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Biological and Bio-inspired Nanomaterials pp 223–263Cite as

Protein Microgels from Amyloid Fibril Networks

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Part of the book series: Advances in Experimental Medicine and Biology ((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.

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References

  1. Hardy J, Selkoe DJ (2002) The amyloid hypothesis of Alzheimer’s disease: progress and problems on the road to therapeutics. Science 297:353–356

    Article  CAS  PubMed  Google Scholar 

  2. Haass C, Selkoe DJ (2007) Soluble protein oligomers in neurodegeneration: lessons from the Alzheimer’s amyloid β-peptide. Nat Rev Mol Cell Biol 8:101–112

    Article  CAS  PubMed  Google Scholar 

  3. Ballard C, Gauthier S, Corbett A, Brayne C, Aarsland D, Jones E (2011) Alzheimer’s disease. Lancet Lond Engl 377:1019–1031

    Article  Google Scholar 

  4. Querfurth HW, LaFerla FM (2010) Mechanisms of disease Alzheimer’s disease. N Engl J Med 362:329–344

    Article  CAS  PubMed  Google Scholar 

  5. Niedowicz DM, Nelson PT, Murphy MP (2011) Alzheimer’s disease: pathological mechanisms and recent insights. Curr Neuropharmacol 9:674–684

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  6. Dobson CM (1999) Protein misfolding, evolution and disease. Trends Biochem Sci 24:329–332

    Article  CAS  PubMed  Google Scholar 

  7. Dobson CM (2003) Protein folding and misfolding. Nature 426:884–890

    Article  CAS  PubMed  Google Scholar 

  8. Chiti F, Dobson CM (2006) Protein misfolding, functional amyloid, and human disease. Annu Rev Biochem 75:333–366

    Article  CAS  PubMed  Google Scholar 

  9. Knowles TPJ, Vendruscolo M, Dobson CM (2014) The amyloid state and its association with protein misfolding diseases. Nat Rev Mol Cell Biol 15:384–396

    Article  CAS  PubMed  Google Scholar 

  10. Stefani M, Dobson CM (2003) Protein aggregation and aggregate toxicity: new insights into protein folding, misfolding diseases and biological evolution. J Mol Med 81:678–699

    Article  CAS  PubMed  Google Scholar 

  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

    Article  CAS  Google Scholar 

  12. Fowler DM, Koulov AV, Balch WE, Kelly JW (2007) Functional amyloid – from bacteria to humans. Trends Biochem Sci 32:217–224

    Article  CAS  PubMed  Google Scholar 

  13. Otzen D, Nielsen PH (2008) We find them here, we find them there: functional bacterial amyloid. Cell Mol Life Sci 65:910–927

    Article  CAS  PubMed  Google Scholar 

  14. Kelly JW, Balch WE (2003) Amyloid as a natural product. J Cell Biol 161:461–462

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  15. Maji SK, Perrin MH, Sawaya MR et al (2009) Functional amyloids as natural storage of peptide hormones in pituitary secretory granules. Science 325:328–332

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  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 114:7–20

    Article  CAS  PubMed  Google Scholar 

  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 32:393–401

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  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 9:858–866

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  19. Li C, Qin R, Liu R, Miao S, Yang P (2018) Functional amyloid materials at surfaces/interfaces. Biomater Sci 6:462–472

    Article  CAS  PubMed  Google Scholar 

  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 28:7414–7423

    Article  CAS  PubMed  Google Scholar 

  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 295:851–855

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  22. Shorter J, Lindquist S (2005) Prions as adaptive conduits of memory and inheritance. Nat Rev Genet 6:435–450

    Article  CAS  PubMed  Google Scholar 

  23. Krishnan R, Lindquist SL (2005) Structural insights into a yeast prion illuminate nucleation and strain diversity. Nature 435:765–772

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  24. Lindquist SL, Henikoff S (2002) Self-perpetuating structural states in biology, disease, and genetics. Proc Natl Acad Sci U S A 99:16377

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  25. Tanaka M, Collins SR, Toyama BH, Weissman JS (2006) The physical basis of how prion conformations determine strain phenotypes. Nature 442:585–589

    Article  CAS  PubMed  Google Scholar 

  26. DePace AH, Weissman JS (2002) Origins and kinetic consequences of diversity in Sup35 yeast prion fibers. Nat Struct Mol Biol 9:389–396

    CAS  Google Scholar 

  27. Lashuel HA, Hartley D, Petre BM, Walz T, Lansbury PT (2002) Neurodegenerative disease: amyloid pores from pathogenic mutations. Nature 418:291–291

    Article  CAS  PubMed  Google Scholar 

  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 416:507–511

    Article  CAS  PubMed  Google Scholar 

  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 416:535–539

    Article  CAS  PubMed  Google Scholar 

  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 26:267–298

    Article  CAS  PubMed  Google Scholar 

  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 106:4012–4017

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  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 35:352–358

