Advertisement

Methods to Characterize the Nanostructure and Molecular Organization of Amphiphilic Peptide Assemblies

  • V. Castelletto
  • I. W. Hamley
Protocol
First Online:
Part of the Methods in Molecular Biology book series (MIMB, volume 1777)

Abstract

Methods to characterize the nanostructure and molecular organization of aggregates of peptides such as amyloid or amphiphilic peptide assemblies are reviewed. We discuss techniques to characterize conformation and secondary structure including circular and linear dichroism and FTIR and Raman spectroscopies, as well as fluorescence methods to detect aggregation. NMR spectroscopy methods, especially solid-state NMR measurements to probe beta-sheet packing motifs, are also briefly outlined. Also discussed are scattering methods including X-ray diffraction and small-angle scattering techniques including SAXS (small-angle X-ray scattering) and SANS (small-angle neutron scattering) and dynamic light scattering. Imaging methods are direct methods to uncover features of peptide nanostructures, and we provide a summary of electron microscopy and atomic force microscopy techniques. Selected examples are highlighted showing data obtained using these techniques, which provide a powerful suite of methods to probe ordering from the molecular scale to the aggregate superstructure.

Key words

Peptides Conformation Secondary structure Characterization methods X-ray diffraction Fluorescence spectroscopy Circular dichroism Linear dichroism FTIR spectroscopy NMR Light scattering Small-angle X-ray scattering (SAXS) Small-angle neutron scattering (SANS) Atomic force microscopy (AFM) Electron microscopy 
This is a preview of subscription content, log in to check access.

Notes

Acknowledgements

This work was supported by EPSRC Platform Grant reference EPSRC EP/L020599/1. We thank our collaborators for their vital contributions to several aspects of our ongoing research, especially in the fields of AFM imaging (Prof Raffaele Mezzenga and Dr. Jozef Adamcik, ETH Zürich) and cryo-TEM imaging (Prof Janne Ruokolainen and his team at Aalto University, Finland).

