Contributions of hydrophobic domain interface interactions to the folding and stability of human γD-crystallin

Protein Science

Volumn 14, Issue 3, 2005, Pages 569-581

  Flaugh, Shannon L ^a   Kosinski Collins, Melissa S ^a   King, Jonathan ^a  

^a MASSACHUSETTS INSTITUTE OF TECHNOLOGY   (United States)

Author keywords

Cataract; Domain interface; Equilibrium unfolding refolding transitions; Human D crystallin; Hydrophobic interactions; Partially folded intermediate

Indexed keywords

AMINO ACID; GAMMA CRYSTALLIN; GUANIDINE; LENS PROTEIN; MUTANT PROTEIN;

AMINO ACID SUBSTITUTION; AMINO TERMINAL SEQUENCE; ARTICLE; CARBOXY TERMINAL SEQUENCE; CLUSTER ANALYSIS; CONFORMATIONAL TRANSITION; HUMAN; HYDROPHOBICITY; KINETICS; LENS NUCLEUS; MUTATIONAL ANALYSIS; PRIORITY JOURNAL; PROTEIN ANALYSIS; PROTEIN DOMAIN; PROTEIN FOLDING; PROTEIN PROTEIN INTERACTION; PROTEIN PURIFICATION; PROTEIN STABILITY; PROTEIN STRUCTURE; STRUCTURE ACTIVITY RELATION; THERMODYNAMICS; WILD TYPE;

CIRCULAR DICHROISM; GAMMA-CRYSTALLINS; HUMANS; HYDROPHOBICITY; MUTATION; PROTEIN DENATURATION; PROTEIN FOLDING; PROTEIN RENATURATION; PROTEIN STRUCTURE, TERTIARY; SPECTROMETRY, FLUORESCENCE;

EID: 14144250992     PISSN: 09618368     EISSN: None     Source Type: Journal    
DOI: 10.1110/ps.041111405     Document Type: Article

References (53)

