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Coupling synthetic biology and programmable materials to construct complex tissue ecosystems

  • Synthetic Biology Prospective
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Abstract

Synthetic biology combines engineering and biology to produce artificial systems with programmable features. Specifically, engineered microenvironments have advanced immensely over the past few decades, owing in part to the merging of materials with biologic mimetic structures. In this review, the authors adapt a traditional definition of community ecology to describe “cellular ecology,” or the study of the distribution of cell populations and interactions within their microenvironment. The authors discuss two exemplar hydrogel platforms: (1) self-assembling peptide hydrogels and (2) poly(ethylene) glycol hydrogels and describe future opportunities for merging smart material design and synthetic biology within the scope of multicellular platforms.

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References

  1. S.A. Benner and A.M. Sismour: Synthetic biology. Nat. Rev. Genet. 6, 533–543 (2005).

    Article  CAS  Google Scholar 

  2. M.A.J. Roberts, R.M. Cranenburgh, M.P. Stevens, and P.C.F. Oyston: Synthetic biology: biology by design. Microbiol. Read. Engl. 159, 1219–1220 (2013).

    Article  CAS  Google Scholar 

  3. G.L. Rosano and E.A. Ceccarelli: Recombinant protein expression in Escherichia coli: advances and challenges. Front. Microbiol. 5, 172 (2014).

    Article  Google Scholar 

  4. J. Yu, M.A. Vodyanik, K. Smuga-Otto, J. Antosiewicz-Bourget, J.L. Frane, S. Tian, J. Nie, G.A. Jonsdottir, V. Ruotti, R. Stewart, I.I. Slukvin, and J.A. Thomson: Induced pluripotent stem cell lines derived from human somatic cells. Science 318, 1917–1920 (2007).

    Article  CAS  Google Scholar 

  5. P.D. Hsu, E.S. Lander, and F. Zhang: Development and applications of CRISPR-Cas9 for genome engineering. Cell 157, 1262–1278 (2014).

    Article  CAS  Google Scholar 

  6. S.K. Sia, B.M. Gillette, and G.J. Yang: Synthetic tissue biology: tissue engineering meets synthetic biology. Birth Defects Res. Part C Embryo Today Rev. 81, 354–361 (2007).

    Article  CAS  Google Scholar 

  7. E. Bianconi, A. Piovesan, F. Facchin, A. Beraudi, R. Casadei, F. Frabetti, L. Vitale, M.C. Pelleri, S. Tassani, F. Piva, S. Perez-Amodio, P. Strippoli, and S. Canaider: An estimation of the number of cells in the human body. Ann. Hum. Biol. 40, 463–471 (2013).

    Article  Google Scholar 

  8. K.K. Bokka, E.C. Jesudason, O.A. Lozoya, F. Guilak, D. Warburton, and S.R. Lubkin: Morphogenetic implications of peristalsis-driven fluid flow in the embryonic lung. PLoS ONE 10, e0132015 (2015).

    Article  Google Scholar 

  9. U.Z. George, K.K. Bokka, D. Warburton, and S.R. Lubkin: Quantifying stretch and secretion in the embryonic lung: implications for morphogenesis. Mech. Dev. 138, 356–363 (2015).

    Article  CAS  Google Scholar 

  10. H.Y. Kim, M.-F. Pang, V.D. Varner, L. Kojima, E. Miller, D.C. Radisky, and C.M. Nelson: Localized smooth muscle differentiation is essential for epithelial bifurcation during branching morphogenesis of the mammalian lung. Dev. Cell 34, 719–726 (2015).

    Article  CAS  Google Scholar 

  11. A. Patel: The primary cilium calcium channels and their role in flow sensing. Pflüg. Arch.––Eur. J. Physiol. 467, 157–165 (2015).

