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Protein Microgels from Amyloid Fibril Networks

  • Lianne W. Y. Roode
  • Ulyana ShimanovichEmail author
  • Si Wu
  • Sarah PerrettEmail author
  • Tuomas P. J. KnowlesEmail author
Chapter
First Online:
Part of the Advances in Experimental Medicine and Biology book series (AEMB, volume 1174)

Abstract

Nanofibrillar forms of amyloidogenic proteins were initially discovered in the context of protein misfolding and disease but have more recently been found at the origin of key biological functionality in many naturally occurring functional materials, such as adhesives and biofilm coatings. Their physiological roles in nature reflect their great strength and stability, which has led to the exploration of their use as the basis of artificial protein-based functional materials. Particularly for biomedical applications, they represent attractive building blocks for the development of, for instance, drug carrier agents due to their inherent biocompatibility and biodegradability. Furthermore, the propensity of proteins to self-assemble into amyloid fibrils can be exploited under microconfinement, afforded by droplet microfluidic techniques. This approach allows the generation of multi-scale functional microgels that can host biological additives and can be designed to incorporate additional functionality, such as to aid targeted drug delivery.

Keywords

Self-assembled amyloid fibrils Protein microgels Droplet microfluidics Drug carrier agents Functional materials 
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References

  1. 1.
    Hardy J, Selkoe DJ (2002) The amyloid hypothesis of Alzheimer’s disease: progress and problems on the road to therapeutics. Science 297:353–356PubMedCrossRefGoogle Scholar
  2. 2.
    Haass C, Selkoe DJ (2007) Soluble protein oligomers in neurodegeneration: lessons from the Alzheimer’s amyloid β-peptide. Nat Rev Mol Cell Biol 8:101–112CrossRefGoogle Scholar
  3. 3.
    Ballard C, Gauthier S, Corbett A, Brayne C, Aarsland D, Jones E (2011) Alzheimer’s disease. Lancet Lond Engl 377:1019–1031CrossRefGoogle Scholar
  4. 4.
    Querfurth HW, LaFerla FM (2010) Mechanisms of disease Alzheimer’s disease. N Engl J Med 362:329–344PubMedCrossRefGoogle Scholar
  5. 5.
    Niedowicz DM, Nelson PT, Murphy MP (2011) Alzheimer’s disease: pathological mechanisms and recent insights. Curr Neuropharmacol 9:674–684PubMedPubMedCentralCrossRefGoogle Scholar
  6. 6.
    Dobson CM (1999) Protein misfolding, evolution and disease. Trends Biochem Sci 24:329–332PubMedPubMedCentralCrossRefGoogle Scholar
  7. 7.
    Dobson CM (2003) Protein folding and misfolding. Nature 426:884–890PubMedCrossRefGoogle Scholar
  8. 8.
    Chiti F, Dobson CM (2006) Protein misfolding, functional amyloid, and human disease. Annu Rev Biochem 75:333–366CrossRefGoogle Scholar
  9. 9.
    Knowles TPJ, Vendruscolo M, Dobson CM (2014) The amyloid state and its association with protein misfolding diseases. Nat Rev Mol Cell Biol 15:384–396CrossRefGoogle Scholar
  10. 10.
    Stefani M, Dobson CM (2003) Protein aggregation and aggregate toxicity: new insights into protein folding, misfolding diseases and biological evolution. J Mol Med 81:678–699PubMedCrossRefPubMedCentralGoogle Scholar
  11. 11.
    Fowler DM, Koulov AV, Alory-Jost C, Marks MS, Balch WE, Kelly JW (2006) Functional amyloid formation within mammalian tissue. PLoS Biol 4(1):100–107.  https://doi.org/10.1371/journal.pbio.0040006 CrossRefGoogle Scholar
  12. 12.
    Fowler DM, Koulov AV, Balch WE, Kelly JW (2007) Functional amyloid – from bacteria to humans. Trends Biochem Sci 32:217–224CrossRefGoogle Scholar
  13. 13.
    Otzen D, Nielsen PH (2008) We find them here, we find them there: functional bacterial amyloid. Cell Mol Life Sci 65:910–927PubMedPubMedCentralCrossRefGoogle Scholar
  14. 14.
    Kelly JW, Balch WE (2003) Amyloid as a natural product. J Cell Biol 161:461–462PubMedPubMedCentralCrossRefGoogle Scholar
  15. 15.
    Maji SK, Perrin MH, Sawaya MR et al (2009) Functional amyloids as natural storage of peptide hormones in pituitary secretory granules. Science 325:328–332PubMedPubMedCentralCrossRefGoogle Scholar
  16. 16.
    Bleem A, Daggett V (2017) Structural and functional diversity among amyloid proteins: agents of disease, building blocks of biology, and implications for molecular engineering. Biotechnol Bioeng 114:7–20PubMedCrossRefPubMedCentralGoogle Scholar
  17. 17.
    Mostaert AS, Higgins MJ, Fukuma T, Rindi F, Jarvis SP (2006) Nanoscale mechanical characterisation of amyloid fibrils discovered in a natural adhesive. J Biol Phys 32:393–401PubMedPubMedCentralCrossRefGoogle Scholar
  18. 18.
    Zhong C, Gurry T, Cheng AA, Downey J, Deng Z, Stultz CM, Lu TK (2014) Strong underwater adhesives made by self-assembling multi-protein nanofibres. Nat Nanotechnol 9:858–866PubMedPubMedCentralCrossRefGoogle Scholar
  19. 19.
    Li C, Qin R, Liu R, Miao S, Yang P (2018) Functional amyloid materials at surfaces/interfaces. Biomater Sci 6:462–472PubMedCrossRefPubMedCentralGoogle Scholar
  20. 20.
    Wang D, Ha Y, Gu J, Li Q, Zhang L, Yang P (2016) 2D protein supramolecular nanofilm with exceptionally large area and emergent functions. Adv Mater 28:7414–7423PubMedCrossRefGoogle Scholar
  21. 21.
    Chapman MR, Robinson LS, Pinkner JS, Roth R, Heuser J, Hammar M, Normark S, Hultgren SJ (2002) Role of Escherichia coli curli operons in directing amyloid fiber formation. Science 295:851–855PubMedPubMedCentralCrossRefGoogle Scholar
  22. 22.
    Shorter J, Lindquist S (2005) Prions as adaptive conduits of memory and inheritance. Nat Rev Genet 6:435–450PubMedCrossRefPubMedCentralGoogle Scholar
  23. 23.
    Krishnan R, Lindquist SL (2005) Structural insights into a yeast prion illuminate nucleation and strain diversity. Nature 435:765–772PubMedPubMedCentralCrossRefGoogle Scholar
  24. 24.
    Lindquist SL, Henikoff S (2002) Self-perpetuating structural states in biology, disease, and genetics. Proc Natl Acad Sci U S A 99:16377PubMedPubMedCentralCrossRefGoogle Scholar
  25. 25.
    Tanaka M, Collins SR, Toyama BH, Weissman JS (2006) The physical basis of how prion conformations determine strain phenotypes. Nature 442:585–589PubMedCrossRefPubMedCentralGoogle Scholar
  26. 26.
    DePace AH, Weissman JS (2002) Origins and kinetic consequences of diversity in Sup35 yeast prion fibers. Nat Struct Mol Biol 9:389–396Google Scholar
  27. 27.
    Lashuel HA, Hartley D, Petre BM, Walz T, Lansbury PT (2002) Neurodegenerative disease: amyloid pores from pathogenic mutations. Nature 418:291–291 PubMedCrossRefPubMedCentralGoogle Scholar
  28. 28.
    Bucciantini M, Giannoni E, Chiti F, Baroni F, Formigli L, Zurdo J, Taddei N, Ramponi G, Dobson CM, Stefani M (2002) Inherent toxicity of aggregates implies a common mechanism for protein misfolding diseases. Nature 416:507–511CrossRefGoogle Scholar
  29. 29.
    Walsh DM, Klyubin I, Fadeeva JV, Cullen WK, Anwyl R, Wolfe MS, Rowan MJ, Selkoe DJ (2002) Naturally secreted oligomers of amyloid β protein potently inhibit hippocampal long-term potentiation in vivo. Nature 416:535–539CrossRefGoogle Scholar
  30. 30.
    Caughey B, Peter T, Lansbury J (2003) Protofibirls, pores, fibrils, and neurodegeneration: separating the responsible protein aggregates from the innocent bystanders. Annu Rev Neurosci 26:267–298PubMedCrossRefGoogle Scholar
  31. 31.
    Koffie RM, Meyer-Luehmann M, Hashimoto T et al (2009) Oligomeric amyloid β associates with postsynaptic densities and correlates with excitatory synapse loss near senile plaques. Proc Natl Acad Sci U S A 106:4012–4017PubMedPubMedCentralCrossRefGoogle Scholar
  32. 32.
