Altered aggregation properties of mutant γ-crystallins cause inherited cataract

EMBO Journal

Volumn 21, Issue 22, 2002, Pages 6005-6014

  Sandilands, Aileen ^a   Hutcheson, Aileen M ^a   Long, Heather A ^b   Prescott, Alan R ^a   Vrensen, Gijs ^d   Löster, Jana ^e   Klopp, Norman ^e   Lutz, Raimund B ^e   Graw, Jochen ^e   Masaki, Shigeo ^f   Dobson, Christopher M ^c   MacPhee, Cait E ^c   Quinlan, Roy A ^b  

^a UNIVERSITY OF DUNDEE   (United Kingdom)

^b DURHAM UNIVERSITY   (United Kingdom)

^c UNIVERSITY OF CAMBRIDGE   (United Kingdom)

^d LEIDEN UNIVERSITY MEDICAL CENTER   (Netherlands)

^e INSTITUTE OF EPIDEMIOLOGY   (Germany)

^f INSTITUTE FOR DEVELOPMENTAL RESEARCH   (Japan)

Author keywords

crystallins; Amyloidosis; Protein misfolding

Indexed keywords

AMYLOID; CONGO RED; GAMMA CRYSTALLIN;

ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CATARACTOGENESIS; CONTROLLED STUDY; ELECTRON MICROSCOPY; EMBRYO; GEL PERMEATION CHROMATOGRAPHY; GENE MUTATION; IMMUNOFLUORESCENCE; IN VITRO STUDY; MOUSE; NONHUMAN; PATHOPHYSIOLOGY; PHENOTYPE; PRIORITY JOURNAL; PROTEIN AGGREGATION; PROTEIN EXPRESSION; PROTEIN FOLDING; PROTEIN LOCALIZATION;

AMYLOID; ANIMALS; CATARACT; CELL NUCLEUS; CODON, NONSENSE; EXONS; GAMMA-CRYSTALLINS; INCLUSION BODIES; LENS, CRYSTALLINE; MICE; MICE, INBRED C3H; MICE, MUTANT STRAINS; MUTAGENESIS, INSERTIONAL; PHENOTYPE; POINT MUTATION; PROTEIN FOLDING; RECOMBINANT FUSION PROTEINS; SEQUENCE DELETION;

ANIMALIA; MURINAE;

EID: 18744404774     PISSN: 02614189     EISSN: None     Source Type: Journal    
DOI: 10.1093/emboj/cdf609     Document Type: Article

References (45)