References

  1. 1.
    Creighton TE (1993) Proteins. Structures and molecular properties. W.H. Freeman, New YorkGoogle Scholar
  2. 2.
    Woolfson DN (2005) The design of coiled-coil structures and assemblies. Adv Protein Chem 70:79–112PubMedCrossRefGoogle Scholar
  3. 3.
    Woolfson DN, Bartlett GJ, Bruning M, Thomson AR (2012) New currency for old rope: from coiled-coil assemblies to α-helical barrels. Curr Opin Struct Biol 11:432–441CrossRefGoogle Scholar
  4. 4.
    Apostolovic B, Danial M, Klok HA (2010) Coiled coils: attractive protein folding motifs for the fabrication of self-assembled, responsive and bioactive materials. Chem Soc Rev 39:3541–3575PubMedCrossRefGoogle Scholar
  5. 5.
    Santoso SS, Vauthey S, Zhang S (2002) Structure, function and applications of amphiphilic peptides. Curr Opin Colloid Interface Sci 7:262–266CrossRefGoogle Scholar
  6. 6.
    Zhang SG (2003) Fabrication of novel biomaterials through molecular self-assembly. Nat Biotechnol 21:1171–1178PubMedPubMedCentralCrossRefGoogle Scholar
  7. 7.
    Zhao X, Zhang S (2004) Fabrication of molecular materials using peptide construction motifs. Trends Biotechnol 22:470–476PubMedCrossRefGoogle Scholar
  8. 8.
    Löwik DWPM, van Hest JCM (2004) Peptide based amphiphiles. Chem Soc Rev 33:234–245PubMedCrossRefGoogle Scholar
  9. 9.
    Cavalli S, Kros A (2008) Scope and applications of amphiphilic alkyl- and lipopeptides. Adv Mater 20:627–631CrossRefGoogle Scholar
  10. 10.
    Versluis F, Marsden HR, Kros A (2010) Power struggles in peptide-amphiphile nanostructures. Chem Soc Rev 39:3434–3444PubMedCrossRefGoogle Scholar
  11. 11.
    Cui HG, Webber MJ, Stupp SI (2010) Self-assembly of peptide amphiphiles: from molecules to nanostructures to biomaterials. Pept Sci 94:1–18CrossRefGoogle Scholar
  12. 12.
    Hamley IW (2011) Self-assembly of amphiphilic peptides. Soft Matter 7:4122–4138CrossRefGoogle Scholar
  13. 13.
    Dehsorkhi A, Castelletto V, Hamley IW (2014) Self-assembling amphiphilic peptides. J Pept Sci 20:453–467PubMedPubMedCentralCrossRefGoogle Scholar
  14. 14.
    Nelson R, Eisenberg D (2006) Recent atomic models of amyloid fibril structure. Curr Opin Struct Biol 16:260–265PubMedCrossRefGoogle Scholar
  15. 15.
    Nelson R, Eisenberg D (2006) Structural models of amyloid-like fibrils. Adv Protein Chem 73:235–282PubMedCrossRefGoogle Scholar
  16. 16.
    Nelson R, Sawaya MR, Balbirnie M, Madsen AO, Riekel C, Grothe R, Eisenberg D (2005) Structure of the cross-β spine of amyloid-like fibrils. Nature (London) 435:773–778CrossRefGoogle Scholar
  17. 17.
    Eanes ED, Glenner GG (1968) X-ray diffraction studies on amyloid filaments. J Histochem Cytochem 16:673–677PubMedCrossRefGoogle Scholar
  18. 18.
    Kirschner DA, Abraham C, Selkoe DJ (1986) X-ray diffraction from intraneuronal paired helical filaments and extraneuronal amyloid fibers in Alzheimer disease indicates cross-β conformation. Proc Natl Acad Sci U S A 83:503–507PubMedPubMedCentralCrossRefGoogle Scholar
  19. 19.
    Sunde M, Blake CCF (1997) The structure of amyloid fibrils by electron microscopy and X-ray diffraction. Adv Protein Chem 50:123–159PubMedCrossRefGoogle Scholar
  20. 20.
    Serpell LC (2000) Alzheimer’s amyloid fibrils: structure and assembly. Biochim Biophys Acta 1502:16–30PubMedCrossRefGoogle Scholar
  21. 21.
    Makin OS, Serpell LC (2005) Structures for amyloid fibrils. FEBS J 272:5950–5961PubMedCrossRefGoogle Scholar
  22. 22.
    Hamley IW, Castelletto V, Moulton CM, Rodriguez-Perez J, Squires AM, Eralp T, Held G, Hicks M, Rodger A (2010) Alignment of a model amyloid peptide fragment in bulk and at a solid surface. J Phys Chem B 114:8244–8254PubMedCrossRefGoogle Scholar
  23. 23.
    Hamley IW (2012) The amyloid beta peptide: a chemist’s perspective. Role in Alzheimer’s and fibrillization. Chem Rev 112:5147–5192PubMedCrossRefGoogle Scholar
