Mutations in the B1 domain of protein G that delay the onset of amyloid fibril formation in vitro

Protein Science

Volumn 12, Issue 3, 2003, Pages 567-576

  Ramírez Alvarado, Marina ^a,b   Cocco, Melanie J ^a   Regan, Lynne ^a  

^a YALE UNIVERSITY   (United States)

^b MAYO CLINIC   (United States)

Author keywords

Amyloid; Amyloid kinetics; Fluorescence; Light scattering; NMR; Protein G B1 domain; Sodium sulfate

Indexed keywords

AMYLOID; BINDING PROTEIN; IMMUNOGLOBULIN G; PROTEIN G; SODIUM SULFATE;

ARTICLE; FLUORESCENCE; IN VITRO STUDY; KINETICS; LIGHT SCATTERING; MUTATION; NUCLEAR MAGNETIC RESONANCE; PRIORITY JOURNAL; PROTEIN DOMAIN; STREPTOCOCCUS;

AMYLOID; BACTERIAL PROTEINS; FLUORESCENCE; HUMANS; MAGNETIC RESONANCE SPECTROSCOPY; MASS SPECTROMETRY; MICROSCOPY, ELECTRON; MUTATION; STREPTOCOCCUS; THIAZOLES;

STREPTOCOCCUS;

EID: 0037369167     PISSN: 09618368     EISSN: None     Source Type: Journal    
DOI: 10.1110/ps.0227403     Document Type: Article

References (60)

