Effects of congenital cataract mutation R116H on αA-crystallin structure, function and stability

Biochimica et Biophysica Acta - Proteins and Proteomics

Volumn 1804, Issue 4, 2010, Pages 948-956

  Pang, Min ^a   Su, Jing Tan ^a   Feng, Shan ^a   Tang, Zhi Wei ^a   Gu, Feng ^a,b   Zhang, Meng ^a,b   Ma, Xu ^a,b   Yan, Yong Bin ^a  

^a TSINGHUA UNIVERSITY   (China)

^b NATIONAL RESEARCH INSTITUTE FOR FAMILY PLANNING   (China)

Author keywords

A crystallin; Autosomal dominant congenital cataract; Missense mutation; Protein aggregation; Protein stability

Indexed keywords

ALPHA CRYSTALLIN; OLIGOMER;

ARTICLE; CONGENITAL CATARACT; MISSENSE MUTATION; POLYACRYLAMIDE GEL ELECTROPHORESIS; PRIORITY JOURNAL; PROTEIN FUNCTION; PROTEIN QUATERNARY STRUCTURE; PROTEIN SECONDARY STRUCTURE; PROTEIN STABILITY; PROTEIN STRUCTURE; STRESS; WILD TYPE;

AMINO ACID SUBSTITUTION; CATARACT; CIRCULAR DICHROISM; CRYSTALLINS; GUANIDINE; HUMANS; MODELS, BIOLOGICAL; MOLECULAR CHAPERONES; MOLECULAR WEIGHT; MUTANT PROTEINS; MUTATION, MISSENSE; PROTEIN DENATURATION; PROTEIN FOLDING; PROTEIN MULTIMERIZATION; PROTEIN STABILITY; PROTEIN STRUCTURE, QUATERNARY; PROTEIN STRUCTURE, SECONDARY; PROTEIN STRUCTURE, TERTIARY; RECOMBINANT PROTEINS; UNFOLDED PROTEIN RESPONSE;

EID: 76849101762     PISSN: 15709639     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.bbapap.2010.01.001     Document Type: Article

References (59)