  24. 24.
    Morris K, Serpell L (2010) From natural to designer self-assembling biopolymers, the structural characterization of fibrous proteins and peptides using fibre diffraction. Chem Soc Rev 39:3445–3453PubMedCrossRefGoogle Scholar
  25. 25.
    Makin OS, Sikorski P, Serpell LC (2007) CLEARER: a new tool for the analysis of X-ray fibre diffraction patterns and diffraction simulation from atomic structural models. J Appl Crystallogr 40:966–972CrossRefGoogle Scholar
  26. 26.
    Squires AM, Devlin GL, Gras SL, Tickler AK, MacPhee CE, Dobson CM (2006) X-ray scattering study of the effect of hydration on the cross-β structure of amyloid fibrils. J Am Chem Soc 128:11738–11739PubMedCrossRefGoogle Scholar
  27. 27.
    Papapostolou D, Smith AM, Atkins EDT, Oliver SJ, Ryadnov MG, Serpell LC, Woolfson DN (2007) Engineering nanoscale order into a designed protein fiber. Proc Natl Acad Sci U S A 104:10853–10858PubMedPubMedCentralCrossRefGoogle Scholar
  28. 28.
    Banwell EF, Abelardo ES, Adams DJ, Birchall MA, Corrigan A, Donald AM, Kirkland M, Serpell LC, Butler MF, Woolfson DN (2009) Rational design and application of responsive alpha-helical peptide hydrogels. Nat Mater 8:596–600PubMedPubMedCentralCrossRefGoogle Scholar
  29. 29.
    Makin OS, Serpell LC (2004) The structure of amyloid. Fibre Diffraction Review 12:29–35Google Scholar
  30. 30.
    Sunde M, Serpell LC, Bartlam M, Fraser PE, Pepys MB, Blake CCF (1997) Common core structure of amyloid fibrils by synchrotron X-ray diffraction. J Mol Biol 273:729–739PubMedCrossRefGoogle Scholar
  31. 31.
    Hill RJA, Sedman VL, Allen S, Williams PM, Paoli M, Adler-Abramovich L, Eaves L, Tendler SJB (2007) Alignment of aromatic peptide tubes in strong magnetic fields. Adv Mater 19:4474–4479CrossRefGoogle Scholar
  32. 32.
    Hamley IW (2007) Peptide fibrillisation. Angew Chem 46:8128–8147CrossRefGoogle Scholar
  33. 33.
    Levine H (1993) Thioflavine T interaction with synthetic Alzheimer’s disease β-amyloid peptides: detection of amyloid aggregation in solution. Protein Sci 2:404–410PubMedPubMedCentralCrossRefGoogle Scholar
  34. 34.
    Wood SJ, Maleef B, Hart T, Wetzel R (1996) Physical, morphological and functional differences between pH 5.8 and 7.4 aggregates of the Alzheimer’s amyloid peptide Aβ. J Mol Biol 256:870–877PubMedCrossRefGoogle Scholar
  35. 35.
    Hamley IW (2007) Introduction to soft matter, Revised edn. Wiley, ChichesterGoogle Scholar
  36. 36.
    Kalyanasundaram K, Thomas JK (1977) Environmental effects on vibronic band intensities in pyrene monomer fluorescence and their application in studies of micellar systems. J Am Chem Soc 99:2039–2044CrossRefGoogle Scholar
  37. 37.
    Winnik FM (1993) Photophysics of preassociated pyrenes in aqueous polymer-solutions and in other organized media. Chem Rev 93:587–614CrossRefGoogle Scholar
  38. 38.
    Guler MO, Claussen RC, Stupp SI (2005) Encapsulation of pyrene within self-assembled peptide amphiphile nanofibers. J Mater Chem 15:4507–4512CrossRefGoogle Scholar
  39. 39.
    Sabate R, Estelrich J (2005) Evidence of the existence of micelles in the fibrillogenesis of beta-amyloid peptide. J Phys Chem B 109:11027–11032PubMedCrossRefGoogle Scholar
  40. 40.
    Castelletto V, Cheng G, Greenland BW, Hamley IW (2011) Tuning the self-assembly of the bioactive dipeptide L-carnosine by incorporation of a bulky aromatic substituent. Langmuir 27:2980–2988PubMedCrossRefGoogle Scholar
  41. 41.
    Castelletto V, Cheng G, Stain C, Connon CJ, Hamley IW (2012) Self-assembly of a peptide amphiphile containing L-carnosine and its mixtures with a multilamellar vesicle forming lipid. Langmuir 28:11599–11608PubMedCrossRefGoogle Scholar
  42. 42.
