Hexafluoroisopropanol induces self-assembly of β-amyloid peptides into highly ordered nanostructures

Journal of Peptide Science

Volumn 18, Issue 4, 2012, Pages 233-241

  Pachahara, Sanjai Kumar ^a   Chaudhary, Nitin ^a,b   Subbalakshmi, Chilukuri ^a   Nagaraj, Ramakrishnan ^a  

^a CENTRE FOR CELLULAR AND MOLECULAR BIOLOGY   (India)

^b INDIAN INSTITUTE OF TECHNOLOGY GUWAHATI   (India)

Author keywords

Amyloid fibrils; Fluorinated alcohol; Ring like structures; Self assembly

Indexed keywords

AMYLOID BETA PROTEIN; AMYLOID BETA PROTEIN[1-40]; AMYLOID BETA PROTEIN[1-42]; HEXAFLUORO 2 PROPANOL; NANOMATERIAL; THIOFLAVINE;

ALPHA HELIX; ARTICLE; DISSOLUTION; INCUBATION TIME; MOLECULAR DYNAMICS; PRIORITY JOURNAL; PROTEIN AGGREGATION; PROTEIN ASSEMBLY; PROTEIN STABILITY; PROTEIN STRUCTURE; STRUCTURE ANALYSIS;

AMYLOID BETA-PEPTIDES; CIRCULAR DICHROISM; FLUORESCENT DYES; HUMANS; MICROSCOPY, ATOMIC FORCE; MICROSCOPY, ELECTRON, SCANNING; NANOSTRUCTURES; PARTICLE SIZE; PEPTIDE FRAGMENTS; PROPANOLS; PROTEIN MULTIMERIZATION; PROTEIN STRUCTURE, QUATERNARY; PROTEIN STRUCTURE, SECONDARY; SPECTROSCOPY, FOURIER TRANSFORM INFRARED; THIAZOLES;

EID: 84858862940     PISSN: 10752617     EISSN: 10991387     Source Type: Journal    
DOI: 10.1002/psc.2391     Document Type: Article

References (70)