1. Benedek G.B. Theory of transparency of the eye. Appl. Optics 10 (1971) 459-473
2. Tholozan F.M.D., and Quinlan R.A. Lens cells: more than meets the eye. Int. J. Biochem. Cell Biol. 39 (2007) 1754-1759
3. Bloemendal H., de Jong W., Jaenicke R., Lubsen N.H., Slingsby C., and Tardieu A. Ageing and vision: structure, stability and function of lens crystallins. Prog. Biophys. Mol. Biol. 86 (2004) 407-485
4. Andley U.P. Crystallins in the eye: function and pathology. Prog. Retin. Eye Res. 26 (2007) 78-98
5. Horwitz J. Alpha-crystallin. Exp. Eye Res. 76 (2003) 145-153
6. Horwitz J. α-Crystallin can function as a molecular chaperone. Proc. Natl. Acad. Sci. U. S. A. 89 (1992) 10449-10453
7. Ingolia T.D., and Craig E.A. Four small Drosophila heat shock proteins are related to each other and to mammalian α-crystallin. Proc. Natl. Acad. Sci. U. S. A. 79 (1982) 2360-2364
8. Jakob U., Gaestel M., Engel K., and Buchner J. Small heat shock proteins are molecular chaperones. J. Biol. Chem. 268 (1993) 1517-1520
9. Raman B., and Rao C.M. Chaperone-like activity and quaternary structure of α-crystallin. J. Biol. Chem. 269 (1994) 27264-27268
10. Wang K.Y., and Spector A. The chaperone activity of bovine alpha-crystallin - interaction with other lens crystallins in native and denatured states. J. Biol. Chem. 269 (1994) 13601-13608
11. Rajaraman K., Raman B., and Rao C.M. Molten-globule state of carbonic anhydrase binds to the chaperone-like α-crystallin. J. Biol. Chem. 271 (1996) 27595-27600
12. Khanova H.A., Markossian K.A., Kurganov B.I., Samoilov A.M., Kleimenov S.Y., Levitsky D.I., Yudin I.K., Timofeeva A.C., Muranov K.O., and Ostrovsky M.A. Mechanism of chaperone-like activity. Suppression of thermal aggregation of βL-crystallin by α-crystallin. Biochemistry 44 (2005) 15480-15487
13. Markossian K., Yudin I., and Kurganov B. Mechanism of suppression of protein aggregation by α-crystallin. Int. J. Mol. Sci. 10 (2009) 1314-1345
14. Shiels A., and Hejtmancik J.F. Genetic origins of cataract. Arch. Ophthalmol. 125 (2007) 165-173
15. Bova M.P., Yaron O., Huang Q., Ding L., Haley D.A., Stewart P.L., and Horwitz J. Mutation R120G in αB-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 (1999) 6137-6142
16. Kumar L.V.S., Ramakrishna T., and Rao C.M. Structural and functional consequences of the mutation of a conserved arginine residue in αA and αB crystallins. J. Biol. Chem. 274 (1999) 24137-24141
17. Andley U.P., Patel H.C., and Xi J.-H. The R116C mutation in αA-crystallin diminishes its protective ability against stress-induced lens epithelial cell apoptosis. J. Biol. Chem. 277 (2002) 10178-10186
18. Koteiche H.A., and McHaourab H.S. Mechanism of a hereditary cataract phenotype: mutations in αA-crystallin activate substrate binding. J. Biol. Chem. 281 (2006) 14273-14279
19. Singh D., Raman B., Ramakrishna T., and Rao C.M. Mixed oligomer formation between human αA-crystallin and its cataract-causing G98R mutant: structural, stability and functional differences. J. Mol. Biol. 373 (2007) 1293-1304
20. Xi J.-h., Bai F., Gross J., Townsend R.R., Menko A.S., and Andley U.P. Mechanism of small heat shock protein function in vivo - a knock-in mouse model demonstrates that the R49C mutation in alpha A-crystallin enhances protein insolubility and cell death. J. Biol. Chem. 283 (2008) 5801-5814
21. Shroff N.P., Cherian-Shaw M., Bera S., and Abraham E.C. Mutation of R116C results in highly oligomerized αA-crystallin with modified structure and defective chaperone-like function. Biochemistry 39 (2000) 1420-1426
22. Bera S., and Abraham E.C. The αA-crystallin R116C mutant has a higher affinity for forming heteroaggregates with αB-crystallin. Biochemistry 41 (2002) 297-305
23. Bera S., Thampi P., Cho W.J., and Abraham E.C. A positive charge preservation at position 116 of αA-crystallin is critical for its structural and functional integrity. Biochemistry 41 (2002) 12421-12426
24. Dobson C.M. Protein folding and misfolding. Nature 426 (2003) 884-890
25. Crowther D.C. Familial conformational diseases and dementias. Hum. Mutat. 20 (2002) 1-14
26. Almstedt K., Lundqvist M., Carlsson J., Karlsson M., Persson B., Jonsson B.H., Carlsson U., and Hammarstrom P. Unfolding a folding disease: folding, misfolding and aggregation of the marble brain syndrome-associated mutant H107Y of human carbonic anhydrase II. J. Mol. Biol. 342 (2004) 619-633
27. Hart P.J. Pathogenic superoxide dismutase structure, folding, aggregation and turnover. Curr. Opin. Chem. Biol. 10 (2006) 131-138
28. Feng S., Zhao T.-J., Zhou H.-M., and Yan Y.-B. Effects of the single point genetic mutation D54G on muscle creatine kinase activity, structure and stability. Int. J. Biochem. Cell Biol. 39 (2007) 392-401
29. Jiang Y., Su J.-T., Zhang J., Wei X., Yan Y.-B., and Zhou H.-M. Reshaping the folding energy landscape of human carbonic anhydrase II by a single point genetic mutation Pro237His. Int. J. Biochem. Cell Biol. 40 (2008) 776-788
30. Gu F., Luo W., Li X., Wang Z., Lu S., Zhang M., Zhao B., Zhu S., Feng S., Yan Y.-B., Huang S., and Ma X. A novel mutation in AlphaA-crystallin (CRYAA) caused autosomal dominant congenital cataract in a large Chinese family. Hum. Mutat. 29 (2008) 769
31. Sreerama N., and Woody R.W. Estimation of protein secondary structure from circular dichroism spectra: comparison of CONTIN, SELCON, and CDSSTR methods with an expanded reference set. Anal. Biochem. 287 (2000) 252-260