    Jones RR, Castelletto V, Connon CJ, Hamley IW (2013) Collagen stimulating effect of peptide amphiphile C16-KTTKS on human fibroblasts. Mol Pharm 10:1063–1069PubMedCrossRefGoogle Scholar
  43. 43.
    Castelletto V, Gouveia RJ, Connon CJ, Hamley IW (2013) New RGD-peptide amphiphile mixtures containing a negatively charged diluent. Faraday Discuss 166:381–397PubMedCrossRefGoogle Scholar
  44. 44.
    Hamley IW, Dehsorkhi A, Castelletto V (2013) Coassembly in binary mixtures of peptide amphiphiles containing oppositely charged residues. Langmuir 29:5050–5059PubMedCrossRefGoogle Scholar
  45. 45.
    Castelletto V, Gouveia RJ, Connon CJ, Hamley IW, Seitsonen J, Nykänen A, Ruokolainen J (2014) Alanine-rich amphiphilic peptide containing the RGD cell adhesion motif: a coating material for human fibroblast attachment and culture. Biomater Sci 2:362–369CrossRefGoogle Scholar
  46. 46.
    Fowler M, Siddique B, Duhamel J (2013) Effect of sequence on the ionization behavior of a series of amphiphilic polypeptides. Langmuir 29:4451–4459PubMedCrossRefGoogle Scholar
  47. 47.
    Hamley IW, Kirkham S, Dehsorkhi A, Castelletto V, Reza M, Ruokolainen J (2014) Toll-like receptor agonist lipopeptides self-assemble into distinct nanostructures. Chem Commun 50:15948–15951CrossRefGoogle Scholar
  48. 48.
    Wilhelm M, Zhao C-L, Wang Y, Xu R, Winnik MA, Mura J-L, Riess G, Croucher MD (1991) Poly(styrene-ethylene oxide) block copolymer micelle formation in water: a fluorescence probe study. Macromolecules 24:1033–1040CrossRefGoogle Scholar
  49. 49.
    Johnsson M, Hansson P, Edwards K (2001) Spherical micelles and other self-assembled structures in dilute aqeuous mixtures of poly(ethylene glycol) lipids. J Phys Chem B 105:8420–8430CrossRefGoogle Scholar
  50. 50.
    Decandio CC, Silva ER, Hamley IW, Castelletto V, Liberato MS, Oliveira VX, Oliveira CLP, Alves WA (2015) Self-assembly of a designed alternating arginine/phenylalanine oligopeptide. Langmuir 31:4513–4523PubMedCrossRefGoogle Scholar
  51. 51.
    LeVine H (1999) Quantification of β-sheet amyloid fibril structures with thioflavin T. In: Wetzel R (ed) Methods in enzymology, vol 309. Academic, San Diego, pp 274–284Google Scholar
  52. 52.
    Santra MK, Banerjee A, Krishnakumar SS, Rahaman O, Panda D (2004) Multiple-probe analysis of folding and unfolding pathways of human serum albumin - evidence for a framework mechanism of folding. Eur J Biochem 271:1789–1797PubMedCrossRefGoogle Scholar
  53. 53.
    Jha S, Snell JM, Sheftic SR, Patil SM, Daniels SB, Kolling FW, Alexandrescu AT (2014) pH dependence of amylin fibrillization. Biochemistry 53:300–310PubMedCrossRefGoogle Scholar
  54. 54.
    van den Heuvel M, Baptist H, Venema P, van der Linden E, Löwik D, van Hest JCM (2011) Mechanical and thermal stabilities of peptide amphiphile fibres. Soft Matter 7:9737–9743CrossRefGoogle Scholar
  55. 55.
    Nagai A, Nagai Y, Qu HJ, Zhang SG (2007) Dynamic behaviors of lipid-like self-assembling peptide A6D and A6K nanotubes. J Nanosci Nanotechnol 7:2246–2252PubMedCrossRefGoogle Scholar
  56. 56.
    Khoe U, Yang YL, Zhang SG (2008) Synergistic effect and hierarchical nanostructure formation in mixing two designer lipid-like peptide surfactants ac-A6D-OH and ac-A6K-NH2. Macromol Biosci 8:1060–1067PubMedCrossRefGoogle Scholar
  57. 57.
    Hamley IW, Nutt DR, Brown GD, Miravet JF, Escuder B, Rodríguez-Llansola F (2010) Influence of the solvent on the self-assembly of a modified amyloid beta peptide fragment. II. NMR and computer simulation investigation. J Phys Chem B 114:940–951PubMedCrossRefGoogle Scholar
  58. 58.
    Miravet JF, Escuder B, Segarra-Maset MD, Tena-Solsona M, Hamley IW, Dehsorkhi A, Castelletto V (2013) Self-assembly of a peptide amphiphile: transition from nanotape fibrils to micelles. Soft Matter 9:3558–3564CrossRefGoogle Scholar
  59. 59.