    CAS  Google Scholar 

  12. R. Kalluri: The biology and function of fibroblasts in cancer. Nat. Rev. Cancer 16, 582–598 (2016).

    Article  CAS  Google Scholar 

  13. E. Boghaert, J.P. Gleghorn, K. Lee, N. Gjorevski, D.C. Radisky, and C.M. Nelson: Host epithelial geometry regulates breast cancer cell invasiveness. Proc. Natl. Acad. Sci. 109, 19632–19637 (2012).

    Article  CAS  Google Scholar 

  14. D. Ameis, N. Khoshgoo, and R. Keijzer: Abnormal lung development in congenital diaphragmatic hernia. Semin. Pediatr. Surg. 26, 123–128 (2017).

    Article  Google Scholar 

  15. W. Zhang, X. Yu, Y. Li, Z. Su, K.D. Jandt, and G. Wei: Protein-mimetic peptide nanofibers: motif design, self-assembly synthesis, and sequencespecific biomedical applications. Prog. Polym. Sci. 80, 94–124 (2018).

    Article  CAS  Google Scholar 

  16. I. Coin, M. Beyermann, and M. Bienert: Solid-phase peptide synthesis: from standard procedures to the synthesis of difficult sequences. Nat. Protoc. 2, 3247 (2007).

    Article  CAS  Google Scholar 

  17. J. Tsukamoto, K. Naruse, Y. Nagai, S. Kan, N. Nakamura, M. Hata, M. Omi, T. Hayashi, T. Kawai, and T. Matsubara: Efficacy of a self-assembling peptide hydrogel, SPG-178-Gel, for bone regeneration and threedimensional osteogenic induction of dental pulp stem cells. Tissue Eng. Part A 23, 1394–1402 (2017).

    Article  CAS  Google Scholar 

  18. H. Tsutsumi, M. Kawamura, and H. Mihara: Osteoblastic differentiation on hydrogels fabricated from Ca 2+-responsive self-assembling peptides functionalized with bioactive peptides. Bioorg. Med. Chem. 26, 3126–3132 (2018).

    Article  CAS  Google Scholar 

  19. R. Li, J. Xu, D.S.H. Wong, J. Li, P. Zhao, and L. Bian: Self-assembled N-cadherin mimetic peptide hydrogels promote the chondrogenesis of mesenchymal stem cells through inhibition of canonical Wnt/β-catenin signaling. Biomaterials 145, 33–43 (2017).

    Article  CAS  Google Scholar 

  20. X. Liu, X. Wang, X. Wang, H. Ren, J. He, L. Qiao, and F.-Z. Cui: Functionalized self-assembling peptide nanofiber hydrogels mimic stem cell niche to control human adipose stem cell behavior in vitro. Acta Biomater. 9, 6798–6805 (2013).

    Article  CAS  Google Scholar 

  21. S. Chen, A. Zhou, B. He, W. Zhao, X. Chen, and D. Jiang: Designer D-form self-assembling peptide scaffolds promote the proliferation and migration of rat bone marrow-derived mesenchymal stem cells. Int. J. Mol. Med. 40, 679–688 (2017).

    Article  CAS  Google Scholar 

  22. J. Shi, X. Du, D. Yuan, J. Zhou, N. Zhou, Y. Huang, and B. Xu: D-amino acids modulate the cellular response of enzymatic-instructed supramolecular nanofibers of small peptides. Biomacromolecules 15, 3559–3568 (2014).

    Article  CAS  Google Scholar 

  23. J. Zhou, X. Du, J. Wang, N. Yamagata, and B. Xu: Enzyme-instructed selfassembly of peptides containing phosphoserine to form supramolecular hydrogels as potential soft biomaterials. Front. Chem. Sci. Eng. 11, 509–515 (2017).

    Article  CAS  Google Scholar 

  24. N.J. Hogrebe, J.W. Reinhardt, N.K. Tram, A.C. Debski, G. Agarwal, M.A. Reilly, and K.J. Gooch: Independent control of matrix adhesiveness and stiffness within a 3D self-assembling peptide hydrogel. Acta Biomater. 70, 110–119 (2018).

