universal motif for binding calcium. Biochemistry 2009, 48:12180-12190.
4. Babizhayev M.A., Burke L., Micans P., Richer S.P. N-Acetylcarnosine sustained drug delivery eye drops to control the signs of ageless vision: glare sensitivity, cataract amelioration and quality of vision currently available treatment for the challenging 50,000-patient population. Journal of Clinical Interventions in Aging 2009, 4:31-50.
5. Baldwin R.L. How Hofmeister ion interactions affect protein stability. Biophysical Journal 1996, 71:2056-2063.
6. Banci L., Bertini I., Cramaro F., Del Conte R., Viezzoli M.S. Solution structure of Apo Cu, Zn superoxide dismutase: role of metal ions in protein folding. Biochemistry 2003, 42:9543-9553.
7. Barnwal R.P., Jobby M.K., Devi K.M., Sharma Y. Solution structure and calcium-binding properties of M-Crystallin, a primordial βγ-Crystallin from Archaea. Journal of Molecular Biology 2009, 386:675-689.
8. Basak A., Bateman O., Slingsby C., Pande A., Asherie N., Ogun O., Benedek G.B., Pande J. High-resolution X-ray crystal structures of human gammaD crystallin (1.25 A) and the R58H mutant (1.15 A) associated with aculeiform cataract. Journal of Molecular Biology 2003, 328:1137-1147.
9. Bottomley S.P., Tew D.J. The citrate ion increases the conformational stability of alpha(1)-antitrypsin. Biochimica et Biophysica Acta 2000, 1481:11-17.
10. Brian G., Taylor H. Cataract blindness - challenges for the 21st century. Bulletin of the World Health Organization 2001, 79:249-256.
11. Busby T.F., Atha D.H., Ingham K.C. Thermal denaturation of antithrombin III. Stabilization by heparin and lyotropic anions. Journal of Biological Chemistry 1981, 256:12140-12147.
12. Clark A.C., Sinclair J.F., Baldwin T.O. Folding of bacterial luciferase involves a non-native heterodimeric intermediate in equilibrium with the native enzyme and the unfolded subunits. Journal of Biological Chemistry 1993, 268:10773-10779.
13. 1H NMR spectroscopic evidence for specific crystallin-crystallin interactions. Experimental Eye Research 1994, 59:607-616.
14. Das P., King J.A., Zhou R. beta-Strand interactions at the domain interface critical for the stability of human lens gammaD-crystallin. Protein Science 2010, 19:131-140.
15. David L.L., Lampi K.J., Lund A.L., Smith J.B. The sequence of human betaB1-crystallin cDNA allows mass spectrometric detection of betaB1 p.otein missing portions of its N-terminal extension. Journal of Biological Chemistry 1996, 271:4273-4279.
16. Delaye M., Tardieu A. Short-range order of crystallin proteins accounts for eye lens transparency. Nature 1983, 302:415-417.
17. Dill K.A., Truskett T.M., Vlachy V., Hribar-Lee B. Modeling water, the hydrophobic effect, and ion solvation. Annual Review of Biophysical and Biomolecular Structure 2005, 34:173-199.
18. Everett C.A., Glenister P.H., Taylor D.M., Lyon M.F., Kratochvilova-Loester J., Favor J. Mapping of six dominant cataract genes in the mouse. Genomics 1994, 20:429-434.
19. Fagerholm P.P., Philipson B.T., Lindström B. Normal human lens - the distribution of protein. Experimental Eye Research 1981, 33:615-620.
20. Flaugh S.L., Kosinski-Collins M.S., King J. Contributions of hydrophobic domain interface interactions to the folding and stability of human gammaD-crystallin. Protein Science 2005, 14:569-581.
21. Flaugh S.L., Kosinski-Collins M.S., King J. Interdomain side-chain interactions in human gammaD crystallin influencing folding and stability. Protein Science 2005, 14:2030-2043.