    Girych M, Gorbenko G, Trusova V, Adachi E, Mizuguchi C, Nagao K, Kawashima H, Akaji K, Lund-Katz S, Phillips MC, Saito H (2014) Interaction of thioflavin T with amyloid fibrils of apolipoprotein A-I N-terminal fragment: resonance energy transfer study. J Struct Biol 185:116–124PubMedCrossRefGoogle Scholar
  60. 60.
    Kelly SM, Jess TJ, Price NC (2005) How to study proteins by circular dichroism. Biochim Biophys Acta 1751:119–139PubMedCrossRefGoogle Scholar
  61. 61.
    Woody RW (1995) Circular dichroism. Methods Enzymol 246:34–71PubMedCrossRefGoogle Scholar
  62. 62.
    Shi ZS, Woody RW, Kallenbach NR (2002) Is polyproline II a major backbone conformation in unfolded proteins? In: Rose GD (ed) Unfolded proteins, Advances in protein chemistry, vol 62. Academic, San Diego, pp 163–240CrossRefGoogle Scholar
  63. 63.
    Paramonov SE, Jun H-W, Hartgerink JD (2006) Self-assembly of peptide-amphiphile nanofibers: the roles of hydrogen bonding and amphiphilic packing. J Am Chem Soc 128:7291–7298PubMedCrossRefGoogle Scholar
  64. 64.
    Woody RW (2009) Circular dichroism spectrum of peptides in the poly(pro)II conformation. J Am Chem Soc 131:8234–8245PubMedCrossRefGoogle Scholar
  65. 65.
    Castelletto V, Hamley IW, Cenker C, Olsson U, Adamcik J, Mezzenga R, Miravet JF, Escuder B, Rodriguez-Llansola F (2011) Influence of end-capping on the self-assembly of model amyloid peptide fragments. J Phys Chem B 115:2107–2116PubMedCrossRefGoogle Scholar
  66. 66.
    Bulheller BM, Rodger A, Hirst JD (2007) Circular and linear dichroism of proteins. Phys Chem Chem Phys 9:2020–2035PubMedCrossRefGoogle Scholar
  67. 67.
    Reed J, Reed A (1997) A set of constructed type spectra for the practical estimation of peptide secondary structure from circular dichroism. Anal Biochem 254:36–40PubMedCrossRefGoogle Scholar
  68. 68.
    Rodger A, Nordén B (1997) Circular dichroism and linear dichroism. Oxford University Press, OxfordGoogle Scholar
  69. 69.
    Nordén B, Rodger A, Dafforn TR (2010) Linear dichroism and circular dichroism: a textbook on polarized-light spectroscopy. Royal Society of Chemistry, CambridgeGoogle Scholar
  70. 70.
    Surewicz WK, Mantsch HH, Chapman D (1993) Determination of protein secondary structure by Fourier transform infrared spectroscopy: a critical assessment. Biochemistry 32:389–394PubMedCrossRefGoogle Scholar
  71. 71.
    Stuart B (1997) Biological applications of infrared spectroscopy. Wiley, ChichesterGoogle Scholar
  72. 72.
    Jackson M, Mantsch HH (1995) The use and misuse of FTIR spectroscopy in the determination of protein structure. Crit Rev Biochem Mol Biol 30:95–120PubMedCrossRefGoogle Scholar
  73. 73.
    Hiramatsu H, Kitagawa T (2005) FT-IR approaches on amyloid fibril structure. Biochim Biophys Acta 1753:100–107PubMedCrossRefGoogle Scholar
  74. 74.
    Haris P, Chapman D (1995) The conformational analysis of peptide using Fourier transform IR spectroscopy. Biopolymers 37:251–263PubMedCrossRefGoogle Scholar
  75. 75.
    Barth A, Zscherp C (2002) What vibrations tell us about proteins. Q Rev Biophys 35:369–430PubMedCrossRefGoogle Scholar
  76. 76.
    Kubelka J, Keiderling TA (2001) The anomalous infrared amide I intensity distribution in 13C isotopically labeled peptide β-sheets comes from extended, multiple-stranded structures. An ab initio study. J Am Chem Soc 123:6142–6150PubMedCrossRefGoogle Scholar
  77. 77.
    Krimm S, Bandekar J (1986) Vibrational spectroscopy and conformation of peptides, polypeptides and proteins. Adv Protein Chem 38:181–364PubMedCrossRefGoogle Scholar
  78. 78.
    Bellamy LJ (1975) The infra-red spectra of complex molecules. Chapman and Hall, LondonCrossRefGoogle Scholar
  79. 79.
    Castelletto V, Moulton CM, Cheng G, Hamley IW, Hicks MR, Rodger A, López-Pérez DE, Revilla-López G, Alemán C (2011) Self-assembly of fmoc-tetrapeptides based on the RGDS cell adhesion motif. Soft Matter 7:11405–11415CrossRefGoogle Scholar