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  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 27:2866–2875

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  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 104:12494–12499

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  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 318:1900–1903

    Article  CAS  PubMed  Google Scholar 

  36. Knowles TPJ, Buehler MJ (2011) Nanomechanics of functional and pathological amyloid materials. Nat Nanotechnol 6:469–479

    Article  CAS  PubMed  Google Scholar 

  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 96:3590–3594

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  38. Chiti F, Dobson CM (2009) Amyloid formation by globular proteins under native conditions. Nat Chem Biol 5:15–22

    Article  CAS  PubMed  Google Scholar 

  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 350:379–392

    Article  CAS  PubMed  Google Scholar 

  40. Knowles TPJ, Mezzenga R (2016) Amyloid fibrils as building blocks for natural and artificial functional materials. Adv Mater 28:6546–6561

    Article  CAS  PubMed  Google Scholar 

  41. Shimanovich U, Bernardes GJ, Knowles TP, Cavaco-Paulo A (2014) Protein micro- and nano-capsules for biomedical applications. Chem Soc Rev 43:1361–1371

    Article  CAS  PubMed  Google Scholar 

  42. Shimanovich U, Efimov I, Mason TO et al (2015) Protein microgels from amyloid fibril networks. ACS Nano 9:43–51

    Article  CAS  PubMed  Google Scholar 

  43. Cao A, Hu D, Lai L (2004) Formation of amyloid fibrils from fully reduced hen egg white lysozyme. Protein Sci Publ Protein Soc 13:319–324

    Article  CAS  Google Scholar 

  44. Kelly JW (2002) Towards an understanding of amyloidogenesis. Nat Struct Mol Biol 9:323–325

    Article  CAS  Google Scholar 

  45. Teh S-Y, Lin R, Hung L-H, Lee AP (2008) Droplet microfluidics. Lab Chip 8:198–220

    Article  CAS  PubMed  Google Scholar 

  46. Zhang H, Tumarkin E, Sullan RMA, Walker GC, Kumacheva E (2007) Exploring microfluidic routes to microgels of biological polymers. Macromol Rapid Commun 28:527–538

    Article  CAS  Google Scholar 

  47. Seiffert S (2013) Microgel capsules tailored by droplet-based microfluidics. ChemPhysChem 14:295–304

    Article  CAS  PubMed  Google Scholar 

  48. Sipe JD, Cohen AS (2000) Review: history of the amyloid fibril. J Struct Biol 130:88–98

    Article  CAS  PubMed  Google Scholar 

  49. Buxbaum JN, Linke RP (2012) A molecular history of the amyloidoses. J Mol Biol 421:142–159

    Article  CAS  PubMed  Google Scholar 

  50. Nilsson MR (2004) Techniques to study amyloid fibril formation in vitro. Methods 34:151–160

    Article  CAS  PubMed  Google Scholar 

  51. Groenning M (2009) Binding mode of Thioflavin T and other molecular probes in the context of amyloid fibrils—current status. J Chem Biol 3:1–18

    Article  PubMed  PubMed Central  Google Scholar 

  52. Hawe A, Sutter M, Jiskoot W (2008) Extrinsic fluorescent dyes as tools for protein characterization. Pharm Res 25:1487–1499

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  53. Khurana R, Uversky VN, Nielsen L, Fink AL (2001) Is Congo Red an amyloid-specific dye? J Biol Chem 276:22715–22721

    Article  CAS  PubMed  Google Scholar 

  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 276:5960–5972

    Article  CAS  PubMed  Google Scholar 

  55. O’Nuallain B, Wetzel R (2002) Conformational Abs recognizing a generic amyloid fibril epitope. Proc Natl Acad Sci 99:1485–1490

    Article  PubMed  CAS  PubMed Central  Google Scholar 

  56. Larsen P, Nielsen JL, Dueholm MS, Wetzel R, Otzen D, Nielsen PH (2007) Amyloid adhesins are abundant in natural biofilms. Environ Microbiol 9:3077–3090

    Article  CAS  PubMed  Google Scholar 

  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 138:2156–2162

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  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 12:673–680

    Article  CAS  Google Scholar 

  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 17:143–149

    Article  CAS  PubMed  Google Scholar 

  60. Fändrich M (2007) On the structural definition of amyloid fibrils and other polypeptide aggregates. Cell Mol Life Sci 64:2066–2078

    Article  PubMed  CAS  Google Scholar 

  61. Greenwald J, Riek R (2010) Biology of amyloid: structure, function, and regulation. Structure 18:1244–1260

    Article  CAS  PubMed  Google Scholar 

  62. Eisenberg D, Jucker M (2012) The amyloid state of proteins in human diseases. Cell 148:1188–1203

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  63. Sawaya MR, Sambashivan S, Nelson R et al (2007) Atomic structures of amyloid cross-β spines reveal varied steric zippers. Nature 447:453–457

