Crowding alone cannot account for cosolute effect on amyloid aggregation

PLoS ONE

Volumn 6, Issue 1, 2011, Pages

  Sukenik, Shahar ^a   Politi, Regina ^a   Ziserman, Lior ^b   Danino, Dganit ^b   Friedler, Assaf ^a   Harries, Daniel ^a  

^a HEBREW UNIVERSITY OF JERUSALEM   (Israel)

^b TECHNION ISRAEL INSTITUTE OF TECHNOLOGY   (Israel)

Author keywords

[No Author keywords available]

Indexed keywords

AMYLOID; GLYCEROL; MACROGOL; MONOMER; POLYOL; SORBITOL; AMYLOID PRECURSOR PROTEIN; APP PROTEIN, HUMAN; MACROGOL DERIVATIVE; POLYMER;

ARTICLE; CIRCULAR DICHROISM; CONCENTRATION (PARAMETERS); CONTROLLED STUDY; CROWDING; EQUILIBRIUM CONSTANT; FLUORESCENCE ANALYSIS; MOLECULAR SIZE; MOLECULAR WEIGHT; PH MEASUREMENT; PROTEIN AGGREGATION; PROTEIN CONFORMATION; PROTEIN FOLDING; PROTEIN INTERACTION; PROTEIN STABILITY; TRANSMISSION ELECTRON MICROSCOPY; BIOLOGICAL MODEL; CELL; CHEMISTRY; HUMAN; KINETICS; PROTEIN SECONDARY STRUCTURE;

AMYLOID; AMYLOID BETA-PROTEIN PRECURSOR; CELLS; CIRCULAR DICHROISM; HUMANS; KINETICS; MODELS, BIOLOGICAL; POLYETHYLENE GLYCOLS; POLYMERS; PROTEIN FOLDING; PROTEIN STRUCTURE, SECONDARY;

EID: 79251538929     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0015608     Document Type: Article

References (71)

