The congenital cataract-linked G61C mutation destabilizes γD-crystallin and promotes non-native aggregation

PLoS ONE

Volumn 6, Issue 5, 2011, Pages

  Zhang, Wang ^a   Cai, Hong Chen ^a   Li, Fei Feng ^a,b,d   Xi, Yi Bo ^a,c   Ma, Xu ^a,b   Yan, Yong Bin ^a  

^a TSINGHUA UNIVERSITY   (China)

^b NATIONAL RESEARCH INSTITUTE FOR FAMILY PLANNING   (China)

^c LANZHOU UNIVERSITY   (China)

^d HARBIN MEDICAL UNIVERSITY   (China)

Author keywords

[No Author keywords available]

Indexed keywords

GAMMA CRYSTALLIN; CRYSTALLIN;

ARTICLE; BIOPHYSICS; BODY TEMPERATURE; CONGENITAL CATARACT; CONTROLLED STUDY; CRYSTAL STRUCTURE; DISEASE ASSOCIATION; G61C GENE; GENE; GENE MUTATION; HUMAN; PH MEASUREMENT; PHASE TRANSITION; PROTEIN AGGREGATION; PROTEIN STABILITY; PROTEIN STRUCTURE; TEMPERATURE SENSITIVITY; CATARACT; CHEMISTRY; GENETICS; METABOLISM; MUTATION; PROTEIN DENATURATION; SITE DIRECTED MUTAGENESIS;

CATARACT; CRYSTALLINS; HUMANS; MUTAGENESIS, SITE-DIRECTED; MUTATION; PROTEIN DENATURATION;

EID: 79957815181     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0020564     Document Type: Article

References (54)