    Article  CAS  Google Scholar 

  25. N.J. Hogrebe and K.J. Gooch: Direct influence of culture dimensionality on human mesenchymal stem cell differentiation at various matrix stiffnesses using a fibrous self-assembling peptide hydrogel: effect of culture dimensionality on HMSC differentiation. J. Biomed. Mater. Res. A 104, 2356–2368 (2016).

    Article  CAS  Google Scholar 

  26. S. Tavakol, S.M.M. Mousavi, B. Tavakol, E. Hoveizi, J. Ai, and S.M.R. Sorkhabadi: Erratum to: mechano-transduction signals derived from selfassembling peptide nanofibers containing long motif of laminin influence neurogenesis in in-vitro and in-vivo. Mol. Neurobiol. 54, 2497–2497 (2017).

    Article  CAS  Google Scholar 

  27. S. Tavakol, R. Saber, E. Hoveizi, B. Tavakol, H. Aligholi, J. Ai, and S.M. Rezayat: Self-assembling peptide nanofiber containing long motif of laminin induces neural differentiation, tubulin polymerization, and neurogenesis: in vitro, ex vivo, and in vivo studies. Mol. Neurobiol. 53, 5288–5299 (2016).

    Article  CAS  Google Scholar 

  28. C. Lu, Y. Wang, S. Yang, C. Wang, X. Sun, J. Lu, H. Yin, W. Jiang, H. Meng, F. Rao, X. Wang, and J. Peng: Bioactive self-assembling peptide hydrogels functionalized with brain-derived neurotrophic factor and nerve growth factor mimicking peptides synergistically promote peripheral nerve regeneration. ACS Biomater. Sci. Eng. 4, 2994–3005 (2018).

    Article  CAS  Google Scholar 

  29. S. Maude, E. Ingham, and A. Aggeli: Biomimetic self-assembling peptides as scaffolds for soft tissue engineering. Nanomed. 8, 823–847 (2013).

    Article  CAS  Google Scholar 

  30. T.-Y. Cheng, H.-C. Wu, M.-Y. Huang, W.-H. Chang, C.-H. Lee, and T.-W. Wang: Self-assembling functionalized nanopeptides for immediate hemostasis and accelerative liver tissue regeneration. Nanoscale 5, 2734 (2013).

    Article  CAS  Google Scholar 

  31. A. Saini, K. Serrano, K. Koss, and L.D. Unsworth: Evaluation of the hemocompatibility and rapid hemostasis of (RADA) 4 peptide-based hydrogels. Acta Biomater. 31, 71–79 (2016).

    Article  CAS  Google Scholar 

  32. S. Yang, S. Wei, Y. Mao, H. Zheng, J. Feng, J. Cui, X. Xie, F. Chen, and H. Li: Novel hemostatic biomolecules based on elastin-like polypeptides and the self-assembling peptide RADA-16. BMC Biotechnol. 18, 12 (2018).

    Article  Google Scholar 

  33. A. Altunbas, S.J. Lee, S.A. Rajasekaran, J.P. Schneider, and D.J. Pochan: Encapsulation of curcumin in self-assembling peptide hydrogels as injectable drug delivery vehicles. Biomaterials 32, 5906–5914 (2011).

    Article  CAS  Google Scholar 

  34. F. Gelain, L.D. Unsworth, and S. Zhang: Slow and sustained release of active cytokines from self-assembling peptide scaffolds. J. Controlled Release 145, 231–239 (2010).

    Article  CAS  Google Scholar 

  35. R. Pugliese, A. Marchini, G.A.A. Saracino, R.N. Zuckermann, and F. Gelain: Cross-linked self-assembling peptide scaffolds. Nano Res. 11, 586–602 (2018).

    Article  CAS  Google Scholar 

  36. L.E. Jansen, N.P. Birch, J.D. Schiffman, A.J. Crosby, and S.R. Peyton: Mechanics of intact bone marrow. J. Mech. Behav. Biomed. Mater. 50, 299–307 (2015).