    Tomic JL, Pensalfini A, Head E, Glabe CG (2009) Soluble fibrillar oligomer levels are elevated in Alzheimer’s disease brain and correlate with cognitive dysfunction. Neurobiol Dis 35:352–358PubMedCrossRefGoogle Scholar
  33. 33.
    Shankar GM, Bloodgood BL, Townsend M, Walsh DM, Selkoe DJ, Sabatini BL (2007) Natural oligomers of the Alzheimer amyloid-β protein induce reversible synapse loss by modulating an NMDA-type glutamate receptor-dependent signaling pathway. J Neurosci 27:2866–2875PubMedCrossRefGoogle Scholar
  34. 34.
    Hammer ND, Schmidt JC, Chapman MR (2007) The curli nucleator protein, CsgB, contains an amyloidogenic domain that directs CsgA polymerization. Proc Natl Acad Sci U S A 104:12494–12499PubMedPubMedCentralCrossRefGoogle Scholar
  35. 35.
    Knowles TP, Fitzpatrick AW, Meehan S, Mott HR, Vendruscolo M, Dobson CM, Welland ME (2007) Role of intermolecular forces in defining material properties of protein nanofibrils. Science 318:1900–1903PubMedCrossRefGoogle Scholar
  36. 36.
    Knowles TPJ, Buehler MJ (2011) Nanomechanics of functional and pathological amyloid materials. Nat Nanotechnol 6:469–479PubMedPubMedCentralCrossRefGoogle Scholar
  37. 37.
    Chiti F, Webster P, Taddei N, Clark A, Stefani M, Ramponi G, Dobson CM (1999) Designing conditions for in vitro formation of amyloid protofilaments and fibrils. Proc Natl Acad Sci U S A 96:3590–3594PubMedCrossRefGoogle Scholar
  38. 38.
    Chiti F, Dobson CM (2009) Amyloid formation by globular proteins under native conditions. Nat Chem Biol 5:15–22PubMedCrossRefGoogle Scholar
  39. 39.
    Pawar AP, DuBay KF, Zurdo J, Chiti F, Vendruscolo M, Dobson CM (2005) Prediction of “aggregation-prone” and “aggregation-susceptible” regions in proteins associated with neurodegenerative diseases. J Mol Biol 350:379–392PubMedCrossRefGoogle Scholar
  40. 40.
    Knowles TPJ, Mezzenga R (2016) Amyloid fibrils as building blocks for natural and artificial functional materials. Adv Mater 28:6546–6561PubMedPubMedCentralCrossRefGoogle Scholar
  41. 41.
    Shimanovich U, Bernardes GJ, Knowles TP, Cavaco-Paulo A (2014) Protein micro- and nano-capsules for biomedical applications. Chem Soc Rev 43:1361–1371PubMedCrossRefGoogle Scholar
  42. 42.
    Shimanovich U, Efimov I, Mason TO et al (2015) Protein microgels from amyloid fibril networks. ACS Nano 9:43–51CrossRefGoogle Scholar
  43. 43.
    Cao A, Hu D, Lai L (2004) Formation of amyloid fibrils from fully reduced hen egg white lysozyme. Protein Sci Publ Protein Soc 13:319–324CrossRefGoogle Scholar
  44. 44.
    Kelly JW (2002) Towards an understanding of amyloidogenesis. Nat Struct Mol Biol 9:323–325CrossRefGoogle Scholar
  45. 45.
    Teh S-Y, Lin R, Hung L-H, Lee AP (2008) Droplet microfluidics. Lab Chip 8:198–220PubMedCrossRefGoogle Scholar
  46. 46.
    Zhang H, Tumarkin E, Sullan RMA, Walker GC, Kumacheva E (2007) Exploring microfluidic routes to microgels of biological polymers. Macromol Rapid Commun 28:527–538CrossRefGoogle Scholar
  47. 47.
    Seiffert S (2013) Microgel capsules tailored by droplet-based microfluidics. ChemPhysChem 14:295–304PubMedCrossRefPubMedCentralGoogle Scholar
  48. 48.
    Sipe JD, Cohen AS (2000) Review: history of the amyloid fibril. J Struct Biol 130:88–98PubMedCrossRefGoogle Scholar
  49. 49.
    Buxbaum JN, Linke RP (2012) A molecular history of the amyloidoses. J Mol Biol 421:142–159PubMedCrossRefGoogle Scholar
  50. 50.
    Nilsson MR (2004) Techniques to study amyloid fibril formation in vitro. Methods 34:151–160PubMedCrossRefGoogle Scholar
  51. 51.
    Groenning M (2009) Binding mode of Thioflavin T and other molecular probes in the context of amyloid fibrils—current status. J Chem Biol 3:1–18PubMedCrossRefGoogle Scholar
  52. 52.
    Hawe A, Sutter M, Jiskoot W (2008) Extrinsic fluorescent dyes as tools for protein characterization. Pharm Res 25:1487–1499PubMedCrossRefGoogle Scholar
  53. 53.
    Khurana R, Uversky VN, Nielsen L, Fink AL (2001) Is Congo Red an amyloid-specific dye? J Biol Chem 276:22715–22721PubMedPubMedCentralCrossRefGoogle Scholar
  54. 54.
    Hudson SA, Ecroyd H, Kee TW, Carver JA (2009) The thioflavin T fluorescence assay for amyloid fibril detection can be biased by the presence of exogenous compounds. FEBS J 276:5960–5972PubMedCrossRefGoogle Scholar
  55. 55.
    O’Nuallain B, Wetzel R (2002) Conformational Abs recognizing a generic amyloid fibril epitope. Proc Natl Acad Sci 99:1485–1490PubMedCrossRefGoogle Scholar
  56. 56.
    Larsen P, Nielsen JL, Dueholm MS, Wetzel R, Otzen D, Nielsen PH (2007) Amyloid adhesins are abundant in natural biofilms. Environ Microbiol 9:3077–3090CrossRefGoogle Scholar
  57. 57.
    Chan FTS, Kaminski Schierle GS, Kumita JR, Bertoncini CW, Dobson CM, Kaminski CF (2013) Protein amyloids develop an intrinsic fluorescence signature during aggregation. Analyst 138:2156–2162PubMedCrossRefGoogle Scholar
  58. 58.
    Kaminski Schierle GS, Bertoncini CW, Chan FTS et al (2011) A FRET sensor for non-invasive imaging of amyloid formation in vivo. Chemphyschem Eur J Chem Phys Phys Chem 12:673–680CrossRefGoogle Scholar
  59. 59.
    Chen W, Young LJ, Lu M, Zaccone A, Ströhl F, Yu N, Kaminski Schierle GS, Kaminski CF (2017) Fluorescence self-quenching from reporter dyes informs on the structural properties of amyloid clusters formed in vitro and in cells. Nano Lett 17:143–149PubMedCrossRefGoogle Scholar
  60. 60.
    Fändrich M (2007) On the structural definition of amyloid fibrils and other polypeptide aggregates. Cell Mol Life Sci 64:2066–2078PubMedCrossRefGoogle Scholar
  61. 61.
    Greenwald J, Riek R (2010) Biology of amyloid: structure, function, and regulation. Structure 18:1244–1260PubMedCrossRefGoogle Scholar
  62. 62.
    Eisenberg D, Jucker M (2012) The amyloid state of proteins in human diseases. Cell 148:1188–1203PubMedPubMedCentralCrossRefGoogle Scholar
  63. 63.
    Sawaya MR, Sambashivan S, Nelson R et al (2007) Atomic structures of amyloid cross-β spines reveal varied steric zippers. Nature 447:453–457CrossRefGoogle Scholar
  64. 64.
    Petkova AT, Ishii Y, Balbach JJ, Antzutkin ON, Leapman RD, Delaglio F, Tycko R (2002) A structural model for Alzheimer’s β-amyloid fibrils based on experimental constraints from solid state NMR. Proc Natl Acad Sci 99:16742–16747PubMedCrossRefGoogle Scholar
  65. 65.
    Wasmer C, Lange A, Van Melckebeke H, Siemer AB, Riek R, Meier BH (2008) Amyloid fibrils of the HET-s(218-289) prion form a beta solenoid with a triangular hydrophobic core. Science 319:1523–1526CrossRefGoogle Scholar
  66. 66.
    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
  67. 67.
    Ritter C, Maddelein M-L, Siemer AB, Lührs T, Ernst M, Meier BH, Saupe SJ, Riek R (2005) Correlation of structural elements and infectivity of the HET-s prion. Nature 435:844–848PubMedPubMedCentralCrossRefGoogle Scholar
  68. 68.
    Tycko R (2011) Solid state NMR studies of amyloid fibril structure. Annu Rev Phys Chem 62:279–299PubMedPubMedCentralCrossRefGoogle Scholar
  69. 69.
