Skip to main content

Thank you for visiting nature.com. You are using a browser version with limited support for CSS. To obtain the best experience, we recommend you use a more up to date browser (or turn off compatibility mode in Internet Explorer). In the meantime, to ensure continued support, we are displaying the site without styles and JavaScript.

  • Article
  • Published:

Directed assembly of bio-inspired hierarchical materials with controlled nanofibrillar architectures

Nature Nanotechnology volume 12, pages 474–480 (2017)Cite this article

Subjects

Abstract

In natural systems, directed self-assembly of structural proteins produces complex, hierarchical materials that exhibit a unique combination of mechanical, chemical and transport properties. This controlled process covers dimensions ranging from the nano- to the macroscale. Such materials are desirable to synthesize integrated and adaptive materials and systems. We describe a bio-inspired process to generate hierarchically defined structures with multiscale morphology by using regenerated silk fibroin. The combination of protein self-assembly and microscale mechanical constraints is used to form oriented, porous nanofibrillar networks within predesigned macroscopic structures. This approach allows us to predefine the mechanical and physical properties of these materials, achieved by the definition of gradients in nano- to macroscale order. We fabricate centimetre-scale material geometries including anchors, cables, lattices and webs, as well as functional materials with structure-dependent strength and anisotropic thermal transport. Finally, multiple three-dimensional geometries and doped nanofibrillar constructs are presented to illustrate the facile integration of synthetic and natural additives to form functional, interactive, hierarchical networks.

This is a preview of subscription content, access via your institution

Access options

Buy this article

  • Purchase on SpringerLink
  • Instant access to full article PDF
Buy now

Prices may be subject to local taxes which are calculated during checkout

Figure 1: Mechanical tension-mediated formation of patterned nanofibrillar structure.
Figure 2: Engineering nanofibrillar order.
Figure 3: Transformation of nanofibrillar shapes in two, three and four dimensions.
Figure 4: Functional nanofibrillar architectures.

Similar content being viewed by others

References

  1. Ortiz, C. & Boyce, M. C. Bioinspired structural materials. Science 319, 1053–1054 (2008).

    Article  CAS  Google Scholar 

  2. Wegst, U. G. K., Bai, H., Saiz, E., Tomsia, A. P. & Ritchie, R. O. Bioinspired structural materials. Nat. Mater. 14, 23–36 (2014).

    Article  Google Scholar 

  3. Lorén, N., Nydén, M. & Hermansson, A.-M. Determination of local diffusion properties in heterogeneous biomaterials. Adv. Colloid Interface Sci. 150, 5–15 (2009).

    Article  Google Scholar 

  4. Jose, R. R., Elia, R., Firpo, M. A., Kaplan, D. L. & Peattie, R. A. Seamless, axially aligned, fiber tubes, meshes, microbundles and gradient biomaterial constructs. J. Mater. Sci. Mater. Med. 23, 2679–2695 (2012).

    Article  CAS  Google Scholar 

  5. Bellail, A. C., Hunter, S. B., Brat, D. J., Tan, C. & Van Meir, E. G. Microregional extracellular matrix heterogeneity in brain modulates glioma cell invasion. Int. J. Biochem. Cell Biol. 36, 1046–1069 (2004).

    Article  CAS  Google Scholar 

  6. Mortarini, R., Anichini, A. & Parmiani, G. Heterogeneity for integrin expression and cytokine-mediated VLA modulation can influence the adhesion of human melanoma cells to extracellular matrix proteins. Int. J. Cancer 47, 551–559 (1991).

    Article  CAS  Google Scholar 

  7. Schneider, D. et al. Nonlinear control of high-frequency phonons in spider silk. Nat. Mater. 15, 1079–1083 (2016).

    Article  CAS  Google Scholar 

  8. Pisignano, D. et al. Polymer nanofibers by soft lithography. Appl. Phys. Lett. 87, 123109 (2005).

    Article  Google Scholar 

  9. Hahn, M. S. et al. Photolithographic patterning of polyethylene glycol hydrogels. Biomaterials 27, 2519–2524 (2006).

    Article  CAS  Google Scholar 

  10. Shi, J., Wang, L. & Chen, Y. Microcontact printing and lithographic patterning of electrospun nanofibers. Langmuir 25, 6015–6018 (2009).

    Article  CAS  Google Scholar 

  11. Hou, H. et al. Electrospun polyacrylonitrile nanofibers containing a high concentration of well-aligned multiwall carbon nanotubes. Chem. Mater. 17, 967–973 (2005).

    Article  CAS  Google Scholar 

  12. Liu, H., Edel, J. B., Bellan, L. M. & Craighead, H. G. Electrospun polymer nanofibers as subwavelength optical waveguides incorporating quantum dots. Small 2, 495–499 (2006).

    Article  CAS  Google Scholar 

  13. Liang, D., Hsiao, B. S. & Chu, B. Functional electrospun nanofibrous scaffolds for biomedical applications. Adv. Drug Deliv. Rev. 59, 1392–1412 (2007).