    Article  CAS  PubMed  Google Scholar 

  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 99:16742–16747

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  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 319:1523–1526

    Article  CAS  PubMed  Google Scholar 

  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 102:17342–17347

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  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 435:844–848

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  68. Tycko R (2011) Solid state NMR studies of amyloid fibril structure. Annu Rev Phys Chem 62:279–299

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  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 273:729–739

    Article  CAS  PubMed  Google Scholar 

  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 102:315–320

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  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 435:773–778

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  72. Adamcik J, Mezzenga R (2012) Study of amyloid fibrils via atomic force microscopy. Curr Opin Colloid Interface Sci 17:369–376

    Article  CAS  Google Scholar 

  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 105:7462–7466

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  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 110:5468–5473

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  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 18:815–821

    Article  PubMed  PubMed Central  Google Scholar 

  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 99:9196–9201

    Article  PubMed  CAS  PubMed Central  Google Scholar 

  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 547:185–190

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  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

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  79. Pedersen JS, Andersen CB, Otzen DE (2010) Amyloid structure – one but not the same: the many levels of fibrillar polymorphism. FEBS J 277:4591–4601

    Article  CAS  PubMed  Google Scholar 

  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 120:8809–8817

    Article  CAS  PubMed  Google Scholar 

  81. Pedersen JS, Otzen DE (2008) Amyloid—a state in many guises: survival of the fittest fibril fold. Protein Sci Publ Protein Soc 17:2–10

    Article  CAS  Google Scholar 

  82. Fändrich M, Meinhardt J, Grigorieff N (2009) Structural polymorphism of Alzheimer Aβ and other amyloid fibrils. Prion 3:89–93

    Article  PubMed  PubMed Central  Google Scholar 

  83. Auer S (2015) Nucleation of polymorphic amyloid fibrils. Biophys J 108:1176–1186

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  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 355:501–523

    Article  CAS  PubMed  Google Scholar 

  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 307:262–265

    Article  CAS  PubMed  Google Scholar 

  86. Dobson CM, Šali A, Karplus M (1998) Protein folding: a perspective from theory and experiment. Angew Chem Int Ed 37:868–893

    Article  Google Scholar 

  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 341:1317–1326

    Article  CAS  PubMed  Google Scholar 

  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 27:15092–15101

    Article  CAS  PubMed  Google Scholar 

  89. Uversky VN, Fink AL (2004) Conformational constraints for amyloid fibrillation: the importance of being unfolded. Biochim Biophys Acta BBA 1698:131–153

    Article  CAS  PubMed  Google Scholar 

  90. Sawyer EB, Claessen D, Gras SL, Perrett S (2012) Exploiting amyloid: how and why bacteria use cross-β fibrils. Biochem Soc Trans 40:728–734

    Article  CAS  PubMed  Google Scholar 

  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:e1000222

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  92. Baldwin AJ, Knowles TPJ, Tartaglia GG et al (2011) Metastability of native proteins and the phenomenon of amyloid formation. J Am Chem Soc 133:14160–14163

    Article  CAS  PubMed  Google Scholar 

  93. Gazit E (2002) The “correctly folded” state of proteins: is it a metastable state? Angew Chem Int Ed 41:257–259

    Article  CAS  Google Scholar 

  94. Dobson CM (2001) The structural basis of protein folding and its links with human disease. Philos Trans R Soc Lond Ser B 356:133–145

    Article  CAS  Google Scholar 

  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

    Article  CAS  PubMed  Google Scholar 

  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 110:9758–9763

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  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 326:1533–1537

    Article  CAS  PubMed  Google Scholar 

  98. Jarrett JT, Lansbury PT (1993) Seeding “one-dimensional crystallization” of amyloid: a pathogenic mechanism in Alzheimer’s disease and scrapie? Cell 73:1055–1058

    Article  CAS  PubMed  Google Scholar 

  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 102:2167–2175

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  100. ten Wolde PR, Frenkel D (1997) Enhancement of protein crystal nucleation by critical density fluctuations. Science 277:1975–1978

    Article  PubMed  Google Scholar 

  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 21:2903–2911

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  102. Jucker M, Walker LC (2011) Pathogenic protein seeding in Alzheimer’s disease and other neurodegenerative disorders. Ann Neurol 70:532–540

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  103. Jones EM, Surewicz WK (2005) Fibril conformation as the basis of species- and strain-dependent seeding specificity of mammalian prion amyloids. Cell 121:63–72

    Article  CAS  PubMed  Google Scholar 

  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 103:15806–15811

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  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 43:1196–1201

    Article  PubMed  Google Scholar 

  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 4:4426–4429

    Article  CAS  PubMed  Google Scholar 

  107. Anderson VJ, Lekkerkerker HNW (2002) Insights into phase transition kinetics from colloid science. Nature 416:811–815