    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 273:729–739CrossRefGoogle Scholar
  70. 70.
    Makin OS, Atkins E, Sikorski P, Johansson J, Serpell LC (2005) Molecular basis for amyloid fibril formation and stability. Proc Natl Acad Sci U S A 102:315–320PubMedPubMedCentralCrossRefGoogle Scholar
  71. 71.
    Nelson R, Sawaya MR, Balbirnie M, Madsen AØ, Riekel C, Grothe R, Eisenberg D (2005) Structure of the cross-β spine of amyloid-like fibrils. Nature 435:773–778PubMedPubMedCentralCrossRefGoogle Scholar
  72. 72.
    Adamcik J, Mezzenga R (2012) Study of amyloid fibrils via atomic force microscopy. Curr Opin Colloid Interface Sci 17:369–376CrossRefGoogle Scholar
  73. 73.
    Sachse C, Fändrich M, Grigorieff N (2008) Paired β-sheet structure of an Aβ(1-40) amyloid fibril revealed by electron microscopy. Proc Natl Acad Sci 105:7462–7466PubMedCrossRefGoogle Scholar
  74. 74.
    Fitzpatrick AWP, Debelouchina GT, Bayro MJ et al (2013) Atomic structure and hierarchical assembly of a cross-β amyloid fibril. Proc Natl Acad Sci U S A 110:5468–5473PubMedPubMedCentralCrossRefGoogle Scholar
  75. 75.
    Jiménez JL, Guijarro JI, Orlova E, Zurdo J, Dobson CM, Sunde M, Saibil HR (1999) Cryo-electron microscopy structure of an SH3 amyloid fibril and model of the molecular packing. EMBO J 18:815–821PubMedPubMedCentralCrossRefGoogle Scholar
  76. 76.
    Jiménez JL, Nettleton EJ, Bouchard M, Robinson CV, Dobson CM, Saibil HR (2002) The protofilament structure of insulin amyloid fibrils. Proc Natl Acad Sci 99:9196–9201PubMedCrossRefGoogle Scholar
  77. 77.
    Fitzpatrick AWP, Falcon B, He S, Murzin AG, Murshudov G, Garringer HJ, Crowther RA, Ghetti B, Goedert M, Scheres SHW (2017) Cryo-EM structures of tau filaments from Alzheimer’s disease. Nature 547:185–190PubMedPubMedCentralCrossRefGoogle Scholar
  78. 78.
    Wei G, Su Z, Reynolds NP, Arosio P, Hamley IW, Gazit E, Mezzenga R (2017) Self-assembling peptide and protein amyloids: from structure to tailored function in nanotechnology. Chem Soc Rev 46(15):4661–4708.  https://doi.org/10.1039/C6CS00542J CrossRefPubMedPubMedCentralGoogle Scholar
  79. 79.
    Pedersen JS, Andersen CB, Otzen DE (2010) Amyloid structure – one but not the same: the many levels of fibrillar polymorphism. FEBS J 277:4591–4601PubMedCrossRefGoogle Scholar
  80. 80.
    VandenAkker CC, Schleeger M, Bruinen AL, Deckert-Gaudig T, Velikov KP, Heeren RMA, Deckert V, Bonn M, Koenderink GH (2016) Multimodal spectroscopic study of amyloid fibril polymorphism. J Phys Chem B 120:8809–8817PubMedCrossRefGoogle Scholar
  81. 81.
    Pedersen JS, Otzen DE (2008) Amyloid—a state in many guises: survival of the fittest fibril fold. Protein Sci Publ Protein Soc 17:2–10CrossRefGoogle Scholar
  82. 82.
    Fändrich M, Meinhardt J, Grigorieff N (2009) Structural polymorphism of Alzheimer Aβ and other amyloid fibrils. Prion 3:89–93PubMedPubMedCentralCrossRefGoogle Scholar
  83. 83.
    Auer S (2015) Nucleation of polymorphic amyloid fibrils. Biophys J 108:1176–1186PubMedPubMedCentralCrossRefGoogle Scholar
  84. 84.
    Pedersen JS, Dikov D, Flink JL, Hjuler HA, Christiansen G, Otzen DE (2006) The changing face of glucagon fibrillation: structural polymorphism and conformational imprinting. J Mol Biol 355:501–523PubMedCrossRefGoogle Scholar
  85. 85.
    Petkova AT, Leapman RD, Guo Z, Yau W-M, Mattson MP, Tycko R (2005) Self-propagating, molecular-level polymorphism in alzheimer’s ß-amyloid fibrils. Science 307:262–265CrossRefGoogle Scholar
  86. 86.
    Dobson CM, Šali A, Karplus M (1998) Protein folding: a perspective from theory and experiment. Angew Chem Int Ed 37:868–893CrossRefGoogle Scholar
  87. 87.
    DuBay KF, Pawar AP, Chiti F, Zurdo J, Dobson CM, Vendruscolo M (2004) Prediction of the absolute aggregation rates of amyloidogenic polypeptide chains. J Mol Biol 341:1317–1326PubMedCrossRefGoogle Scholar
  88. 88.
    Phan-Xuan T, Durand D, Nicolai T, Donato L, Schmitt C, Bovetto L (2011) On the crucial importance of the pH for the formation and self-stabilization of protein microgels and strands. Langmuir 27:15092–15101PubMedCrossRefGoogle Scholar
  89. 89.
    Uversky VN, Fink AL (2004) Conformational constraints for amyloid fibrillation: the importance of being unfolded. Biochim Biophys Acta BBA 1698:131–153PubMedCrossRefGoogle Scholar
  90. 90.
    Sawyer EB, Claessen D, Gras SL, Perrett S (2012) Exploiting amyloid: how and why bacteria use cross-β fibrils. Biochem Soc Trans 40:728–734PubMedCrossRefGoogle Scholar
  91. 91.
    Auer S, Meersman F, Dobson CM, Vendruscolo M (2008) A generic mechanism of emergence of amyloid protofilaments from disordered oligomeric aggregates. PLoS Comput Biol 4:e1000222PubMedPubMedCentralCrossRefGoogle Scholar
  92. 92.
    Baldwin AJ, Knowles TPJ, Tartaglia GG et al (2011) Metastability of native proteins and the phenomenon of amyloid formation. J Am Chem Soc 133:14160–14163PubMedCrossRefGoogle Scholar
  93. 93.
    Gazit E (2002) The “correctly folded” state of proteins: is it a metastable state? Angew Chem Int Ed 41:257–259CrossRefGoogle Scholar
  94. 94.
    Dobson CM (2001) The structural basis of protein folding and its links with human disease. Philos Trans R Soc Lond Ser B 356:133–145CrossRefGoogle Scholar
  95. 95.
    Cohen SIA, Vendruscolo M, Dobson CM, Knowles TPJ (2012) From macroscopic measurements to microscopic mechanisms of protein aggregation. J Mol Biol 421:160–171 PubMedPubMedCentralCrossRefGoogle Scholar
  96. 96.
    Cohen SIA, Linse S, Luheshi LM, Hellstrand E, White DA, Rajah L, Otzen DE, Vendruscolo M, Dobson CM, Knowles TPJ (2013) Proliferation of amyloid-β42 aggregates occurs through a secondary nucleation mechanism. Proc Natl Acad Sci 110:9758–9763PubMedPubMedCentralCrossRefGoogle Scholar
  97. 97.
    Knowles TPJ, Waudby CA, Devlin GL, Cohen SIA, Aguzzi A, Vendruscolo M, Terentjev EM, Welland ME, Dobson CM (2009) An analytical solution to the kinetics of breakable filament assembly. Science 326:1533–1537PubMedPubMedCentralCrossRefGoogle Scholar
  98. 98.
    Jarrett JT, Lansbury PT (1993) Seeding “one-dimensional crystallization” of amyloid: a pathogenic mechanism in Alzheimer’s disease and scrapie? Cell 73:1055–1058CrossRefGoogle Scholar
  99. 99.
    Lorenzen N, Cohen SIA, Nielsen SB, Herling TW, Christiansen G, Dobson CM, Knowles TPJ, Otzen D (2012) Role of elongation and secondary pathways in S6 amyloid fibril growth. Biophys J 102:2167–2175PubMedPubMedCentralCrossRefGoogle Scholar
  100. 100.
    ten Wolde PR, Frenkel D (1997) Enhancement of protein crystal nucleation by critical density fluctuations. Science 277:1975–1978PubMedCrossRefGoogle Scholar
  101. 101.
    Bousset L, Thomson NH, Radford SE, Melki R (2002) The yeast prion Ure2p retains its native α-helical conformation upon assembly into protein fibrils in vitro. EMBO J 21:2903–2911PubMedCrossRefGoogle Scholar
  102. 102.
