Mechanism of cataract formation in αA-crystallin Y118D mutation

Investigative Ophthalmology and Visual Science

Volumn 50, Issue 6, 2009, Pages 2919-2926

  Huang, Qingling ^a   Ding, Linlin ^a   Phan, Kim B ^a   Cheng, Catherine ^b   Xia, Chun Hong ^b   Gong, Xiaohua ^b   Horwitz, Joseph ^a  

^a JULES STEIN EYE INSTITUTE   (United States)

^b UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ALPHA CRYSTALLIN; CHAPERONE; MUTANT PROTEIN; RECOMBINANT ALPHA CRYSTALLIN; UNCLASSIFIED DRUG;

ANIMAL TISSUE; ARTICLE; CATARACT; CATARACTOGENESIS; CIRCULAR DICHROISM; CONTROLLED STUDY; FLUORESCENCE; GEL FILTRATION; GENE MUTATION; HETEROZYGOTE; LIGHT SCATTERING; MOLECULAR WEIGHT; MOUSE; NONHUMAN; PHYSICAL CHEMISTRY; PRIORITY JOURNAL; PROTEIN AGGREGATION; PROTEIN FUNCTION; PROTEIN LOCALIZATION; PROTEIN SECONDARY STRUCTURE; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; TWO DIMENSIONAL GEL ELECTROPHORESIS; WILD TYPE; ANIMAL; GEL CHROMATOGRAPHY; GENETICS; LENS; LIGHT; POINT MUTATION; RADIATION SCATTERING;

ALPHA-CRYSTALLIN A CHAIN; ANIMALS; CATARACT; CHROMATOGRAPHY, GEL; CIRCULAR DICHROISM; ELECTROPHORESIS, GEL, TWO-DIMENSIONAL; LENS, CRYSTALLINE; LIGHT; MICE; POINT MUTATION; REVERSE TRANSCRIPTASE POLYMERASE CHAIN REACTION; SCATTERING, RADIATION;

EID: 66849114922     PISSN: 01460404     EISSN: 15525783     Source Type: Journal    
DOI: 10.1167/iovs.08-3070     Document Type: Article

References (59)