    Article  CAS  PubMed  Google Scholar 

  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 101:14420–14424

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  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 82:241–252

    Article  CAS  PubMed  Google Scholar 

  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 129:7517–7522

    Article  CAS  PubMed  Google Scholar 

  111. Ashby MF, Gibson LJ, Wegst U, Olive R (1995) The mechanical properties of natural materials. Proc R Soc Lond Math Phys Eng Sci 450:123–140

    Article  Google Scholar 

  112. Wegst UGK, Ashby MF (2004) The mechanical efficiency of natural materials. Philos Mag 84:2167–2186

    Article  CAS  Google Scholar 

  113. Shen ZL, Dodge MR, Kahn H, Ballarini R, Eppell SJ (2008) Stress-strain experiments on individual collagen fibrils. Biophys J 95:3956–3963

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  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:160–168

    Article  CAS  Google Scholar 

  115. Slotta U, Hess S, Spieß K, Stromer T, Serpell L, Scheibel T (2007) Spider silk and amyloid fibrils: a structural comparison. Macromol Biosci 7:183–188

    Article  CAS  PubMed  Google Scholar 

  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 9:359–367

    Article  CAS  PubMed  Google Scholar 

  117. Fratzl P, Weinkamer R (2007) Nature’s hierarchical materials. Prog Mater Sci 52:1263–1334

    Article  CAS  Google Scholar 

  118. Kreplak L, Bär H, Leterrier JF, Herrmann H, Aebi U (2005) Exploring the mechanical behavior of single intermediate filaments. J Mol Biol 354:569–577

    Article  CAS  PubMed  Google Scholar 

  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

    Article  PubMed  PubMed Central  Google Scholar 

  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 5:1343–1346

    Article  CAS  PubMed  Google Scholar 

  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 5:423–428

    Article  CAS  PubMed  Google Scholar 

  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 29:665–670

    Article  CAS  Google Scholar 

  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 49:1321–1323

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  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 90:2510–2524

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  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 98:1277–1284

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  126. Guo S, Akhremitchev BB (2006) Packing density and structural heterogeneity of insulin amyloid fibrils measured by AFM nanoindentation. Biomacromolecules 7:1630–1636

    Article  CAS  PubMed  Google Scholar 

  127. Ashby MF, Gibson LJ, Wegst U, Olive R (1995) The mechanical properties of natural materials. Proc Math Phys Sci 450:123–140

    Article  Google Scholar 

  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

    Article  Google Scholar 

  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 6:1629–1634

    Article  CAS  PubMed  Google Scholar 

  130. Hauser CAE, Maurer-Stroh S, Martins IC (2014) Amyloid-based nanosensors and nanodevices. Chem Soc Rev 43:5326–5345

    Article  CAS  PubMed  Google Scholar 

  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 31:1802–1810

    Article  CAS  PubMed  Google Scholar 

  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 8:1736–1740

    Article  CAS  PubMed  Google Scholar 

  133. Li C, Born A-K, Schweizer T, Zenobi-Wong M, Cerruti M, Mezzenga R (2014) Amyloid-hydroxyapatite bone biomimetic composites. Adv Mater 26:3207–3212

    Article  CAS  PubMed  Google Scholar 

  134. Meier C, Welland ME (2011) Wet-spinning of amyloid protein nanofibers into multifunctional high-performance biofibers. Biomacromolecules 12:3453–3459

    Article  CAS  PubMed  Google Scholar 

  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 54:97–105

    Article  CAS  PubMed  Google Scholar 

  136. Reynolds NP, Charnley M, Mezzenga R, Hartley PG (2014) Engineered lysozyme amyloid fibril networks support cellular growth and spreading. Biomacromolecules 15:599–608

    Article  CAS  PubMed  Google Scholar 

  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 29:1553–1562

    Article  CAS  PubMed  Google Scholar 

  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, 419–420

    Article  CAS  PubMed  Google Scholar 

  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

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  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 29:10205–10212

    Article  CAS  PubMed  Google Scholar 

  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 55:9877–9882

    Article  CAS  PubMed  Google Scholar 

  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 9:1474–1479

    Article  CAS  PubMed  Google Scholar 

  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 58:9800–9808

    Article  CAS  PubMed  Google Scholar 

  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 59:9605–9611

    Article  CAS  PubMed  Google Scholar 

  145. Graveland-Bikker JF, de Kruif CG (2006) Unique milk protein based nanotubes: food and nanotechnology meet. Trends Food Sci Technol 17:196–203

    Article  CAS  Google Scholar 

  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 28:248–256

    Article  CAS  PubMed  Google Scholar 

  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 25:3694–3700

    Article  CAS  PubMed  Google Scholar 

  148. Li C, Adamcik J, Mezzenga R (2012) Biodegradable nanocomposites of amyloid fibrils and graphene with shape-memory and enzyme-sensing properties. Nat Nanotechnol 7:421–427

