Transient aggregation and stable dimerization induced by introducing an Alzheimer sequence into a water-soluble protein

Biochemistry

Volumn 43, Issue 41, 2004, Pages 12964-12978

  Otzen, Daniel E ^a   Miron, Simona ^b,d   Akke, Mikael ^b   Oliveberg, Mikael ^c  

^a AALBORG UNIVERSITY   (Denmark)

^b LUND UNIVERSITY   (Sweden)

^c UMEÅ UNIVERSITY   (Sweden)

^d UNIVERSITÉ D'ORLÉANS   (France)

Author keywords

[No Author keywords available]

Indexed keywords

DIMERIZATION; HYDROPHOBICITY; MUTAGENESIS; NUCLEAR MAGNETIC RESONANCE; PARAMETER ESTIMATION; POLYPEPTIDES;

FIBRILLATION; HOMOLOGY; PROTEIN AGGREGATION; PROTEIN ENGINEERING;

PROTEINS;

8 ANILINO 1 NAPHTHALENESULFONIC ACID; AMYLOID BETA PROTEIN; DIMER; GUANIDINE; NITROGEN 15; PROTEIN; PROTEIN U1A; PROTEIN U1A G; PROTEIN U1A J; UNCLASSIFIED DRUG; WATER;

AMINO ACID SEQUENCE; ARTICLE; BETA SHEET; BINDING AFFINITY; CARBOXY TERMINAL SEQUENCE; CONCENTRATION (PARAMETERS); CORRELATION ANALYSIS; DIMERIZATION; EXPERIMENT; EXPOSURE; HYDROPHOBICITY; MEASUREMENT; MOLECULAR INTERACTION; MUTANT; NUCLEAR MAGNETIC RESONANCE; PARAMETER; PRIORITY JOURNAL; PROTEIN AGGREGATION; PROTEIN BINDING; PROTEIN DENATURATION; PROTEIN ENGINEERING; PROTEIN FOLDING; PROTEIN STABILITY; PROTEIN STRUCTURE; SEQUENCE ANALYSIS; SEQUENCE HOMOLOGY; STRUCTURE ANALYSIS; SURFACE PROPERTY; WILD TYPE;

ALZHEIMER DISEASE; AMINO ACID SEQUENCE; AMYLOID BETA-PROTEIN; ANILINO NAPHTHALENESULFONATES; DIMERIZATION; GUANIDINE; HUMANS; HYDROPHOBICITY; MOLECULAR SEQUENCE DATA; MUTAGENESIS, SITE-DIRECTED; PEPTIDE FRAGMENTS; PROTEIN BINDING; PROTEIN DENATURATION; PROTEIN FOLDING; PROTEIN STRUCTURE, TERTIARY; RIBONUCLEOPROTEIN, U1 SMALL NUCLEAR; RNA-BINDING PROTEINS; SEQUENCE HOMOLOGY, AMINO ACID; SOLUBILITY; WATER;

EID: 5444246037     PISSN: 00062960     EISSN: None     Source Type: Journal    
DOI: 10.1021/bi048509k     Document Type: Article

References (63)