1. Chiti F, Dobson CM (2006) Protein misfolding, functional amyloid, and human disease. Annu Rev Biochem 75: 333-366.
2. Haass C, Selkoe DJ (2007) Soluble protein oligomers in neurodegeneration: lessons from the Alzheimer's amyloid b-peptide. Nat Rev Mol Cell Biol 8: 101-112.
3. Harper JD, Lansbury PT (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.
4. Glenner GG (1980) Amyloid Deposits and Amyloidosis - the b-Fibrilloses. N Engl J Med 302: 1333-1343.
5. Dobson CM (1999) Protein misfolding, evolution and disease. Trends Biochem Sci 24: 329-332.
6. Izhack C, Ehud G (2008) Amyloids: Not Only Pathological Agents but Also Ordered Nanomaterials. Angew Chem 47: 4062-4069.
7. Dobson CM (2003) Protein folding and misfolding. Nature 426: 884-890.
8. LeVinne HI (1993) Thioflavine T interaction with synthetic Alzheimer's disease b-amyloid peptides: Detection of amyloid aggregation in solution. Protein Sci 2: 404-410.
9. Calamai M, Chiti F, Dobson CM (2005) Amyloid Fibril Formation Can Proceed from Different Conformations of a Partially Unfolded Protein. Biophys J 89: 4201-4210.
10. Morris AM, Watzky MA, Finke RG (2009) Protein aggregation kinetics, mechanism, and curve-fitting: A review of the literature. Biochim Biophys Acta 1794: 375-397.
11. Xu YC, Shen JJ, Luo XM, Zhu WL, Chen KX, et al. (2005) Conformational transition of amyloid b-peptide. Proc Natl Acad Sci U S A 102: 5403-5407.
12. Ignatova Z, Gierasch LM (2006) Inhibition of protein aggregation in vitro and in vivo by a natural osmoprotectant. Proc Natl Acad Sci U S A 103: 13357-13361.
13. Natalello A, Liu J, Ami D, Doglia SM, de Marco A (2009) The osmolyte betaine promotes protein misfolding and disruption of protein aggregates. Proteins Struct Funct Bioinformat 75: 509-517.
14. De Felice FG, Vieira MNN, Meirelles MNL, Morozova-Roche LA, Dobson CM, et al. (2004) Formation of amyloid aggregates from human lysozyme and its disease-associated variants using hydrostatic pressure. FASEB J 18: 1099-1101.
15. Picotti P, De Franceschi G, Frare E, Spolaore B, Zambonin M, et al. (2007) Amyloid fibril formation and disaggregation of fragment 1-29 of apomyoglobin: Insights into the effect of pH on protein fibrillogenesis. J Mol Biol 367: 1237-1245.
16. Yancey PH, Clark ME, Hand SC, Bowlus RD, Somero GN (1982) Living with water stress: evolution of osmolyte systems. Science 217: 1214-1222.
17. Ellis RJ (2001) Macromolecular crowding: an important but neglected aspect of the intracellular environment. Curr Opin Struct Biol 11: 114-119.
18. Zimmerman SB, Minton AP (1993) Macromolecular Crowding - Biochemical, Biophysical and Physiological Consequences. Annu Rev Biophys Biomol Struct 22: 27-65.
19. Zimmerman SB, Trach SO (1988) Effects of macromolecular crowding on the association of E.coli ribosomal particles. Nucleic Acids Res 16: 6309-6326.
20. Munishkina LA, Ahmad A, Fink AL, Uversky VN (2008) Guiding Protein Aggregation with Macromolecular Crowding. Biochemistry 47: 8993-9006.
21. Minton AP (2000) Implications of macromolecular crowding for protein assembly. Curr Opin Struct Biol 10: 34-39.
22. Minton AP (2001) The influence of macromolecular crowding and macromolecular confinement on biochemical reactions in physiological media. J Biol Chem 276: 10577-10580.
23. Wyman Jr J, CBAnfinsen J, Anson ML, Edsall JT, Frederic MR (1964) Linked Functions and Reciprocal Effects in Hemoglobin: A Second Look. Adv Protein Chem: Academic Press. pp 223-286.
24. Adrian Parsegian V (2002) Protein-water interactions. In: Thomas Z, Wilfred DS, eds. International Review of Cytology: A survey of Cell Biology;Molecular Mechanisms of Water Transport across Biological Membranes: Academic Press. pp 1-31.
25. Gibbs JW (1993) On the equilibrium of heterogeneous substances; HAB, RGvN, eds. Woodbridge: Ox Bow.
26. Harries D, Rosgen J (2008) A practical guide on how osmolytes modulate macromolecular properties. Biophysical Tools for Biologists: Vol 1 In Vitro Techniques. Maryland Heights: Elsevier Academic Press, Inc.