    Article  CAS  PubMed  Google Scholar 

  149. Mi R, Liu Y, Chen X, Shao Z (2016) Structure and properties of various hybrids fabricated by silk nanofibrils and nanohydroxyapatite. Nanoscale 8:20096–20102

    Article  CAS  PubMed  Google Scholar 

  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 111:191–196

    Article  CAS  PubMed  Google Scholar 

  151. Li D, Jones EM, Sawaya MR et al (2014) Structure-based design of functional amyloid materials. J Am Chem Soc 136:18044–18051

    Article  CAS  PubMed  Google Scholar 

  152. Bolisetty S, Mezzenga R (2016) Amyloid–carbon hybrid membranes for universal water purification. Nat Nanotechnol 11:365–371

    Article  CAS  PubMed  Google Scholar 

  153. Bolisetty S, Arcari M, Adamcik J, Mezzenga R (2015) Hybrid amyloid membranes for continuous flow catalysis. Langmuir 31:13867–13873

    Article  CAS  PubMed  Google Scholar 

  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 28:1704476

    Article  CAS  Google Scholar 

  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 9:198–210

    Article  CAS  PubMed  Google Scholar 

  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 6:4645–4655

    Article  CAS  PubMed  Google Scholar 

  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 28:579–587

    Article  CAS  PubMed  Google Scholar 

  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 4:1601223

    Article  CAS  Google Scholar 

  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 147:251–262

    Article  CAS  Google Scholar 

  160. Das M, Zhang H, Kumacheva E (2006) Microgels: old materials with new applications. Annu Rev Mater Res 36:117–142

    Article  CAS  Google Scholar 

  161. Seiffert S (2013) Small but smart: sensitive microgel capsules. Angew Chem Int Ed 52:11462–11468

    Article  CAS  Google Scholar 

  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 147:88–108

    Article  CAS  Google Scholar 

  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 71:815–822

    Article  CAS  Google Scholar 

  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 289:10399–10410

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  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 56:6739–6743

    Article  CAS  Google Scholar 

  166. Hu Z, Chen Y, Wang C, Zheng Y, Li Y (1998) Polymer gels with engineered environmentally responsive surface patterns. Nature 393:149–152

    Article  CAS  Google Scholar 

  167. Lu Y, Mei Y, Ballauff M, Drechsler M (2006) Thermosensitive core−shell particles as carrier systems for metallic nanoparticles. J Phys Chem B 110:3930–3937

    Article  CAS  PubMed  Google Scholar 

  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 289:693–698

    Article  CAS  Google Scholar 

  169. Vinogradov SV (2006) Colloidal microgels in drug delivery applications. Curr Pharm Des 12:4703–4712

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  170. Oh JK, Drumright R, Siegwart DJ, Matyjaszewski K (2008) The development of microgels/nanogels for drug delivery applications. Prog Polym Sci Oxf 33:448–477

    Article  CAS  Google Scholar 

  171. Lopez VC, Hadgraft J, Snowden MJ (2005) The use of colloidal microgels as a (trans)dermal drug delivery system. Int J Pharm 292:137–147

    Article  CAS  PubMed  Google Scholar 

  172. Hoare TR, Kohane DS (2008) Hydrogels in drug delivery: progress and challenges. Polymer 49:1993–2007

    Article  CAS  Google Scholar 

  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 4:3054–3064

    Article  CAS  PubMed  Google Scholar 

  174. Du X, Zhou J, Shi J, Xu B (2015) Supramolecular hydrogelators and hydrogels: from soft matter to molecular biomaterials. Chem Rev 115:13165–13307

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  175. Velasco D, Tumarkin E, Kumacheva E (2012) Microfluidic encapsulation of cells in polymer microgels. Small 8:1633–1642

    Article  CAS  PubMed  Google Scholar 

  176. Lipinski CA (2000) Drug-like properties and the causes of poor solubility and poor permeability. J Pharmacol Toxicol Methods 44:235–249

    Article  CAS  PubMed  Google Scholar 

  177. Stella VJ, Nti-Addae KW (2007) Prodrug strategies to overcome poor water solubility. Adv Drug Deliv Rev 59:677–694

    Article  CAS  PubMed  Google Scholar 

  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 21:3659–3666

    Article  CAS  Google Scholar 

  179. Angel (Shimanovich) U, Matas D, Michaeli S, Cavaco-Paulo A, Gedanken A (2010) Microspheres of mixed proteins. Chem Eur J 16:2108–2114

    Article  CAS  Google Scholar 

  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 1:82–90

    Article  PubMed  Google Scholar 

  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 6:19370

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  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 12:3558–3569

