Agitation and high ionic strength induce amyloidogenesis of a folded PDZ domain in native conditions

Biophysical Journal

Volumn 96, Issue 6, 2009, Pages 2289-2298

  Sicorello, Alessandro ^a   Torrassa, Silvia ^b   Soldi, Gemma ^a   Gianni, Stefano ^c   Travaglini Allocatelli, Carlo ^c   Taddei, Niccolò ^a   Relini, Annalisa ^b,d   Chiti, Fabrizio ^a,e  

^a UNIVERSITY OF FLORENCE   (Italy)

^b UNIVERSITY OF GENOA   (Italy)

^c SAPIENZA UNIVERSITY OF ROME   (Italy)

^d Consorzio Nazionale Interuniversitario Per le Scienze Fisiche Della Materia ^*  (Italy)

^e NATIONAL INSTITUTE OF BIOSTRUCTURES AND BIOSYSTEMS   (Italy)

Author keywords

[No Author keywords available]

Indexed keywords

AMYLOID; 8 ANILINO 1 NAPHTHALENESULFONIC ACID; 8-ANILINO-1-NAPHTHALENESULFONIC ACID; NON RECEPTOR PROTEIN TYROSINE PHOSPHATASE 13; THIAZOLE DERIVATIVE; THIOFLAVINE;

AGITATION; ARTICLE; BETA SHEET; CIRCULAR DICHROISM; INFRARED SPECTROSCOPY; PDZ DOMAIN; PH MEASUREMENT; PROTEIN AGGREGATION; PROTEIN FOLDING; PROTEIN STRUCTURE; ANIMAL; ATOMIC FORCE MICROSCOPY; CHEMICAL STRUCTURE; CHEMISTRY; FLUORESCENCE; ISOLATION AND PURIFICATION; KINETICS; MOTION; MOUSE; OSMOLARITY; PROTEIN SECONDARY STRUCTURE;

AMYLOID; ANILINO NAPHTHALENESULFONATES; ANIMALS; CIRCULAR DICHROISM; FLUORESCENCE; KINETICS; MICE; MICROSCOPY, ATOMIC FORCE; MODELS, MOLECULAR; MOTION; OSMOLAR CONCENTRATION; PDZ DOMAINS; PROTEIN FOLDING; PROTEIN STRUCTURE, SECONDARY; PROTEIN TYROSINE PHOSPHATASE, NON-RECEPTOR TYPE 13; SPECTROSCOPY, FOURIER TRANSFORM INFRARED; THIAZOLES;

EID: 66149144761     PISSN: 00063495     EISSN: 15420086     Source Type: Journal    
DOI: 10.1016/j.bpj.2008.11.042     Document Type: Article

References (50)