    Jucker M, Walker LC (2011) Pathogenic protein seeding in Alzheimer’s disease and other neurodegenerative disorders. Ann Neurol 70:532–540PubMedCrossRefGoogle Scholar
  103. 103.
    Jones EM, Surewicz WK (2005) Fibril conformation as the basis of species- and strain-dependent seeding specificity of mammalian prion amyloids. Cell 121:63–72PubMedCrossRefGoogle Scholar
  104. 104.
    Smith JF, Knowles TPJ, Dobson CM, MacPhee CE, Welland ME (2006) Characterization of the nanoscale properties of individual amyloid fibrils. Proc Natl Acad Sci U S A 103:15806–15811PubMedPubMedCentralCrossRefGoogle Scholar
  105. 105.
    Paparcone R, Keten S, Buehler MJ (2010) Atomistic simulation of nanomechanical properties of Alzheimer’s Aβ(1–40) amyloid fibrils under compressive and tensile loading. J Biomech 43:1196–1201PubMedCrossRefPubMedCentralGoogle Scholar
  106. 106.
    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
  107. 107.
    Anderson VJ, Lekkerkerker HNW (2002) Insights into phase transition kinetics from colloid science. Nature 416:811–815PubMedCrossRefGoogle Scholar
  108. 108.
    Krebs MRH, MacPhee CE, Miller AF, Dunlop IE, Dobson CM, Donald AM (2004) The formation of spherulites by amyloid fibrils of bovine insulin. Proc Natl Acad Sci U S A 101:14420–14424PubMedCrossRefGoogle Scholar
  109. 109.
    Rogers SS, Venema P, van der Ploeg JPM, van der Linden E, Sagis LMC, Donald AM (2006) Investigating the permanent electric dipole moment of β-lactoglobulin fibrils, using transient electric birefringence. Biopolymers 82:241–252PubMedCrossRefGoogle Scholar
  110. 110.
    Dzwolak W, Loksztejn A, Galinska-Rakoczy A, Adachi R, Goto Y, Rupnicki L (2007) Conformational indeterminism in protein misfolding: chiral amplification on amyloidogenic pathway of insulin. J Am Chem Soc 129:7517–7522PubMedCrossRefPubMedCentralGoogle Scholar
  111. 111.
    Ashby MF, Gibson LJ, Wegst U, Olive R (1995) The mechanical properties of natural materials. Proc R Soc Lond Math Phys Eng Sci 450:123–140CrossRefGoogle Scholar
  112. 112.
    Wegst UGK, Ashby MF (2004) The mechanical efficiency of natural materials. Philos Mag 84:2167–2186CrossRefGoogle Scholar
  113. 113.
    Shen ZL, Dodge MR, Kahn H, Ballarini R, Eppell SJ (2008) Stress-strain experiments on individual collagen fibrils. Biophys J 95:3956–3963PubMedPubMedCentralCrossRefGoogle Scholar
  114. 114.
    Yang L, van der Werf KO, Koopman BFJM, Subramaniam V, Bennink ML, Dijkstra PJ, Feijen J (2007) Micromechanical bending of single collagen fibrils using atomic force microscopy. J Biomed Mater Res A 82A:160–168CrossRefGoogle Scholar
  115. 115.
    Slotta U, Hess S, Spieß K, Stromer T, Serpell L, Scheibel T (2007) Spider silk and amyloid fibrils: a structural comparison. Macromol Biosci 7:183–188PubMedCrossRefPubMedCentralGoogle Scholar
  116. 116.
    Keten S, Xu Z, Ihle B, Buehler MJ (2010) Nanoconfinement controls stiffness, strength and mechanical toughness of β-sheet crystals in silk. Nat Mater 9:359–367PubMedCrossRefGoogle Scholar
  117. 117.
    Fratzl P, Weinkamer R (2007) Nature’s hierarchical materials. Prog Mater Sci 52:1263–1334CrossRefGoogle Scholar
  118. 118.
    Kreplak L, Bär H, Leterrier JF, Herrmann H, Aebi U (2005) Exploring the mechanical behavior of single intermediate filaments. J Mol Biol 354:569–577PubMedCrossRefPubMedCentralGoogle Scholar
  119. 119.
    Vendruscolo M, Knowles TPJ, Dobson CM (2011) Protein solubility and protein homeostasis: a generic view of protein misfolding disorders. Cold Spring Harb Perspect Biol.  https://doi.org/10.1101/cshperspect.a010454 PubMedPubMedCentralCrossRefGoogle Scholar
  120. 120.
    Kol N, Adler-Abramovich L, Barlam D, Shneck RZ, Gazit E, Rousso I (2005) Self-assembled peptide nanotubes are uniquely rigid bioinspired supramolecular structures. Nano Lett 5:1343–1346PubMedCrossRefPubMedCentralGoogle Scholar
  121. 121.
    Adamcik J, Jung J-M, Flakowski J, De Los Rios P, Dietler G, Mezzenga R (2010) Understanding amyloid aggregation by statistical analysis of atomic force microscopy images. Nat Nanotechnol 5:423–428PubMedCrossRefPubMedCentralGoogle Scholar
  122. 122.
    Meersman F, Cabrera RQ, McMillan PF, Dmitriev V (2009) Compressibility of insulin amyloid fibrils determined by X-ray diffraction in a diamond anvil cell. High Press Res 29:665–670CrossRefGoogle Scholar
  123. 123.
    Sachse C, Grigorieff N, Fändrich M (2010) Nanoscale flexibility parameters of Alzheimer amyloid fibrils determined by electron cryo-microscopy. Angew Chem Int Ed Engl 49:1321–1323PubMedPubMedCentralCrossRefGoogle Scholar
  124. 124.
    Park J, Kahng B, Kamm RD, Hwang W (2006) Atomistic simulation approach to a continuum description of self-assembled β-sheet filaments. Biophys J 90:2510–2524PubMedPubMedCentralCrossRefGoogle Scholar
  125. 125.
    Relini A, Torrassa S, Ferrando R, Rolandi R, Campioni S, Chiti F, Gliozzi A (2010) Detection of populations of amyloid-like protofibrils with different physical properties. Biophys J 98:1277–1284PubMedPubMedCentralCrossRefGoogle Scholar
  126. 126.
    Guo S, Akhremitchev BB (2006) Packing density and structural heterogeneity of insulin amyloid fibrils measured by AFM nanoindentation. Biomacromolecules 7:1630–1636PubMedCrossRefPubMedCentralGoogle Scholar
  127. 127.
    Ashby MF, Gibson LJ, Wegst U, Olive R (1995) The mechanical properties of natural materials. Proc Math Phys Sci 450:123–140CrossRefGoogle Scholar
  128. 128.
    Mankar S, Anoop A, Sen S, Maji SK (2011) Nanomaterials: amyloids reflect their brighter side. Nano Rev 2:1–12.  https://doi.org/10.3402/nano.v2i0.6032 CrossRefGoogle Scholar
  129. 129.
    Sasso L, Suei S, Domigan L, Healy J, Nock V, MAK W, Gerrard JA (2014) Versatile multi-functionalization of protein nanofibrils for biosensor applications. Nanoscale 6:1629–1634PubMedCrossRefPubMedCentralGoogle Scholar
  130. 130.
    Hauser CAE, Maurer-Stroh S, Martins IC (2014) Amyloid-based nanosensors and nanodevices. Chem Soc Rev 43:5326–5345PubMedCrossRefPubMedCentralGoogle Scholar
  131. 131.
    Yang JE, Park JS, Cho E, Jung S, Paik SR (2015) Robust polydiacetylene-based colorimetric sensing material developed with amyloid fibrils of α-synuclein. Langmuir 31:1802–1810PubMedCrossRefPubMedCentralGoogle Scholar
  132. 132.
    Hamedi M, Herland A, Karlsson RH, Inganäs O (2008) Electrochemical devices made from conducting nanowire networks self-assembled from amyloid fibrils and alkoxysulfonate PEDOT. Nano Lett 8:1736–1740PubMedCrossRefPubMedCentralGoogle Scholar
  133. 133.
    Li C, Born A-K, Schweizer T, Zenobi-Wong M, Cerruti M, Mezzenga R (2014) Amyloid-hydroxyapatite bone biomimetic composites. Adv Mater 26:3207–3212CrossRefGoogle Scholar
  134. 134.
    Meier C, Welland ME (2011) Wet-spinning of amyloid protein nanofibers into multifunctional high-performance biofibers. Biomacromolecules 12:3453–3459PubMedCrossRefPubMedCentralGoogle Scholar
  135. 135.
    Jacob RS, Ghosh D, Singh PK et al (2015) Self healing hydrogels composed of amyloid nano fibrils for cell culture and stem cell differentiation. Biomaterials 54:97–105CrossRefGoogle Scholar
  136. 136.