27. Rosgen J (2007) Molecular basis of osmolyte effects on protein and metabolites. Methods Enzymol 428: 459-486.
28. Hatters DM, Minton AP, Howlett GJ (2002) Macromolecular crowding accelerates amyloid formation by human apolipoprotein C-II. J Biol Chem 277: 7824-7830.
29. Munishkina LA, Cooper EM, Uversky VN, Fink AL (2004) The effect of macromolecular crowding on protein aggregation and amyloid fibril formation. J Mol Recognit 17: 456-464.
30. Parsegian VA, Rand RP, Rau DC, Michael LJ, Gary KA (1995) Macromolecules and water: Probing with osmotic stress. Methods Enzymol: Academic Press. pp 43-94.
31. Parsegian VA, Rand RP, Rau DC (2000) Osmotic stress, crowding, preferential hydration, and binding: A comparison of perspectives. Proc Natl Acad Sci U S A 97: 3987-3992.
32. Liu F-F, Ji L, Dong X-Y, Sun Y (2009) Molecular Insight into the Inhibition Effect of Trehalose on the Nucleation and Elongation of Amyloid b-Peptide Oligomers. J Phys Chem B 113: 11320-11329.
33. McLaurin J, Golomb R, Jurewicz A, Antel JP, Fraser PE (2000) Inositol stereoisomers stabilize an oligomeric aggregate of Alzheimer amyloid b peptide and inhibit abeta -induced toxicity. J Biol Chem 275: 18495-18502.
34. Maynard AJ, Sharman GJ, Searle MS (1998) Origin of b-Hairpin Stability in Solution: Structural and Thermodynamic Analysis of the Folding of a Model Peptide Supports Hydrophobic Stabilization in Water. J Am Chem Soc 120: 1996-2007.
35. Griffiths-Jones SR, Maynard AJ, Searle MS (1999) Dissecting the stability of a bhairpin peptide that folds in water: NMR and molecular dynamics analysis of the b-turn and b-strand contributions to folding. J Mol Biol 292: 1051-1069.
36. Politi R, Harries D (2010) An enthalpic mechanism for peptide stabilization by protecting osmolytes. Chem Commun 46: 6449-6451.
37. Shi Z, Woody RW, Kallenbach NR, George DR (2002) Is polyproline II a major backbone conformation in unfolded proteins? Adv Protein Chem: Academic Press. pp 163-240.
38. Sreerama N, Woody RW (1994) Poly(Pro)II Helixes in Globular Proteins: Identification and Circular Dichroic Analysis. Biochemistry 33: 10022-10025.
39. Syme CD, Blanch EW, Holt C, Jakes R, Goedert M, et al. (2002) A Raman optical activity study of rheomorphism in caseins, synucleins and tau. Eur J Biochem 269: 148-156.
40. Eker F, Griebenow K, Schweitzer-Stenner R (2004) Ab1-28 Fragment of the Amyloid Peptide Predominantly Adopts a Polyproline II Conformation in an Acidic Solution. Biochemistry 43: 6893-6898.
41. Blanch EW, Morozova-Roche LA, Cochran DAE, Doig AJ, Hecht L, et al. (2000) Is polyproline II helix the killer conformation? a raman optical activity study of the amyloidogenic prefibrillar intermediate of human lysozyme. J Mol Biol 301: 553-563.
42. Perczel A, Hollosi M, Tusnady G, Fasman GDF (1991) Convex constraint analysis: a natural deconvolution of circular dichroism curves of proteins. Protein Eng 4: 669-679.
43. Siligardi G, Drake AF (1995) The importance of extended conformations and, in particular, the PII conformation for the molecular recognition of peptides. Biopolymers 37: 281-292.
44. Auton M, Bolen DW (2005) Predicting the energetics of osmolyte-induced protein folding/unfolding. Proc Natl Acad Sci U S A 102: 15065-15068.
45. Stanley CB, Strey HH (2008) Osmotically Induced Helix-Coil Transition in Poly(Glutamic Acid). Biophys J 94: 4427-4434.
46. Stagg L, Zhang S-Q, Cheung MS, Wittung-Stafshede P (2007) Molecular crowding enhances native structure and stability of a/bprotein flavodoxin. Proc Natl Acad Sci U S A 104: 18976-18981.
47. Fersht AR (1999) Structure and Mechanism in Protein Science. New York: W H Freeman & Co.
48. Gee MB, Smith PE (2009) Kirkwood-Buff theory of molecular and protein association, aggregation, and cellular crowding. J Chem Phys 131: 165101-165111.
49. Guo F, Friedman JM (2009) Osmolyte-Induced Perturbations of Hydrogen Bonding between Hydration Layer Waters: Correlation with Protein Conformational Changes. J Phys Chem B 113: 16632-16642.
