Insights into the origin of the tendency of the PI3-SH3 domain to form amyloid fibrils

Journal of Molecular Biology

Volumn 322, Issue 5, 2002, Pages 1147-1158

  Ventura, Salvador ^a   Lacroix, Emmanuel ^a   Serrano, Luis ^a  

^a EUROPEAN MOLECULAR BIOLOGY LABORATORY   (Germany)

Author keywords

Amyloid formation; Conformational stability; Protein engineering; Protein folding; SH3 domain

Indexed keywords

AMYLOID; PROTEIN TYROSINE KINASE; SPECTRIN;

AMINO ACID SEQUENCE; ARTICLE; BETA SHEET; CHIMERA; COMPARATIVE STUDY; FIBER; IN VITRO STUDY; PH; PRIORITY JOURNAL; PROTEIN AGGREGATION; PROTEIN DOMAIN; SOLUBILITY;

EID: 0036411969     PISSN: 00222836     EISSN: None     Source Type: Journal    
DOI: 10.1016/S0022-2836(02)00783-0     Document Type: Article

References (41)

1. Tan, S. Y. & Pepys, M. B. (1994). Amyloidosis. Histopathology, 25, 403-414.
2. Sunde, M. & Blake, C. C. (1998). From the globular to the fibrous state: protein structure and structural conversion in amyloid formation. Quart. Rev. Biophys. 31, 1-39.
3. Dobson, C. M. (2001). The structural basis of protein folding and its links with human disease. Phil. Trans. Roy. Soc. Lond. 356, 133-146.
4. Guijarro, J. I., Sunde, M., Jones, J. A., Campbell, I. D. & Dobson, C. M. (1998). Amyloid fibril formation by an SH3 domain. Proc. Natl Acad. Sci. USA, 95, 4224-4228.
5. Dobson, C. M. (1999). Protein misfolding, evolution and disease. Trends Biochem. Sci. 24, 329-332.
6. Mayer, B. J. (2001). SH3 domains: complexity in moderation. J. Cell. Sci. 114, 1253-1263.
7. Guijarro, J. I., Morton, C. J., Plaxco, K. W., Campbell, I. D. & Dobson, C. M. (1998). Folding kinetics of the SH3 domain of PI3 kinase by real-time NMR combined with optical spectroscopy. J. Mol. Biol. 276, 657-667.
8. Plaxco, K. W., Guijarro, J. I., Morton, C. J., Pitkeathly, M., Campbell, I. D. & Dobson, C. M. (1998). The folding kinetics and thermodynamics of the Fyn-SH3 domain. Biochemistry, 37, 2529-2537.
9. Grantcharova, V. P. & Baker, D. (1997). Folding dynamics of the src SH3 domain. Biochemistry, 36, 15685-15692.
10. Viguera, A. R., Martinez, J. C., Filimonov, V. V., Mateo, P. L. & Serrano, L. (1994). Thermodynamic and kinetic analysis of the SH3 domain of spectrin shows a two-state folding transition. Biochemistry, 33, 2142-2150.
11. Filimonov, V. V., Azuaga, A. I., Viguera, A. R., Serrano, L. & Mateo, P. L. A. (1999). Thermodynamic analysis of a family of small globular proteins: SH3 domains. Biophys. Chem. 77, 195-208.
12. Grantcharova, V. P., Riddle, D., Santiago, J. V. & Baker, D. (1998). Important role of hydrogen bonds in the structurally polarized transition state for folding of the src SH3 domain. Nature Struct. Biol. 5, 714-720.
13. Rath, A. & Davidson, A. R. (2000). The design of a hyperstable mutant of the Abp1p SH3 domain by sequence alignment analysis. Protein Sci. 9, 2457-2469.
14. Chen, Y. J., Lin, S. C., Tzeng, S. R., Patel, H. V., Lyu, P. C., Cheng, J. W. et al. (1996). Stability and folding of the SH3 domain of Bruton's tyrosine kinase. Proteins: Struct. Funct. Genet. 26, 465-471.
15. Lim, W. A., Fox, R. O. & Richards, F. M. (1994). Stability and peptide binding affinity of an SH3 domain from the Caenorhabditis elegans signaling protein Sem-5. Protein Sci. 3, 1261-1266.
16. Zhang, O., Kay, L. E., Olivier, J. P. & Forman-Kay, J. D. (1994). Backbone 1H and 15N resonance assignments of the N-terminal SH3 domain of drk in folded and unfolded states using enhanced-sensitivity pulsed field gradient NMR techniques. J. Biomol. NMR, 4, 845-858.
17. Zurdo, J., Guijarro, J. I., Jimenez, J. L., Saibil, H. R. & Dobson, C. M. (2001). Dependence on solution conditions of aggregation and amyloid formation by an SH3 domain. J. Mol. Biol. 311, 325-340.
18. Otzen, D. E., Kristensen, O. & Oliveberg, M. (2000). Designed protein tetramer zipped together with a hydrophobic Alzheimer homology: a structural clue to amyloid assembly. Proc. Natl Acad. Sci. USA, 97, 9907-9912.
19. Lacroix, E. (1999). PhD Thesis. Protein Design: a Computer-based Approach. Universite Libre de Bruxelles.
20. Fisinger, S., Serrano, L. & Lacroix, E. (2001). Computational estimation of specific side chain interaction energies in alpha helices. Protein Sci. 10, 809-818.
