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Biomimetic 4D printing

Nature Materials volume 15, pages 413–418 (2016)Cite this article

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Abstract

Shape-morphing systems can be found in many areas, including smart textiles1, autonomous robotics2, biomedical devices3, drug delivery4 and tissue engineering5. The natural analogues of such systems are exemplified by nastic plant motions, where a variety of organs such as tendrils, bracts, leaves and flowers respond to environmental stimuli (such as humidity, light or touch) by varying internal turgor, which leads to dynamic conformations governed by the tissue composition and microstructural anisotropy of cell walls6,7,8,9,10. Inspired by these botanical systems, we printed composite hydrogel architectures that are encoded with localized, anisotropic swelling behaviour controlled by the alignment of cellulose fibrils along prescribed four-dimensional printing pathways. When combined with a minimal theoretical framework that allows us to solve the inverse problem of designing the alignment patterns for prescribed target shapes, we can programmably fabricate plant-inspired architectures that change shape on immersion in water, yielding complex three-dimensional morphologies.

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Figure 1: Programming localized anisotropy via biomimetic 4D printing.
Figure 2: Printing simple architectures with precise control over mean and Gaussian curvatures.
Figure 3: Complex flower morphologies generated by biomimetic 4D printing.
Figure 4: Predictive 4D printing of biomimetic architectures.

References

  1. Hu, J., Meng, H., Li, G. & Ibekwe, S. I. A review of stimuli-responsive polymers for smart textile applications. Smart Mater. Struct. 21, 053001 (2012).

    Article  Google Scholar 

  2. Felton, S., Tolley, M., Demaine, E., Rus, D. & Wood, R. A method for building self-folding machines. Science 345, 644–646 (2014).

    CAS  Article  Google Scholar 

  3. Randall, C. L., Gultepe, E. & Gracias, D. H. Self-folding devices and materials for biomedical applications. Trends Biotechnol. 30, 138–146 (2012).

    CAS  Article  Google Scholar 

  4. Fernandes, R. & Gracias, D. H. Self-folding polymeric containers for encapsulation and delivery of drugs. Adv. Drug Deliv. Rev. 64, 1579–1589 (2012).

    CAS  Article  Google Scholar 

  5. Kuribayashi-Shigetomi, K., Onoe, H. & Takeuchi, S. Cell origami: self-folding of three-dimensional cell-laden microstructures driven by cell traction force. PLoS ONE 7, e51085 (2012).

    CAS  Article  Google Scholar 

  6. Forterre, Y., Skotheim, J., Dumais, J. & Mahadevan, L. How the Venus flytrap snaps. Nature 433, 421–425 (2005).

    CAS  Article  Google Scholar 

  7. Awell, B. J., Kriedemann, P. E. & Turnbull, C. G. N. Plants in Action (Macmillan Education AU, 1999).

    Google Scholar 

  8. Reyssat, E. & Mahadevan, L. Hygromorphs: from pine cones to biomimetic bilayers. J. R. Soc. Interface 6, 951–957 (2009).

    CAS  Article  Google Scholar 

  9. Armon, S., Efrati, E., Kupferman, R. & Sharon, E. Geometry and mechanics in the opening of chiral seed pods. Science 333, 1726–1730 (2011).

    CAS  Article  Google Scholar 

  10. Fratzl, P. & Burgert, I. Actuation systems in plants as prototypes for bioinspired devices. Phil. Trans. R. Soc. A 6, 1541–1557 (2009).

    Google Scholar 

  11. Ge, Q., Qi, H. J. & Dunn, M. L. Active materials by four-dimension printing. Appl. Phys. Lett. 103, 131901 (2013).

    Article  Google Scholar 

  12. Ratna, D. & Karger-Kocsis, J. Recent advances in shape memory polymers and composites: a review. J. Mater. Sci. 43, 254–260 (2008).

    CAS  Article  Google Scholar 

  13. Erb, R. M., Sander, J. S., Grisch, R. & Studart, A. E. R. Self-shaping composites with programmable bioinspired microstructures. Nature Commun. 4, 1712 (2012).

    Article  Google Scholar 

  14. Thérien-Aubin, H., Wu, Z. L., Nie, Z. & Kumacheva, E. Multiple shape transformations of composite hydrogel sheets. J. Am. Chem. Soc. 125, 4834–4839 (2013).

    Article  Google Scholar 

  15. Tibbits, S. 4D printing: multi-material shape change. Archit. Des. 84, 116–121 (2014).

    Google Scholar 

  16. Ionov, L. Bioinspired microorigami by self-folding polymer films. Macromol. Chem. Phys. 214, 1178–1183 (2012).

    Article  Google Scholar 

  17. Na, J. H. et al. Programming reversibly self-folding origami with micropatterned photo-crosslinkable polymer trilayers. Adv. Mat. 27, 79–85 (2015).

    CAS  Article  Google Scholar 

  18. Liu, Y., Boyles, J. K., Genzer, J. & Dickey, M. D. Self-folding of polymer sheets using local light absorption. Soft Matter 8, 1764–1769 (2012).

    CAS  Article  Google Scholar 

  19. Lewis, J. A. Direct ink writing of 3D functional materials. Adv. Funct. Mater. 16, 2193–2204 (2006).

    CAS  Article  Google Scholar 

  20. Oytun, F., Kahveci, M. U. & Yagci, Y. Sugar overcomes oxygen inhibition in photoinitiated free radical polymerization. J. Polym. Sci. A 51, 1685–1689 (2013).

    CAS  Article  Google Scholar 

  21. Josset, S. et al. Energy consumption of the nanofibrillation of bleached pulp, wheat straw and recycled newspaper through a grinding process. Nord. Pulp Paper Res. J. 29, 167–175 (2014).