  80. 80.
    Pelton JT, McLean LR (2000) Spectroscopic methods for analysis of protein secondary structure. Anal Biochem 277:167–176PubMedCrossRefGoogle Scholar
  81. 81.
    Gaussier H, Morency H, Lavoie MC, Subirade M (2002) Replacement of trifluoroacetic acid with HCl in the hydrophobic purification steps of pediocin PA-1: a structural effect. Appl Environ Microbiol 68:4803–4808PubMedPubMedCentralCrossRefGoogle Scholar
  82. 82.
    Eker F, Griebenow K, Schweitzer-Stenner R (2004) Aβ1-28 fragment of the amyloid peptide predominantly adopts a polypropyline II conformation in acidic solution. Biochemistry 43:6893–6898PubMedCrossRefGoogle Scholar
  83. 83.
    Liang Y, Pingali SV, Jogalekar AS, Snyder JP, Thiyagarajan P, Lynn DG (2008) Cross-strand pairing and amyloid assembly. Biochemistry 47:10018–10026PubMedCrossRefGoogle Scholar
  84. 84.
    Mehta AK, Lu K, Childers WS, Liang S, Dong J, Snyder JP, Pingali SV, Thiyagarajan P, Lynn DG (2008) Facial symmetry in protein self-assembly. J Am Chem Soc 130:9829–9835PubMedCrossRefGoogle Scholar
  85. 85.
    Rodríguez-Pérez J, Hamley IW, Gras SL, Squires AM (2012) Local orientational disorder in peptide fibrils probed by a combination of residue-specific 13C-18O labelling, polarised infrared spectroscopy and molecular combing. Chem Commun 48:11835–11837CrossRefGoogle Scholar
  86. 86.
    Middleton DA, Madine J, Castelletto V, Hamley IW (2013) New insights into the molecular architecture of a peptide nanotube using FTIR and solid-state NMR spectroscopy combined with sample alignment. Angew Chem Int Ed Engl 52:10537–10540PubMedPubMedCentralCrossRefGoogle Scholar
  87. 87.
    Rodriguez-Perez J, Hamley IW, Squires AM (2011) Infrared linear dichroism spectroscopy on amyloid fibrils aligned by molecular combing. Biomacromolecules 12:1810–1821PubMedCrossRefGoogle Scholar
  88. 88.
    Nafie LA (1997) Infrared and raman vibrational optical activity: theoretical and experimental aspects. Annu Rev Phys Chem 48:357–386PubMedCrossRefGoogle Scholar
  89. 89.
    Keiderling TA (2002) Protein and peptide secondary structure and conformational determination with vibrational circular dichroism. Curr Opin Chem Biol 6:682–688PubMedCrossRefGoogle Scholar
  90. 90.
    Costa PR, Kocisko DA, Sun BQ, Lansbury PT, Griffin RG (1997) Determination of peptide amide configuration in a model amyloid fibril by solid-state NMR. J Am Chem Soc 119:10487–10493CrossRefGoogle Scholar
  91. 91.
    Benzinger TLS, Gregory DM, Burkoth TS, Miller-Auer H, Lynn DG, Botto RE, Meredith SC (2000) Two-dimensional structure of β-amyloid(10-35) fibrils. Biochemistry 39:3491–3499PubMedCrossRefGoogle Scholar
  92. 92.
    Siemer AB, Ritter C, Ernst M, Riek R, Meier BH (2005) High-resolution solid-state NMR spectroscopy of the prion protein HET-s in its amyloid conformation. Angew Chem Int Ed Engl 44:2441–2444PubMedCrossRefGoogle Scholar
  93. 93.
    Heise H, Hoyer W, Becker S, Andronesi OC, Riedel D, Baldus M (2005) Molecular-level secondary structure, polymorphism, and dynamics of full-length alpha-synuclein fibrils studied by solid-state NMR. Proc Natl Acad Sci U S A 102:15871–15876PubMedPubMedCentralCrossRefGoogle Scholar
  94. 94.
    Balbach JJ, Ishii Y, Antzutkin ON, Leapman RD, Rizzo NW, Dyda F, Reed J, Tycko R (2000) Amyloid fibril formation by Aβ16-22, a seven-residue fragment of the Alzheimer’s β-amyloid peptide, and structural characterization by solid state NMR. Biochemistry 39:13748–13759PubMedCrossRefGoogle Scholar
  95. 95.
    Ma BY, Nussinov R (2002) Stabilities and conformations of Alzheimer’s beta-amyloid peptide oligomers (Aβ16-22, Aβ16-35, and Aβ10-35): sequence effects. Proc Natl Acad Sci U S A 99:14126–14131PubMedPubMedCentralCrossRefGoogle Scholar
  96. 96.
