The design of reversible hydrogels to capture extracellular matrix dynamics

Nature Reviews Materials

Volumn 1, Issue 2, 2016, Pages

  Rosales, Adrianne M ^a   Anseth, Kristi S ^a,b  

^a UCB 450   (United States)

^b UNIVERSITY OF COLORADO   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

EID: 85019161196     PISSN: None     EISSN: 20588437     Source Type: Journal    
DOI: 10.1038/natrevmats.2015.12     Document Type: Review

References (176)

1. Nelson, C. M. & Bissell, M. J. Of extracellular matrix, scaffolds, and signaling: tissue architecture regulates development, homeostasis, and cancer. Annu. Rev. Cell Dev. Biol. 22, 287-309 (2006).
2. Midwood, K. S., Williams, L. V. & Schwarzbauer, J. E. Tissue repair and the dynamics of the extracellular matrix. Int. J. Biochem. Cell Biol. 36, 1031-1037 (2004).
3. Vlodavsky, I. et al. Endothelial cell-derived basic fibroblast growth factor: synthesis and deposition into subendothelial extracellular matrix. Proc. Natl Acad. Sci. USA 84, 2292-2296 (1987).
4. Wipff, P.-J., Rifkin, D. B., Meister, J.J. & Hinz, B. Myofibroblast contraction activates latent TGF-β1 from the extracellular matrix. J. Cell Biol. 179, 1311-1323 (2007).
5. Bissell, M. J., Hall, H. G. & Parry, G. How does the extracellular matrix direct gene expression? J. Theor. Biol. 99, 31-68 (1982).
6. Blau, H. et al. Plasticity of the differentiated state. Science 230, 758-766 (1985).
7. Slaughter, B. V., Khurshid, S. S., Fisher, O. Z., Khademhosseini, A. & Peppas, N. A. Hydrogels in regenerative medicine. Adv. Mater. 21, 3307-3329 (2009).
8. Place, E. S., Evans, N. D. & Stevens, M. M. Complexity in biomaterials for tissue engineering. Nat. Mater. 8, 457-470 (2009).
9. Fisher, O. Z., Khademhosseini, A., Langer, R. & Peppas, N. A. Bioinspired materials for controlling stem cell fate. Acc. Chem. Res. 43, 419-428 (2010).
10. Burdick, J. A. & Murphy, W. L. Moving from static to dynamic complexity in hydrogel design. Nat. Commun. 3, 1269 (2012).
11. Hartgerink, J. D., Beniash, E. & Stupp, S. I. Self-assembly and mineralization of peptide-amphiphile nanofibers. Science 294, 1684-1688 (2001).
12. Nowak, A. P. et al. Rapidly recovering hydrogel scaffolds from self-assembling diblock copolypeptide amphiphiles. Nature 417, 424-428 (2002).
13. Peppas, N. A., Hilt, J. Z., Khademhosseini, A. & Langer, R. Hydrogels in biology and medicine: from molecular principles to bionanotechnology. Adv. Mater. 18, 1345-1360 (2006).
14. Buwalda, S. J. et al. Hydrogels in a historical perspective: from simple networks to smart materials. J. Control. Release 190, 254-273 (2014).
15. Engler, A. J., Sen, S., Sweeney, H. L. & Discher, D. E. Matrix elasticity directs stem cell lineage specification. Cell 126, 677-689 (2006).
16. Wang, Y.-L. & Pelham, R. J. Jr in Methods in Enzymology (ed. Richard, B. V.) 489-496 (Academic Press, 1998).
17. Pelham, R. J. Jr & Wang, Y.-l. Cell locomotion and focal adhesions are regulated by substrate flexibility. Proc. Natl Acad. Sci. USA 94, 13661-13665 (1997).
18. Dvir, T., Timko, B. P., Kohane, D. S. & Langer, R. Nanotechnological strategies for engineering complex tissues. Nat. Nano 6, 13-22 (2011).
19. Roy, D., Cambre, J. N. & Sumerlin, B. S. Future perspectives and recent advances in stimuli-responsive materials. Prog. Polym. Sci. 35, 278-301 (2010).
20. Zhang, J. & Peppas, N. A. Synthesis and characterization of pH- and temperature-sensitive poly(methacrylic acid)/poly(N-isopropylacrylamide) interpenetrating polymeric networks. Macromolecules 33, 102-107 (2000).
21. Lowman, A. M., Morishita, M., Kajita, M., Nagai, T. & Peppas, N. A. Oral delivery of insulin using pH-responsive complexation gels. J. Pharm. Sci. 88, 933-937 (1999).
22. Hoffman, A. S. Applications of thermally reversible polymers and hydrogels in therapeutics and diagnostics. J. Control. Release 6, 297-305 (1987).
23. Cole, M. A., Voelcker, N. H., Thissen, H. & Griesser, H. J. Stimuli-responsive interfaces and systems for the control of protein-surface and cell-surface interactions. Biomaterials 30, 1827-1850 (2009).
24. 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).
25. Zrínyi, M. Intelligent polymer gels controlled by magnetic fields. Colloid Polym. Sci. 278, 98-103 (2000).
26. Kloxin, A. M., Kloxin, C. J., Bowman, C. N. & Anseth, K. S. Mechanical properties of cellularly responsive hydrogels and their experimental determination. Adv. Mater. 22, 3484-3494 (2010).
27. Miyata, T., Uragami, T. & Nakamae, K. Biomolecule-sensitive hydrogels. Adv. Drug Delivery Rev. 54, 79-98 (2002).