1. Selkoe DJ. Translating cell biology into therapeutic advances in Alzheimer's disease. Nature 1999; 399: A23-31.
2. LaFerla FM, Green KN, Oddo S. Intracellular amyloid-β in Alzheimer's disease. Nat. Rev. Neurosci. 2007; 8: 499-509.
3. Woo HN, Baik SH, Park JS, Gwon AR, Yang S, Yun YK, Jo DG. Secretases as therapeutic targets for Alzheimer's disease. Biochem. Biophys. Res. Commun. 2011; 404: 10-15.
4. Kuperstein I, Broersen K, Benilova I, Rozenski J, Jonckheere W, Debulpaep M, Vandersteen A, Segers-Nolten I, Van Der Werf K, Subramaniam V, Braeken D, Callewaert G, Bartic C, D'Hooge R, Martins IC, Rousseau F, Schymkowitz J, De Strooper B. Neurotoxicity of Alzheimer's disease Aβ peptides is induced by small changes in the Aβ42 to Aβ40 ratio. EMBO J. 2010; 29: 3408-3420.
5. Welander H, Franberg J, Graff C, Sundstrom E, Winblad B, Tjernberg LO. Aβ43 is more frequent than Aβ40 in amyloid plaque cores from Alzheimer disease brains. J. Neurochem. 2009; 110: 697-706.
6. Delacourte A, Sergeant N, Champain D, Wattez A, Maurage CA, Lebert F, Pasquier F, David JP. Nonoverlapping but synergetic tau and APP pathologies in sporadic Alzheimer's disease. Neurology 2002; 59: 398-407.
7. Zagorski MG, Yang J, Shao H, Ma K, Zeng H, Hong A. Methodological and chemical factors affecting amyloid β peptide amyloidogenicity. Methods Enzymol. 1999; 309: 189-204.
8. Sciarretta KL, Gordon DJ, Petkova AT, Tycko R, Meredith SC. Aβ40-Lactam(D23/K28) models a conformation highly favorable for nucleation of amyloid. Biochemistry 2005; 44: 6003-6014.
9. Touchette JC, Williams LL, Ajit D, Gallazzi F, Nichols MR. Probing the amyloid-β(1-40) fibril environment with substituted tryptophan residues. Arch. Biochem. Biophys. 2010; 494: 192-197.
10. Finder VH, Vodopivec I, Nitsch RM, Glockshuber R. The recombinant amyloid-β peptide Aβ1-42 aggregates faster and is more neurotoxic than synthetic Aβ1-42. J. Mol. Biol. 2010; 396: 9-18.
11. Anguiano M, Nowak RJ, Lansbury PT Jr. Protofibrillar islet amyloid polypeptide permeabilizes synthetic vesicles by a pore-like mechanism that may be relevant to type II diabetes. Biochemistry 2002; 41: 11338-11343.
12. Chromy BA, Nowak RJ, Lambert MP, Viola KL, Chang L, Velasco PT, Jones BW, Fernandez SJ, Lacor PN, Horowitz P, Finch CE, Krafft GA, Klein WL. Self-assembly of Aβ(1-42) into globular neurotoxins. Biochemistry 2003; 42: 12749-12760.
13. Avidan-Shpalter C, Gazit E. The early stages of amyloid formation: biophysical and structural characterization of human calcitonin pre-fibrillar assemblies. Amyloid 2006; 13: 216-225.
14. Anderson VL, Ramlall TF, Rospigliosi CC, Webb WW, Eliezer D. Identification of a helical intermediate in trifluoroethanol-induced alpha-synuclein aggregation. Proc. Natl. Acad. Sci. U.S.A. 2010; 107: 18850-18855.
15. Stine WB Jr, Dahlgren KN, Krafft GA, LaDu MJ. In vitro characterization of conditions for amyloid-β peptide oligomerization and fibrillogenesis. J. Biol. Chem. 2003; 278: 11612-11622.
16. Wood SJ, Maleeff B, Hart T, Wetzel R. Physical, morphological and functional differences between pH 5.8 and 7.4 aggregates of the Alzheimer's amyloid peptide Aβ. J. Mol. Biol. 1996; 256: 870-877.
17. Dai X, Sun Y, Gao Z, Jiang Z. Copper enhances amyloid-β peptide neurotoxicity and non β-aggregation: a series of experiments conducted upon copper-bound and copper-free amyloid-β peptide. J. Mol. Neurosci. 2010; 41: 66-73.
18. Chaudhary N, Singh S, Nagaraj R. Organic solvent mediated self-association of an amyloid forming peptide from β2-microglobulin: an atomic force microscopy study. Biopolymers 2008; 90: 783-791.