    Reynolds NP, Charnley M, Mezzenga R, Hartley PG (2014) Engineered lysozyme amyloid fibril networks support cellular growth and spreading. Biomacromolecules 15:599–608CrossRefGoogle Scholar
  137. 137.
    Gras SL, Tickler AK, Squires AM, Devlin GL, Horton MA, Dobson CM, MacPhee CE (2008) Functionalised amyloid fibrils for roles in cell adhesion. Biomaterials 29:1553–1562CrossRefGoogle Scholar
  138. 138.
    Yan H, Nykanen A, Ruokolainen J, Farrar D, Gough JE, Saiani A, Miller AF (2008) Thermo-reversible protein fibrillar hydrogels as cell scaffolds. Faraday Discuss 139:71–84; discussion 105–128, 419–420PubMedCrossRefPubMedCentralGoogle Scholar
  139. 139.
    Maji SK, Schubert D, Rivier C, Lee S, Rivier JE, Riek R (2008) Amyloid as a depot for the formulation of long-acting drugs. PLoS Biol 6:e17 PubMedPubMedCentralCrossRefGoogle Scholar
  140. 140.
    Silva RF, Araújo DR, Silva ER, Ando RA, Alves WA (2013) L-diphenylalanine microtubes as a potential drug-delivery system: characterization, release kinetics, and cytotoxicity. Langmuir 29:10205–10212CrossRefGoogle Scholar
  141. 141.
    Akkermans C, Van der Goot AJ, Venema P, Gruppen H, Vereijken JM, Van der Linden E, Boom RM (2007) Micrometer-sized fibrillar protein aggregates from soy glycinin and soy protein isolate. J Agric Food Chem 55:9877–9882PubMedCrossRefPubMedCentralGoogle Scholar
  142. 142.
    Akkermans C, Venema P, van der Goot AJ, Gruppen H, Bakx EJ, Boom RM, van der Linden E (2008) Peptides are building blocks of heat-induced fibrillar protein aggregates of β-lactoglobulin formed at pH 2. Biomacromolecules 9:1474–1479PubMedCrossRefPubMedCentralGoogle Scholar
  143. 143.
    Bateman L, Ye A, Singh H (2010) In vitro digestion of β-lactoglobulin fibrils formed by heat treatment at low pH. J Agric Food Chem 58:9800–9808PubMedCrossRefPubMedCentralGoogle Scholar
  144. 144.
    Bateman L, Ye A, Singh H (2011) Re-formation of fibrils from hydrolysates of β-lactoglobulin fibrils during in vitro gastric digestion. J Agric Food Chem 59:9605–9611PubMedCrossRefPubMedCentralGoogle Scholar
  145. 145.
    Graveland-Bikker JF, de Kruif CG (2006) Unique milk protein based nanotubes: food and nanotechnology meet. Trends Food Sci Technol 17:196–203CrossRefGoogle Scholar
  146. 146.
    Rao SP, Meade SJ, Healy JP, Sutton KH, Larsen NG, Staiger MP, Gerrard JA (2012) Amyloid fibrils as functionalizable components of nanocomposite materials. Biotechnol Prog 28:248–256PubMedCrossRefPubMedCentralGoogle Scholar
  147. 147.
    Li C, Bolisetty S, Mezzenga R (2013) Hybrid nanocomposites of gold single-crystal platelets and amyloid fibrils with Tunable fluorescence, conductivity, and sensing properties. Adv Mater 25:3694–3700PubMedCrossRefPubMedCentralGoogle Scholar
  148. 148.
    Li C, Adamcik J, Mezzenga R (2012) Biodegradable nanocomposites of amyloid fibrils and graphene with shape-memory and enzyme-sensing properties. Nat Nanotechnol 7:421–427PubMedCrossRefPubMedCentralGoogle Scholar
  149. 149.
    Mi R, Liu Y, Chen X, Shao Z (2016) Structure and properties of various hybrids fabricated by silk nanofibrils and nanohydroxyapatite. Nanoscale 8:20096–20102PubMedCrossRefPubMedCentralGoogle Scholar
  150. 150.
    Li D, Furukawa H, Deng H, Liu C, Yaghi OM, Eisenberg DS (2014) Designed amyloid fibers as materials for selective carbon dioxide capture. Proc Natl Acad Sci U S A 111:191–196PubMedCrossRefPubMedCentralGoogle Scholar
  151. 151.
    Li D, Jones EM, Sawaya MR et al (2014) Structure-based design of functional amyloid materials. J Am Chem Soc 136:18044–18051PubMedCrossRefPubMedCentralGoogle Scholar
  152. 152.
    Bolisetty S, Mezzenga R (2016) Amyloid–carbon hybrid membranes for universal water purification. Nat Nanotechnol 11:365–371PubMedCrossRefPubMedCentralGoogle Scholar
  153. 153.
    Bolisetty S, Arcari M, Adamcik J, Mezzenga R (2015) Hybrid amyloid membranes for continuous flow catalysis. Langmuir 31:13867–13873PubMedCrossRefPubMedCentralGoogle Scholar
  154. 154.
    Ha Y, Yang J, Tao F, Wu Q, Song Y, Wang H, Zhang X, Yang P (2018) Phase-transited lysozyme as a universal route to bioactive hydroxyapatite crystalline film. Adv Funct Mater 28:1704476CrossRefGoogle Scholar
  155. 155.
    Gu J, Su Y, Liu P, Li P, Yang P (2017) An environmentally benign antimicrobial coating based on a protein supramolecular assembly. ACS Appl Mater Interfaces 9:198–210PubMedCrossRefGoogle Scholar
  156. 156.
    Zhao J, Qu Y, Chen H, Xu R, Yu Q, Yang P (2018) Self-assembled proteinaceous wound dressings attenuate secondary trauma and improve wound healing in vivo. J Mater Chem B 6:4645–4655CrossRefGoogle Scholar
  157. 157.
    Gao A, Wu Q, Wang D, Ha Y, Chen Z, Yang P (2016) A superhydrophobic surface templated by protein self-assembly and emerging application toward protein crystallization. Adv Mater 28:579–587PubMedCrossRefGoogle Scholar
  158. 158.
    Jiang B, Yang J, Li C, Zhang L, Zhang X, Yang P (2017) Water-based photo- and electron-beam lithography using egg white as a resist. Adv Mater Interfaces 4:1601223CrossRefGoogle Scholar
  159. 159.
    Saunders BR, Laajam N, Daly E, Teow S, Hu X, Stepto R (2009) Microgels: from responsive polymer colloids to biomaterials. Adv Colloid Interf Sci 147:251–262CrossRefGoogle Scholar
  160. 160.
    Das M, Zhang H, Kumacheva E (2006) Microgels: old materials with new applications. Annu Rev Mater Res 36:117–142CrossRefGoogle Scholar
  161. 161.
    Seiffert S (2013) Small but smart: sensitive microgel capsules. Angew Chem Int Ed 52:11462–11468 CrossRefGoogle Scholar
  162. 162.
    Fernández-Barbero A, Suárez IJ, Sierra-Martín B, Fernández-Nieves A, de las Nieves FJ, Marquez M, Rubio-Retama J, López-Cabarcos E (2009) Gels and microgels for nanotechnological applications. Adv Colloid Interf Sci 147:88–108CrossRefGoogle Scholar
  163. 163.
    Maes D, Vorontsova MA, Potenza MA, Sanvito T, Sleutel M, Giglio M, Vekilov PG (2015) Do protein crystals nucleate within dense liquid clusters? Acta Crystallogr Sect F Struct Biol Commun 71:815–822CrossRefGoogle Scholar
  164. 164.
    Chatani E, Imamura H, Yamamoto N, Kato M (2014) Stepwise organization of the β-structure identifies key regions essential for the propagation and cytotoxicity of insulin amyloid fibrils. J Biol Chem 289:10399–10410PubMedPubMedCentralCrossRefGoogle Scholar
  165. 165.
    Yuyama K, Ueda M, Nagao S, Hirota S, Sugiyama T, Masuhara H (2017) A single spherical assembly of protein amyloid fibrils formed by laser trapping. Angew Chem Int Ed 56:6739–6743CrossRefGoogle Scholar
  166. 166.
    Hu Z, Chen Y, Wang C, Zheng Y, Li Y (1998) Polymer gels with engineered environmentally responsive surface patterns. Nature 393:149–152CrossRefGoogle Scholar
  167. 167.
    Lu Y, Mei Y, Ballauff M, Drechsler M (2006) Thermosensitive core−shell particles as carrier systems for metallic nanoparticles. J Phys Chem B 110:3930–3937PubMedCrossRefGoogle Scholar
  168. 168.