    Tycko R (2004) Progress towards a molecular-level structural understanding of amyloid fibrils. Curr Opin Struct Biol 14:96–103PubMedCrossRefGoogle Scholar
  97. 97.
    Tycko R (2006) Molecular structure of amyloid fibrils: insights from solid-state NMR. Q Rev Biophys 39:1–55PubMedPubMedCentralCrossRefGoogle Scholar
  98. 98.
    Lührs T, Ritter C, Adrian M, Riek-Loher D, Bohrmann B, Döbeli H, Schubert D, Riek R (2005) 3D structure of Alzheimer’s amyloid-β(1-42) fibrils. Proc Natl Acad Sci U S A 102:17342–17347PubMedPubMedCentralCrossRefGoogle Scholar
  99. 99.
    Castelletto V, Hamley IW, Segarra-Maset MD, Gumbau CB, Miravet JF, Escuder B, Seitsonen J, Ruokolainen J (2014) Tuning chelation by the surfactant-like peptide A6H using predetermined pH values. Biomacromolecules 15:591–598PubMedCrossRefGoogle Scholar
  100. 100.
    Lomakin A, Chung DS, Benedek GB, Kirschner DA, Teplow DB (1996) On the nucleation and growth of amyloid β-protein fibrils: detection of nuclei and quantitation of rate constants. Proc Natl Acad Sci U S A 93:1125–1129PubMedPubMedCentralCrossRefGoogle Scholar
  101. 101.
    Riseman J, Kirkwood JG (1950) J Chem Phys 18:512–516CrossRefGoogle Scholar
  102. 102.
    Pallitto MM, Ghanta J, Heinzelman P, Kiessling LL, Murphy RM (1999) Recognition sequence design for peptidyl modulators of β-amyloid aggregation and toxicity. Biochemistry 38:3570–3578PubMedCrossRefGoogle Scholar
  103. 103.
    Shen C-L, Fitzgerald MC, Murphy RM (1994) Effect of acid predissolution on fibril size and fibril flexibility of synthetic β-amyloid peptide. Biophys J 67:1238–1246PubMedPubMedCentralCrossRefGoogle Scholar
  104. 104.
    Krysmann MJ, Castelletto V, Kelarakis A, Hamley IW, Hule RA, Pochan DJ (2008) Self-assembly and hydrogelation of an amyloid peptide fragment. Biochemistry 47:4597–4605PubMedCrossRefGoogle Scholar
  105. 105.
    Walsh DM, Lomakin A, Benedek GB, Condron MM, Teplow DB (1997) Amyloid β-protein fibrillogenesis. Detection of a protofibrillar intermediate. J Biol Chem 272:22364–22372PubMedCrossRefGoogle Scholar
  106. 106.
    Kusumoto Y, Lomakin A, Teplow DB, Benedek GB (1998) Temperature dependence of amyloid β-protein fibrillization. Proc Natl Acad Sci U S A 95:12277–12282PubMedPubMedCentralCrossRefGoogle Scholar
  107. 107.
    Sokolowski F, Modler AJ, Masuch R, Zirwer D, Baier M, Lutsch G, Moss DA, Gast K, Naumann D (2003) Formation of critical oligomers is a key event during conformational transition of recombinant Syrian hamster prion protein. J Biol Chem 278:40481–40492PubMedCrossRefGoogle Scholar
  108. 108.
    Modler AJ, Gast K, Lutsch G, Damaschun G (2003) Assembly of amyloid protofibrils via critical oligomers—a novel pathway of amyloid formation. J Mol Biol 325:135–148PubMedCrossRefGoogle Scholar
  109. 109.
    Pedersen JS (1997) Analysis of small-angle scattering data from colloids and polymer solutions: modeling and least-squares fitting. Adv Colloid Interf Sci 70:171–210CrossRefGoogle Scholar
  110. 110.
    Hamley IW, Krysmann MJ, Castelletto V, Kelarakis A, Noirez L, Hule RA, Pochan D (2008) Nematic and columnar ordering of a PEG-peptide conjugate in aqueous solution. Chem Eur J 14:11369–11374PubMedCrossRefGoogle Scholar
  111. 111.
    Hamley IW, Krysmann MJ, Castelletto V, Noirez L (2008) Multiple lyotropic polymorphism of a PEG-peptide diblock copolymer in aqueous solution. Adv Mater 20:4394–4397CrossRefGoogle Scholar
  112. 112.
    Pabst G, Rappolt M, Amenitsch H, Laggner P (2000) Structural information from multilamellar liposomes at full hydration: full q-range fitting with high quality X-ray data. Phys Rev E 62:4000–4009CrossRefGoogle Scholar
  113. 113.
    Hamley IW, Dehsorkhi A, Castelletto V (2013) Self-assembled arginine-coated peptide nanosheets in water. Chem Commun 49:1850–1852CrossRefGoogle Scholar
  114. 114.
  115. 115.