1. Bloemendal H, de Jong W, Jaenicke R, Lubsen NH, Slingsby C, Tardieu A. Ageing and vision: structure, stability and function of lens crystallins. Prog Biophys Mol Biol. 2004;86:407-485.
2. Horwitz J. Alpha-crystallin. Exp Eye Res. 2003;76:145-153.
3. Siezen RJ, Bindels JG, Hoenders HJ. The quaternary structure of bovine alpha-crystallin. Effects of variation in alkaline pH, ionic strength, temperature and calcium ion concentration. Eur J Biochem. 1980;111:435-444.
4. van den Oetelaar PJ, van Someren PF, Thomson JA, Siezen RJ, Hoenders HJ. A dynamic quaternary structure of bovine alpha-crystallin as indicated from intermolecular exchange of subunits. Biochemistry. 1990;29:3488-3493.
5. Bova MP, Ding LL, Horwitz J, Fung BK. Subunit exchange of A-crystallin. J Biol Chem. 1997;272:29511-29517.
6. Klemenz R, Frohli E, Steiger RH, Schafer R, Aoyama A. Alpha B-crystallin is a small heat shock protein. Proc Natl Acad Sci U S A. 1991;88:3652-3656.
7. Kato K, Shinohara H, Kurobe N, Goto S, Inaguma Y, Ohshima K. Immunoreactive alpha A crystallin in rat non-lenticular tissues detected with a sensitive immunoassay method. Biochim Biophys Acta. 1991;1080:173-180.
8. Srinivasan AN, Nagineni CN, Bhat SP. Alpha A-crystallin is expressed in non-ocular tissues. J Biol Chem. 1992;267:23337-23341.
9. Atomi Y, Yamada S, Strohman R, Nonomura Y. Alpha B-crystallin in skeletal muscle: purification and localization. J Biochem. 1991; 110:812-822.
10. Bhat SP, Nagineni CN. 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.
11. Iwaki T, Kume-Iwaki A, Goldman JE. Cellular distribution of alpha B-crystallin in non-lenticular tissues. J Histochem Cytochem. 1990; 38:31-39.
12. Aoyama A, Frohli E, Schafer R, Klemenz R. Alpha B-crystallin expression in mouse NIH 3T3 fibroblasts: glucocorticoid responsiveness and involvement in thermal protection. Mol Cell Biol. 1993;13:1824-1835.
13. van den IPR, Overkamp P, Knauf U, Gaestel M, de Jong WW. Alpha A-crystallin confers cellular thermoresistance. FEBS Lett. 1994;355: 54-56.
14. Dasgupta S, Hohman TC, Carper D. Hypertonic stress induces alpha B-crystallin expression. Exp Eye Res. 1992;54:461-470.
15. Mehlen P, Preville X, Chareyron P, Briolay J, Klemenz R, Arrigo AP. Constitutive expression of human hsp27, Drosophila hsp27, or human alpha B-crystallin confers resistance to TNF- and oxidative stress-induced cytotoxicity in stably transfected murine L929 fibroblasts. J Immunol. 1995;154:363-374.
16. Mehlen P, Schulze-Osthoff K, Arrigo AP. Small stress proteins as novel regulators of apoptosis. Heat shock protein 27 blocks Fas/ APO-1- and staurosporine-induced cell death. J Biol Chem. 1996; 271:16510-16514.
17. Horwitz J. Alpha-crystallin can function as a molecular chaperone. Proc Natl Acad Sci U S A. 1992;89:10449-10453.
18. Muchowski PJ, Bassuk JA, Lubsen NH, Clark JI. Human alphaB-crystallin. Small heat shock protein and molecular chaperone. J Biol Chem. 1997;272:2578-2582.
19. Velasco PT, Lukas TJ, Murthy SN, Duglas-Tabor Y, Garland DL, Lorand L. Hierarchy of lens proteins requiring protection against heat-induced precipitation by the alpha crystallin chaperone. Exp Eye Res. 1997;65:497-505.
20. Nicholl ID, Quinlan RA. Chaperone activity of alpha-crystallins modulates intermediate filament assembly. EMBO J. 1994;13:945-953.
21. Muchowski PJ, Valdez MM, Clark JI. AlphaB-crystallin selectively targets intermediate filament proteins during thermal stress. Invest Ophthalmol Vis Sci. 1999;40:951-958.
22. Wang K, Spector A. Alpha-crystallin stabilizes actin filaments and prevents cytochalasin-induced depolymerization in a phosphorylation-dependent manner. Eur J Biochem. 1996;242:56-66.
23. Brady JP, Garland D, Duglas-Tabor Y, Robison WG, Jr, Groome A, Wawrousek EF. Targeted disruption of the mouse alpha A-crystallin gene induces cataract and cytoplasmic inclusion bodies containing the small heat shock protein alpha B-crystallin. Proc Natl Acad Sci U S A. 1997;94:884-889.
24. Brady JP, Garland DL, Green DE, Tamm ER, Giblin FJ, Wawrousek EF. AlphaB-crystallin in lens development and muscle integrity: a gene knockout approach. Invest Ophthalmol Vis Sci. 2001;42: 2924-2934.
25. Bai F, Xi JH, Wawrousek EF, Fleming TP, Andley UP. Hyperproliferation and p53 status of lens epithelial cells derived from alpha B-crystallin knockout mice. J Biol Chem. 2003;278:36876-36886.
26. Mackay DS, Andley UP, Shiels A. Cell death triggered by a novel mutation in the alpha A-crystallin gene underlies autosomal dominant cataract linked to chromosome 21q. Eur J Hum Genet. 2003;11:784-793.
27. Litt M, Kramer P, LaMorticella DM, Murphey W, Lovrien EW, Weleber RG. Autosomal dominant congenital cataract associated with a missense mutation in the human alpha crystallin gene CRYAA. Hum Mol Genet. 1998;7:471-474.
28. Graw J, Loster J, Soewarto D, et al. Characterization of a new, dominant V124E mutation in the mouse alpha A-crystallin-encoding gene. Invest Ophthalmol Vis Sci. 2001;42:2909-2915.
29. Hansen L, Yao W, Eiberg H, et al. Genetic heterogeneity in microcornea-cataract: five novel mutations in CRYAA, CRYGD, and GJA8. Invest Ophthalmol Vis Sci. 2007;48:3937-3944.