22. Flaugh S.L., Mills I.A., King J. Glutamine deamidation destabilizes human gammaD-crystallin and lowers the kinetic barrier to unfolding. Journal of Biological Chemistry 2006, 281:30782-30793.
23. Friedman, D.S., Congdon, N., Kempen, J., Tielsch, J.M., 2008, Vision Problems In the US. National Eye Institute. 1-42.
24. Getzoff E.D., Tainer J.A., Stempien M.M., Bell G.I., Hallewell R.A. Evolution of CuZn superoxide dismutase and the Greek key beta-barrel structural motif. Proteins 1989, 5:322-336.
25. Graw J. Genetics of crystallins: cataract and beyond. Experimental Eye Research 2009, 88:173-189.
26. Graw J., Neuhäuser-Klaus A., Klopp N., Selby P.B., Löster J., Favor J. Genetic and allelic heterogeneity of Cryg mutations in eight distinct forms of dominant cataract in the mouse. Investigative Ophthalmology and Visual Science 2004, 45:1202-1213.
27. Greene R.F., Pace C.N. Urea and guanidine hydrochloride denaturation of ribonuclease, lysozyme, alpha-chymotrypsin, and beta-lactoglobulin. Journal of Biological Chemistry 1974, 249:5388-5393.
28. Hains P.G., Truscott R.J. Age-dependent deamidation of lifelong proteins in the human lens. Investigative Ophthalmology and Visual Science 2010, 51:3107-3114.
29. Hains P.G., Truscott R.J.W. Post-translational modifications in the nuclear region of young, aged, and cataract human lenses. Journal of Proteome Research 2007, 6:3935-3943.
30. Hanson S.R., Hasan A., Smith D.L., Smith J.B. The major in vivo modifications of the human water-insoluble lens crystallins are disulfide bonds, deamidation, methionine oxidation and backbone cleavage. Experimental Eye Research 2000, 71:195-207.
31. Harrington V., Srivastava O.P., Kirk M. Proteomic analysis of water insoluble proteins from normal and cataractous human lenses. Molecular Vision 2007, 13:1680-1694.
32. Knee K.M., Goulet D.R., Zhang J., Chen B., Chiu W., King J.A. The group II chaperonin Mm-Cpn binds and refolds human γD crystallin. Protein Science 2011, 20:30-41.
33. Kosinski-Collins M.S., Flaugh S.L., King J. Probing folding and fluorescence quenching in human gammaD crystallin Greek key domains using triple tryptophan mutant proteins. Protein Science 2004, 13:2223-2235.
34. Kosinski-Collins M.S., King J. In vitro unfolding, refolding, and polymerization of human gammaD crystallin, a protein involved in cataract formation. Protein Science 2003, 12:480-490.
35. Kretschmar M., Mayr E.M., Jaenicke R. Kinetic and thermodynamic stabilization of the betagamma-crystallin homolog spherulin 3a from Physarum polycephalum by calcium binding. Journal of Molecular Biology 1999, 289:701-705.
36. Kronman M.J., Sinha S.K., Brew K. Characteristics of the binding of Ca2+ and other divalent metal ions to bovine alpha-lactalbumin. Journal of Biological Chemistry 1981, 256:8582-8587.
37. Kurzel R.B., Wolbarsht M., Yamanashi B.S., Staton G.W., Borkman R.F. Tryptophan excited states and cataracts in the human lens. Nature 1973, 241:132-133.
38. Lampi K.J., Ma Z., Hanson S.R., Azuma M., Shih M., Shearer T.R., Smith D.L., Smith J.B., David L.L. Age-related changes in human lens crystallins identified by two-dimensional electrophoresis and mass spectrometry. Experimental Eye Research 1998, 67:31-43.
39. Lee S., Mahler B., Toward J., Jones B., Wyatt K., Dong L., Wistow G., Wu Z. A single destabilizing mutation (F9S) promotes concerted unfolding of an entire globular domain in gammaS-crystallin. Journal of Molecular Biology 2010, 399:320-330.