50. Welch WJ, Brown CR (1996) Influence of Molecular and Chemical Chaperones on Protein Folding. Cell Stress Chaperones 1: 109-115.
51. Politi R, Sapir L, Harries D (2009) The Impact of Polyols on Water Structure in Solution: A Computational Study. J Phys Chem A 113: 7548-7555.
52. Kuffel A, Zielkiewicz J (2010) The hydrogen bond network structure within the hydration shell around simple osmolytes: Urea, tetramethylurea, and trimethylamine-N-oxide, investigated using both a fixed charge and a polarizable water model. The Journal of Chemical Physics 133: 035102-035108.
53. Cannon MJ, Williams AD, Wetzel R, Myszka DG (2004) Kinetic analysis of bamyloid fibril elongation. Anal Biochem 328: 67-75.
54. Nguyen PH, Li MS, Stock G, Straub JE, Thirumalai D (2007) Monomer adds to preformed structured oligomers of Ab-peptides by a two-stage dock-lock mechanism. Proc Natl Acad Sci U S A 104: 111-116.
55. Sidorova NY, Rau DC (2000) The dissociation rate of the EcoRI-DNA-specific complex is linked to water activity. Biopolymers 53: 363-368.
56. Gurnev AP, Harries D, Parsegian VA, Sergey MB (2009) The Dynamic Side of the Hofmeister Effect: A Single-Molecule Nanopore Study of Specific Complex Formation. ChemPhysChem 10: 1445-1449.
57. Minton AP (2000) Effects of excluded surface area and adsorbate clustering on surface adsorption of proteins: I. Equilibrium models. Biophys Chem 86: 239-247.
58. Minton AP (2001) Effects of Excluded Surface Area and Adsorbate Clustering on Surface Adsorption of Proteins. II. Kinetic Models. Biophys J 80: 1641-1648.
59. White DA, Buell AK, Knowles TPJ, Welland ME, Dobson CM (2010) Protein Aggregation in Crowded Environments. J Am Chem Soc 132: 5170-5175.
60. Sun J, Weinstein H (2007) Toward realistic modeling of dynamic processes in cell signaling: Quantification of macromolecular crowding effects. J Chem Phys 127: 155105-155110.
61. Rudan-Tasic D, Klofutar C (2003) Osmotic coefficients and salvation thermodynamics of aqueous solutions of some lower poly(ethylene glycol)s at different temperatures. J Mol Liq 103: 187-200.
62. DiPaola G, Belleau B (1977) Polyol-Water interactions. Apparent molal heat capacities and volumes of aqueous polyol solutions. Can J Chem 55: 3825-3830.
63. Bolen DW, Baskakov IV (2001) The osmophobic effect: natural selection of a thermodynamic force in protein folding. J Mol Biol 310: 955-963.
64. Capp MW, Pegram LM, Saecker RM, Kratz M, Riccardi D, et al. (2009) Interactions of the Osmolyte Glycine Betaine with Molecular Surfaces in Water: Thermodynamics, Structural Interpretation, and Prediction of m-Values. Biochemistry 48: 10372-10379.
65. Rosgen J, Pettitt BM, Bolen DW (2007) An analysis of the molecular origin of osmolyte-dependent protein stability. Protein Sci 16: 733-743.
66. Athawale MV, Dordick JS, Garde S (2005) Osmolyte Trimethylamine-N-Oxide Does Not Affect the Strength of Hydrophobic Interactions: Origin of Osmolyte Compatibility. Biophys J 89: 858-866.
67. Blodgett MB, Ziemer SP, Brown BR, Niederhauser TL, Woolley EM (2007) Apparent molar volumes and apparent molar heat capacities of aqueous adonitol, dulcitol, glycerol, meso-erythritol, myo-inositol, D-sorbitol, and xylitol at temperatures from (278.15 to 368.15) K and at the pressure 0.35 MPa. J Chem Thermodyn 39: 627-644.
68. Eliassi A, Modarress H, Mansoori GA (1998) Densities of Poly(ethylene glycol) + Water Mixtures in the 298.15 K to 328.15 K Temperature Range. J Chem Eng Data 43: 719-721.
69. Abramoff MD, Magelhaes PJ, Ram SJ (2004) Image Processing with ImageJ. Biophotonics International 11: 36-42.
70. Hamley I, Castelletto V, Moulton C, Siligardi G, Oliveira C, et al. (2010) A Modified Amyloid Peptide Fragment Forming a Nematic Phase of Aligned Fibrils at Very Low Concentration. Macromolecular Biosciences 10: 40-48.
71. Perczel A, Park K, Fasman GD (1992) Analysis of the circular dichroism spectrum of proteins using the convex constraint algorithm: A practical guide. Anal Biochem 203: 83-93.