    Article  Google Scholar 

  37. Z. Zhang, G. Wu, Y. Cao, C. Liu, Y. Jin, Y. Wang, L. Yang, J. Guo, and L. Zhu: Self-assembling peptide and nHA/CTS composite scaffolds promote bone regeneration through increasing seed cell adhesion. Mater. Sci. Eng. C 93, 445–454 (2018).

    Article  CAS  Google Scholar 

  38. T. Hou, Z. Li, F. Luo, Z. Xie, X. Wu, J. Xing, S. Dong, and J. Xu: A composite demineralized bone matrix––self assembling peptide scaffold for enhancing cell and growth factor activity in bone marrow. Biomaterials 35, 5689–5699 (2014).

    Article  CAS  Google Scholar 

  39. K. Li, Z. Zhang, D. Li, W. Zhang, X. Yu, W. Liu, C. Gong, G. Wei, and Z. Su: Biomimetic ultralight, highly porous, shape-adjustable, and biocompatible 3D graphene minerals via incorporation of self-assembled peptide nanosheets. Adv. Funct. Mater. 28, 1801056 (2018).

    Article  Google Scholar 

  40. G. Wu, M. Pan, X. Wang, J. Wen, S. Cao, Z. Li, Y. Li, C. Qian, Z. Liu, W. Wu, L. Zhu, and J. Guo: Osteogenesis of peripheral blood mesenchymal stem cells in self assembling peptide nanofiber for healing critical size calvarial bony defect. Sci. Rep. 5, 16681 (2015).

    Article  CAS  Google Scholar 

  41. N.R. Schiele, J.E. Marturano, and C.K. Kuo: Mechanical factors in embryonic tendon development: potential cues for stem cell tenogenesis. Curr. Opin. Biotechnol. 24, 834–840 (2013).

    Article  CAS  Google Scholar 

  42. N. Annabi, J.W. Nichol, X. Zhong, C. Ji, S. Koshy, A. Khademhosseini, and F. Dehghani: Controlling the porosity and microarchitecture of hydrogels for tissue engineering. Tissue Eng. Part B Rev. 16, 371–383 (2010).

    Article  CAS  Google Scholar 

  43. S.R. Peyton, C.B. Raub, V.P. Keschrumrus, and A.J. Putnam: The use of poly(ethylene glycol) hydrogels to investigate the impact of ECM chemistry and mechanics on smooth muscle cells. Biomaterials 27, 4881–4893 (2006).

    Article  CAS  Google Scholar 

  44. N. Huettner, T.R. Dargaville, and A. Forget: Discovering cell-adhesion peptides in tissue engineering: beyond RGD. Trends Biotechnol. 36, 372–383 (2018).

    Article  CAS  Google Scholar 

  45. R. Visser, G.A. Rico-Llanos, H. Pulkkinen, and J. Becerra: Peptides for bone tissue engineering. J. Controlled Release 244, 122–135 (2016).

    Article  CAS  Google Scholar 

  46. A. Naba, K.R. Clauser, S. Hoersch, H. Liu, S.A. Carr, and R.O. Hynes: The matrisome: in silico definition and in vivo characterization by proteomics of normal and tumor extracellular matrices. Mol. Cell. Proteomics 11, M111.014647 (2012).

    Article  Google Scholar 

  47. L. Jansen, T. McCarthy, M. Lee, and S. Peyton: A synthetic, threedimensional bone marrow hydrogel. University of Massachusetts Medical School Faculty Publications. 1528 (2018).

    Google Scholar 

  48. F. Anjum, P.S. Lienemann, S. Metzger, J. Biernaskie, M.S. Kallos, and M. Ehrbar: Enzyme responsive GAG-based natural-synthetic hybrid hydrogel for tunable growth factor delivery and stem cell differentiation. Biomaterials 87, 104–117 (2016).