40. Livingston P.M., Carson C.A., Taylor H.R. The epidemiology of cataract: a review of the literature. Ophthalmic Epidemiology 1995, 2:151-164.
41. McCarty C.A., Taylor H.R. A review of the epidemiologic evidence linking ultraviolet radiation and cataracts. Developmental Ophthalmology 2002, 35:21-31.
42. McFall-Ngai M.J., Ding L.L., Takemoto L.J., Horwitz J. Spatial and temporal mapping of the age-related changes in human lens crystallins. Experimental Eye Research 1985, 41:745-758.
43. 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 gammaD-crystallin and gammaS-crystallin. Protein Science 2007, 16:2427-2444.
44. Moreau K.L., King J. Hydrophobic core mutations associated with cataract development in mice destabilize human gammaD-crystallin. Journal of Biological Chemistry 2009, 284:33285-33295.
45. Muzammil S., Kumar Y., Tayyab S. Anion-induced stabilization of human serum albumin prevents the formation of intermediate during urea denaturation. Proteins 2000, 40:29-38.
46. Nanavaty M.A., Vasavada A.R., Gupta P.D. Age-related cataract: management and prevention. Prevention and Treatment of Age-related Diseases 2006, 159-174. Springer, Dordrecht. S. Rattan, M. Kassem (Eds.).
47. Nagai R., Nagai M., Shimasaki S., Baynes J.W., Fujiwara Y. Citric acid inhibits development of cataracts, proteinuria and ketosis in streptozotocin (type 1) diabetic rats. Biochemical and Biophysical Research Communications 2010, 393:118-122.
48. Oyster C.W. The Human Eye: Structure and Function 1999, Sinauer Associates, Inc., Sunderland.
49. Pace C.N. Contribution of the hydrophobic effect to globular protein stability. Journal of Molecular Biology 1992, 226:29-35.
50. Pace C.N., McGrath T. Substrate stabilization of lysozyme to thermal and guanidine hydrochloride denaturation. Journal of Biological Chemistry 1980, 255:3862-3865.
51. Parge H.E., Hallewell R.A., Tainer J.A. Atomic structures of wild-type and thermostable mutant recombinant human Cu, Zn superoxide dismutase. Proceedings of the National Academy of Science 1992, 89:6109-6113.
52. Pearce M.C., Morton C.J., Feil S.C., Hansen G., Adams J.J., Parker M.W., Bottomley S.P. Preventing serpin aggregation: the molecular mechanism of citrate action upon antitrypsin unfolding. Protein Science 2008, 17:2127-2133.
53. Permyakov E.A., Berliner L.J. alpha-Lactalbumin: structure and function. FEBS Letters 2000, 473:269-274.
54. Purkiss A., Bateman O., Wyatt K., Wilmarth P., David L., Wistow G., Slingsby C. Biophysical properties of γC-crystallin in human and mouse eye lens: the role of molecular dipoles. Journal of Molecular Biology 2007, 372:205-222.
55. Ramos C., Baldwin R. Sulfate anion stabilization of native ribonuclease A both by anion binding and by the Hofmeister effect. Protein Science 2002, 11:1771-1778.
56. Roder H., Colón W. Kinetic role of early intermediates in protein folding. Current Opinion in Structural Biology 1997, 7:15-28.
57. Schneider C.P., Trout B. Investigation of cosolute-protein preferential interaction coefficients: new insight into the mechanism by which arginine iInhibits aggregation. The Journal of Physical Chemistry B 2009, 113:2050-2058.
58. 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. Molecular Vision 2009, 15:2129-2138.
59. Siezen R.J., Thomson J.A., Kaplan E.D., Benedek G.B. Human lens gamma-crystallins: isolation, identification, and characterization of the expressedgene products. Proceedings of the National Academy of Science 1987, 84:6088-6092.