    Article  CAS  PubMed  Google Scholar 

  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 19:512–521

    Article  CAS  Google Scholar 

  184. Branco MC, Pochan DJ, Wagner NJ, Schneider JP (2009) Macromolecular diffusion and release from self-assembled β-hairpin peptide hydrogels. Biomaterials 30:1339–1347

    Article  CAS  PubMed  Google Scholar 

  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 106:4623–4628

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  186. Ramachandran S, Tseng Y, Yu YB (2005) Repeated rapid shear-responsiveness of peptide hydrogels with tunable shear modulus. Biomacromolecules 6:1316–1321

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  187. Stendahl JC, Wang LJ, Chow LW, Kaufman DB, Stupp SI (2008) Growth factor delivery from self-assembling nanofibers to facilitate islet transplantation. Transplantation 86:478–481

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  188. Baldwin AJ, Bader R, Christodoulou J, MacPhee CE, Dobson CM, Barker PD (2006) Cytochrome display on amyloid fibrils. J Am Chem Soc 128:2162–2163

    Article  CAS  PubMed  Google Scholar 

  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 65:175–187

    Article  CAS  PubMed  Google Scholar 

  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 7:391–399

    Article  CAS  PubMed  Google Scholar 

  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:ncomms12934

    Article  CAS  Google Scholar 

  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 87:244104

    Article  CAS  Google Scholar 

  193. Gedanken A (2008) Preparation and properties of proteinaceous microspheres made sonochemically. Chem Eur J 14:3840–3853

    Article  CAS  PubMed  Google Scholar 

  194. Silva R, Ferreira H, Cavaco-Paulo A (2011) Sonoproduction of liposomes and protein particles as templates for delivery purposes. Biomacromolecules 12:3353–3368

    Article  CAS  PubMed  Google Scholar 

  195. Xu H, Zeiger BW, Suslick KS (2013) Sonochemical synthesis of nanomaterials. Chem Soc Rev 42:2555–2567

    Article  CAS  PubMed  Google Scholar 

  196. Whitesides GM (2006) The origins and the future of microfluidics. Nature 442:368–373

    Article  CAS  PubMed  Google Scholar 

  197. Squires TM, Quake SR (2005) Microfluidics: fluid physics at the nanoliter scale. Rev Mod Phys 77:977–1026

    Article  CAS  Google Scholar 

  198. Wang J-T, Wang J, Han J-J (2011) Fabrication of advanced particles and particle-based materials assisted by droplet-based microfluidics. Small 7:1728–1754

    Article  CAS  PubMed  Google Scholar 

  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 128:12205–12210

    Article  CAS  PubMed  Google Scholar 

  200. Tumarkin E, Kumacheva E (2009) Microfluidic generation of microgels from synthetic and natural polymers. Chem Soc Rev 38:2161–2168

    Article  CAS  PubMed  Google Scholar 

  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 32:702–708

    Article  CAS  Google Scholar 

  202. Shum HC, Kim J-W, Weitz DA (2008) Microfluidic fabrication of monodisperse biocompatible and biodegradable polymersomes with controlled permeability. J Am Chem Soc 130:9543–9549

    Article  CAS  PubMed  Google Scholar 

  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 26:3716–3724

    Article  CAS  PubMed  Google Scholar 

  204. Xia Y, Whitesides GM (1998) Soft lithography. Angew Chem Int Ed 37:550–575

    Article  CAS  Google Scholar 

  205. McDonald JC, Duffy DC, Anderson JR, Chiu DT, Wu H, Schueller OJA, Whitesides GM (2000) Fabrication of microfluidic systems in poly(dimethylsiloxane). Electrophoresis 21:27–40

    Article  CAS  PubMed  Google Scholar 

  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 8:870–891

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  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 1:688–692

    Article  PubMed  CAS  Google Scholar 

  208. Baroud CN, Gallaire F, Dangla R (2010) Dynamics of microfluidic droplets. Lab Chip 10:2032–2045

    Article  CAS  PubMed  Google Scholar 

  209. Abate AR, Weitz DA (2009) High-order multiple emulsions formed in poly(dimethylsiloxane) microfluidics. Small 5:2030–2032

    Article  CAS  PubMed  Google Scholar 

  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 133:15165–15171

    Article  CAS  PubMed  Google Scholar 

  211. Seo M, Paquet C, Nie Z, Xu S, Kumacheva E (2007) Microfluidic consecutive flow-focusing droplet generators. Soft Matter 3:986–992

    Article  CAS  PubMed  Google Scholar 

  212. Keating CD (2012) Aqueous phase separation as a possible route to compartmentalization of biological molecules. Acc Chem Res 45:2114–2124

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  213. Plamper FA, Richtering W (2017) Functional microgels and microgel systems. Acc Chem Res 50:131–140

    Article  CAS  PubMed  Google Scholar 

  214. Thorne JB, Vine GJ, Snowden MJ (2011) Microgel applications and commercial considerations. Colloid Polym Sci 289:625