19. Chaudhary N, Singh S, Nagaraj R. Morphology of self-assembled structures formed by short peptides from the amyloidogenic protein tau depends on the solvent in which the peptides are dissolved. J. Pept. Sci. 2009; 15: 675-684.
20. Sanchez L, Madurga S, Pukala T, Vilaseca M, Lopez-Iglesias C, Robinson CV, Giralt E, Carulla N. Aβ40 and Aβ42 amyloid fibrils exhibit distinct molecular recycling properties. J. Am. Chem. Soc. 2011; 133: 6505-6508.
21. Ban T, Morigaki K, Yagi H, Kawasaki T, Kobayashi A, Yuba S, Naiki H, Goto Y. Real-time and single fibril observation of the formation of amyloid β spherulitic structures. J. Biol. Chem. 2006; 281: 33677-33683.
22. Exley C, House E, Collingwood JF, Davidson MR, Cannon D, Donald AM. Spherulites of amyloid-β42 in vitro and in Alzheimer's disease. J. Alzheimers Dis. 2010; 20: 1159-1165.
23. Matsumura S, Shinoda K, Yamada M, Yokojima S, Inoue M, Ohnishi T, Shimada T, Kikuchi K, Masui D, Hashimoto S, Sato M, Ito A, Akioka M, Takagi S, Nakamura Y, Nemoto K, Hasegawa Y, Takamoto H, Inoue H, Nakamura S, Nabeshima Y, Teplow DB, Kinjo M, Hoshi M. Two distinct amyloid β-protein (Aβ) assembly pathways leading to oligomers and fibrils identified by combined fluorescence correlation spectroscopy, morphology, and toxicity analyses. J. Biol. Chem. 2011; 286: 11555-11562.
24. Lu K, Jacob J, Thiyagarajan P, Conticello VP, Lynn DG. Exploiting amyloid fibril lamination for nanotube self-assembly. J. Am. Chem. Soc. 2003; 125: 6391-6393.
25. Chaudhary N, Nagaraj R. Impact on the replacement of Phe by Trp in a short fragment of Aβ amyloid peptide on the formation of fibrils. J. Pept. Sci. 2011; 17: 115-123.
26. Arimon M, Diez-Perez I, Kogan MJ, Durany N, Giralt E, Sanz F, Fernandez-Busquets X. Fine structure study of Aβ1-42 fibrillogenesis with atomic force microscopy. FASEB J. 2005; 19: 1344-1346.
27. Mastrangelo IA, Ahmed M, Sato T, Liu W, Wang C, Hough P, Smith SO. High-resolution atomic force microscopy of soluble Aβ42 oligomers. J. Mol. Biol. 2006; 358: 106-119.
28. Sato T, Kienlen-Campard P, Ahmed M, Liu W, Li H, Elliott JI, Aimoto S, Constantinescu SN, Octave JN, Smith SO. Inhibitors of amyloid toxicity based on β-sheet packing of Aβ40 and Aβ42. Biochemistry 2006; 45: 5503-5516.
29. Sreerama N, Woody RW. Estimation of protein secondary structure from circular dichroism spectra: comparison of CONTIN, SELCON, and CDSSTR methods with an expanded reference set. Anal. Biochem. 2000; 287: 252-260.
30. Sreerama N, Woody RW. On the analysis of membrane protein circular dichroism spectra. Protein Sci. 2004; 13: 100-112.
31. Torok M, Milton S, Kayed R, Wu P, McIntire T, Glabe CG, Langen R. Structural and dynamic features of Alzheimer's Aβ peptide in amyloid fibrils studied by site-directed spin labeling. J. Biol. Chem. 2002; 277: 40810-40815.
32. Petkova AT, Ishii Y, Balbach JJ, Antzutkin ON, Leapman RD, Delaglio F, Tycko R. A structural model for Alzheimer's β -amyloid fibrils based on experimental constraints from solid state NMR. Proc. Natl. Acad. Sci. U.S.A. 2002; 99: 16742-16747.
33. Luhrs T, Ritter C, Adrian M, Riek-Loher D, Bohrmann B, Dobeli H, Schubert D, Riek R. 3D structure of Alzheimer's amyloid-β(1-42) fibrils. Proc. Natl. Acad. Sci. U.S.A. 2005; 102: 17342-17347.
34. Gupta M, Bagaria A, Mishra A, Mathur P, Basu A, Ramakumar S, Chauhan VS. Self-assembly of a dipeptide- containing conformationally restricted dehydrophenylalanine residue to form ordered nanotubes. Adv. Mater. 2007; 19: 858-861.