1. Bhat, S.P., Hale, I.L., Matsumoto, B. and Elghanayan, D. (1999) Ectopic expression of αB-crystallin in Chinese hamster ovary cells suggests a nuclear role for this protein. Eur. J. Cell Biol., 78, 143-150.
2. Bradford, M. (1976) A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding. Anal. Biochem., 72, 248-254.
3. Bruijn, L.I., Houseweart, M.K., Kato, S., Anderson, K.L., Anderson, S.D., Ohama, E., Reaume, A.G., Scott, R.W. and Cleveland, D.W. (1998) Aggregation and motor neuron toxicity of an ALS-linked SOD1 mutant independent from wild-type SOD1. Science, 281, 1851-1854.
4. Bucciantini, M. et al. (2002) Inherent toxicity of aggregates implies a common mechanism for protein misfolding diseases. Nature, 416, 507-511.
5. Carter, J.M., Hutcheson, A.M. and Quinlan, R.A. (1995) In vitro studies on the assembly properties of the lens beaded filament proteins: Co-assembly with α-crystallin but not with vimentin. Exp. Eye Res., 60, 181-192.
6. Dahm, R., Gribbon, C., Quinlan, R.A. and Prescott, A.R. (1998) Changes in the nucleolar and coiled body compartments precede lamina and chromatin reorganization during fibre cell denucleation in the bovine lens. Eur. J. Cell Biol., 75, 237-246.
7. DiFiglia, M., Sapp, E., Chase, K.O., Davies, S.W., Bates, G.P., Vonsattel, J.P. and Aronin, N. (1997) Aggregation of huntingtin in neuronal intranuclear inclusions and dystrophic neurites in brain. Science, 277, 1990-1993.
8. Dunah, A.W. et al. (2002) Sp1 and TAFII130 transcriptional activity disrupted in early Huntington's disease. Science, 296. 2238-2243.
9. FitzGerald, P.G. and Graham, D. (1991) Ultrastructural localization of αA-crystallin to the bovine lens fiber cell cytoskeleton. Curr. Eye Res., 10, 417-436.
10. Foster, A. (1999) Cataract - A global perspective: Output, outcome and outlay. Eye, 13, 449-453.
11. Getzoff, E.D., Tainer, J.A., Stempien, M.M., Bell, G.I. and Hallewell, R.A. (1989) Evolution of CuZn superoxide dismutase and the Greek key β-barrel structural motif. Proteins, 5, 322-336.
12. Graw, J. (1999) Mouse models of congenital cataract. Eye, 13, 438-444.
13. Hatters, D.M., Lindner, R.A., Carver, J.A. and Howlett, G.J. (2001) The molecular chaperone, α-crystallin, inhibits amyloid formation by apolipoprotein C-II. J. Biol. Chem., 276, 33755-33761.
14. Head, M.W., Peter, A. and Clayton, R.M. (1991) Evidence for the extralenticular expression of members of the β-crystallin gene family in the chick and a comparison with δ-crystallin during differentiation and transdifferentiation. Differentiation, 48, 147-156.
15. Heon, E., Priston, M., Schorderet, D.F., Billingsley, G.D., Girard, P.O., Lubsen, N. and Munier, F.L. (1999) The γ-crystallins and human cataracts: A puzzle made clearer. Am. J. Hum. Genet., 65, 1261-1267.
16. Horwitz, J. (1992) α-crystallin can function as a molecular chaperone. Proc. Natl Acad. Sci. USA, 89, 10449-10453.
17. Hurle, M.R., Helms, L.R., Li, L., Chan, W. and Wetzel, R. (1994) A role for destabilizing amino acid replacements in light-chain amyloidosis. Proc. Natl Acad. Sci. USA, 91, 5446-5450.
18. Ireland, M.E. et al. (2000) Up-regulation of novel intermediate filament proteins in primary fiber cells: An indicator of all vertebrate lens fiber differentiation? Anat. Rec., 258, 25-33.
19. Jacobson, D.R. and Buxbaum, J.N. (1991) Genetic aspects of amyloidosis. Adv. Hum. Genet., 20, 69-123.
20. Kegel, K.B. et al. (2002) Huntingtin is present in the nucleus, interacts with the transcriptional corepressor C-terminal binding protein and represses transcription. J. Biol. Chem., 277, 7466-7476.
21. Klopp, N. et al. (1998) Three murine cataract mutants (Cat2) are defective in different γ-crystallin genes. Genomics, 52, 152-158.
22. Klopp, N., Löster, J. and Graw, J. (2001) Characterization of a 1-bp deletion in the γE-crystallin gene leading to a nuclear and zonular cataract in the mouse. Invest. Ophthalmol. Vis. Sci., 42, 183-187.
23. Kmoch, S. 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.
24. Laemmli, U. (1970) Cleavage of structural proteins during the assembly of the head of bacteriophage T4. Nature, 277, 680-685.
25. Lashuel, H.A., Wurth, C., Woo, L. and Kelly, J.W. (1999) The most pathogenic transthyretin variant, L55P, forms amyloid fibrils under acidic conditions and protofilaments under physiological conditions. Biochemistry, 38, 13560-13573.