    Caillé A (1972) X-ray scattering by smectic-a crystals. CR Hebd Seances Acad Sci (Paris) B 274:891–893Google Scholar
  116. 116.
    Lu K, Jacob J, Thiyagarajan P, Conticello VP, Lynn DG (2003) Exploiting amyloid fibril lamination for nanotube self assembly. J Am Chem Soc 125:6391–6393PubMedCrossRefGoogle Scholar
  117. 117.
    Hamley IW, Dehsorkhi A, Castelletto V, Furzeland S, Atkins D, Seitsonen J, Ruokolainen J (2013) Reversible helical ribbon unwinding transition of a self-assembling peptide amphiphile. Soft Matter 9:9290–9293CrossRefGoogle Scholar
  118. 118.
    Dehsorkhi A, Hamley IW, Seitsonen J, Ruokolainen J (2013) Tuning self-assembled nanostructures through enzymatic degradation of a peptide amphiphile. Langmuir 29:6665–6672PubMedPubMedCentralCrossRefGoogle Scholar
  119. 119.
    Hamley IW, Dehsorkhi A, Jauregi P, Seitsonen J, Ruokolainen J, Coutte F, Chataigné G, Jacques P (2013) Self-assembly of three bacterially-derived bioactive lipopeptides. Soft Matter 9:9572–9578PubMedCrossRefGoogle Scholar
  120. 120.
    Dehsorkhi A, Gouveia RJ, Smith AM, Hamley IW, Castelletto V, Connon CJ, Reza M, Ruokolainen J (2015) Self-assembly of a dual functional bioactive peptide amphiphile incorporating both matrix metalloprotease substrate and cell adhesion motifs. Soft Matter 11:3115–3124PubMedCrossRefGoogle Scholar
  121. 121.
    Adamcik J, Mezzenga R (2012) Study of amyloid fibrils via atomic force microscopy. Curr Opin Colloid Interface Sci 17:369–376CrossRefGoogle Scholar
  122. 122.
    Usov I, Adamcik J, Mezzenga R (2013) Polymorphism in bovine serum albumin fibrils: morphology and statistical analysis. Faraday Discuss 166:151–162PubMedCrossRefGoogle Scholar
  123. 123.
    Usov I, Mezzenga R (2014) Correlation between nanomechanics and polymorphic conformations in amyloid fibrils. ACS Nano 8:11035–11041PubMedCrossRefGoogle Scholar
  124. 124.
    Usov I, Mezzenga R (2015) FiberApp: an open-source software for tracking and analyzing polymers, filaments, biomacromolecules, and fibrous objects. Macromolecules 48:1269–1280CrossRefGoogle Scholar
  125. 125.
    Adamcik J, Lara C, Usov I, Jeong JS, Ruggeri FS, Dietler G, Lashuel HA, Hamley IW, Mezzenga R (2012) Measurement of intrinsic properties of amyloid fibrils by the peak force QNM method. Nanoscale 4:4426–4429PubMedCrossRefGoogle Scholar
  126. 126.
    Cui H, Hodgdon TK, Kaler EW, Abezgaous L, Danino D, Lubovsky M, Talmon Y, Pochan DJ (2007) Elucidating the assembled structure of amphiphiles in solution via cryogenic-transmission electron microscopy. Soft Matter 3:945–955CrossRefGoogle Scholar
  127. 127.
    Castelletto V, Hamley IW, Perez J, Abezgauz L, Danino D (2010) Fibrillar superstructure from extended nanotapes formed by a collagen-stimulating peptide. Chem Commun 46:9185–9187CrossRefGoogle Scholar
  128. 128.
    Castelletto V, Gouveia RJ, Connon CJ, Hamley IW, Seitsonen J, Ruokolainen J, Longo E, Siligardi G (2014) Influence of elastase on alanine-rich peptide hydrogels. Biomater Sci 2:867–874CrossRefGoogle Scholar
  129. 129.
    Hamley IW, Dehsorkhi A, Castelletto V, Walter MNM, Connon CJ, Reza M, Ruokolainen J (2015) Self-assembly and collagen stimulating activity of a peptide amphiphile incorporating a peptide sequence from lumican. Langmuir 31:4490–4495PubMedCrossRefGoogle Scholar
  130. 130.
    Castelletto V, Kirkham S, Hamley IW, Kowalczyk R, Rabe M, Reza M, Ruokolainen J (2016) Self-assembly of the toll-like receptor agonist macrophage-activating lipopeptide MALP-2 and of its constituent peptide. Biomacromolecules 17:631–640PubMedCrossRefGoogle Scholar

Copyright information

© Springer Science+Business Media, LLC, part of Springer Nature 2018

Authors and Affiliations

  1. 1.Department of ChemistryUniversity of ReadingReadingUK

Personalised recommendations

Cite protocol

Buy options