35. Krysmann MJ, Castelletto V, Kelarakis A, Hamley IW, Hule RA, Pochan DJ. Self-assembly and hydrogelation of an amyloid peptide fragment. Biochemistry 2008; 47: 4597-4605.
36. Jackson M, Mantsch HH. The use and misuse of FTIR spectroscopy in the determination of protein structure. Crit. Rev. Biochem. Mol. Biol. 1995; 30: 95-120.
37. Zurdo J, Guijarro JI, Dobson CM. Preparation and characterization of purified amyloid fibrils. J. Am. Chem. Soc. 2001; 123: 8141-8142.
38. Andersen CB, Hicks MR, Vetri V, Vandahl B, Rahbek-Nielsen H, Thogersen H, Thogersen IB, Enghild JJ, Serpell LC, Rischel C, Otzen DE. Glucagon fibril polymorphism reflects differences in protofilament backbone structure. J. Mol. Biol. 2010; 397: 932-946.
39. Haris PI, Chapman D. The conformational analysis of peptides using Fourier transform IR spectroscopy. Biopolymers 1995; 37: 251-263.
40. Pelton JT, McLean LR. Spectroscopic methods for analysis of protein secondary structure. Anal. Biochem. 2000; 277: 167-176.
41. Surewicz WK, Mantsch HH, Chapman D. Determination of protein secondary structure by Fourier transform infrared spectroscopy: a critical assessment. Biochemistry 1993; 32: 389-394.
42. Juszczyk P, Kolodziejczyk AS, Grzonka Z. FTIR spectroscopic studies on aggregation process of the β-amyloid 11-28 fragment and its variants. J. Pept. Sci. 2009; 15: 23-29.
43. Santini S, Wei G, Mousseau N, Derreumaux P. Pathway complexity of Alzheimer's β-amyloid Aβ16-22 peptide assembly. Structure 2004; 12: 1245-1255.
44. Jakob-Roetne R, Jacobsen H. Alzheimer's disease: from pathology to therapeutic approaches. Angew. Chem. Int. Ed Engl. 2009; 48: 3030-3059.
45. Kuo YM, Emmerling MR, Vigo-Pelfrey C, Kasunic TC, Kirkpatrick JB, Murdoch GH, Ball MJ, Roher AE. Water-soluble Aβ (N-40, N-42) oligomers in normal and Alzheimer disease brains. J. Biol. Chem. 1996; 271: 4077-4081.
46. Haass C, Selkoe DJ. Soluble protein oligomers in neurodegeneration: lessons from the Alzheimer's amyloid β-peptide. Nat. Rev. Mol. Cell Biol. 2007; 8: 101-112.
47. Goldsbury C, Frey P, Olivieri V, Aebi U, Muller SA. Multiple assembly pathways underlie amyloid-β fibril polymorphisms. J. Mol. Biol. 2005; 352: 282-298.
48. Losic D, Martin LL, Mechler A, Aguilar MI, Small DH. High resolution scanning tunnelling microscopy of the β-amyloid protein (Aβ1-40) of Alzheimer's disease suggests a novel mechanism of oligomer assembly. J. Struct. Biol. 2006; 155: 104-110.
49. Meinhardt J, Sachse C, Hortschansky P, Grigorieff N, Fandrich M. Aβ(1-40) fibril polymorphism implies diverse interaction patterns in amyloid fibrils. J. Mol. Biol. 2009; 386: 869-877.
50. Ward RV, Jennings KH, Jepras R, Neville W, Owen DE, Hawkins J, Christie G, Davis JB, George A, Karran EH, Howlett DR. Fractionation and characterization of oligomeric, protofibrillar and fibrillar forms of β-amyloid peptide. Biochem. J. 2000; 348 Pt 1: 137-144.
51. Cheon M, Chang I, Mohanty S, Luheshi LM, Dobson CM, Vendruscolo M, Favrin G. Structural reorganisation and potential toxicity of oligomeric species formed during the assembly of amyloid fibrils. PLoS Comput. Biol. 2007; 3: 1727-1738.
52. Gordon DJ, Sciarretta KL, Meredith SC. Inhibition of β-amyloid(40) fibrillogenesis and disassembly of β-amyloid(40) fibrils by short β-amyloid congeners containing N-methyl amino acids at alternate residues. Biochemistry 2001; 40: 8237-8245.