1. Fink, A. L. (1998) Protein aggregation: folding aggregates, inclusion bodies and amyloid, Folding Des. 3, R9-R29.
2. Rochet, J.-C., and Lansbury, P. T. (2000) Amyloid fibrillogenesis: themes and variations, Curr. Opin. Struct. Biol. 10, 60-68.
3. Kelly, J. W. (1998) The alternative conformations of amyloidogenic proteins and their multistep assembly pathways, Curr. Opin. Struct. Biol. 8, 101-106.
4. London, J., Skrzynia, C., and Goldberg, M. E. (1974) Renaturation of Escherichia coli tryptophanase after exposure to 8M urea. Evidence for the existence of nucleation centers, Eur. J. Biochem. 47, 409-415.
5. Halverson, K., Fraser, P. E., Kirschner, D. A., and Lansbury, P. T., Jr. (1990) Molecular determinants of amyloid deposition in Alzheimer's Disease: Conformational studies of synthetic β-protein fragments, Biochemistry 29, 2639-2644.
6. Silow, M., and Oliveberg, M. (1997) Transient aggregates in protein folding are easily mistaken for folding intermediates, Proc. Natl. Acad. Sci. U.S.A. 94, 6084-6086.
7. Chiti, F., Taddei, N., Bucciantini, M., White, P., Ramponi, G., and Dobson, C. M. (2000) Mutational analysis of the propensity for amyloid formation by a globular protein, EMBO J. 19, 1441-1449.
8. Chiti, F., Stefani, M., Taddei, N., Ramponi, G., and Dobson, C. M. (2003) Rationalization of the effects of mutations on peptide and protein aggregation rates, Nature 424, 805-808.
9. Harper, J. D., and Lansbury, P. T. J. (1997) Models of amyloid seeding in Alzheimer's disease and scrapie: mechanistic truths and physiological consequences of the time-dependent solubility of amyloid proteins, Annu. Rev. Biochem. 66, 385-407.
10. Pedersen, J. S., Christiansen, G., and Otzen, D. E. (2004) Modulation of S6 fibrillation by unfolding rates and gatekeeper residues, J. Mol. Biol., in press.
11. Chiti, F., Taddei, N., Baroni, F., Capanni, C., Stefani, M., Ramponi, G., and Dobson, C. M. (2002) Kinetic partitioning of protein folding and aggregation, Nat. Struct. Biol. 9, 137-143.
12. Otzen, D. E., Kristensen, P., and Oliveberg, M. (2000) Designed protein tetramer zipped together with an Alzheimer sequence: a structural clue to amyloid assembly, Proc. Natl. Acad. Sci. U.S.A. 97, 9907-9912.
13. Ventura, S., Zurdo, J., Narayanan, S., parreno, M., Mangues, R., Reif, B., Chiti, F., Giannoni, E., Dobson, C. M., Aviles, F. X., and Serrano, L. (2004) Short amino acid stretches can mediate amyloid formation in globular proteins: the Src homology 3 (SH3) case, Proc. Natl. Acad. Sci. U.S.A. 101, 7258-7263.
14. Iversen, L. L., Mortishire-Smith, R. J., Pollack, S. J., and Shearman, M. S. (1995) The toxicity in vitro of β-amyloid protein, Biochem. J. 311, 1-16.
15. Benzinger, T. L. S., Gregory, D. M., Burkoth, T. S., Miller-Auer, H., Lynn, D. G., Botto, R. E., and Meredith, S. C. (1998) Propagating structure of Alzheimer's β-amyloid(10-35) is parallel β-sheet with residues in exact register, Proc. Natl. Acad. Sci. U.S.A. 95, 13407-13412.
16. Kirschner, D. A., Inouye, H., Duffy, L. K., Sinclair, A., Lind, M., and Selkoe, D. J. (1987) Synthetic peptide homologous to β protein from Alzheimer disease forms amyloid-like fibrils in vitro, Proc. Natl. Acad. Sci. U.S.A. 84, 6953-6957.
17. Lansbury, P. T. J., Costa, P. R., Griffiths, J. M., Simon, E. J., Auger, M., Halverson, K. J., Kocisko, D. A., Hendsch, Z. S., Ashburn, T. T., Spencer, R. G. S., Tidor, B., and Griffin, R. G. (1995) Structural model for the β-amyloid fibril based on interstrand alignment of an antiparallel-sheet comprising a C-terminal peptide, Nat. Struct. Biol. 2, 990-998.
18. Kheterpal, I., Wetzel, R., and Cook, K. D. (2003) Enhanced correction methods for hydrogen exchange-mass spectrometric studies of amyloid fibrils, Protein Sci. 12, 635-643.
19. Jarrett, J. T., Berger, E. P., and Lansbury, P. T., Jr. (1993) The carboxy terminus of the β amyloid protein is critical for the seeding of amyloid formation: implications for the pathogenesis of Alzheimer's Disease, Biochemsitry 32, 4693-4697.
20. Hilbich, C., Kisters-Woike, B., Reed, J., Masters, C., and Beyreuther, K. (1991) Aggregation and secondary structure of synthetic amyloid βA4 peptides of Alzheimer's disease, J. Mol. Biol. 218, 149-163.