26. LeVine, H., III (1999) Quantification of β-sheet amyloid fibril structures with thioflavin T. Methods Enzymol., 309, 274-284.
27. Linke, R.P. (2000) Highly sensitive diagnosis of amyloid and various amyloid syndromes using Congo red fluorescence. Virchows Arch., 436, 439-448.
28. McGowan, D.P., van Roon-Mom, W., Holloway, H., Bates, G.P., Mangiarini, L., Cooper, G.J., Faull, R.L. and Snell, R.G. (2000) Amyloid-like inclusions in Huntington's disease. Neuroscience, 100, 677-680.
29. Nicholl, I.D. and Quinlan, R.A. (1994) Chaperone activity of α-crystallins modulates intermediate filament assembly. EMBO J., 13, 945-953.
30. Pande, A., Pande, J., Asherie, N., Lomakin, A., Ogun, O., King, J. and Benedek, G.B. (2001) Crystal cataracts: Human genetic cataract caused by protein crystallization. Proc. Natl Acad. Sci. USA, 98, 6116-6120.
31. Pepys, M.B. (2001) Pathogenesis, diagnosis and treatment of systemic amyloidosis. Philos. Trans. R. Soc. Lond. B Biol. Sci., 356, 203-211.
32. Perng, M.D., Cairns, L., van den IJssel, P., Prescott, A., Hutcheson, A.M. and Quinlan, R.A. (1999a) Intermediate filament interactions can be altered by HSP27 and αB-crystallin. J. Cell Sci., 112, 2099-2112.
33. Perng, M.D., Muchowski, P.J., van den IJssel, P., Wu, G.J.S., Clark, J.I. and Quinlan, R.A. (1999b) The cardiomyopathy and lens cataract mutation in αB-crystallin compromises secondary, tertiary and quaternary protein structure and reduces in vitro chaperone activity. J. Biol. Chem., 274, 33235-33243.
34. Ray, M.E., Wistow, G., Su, Y.A., Meltzer, P.S. and Trent, J.M. (1997) AIM1, a novel non-lens member of the βγ-crystallin superfarmily, is associated with the control of tumorigenicity in human malignant melanoma. Proc. Natl Acad. Sci. USA, 94, 3229-3234.
35. Sandilands, A., Prescott, A.R., Carter, J.M., Hutcheson, A.M., Quinlan, R.A., Richards, J. and FitzGerald, P.G. (1995) Vimentin and CP49/filensin form distinct networks in the lens which are independently modulated during lens fibre cell differentiation. J. Cell Sci., 108, 1397-1406.
36. Santhiya, S.T., Shyam Manohar, M., Rawlley, D., Vijayalakshmi, P., Namperumalsamy, P., Gopinath, P.M., Löster, J. and Graw, J. (2002) Novel mutations in the γ-crystallin genes cause autosomal dominant congenital cataracts. J. Med. Genet., 39, 352-358.
37. Sisodia, S.S. (1998) Nuclear inclusions in glutamine repeat disorders: Are they pernicious, coincidental, or beneficial? Cell, 95, 1-4.
38. Stege, G.J., Renkawek, K., Overkamp, P.S., Verschuure, P., van Rijk, A.F., Reijnen-Aalbers, A., Boelens, W.C., Bosman, G.J. and de Jong, W.W. (1999) The molecular chaperone αB-crystallin enhances amyloid β neurotoxicity. Biochem. Biophys. Res. Commun., 262, 152-156.
39. Stokes, G. (1976) An improved Congo red method for amyloid. Med. Lab. Sci., 33, 79-80.
40. Suhr, S.T., Senut, M.C., Whitelegge, J.P., Faull, K.F., Cuizon, D.B. and Gage, F.H. (2001) Identities of sequestered proteins in aggregates from cells with induced polyglutamine expression. J. Cell Biol., 153, 283-294.
41. Teichmann, U., Ray, M.E., Ellison, J., Graham, C., Wistow, G., Meltzer, P.S., Trent, J.M. and Pavan W.J. (1998) Cloning and tissue expression of the mouse ortholog of AIM1, a βγ-crystallin superfamily member. Mamm. Genome, 9, 715-720.
42. Walsh, D.M., Klyubin, I., Fadeeva, J.V., Cullen, W.K., Anwyl, R., Wolfe, M.S., Rowan, M.J. and Selkoe, D.J. (2002) Naturally secreted oligomers of amyloid β protein potently inhibit hippocampal long-term potentiation in vivo. Nature, 416, 535-539.
43. Warrick, J.M., Paulson, H.L., Gray-Board, G.L., Bui, Q.T., Fischbeck, K.H., Pittman, R.N. and Bonini, N.M. (1998) Expanded polyglutamine protein forms nuclear inclusions and causes neural degeneration in Drosophila. Cell, 93, 939-949.
44. Wigle, J.T., Chowdhury, K., Gruss, P. and Oliver, G. (1999) Prox1 function is crucial for mouse lens-fibre elongation. Nat. Genet., 21, 318-322.
45. Wyttenbach, A., Sauvageot, O., Carmichael, J., Diaz-Latoud, C., Arrigo, A.P. and Rubinsztein, D.C. (2002) Heat shock protein 27 prevents cellular polyglutamine toxicity and suppresses the increase of reactive oxygen species caused by huntingtin. Hum. Mol. Genet., 11, 1137-1151.