53. Green JD, Goldsbury C, Kistler J, Cooper GJ, Aebi U. Human amylin oligomer growth and fibril elongation define two distinct phases in amyloid formation. J. Biol. Chem. 2004; 279: 12206-12212.
54. Lesne S, Koh MT, Kotilinek L, Kayed R, Glabe CG, Yang A, Gallagher M, Ashe KH. A specific amyloid-β protein assembly in the brain impairs memory. Nature 2006; 440: 352-357.
55. Ryu J, Girigoswami K, Ha C, Ku SH, Park CB. Influence of multiple metal ions on β-amyloid aggregation and dissociation on a solid surface. Biochemistry 2008; 47: 5328-5335.
56. Aileen Funke S, van Groen T, Kadish I, Bartnik D, Nagel-Steger L, Brener O, Sehl T, Batra-Safferling R, Moriscot C, Schoehn G, Horn AHC, Muller-Schiffmann A, Korth C, Sticht H, Willbold D. Oral treatment with the d-enantiomeric peptide D3 improves the pathology and behavior of Alzheimer's disease transgenic mice. ACS Chem. Neurosci. 2010; 1: 639-648.
57. Fulop L, Zarandi M, Soos K, Penke B. Self-assembly of Alzheimer's disease-related amyloid peptides into highly ordered nanostructures. Nanopages 2006; 1: 69-83.
58. Nichols MR, Moss MA, Reed DK, Cratic-McDaniel S, Hoh JH, Rosenberry TL. Amyloid-β protofibrils differ from amyloid-β aggregates induced in dilute hexafluoroisopropanol in stability and morphology. J. Biol. Chem. 2005; 280: 2471-2480.
59. Walsh DM, Hartley DM, Kusumoto Y, Fezoui Y, Condron MM, Lomakin A, Benedek GB, Selkoe DJ, Teplow DB. Amyloid β-protein fibrillogenesis. Structure and biological activity of protofibrillar intermediates. J. Biol. Chem. 1999; 274: 25945-25952.
60. Janek K, Rothemund S, Gast K, Beyermann M, Zipper J, Fabian H, Bienert M, Krause E. Study of the conformational transition of A β(1-42) using D-amino acid replacement analogues. Biochemistry 2001; 40: 5457-5463.
61. Kirkitadze MD, Condron MM, Teplow DB. Identification and characterization of key kinetic intermediates in amyloid β-protein fibrillogenesis. J. Mol. Biol. 2001; 312: 1103-1119.
62. Fezoui Y, Teplow DB. Kinetic studies of amyloid β-protein fibril assembly. Differential effects of alpha-helix stabilization. J. Biol. Chem. 2002; 277: 36948-36954.
63. Arispe N, Pollard HB, Rojas E. Giant multilevel cation channels formed by Alzheimer disease amyloid β-protein [AβP-(1-40)] in bilayer membranes. Proc. Natl. Acad. Sci. U.S.A. 1993; 90: 10573-10577.
64. Lin H, Bhatia R, Lal R. Amyloid β protein forms ion channels: implications for Alzheimer's disease pathophysiology. FASEB J. 2001; 15: 2433-2444.
65. Lal R, Lin H, Quist AP. Amyloid beta ion channel: 3D structure and relevance to amyloid channel paradigm. Biochim. Biophys. Acta 2007; 1768: 1966-1975.
66. Quist A, Doudevski I, Lin H, Azimova R, Ng D, Frangione B, Kagan B, Ghiso J, Lal R. Amyloid ion channels: a common structural link for protein-misfolding disease. Proc. Natl. Acad. Sci. U.S.A. 2005; 102: 10427-10432.
67. Zhu M, Han S, Zhou F, Carter SA, Fink AL. Annular oligomeric amyloid intermediates observed by in situ atomic force microscopy. J. Biol. Chem. 2004; 279: 24452-24459.
68. Malisauskas M, Zamotin V, Jass J, Noppe W, Dobson CM, Morozova-Roche LA. Amyloid protofilaments from the calcium-binding protein equine lysozyme: formation of ring and linear structures depends on pH and metal ion concentration. J. Mol. Biol. 2003; 330: 879-890.
69. Joshi KB, Verma S. Sequence shuffle controls morphological consequences in a self-assembling tetrapeptide. J. Pept. Sci. 2008; 14: 118-126.
70. Jang H, Arce FT, Ramachandran S, Capone R, Lal R, Nussinov R β-Barrel topology of Alzheimer's β-amyloid ion channels. J. Mol. Biol. 2010; 404: 917-934.