    Article  CAS  Google Scholar 

  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 21:1362–1373

    Article  CAS  PubMed  Google Scholar 

  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 32:1477–1483

    Article  CAS  PubMed  Google Scholar 

  217. Agnihotri SA, Mallikarjuna NN, Aminabhavi TM (2004) Recent advances on chitosan-based micro- and nanoparticles in drug delivery. J Control Release 100:5–28

    Article  CAS  PubMed  Google Scholar 

  218. Mitra A, Dey B (2011) Chitosan microspheres in novel drug delivery systems. Indian J Pharm Sci 73:355–366

    CAS  PubMed  PubMed Central  Google Scholar 

  219. Augst AD, Kong HJ, Mooney DJ (2006) Alginate hydrogels as biomaterials. Macromol Biosci 6:623–633

    Article  CAS  PubMed  Google Scholar 

  220. Tan W-H, Takeuchi S (2007) Monodisperse alginate hydrogel microbeads for cell encapsulation. Adv Mater 19:2696–2701

    Article  CAS  Google Scholar 

  221. Gazit E (2007) Self-assembled peptide nanostructures: the design of molecular building blocks and their technological utilization. Chem Soc Rev 36:1263–1269

    Article  CAS  PubMed  Google Scholar 

  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 8:7005–7013

    Article  CAS  PubMed  Google Scholar 

  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 8:128–138

    Article  CAS  PubMed  Google Scholar 

  224. Bhak G, Lee S, Park JW, Cho S, Paik SR (2010) Amyloid hydrogel derived from curly protein fibrils of α-synuclein. Biomaterials 31:5986–5995

    Article  CAS  PubMed  Google Scholar 

  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 49:5082–5084

    Article  CAS  Google Scholar 

  226. Gosal WS, Clark AH, Ross-Murphy SB (2004) Fibrillar β-lactoglobulin gels: Part 2. Dynamic mechanical characterization of heat-set systems. Biomacromolecules 5:2420–2429

    Article  CAS  PubMed  Google Scholar 

  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 13:3241–3252

    Article  CAS  PubMed  Google Scholar 

  228. Jung J-M, Mezzenga R (2010) Liquid crystalline phase behavior of protein Fibers in water: experiments versus theory. Langmuir 26:504–514

    Article  CAS  PubMed  Google Scholar 

  229. Nyström G, Fong W-K, Mezzenga R (2017) Ice-templated and cross-linked amyloid fibril aerogel scaffolds for cell growth. Biomacromolecules 18:2858–2865

    Article  PubMed  CAS  Google Scholar 

  230. Langton M, Hermansson A-M (1992) Fine-stranded and particulate gels of β-lactoglobulin and whey protein at varying pH. Food Hydrocoll 5:523–539

    Article  CAS  Google Scholar 

  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 9:5772–5781

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  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 9:3079–3088

    Article  CAS  PubMed  Google Scholar 

  233. Shimanovich U, Ruggeri FS, Genst ED et al (2017) Silk micrococoons for protein stabilisation and molecular encapsulation. Nat Commun 8:ncomms15902

    Article  CAS  Google Scholar 

  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 14:1315–1319

    Article  PubMed  Google Scholar 

  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 366:705–707

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  236. Subia B, Kundu SC (2013) Drug loading and release on tumor cells using silk fibroin–albumin nanoparticles as carriers. Nanotechnology 24:035103

    Article  CAS  PubMed  Google Scholar 

  237. Shimanovich U, Volkov V, Eliaz D, Aizer A, Michaeli S, Gedanken A (2011) Stabilizing RNA by the sonochemical formation of RNA nanospheres. Small 7:1068–1074

    Article  CAS  PubMed  Google Scholar 

  238. Shimanovich U, Eliaz D, Aizer A, Vayman I, Michaeli S, Shav-Tal Y, Gedanken A (2011) Sonochemical synthesis of DNA nanospheres. Chembiochem 12:1678–1681

    Article  CAS  PubMed  Google Scholar 

  239. Li C, Xu L, Zuo YY, Yang P (2018) Tuning protein assembly pathways through superfast amyloid-like aggregation. Biomater Sci 6:836–841

    Article  CAS  PubMed  Google Scholar 

  240. Shimanovich U, Song Y, Brujic J, Shum HC, Knowles TPJ (2015) Multiphase protein microgels. Macromol Biosci 15:501–508

    Article  CAS  PubMed  Google Scholar 

  241. Knowles T, Shimanovich U, Dobson C, Weitz D (2016) Protein Capsules

    Google Scholar 

  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 4:7989–7999

    Article  CAS  PubMed  Google Scholar 

  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 5:233–234

    Article  Google Scholar 

  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 104:217–239

    Article  CAS  PubMed  Google Scholar 

  245. Diamond AD, Hsu JT (1990) Protein partitioning in PEG/dextran aqueous two-phase systems. AICHE J 36:1017–1024

    Article  CAS  Google Scholar 

  246. Fele L, Fermeglia M (1996) Partition coefficients of proteins in poly(ethylene glycol) + dextran + water at 298 K. J Chem Eng Data 41:331–334

