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Biodegradable nanocomposites of amyloid fibrils and graphene with shape-memory and enzyme-sensing properties

Abstract

Graphene has exceptional mechanical and electronic properties1,2,3, but its hydrophobic nature is a disadvantage in biologically related applications4,5. Amyloid fibrils are naturally occurring protein aggregates that are stable in solution or under highly hydrated conditions, have well-organized supramolecular structures and outstanding strength6,7. Here, we show that graphene and amyloid fibrils can be combined to create a new class of biodegradable composite materials with adaptable properties. This new composite material is inexpensive, highly conductive and can be degraded by enzymes. Furthermore, it can reversibly change shape in response to variations in humidity, and can be used in the design of biosensors for quantifying the activity of enzymes. The properties of the composite can be fine-tuned by changing the graphene-to-amyloid ratio.

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Figure 1: Schematic representation showing the fabrication of free-standing films of amyloid fibrils–graphene composites.
Figure 2: Interaction of amyloid fibrils and GO.
Figure 3: Interaction of reduced graphene nanosheets with amyloid fibrils.
Figure 4: Structural characterization of free-standing hybrid nanocomposite films.
Figure 5: Physical, biodegradable and enzyme-sensing properties of the hybrid nanocomposite films.

References

  1. 1

    Rao, C. N. R., Sood, A. K., Subrahmanyam, K. S. & Govindaraj, A. Graphene: the new two-dimensional nanomaterial. Angew. Chem. Int. Ed. 48, 7752–7777 (2009).

    CAS  Article  Google Scholar 

  2. 2

    Stankovich, S. et al. Graphene-based composite materials. Nature 442, 282–286 (2006).

    CAS  Article  Google Scholar 

  3. 3

    Geim, A. K. & Novoselov, K. S. The rise of graphene. Nature Mater. 6, 183–191 (2007).

    CAS  Article  Google Scholar 

  4. 4

    Patil, A. J., Vickery, J. L., Scott, T. B. & Mann, S. Aqueous stabilization and self-assembly of graphene sheets into layered bio-nanocomposites using DNA. Adv. Mater. 21, 3159–3164 (2009).

    CAS  Article  Google Scholar 

  5. 5

    Fan, H. et al. Fabrication, mechanical properties, and biocompatibility of graphene-reinforced chitosan composites. Biomacromolecules 11, 2345–2351 (2010).

    CAS  Article  Google Scholar 

  6. 6

    Cherny, I. & Gazit, E. Amyloids: not only pathological agents but also ordered nanomaterials. Angew. Chem. Int. Ed. 47, 4062–4069 (2008).

    CAS  Article  Google Scholar 

  7. 7

    Knowles, T. P. J. & Buehler, M. J. Nanomechanics of functional and pathological amyloid materials. Nature Nanotech. 6, 469–479 (2011).

    CAS  Article  Google Scholar 

  8. 8

    Park, S. & Ruoff, R. S. Chemical methods for the production of graphenes. Nature Nanotech. 4, 217–224 (2009).

    CAS  Article  Google Scholar 

  9. 9

    Laaksonen, P. et al. Interfacial engineering by proteins: exfoliation and functionalization of graphene by hydrophobins. Angew. Chem. Int. Ed. 122, 5066–5069 (2010).

    Article  Google Scholar 

  10. 10

    Han, T. H. et al. Peptide/graphene hybrid assembly into core/shell nanowires. Adv. Mater. 22, 2060–2064 (2010).

    CAS  Article  Google Scholar 

  11. 11

    Laaksonen, P. et al. Genetic engineering of biomimetic nanocomposites: diblock proteins, graphene, and nanofibrillated cellulose. Angew. Chem. Int. Ed. 50, 8688–8691 (2011).

    CAS  Article  Google Scholar 

  12. 12

    Park, S. et al. Biocompatible, robust free-standing paper composed of a TWEEN/graphene composite. Adv. Mater. 22, 1736–1740 (2010).

    CAS  Article  Google Scholar 

  13. 13

    Chung, W-J. et al. Biomimetic self-templating supramolecular structures. Nature 478, 364–368 (2011).