1. Tholozan FMD, Quinlan RA, (2007) Lens cells: more than meets the eye. Int J Biochem Cell Biol 39: 1754-1759.
2. Kuszak JR, Bertram BA, Macsai MS, Rae JL, (1984) Sutures of the crystalline lens: a review. Scan Electron Microsc pp. 1369-1378.
3. Benedek GB, (1971) Theory of transparency of the eye. Appl Opt 10: 459-473.
4. Zinn KM, Mockel-Pohl S, (1973) Fine structure and function of ocular tissues. The lens and zonules. Int Ophthalmol Clin 13: 143-155.
5. Bassnett S, (2002) Lens organelle degradation. Exp Eye Res 74: 1-6.
6. Banh A, Bantseev V, Choh V, Moran KL, Sivak JG, (2006) The lens of the eye as a focusing device and its response to stress. Prog Retin Eye Res 25: 189-206.
7. Andley UP, (2007) Crystallins in the eye: function and pathology. Prog Retin Eye Res 26: 78-98.
8. Graw J, (2009) Genetics of crystallins: Cataract and beyond. Exp Eye Res 88: 173-189.
9. Piatigorsky J, (1989) Lens crystallins and their genes: diversity and tissue-specific expression. FASEB J 3: 1933-1940.
10. Bron AJ, Vrensen GF, Koretz J, Maraini G, Harding JJ, (2000) The ageing lens. Ophthalmologica 214: 86-104.
11. Graw J, (1997) The crystallins: genes, proteins and diseases. Biol Chem 378: 1331-1348.
12. Horwitz J, (1992) α-Crystallin can function as a molecular chaperone. Proc Natl Acad Sci USA 89: 10449-10453.
13. Wang KY, Spector A, (1994) The chaperone activity of bovine α-crystallin- Interaction with other lens crystallins in native and denatured states. J Biol Chem 269: 13601-13608.
14. Brakenhoff RH, Aarts HJM, Reek FH, Lubsen NH, Schoenmakers JGG, (1990) Human γ-crystallin genes: a gene family on its way to extinction. J Mol Biol 216: 519-532.
15. Devi RR, Yao W, Vijayalakshmi P, Sergeev YV, Sundaresan P, et al. (2008) Crystallin gene mutations in Indian families with inherited pediatric cataract. Mol Vis 14: 1157-1170.
16. Gu F, Li R, Ma XX, Shi LS, Huang SZ, et al. (2006) A missense mutation in the γD-crystallin gene CRYGD associated with autosomal dominant congenital cataract in a Chinese family. Mol Vis 12: 26-31.
17. Gu J, Qi Y, Wang L, Wang J, Shi L, et al. (2005) A new congenital nuclear cataract caused by a missense mutation in the γD-crystallin gene (CRYGD) in a Chinese family. Mol Vis 11: 971-976.
18. Hansen L, Yao W, Eiberg H, Kjaer KW, Baggesen K, et al. (2007) Genetic heterogeneity in microcornea-cataract: five novel mutations in CRYAA, CRYGD, and GJA8. Invest Ophthalmol Vis Sci 48: 3937-3944.
19. Héon E, Priston M, Schorderet DF, Billingsley GD, Girard PO, et al. (1999) The γ-crystallins and human cataracts: a puzzle made clearer. Am J Hum Genet 65: 1261-1267.
20. Khan AO, Aldahmesh MA, Ghadhfan FE, Al-Mesfer S, Alkuraya FS, (2009) Founder heterozygous P23T CRYGD mutation associated with cerulean (and coralliform) cataract in 2 Saudi families. Mol Vis 15: 1407-1411.
21. Kmoch S, Brynda J, Asfaw B, Bezouska K, Novak P, et al. (2000) Link between a novel human γD-crystallin allele and a unique cataract phenotype explained by protein crystallography. Hum Mol Genet 9: 1779-1786.
22. Mackay DS, Andley UP, Shiels A, (2004) A missense mutation in the γD crystallin gene (CRYGD) associated with autosomal dominant "coral-like" cataract linked to chromosome 2q. Mol Vis 10: 155-162.
23. McManus JJ, Lomakin A, Ogun O, Pande A, Basan M, et al. (2007) Altered phase diagram due to a single point mutation in human γD-crystallin. Proc Natl Acad Sci USA 104: 16856-16861.
24. Messina-Baas OM, Gonzalez-Huerta LM, Cuevas-Covarrubias SA, (2006) Two affected siblings with nuclear cataract associated with a novel missense mutation in the CRYGD gene. Mol Vis 12: 995-1000.
25. Nandrot E, Slingsby C, Basak A, Cherif-Chefchaouni M, Benazzouz B, et al. (2003) Gamma-D crystallin gene (CRYGD) mutation causes autosomal dominant congenital cerulean cataracts. J Med Genet 40: 262-267.
26. Roshan M, Vijaya PH, Lavanya GR, Shama PK, Santhiya ST, et al. (2010) A novel human CRYGD mutation in a juvenile autosomal dominant cataract. Mol Vis 16: 887-896.
27. Santana A, Waiswol M, Arcieri ES, Cabral de Vasconcellos JP, Barbosa de Melo M, (2009) Mutation analysis of CRYAA, CRYGC, and CRYGD associated with autosomal dominant congenital cataract in Brazilian families. Mol Vis 15: 793-800.
28. Shentu X, Yao K, Xu W, Zheng S, Hu S, et al. (2004) Special fasciculiform cataract caused by a mutation in the γD-crystallin gene. Mol Vis 10: 233-239.
29. Stephan DA, Gillanders E, Vanderveen D, Freas-Lutz D, Wistow G, et al. (1999) Progressive juvenile-onset punctate cataracts caused by mutation of the γD-crystallin gene. Proc Natl Acad Sci USA 96: 1008-1012.
30. Wang B, Yu C, Xi YB, Cai HC, Wang J, et al. (2011) A novel CRYGD mutation (p.Trp43Arg) causing autosomal dominant congenital cataract in a Chinese family. Hum Mutat 32: E1939-E1947.
