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Dynamic display of biomolecular patterns through an elastic creasing instability of stimuli-responsive hydrogels

Abstract

Surfaces with physicochemical properties that can be modulated using external stimuli offer great promise for designing responsive or adaptive materials. Here, we describe biocompatible dynamic scaffolds based on thin hydrogel coatings that reversibly hide and display surface chemical patterns in response to temperature changes. At room temperature, the gel absorbs water, triggering an elastic creasing instability that sequesters functionalized regions within tight folds in the surface. Deswelling at 37 C causes the gel surface to unfold, thereby regenerating the biomolecular patterns. Crease positions are directed by topographic features on the underlying substrate, and are translated into two-dimensional micrometre-scale surface chemical patterns through selective deposition of biochemically functionalized polyelectrolytes. We demonstrate specific applications of these dynamic scaffolds—selective capture, sequestration and release of micrometre-sized beads, tunable activity of surface-immobilized enzymes and reversible encapsulation of adherent cells—which offer promise for incorporation within lab-on-a-chip devices or as dynamic substrates for cellular biology.

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Figure 1: Fabrication and characterization of scaffolds with dynamic biomolecular patterns.
Figure 2: Patterning functional polyelectrolytes on dynamic scaffolds.
Figure 3: The role of substrate topography in directing crease formation.
Figure 4: Applications of dynamic hydrogel scaffolds.

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References

  1. Mather, P. T. Soft answers for hard problems. Nature Mater. 6, 93–94 (2007).

    Article  CAS  Google Scholar 

  2. Russell, T. P. Surface-responsive materials. Science 297, 964–967 (2002).

    Article  CAS  Google Scholar 

  3. Lahann, J. & Langer, R. Smart materials with dynamically controllable surfaces. MRS Bull. 30, 185–188 (2005).

    Article  CAS  Google Scholar 

  4. Wang, R. et al. Light-induced amphiphilic surfaces. Nature 388, 431–432 (1997).

    Article  CAS  Google Scholar 

  5. Ichimura, K., Oh, S. K. & Nakagawa, M. Light-driven motion of liquids on a photoresponsive surface. Science 288, 1624–1626 (2000).

    Article  CAS  Google Scholar 

  6. Lahann, J. et al. A reversibly switching surface. Science 299, 371–374 (2003).

    Article  CAS  Google Scholar 

  7. Sun, T. L. et al. Reversible switching between superhydrophilicity and superhydrophobicity. Angew. Chem. Int. Ed. 43, 357–360 (2004).

    Article  CAS  Google Scholar 

  8. Fu, Q. et al. Reversible control of free energy and topography of nanostructured surfaces. J. Am. Chem. Soc. 126, 8904–8905 (2004).

    Article  CAS  Google Scholar 

  9. Ionov, L. et al. Reversible chemical patterning on stimuli-responsive polymer film: Environment-responsive lithography. J. Am. Chem. Soc. 125, 8302–8306 (2003).

    Article  CAS  Google Scholar 

  10. Lim, H. S., Han, J. T., Kwak, D., Jin, M. H. & Cho, K. Photoreversibly switchable superhydrophobic surface with erasable and rewritable pattern. J. Am. Chem. Soc. 128, 14458–14459 (2006).

    Article  CAS  Google Scholar 

  11. Chung, J. Y., Youngblood, J. P. & Stafford, C. M. Anisotropic wetting on tunable micro-wrinkled surfaces. Soft Matter 3, 1163–1169 (2007).

    Article  CAS  Google Scholar 

  12. Crevoisier, G. B., Fabre, P., Corpart, J. M. & Leibler, L. Switchable tackiness and wettability of a liquid crystalline polymer. Science 285, 1246–1249 (1999).

    Article  Google Scholar 

  13. Jones, D. M., Smith, J. R., Huck, W. T. S. & Alexander, C. Variable adhesion of micropatterned thermoresponsive polymer brushes: AFM investigations of poly (N-isopropylacrylamide) brushes prepared by surface-initiated polymerizations. Adv. Mater. 14, 1130–1134 (2002).

    Article  CAS  Google Scholar 

  14. Lin, P. C., Vajpayee, S., Jagota, A., Hui, C. Y. & Yang, S. Mechanically tunable dry adhesive from wrinkled elastomers. Soft Matter 4, 1830–1835 (2008).

    Article  CAS  Google Scholar 

  15. Kang, Y., Walish, J. J., Gorishnyy, T. & Thomas, E. L. Broad-wavelength-range chemically tunable block-copolymer photonic gels. Nature Mater. 6, 957–960 (2007).

    Article  CAS  Google Scholar 

  16. Hu, Z. B., Chen, Y. Y., Wang, C. J., Zheng, Y. D. & Li, Y. Polymer gels with engineered environmentally responsive surface patterns. Nature 393, 149–152 (1998).

    Article  CAS  Google Scholar 

  17. Jiang, X. Y., Ferrigno, R., Mrksich, M. & Whitesides, G. M. Electrochemical desorption of self-assembled monolayers noninvasively releases patterned cells from geometrical confinements. J. Am. Chem. Soc. 125, 2366–2367 (2003).

    Article  CAS  Google Scholar 

  18. Yeo, W. S., Yousaf, M. N. & Mrksich, M. Dynamic interfaces between cells and surfaces: Electroactive substrates that sequentially release and attach cells. J. Am. Chem. Soc. 125, 14994–14995 (2003).