    Schachschal S, Adler H-J, Pich A, Wetzel S, Matura A, van Pee K-H (2011) Encapsulation of enzymes in microgels by polymerization/cross-linking in aqueous droplets. Colloid Polym Sci 289:693–698CrossRefGoogle Scholar
  169. 169.
    Vinogradov SV (2006) Colloidal microgels in drug delivery applications. Curr Pharm Des 12:4703–4712PubMedPubMedCentralCrossRefGoogle Scholar
  170. 170.
    Oh JK, Drumright R, Siegwart DJ, Matyjaszewski K (2008) The development of microgels/nanogels for drug delivery applications. Prog Polym Sci Oxf 33:448–477CrossRefGoogle Scholar
  171. 171.
    Lopez VC, Hadgraft J, Snowden MJ (2005) The use of colloidal microgels as a (trans)dermal drug delivery system. Int J Pharm 292:137–147PubMedCrossRefGoogle Scholar
  172. 172.
    Hoare TR, Kohane DS (2008) Hydrogels in drug delivery: progress and challenges. Polymer 49:1993–2007CrossRefGoogle Scholar
  173. 173.
    Fettis MM, Wei Y, Restuccia A, Kurian JJ, Wallet SM, Hudalla GA (2016) Microgels with tunable affinity-controlled protein release via desolvation of self-assembled peptide nanofibers. J Mater Chem B 4:3054–3064CrossRefGoogle Scholar
  174. 174.
    Du X, Zhou J, Shi J, Xu B (2015) Supramolecular hydrogelators and hydrogels: from soft matter to molecular biomaterials. Chem Rev 115:13165–13307PubMedPubMedCentralCrossRefGoogle Scholar
  175. 175.
    Velasco D, Tumarkin E, Kumacheva E (2012) Microfluidic encapsulation of cells in polymer microgels. Small 8:1633–1642PubMedCrossRefGoogle Scholar
  176. 176.
    Lipinski CA (2000) Drug-like properties and the causes of poor solubility and poor permeability. J Pharmacol Toxicol Methods 44:235–249PubMedCrossRefPubMedCentralGoogle Scholar
  177. 177.
    Stella VJ, Nti-Addae KW (2007) Prodrug strategies to overcome poor water solubility. Adv Drug Deliv Rev 59:677–694PubMedCrossRefGoogle Scholar
  178. 178.
    Shimanovich U, Tkacz ID, Eliaz D, Cavaco-Paulo A, Michaeli S, Gedanken A (2011) Encapsulation of RNA molecules in BSA microspheres and internalization into Trypanosoma Brucei parasites and human U2OS cancer cells. Adv Funct Mater 21:3659–3666CrossRefGoogle Scholar
  179. 179.
    Angel (Shimanovich) U, Matas D, Michaeli S, Cavaco-Paulo A, Gedanken A (2010) Microspheres of mixed proteins. Chem Eur J 16:2108–2114CrossRefGoogle Scholar
  180. 180.
    Shimanovich U, Eliaz D, Zigdon S, Volkov V, Aizer A, Cavaco-Paulo A, Michaeli S, Shav-Tal Y, Gedanken A (2012) Proteinaceous microspheres for targeted RNA delivery prepared by an ultrasonic emulsification method. J Mater Chem B 1:82–90CrossRefGoogle Scholar
  181. 181.
    Ma X, Sun X, Hargrove D, Chen J, Song D, Dong Q, Lu X, Fan T-H, Fu Y, Lei Y (2016) A biocompatible and biodegradable protein hydrogel with green and red autofluorescence: preparation, characterization and In Vivo biodegradation tracking and modeling. Sci Rep 6:19370PubMedPubMedCentralCrossRefGoogle Scholar
  182. 182.
    Sarkar A, Murray B, Holmes M, Ettelaie R, Abdalla A, Yang X (2016) In vitro digestion of Pickering emulsions stabilized by soft whey protein microgel particles: influence of thermal treatment. Soft Matter 12:3558–3569PubMedCrossRefGoogle Scholar
  183. 183.
    O’Neill GJ, Jacquier JC, Mukhopadhya A, Egan T, O’Sullivan M, Sweeney T, O’Riordan ED (2015) In vitro and in vivo evaluation of whey protein hydrogels for oral delivery of riboflavin. J Funct Foods 19:512–521CrossRefGoogle Scholar
  184. 184.
    Branco MC, Pochan DJ, Wagner NJ, Schneider JP (2009) Macromolecular diffusion and release from self-assembled β-hairpin peptide hydrogels. Biomaterials 30:1339–1347PubMedCrossRefGoogle Scholar
  185. 185.
    Koutsopoulos S, Unsworth LD, Nagai Y, Zhang S (2009) Controlled release of functional proteins through designer self-assembling peptide nanofiber hydrogel scaffold. Proc Natl Acad Sci 106:4623–4628PubMedCrossRefGoogle Scholar
  186. 186.
    Ramachandran S, Tseng Y, Yu YB (2005) Repeated rapid shear-responsiveness of peptide hydrogels with tunable shear modulus. Biomacromolecules 6:1316–1321PubMedPubMedCentralCrossRefGoogle Scholar
  187. 187.
    Stendahl JC, Wang LJ, Chow LW, Kaufman DB, Stupp SI (2008) Growth factor delivery from self-assembling nanofibers to facilitate islet transplantation. Transplantation 86:478–481PubMedPubMedCentralCrossRefGoogle Scholar
  188. 188.
    Baldwin AJ, Bader R, Christodoulou J, MacPhee CE, Dobson CM, Barker PD (2006) Cytochrome display on amyloid fibrils. J Am Chem Soc 128:2162–2163PubMedCrossRefGoogle Scholar
  189. 189.
    Maschke A, Becker C, Eyrich D, Kiermaier J, Blunk T, Göpferich A (2007) Development of a spray congealing process for the preparation of insulin-loaded lipid microparticles and characterization thereof. Eur J Pharm Biopharm 65:175–187PubMedCrossRefGoogle Scholar
  190. 190.
    Jiang G, Thanoo BC, DeLuca PP (2002) Effect of osmotic pressure in the solvent extraction phase on BSA release profile from PLGA microspheres. Pharm Dev Technol 7:391–399PubMedCrossRefGoogle Scholar
  191. 191.
    Song Y, Shimanovich U, Michaels TCT, Ma Q, Li J, Knowles TPJ, Shum HC (2016) Fabrication of fibrillosomes from droplets stabilized by protein nanofibrils at all-aqueous interfaces. Nat Commun 7:ncomms12934CrossRefGoogle Scholar
  192. 192.
    Erni P, Fischer P, Windhab EJ (2005) Deformation of single emulsion drops covered with a viscoelastic adsorbed protein layer in simple shear flow. Appl Phys Lett 87:244104CrossRefGoogle Scholar
  193. 193.
    Gedanken A (2008) Preparation and properties of proteinaceous microspheres made sonochemically. Chem Eur J 14:3840–3853PubMedCrossRefGoogle Scholar
  194. 194.
    Silva R, Ferreira H, Cavaco-Paulo A (2011) Sonoproduction of liposomes and protein particles as templates for delivery purposes. Biomacromolecules 12:3353–3368PubMedCrossRefGoogle Scholar
  195. 195.
    Xu H, Zeiger BW, Suslick KS (2013) Sonochemical synthesis of nanomaterials. Chem Soc Rev 42:2555–2567PubMedCrossRefPubMedCentralGoogle Scholar
  196. 196.
    Whitesides GM (2006) The origins and the future of microfluidics. Nature 442:368–373PubMedCrossRefGoogle Scholar
  197. 197.
    Squires TM, Quake SR (2005) Microfluidics: fluid physics at the nanoliter scale. Rev Mod Phys 77:977–1026CrossRefGoogle Scholar
  198. 198.
    Wang J-T, Wang J, Han J-J (2011) Fabrication of advanced particles and particle-based materials assisted by droplet-based microfluidics. Small 7:1728–1754PubMedCrossRefGoogle Scholar
  199. 199.
    Zhang H, Tumarkin E, Peerani R, Nie Z, Sullan RMA, Walker GC, Kumacheva E (2006) Microfluidic production of biopolymer microcapsules with controlled morphology. J Am Chem Soc 128:12205–12210PubMedCrossRefGoogle Scholar
  200. 200.
    Tumarkin E, Kumacheva E (2009) Microfluidic generation of microgels from synthetic and natural polymers. Chem Soc Rev 38:2161–2168PubMedCrossRefGoogle Scholar
  201. 201.
    Utada AS, Chu L-Y, Fernandez-Nieves A, Link DR, Holtze C, Weitz DA (2007) Dripping, jetting, drops, and wetting: the magic of microfluidics. MRS Bull 32:702–708CrossRefGoogle Scholar
  202. 202.