1. Alexander, P., Fahnestock, S., Lee, T., Orban, J., and Bryan, P. 1992a. Thermodynamic analysis of the folding of the streptococcal protein G IgG-binding domains B1 and B2: Why small proteins tend to have high denaturation temperatures. Biochemistry 31: 3597-3603.
2. Alexander, P., Orban, J., and Bryan, P. 1992b. Kinetic analysis of folding and unfolding the 56 amino acid IgG-binding domain of streptococcal protein G. Biochemistry 31: 7243-7248.
3. Altieri, A.S. and Byrd, R.A. 1995. Randomization approach to water suppression in multidimensional NMR using pulsed field gradients. J. Magn. Reson. B. 107: 260-266.
4. Blake, C. and Serpell, L. 1996. Synchrotron X-ray studies suggests that the core of the transthyretin amyloid fibril is a continuous β-sheet helix. Structure 4: 989-998.
5. 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.
6. Bucciantini, M., Giannoni, E., Chiti, F., Baroni, F., Formigli, L., Zurdo, J., Taddei, N., Ramponi, G., Dobson, C.M., and Stefani, M. 2002. Inherent toxicity of aggregates implies a common mechanism for protein misfolding diseases. Nature 416: 507-511.
7. Canet, D., Sunde, M., Last, A.M., Miranker, A., Spencer, A., Robinson. C.V., and 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.
8. Canet, D., Last, A.M., Tito, P., Sunde, M., Spencer, A., Archer, D.B., Redfield, C., Robinson, C.V., and Dobson, C.M. 2002. Local cooperativity in the unfolding of an amyloidogenic variant of human lysozyme. Nat. Struct. Biol. 9: 308-315.
9. Carrell, R.W. and Lomas, D.A. 1997. Conformational disease. Lancet 350: 134-138.
10. Chiti, F., Webster, P., Taddei, N., Clark, A., Stefani, M., Ramponi, G., and Dobson, C.M. 1999. Designing conditions for in vitro formation of amyloid protofilaments and fibrils. Proc. Natl. Acad. Sci. 96: 3590-3594.
11. Chiti, F., Mangione, P., Andreola, A., Giorgetti, S., Stefani, M., Dobson, C.M., Bellotti, V., and Taddei, N. 2001. Detection of two partially structured species in the folding process of the amyloidogenic protein β2-microglobulin. J. Mol. Biol. 307: 379-391.
12. Damas, A.M., Ribeiro, S., Lamzin, V.S., Palha, J.A., and Saraiva, M.J. 1996. Structure of Val122Ile variant transthyretin - A cardiomyopathic mutant. Acta Crystallogr. D Biol. Crystallogr. 52: 966-972.
13. Delaglio, F., Grzesiek, S., Vuister, G.W., Zhu, G., Pfeifer, J., and Bax, A. 1995. NMRPipe: A multidimensional spectral processing system based on UNIX pipes. J. Biomol. NMR 6: 277-293.
14. Esturau, N., Sanchez- Ferrando, F., Gavin, J.A., Roumestand, C., Delsuc, M.A., and Parella, T. 2001. The use of sample rotation for minimizing convection effects in self-diffusion NMR measurements. J. Magn. Reson. 153: 48-55.
15. Fandrich, M., Fletcher, M.A., and Dobson, C.M. 2001. Amyloid fibrils from muscle myoglobin. Nature 410: 165-166.
16. Ferguson, N., Capaldi, A.P., James, R., Kleanthous, C., and Radford, S.E. 1999. Rapid folding with and without populated intermediates in the homologous four-helix proteins Im7 and Im9. J. Mol. Biol. 286: 1597-608.
17. Gallagher, T., Alexander, P., Bryan, P., and Gilliland, G.L. 1994. Two crystal structures of the B1 immunoglobulin-binding domain of streptococcal protein G and comparison with NMR. Biochemistry 33: 4721-4729.
18. Gronenborn, A.M., Filpula, D.R., Essig, N.Z., Achari, A., Whitlow, M., Wingfield, P.T., and Clore, G.M. 1991. A novel, highly stable fold of the immunoglobulin binding domain of streptococcal protein G. Science 253: 657-661.
19. Gross, M., Wilkins, D.K., Pitkeathly, M.C., Chung, E.W., Higham, C., Clark, A., and Dobson, C.M. 1999. Formation of amyloid fibrils by peptides derived from the bacterial cold shock protein CspB. Protein Sci. 8: 1350-1357.
20. Guijarro, J.I., Sunde, M., Jones, J.A., Campbell, I.D., and Dobson, C.M. 1998. Amyloid fibril formation by an SH3 domain. Proc. Natl. Acad. Sci. 95: 4224-4228.
21. Hamilton, J.A., Steinrauf, L.K., Braden, B.C., Liepnieks, J., Benson, M.D., Holmgren, G., Sandgren, O., and Steen, L. 1993. The x-ray crystal structure refinements of normal human transthyretin and the amyloidogenic Val-30 → Met variant to 1.7Å resolution. J. Biol. Chem. 268: 2416-2424.
22. Harper, J.D., Wong, S.S., Lieber, C.M., and Lansbury, Jr., P.T. 1999. Assembly of Ab amyloid protofibrils: An in vitro model for a possible early event in Alzheimer's disease. Biochemistry 38: 8972-8980.
23. Hoyer, S. 1993. Brain oxidative energy and related metabolism, neuronal stress and Alzheimer's disease: A speculative synthesis. J. Geriatr. Psychiatry Neurol. 6: 3-13.
24. 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. 91: 5446-5450.
25. Jimenez, J.L., Guijarro, J.I., Orlova, E., Zurdo, J., Dobson, C.M., Sunde, M., and Saibil, H.R. 1999. Cryo-electron microscopy structure of an SH3 amyloid fibril and model of the molecular packing. EMBO J. 18: 815-821.
26. Kelly, J.W. 1996. Alternative conformations of amyloidogenic proteins govern their behavior. Curr. Opin. Struct. Biol. 6: 11-17.
27. -. 1998. The alternative conformations of amyloidogenic proteins and their multistep assembly pathways. Curr. Opin. Struct. Biol. 8: 101-106.
28. Kelly, J.W. and Lansbury, P.T. 1994. A chemical approach to elucidate the mechanism of transthyretin and β-protein amyloid fibril formation. Amyloid 1: 186-205.
29. Konno, T., Murata, K., and Nagayama, K. 1999. Amyloid-like aggregates of a plant protein: A case of a sweet-tasting protein, monellin. FEBS Lett. 454: 122-126.
30. Krebs, M.R., Wilkins, D.K., Chung, E.W., Pitkeathly, M.C., Chamberlain, A.K., Zurdo, J., Robinson, C.V., and Dobson, C.M. 2000. Formation and seeding of amyloid fibrils from wild-type hen lysozyme and a peptide fragment from the β-domain. J. Mol. Biol. 300: 541-549.