    CAS  Article  Google Scholar 

  14. 14

    Dvir, T., Timko, B. P., Kohane, D. S. & Langer, R. Nanotechnological strategies for engineering complex tissues. Nature Nanotech. 6, 13–22 (2011).

    CAS  Article  Google Scholar 

  15. 15

    Nudelman, F. et al. The role of collagen in bone apatite formation in the presence of hydroxyapatite nucleation inhibitors. Nature Mater. 9, 1004–1009 (2010).

    CAS  Article  Google Scholar 

  16. 16

    Mostaert, A. S. & Jarvis, S. P. Beneficial characteristics of mechanically functional amyloid fibrils evolutionarily preserved in natural adhesives. Nanotechnology 18, 044010 (2007).

    Article  Google Scholar 

  17. 17

    Mostaert, A. S. et al. Characterisation of amyloid nanostructures in the natural adhesive of unicellular subaerial algae. J. Adhesion 85, 465–483 (2009).

    CAS  Article  Google Scholar 

  18. 18

    Losic, D., Martin, L. L., Aguilar, M. & Small, D. H. β-Amyloid fibril formation is promoted by step edges of highly oriented pyrolytic graphite. Pept. Sci. 84, 519–526 (2006).

    CAS  Article  Google Scholar 

  19. 19

    Gras, S. L. in Engineering Aspects of Self-Organizing Materials (ed. Koopmans, R. J.) 161–209 (Academic, 2009).

    Book  Google Scholar 

  20. 20

    Bolisetty, S. et al. Amyloid-mediated synthesis of giant, fluorescent, gold single crystals and their hybrid sandwiched composites driven by liquid crystalline interactions. J. Colloid Interf. Sci. 361, 90–96 (2011).

    CAS  Article  Google Scholar 

  21. 21

    Jung, J-M., Savin, G., Pouzot, M., Schmitt, C. & Mezzenga, R. Structure of heat-induced β-lactoglobulin aggregates and their complexes with sodium-dodecyl sulfate. Biomacromolecules 9, 2477–2486 (2008).

    CAS  Article  Google Scholar 

  22. 22

    Adamcik, J. et al. Understanding amyloid aggregation by statistical analysis of atomic force microscopy images. Nature Nanotech. 5, 423–428 (2010).

    CAS  Article  Google Scholar 

  23. 23

    Bolisetty, S., Adamcik, J. & Mezzenga, R. Snapshots of fibrillation and aggregation kinetics in multistranded amyloid β-lactoglobulin fibrils. Soft Matter 7, 493–499 (2011).

    CAS  Article  Google Scholar 

  24. 24

    Lara, C., Adamcik, J., Jordens, S. & Mezzenga, R. General self-assembly mechanism converting hydrolyzed globular proteins into giant multistranded amyloid ribbons. Biomacromolecules 12, 1868–1875 (2011).

    CAS  Article  Google Scholar 

  25. 25

    Zhu, Y. et al. Graphene and graphene oxide: synthesis, properties, and applications. Adv. Mater. 22, 3906–3924 (2010).

    CAS  Article  Google Scholar 

  26. 26

    Li, D., Muller, M. B., Gilje, S., Kaner, R. B. & Wallace, G. G. Processable aqueous dispersions of graphene nanosheets. Nature Nanotech. 3, 101–105 (2008).

    CAS  Article  Google Scholar 

  27. 27

    Jung, J-M., Gunes, D. Z. & Mezzenga, R. Interfacial activity and interfacial shear rheology of native β-lactoglobulin monomers and their heat-induced fibers. Langmuir 26, 15366–15375 (2010).

    CAS  Article  Google Scholar 

  28. 28

    Isa, L., Jung, J-M. & Mezzenga, R. Unravelling adsorption and alignment of amyloid fibrils at interfaces by probe particle tracking. Soft Matter 7, 8127–8134 (2011).

    CAS  Article  Google Scholar 

  29. 29

    Peng, X., Jin, J., Ericsson, E. M. & Ichinose, I. General method for ultrathin free-standing films of nanofibrous composite materials. J. Am. Chem. Soc. 129, 8625–8633 (2007).