    Shum HC, Kim J-W, Weitz DA (2008) Microfluidic fabrication of monodisperse biocompatible and biodegradable polymersomes with controlled permeability. J Am Chem Soc 130:9543–9549PubMedCrossRefGoogle Scholar
  203. 203.
    Ward T, Faivre M, Abkarian M, Stone HA (2005) Microfluidic flow focusing: drop size and scaling in pressure versus flow-rate-driven pumping. Electrophoresis 26:3716–3724PubMedCrossRefGoogle Scholar
  204. 204.
    Xia Y, Whitesides GM (1998) Soft lithography. Angew Chem Int Ed 37:550–575CrossRefGoogle Scholar
  205. 205.
    McDonald JC, Duffy DC, Anderson JR, Chiu DT, Wu H, Schueller OJA, Whitesides GM (2000) Fabrication of microfluidic systems in poly(dimethylsiloxane). Electrophoresis 21:27–40PubMedCrossRefGoogle Scholar
  206. 206.
    Mazutis L, Gilbert J, Ung WL, Weitz DA, Griffiths AD, Heyman JA (2013) Single-cell analysis and sorting using droplet-based microfluidics. Nat Protoc 8:870–891PubMedCrossRefGoogle Scholar
  207. 207.
    Martín-Banderas L, Flores-Mosquera M, Riesco-Chueca P, Rodríguez-Gil A, Cebolla Á, Chávez S, Gañán-Calvo AM (2005) Flow focusing: a versatile technology to produce size-controlled and specific-morphology microparticles. Small 1:688–692PubMedCrossRefGoogle Scholar
  208. 208.
    Baroud CN, Gallaire F, Dangla R (2010) Dynamics of microfluidic droplets. Lab Chip 10:2032–2045PubMedCrossRefGoogle Scholar
  209. 209.
    Abate AR, Weitz DA (2009) High-order multiple emulsions formed in poly(dimethylsiloxane) microfluidics. Small 5:2030–2032PubMedCrossRefGoogle Scholar
  210. 210.
    Kim S-H, Shum HC, Kim JW, Cho J-C, Weitz DA (2011) Multiple polymersomes for programmed release of multiple components. J Am Chem Soc 133:15165–15171PubMedCrossRefPubMedCentralGoogle Scholar
  211. 211.
    Seo M, Paquet C, Nie Z, Xu S, Kumacheva E (2007) Microfluidic consecutive flow-focusing droplet generators. Soft Matter 3:986–992CrossRefGoogle Scholar
  212. 212.
    Keating CD (2012) Aqueous phase separation as a possible route to compartmentalization of biological molecules. Acc Chem Res 45:2114–2124PubMedPubMedCentralCrossRefGoogle Scholar
  213. 213.
    Plamper FA, Richtering W (2017) Functional microgels and microgel systems. Acc Chem Res 50:131–140PubMedCrossRefPubMedCentralGoogle Scholar
  214. 214.
    Thorne JB, Vine GJ, Snowden MJ (2011) Microgel applications and commercial considerations. Colloid Polym Sci 289:625CrossRefGoogle Scholar
  215. 215.
    Wang Y-X, Robertson JL, Spillman WB, Claus RO (2004) Effects of the chemical structure and the surface properties of polymeric biomaterials on their biocompatibility. Pharm Res 21:1362–1373PubMedCrossRefPubMedCentralGoogle Scholar
  216. 216.
    Kumachev A, Greener J, Tumarkin E, Eiser E, Zandstra PW, Kumacheva E (2011) High-throughput generation of hydrogel microbeads with varying elasticity for cell encapsulation. Biomaterials 32:1477–1483PubMedCrossRefPubMedCentralGoogle Scholar
  217. 217.
    Agnihotri SA, Mallikarjuna NN, Aminabhavi TM (2004) Recent advances on chitosan-based micro- and nanoparticles in drug delivery. J Control Release 100:5–28PubMedCrossRefPubMedCentralGoogle Scholar
  218. 218.
    Mitra A, Dey B (2011) Chitosan microspheres in novel drug delivery systems. Indian J Pharm Sci 73:355–366PubMedPubMedCentralGoogle Scholar
  219. 219.
    Augst AD, Kong HJ, Mooney DJ (2006) Alginate hydrogels as biomaterials. Macromol Biosci 6:623–633PubMedCrossRefPubMedCentralGoogle Scholar
  220. 220.
    Tan W-H, Takeuchi S (2007) Monodisperse alginate hydrogel microbeads for cell encapsulation. Adv Mater 19:2696–2701CrossRefGoogle Scholar
  221. 221.
    Gazit E (2007) Self-assembled peptide nanostructures: the design of molecular building blocks and their technological utilization. Chem Soc Rev 36:1263–1269PubMedCrossRefGoogle Scholar
  222. 222.
    Bai S, Pappas C, Debnath S, Frederix PWJM, Leckie J, Fleming S, Ulijn RV (2014) Stable emulsions formed by self-assembly of interfacial networks of dipeptide derivatives. ACS Nano 8:7005–7013PubMedCrossRefGoogle Scholar
  223. 223.
    Flamia R, Salvi AM, D’Alessio L, Castle JE, Tamburro AM (2007) Transformation of amyloid-like fibers, formed from an elastin-based biopolymer, into a hydrogel: an X-ray photoelectron spectroscopy and atomic force microscopy study. Biomacromolecules 8:128–138PubMedCrossRefGoogle Scholar
  224. 224.
    Bhak G, Lee S, Park JW, Cho S, Paik SR (2010) Amyloid hydrogel derived from curly protein fibrils of α-synuclein. Biomaterials 31:5986–5995CrossRefGoogle Scholar
  225. 225.
    Mains J, Lamprou D, McIntosh L, Oswald IH, Urquhart A (2013) Beta-adrenoceptor antagonists affect amyloid nanostructure; amyloid hydrogels as drug delivery vehicles. Chem Commun 49:5082–5084CrossRefGoogle Scholar
  226. 226.
    Gosal WS, Clark AH, Ross-Murphy SB (2004) Fibrillar β-lactoglobulin gels: Part 2. Dynamic mechanical characterization of heat-set systems. Biomacromolecules 5:2420–2429PubMedCrossRefGoogle Scholar
  227. 227.
    Bolisetty S, Harnau L, Jung J, Mezzenga R (2012) Gelation, phase behavior, and dynamics of β-lactoglobulin amyloid fibrils at varying concentrations and ionic strengths. Biomacromolecules 13:3241–3252PubMedCrossRefGoogle Scholar
  228. 228.
    Jung J-M, Mezzenga R (2010) Liquid crystalline phase behavior of protein Fibers in water: experiments versus theory. Langmuir 26:504–514PubMedCrossRefGoogle Scholar
  229. 229.
    Nyström G, Fong W-K, Mezzenga R (2017) Ice-templated and cross-linked amyloid fibril aerogel scaffolds for cell growth. Biomacromolecules 18:2858–2865PubMedCrossRefGoogle Scholar
  230. 230.
    Langton M, Hermansson A-M (1992) Fine-stranded and particulate gels of β-lactoglobulin and whey protein at varying pH. Food Hydrocoll 5:523–539CrossRefGoogle Scholar
  231. 231.
    Zhou X-M, Shimanovich U, Herling TW, Wu S, Dobson CM, Knowles TPJ, Perrett S (2015) Enzymatically active microgels from self-assembling protein nanofibrils for microflow chemistry. ACS Nano 9:5772–5781PubMedPubMedCentralCrossRefGoogle Scholar
  232. 232.
    Silva R, Ferreira H, Azoia NG, Shimanovich U, Freddi G, Gedanken A, Cavaco-Paulo A (2012) Insights on the mechanism of formation of protein microspheres in a biphasic system. Mol Pharm 9:3079–3088PubMedCrossRefPubMedCentralGoogle Scholar
  233. 233.
    Shimanovich U, Ruggeri FS, Genst ED et al (2017) Silk micrococoons for protein stabilisation and molecular encapsulation. Nat Commun 8:ncomms15902CrossRefGoogle Scholar
  234. 234.
    Müller T, Simone Ruggeri F, Kulik J, Shimanovich U, Mason TO, Knowles TPJ, Dietler G (2014) Nanoscale spatially resolved infrared spectra from single microdroplets. Lab Chip 14:1315–1319PubMedCrossRefPubMedCentralGoogle Scholar
  235. 235.
    Avivi S, Gedanken A (2002) S–S bonds are not required for the sonochemical formation of proteinaceous microspheres: the case of streptavidin. Biochem J 366:705–707PubMedPubMedCentralCrossRefGoogle Scholar
  236. 236.
    Subia B, Kundu SC (2013) Drug loading and release on tumor cells using silk fibroin–albumin nanoparticles as carriers. Nanotechnology 24:035103PubMedCrossRefPubMedCentralGoogle Scholar
  237. 237.