30. Pras E, Frydman M, Levy-Nissenbaum E, et al. A nonsense mutation (W9X) in CRYAA causes autosomal recessive cataract in an inbred Jewish Persian family. Invest Ophthalmol Vis Sci. 2000;41:3511-3515.
31. Khan AO, Aldahmesh MA, Meyer B. Recessive congenital total cataract with microcornea and heterozygote carrier signs caused by a novel missense CRYAA mutation (R54C). Am J Ophthalmol. 2007;144:949-952.
32. Chang B, Hawes NL, Smith RS, Heckenlively JR, Davisson MT, Roderick TH. Chromosomal localization of a new mouse lens opacity gene (lop18). Genomics. 1996;36:171-173.
33. Xia CH, Liu H, Chang B, et al. Arginine 54 and Tyrosine 118 residues of alphaA-crystallin are crucial for lens formation and transparency. Invest Ophthalmol Vis Sci. 2006;47:3004-3010.
34. Vicart P, Caron A, Guicheney P, et al. A missense mutation in the alpha B-crystallin chaperone gene causes a desmin-related myopathy. Nat Genet. 1998;20:92-95.
35. Bova MP, Yaron O, Huang Q, et al. Mutation R120G in alpha B-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. 1999;96:6137-6142.
36. Cobb BA, Petrash JM. Structural and functional changes in the alpha A-crystallin R116C mutant in hereditary cataracts. Biochemistry. 2000;39:15791-15798.
37. Shroff NP, Cherian-Shaw M, Bera S, Abraham EC. Mutation of R116C results in highly oligomerized alpha A-crystallin with modified structure and defective chaperone-like function. Biochemistry. 2000;39:1420-1426.
38. Hsu CD, Kymes S, Petrash JM. A transgenic mouse model for human autosomal dominant cataract. Invest Ophthalmol Vis Sci. 2006;47:2036-2044.
39. Liu Y, Zhang X, Luo L, et al. A novel alpha B-crystallin mutation associated with autosomal dominant congenital lamellar cataract. Invest Ophthalmol Vis Sci. 2006;47:1069-1075.
40. Horwitz J, Huang QL, Ding L, Bova MP. Lens alpha-crystallin: chaperone-like properties. Methods Enzymol. 1998;290:365-383.
41. Ho SN, Hunt HD, Horton RM, Pullen JK, Pease LR. Site-directed mutagenesis by overlap extension using the polymerase chain reaction. Gene. 1989;77:51-59.
42. Mach H, Middaugh CR, Lewis RV. Statistical determination of the average values of the extinction coefficients of tryptophan and tyrosine in native proteins. Anal Biochem. 1992;200:74-80.
43. Folta-Stogniew E, Williams KR. Determination of molecular masses of proteins in solution: implementation of an HPLC size exclusion chromatography and laser light scattering service in a core laboratory. J Biomol Tech. 1999;10:51-63.
44. Wen J, Arakawa T, Philo JS. Size-exclusion chromatography with on-line light-scattering, absorbance, and refractive index detectors for studying proteins and their interactions. Anal Biochem. 1996; 240:155-166.
45. Wyatt PJ. Light scattering and the absolute characterization of macromolecules. Anal Chim Acta. 1993;272:1-40.
46. Sreerama N, Woody RW. Estimation of protein secondary structure from circular dichroism spectra: comparison of CONTIN, SELCON, and CDSSTR methods with an expanded reference set. Anal Biochem. 2000;287:252-260.
47. Sreerama N, Woody RW. Computation and analysis of protein circular dichroism spectra. Methods Enzymol. 2004;383:318-351.
48. Horwitz J. Protein Folding Handbook. Weinheim: Wiley-VCH Verlag GmbH; 2005:858-875.
49. Horwitz J. Some properties of the low molecular weight alpha-crystallin from normal human lens: comparison with bovine lens. Exp Eye Res. 1976;23:471-481.
50. Strickland EH. Aromatic contributions to circular dichroism spectra of proteins. CRC Crit Rev Biochem. 1974;2:113-175.
51. Berengian AR, Bova MP, McHaourab HS. Structure and function of the conserved domain in alpha A-crystallin. Site-directed spin labeling identifies a beta-strand located near a subunit interface. Biochemistry. 1997;36:9951-9957.
52. Berengian AR, Parfenova M, McHaourab HS. Site-directed spin labeling study of subunit interactions in the alpha-crystallin domain of small heat-shock proteins. Comparison of the oligomer symmetry in alpha A-crystallin, HSP 27, and HSP 16.3. J Biol Chem. 1999;274:6305-6314.
53. Regan L. Protein structure. Born to be beta. Curr Biol. 1994;4: 656-658.
54. de Jong WW, Caspers GJ, Leunissen JA. Genealogy of the alpha-crystallin-small heat-shock protein superfamily. Int J Biol Macromol. 1998;22:151-162.
55. Hejtmancik JF. Congenital cataracts and their molecular genetics. Semin Cell Dev Biol. 2008;19:134-149.
56. Murugesan R, Santhoshkumar P, Sharma KK. Cataract-causing alphaAG98R mutant shows substrate-dependent chaperone activity. Mol Vis. 2007;13:2301-2309.
57. Bera S, Abraham EC. The alpha A-crystallin R116C mutant has a higher affinity for forming heteroaggregates with alpha B-crystallin. Biochemistry. 2002;41:297-305.
58. Siezen RJ, Hoenders HJ. The quaternary structure of bovine alpha-crystallin. Surface probing by limited proteolysis in vitro. Eur J Biochem. 1979;96:431-440.
59. Koteiche HA, McHaourab HS. Mechanism of a hereditary cataract phenotype. Mutations in alpha A-crystallin activate substrate binding. J Biol Chem. 2006;281:14273-14279.