31. Xu WZ, Zheng S, Xu SJ, Huang W, Yao K, et al. (2004) Autosomal dominant coralliform cataract related to a missense mutation of the γD-crystallin gene. Chin Med J (Engl) 117: 727-732.
32. Zhang LY, Gong B, Tong JP, Fan DS, Chiang SW, et al. (2009) A novel γD-crystallin mutation causes mild changes in protein properties but leads to congenital coralliform cataract. Mol Vis 15: 1521-1529.
33. Zhang LY, Yam GH, Fan DS, Tam PO, Lam DS, et al. (2007) A novel deletion variant of γD-crystallin responsible for congenital nuclear cataract. Mol Vis 13: 2096-2104.
34. Basak A, Bateman O, Slingsby C, Pande A, Asherie N, et al. (2003) High-resolution X-ray crystal structures of human γD crystallin (1.25 Å) and the R58H mutant (1.15 Å) associated with aculeiform cataract. J Mol Biol 328: 1137-1147.
35. Li F, Wang S, Gao C, Liu S, Zhao B, et al. (2008) Mutation G61C in the CRYGD gene causing autosomal dominant congenital coralliform cataracts. Mol Vis 14: 378-386.
36. Bradford MM, (1976) A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding. Anal Biochem 72: 248-252.
37. Pang M, Su JT, Feng S, Tang ZW, Gu F, et al. (2010) Effects of congenital cataract mutation R116H on αA-crystallin structure, function and stability. Biochim Biophys Acta- Proteins & Proteomics 1804: 948-956.
38. He GJ, Zhang A, Liu WF, Cheng Y, Yan YB, (2009) Conformational stability and multistate unfolding of poly(A)-specific ribonuclease. FEBS J 276: 2849-2860.
39. He HW, Zhang J, Zhou HM, Yan YB, (2005) Conformational change in the C-terminal domain is responsible for the initiation of creatine kinase thermal aggregation. Biophys J 89: 2650-2658.
40. Su JT, Kim SH, Yan YB, (2007) Dissecting the pretransitional conformational changes in aminoacylase I thermal denaturation. Biophys J 92: 578-587.
41. Bushmarina NA, Kuznetsova IM, Biktashev AG, Turoverov KK, Uversky VN, (2001) Partially folded conformations in the folding pathway of bovine carbonic anhydrase II: a fluorescence spectroscopic analysis. ChemBioChem 2: 813-821.
42. Burstein EA, Abornev SM, Reshetnyak YK, (2001) Decomposition of protein tryptophan fluorescence spectra into log-normal components. I. Decomposition algorithms. Biophys J 81: 1699-1709.
43. Papanikolopoulou K, Mills-Henry I, Thol SL, Wang Y, Gross AA, et al. (2008) Formation of amyloid fibrils in vitro by human γD-crystallin and its isolated domains. Mol Vis 14: 81-89.
44. Almarza J, Rincon L, Bahsas A, Brito F, (2009) Molecular mechanism for the denaturation of proteins by urea. Biochemistry 48: 7608-7613.
45. Rosen C, Weber G, (1969) Dimer formation from 1-amino-8-naphthalenesulfonate catalyzed by bovine serum albumin. A new fluorescent molecule with exceptional binding properties. Biochemistry 8: 3915-3920.
46. Reshetnyak YK, Koshevnik Y, Burstein EA, (2001) Decomposition of protein tryptophan fluorescence spectra into log-normal components. III. Correlation between fluorescence and microenvironment parameters of individual tryptophan residues. Biophys J 81: 1735-1758.
47. Kosinski-Collins MS, Flaugh SL, King J, (2004) Probing folding and fluorescence quenching in human γD crystallin Greek key domains using triple tryptophan mutant proteins. Protein Sci 13: 2223-2235.
48. Kosinski-Collins MS, King J, (2003) In vitro unfolding, refolding, and polymerization of human γD crystallin, a protein involved in cataract formation. Protein Sci 12: 480-490.
49. Flaugh SL, Kosinski-Collins MS, King J, (2005) Contributions of hydrophobic domain interface interactions to the folding and stability of human γD-crystallin. Protein Sci 14: 569-581.
50. Pande A, Pande J, Asherie N, Lomakin A, Ogun O, et al. (2000) Molecular basis of a progressive juvenile-onset hereditary cataract. Proc Natl Acad Sci USA 97: 1993-1998.
51. Pande A, Ghosh KS, Banerjee PR, Pande J, (2010) Increase in surface hydrophobicity of the cataract-associated P23T mutant of human γD-crystallin is responsible for its dramatically lower, retrograde solubility. Biochemistry 49: 6122-6129.
52. Banerjee PR, Pande A, Patrosz J, Thurston GM, Pande J, (2011) Cataract-associated mutant E107A of human γD-crystallin shows increased attraction to α-crystallin and enhanced light scattering. Proc Natl Acad Sci USA 108: 574-579.
53. Bera S, Abraham EC, (2002) The αA-crystallin R116C mutant has a higher affinity for forming heteroaggregates with aB-crystallin. Biochemistry 41: 297-305.
54. Wang KJ, Wang S, Cao NQ, Yan YB, Zhu SQ, (2011) A novel mutation in CRYBB1 associated with congenital cataract-microcornea syndrome: the p.Ser129Arg mutation destabilizes the βB1/βA3-crystallin heteromer but not the βB1-crystallin homomer. Hum Mutat 32: E2050-E2060.