21. Zagorski, M. G., and Barrow, C. J. (1992) NMR studies of amyloid β-peptides: proton assignments, secondary structure, and mechanism of an α-helix - β-sheet conversion for a homologous, 28-residue, N-terminal fragment, Biochemistry 31, 5621-5631.
22. Gorevic, P. D., Castano, E. M., Sarma, R., and Frangione, B. (1987) Ten to fourteen residue peptides of Alzheimer's Disease protein are sufficient for amyloid fibril formation and its characteristic X-ray diffraction pattern, Biochem. Biophys. Res. Comm. 147, 854-862.
23. Volles, M. J., and Lansbury, P. T. (2003) Zeroing in on the pathogenic form of alpha-synuclein and its mechanism of neurotoxicity in Parkinson's Disease, Biochemistry 42, 7871-7878.
24. Hardy, J., and Selkoe, D. J. (2002) The amyloid hypothesis of Alzheimer's disease: progress and problems on the road to therapeutics, Science 297, 353-356.
25. Avis, J. M., Allain, F. H., Howe, P. W., Varani, G., Nagai, K., and Neuhaus, D. (1996) Solution structure of the N-terminal RNP domain of U1A protein: the role of C-terminal residues in structure stability and RNA binding, J. Mol. Biol. 257, 398-411.
26. Silow, M., and Oliveberg, M. (1997) High-energy channelling in protein folding, Biochemistry 36, 7633-7637.
27. Otzen, D. E., Kristensen, O., Proctor, M., and Oliveberg, M. (1999) Structural changes in the transition state of protein folding: an alternative interpretation of curved chevron plots, Biochemistry 38, 6499-6511.
28. Nagai, K., Oubridge, C, Jessen, T.-H., Li, J., and Evans, P. R. (1990) Crystal structure of the RNA-binding domain of the U1 small nuclear ribonucleoprotein A, Nature 348, 515-520.
29. Lu, J., and Hall, K. B. (1997) Tertiary structure of RBD2 and backbone dynamics of RBD1 and RBD2 of the human U1A protein determined by NMR spectroscopy, Biochemistry 36, 10393-10405.
30. Palmer, A. G., Cavanagh, J., Wright, P. E., and Ranee, M. (1991) Sensitivity Improvement in Proton-Detected 2-Dimensional Heteronuclear Correlation NMR Spectroscopy, J. Magn. Reson. 93, 151-170.
31. Kay, L. E., Keifer, P., and Saarinen, T. (1992) Pure absorption gradient enhanced heteronuclear single quantum correlation spectroscopy with improved sensitivity, J. Am. Chem. Soc. 114, 10663-10665.
32. Zhang, O., Kay, L. E., Olivier, J. P., and 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.
33. Shaka, A. J., Barker, P. B., and Freeman, R. (1985) Computer-optimized decoupling scheme for wideband applications and low-level operation, J. Magn. Reson. 64, 547-552.
34. Wishart, D. S., Bigam, C. G., Yao, J., Abildgaard, F., Dyson, H. J., Oldfleld, E., Markley, J., and Sykes, B. D. (1995) 1H, 13C and 15N chemical shift referencing in biomolecular NMR, J. Biomol. NMR 6, 135-140.
35. Farrow, N. A., Muhandiram, R., Singer, A. U., Pascal, S. M., Kay, C. M., Gish, G., Shoelson, S. E., Pawson, T., Forman-Kay, J. D., and Kay, L. E. (1994) Backbone Dynamics of a Free and a Phosphopeptide-Complexed Src Homology 2 Domain Studied by 15N NMR Relaxation, Biochemistry 33, 5984-6003.
36. 15N Chemical Shift Anisotropy Relaxation Interference: Unambiguous Determination of Rotational Diffusion Tensors and Chemical Exchange Effects in Biological Macromolecules, J. Am. Chem. Soc. 120, 7905-7915.
37. Skelton, N. J., Palmer, A. G., Akke, M., Kordel, J., Rance, M., and Chazin, W. J. (1993) Practical aspects of two-dimensional proton-detected 15N spin relaxation measurements, J. Magn. Reson., Ser. B 102, 729-739.
38. Mulqueen, P. M., and Kronman, M. J. (1982) Binding of naphthalene dyes to the N and A conformsers of bovine alpha-lactalbumin, Arch. Biochem. Biophys. 215, 28-39.
39. Semisotnov, G. V., Rodinova, N. A., Razgulyaev, O. I., Uversky, V. N., Gripas', A. F., and Gilmanshin, R. I. (1991) Study of the "Molten Globule" Intermediate State in Protein Folding by a Hydrophobic Fluorescent Probe, Biopolymers 31, 119-128.
40. Lacroix, E., Viguera, A. R., and Serrano, L. (1998) Elucidating the folding problem of alpha-helices: local motifs, long-range elctrostatics, ionic-strength dependence and prediction of NMR parameters, J. Mol. Biol. 284, 173-191.