    Article  CAS  Google Scholar 

  14. Pati, F. et al. Printing three-dimensional tissue analogues with decellularized extracellular matrix bioink. Nat. Commun. 5, 3935 (2014).

    Article  CAS  Google Scholar 

  15. Sydney Gladman, A., Matsumoto, E. A., Nuzzo, R. G., Mahadevan, L. & Lewis, J. A. Biomimetic 4D printing. Nat. Mater. 15, 413–418 (2016).

    Article  CAS  Google Scholar 

  16. Yang, M. et al. Ca2+-induced self-assembly of Bombyx mori silk sericin into a nanofibrous network-like protein matrix for directing controlled nucleation of hydroxylapatite nano-needles. J. Mater. Chem. B 3, 2455–2462 (2015).

    Article  CAS  Google Scholar 

  17. Hsu, L.-H. et al. Nanofibrous hydrogels self-assembled from naphthalene diimide (NDI)/amino acid conjugates. RSC Adv. 5, 20410–20413 (2015).

    Article  CAS  Google Scholar 

  18. Bouville, F. et al. Strong, tough and stiff bioinspired ceramics from brittle constituents. Nat. Mater. 13, 508–514 (2014).

    Article  CAS  Google Scholar 

  19. Olsson, R. T. et al. Making flexible magnetic aerogels and stiff magnetic nanopaper using cellulose nanofibrils as templates. Nat. Nanotech. 5, 584–588 (2010).

    Article  CAS  Google Scholar 

  20. Omenetto, F. G. & Kaplan, D. L. A new route for silk. Nat. Photon. 2, 641–643 (2008).

    Article  CAS  Google Scholar 

  21. Rockwood, D. N. et al. Materials fabrication from Bombyx mori silk fibroin. Nat. Protoc. 6, 1612–1631 (2011).

    Article  CAS  Google Scholar 

  22. Zhu, B. et al. Silk fibroin for flexible electronic devices. Adv. Mater. 28, 4250–4265 (2016).

    Article  CAS  Google Scholar 

  23. Harsh, K. F., Bright, V. M. & Lee, Y. C. Solder self-assembly for three-dimensional microelectromechanical systems. Sens. Actuat. Phys. 77, 237–244 (1999).

    Article  CAS  Google Scholar 

  24. Akiyama, T., Collard, D. & Fujita, H. Scratch drive actuator with mechanical links for self-assembly of three-dimensional MEMS. J. Microelectromech. Syst. 6, 10–17 (1997).

    Article  CAS  Google Scholar 

  25. Xu, S. et al. Assembly of micro/nanomaterials into complex, three-dimensional architectures by compressive buckling. Science 347, 154–159 (2015).

    Article  CAS  Google Scholar 

  26. Khang, D.-Y. et al. Molecular scale buckling mechanics in individual aligned single-wall carbon nanotubes on elastomeric substrates. Nano Lett. 8, 124–130 (2008).

    Article  CAS  Google Scholar 

  27. Syms, R. R. A., Yeatman, E. M., Bright, V. M. & Whitesides, G. M. Surface tension-powered self-assembly of microstructures—the state-of-the-art. J. Microelectromech. Syst. 12, 387–417 (2003).

    Article  Google Scholar 

  28. Srinivasan, U., Liepmann, D. & Howe, R. T. Microstructure to substrate self-assembly using capillary forces. J. Microelectromech. Syst. 10, 17–24 (2001).

    Article  CAS  Google Scholar 

  29. Mastrangeli, M. et al. Self-assembly from milli- to nanoscales methods and applications. J. Micromech. Microeng. 19, 83001 (2009).

    Article  CAS  Google Scholar 

  30. Nogueira, G. M. et al. Preparation and characterization of ethanol-treated silk fibroin dense membranes for biomaterials application using waste silk fibers as raw material. Bioresour. Technol. 101, 8446–8451 (2010).

    Article  CAS  Google Scholar 

  31. Chen, X., Shao, Z., Knight, D. P. & Vollrath, F. Conformation transition kinetics of Bombyx mori silk protein. Proteins 68, 223–231 (2007).

    Article  CAS  Google Scholar 

  32. Lin, Y. et al. Tuning chemical and physical crosslinks in silk electrogels for morphological analysis and mechanical reinforcement. Biomacromolecules 14, 2629–2635 (2013).

    Article  CAS  Google Scholar 

  33. Humenik, M., Smith, A. M. & Scheibel, T. Recombinant spider silks—biopolymers with potential for future applications. Polymers 3, 640–661 (2011).

    Article  CAS  Google Scholar 

  34. Partlow, B. P. et al. Highly tunable elastomeric silk biomaterials. Adv. Funct. Mater. 24, 4615–4624 (2014).

    Article  CAS  Google Scholar 

  35. Mitropoulos, A. N. et al. Transparent, nanostructured silk fibroin hydrogels with tunable mechanical properties. ACS Biomater. Sci. Eng. 1, 964–970 (2015).