60. Siezen R.J., Wu E., Kaplan E.D., Thomson J.A., Benedek G.B. Rat lens gamma-crystallins. Characterization of the six gene products and their spatial and temporal distribution resulting from differential synthesis. Journal of Molecular Biology 1988, 199:475-490.
61. Sikkink L.A., Ramirez-Alvarado M. Salts enhance both protein stability and amyloid formation of an immunoglobulin light chain. Biophysical Chemistry 2008, 135:25-31.
62. Sinha D., Wyatt M.K., Sarra R., Jaworski C., Slingsby C., Thaung C., Pannell L., Robison W.G., Favor J., Lyon M., Wistow G. A temperature-sensitive mutation of Crygs in the murine Opj cataract. Journal of Biological Chemistry 2001, 276:9308-9315.
63. Slingsby C., Clout N.J. Structure of the crystallins. Eye (London) 1999, 13:395-402.
64. Street T.O., Bolen D.W., Rose G.D. A molecular mechanism for osmolyte-induced protein stability. Proceedings of the National Academy of Science of the United States of America 2006, 103:13997-14002.
65. Tadeo X., López-Méndez B., Castaño D., Trigueros T., Millet O. Protein stabilization and the Hofmeister effect: the role of hydrophobic solvation. Biophysical Journal 2009, 97:2595-2603.
66. Takata T., Oxford J.T., Demeler B., Lampi K.J. Deamidation destabilizes and triggers aggregation of a lens protein, betaA3-crystallin. Protein Science 2008, 17:1565-1575.
67. Takemoto L.J., Hansen J.S., Zigler J.S., Horwitz J. Characterization of polypeptides from human nuclear cataracts by Western blot analysis. Experimental Eye Research 1985, 40:205-212.
68. Ueda Y., Duncan M.K., David L.L. Lens proteomics: the accumulation of crystallin modifications in the mouse lens with age. Investigative Ophthalmology and Visual Science 2002, 43:205-215.
69. Vagenende V., Yap M., Trout B. Mechanisms of protein stabilization and prevention of protein aggregation by glycerol. Biochemistry 2009, 48:11084-11096.
70. Van Ceunebroeck J.C., Hanssens I., Joniau M., Van Cauwelaert F. Thermodynamics of the Ca2+ binding to bovine alpha-lactalbumin. Journal of Biological Chemistry 1985, 260:10944-10947.
71. Von Hippel P.H., Wong K.Y. On the conformational stability of globular proteins. The effects of various electrolytes and nonelectrolytes on the thermal ribonuclease transition. Journal of Biological Chemistry 1965, 240:3909-3923.
72. Wang Y., Petty S., Trojanowski A., Knee K., Goulet D., Mukerji I., King J. Formation of amyloid fibrils in vitro from partially unfolded intermediates of human gammaC-crystallin. Investigative Ophthalmology and Visual Science 2010, 51:672-678.
73. Wenk M., Jaenicke R. Calorimetric analysis of the Ca(2+)-binding betagamma-crystallin homolog protein S from Myxococcus xanthus: intrinsic stability and mutual stabilization of domains. Journal of Molecular Biology 1999, 293:117-124.
74. Yamashita M.M., Wesson L., Eisenman G., Eisenberg D. Where metal ions bind in proteins. Proceedings of the National Academy of Science of the United States of America 1990, 87:5648-5652.
75. Yan H., Guo Y., Zhang J., Ding Z., Ha W., Harding J.J. Effect of carnosine, aminoguanidine, and aspirin drops on the prevention of cataracts in diabetic rats. Molecular Vision 2008, 14:2282-2291.
76. Zhang Y., Cremer P.S. Interactions between macromolecules and ions: the Hofmeister series. Current Opinion in Chemical Biology 2006, 10:658-663.
77. Zhang Y., Cremer P.S. Chemistry of Hofmeister anions and osmolytes. Annual Review Physical Chemistry 2010, 61:63-83.
78. Zigler J.S., Goosey J.D. Singlet oxygen as a possible factor in human senile nuclear cataract development. Current Eye Research 1984, 3:59-65.