31. Lai, Z., Colon, W., and Kelly, J.W. 1996. The acid-mediated denaturation pathway of transthyretin yields a conformational intermediate that can self-assemble into amyloid. Biochemistry 35: 6470-6482.
32. Lansbury, Jr., P.T. 1999. Evolution of amyloid: What normal protein folding may tell us about fibrillogenesis and disease. Proc. Natl. Acad. Sci. 96: 3342-3344.
33. Lapham, J., Rife, J.P., Moore, P.B., and Crothers, D.M. 1997. Measurement of diffusion constants for nucleic acids by NMR. J. Biomol. NMR. 10: 255-262.
34. Le Vine, H. 1993. Thioflavine T interaction with synthetic Alzheimer's disease β-amyloid peptides: Detection of amyloid aggregation in solution. Protein Sci. 2: 404-410.
35. Litvinovich, S.V., Brew, S.A., Aota, S., Akiyama, S.K., Haudenschild, C., and Ingham, K.C. 1998. Formation of amyloid-like fibrils by self-association of a partially unfolded fibronectin type III module. J. Mol. Biol. 280: 245-258.
36. Liu, K., Cho, H.S., Lashuel, H.A., Kelly, J.W., and Wemmer, D.E. 2000. A glimpse of a possible amyloidogenic intermediate of transthyretin. Nat. Struct. Biol. 7: 754-757.
37. McParland, V.J., Kad, N.M., Kalverda, A.P., Brown, A., Kirwin-Jones, P., Hunter, M.G., Sunde, M., and Radford, S.E. 2000. Partially unfolded states of β2-microglobulin and amyloid formation in vitro. Biochemistry 39: 8735-8746.
38. Merkel, J.S., and Regan, L. 1998. Aromatic rescue of glycine in β-sheets. Fold Des. 3: 449-455.
39. Merkel, J.S., Sturtevant, J.M., and Regan, L. 1999. Side-chain interactions in parallel β-sheets: The energetics of cross-strand pairings. Structure Fold Des. 7: 1333-1343.
40. Morgan, C.J., Gelfand, M., Atreya, C., and Miranker, A.D. 2001. Kidney dialysis-associated amyloidosis: A molecular role for copper in fiber formation. J. Mol. Biol. 309: 339-345.
41. Nishimura, C., Uversky, V.N., and Fink, A.L. 2001. Effects of salts on the stability and folding of staphylococcal nuclease. Biochemistry 40: 2113-2128.
42. Ohnishi, S., Koide, A., and Koide, S. 2000. Solution conformation and amyloid-like fibril formation of a polar peptide derived from a β-hairpin in the OspA single-layer β-sheet. J. Mol. Biol. 301: 477-489.
43. Orpiszewski, J., and Benson, M.D. 1999. Induction of β-sheet structure in amyloidogenic peptides by neutralization of aspartate: A model for amyloid nucleation. J. Mol. Biol. 289: 413-428.
44. Park, S.H., O'Neil, K.T., and Roder, H. 1997. An early intermediate in the folding reaction of the B I domain of protein G contains a native-like core. Biochemistry 36: 14277-14283.
45. Park, S.H., Shastry, M.C., and Roder, H. 1999. Folding dynamics of the B1 domain of protein G explored by ultrarapid mixing. Nat. Struct. Biol. 6: 943-947.
46. Piotto, M., Saudek, V., and Sklenar, V. 1992. Gradient-tailored excitation for single-quantum NMR spectroscopy of aqueous solutions. J. Biomol. NMR. 2: 661-665.
47. Ramírez-Alvarado, M., Merkel, J.S., and Regan, L. 2000. A systematic exploration of the influence of the protein stability on amyloid fibril formation in vitro. Proc. Natl. Acad. Sci. 97: 8979-8984.
48. Sari, N., Alexander, P., Bryan, P.N., and Orban, J. 2000. Structure and dynamics of an acid-denatured protein G mutant. Biochemistry 39: 965-977.
49. Sebastiao, M.P., Saraiva, M.J., and Damas, A.M. 1998. The crystal structure of amyloidogenic Leu55 → Pro transthyretin variant reveals a possible pathway for transthyretin polymerization into amyloid fibrils. J. Biol. Chem. 273: 24715-24722.
50. Serpell, L.C., Sunde, M., and Blake, C.C. 1997. The molecular basis of amyloidosis. Cell. Mol. Life Sci. 53: 871-887.
51. Smith, C.K., and Regan, L. 1995. Guidelines for protein design: The energetics of β-sheet side chain interactions. Science 270: 980-982.
52. Smith, C.K., Withka, J.M., and Regan, L. 1994. A thermodynamic scale for the β-sheet forming tendencies of the amino acids. Biochemistry 33: 5510-5517.
53. Sunde, M., Serpell, L.C., Bartlam, M., Fraser, P.E., Pepys, M.B., and Blake, C.C. 1997. Common core structure of amyloid fibrils by synchrotron X-ray diffraction. J. Mol. Biol. 273: 729-739.
54. Takano, K., Funahashi, J., and Yutani, K. 2001. The stability and folding process of amyloidogenic mutant human lysozymes. Eur. J. Biochem. 268: 155-159.
55. Tanner, J.E. 1970. Use of the stimulated echo in NMR diffusion studies. J. Chem. Phys. 52: 2523-2526.
56. Terry, C.J., Damas, A.M., Oliveira, P., Saraiva, M.J., Alves, I.L., Costa, P.P., Matias, P.M., Sakaki, Y., and Blake, C.C. 1993. Structure of Met30 variant of transthyretin and its amyloidogenic implications. EMBO J. 12: 735-741.
57. Villegas, V., Zurdo, J., Filimonov, V.V., Aviles, F.X., Dobson, C.M., and Serrano, L. 2000. Protein engineering as a strategy to avoid formation of amyloid fibrils. Protein Sci. 9: 1700-1708.
58. Wall, J., Schell, M., Murphy, C., Hrncic, R., Stevens, F.J., and Solomon, A. 1999. Thermodynamic instability of human 16 light chains: Correlation with fibrillogenicity. Biochemistry 38: 14101-14108.
59. West, M.W., Wang, W., Patterson, J., Mancias, J.D., Beasley, J.R., and Hecht, M.H. 1999. De novo amyloid proteins from designed combinatorial libraries. Proc. Natl. Acad. Sci. 96: 11211-11216.
60. Yutani, K., Takayama, G., Goda, S., Yamagata, Y., Maki, S., Namba, K., Tsunasawa, S., and Ogasahara, K. 2000. The process of amyloid-like fibril formation by methionine aminopeptidase from a hyperthermophile, Pyrococcus furiosus. Biochemistry 39: 2769-2777.