1. Stefani, M., and C. M. Dobson. 2003. Protein aggregation and aggregate toxicity: new insights into protein folding, misfolding diseases and biological evolution. J. Mol. Med. 81:678-699.
2. Uversky, V. N., and A. L. Fink. 2004. Conformational constraints for amyloid fibrillation: the importance of being unfolded. Biochim. Biophys. Acta. 1698:131-153.
3. Selkoe, D. J. 2003. Folding proteins in fatal ways. Nature. 426: 900-904.
4. Chiti, F., and C. M. Dobson. 2006. Protein misfolding, functional amyloid, and human disease. Annu. Rev. Biochem. 75:333-366.
5. Fowler, D. M., A. V. Koulov, W. E. Balch, and J. W. Kelly. 2007. Functional amyloid - from bacteria to humans. Trends Biochem. Sci. 32:217-224.
6. Gazit, E. 2007. Use of biomolecular templates for the fabrication of metal nanowires. FEBS J. 274:317-322.
7. Hamley, I. W. 2007. Peptide fibrillization. Angew. Chem. Int. Ed. Engl. 46:8128-8147.
8. Guijarro, J. I., M. Sunde, J. A. Jones, I. D. Campbell, and C. M. Dobson. 1998. Amyloid fibril formation by an SH3 domain. Proc. Natl. Acad. Sci. USA. 95:4224-4228.
9. McParland, V. J., N. M. Kad, A. P. Kalverda, A. Brown, P. Kirwin-Jones, et al. 2000. Partially unfolded states of β(2)-microglobulin and amyloid formation in vitro. Biochemistry. 39:8735-8746.
10. Litvinovich, S. V., S. A. Brew, S. Aota, S. K. Akiyama, C. Haudenschild, et al. 1998. Formation of amyloid-like fibrils by self-association of a partially unfolded fibronectin type IIImodule. J. Mol. Biol. 280:245-258.
11. Fändrich, M., M. A. Fletcher, and C. M. Dobson. 2001. Amyloid fibrils from muscle myoglobin. Nature. 410:165-166.
12. Ferrão-Gonzales, A. D., S. O. Souto, J. L. Silva, and D. Foguel. 2000. The preaggregated state of an amyloidogenic protein: hydrostatic pressure converts native transthyretin into the amyloidogenic state. Proc. Natl. Acad. Sci. USA. 97:6445-6450.
13. De Felice, F. G., M. N. Vieira, M. N. Meirelles, L. A. Morozova-Roche, C. M. Dobson, et al. 2004. Formation of amyloid aggregates from human lysozyme and its disease-associated variants using hydrostatic pressure. FASEB J. 18:1099-1101.
14. Chiti, F., P. Webster, N. Taddei, A. Clark, M. Stefani, et al. 1999. Designing conditions for in vitro formation of amyloid protofilaments and fibrils. Proc. Natl. Acad. Sci. USA. 96:3590-3594.
15. Schmittschmitt, J. P., and J. M. Scholtz. 2003. The role of protein stability, solubility, and net charge in amyloid fibril formation. Protein Sci. 12:2374-2378.
16. Sasahara, K., H. Yagi, H. Naiki, and Y. Goto. 2007. Heat-induced conversion of β(2)-microglobulin and hen egg-white lysozyme into amyloid fibrils. J. Mol. Biol. 372:981-991.
17. 2-microglobulin under acidic and neutral pH conditions. Biochemistry. 47:2650-2660.
18. Hung, A. Y., and M. Sheng. 2002. PDZ domains: structural modules for protein complex assembly. J. Biol. Chem. 277:5699-5702.
19. Chi, C. N., S. Gianni, N. Calosci, C. Travaglini-Allocatelli, K. Engström, et al. 2007. A conserved folding mechanism for PDZ domains. FEBS Lett. 581:1109-1113.
20. Gianni, S., N. Calosci, J. M. Aelen, G. W. Vuister, M. Brunori, et al. 2005. Kinetic folding mechanism of PDZ2 from PTP-BL. Protein Eng. Des. Sel. 18:389-395.
21. Ivarsson, Y., C. Travaglini-Allocatelli, P. Jemth, F. Malatesta, M. Brunori, et al. 2007. An on-pathway intermediate in the folding of a PDZ domain. J. Biol. Chem. 282:8568-8572.
22. Gianni, S., C. D. Geierhaas, N. Calosci, P. Jemth, G. W. Vuister, et al. 2007. A PDZ domain recapitulates a unifying mechanism for protein folding. Proc. Natl. Acad. Sci. USA. 104:128-133.
23. Jemth, P., and S. Gianni. 2007. PDZ domains: folding and binding. Biochemistry. 46:8701-8708.
24. Walma, T., C. A. Spronk, M. Tessari, J. Aelen, J. Schepens, et al. 2002. Structure, dynamics and binding characteristics of the second PDZ domain of PTP-BL. J. Mol. Biol. 316:1101-1110.
25. Campioni, S., M. F. Mossuto, S. Torrassa, G. Calloni, P. P. de Laureto, et al. 2008. Conformational properties of the aggregation precursor state of HypF-N. J. Mol. Biol. 379:554-567.
26. Santoro, M. M., and D. W. Bolen. 1998. Unfolding free energy changes determined by the linear extrapolation method. 1. Unfolding of phenylmethanesulfonyl α-chymotrypsin using different denaturants. Biochemistry. 27:8063-8068.
27. Jaikaran, E. T., C. E. Higham, L. C. Serpell, J. Zurdo, M. Gross, et al. 2001. Identification of a novel human islet amyloid polypeptide β-sheet domain and factors influencing fibrillogenesis. J. Mol. Biol. 308:515-525.