    Article  CAS  Google Scholar 

  19. Akiyama, Y., Kikuchi, A., Yamato, M. & Okano, T. Ultrathin poly(N-isopropylacrylamide) grafted layer on polystyrene surfaces for cell adhesion/detachment control. Langmuir 20, 5506–5511 (2004).

    Article  CAS  Google Scholar 

  20. Zhu, X. Y. et al. Fabrication of reconfigurable protein matrices by cracking. Nature Mater. 4, 403–406 (2005).

    Article  CAS  Google Scholar 

  21. Frey, W., Meyer, D. E. & Chilkoti, A. Dynamic addressing of a surface pattern by a stimuli-responsive fusion protein. Adv. Mater. 15, 248–251 (2003).

    Article  CAS  Google Scholar 

  22. Sikes, H. D. et al. Using polymeric materials to generate an amplified response to molecular recognition events. Nature Mater. 7, 52–56 (2008).

    Article  CAS  Google Scholar 

  23. Tojo, E., Nagao, K., Miura, T. & Nagamoto, S. in Photographic Gelatin (ed. Cox, R. J.) 49–61 (Academic, 1972).

    Google Scholar 

  24. Tanaka, T. et al. Mechanical instability of gels at the phase-transition. Nature 325, 796–798 (1987).

    Article  CAS  Google Scholar 

  25. Trujillo, V., Kim, J. & Hayward, R. C. Creasing instability of surface-attached hydrogels. Soft Matter 4, 564–569 (2008).

    Article  CAS  Google Scholar 

  26. Hirotsu, S., Hirokawa, Y. & Tanaka, T. Volume-phase transitions of ionized N-isopropylacrylamide gels. J. Chem. Phys. 87, 1392–1395 (1987).

    Article  CAS  Google Scholar 

  27. Li, C. F., Hu, Z. B. & Li, Y. Temperature and time dependencies of surface patterns in constrained ionic N-isopropylacrylamide gels. J. Chem. Phys. 100, 4645–4652 (1994).

    Article  CAS  Google Scholar 

  28. Bysell, H. & Malmsten, M. Visualizing the interaction between poly-L-lysine and poly(acrylic acid) microgels using microscopy techniques: Effect of electrostatics and peptide size. Langmuir 22, 5476–5484 (2006).

    Article  CAS  Google Scholar 

  29. Hermanson, G. T. Bioconjugate Techniques 1st edn (Academic, 1996).

    Google Scholar 

  30. Kenausis, G. L. et al. Poly(L-lysine)-g-poly(ethylene glycol) layers on metal oxide surfaces: Attachment mechanism and effects of polymer architecture on resistance to protein adsorption. J. Phys. Chem. B 104, 3298–3309 (2000).

    Article  CAS  Google Scholar 

  31. VandeVondele, S., Voros, J. & Hubbell, J. A. RGD-grafted poly-L-lysine-graft-(polyethylene glycol) copolymers block non-specific protein adsorption while promoting cell adhesion. Biotechnol. Bioeng. 82, 784–790 (2003).

    Article  CAS  Google Scholar 

  32. Hong, W., Liu, Z. & Suo, Z. Inhomogeneous swelling of a gel in equilibrium with a solvent and mechanical load. Int. J. Solids Struct. 204, 3282–3289 (2009).

    Article  Google Scholar 

  33. Panteghini, M., Bonora, R. & Pagani, F. Measurement of pancreatic lipase activity in serum by a kinetic colorimetric assay using a new chromogenic substrate. Ann. Clin. Biochem. 38, 365–370 (2001).

    Article  CAS  Google Scholar 

  34. Kamenjicki, M., Lednev, I. K., Mikhonin, A., Kesavamoorthy, R. & Asher, S. A. Photochemically controlled photonic crystals. Adv. Funct. Mater. 13, 774–780 (2003).

    Article  CAS  Google Scholar 

  35. Miyata, T., Asami, N. & Uragami, T. A reversibly antigen-responsive hydrogel. Nature 399, 766–769 (1999).

    Article  CAS  Google Scholar 

  36. Zhao, X. M., Xia, Y. N. & Whitesides, G. M. Soft lithographic methods for nano-fabrication. J. Mater. Chem. 7, 1069–1074 (1997).

    Article  CAS  Google Scholar 

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Acknowledgements

We are grateful to Z. Suo and X. Zhao for helpful discussions and for providing the user-defined Abaqus subroutines used to model swelling of hyperelastic gels, and to P. Wadsworth and C. Fagerstrom for providing cells and assisting with cell culture experiments. This work was primarily financially supported by the National Science Foundation through grant DMR-0747756 with further support provided by a 3M Nontenured Faculty Grant, and made use of facilities supported by the NSF MRSEC at UMass (DMR-0820506) and NSF grant BBS-8714235. J.Y. is partially supported by the Korean Research Foundation (KRF-2008-357-D00079).

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R.C.H. and J.K. designed the research project and experiments. J.K. carried out the bulk of experiments and simulations; J.Y. characterized temperature-dependent swelling behaviours of the gel networks. R.C.H. and J.K. primarily wrote the paper with input and comments from J.Y.

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Correspondence to Ryan C. Hayward.

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The authors declare no competing financial interests.

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Kim, J., Yoon, J. & Hayward, R. Dynamic display of biomolecular patterns through an elastic creasing instability of stimuli-responsive hydrogels. Nature Mater 9, 159–164 (2010). https://doi.org/10.1038/nmat2606

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