41. Street, A. G., and Mayo, S. L. (1999) Intrinsic beta-sheet propensities result from van der Waals interactions between side chains and the local backbone, Proc. Natl. Acad. Sci. U.S.A. 96, 9074-9076.
42. Roseman, M. A. (1988) Hydrophilicity of polar amino acid side-chains is markedly reduced by flanking peptide bonds, J. Mol. Biol. 200, 513-522.
43. Levine, H. I. (1999) Quantification of β-sheet amyloid fibril structures with thioflavin T, Methods Enzymol. 309, 274-284.
44. Wishart, D. S., Sykes, B. D., and Richards, F. M. (1991) Relationship between nuclear magnetic resonance chemical shift and protein secondary structure, J. Mol. Biol. 222, 311-333.
45. Wüthrich, K. (1986) NMR of Proteins and Nucleic Acids, Wiley, New York.
46. Åkerud, T., Thulin, E., Van Etten, R. L., and Akke, M. (2002) Intramolecular dynamics of low-molecular weight protein tyrosine phosphatase in monomer-dimer equilibrium studied by NMR: a model for changes in dynamics upon target binding, J. Mol. Biol. 322, 137-152.
47. Harper, J. D., Wong, S. S., Lieber, C. M., and Lansbury, P. T. J. (1999) Assembly of Aβ amyloid protofibrils: An in vitro model for a possible early event in Alzheimer's disease, Biochemistry 38, 8972-8980.
48. Tsai, C.-J., Kumar, S., Ma, B., and Nussinov, R. (1999) Folding funnels, binding funnels and protein function, Protein Sci. 8, 1181-1190.
49. Souillac, P. O., Uversky, V. N., Millett, I. S., Khurana, R., Doniach, S., and Fink, A. L. (2002) Elucidation of the molecular mechanism during the early events in immunoglobulin light chain amyloid fibrillation, J. Biol. Chem. 277, 12666-12679.
50. Nielsen, L., Khurana, R., Coats, A., Frøkjær, S., Brange, J., Vyas, S., Uversky, V. N., and Fink, A. L. (2001) Effect of environmental factors on the kinetics of insulin fibril formation: Elucidation of the molecular mechanism, Biochemistry 40, 6036-6046.
51. Barrow, C. J., and Zagorski, M. G. (1991) Solution structures of β peptide and its constituent fragments: relation to amyloid deposition, Science 253, 179-182.
52. Otzen, D. E., and Oliveberg, M. (2004) Transient formation of nanocrystalline structures during fibrillation of an Alzheimer-like peptide, Protein Sci. 13, 1417-1421.
53. Helms, L. R., and Wetzel, R. (1996) Specificity of abnormal assembly in immunoglobulin light chain deposition disease and amyloidosis, J. Mol. Biol. 257, 77-86.
54. Dill, K. A., and Chan, H. S. (1997) From Levinthal to pathways to funnels, Nat. Struct. Biol. 4, 10-19.
55. Silow, M., and Oliveberg, O. (2003) High concentrations of viscogens decrease the protein folding rate constant by prematurely collapsing the coil, J. Mol. Biol. 326, 263-271.
56. Fandrich, M., Forge, V., Buder, K., Kittler, M., Dobson, C. M., and Diekmann, S. (2003) Myoglobin forms amyloid fibrils by association of unfolded polypeptide segments, Proc. Natl. Acad. Sci. U.S.A. 100, 15463-15468.
57. Kranz, J. K., and Hall, K. B. (1999) RNA recognition by the human U1A protein is mediated by a network of local cooperative interactions that create the optimal binding surface, J. Mol. Biol. 285, 215-231.
58. Kranz, J. F., Lu, J., and Hall, K. B. (1996) Contribution of the tyrosines to the structure and function of the human U1A N-terminal RNA binding domain, Protein Sci. 5, 1567-1583.
59. Jean, J. M., Clerte, C., and Hall, K. B. (1999) Global and local dynamics of the human U1A protein determined by tryptophan fluorescence, Protein Sci. 8, 2110-2120.
60. Branden, C. I., and Tooze, J. (1999) Introduction to Protein Structure, 2nd ed., Garland, New York.
61. Clarke, J., and Fersht, A. R. (1993) Engineered disulfide bonds as probes of the folding pathway of barnase: increasing the stability of proteins against the rate of denaturation, Biochemistry 32, 4322-4329.
62. Kraulis, P. J. (1991) MOLSCRIPT: a program to produce both detailed and schematic plots of protein structure, J. Appl. Crystallogr. 24, 946-950.
63. Corpet, F. (1988) Multiple sequence alignment with hierarchical clustering, Nucleic Acids Res. 16, 10881-10890.