28. Soldi, G., F. Bemporad, S. Torrassa, A. Relini, M. Ramazzotti, et al. 2005. Amyloid formation of a protein in the absence of initial unfolding and destabilization of the native state. Biophys. J. 89:4234-4244.
29. Castiglioni, E., S. Abbate, G. Longhi, and R. Gangemi. 2007. Wavelength shifts in solid-state circular dichroism spectra: a possible explanation. Chirality. 19:491-496.
30. Zandomeneghi, G., M. R. Krebs, M. G. McCammon, and M. Fändrich. 2004. FTIR reveals structural differences between native β-sheet proteins and amyloid fibrils. Protein Sci. 13:3314-3321.
31. Seshadri, S., R. Khurana, and A. L. Fink. 1999. Fourier transform infrared spectroscopy in analysis of protein deposits. Methods Enzymol. 309:559-576.
32. Harper, J. D., S. S. Wong, C. M. Lieber, and P. T. Lansbury. 1997. Observation of metastable Aβ amyloid protofibrils by atomic force microscopy. Chem. Biol. 4:119-122.
33. Kihara, M., E. Chatani, M. Sakai, K. Hasegawa, H. Naiki, et al. 2005. Seeding-dependent maturation of β2-microglobulin amyloid fibrils at neutral pH. J. Biol. Chem. 280:12012-12018.
34. Morozova-Roche, L. A., J. Zurdo, A. Spencer, W. Noppe, V. Receveur, et al. 2000. Amyloid fibril formation and seeding by wild-type human lysozyme and its disease-related mutational variants. J. Struct. Biol. 130:339-351.
35. Peim, A., P. Hortschansky, T. Christopeit, V. Schroeckh, W. Richter, et al. 2006. Mutagenic exploration of the cross-seeding and fibrillation propensity of Alzheimer's β-amyloid peptide variants. Protein Sci. 15:1801-1805.
36. Cacace, M. G., E. M. Landau, and J. J. Ramsden. 1997. The Hofmeister series: salt and solvent effects on interfacial phenomena. Q. Rev. Biophys. 30:241-277.
37. Taddei, N., F. Chiti, P. Paoli, T. Fiaschi, M. Bucciantini, et al. 1999. Thermodynamics and kinetics of folding of common-type acylphosphatase: comparison to the highly homologous muscle isoenzyme. Biochemistry. 38:2135-2142.
38. Zurdo, J., J. I. Guijarro, J. L. Jiménez, H. R. Saibil, and C. M. Dobson. 2001. Dependence on solution conditions of aggregation and amyloid formation by an SH3 domain. J. Mol. Biol. 311:325-340.
39. Munishkina, L. A., J. Henriques, V. N. Uversky, and A. L. Fink. 2004. Role of protein-water interactions and electrostatics in α-synuclein fibril formation. Biochemistry. 43:3289-3300.
40. Raman, B., E. Chatani, M. Kihara, T. Ban, M. Sakai, et al. 2005. Critical balance of electrostatic and hydrophobic interactions is required for β2-microglobulin amyloid fibril growth and stability. Biochemistry. 44:1288-1299.
41. Creighton, T. E. 1992. Proteins: Structures and Molecular Properties, 2nd ed. W. H. Freeman and Company, New York. 155-156.
42. Collins, K. D., and M. W. Washabaugh. 1985. The Hofmeister effect and the behaviour of water at interfaces. Q. Rev. Biophys. 18:323-422.
43. Klement, K., K. Wieligmann, J. Meinhardt, P. Hortschansky, W. Richter, et al. 2007. Effect of different salt ions on the propensity of aggregation and on the structure of Alzheimer's Aβ(1-40) amyloid fibrils. J. Mol. Biol. 373:1321-1333.
44. Collins, S. R., A. Douglass, R. D. Vale, and J. S. Weissman. 2004. Mechanism of prion propagation: amyloid growth occurs by monomer addition. PLoS Biol. 2:1582-1590.
45. Liu, J. J., and S. Lindquist. 1999. Oligopeptide-repeat expansions modulate 'protein-only' inheritance in yeast. Nature. 400:573-576.
46. Serpell, L. C., J. Berriman, R. Jakes, M. Goedert, and R. A. Crowther. 2000. Fiber diffraction of synthetic α-synuclein filaments shows amyloid-like cross-β conformation. Proc. Natl. Acad. Sci. USA. 97:4897-4902.
47. Hill, E. K., B. Krebs, D. G. Goodall, G. J. Howlett, and D. E. Dunstan. 2006. Shear flow induces amyloid fibril formation. Biomacromolecules. 7:10-13.
48. Petkova, A. T., R. D. Leapman, Z. Guo, W. M. Yau, M. P. Mattson, et al. 2005. Self-propagating, molecular-level polymorphism in Alzheimer's β-amyloid fibrils. Science. 307:262-265.
49. Shorter, J., and S. Lindquist. 2004. Hsp104 catalyzes formation and elimination of self-replicating Sup35 prion conformers. Science. 304:1793-1797.
50. Sun, Y., N. Makarava, C. I. Lee, P. Laksanalamai, F. T. Robb, et al. 2008. Conformational stability of PrP amyloid fibrils controls their smallest possible fragment size. J. Mol. Biol. 376:1155-1167.