1. Andley, U.P., Mathur, S., Griest, T.A., and Petrash, J.M. 1996. Cloning, expression, and chaperone-like activity of human αA-crystallin. J. Biol. Chem. 271: 31973-31980.
2. Basak, A., Bateman, O., Slingsby, C., Pande, A., Asherie, N., Ogun, O., Benedek, G.B., and Pande, J. 2003. High-resolution X-ray crystal structures of human γD crystallin (1.25Å) and the R58H mutant (1.15Å) associated with aculeiform cataract. J. Mol. Biol. 328: 1137-1147.
3. Bateman, O.A., Sarra, R., van Genesen, S.T., Kappe, G., Lubsen, N.H., and Slingsby, C. 2003. The stability of human acidic β-crystallin oligomers and hetero-oligomers. Exp. Eye Res. 77: 409-422.
4. Bax, B., Lapatto, R., Nalini, V., Driessen, H., Lindley, P.F., Mahadevan, D., Blundell, T.L., and Slingsby, C. 1990. X-ray analysis of β B2-crystallin and evolution of oligomeric lens proteins. Nature 347: 776-780.
5. Beechem, J.M., Sherman, M.A., and Mas, M.T. 1995. Sequential domain unfolding in phosphoglycerate kinase: Fluorescence intensity and anisotropy stopped-flow kinetics of several tryptophan mutants. Biochemistry 34: 13943-13948.
6. Beeser, S.A., Goldenberg, D.P., and Oas, T.G. 1997. Enhanced protein flexibility caused by a destabilizing amino acid replacement in BPTI. J. Mol. Biol. 269: 154-164.
7. Booth, D.R., Sunde, M., Bellotti, V., Robinson, C.V., Hutchinson, W.L., Fraser, P.E., Hawkins, P.N., Dobson, C.M., Radford, S.E., Blake, C.C., et al. 1997. Instability, unfolding and aggregation of human lysozyme variants underlying amyloid fibrillogenesis. Nature 385: 787-793.
8. Boyle, D. and Takemoto, L. 1994. Characterization of the α-γy and α-β complex: Evidence for an in vivo functional role of α-crystallin as a molecular chaperone. Exp. Eye Res. 58: 9-15.
9. Clark, A.C., Sinclair, J.F., and Baldwin, T.O. 1993. Folding of bacterial luciferase involves a non-native heterodimeric intermediate in equilibrium with the native enzyme and the unfolded subunits. J. Biol. Chem. 268: 10773-10779.
10. Clark, P.L., Weston, B.F., and Gierasch, L.M. 1998. Probing the folding pathway of a β-clam protein with single-tryptophan constructs. Fold Des. 3: 401-412.
11. Delaye, M. and Tardieu, A. 1983. Short-range order of crystallin proteins accounts for eye lens transparency. Nature 302: 415-417.
12. 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.
13. Fernald, R.D. and Wright, S.E. 1983. Maintenance of optical quality during crystalline lens growth. Nature 301: 618-620.
14. Greene Jr., R.F. and Pace, C.N. 1974. Urea and guanidine hydrochloride denaturation of ribonuclease, lysozyme, α-chymotrypsin, and β-lactoglobulin. J. Biol. Chem. 249: 5388-5393.
15. Hanson, S.R., Smith, D.L., and Smith, J.B. 1998. Deamidation and disulfide bonding in human lens γ-crystallins. Exp. Eye Res. 67: 301-312.
16. Hanson, S.R., Hasan, A., Smith, D.L., and Smith, J.B. 2000. The major in vivo modifications of the human water-insoluble lens crystallins are disulfide bonds, deamidation, methionine oxidation and backbone cleavage. Exp. Eye Res. 71: 195-207.
17. 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.
18. Hoenders, H.J. and Bloemendal, H. 1983. Lens proteins and aging. J. Gerontol. 38: 278-286.
19. Hope, J.N., Chen, H.C., and Hejtmancik, J.F. 1994. Aggregation of β A3-crystallin is independent of the specific sequence of the domain connecting peptide. J. Biol. Chem. 269: 21141-21145.
20. Horwitz, J. 1992. α-crystallin can function as a molecular chaperone. Proc. Natl. Acad. Sci. 89: 10449-10453.
21. Jaenicke, R. 1999. Stability and folding of domain proteins. Prog. Biophys. Mol. Biol. 71: 155-241.
22. Jiang, X., Smith, C.S., Petrassi, H.M., Hammarstrom, P., White, J.T., Sacchettini, J.C., and Kelly, J.W. 2001. An engineered transthyretin monomer that is nonamyloidogenic, unless it is partially denatured. Biochemistry 40: 11442-11452.
23. Jones, S., Marin, A., and Thornton, J.M. 2000. Protein domain interfaces: Characterization and comparison with oligomeric protein interfaces. Protein Eng. 13: 77-82.
24. Kim, Y.H., Kapfer, D.M., Boekhorst, J., Lubsen, N.H., Bachinger, H.P., Shearer, T.R., David, L.L., Feix, J.B., and Lampi, K.J. 2002. Deamidation, but not truncation, decreases the urea stability of a lens structural protein, βB1-crystallin. Biochemistry 41: 14076-14084.
25. Kosinski-Collins, M.S. and King, J. 2003. In vitro unfolding, refolding, and polymerization of human γD crystallin, a protein involved in cataract formation. Protein Sci. 12: 480-490.
26. Kosinski-Collins, M.S., Flaugh, S.L., and 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.
27. Lampi, K.J., Ma, Z., Shih, M., Shearer, T.R., Smith, J.B., Smith, D.L., and David, L.L. 1997. Sequence analysis of βA3, βB3, and βA4 crystallins completes the identification of the major proteins in the young human lens. J. Biol. Chem. 272: 2268-2275.