    Article  CAS  Google Scholar 

  49. H. Lv, L. Li, M. Sun, Y. Zhang, L. Chen, Y. Rong, and Y. Li: Mechanism of regulation of stem cell differentiation by matrix stiffness. Stem Cell Res. Ther. 6, 103 (2015).

    Article  Google Scholar 

  50. M.S. Rehmann, J.I. Luna, E. Maverakis, and A.M. Kloxin: Tuning microenvironment modulus and biochemical composition promotes human mesenchymal stem cell tenogenic differentiation: human mesenchymal stem cell tenogenic differentiation. J. Biomed. Mater. Res. A 104, 1162–1174 (2016).

    Article  CAS  Google Scholar 

  51. U. Blache, S. Metzger, Q. Vallmajo-Martin, I. Martin, V. Djonov, and M. Ehrbar: Dual role of mesenchymal stem cells allows for microvascularized bone tissue-like environments in PEG hydrogels. Adv. Healthc. Mater. 5, 489–498 (2016).

    Article  CAS  Google Scholar 

  52. S. Mahadevaiah, K.G. Robinson, P.M. Kharkar, K.L. Kiick, and R.E. Akins: Decreasing matrix modulus of PEG hydrogels induces a vascular phenotype in human cord blood stem cells. Biomaterials 62, 24–34 (2015).

    Article  CAS  Google Scholar 

  53. E.B. Peters, N. Christoforou, K.W. Leong, G.A. Truskey, and J.L. West: Poly(ethylene glycol) hydrogel scaffolds containing cell-adhesive and protease-sensitive peptides support microvessel formation by endothelial progenitor cells. Cell. Mol. Bioeng. 9, 38–54 (2016).

    Article  CAS  Google Scholar 

  54. K.M. Mabry, R.L. Lawrence, and K.S. Anseth: Dynamic stiffening of poly (ethylene glycol)-based hydrogels to direct valvular interstitial cell phenotype in a three-dimensional environment. Biomaterials 49, 47–56 (2015).

    Article  CAS  Google Scholar 

  55. S.P. Singh, M.P. Schwartz, J.Y. Lee, B.D. Fairbanks, and K.S. Anseth: A peptide functionalized poly(ethylene glycol) (PEG) hydrogel for investigating the influence of biochemical and biophysical matrix properties on tumor cell migration. Biomater. Sci. 2, 1024 (2014).

    Article  CAS  Google Scholar 

  56. P. Soman, J.A. Kelber, J.W. Lee, T.N. Wright, K.S. Vecchio, R.L. Klemke, and S. Chen: Cancer cell migration within 3D layer-by-layer microfabricated photocrosslinked PEG scaffolds with tunable stiffness. Biomaterials 33, 7064–7070 (2012).

    Article  CAS  Google Scholar 

  57. R. Sunyer, A.J. Jin, R. Nossal, and D.L. Sackett: Fabrication of hydrogels with steep stiffness gradients for studying cell mechanical response. PLoS ONE 7, e46107 (2012).

    Article  CAS  Google Scholar 

  58. C. Yang, F.W. DelRio, H. Ma, A.R. Killaars, L.P. Basta, K.A. Kyburz, and K.S. Anseth: Spatially patterned matrix elasticity directs stem cell fate. Proc. Natl. Acad. Sci. 113, E4439–E4445 (2016).

    Article  CAS  Google Scholar 

  59. M.S. Hahn, J.S. Miller, and J.L. West: Three-dimensional biochemical and biomechanical patterning of hydrogels for guiding cell behavior. Adv. Mater. 18, 2679–2684 (2006).

    Article  CAS  Google Scholar 

  60. S. Nemir, H.N. Hayenga, and J.L. West: PEGDA hydrogels with patterned elasticity: novel tools for the study of cell response to substrate rigidity. Biotechnol. Bioeng. 105, 636–644 (2010).