    CAS  Article  Google Scholar 

  22. Haraguchi, K. & Takehisa, T. Nanocomposite hydrogels: a unique organic-inorganic network structure with extraordinary mechanical, optical, and swelling/de-swelling properties. Adv. Mater. 14, 1120–1124 (2002).

    CAS  Article  Google Scholar 

  23. Compton, B. G. & Lewis, J. A. 3D-printing of lightweight cellular composites. Adv. Mater. 26, 5930–5935 (2014).

    CAS  Article  Google Scholar 

  24. Smay, J. E., Cesarano, J. & Lewis, J. A. Colloidal inks for directed assembly of 3-D periodic structures. Langmuir 18, 5429–5437 (2002).

    CAS  Article  Google Scholar 

  25. Aharoni, H., Sharon, E. & Kupferman, R. Geometry of thin nematic elastomer sheets. Phys. Rev. Lett. 113, 257801 (2014).

    Article  Google Scholar 

  26. Timoshenko, S. Analysis of bi-metal thermostats. J. Opt. Soc. Am. 11, 233–255 (1925).

    CAS  Article  Google Scholar 

  27. Modes, C. D., Bhattacharya, K. & Warner, M. Gaussian curvature from flat elastic sheets. Proc. R. Soc. A 467, 1121–1140 (2011).

    Article  Google Scholar 

  28. Abraham, Y. et al. Titled cellulose arrangement as a novel mechanism for hygroscopic coiling in the stork’s bill awn. J. R. Soc. Interface 9, 640–647 (2012).

    Article  Google Scholar 

  29. Liang, H. & Mahadevan, L. The shape of a long leaf. Proc. Natl Acad. Sci. USA 106, 22049–22054 (2009).

    CAS  Article  Google Scholar 

  30. Liang, H. & Mahadevan, L. Growth, geometry, and mechanics of a blooming lily. Proc. Natl Acad. Sci. USA 108, 5516–5521 (2011).

    CAS  Article  Google Scholar 

  31. van Doorn, W. G. Flower opening and closure: a review. J. Exp. Bot. 54, 1801–1812 (2003).

    CAS  Article  Google Scholar 

  32. Haraguchi, K., Li, H.-J., Matsuda, K., Takehisa, T. & Elliott, E. Mechanism of forming organic/inorganic network structures during in-situ free-radical polymerization in PNIPA-clay nanocomposite hydrogels. Macromolecules 38, 3482–3490 (2005).

    CAS  Article  Google Scholar 

  33. Yong, X., Kuksenok, O. & Balazs, A. C. Modeling free radical polymerization using dissipative particle dynamics. Polymer 72, 217–225 (2015).

    CAS  Article  Google Scholar 

  34. Haraguchi, K., Murata, K. & Takehisa, T. Stimuli-responsive nanocomposite gels and soft nanocomposites consisting of inorganic clays and copolymers with different chemical affinities. Macromolecules 45, 385–391 (2012).

    CAS  Article  Google Scholar 

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Acknowledgements

A.S.G. and J.A.L. were supported by the Army Research Office Award No. W911NF-13-0489. E.A.M. and L.M. werez supported by the NSF DMR 14-20570, Materials Research Science and Engineering Center, MRSEC and NSF DMREF 15-33985. We thank D. Stepp (ARO), A. Balazs (U. Pittsburgh), M. Brenner (Harvard) and B. Compton for useful discussions. We thank T. Zimmermann and the researchers at the Applied Wood Materials Laboratory at EMPA for providing samples of nanofibrillated cellulose. We also thank D. Kolesky for assistance with confocal imaging, D. Fitzgerald and J. Minardi for help with initial G-code programming, R. Valentin for permission to print a copy of his orchid photograph, and L. K. Sanders for help with photography and videography.

Author information

Author notes

  1. A. Sydney Gladman and Elisabetta A. Matsumoto: These authors contributed equally to this work.

Authors and Affiliations

  1. John A. Paulson School of Engineering and Applied Sciences, Harvard University, 29 Oxford Street, Cambridge, Massachusetts 02138, USA

    A. Sydney Gladman, Elisabetta A. Matsumoto, L. Mahadevan & Jennifer A. Lewis

  2. Wyss Institute for Biologically Inspired Engineering, Harvard University, 60 Oxford Street, Cambridge, Massachusetts 02138, USA

    A. Sydney Gladman, Elisabetta A. Matsumoto, L. Mahadevan & Jennifer A. Lewis

  3. School of Chemical Sciences, University of Illinois Urbana-Champaign, Urbana, Illinois 61801, USA

    Ralph G. Nuzzo

  4. Departments of Physics and Organismic and Evolutionary Biology, and Kavli Institute for NanoBio Science and Technology, Harvard University, 29 Oxford Street, Cambridge, Massachusetts 02138, USA

    L. Mahadevan

Authors
  1. A. Sydney Gladman
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  4. L. Mahadevan
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Contributions

A.S.G., R.G.N. and J.A.L. developed the 4D printing concept. A.S.G. designed the ink composition, printed and prepared all samples, obtained photographic images, and characterized alignment, swelling, mechanical and rheological properties. E.A.M. and L.M. developed the theoretical model. E.A.M. rendered and calculated the desired shapes and print paths, and generated the G-code for printing. A.S.G., E.A.M., L.M. and J.A.L. wrote the manuscript. A.S.G. and E.A.M. developed the figures. All authors commented on the manuscript.

Corresponding authors

Correspondence to L. Mahadevan or Jennifer A. Lewis.

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The authors declare no competing financial interests.

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Sydney Gladman, A., Matsumoto, E., Nuzzo, R. et al. Biomimetic 4D printing. Nature Mater 15, 413–418 (2016). https://doi.org/10.1038/nmat4544

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