28. Lampi, K.J., Kim, Y.H., Bachinger, H.P., Boswell, B.A., Lindner, R.A., Carver, J.A., Shearer, T.R., David, L.L., and Kapfer, D.M. 2002. Decreased heat stability and increased chaperone requirement of modified human βB1-crystallins. Mol. Vis. 8: 359-366.
29. Lapatto, R., Nalini, V., Bax, B., Driessen, H., Lindley, P.F., Blundell, T.L., and Slingsby, C. 1991. High resolution structure of an oligomeric eye lens β-crystallin. Loops, arches, linkers and interfaces in β B2 dimer compared to a monomeric γ-crystallin. J. Mol. Biol. 222: 1067-1083.
30. Liang, J.J. 2004. Interactions and chaperone function of αA-crystallin with T5P γC-crystallin mutant. Protein Sci. 13: 2476-2482.
31. Mayr, E.M., Jaenicke, R., and Glockshuber, R. 1994. Domain interactions and connecting peptides in lens crystallins. J. Mol. Biol. 235: 84-88.
32. _. 1997. The domains in γB-crystallin: Identical fold-different stabilities. J. Mol. Biol. 269: 260-269.
33. Mitraki, A. and King, J. 1989. Protein folding intermediates and inclusion body formation. Biotechnology 7: 690-697.
34. National Eye Institute (U.S.) 2002. "Vision problems in the U.S." Prevent Blindness in America, Bethesda, MD.
35. Nicholson, E.M., Mo, H., Prusiner, S.B., Cohen, F.E., and Marqusee, S. 2002. Differences between the prion protein and its homolog Doppel: A partially structured state with implications for scrapie formation. J. Mol. Biol. 316: 807-815.
36. Oyster, C.W. 1999. The human eye: Structure and function., Chap. 12. Sinauer Associates, Inc., Sunderland, MA.
37. Palme, S., Slingsby, C., and Jaenicke, R. 1997. Mutational analysis of hydrophobic domain interactions in γB-crystallin from bovine eye lens. Protein Sci. 6: 1529-1536.
38. Palme, S., Jaenicke, R., and Slingsby, C. 1998. X-ray structures of three interface mutants of γB-crystallin from bovine eye lens. Protein Sci. 7: 611-618.
39. Pande, A., Pande, J., Asherie, N., Lomakin, A., Ogun, O., King, J.A., Lubsen, N.H., Walton, D., and Benedek, G.B. 2000. Molecular basis of a progressive juvenile-onset hereditary cataract. Proc. Natl. Acad. Sci. 97: 1993-1998.
40. 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. 98: 6116-6120.
41. Rose, G.D., Geselowitz, A.R., Lesser, G.J., Lee, R.H., and Zehfus, M.H. 1985. Hydrophobicity of amino acid residues in globular proteins. Science 229: 834-838.
42. Santhiya, S.T., Shyam Manohar, M., Rawlley, D., Vijayalakshmi, P., Namperumalsamy, P., Gopinath, P.M., Loster, J., and Graw, J. 2002. Novel mutations in the γ-crystallin genes cause autosomal dominant congenital cataracts. J. Med. Genet. 39: 352-358.
43. Sathish, H.A., Koteiche, H.A., and McHaourab, H.S. 2004. Binding of destabilized βB2-crystallin mutants to α-crystallin: The role of a folding intermediate. J. Biol. Chem. 279: 16425-16432.
44. Sharma, A.K., Minke-Gogl, V., Gohl, P., Siebendritt, R., Jaenicke, R., and Rudolph, R. 1990. Limited proteolysis of γ II-crystallin from calf eye lens. Physicochemical studies on the N-terminal domain and the intact two-domain protein. Eur. J. Biochem. 194: 603-609.
45. Sherman, M.A., Beechem, J.M., and Mas, M.T. 1995. Probing intradomain and interdomain conformational changes during equilibrium unfolding of phosphoglycerate kinase: Fluorescence and circular dichroism study of tryptophan mutants. Biochemistry 34: 13934-13942.
46. Slingsby, C., Norledge, B., Simpson, A., Bateman, O.A., Wright, G., Driessen, H.P.C., Lindley, P.F., Moss, D.S., and Bax, B. 1997. X-ray diffraction and structure of crystallins. Prog. Ret. and Eye Res. 16: 3-29.
47. Trinkl, S., Glockshuber, R., and Jaenicke, R. 1994. Dimerization of β B2-crystallin: The role of the linker peptide and the N- and C-terminal extensions. Protein Sci. 3: 1392-1400.
48. Wenk, M., Herbst, R., Hoeger, D., Kretschmar, M., Lubsen, N.H., and Jaenicke, R. 2000. γ S-crystallin of bovine and human eye lens: Solution structure, stability and folding of the intact two-domain protein and its separate domains. Biophys. Chem. 86: 95-108.
49. Westermark, P., Sletten, K., Johansson, B., and Cornwell 3rd, G.G. 1990. Fibril in senile systemic amyloidosis is derived from normal transthyretin. Proc. Natl. Acad. Sci. 87: 2843-2845.
50. Wetzel, R. 1994. Mutations and off-pathway aggregation of proteins. Trends Biotechnol. 12: 193-198.
51. Wieligmann, K., Mayr, E.M., and Jaenicke, R. 1999. Folding and self-assembly of the domains of βB2-crystallin from rat eye lens. J. Mol. Biol. 286: 989-994.
52. Wistow, G., Turnell, B., Summers, L., Slingsby, C., Moss, D., Miller, L., Lindley, P., and Blundell, T. 1983. X-ray analysis of the eye lens protein γ-II crystallin at 1.9Å resolution. J. Mol. Biol. 170: 175-202.
53. Zhou, H. and Zhou, Y. 2004. Quantifying the effect of burial of amino acid residues on protein stability. Proteins 54: 315-322.