21. López de la Paz', M., Lacroix, E., Ramírez-Alvarado, M. & Serrano, L. (2001). De novo automatic design of β-sheet model peptides. J. Mol. Biol. 312, 229-246.
22. Martinez, J. C. & Serrano, L. (1999). The folding transition-state between SH3 domains is conformationally restricted and evolutionarily conserved. Nature Struct. Biol. 6, 1010-1016.
23. Myers, J. K., Pace, C. N. & Scholtz, J. M. (1995). Denaturant m values and heat capacity changes: relation to changes in accessible surface areas of protein unfolding. Protein Sci. 4, 2138-2148.
24. Semisotnov, G. V., Rodionova, N. A., Razgulyaev, O. I., Uversky, V. N., Gripas', A. F. & Gilmanshin, R. I. (1991). Study of the "molten globule" intermediate state in protein folding by a hydrophobic fluorescent probe. Biopolymers, 31, 119-128.
25. Sholtz, J. M. & Baldwin, R. L. (1993). Perchlorate-induced denaturation of ribonuclease-A: investigation of possible folding intermediates. Biochemistry, 32, 4604-4608.
26. Klunk, W. E., Pettegrew, J. W. & Abraham, D. J. (1989). Quantitative evaluation of Congo Red binding to amyloid-like proteins with a beta-pleated sheet conformation. J. Histochem. Cytochem. 37, 1273-1281.
27. Balbirnie, M., Grothe, R. & Eisenberg, D. S. (2001). An amyloid-forming peptide from the yeast prion Sup35 reveals a dehydrated beta-sheet structure for amyloid. Proc. Natl Acad. Sci. USA, 98, 2375-2380.
28. McParland, V. J., Kad, N. M., Kalverda, A. P., Brown, A., Kirwin-Jones, P., Hunter, M. G. et al. (2000). Partially unfolded states of beta(2)-microglobulin and amyloid formation in vitro. Biochemistry, 39, 8735-8746.
29. Grantcharova, V. P., Riddle, D. S., Santiago, J. V. & Baker, D. (1998). Important role of hydrogen bonds in the structurally polarized transition state for folding of the src SH3 domain. Nature Struct. Biol. 5, 714-720.
30. Plaza del Pino, I. M., Ibarra-Molero, B. & Sanchez-Ruiz, J. M. (2000). Lower kinetic limit to protein thermal stability: a proposal regarding protein stability in vivo and its relation with misfolding diseases. Proteins: Struct. Funct. Genet. 40, 58-70.
31. Canet, D., Sunde, M., Last, A. M., Miranker, A., Spencer, A., Robinson, C. V. & Dobson, C. M. (1999). Mechanistic studies of the folding of human lysozyme and the origin of amyloidogenic behavior in its disease-related variants. Biochemistry, 38, 6419-6427.
32. Guerois, R. & Serrano, L. (2001). Protein design based on folding models. Curr. Opin. Struct. Biol. 11, 101-106. Review.
33. Guerois, R. & Serrano, L. (2000). The SH3-fold family: experimental evidence and prediction of variations in the folding pathways. J. Mol. Biol. 304, 967-982.
34. Koehl, P. & Delarue, M. (1994). Application of a self-consistent mean field theory to predict protein side-chains conformation and estimate their conformational entropy. J. Mol. Biol. 239, 249-275.
35. Momani, F. A., McGuire, R. F., Burgess, A. W. & Scheraga, H. A. (1975). Energy parameters in polypeptides. VII geometric parameters, partial atomic charges, nonbonded interactions, hydrogen bond interactions and intrinsic torsional potentials for the naturally occurring amino acids. J. Phys. Chem. 79, 2361-2381.
36. Nemethy, G., Pottle, M. S. & Scheraga, H. A. (1983). Updating of geometrical parameters, nonbonded interactions and hydrogen bond interactions for the naturally occurring amino acids. J. Phys. Chem. 87, 1883-1887.
37. Street, A. G. & Mayo, S. L. (1998). Pairwise calculation of protein solvent-accessible surface areas. Fold. Des. 3, 253-258.
38. Eisenberg, D. & McLachlan, A. D. (1986). Solvation energy in protein folding and binding. Nature, 319, 199-203.
39. Eisenhaber, F., Lijnzaad, P., Argos, P., Sander, C. & Scharf, M. (1995). The double cubic lattice method: efficient approaches to numerical integration of surface area and volume and to dot surface contouring of molecular assemblies. J. Comp. Chem. 16, 273-284.
40. Muñoz, V. & Serrano, L. (1994). Intrinsic secondary structure propensities of the amino acids, using statistical phi-psi matrices: comparison with experimental scales. Proteins: Struct. Funct. Genet. 20, 301-311.
41. Mossakowska, D. E., Nyberg, K. & Fersht, A. R. (1989). Kinetic characterization of the recombinant ribonuclease from Bacillus amyloliquefaciens (barnase) and investigation of key residues in catalysis by site-directed mutagenesis. Biochemistry, 28, 3843-3850.