    Article  CAS  Google Scholar 

  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 84:451–456

    Article  CAS  Google Scholar 

  248. Sah H (1999) Stabilization of proteins against methylene chloride/water interface-induced denaturation and aggregation. J Control Release 58:143–151

    Article  CAS  PubMed  Google Scholar 

  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 28:3831–3839

    Article  CAS  PubMed  Google Scholar 

  250. Balakrishnan G, Nicolai T, Benyahia L, Durand D (2012) Particles trapped at the droplet interface in water-in-water emulsions. Langmuir 28:5921–5926

    Article  CAS  PubMed  Google Scholar 

  251. Nguyen BT, Nicolai T, Benyahia L (2013) Stabilization of water-in-water emulsions by addition of protein particles. Langmuir 29:10658–10664

    Article  CAS  PubMed  Google Scholar 

  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 427:460–466

    Article  CAS  PubMed  Google Scholar 

  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 17:11171–11177

    CAS  Google Scholar 

  254. Krysmann MJ, Castelletto V, Kelarakis A, Hamley IW, Hule RA, Pochan DJ (2008) Self-assembly and hydrogelation of an amyloid peptide fragment. Biochemistry 47:4597–4605

    Article  CAS  PubMed  Google Scholar 

  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 6:1961–1968

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  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 7:2876–2880

    Article  CAS  PubMed  Google Scholar 

  257. Li M-H, Keller P (2009) Stimuli-responsive polymer vesicles. Soft Matter 5:927–937

    Article  CAS  Google Scholar 

  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 8:130–136

    Article  CAS  PubMed  Google Scholar 

  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 112:2996–3001

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  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 15:2793–2799

    Article  CAS  PubMed  Google Scholar 

  261. Shen Y, Posavec L, Bolisetty S et al (2017) Amyloid fibril systems reduce, stabilize and deliver bioavailable nanosized iron. Nat Nanotechnol 12:642–647

    Article  CAS  PubMed  Google Scholar 

  262. Levin A, Mason TO, Knowles TPJ, Shimanovich U (2017) Self-assembled protein fibril-metal oxide nanocomposites. Isr J Chem 57(7):724–728

    Article  CAS  Google Scholar 

  263. Sandhu A, Handa H, Abe M (2010) Synthesis and applications of magnetic nanoparticles for biorecognition and point of care medical diagnostics. Nanotechnology 21:442001

    Article  PubMed  CAS  Google Scholar 

  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 27:843–850

    Article  CAS  PubMed  Google Scholar 

  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 30:10090–10097

    Article  CAS  PubMed  Google Scholar 

  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 104:8691–8696

    Article  CAS  PubMed  PubMed Central  Google Scholar 

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Authors and Affiliations

  1. Centre for Misfolding Diseases, Department of Chemistry, University of Cambridge, Cambridge, UK

    Lianne W. Y. Roode & Tuomas P. J. Knowles

  2. Department of Materials and Interfaces, Weizmann Institute of Science, Rehovot, Israel

    Ulyana Shimanovich

  3. National Laboratory of Biomacromolecules, CAS Center for Excellence in Biomacromolecules, Institute of Biophysics, Chinese Academy of Sciences, Beijing, China

    Si Wu & Sarah Perrett

  4. University of the Chinese Academy of Sciences, Beijing, China

    Si Wu & Sarah Perrett

  5. Cavendish Laboratory, University of Cambridge, Cambridge, UK

    Tuomas P. J. Knowles

Authors
  1. Lianne W. Y. Roode
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  2. Ulyana Shimanovich
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  3. Si Wu
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  4. Sarah Perrett
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  5. Tuomas P. J. Knowles
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Corresponding authors

Correspondence to Ulyana Shimanovich , Sarah Perrett or Tuomas P. J. Knowles .

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Editors and Affiliations

  1. National Laboratory of Biomacromolecules, Institute of Biophysics Chinese Academy of Sciences, Beijing, China

    Sarah Perrett

  2. Department of Biotechnology and Biomedicine, Technical University of Denmark DTU, Lyngby, Denmark

    Alexander K. Buell

  3. Department of Chemistry, University of Cambridge, Cambridge, UK

    Tuomas P.J. Knowles

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Roode, L.W.Y., Shimanovich, U., Wu, S., Perrett, S., Knowles, T.P.J. (2019). Protein Microgels from Amyloid Fibril Networks. In: Perrett, S., Buell, A., Knowles, T. (eds) Biological and Bio-inspired Nanomaterials. Advances in Experimental Medicine and Biology, vol 1174. Springer, Singapore. https://doi.org/10.1007/978-981-13-9791-2_7

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