    Article  CAS  Google Scholar 

  61. Y. Ma, M. Lin, G. Huang, Y. Li, S. Wang, G. Bai, T.J. Lu, and F. Xu: 3D spatiotemporal mechanical microenvironment: a hydrogel-based platform for guiding stem cell fate. Adv. Mater. 30, 1705911 (2018).

    Article  Google Scholar 

  62. A.M. Kloxin, C.J. Kloxin, C.N. Bowman, and K.S. Anseth: Mechanical properties of cellularly responsive hydrogels and their experimental determination. Adv. Mater. 22, 3484–3494 (2010).

    Article  CAS  Google Scholar 

  63. A.M. Kloxin, M.W. Tibbitt, A.M. Kasko, J.A. Fairbairn, and K.S. Anseth: Tunable hydrogels for external manipulation of cellular microenvironments through controlled photodegradation. Adv. Mater. 22, 61–66 (2010).

    Article  CAS  Google Scholar 

  64. E.M. Sletten and C.R. Bertozzi: Bioorthogonal chemistry: fishing for selectivity in a sea of functionality. Angew. Chem. Int. Ed. 48, 6974–6998 (2009).

    Article  CAS  Google Scholar 

  65. X. Wu, W. Huang, W.-H. Wu, B. Xue, D. Xiang, Y. Li, M. Qin, F. Sun, W. Wang, W.-B. Zhang, and Y. Cao: Reversible hydrogels with tunable mechanical properties for optically controlling cell migration. Nano Res. 11, 5556–5565 (2018).

    Article  CAS  Google Scholar 

  66. S.C.P. Norris, P. Tseng, and A.M. Kasko: Direct gradient photolithography of photodegradable hydrogels with patterned stiffness control with submicrometer resolution. ACS Biomater. Sci. Eng. 2, 1309–1318 (2016).

    Article  CAS  Google Scholar 

  67. A. Desmouliere, I.A. Darby, B. Laverdet, and F. Bonté: Fibroblasts and myofibroblasts in wound healing. Clin. Cosmet. Investig. Dermatol. 7, 301 (2014).

    Article  Google Scholar 

  68. A.J. Hughes, H. Miyazaki, M.C. Coyle, J. Zhang, M.T. Laurie, D. Chu, Z. Vavrušová, R.A. Schneider, O.D. Klein, and Z.J. Gartner: Engineered tissue folding by mechanical compaction of the mesenchyme. Dev. Cell 44, 165–178.e6 (2018).

    Article  CAS  Google Scholar 

  69. T.K. Merceron, M. Burt, Y.-J. Seol, H.-W. Kang, S.J. Lee, J.J. Yoo, and A. Atala: A 3D bioprinted complex structure for engineering the muscle–tendon unit. Biofabrication. 7, 035003 (2015).

    Article  Google Scholar 

  70. A. Skardal, M. Devarasetty, H.-W. Kang, I. Mead, C. Bishop, T. Shupe, S.J. Lee, J. Jackson, J. Yoo, S. Soker, and A. Atala: A hydrogel bioink toolkit for mimicking native tissue biochemical and mechanical properties in bioprinted tissue constructs. Acta Biomater. 25, 24–34 (2015).

    Article  CAS  Google Scholar 

  71. D.B. Kolesky, R.L. Truby, A.S. Gladman, T.A. Busbee, K.A. Homan, and J.A. Lewis: 3D bioprinting of vascularized, heterogeneous cell-laden tissue constructs. Adv. Mater. 26, 3124–3130 (2014).

    Article  CAS  Google Scholar 

  72. X. Ma, X. Qu, W. Zhu, Y.-S. Li, S. Yuan, H. Zhang, J. Liu, P. Wang, C.S.E. Lai, F. Zanella, G.-S. Feng, F. Sheikh, S. Chien, and S. Chen: Deterministically patterned biomimetic human iPSC-derived hepatic model via rapid 3D bioprinting. Proc. Natl. Acad. Sci. 113, 2206–2211 (2016).