    CAS  Article  Google Scholar 

  30. 30

    Walther, A. et al. Large-area, lightweight and thick biomimetic composites with superior material properties via fast, economic, and green pathways. Nano. Lett. 10, 2742–2748 (2010).

    CAS  Article  Google Scholar 

  31. 31

    Knowles, T. P. J., Oppenheim, T. W., Buell, A. K., Chirgadze, D. Y. & Welland, M. E. Nanostructured films from hierarchical self-assembly of amyloidogenic proteins. Nature Nanotech. 5, 204–207 (2010).

    CAS  Article  Google Scholar 

  32. 32

    Gao, J. et al. Environment-friendly method to produce graphene that employs vitamin C and amino acid. Chem. Mater. 22, 2213–2218 (2010).

    CAS  Article  Google Scholar 

  33. 33

    Xu, Y., Bai, H., Lu, G., Li, C. & Shi, G. Flexible graphene films via the filtration of water-soluble noncovalent functionalized graphene sheets. J. Am. Chem. Soc. 130, 5856–5857 (2008).

    CAS  Article  Google Scholar 

  34. 34

    Lee, C., Wei, X., Kysar, J. W. & Hone, J. Measurement of the elastic properties and intrinsic strength of monolayer graphene. Science 321, 385–388 (2008).

    CAS  Article  Google Scholar 

  35. 35

    Paparcone, R., Keten, S. & Buehler, M. J. Atomistic simulation of nanomechanical properties of Alzheimer's Aβ(1–40) amyloid fibrils under compressive and tensile loading. J. Biomech. 43, 1196–1201 (2010).

    Article  Google Scholar 

  36. 36

    Smith, J. F., Knowles, T. P. J., Dobson, C. M., Macphee, C. E. & Welland, M. E. Characterization of the nanoscale properties of individual amyloid fibrils. Proc. Natl Acad. Sci. USA 103, 15806–15811 (2006).

    CAS  Article  Google Scholar 

  37. 37

    Knowles, T. P. et al. Role of intermolecular forces in defining material properties of protein nanofibrils. Science 318, 1900–1903 (2007).

    CAS  Article  Google Scholar 

  38. 38

    Adamcik, J., Berquand, A. & Mezzenga, R. Single-step direct measurement of amyloid fibrils stiffness by peak force quantitative nanomechanical atomic force microscopy. Appl. Phys. Lett. 98, 193701 (2011).

    Article  Google Scholar 

  39. 39

    Nair, R. R., Wu, H. A., Jayaram, P. N., Grigorieva, I. V. & Geim, A. K. Unimpeded permeation of water through helium-leak-tight graphene-based membranes. Science 335, 442–444 (2012).

    CAS  Article  Google Scholar 

  40. 40

    Park, S., An, J., Suk, J. W. & Ruoff, R. S. Graphene-based actuators. Small 6, 210–212 (2010).

    CAS  Article  Google Scholar 

  41. 41

    Bateman, L., Ye, A. & Singh, H. In vitro digestion of β-lactoglobulin fibrils formed by heat treatment at low pH. J. Agric. Food Chem. 58, 9800–9808 (2010).

    CAS  Article  Google Scholar 

  42. 42

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

    CAS  Article  Google Scholar 

  43. 43

    Marcano, D. C. et al. Improved synthesis of graphene oxide. ACS Nano 4, 4806–4814 (2010).

    CAS  Article  Google Scholar 

Download references

Acknowledgements

The authors thank S. Handschin for SEM images. H. Adelmann, J. Rao and T. Schweizer are acknowledged for assistance with mechanical, electrical conductivity and thermal gravimetric analysis measurements, respectively.

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C.L. performed the study, the experiments and wrote the paper. J.A. performed the AFM analysis. R.M. designed the study, directed the work and wrote the paper.

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Correspondence to Raffaele Mezzenga.

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Li, C., Adamcik, J. & Mezzenga, R. Biodegradable nanocomposites of amyloid fibrils and graphene with shape-memory and enzyme-sensing properties. Nature Nanotech 7, 421–427 (2012). https://doi.org/10.1038/nnano.2012.62

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