    Shimanovich U, Volkov V, Eliaz D, Aizer A, Michaeli S, Gedanken A (2011) Stabilizing RNA by the sonochemical formation of RNA nanospheres. Small 7:1068–1074PubMedCrossRefPubMedCentralGoogle Scholar
  238. 238.
    Shimanovich U, Eliaz D, Aizer A, Vayman I, Michaeli S, Shav-Tal Y, Gedanken A (2011) Sonochemical synthesis of DNA nanospheres. Chembiochem 12:1678–1681PubMedCrossRefPubMedCentralGoogle Scholar
  239. 239.
    Li C, Xu L, Zuo YY, Yang P (2018) Tuning protein assembly pathways through superfast amyloid-like aggregation. Biomater Sci 6:836–841PubMedCrossRefPubMedCentralGoogle Scholar
  240. 240.
    Shimanovich U, Song Y, Brujic J, Shum HC, Knowles TPJ (2015) Multiphase protein microgels. Macromol Biosci 15:501–508PubMedCrossRefPubMedCentralGoogle Scholar
  241. 241.
    Knowles T, Shimanovich U, Dobson C, Weitz D (2016) Protein CapsulesGoogle Scholar
  242. 242.
    Volpatti LR, Shimanovich U, Ruggeri FS, Bolisetty S, Müller T, Mason TO, Michaels TCT, Mezzenga R, Dietler G, Knowles TPJ (2016) Micro- and nanoscale hierarchical structure of core–shell protein microgels. J Mater Chem B 4:7989–7999CrossRefGoogle Scholar
  243. 243.
    Peters TJ (1987) Partition of cell particles and macromolecules: separation and purification of biomolecules, cell organelles, membranes and cells in aqueous polymer two phase systems and their use in biochemical analysis and biotechnology. Cell Biochem Funct 5:233–234CrossRefGoogle Scholar
  244. 244.
    Kroner KH, Hustedt H, Granda S, Kula M-R, Introduction by T Alan Hatton (2009) Technical aspects of separation using aqueous two-phase systems in enzyme isolation processes. Biotechnol Bioeng 104:217–239PubMedCrossRefPubMedCentralGoogle Scholar
  245. 245.
    Diamond AD, Hsu JT (1990) Protein partitioning in PEG/dextran aqueous two-phase systems. AICHE J 36:1017–1024CrossRefGoogle Scholar
  246. 246.
    Fele L, Fermeglia M (1996) Partition coefficients of proteins in poly(ethylene glycol) + dextran + water at 298 K. J Chem Eng Data 41:331–334CrossRefGoogle Scholar
  247. 247.
    Osborn HT, Akoh CC (2004) Effect of emulsifier type, droplet size, and oil concentration on lipid oxidation in structured lipid-based oil-in-water emulsions. Food Chem 84:451–456CrossRefGoogle Scholar
  248. 248.
    Sah H (1999) Stabilization of proteins against methylene chloride/water interface-induced denaturation and aggregation. J Control Release 58:143–151PubMedCrossRefPubMedCentralGoogle Scholar
  249. 249.
    Liu Y, Lipowsky R, Dimova R (2012) Concentration dependence of the interfacial tension for aqueous two-phase polymer solutions of dextran and polyethylene glycol. Langmuir 28:3831–3839PubMedCrossRefPubMedCentralGoogle Scholar
  250. 250.
    Balakrishnan G, Nicolai T, Benyahia L, Durand D (2012) Particles trapped at the droplet interface in water-in-water emulsions. Langmuir 28:5921–5926PubMedCrossRefPubMedCentralGoogle Scholar
  251. 251.
    Nguyen BT, Nicolai T, Benyahia L (2013) Stabilization of water-in-water emulsions by addition of protein particles. Langmuir 29:10658–10664PubMedCrossRefPubMedCentralGoogle Scholar
  252. 252.
    Rollett A, Reiter T, Nogueira P, Cardinale M, Loureiro A, Gomes A, Cavaco-Paulo A, Moreira A, Carmo AM, Guebitz GM (2012) Folic acid-functionalized human serum albumin nanocapsules for targeted drug delivery to chronically activated macrophages. Int J Pharm 427:460–466PubMedCrossRefPubMedCentralGoogle Scholar
  253. 253.
    Richman M, Wilk S, Skirtenko N, Perelman A, Rahimipour S (2011) Surface-modified protein microspheres capture amyloid-β and inhibit its aggregation and toxicity. Chem Weinh Bergstr Ger 17:11171–11177Google Scholar
  254. 254.
    Krysmann MJ, Castelletto V, Kelarakis A, Hamley IW, Hule RA, Pochan DJ (2008) Self-assembly and hydrogelation of an amyloid peptide fragment. Biochemistry 47:4597–4605PubMedCrossRefPubMedCentralGoogle Scholar
  255. 255.
    Zhou X-M, Entwistle A, Zhang H, Jackson AP, Mason TO, Shimanovich U, Knowles TPJ, Smith AT, Sawyer EB, Perrett S (2014) Self-assembly of amyloid fibrils that display active enzymes. ChemCatChem 6:1961–1968PubMedPubMedCentralCrossRefGoogle Scholar
  256. 256.
    Kim J-W, Fernández-Nieves A, Dan N, Utada AS, Marquez M, Weitz DA (2007) Colloidal assembly route for responsive colloidosomes with tunable permeability. Nano Lett 7:2876–2880PubMedCrossRefPubMedCentralGoogle Scholar
  257. 257.
    Li M-H, Keller P (2009) Stimuli-responsive polymer vesicles. Soft Matter 5:927–937CrossRefGoogle Scholar
  258. 258.
    Yolamanova M, Meier C, Shaytan AK et al (2013) Peptide nanofibrils boost retroviral gene transfer and provide a rapid means for concentrating viruses. Nat Nanotechnol 8:130–136PubMedCrossRefPubMedCentralGoogle Scholar
  259. 259.
    Dai B, Li D, Xi W et al (2015) Tunable assembly of amyloid-forming peptides into nanosheets as a retrovirus carrier. Proc Natl Acad Sci 112:2996–3001PubMedCrossRefPubMedCentralGoogle Scholar
  260. 260.
    Bolisetty S, Boddupalli CS, Handschin S, Chaitanya K, Adamcik J, Saito Y, Manz MG, Mezzenga R (2014) Amyloid fibrils enhance transport of metal nanoparticles in living cells and induced cytotoxicity. Biomacromolecules 15:2793–2799PubMedCrossRefPubMedCentralGoogle Scholar
  261. 261.
    Shen Y, Posavec L, Bolisetty S et al (2017) Amyloid fibril systems reduce, stabilize and deliver bioavailable nanosized iron. Nat Nanotechnol 12:642–647CrossRefGoogle Scholar
  262. 262.
    Levin A, Mason TO, Knowles TPJ, Shimanovich U (2017) Self-assembled protein fibril-metal oxide nanocomposites. Isr J Chem 57(7):724–728CrossRefGoogle Scholar
  263. 263.
    Sandhu A, Handa H, Abe M (2010) Synthesis and applications of magnetic nanoparticles for biorecognition and point of care medical diagnostics. Nanotechnology 21:442001PubMedCrossRefPubMedCentralGoogle Scholar
  264. 264.
    Wiogo HTR, Lim M, Bulmus V, Yun J, Amal R (2011) Stabilization of magnetic iron oxide nanoparticles in biological media by eetal bovine serum (FBS). Langmuir 27:843–850PubMedCrossRefPubMedCentralGoogle Scholar
  265. 265.
    Jordens S, Rühs PA, Sieber C, Isa L, Fischer P, Mezzenga R (2014) Bridging the gap between the nanostructural organization and macroscopic interfacial rheology of amyloid fibrils at liquid interfaces. Langmuir 30:10090–10097PubMedCrossRefPubMedCentralGoogle Scholar
  266. 266.
    Linse S, Cabaleiro-Lago C, Xue W-F, Lynch I, Lindman S, Thulin E, Radford SE, Dawson KA (2007) Nucleation of protein fibrillation by nanoparticles. Proc Natl Acad Sci U S A 104:8691–8696PubMedPubMedCentralCrossRefGoogle Scholar

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© Springer Nature Singapore Pte Ltd. 2019

Authors and Affiliations

  1. 1.Centre for Misfolding Diseases, Department of ChemistryUniversity of CambridgeCambridgeUK
  2. 2.Department of Materials and InterfacesWeizmann Institute of ScienceRehovotIsrael
  3. 3.National Laboratory of Biomacromolecules, CAS Center for Excellence in BiomacromoleculesInstitute of Biophysics, Chinese Academy of SciencesBeijingChina
  4. 4.University of the Chinese Academy of SciencesBeijingChina
  5. 5.Cavendish Laboratory, University of CambridgeCambridgeUK

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