    Article  CAS  Google Scholar 

  36. Applegate, M. B. et al. Laser-based three-dimensional multiscale micropatterning of biocompatible hydrogels for customized tissue engineering scaffolds. Proc. Natl Acad. Sci. USA 112, 12052–12057 (2015).

    Article  CAS  Google Scholar 

  37. Mallepally, R. R. et al. Silk fibroin aerogels potential scaffolds for tissue engineering applications. Biomed. Mater. 10, 35002 (2015).

    Article  Google Scholar 

  38. Marin, M. A., Mallepally, R. R. & McHugh, M. A. Silk fibroin aerogels for drug delivery applications. J. Supercrit. Fluids 91, 84–89 (2014).

    Article  CAS  Google Scholar 

  39. Jin, H.-J. et al. Water-stable silk films with reduced β-sheet content. Adv. Funct. Mater. 15, 1241–1247 (2005).

    Article  CAS  Google Scholar 

  40. Boudaoud, A. et al. Fibriltool, an ImageJ plug-in to quantify fibrillar structures in raw microscopy images. Nat. Protoc. 9, 457–463 (2014).

    Article  CAS  Google Scholar 

  41. Lu, S. et al. Insoluble and flexible silk films containing glycerol. Biomacromolecules 11, 143–150 (2010).

    Article  CAS  Google Scholar 

  42. Fernandes, H., Zhang, H. & Maldague, X. An active infrared thermography method for fiber orientation assessment of fiber-reinforced composite materials. Infrared Phys. Technol. 72, 286–292 (2015).

    Article  CAS  Google Scholar 

Download references

Acknowledgements

This work was partially supported through the Office of Naval Research (award N-000141310596). P.T. acknowledges support from the NIH National Institute of Biomedical Imaging and Bioengineering under NRSA fellowship no. F32EB021159. Support from the AFOSR is also acknowledged.

Author information

Author notes

  1. Benedetto Marelli

    Present address: Present Address: Department of Civil and Environmental Engineering, Massachusetts Institute of Technology, 77 Massachusetts Avenue, Room 1-348, Cambridge, Massachusetts 02139–4307, USA,

Authors and Affiliations

  1. Silklab, Tufts University, 200 Boston Avenue, Suite 4875, Medford, 02155, Massachusetts, USA

    Peter Tseng, Bradley Napier, Matthew B. Applegate, Benedetto Marelli, David L. Kaplan & Fiorenzo G. Omenetto

  2. Department of Biomedical Engineering, Tufts University, Medford, 02155, Massachusetts, USA

    Siwei Zhao, Alexander N. Mitropoulos, David L. Kaplan & Fiorenzo G. Omenetto

  3. Department of Chemical Engineering, Tufts University, Medford, 02155, Massachusetts, USA

    David L. Kaplan

  4. Department of Electrical and Computer Engineering, Tufts University, Medford, 02155, Massachusetts, USA

    Fiorenzo G. Omenetto

  5. Department of Physics, Tufts University, Medford, 02155, Massachusetts, USA

    Fiorenzo G. Omenetto

Authors
  1. Peter Tseng
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Bradley Napier
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Siwei Zhao
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Alexander N. Mitropoulos
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Matthew B. Applegate
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Benedetto Marelli
    View author publications

    You can also search for this author in PubMed Google Scholar

  7. David L. Kaplan
    View author publications

    You can also search for this author in PubMed Google Scholar

  8. Fiorenzo G. Omenetto
    View author publications

    You can also search for this author in PubMed Google Scholar

Contributions

P.T., B.M., A.N.M., D.L.K. and F.G.O. contributed to the initial concept. P.T., D.L.K. and F.G.O. designed the test structures. P.T. and S.Z. fabricated the structures. P.T. and B.N. performed the infrared thermography. B.N. performed mechanical testing. P.T. executed mechanical simulations in Comsol. P.T. imaged the samples under SEM and polarization microscopy. M.B.A. performed confocal microscopy. P.T., D.L.K. and F.G.O. wrote the manuscript, and all authors commented on the manuscript.

Corresponding author

Correspondence to Fiorenzo G. Omenetto.

Ethics declarations

Competing interests

The authors declare no competing financial interests.

Supplementary information

Supplementary information

Supplementary information (PDF 1216 kb)

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Tseng, P., Napier, B., Zhao, S. et al. Directed assembly of bio-inspired hierarchical materials with controlled nanofibrillar architectures. Nature Nanotech 12, 474–480 (2017). https://doi.org/10.1038/nnano.2017.4

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1038/nnano.2017.4

This article is cited by

Search

Advanced search

Quick links

Nature Briefing: Translational Research

Sign up for the Nature Briefing: Translational Research newsletter — top stories in biotechnology, drug discovery and pharma.

Get what matters in translational research, free to your inbox weekly. Sign up for Nature Briefing: Translational Research