32. Bushmarina N.A., Kuznetsova I.M., Biktashev A.G., Turoverov K.K., and Uversky V.N. Partially folded conformations in the folding pathway of bovine carbonic anhydrase II: a fluorescence spectroscopic analysis. ChemBioChem 2 (2001) 813-821
33. Su J.-T., Kim S.-H., and Yan Y.-B. Dissecting the pretransitional conformational changes in aminoacylase I thermal denaturation. Biophys. J. 92 (2007) 578-587
34. Pasternack R., and Collings P. Resonance light scattering: a new technique for studying chromophore aggregation. Science 269 (1995) 935-939
35. He G.-J., Zhang A., Liu W.-F., Cheng Y., and Yan Y.-B. Conformational stability and multistate unfolding of poly(A)-specific ribonuclease. FEBS J. 276 (2009) 2849-2860
36. Li Y., Schmitz K.R., Salerno J.C., and Koretz J.F. The role of the conserved COOH-terminal triad in αA-crystallin aggregation and functionality. Mol. Vis. 13 (2007) 1758-1768
37. Wang X., and Bettelheim F.A. Second viral coefficient of α-crystallin. Proteins: Struct. Funct. Genet. 5 (1989) 166-169
38. Aquilina J.A., Benesch J.L.P., Bateman O.A., Slingsby C., and Robinson C.V. Polydispersity of a mammalian chaperone: mass spectrometry reveals the population of oligomers in αB-crystallin. Proc. Natl. Acad. Sci. U. S. A. 100 (2003) 10611-10616
39. Peschek J., Braun N., Franzmann T.M., Georgalis Y., Haslbeck M., Weinkauf S., and Buchner J. The eye lens chaperone α-crystallin forms defined globular assemblies. Proc. Natl. Acad. Sci. U. S. A. 106 (2009) 13272-13277
40. Cobb B.A., and Petrash J.M. Structural and functional changes in the αA-crystallin R116C mutant in hereditary cataracts. Biochemistry 39 (2000) 15791-15798
41. Perng M.D., Muchowski P.J., van Den I.P., Wu G.J., Hutcheson A.M., Clark J.I., and Quinlan R.A. The cardiomyopathy and lens cataract mutation in αB-crystallin alters its protein structure, chaperone activity, and interaction with intermediate filaments in vitro. J. Biol. Chem. 274 (1999) 33235-33243
42. Siezen R.J., and Argos P. Structural homology of lens crystallins: III. Secondary structure estimation from circular dichroism and prediction from amino acid sequences. Biochim. Biophys. Acta 748 (1983) 56-67
43. Lamba O.P., Borchman D., Sinha S.K., Shah J., Renugopalakrishnan V., and Yappert M.C. Estimation of the secondary structure and conformation of bovine lens crystallins by infrared spectroscopy: quantitative analysis and resolution by Fourier self-deconvolution and curve fit. Biochim. Biophys. Acta 1163 (1993) 113-123
44. Bloemendal M., Toumadje A., and Johnson W.C. Bovine lens crystallins do contain helical structure: a circular dichroism study. Biochim. Biophys. Acta 1432 (1999) 234-238
45. Reshetnyak Y.K., Koshevnik Y., and Burstein E.A. Decomposition of protein tryptophan fluorescence spectra into log-normal components. III. Correlation between fluorescence and microenvironment parameters of individual tryptophan residues. Biophys. J. 81 (2001) 1735-1758
46. Derham B.K., and Harding J.J. α-crystallin as a molecular chaperone. Prog. Retin. Eye Res. 18 (1999) 463-509
47. Murugesan R., Santhoshkumar P., and Sharma K.K. Cataract-causing αAG98R mutant shows substrate-dependent chaperone activity. Mol. Vis. 13 (2007) 2301-2309
48. Treweek T.M., Rekas A., Lindner R.A., Walker M.J., Aquilina J.A., Robinson C.V., Horwitz J., Perng M.D., Quinlan R.A., and Carver J.A. R120G αB-crystallin promotes the unfolding of reduced alpha-lactalbumin and is inherently unstable. FEBS J. 272 (2005) 711-724
49. Wang S., Liu W.-F., He Y.-Z., Zhang A., Huang L., Dong Z.-Y., and Yan Y.-B. Multistate folding of a hyperthermostable Fe-superoxide dismutase (TcSOD) in guanidinium hydrochloride: the importance of the quaternary structure. Biochim. Biophys. Acta - Proteins Proteomics 1784 (2008) 445-454
50. Kuznetsova I.M., Stepanenko O.V., Turoverov K.K., Zhu L., Zhou J.-M., Fink A.L., and Uversky V.N. Unraveling multistate unfolding of rabbit muscle creatine kinase. Biochim. Biophys. Acta 1596 (2002) 138-155
51. van Montfort R.L.M., Basha E., Friedrich K.L., Slingsby C., and Vierling E. Crystal structure and assembly of a eukaryotic small heat shock protein. Nature Struct. Biol. 8 (2001) 1025-1030
52. Fink A.L. Molten globules. Methods Mol. Biol. 40 (1995) 343-360
53. Das B.K., and Liang J.J.N. Detection and characterization of α-crystallin intermediate with maximal chaperone-like activity. Biochem. Biophys. Res. Commun. 236 (1997) 370-374
54. Sun T.-X., Akhtar N.J., and Liang J.J.N. Thermodynamic stability of human lens recombinant αA- and αB-crystallins. J. Biol. Chem. 274 (1999) 34067-34071
55. van den Oetelaar P.J.M., and Hoenders H.J. Folding-unfolding and aggregation-dissociation of bovine [alpha]-crystallin subunits; evidence for unfolding intermediates of the [alpha]A subunits. Biochim. Biophys. Acta - Protein Struct. Mol. Enzymol. 995 (1989) 91-96
56. Pace C.N. Determination and analysis of urea and guanidine hydrochloride denaturation curves. Method Enzymol. 131 (1986) 266-280
57. Litt M., Kramer P., LaMorticella D.M., Murphey W., Lovrien E.W., and Weleber R.G. Autosomal dominant congenital cataract associated with a missense mutation in the human alpha crystallin gene CRYAA. Hum. Mol. Genet. 7 (1998) 471-474
58. Vicart P., Caron A., Guicheney P., Li Z.L., Prevost M.C., Faure A., Chateau D., Chapon F., Tome F., Dupret J.M., Paulin D., and Fardeau M. A missense mutation in the αB-crystallin chaperone gene causes a desmin-related myopathy. Nat. Genet. 20 (1998) 92-95
59. Stefani M., and Dobson C.M. Protein aggregation and aggregate toxicity: new insights into protein folding, misfolding diseases and biological evolution. J. Mol. Med. 81 (2003) 678-699