    Article  CAS  Google Scholar 

  73. P. Soman, P.H. Chung, A.P. Zhang, and S. Chen: Digital microfabrication of user-defined 3D microstructures in cell-laden hydrogels: 3D microstructures in cell-laden hydrogels. Biotechnol. Bioeng. 110, 3038–3047 (2013).

    Article  CAS  Google Scholar 

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

    Article  CAS  Google Scholar 

  75. J. Guan, H. He, D.J. Hansford, and L.J. Lee: Self-Folding of threedimensional hydrogel microstructures. J. Phys. Chem. B 109, 23134–23137 (2005).

    Article  CAS  Google Scholar 

  76. C. Yoon, R. Xiao, J. Park, J. Cha, T.D. Nguyen, and D.H. Gracias: Functional stimuli responsive hydrogel devices by self-folding. Smart Mater. Struct. 23, 094008 (2014).

    Article  CAS  Google Scholar 

  77. S. Naficy, R. Gately, R. Gorkin, H. Xin, and G.M. Spinks: 4D printing of reversible shape morphing hydrogel structures. Macromol. Mater. Eng. 302, 1600212 (2017).

    Article  Google Scholar 

  78. H.R. Kwag, J.V. Serbo, P. Korangath, S. Sukumar, L.H. Romer, and D.H. Gracias: A self-folding hydrogel in vitro model for ductal carcinoma. Tissue Eng. Part C Methods 22, 398–407 (2016).

    Article  CAS  Google Scholar 

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

    Article  CAS  Google Scholar 

  80. N. Bassik, G.M. Stern, M. Jamal, and D.H. Gracias: Patterning thin film mechanical properties to drive assembly of complex 3D structures. Adv. Mater. 20, 4760–4764 (2008).

    Article  CAS  Google Scholar 

  81. J. Bae, J.-H. Na, C.D. Santangelo, and R.C. Hayward: Edge-defined metric buckling of temperature-responsive hydrogel ribbons and rings. Polymer 55, 5908–5914 (2014).

    Article  CAS  Google Scholar 

  82. T. Li, J. Wang, L. Zhang, J. Yang, M. Yang, D. Zhu, X. Zhou, S. Handschuh-Wang, Y. Liu, and X. Zhou: “Freezing”, morphing, and folding of stretchy tough hydrogels. J. Mater. Chem. B 5, 5726–5732 (2017).

    Article  CAS  Google Scholar 

  83. S.-J. Jeon, A.W. Hauser, and R.C. Hayward: Shape-morphing materials from stimuli-responsive hydrogel hybrids. Acc. Chem. Res. 50, 161–169 (2017).

    Article  CAS  Google Scholar 

  84. S.-J. Park, M. Gazzola, K.S. Park, S. Park, V. Di Santo, E.L. Blevins, J.U. Lind, P.H. Campbell, S. Dauth, A.K. Capulli, F.S. Pasqualini, S. Ahn, A. Cho, H. Yuan, B.M. Maoz, R. Vijaykumar, J.-W. Choi, K. Deisseroth, G.V. Lauder, L. Mahadevan, and K.K. Parker: Phototactic guidance of a tissue-engineered soft-robotic ray. Science 353, 158–162 (2016).

    Article  CAS  Google Scholar 

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Acknowledgments

The authors would like to thank Dr. Rahul Chib for thoughtful discussions and comments. This work was supported in part by grants from the National Institutes of Health (R01HL133163, R21ES027962, T32GM008550 to A.M.D.), the National Science Foundation (1537256), the Burroughs Wellcome Fund (1017521), and the March of Dimes Basil O’Connor Award (5-FY16-33 to J.P.G).

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Correspondence to Jason P. Gleghorn.

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Millar-Haskell, C.S., Dang, A.M. & Gleghorn, J.P. Coupling synthetic biology and programmable materials to construct complex tissue ecosystems. MRS Communications 9, 421–432 (2019). https://doi.org/10.1557/mrc.2019.69

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