28. Miyata, T., Asami, N. & Uragami, T. A reversibly antigen-responsive hydrogel. Nature 399, 766-769 (1999).
29. Miyata, T., Jikihara, A., Nakamae, K. & Hoffman, A. S. Preparation of reversibly glucose-responsive hydrogels by covalent immobilization of lectin in polymer networks having pendant glucose. J. Biomater. Sci. Polym. Ed. 15, 1085-1098 (2004).
30. Hassan, C. M., Doyle, F. J. & Peppas, N. A. Dynamic behavior of glucose-responsive poly(methacrylic acid-g-ethylene glycol) hydrogels. Macromolecules 30, 6166-6173 (1997).
31. Kost, J. & Langer, R. Responsive polymeric delivery systems. Adv. Drug Delivery Rev. 64 (Suppl.), 327-341 (2012).
32. Bryant, S. J. & Anseth, K. S. Controlling the spatial distribution of ECM components in degradable PEG hydrogels for tissue engineering cartilage. J. Biomed. Mater. Res. Part A 64A, 70-79 (2003).
33. Zustiak, S. P. & Leach, J. B. Hydrolytically degradable poly(ethylene glycol) hydrogel scaffolds with tunable degradation and mechanical properties. Biomacromolecules 11, 1348-1357 (2010).
34. Metters, A. T., Anseth, K. S. & Bowman, C. N. Fundamental studies of a novel, biodegradable PEG-b-PLA hydrogel. Polymer 41, 3993-4004 (2000).
35. Chung, C., Beecham, M., Mauck, R. L. & Burdick, J. A. The influence of degradation characteristics of hyaluronic acid hydrogels on in vitro neocartilage formation by mesenchymal stem cells. Biomaterials 30, 4287-4296 (2009).
36. Lutolf, M. P. et al. Synthetic matrix metalloproteinase-sensitive hydrogels for the conduction of tissue regeneration: engineering cell-invasion characteristics. Proc. Natl Acad. Sci. USA 100, 5413-5418 (2003).
37. Kloxin, A. M., Kasko, A. M., Salinas, C. N. & Anseth, K. S. Photodegradable hydrogels for dynamic tuning of physical and chemical properties. Science 324, 59-63 (2009).
38. Baker, B. M. & Chen, C. S. Deconstructing the third dimension - how 3D culture microenvironments alter cellular cues. J. Cell Sci. 125, 3015-3024 (2012).
39. Hynes, R. O. Extracellular matrix: not just pretty fibrils. Science 326, 1216-1219 (2009).
40. Martino, M. M. & Hubbell, J. A. The 12th-14th type III repeats of fibronectin function as a highly promiscuous growth factor-binding domain. FASEB J. 24, 4711-4721 (2010).
41. Droguett, R., Cabello-Verrugio, C., Riquelme, C. & Brandan, E. Extracellular proteoglycans modify TGF-β bio-availability attenuating its signaling during skeletal muscle differentiation. Matrix Biol. 25, 332-341 (2006).
42. Baneyx, G., Baugh, L. & Vogel, V. Fibronectin extension and unfolding within cell matrix fibrils controlled by cytoskeletal tension. Proc. Natl Acad. Sci. USA 99, 5139-5143 (2002).
43. Baldwin, A. D. & Kiick, K. L. Polysaccharide-modified synthetic polymeric biomaterials. Biopolymers 94, 128-140 (2010).
44. Lin, C.-C. & Anseth, K. S. Controlling affinity binding with peptide-functionalized poly(ethylene glycol) hydrogels. Adv. Funct. Mater. 19, 2325-2331 (2009).
45. McCall, J. D., Lin, C.C. & Anseth, K. S. Affinity peptides protect transforming growth factor β during encapsulation in poly(ethylene glycol) hydrogels. Biomacromolecules 12, 1051-1057 (2011).
46. Azagarsamy, M. A. & Anseth, K. S. Bioorthogonal click chemistry: an indispensable tool to create multifaceted cell culture scaffolds. ACS macro Lett. 2, 5-9 (2013).
47. Nimmo, C. M. & Shoichet, M. S. Regenerative biomaterials that "click": simple, aqueous-based protocols for hydrogel synthesis, surface immobilization, and 3D patterning. Bioconjugate Chem. 22, 2199-2209 (2011).
48. DeForest, C. A. & Anseth, K. S. Photoreversible patterning of biomolecules within click-based hydrogels. Angew. Chem. Int. Ed. Engl. 51, 1816-1819 (2012).
49. DeForest, C. A. & Tirrell, D. A. A photoreversible protein-patterning approach for guiding stem cell fate in three-dimensional gels. Nat. Mater. 14, 523-531 (2015).
50. Azagarsamy, M. A. & Anseth, K. S. Wavelength-controlled photocleavage for the orthogonal and sequential release of multiple proteins. Angew. Chem. Int. Ed. Engl. 52, 13803-13807 (2013).
51. Sur, S., Matson, J. B., Webber, M. J., Newcomb, C. J. & Stupp, S. I. Photodynamic control of bioactivity in a nanofiber matrix. ACS Nano 6, 10776-10785 (2012).
52. Lee, T. T. et al. Light-triggered in vivo activation of adhesive peptides regulates cell adhesion, inflammation and vascularization of biomaterials. Nat. Mater. 14, 352-360 (2015).
53. Petersen, S. et al. Phototriggering of cell adhesion by caged cyclic RGD peptides. Angew. Chem. Int. Ed. Engl. 47, 3192-3195 (2008).
54. Gandavarapu, N. R., Azagarsamy, M. A. & Anseth, K. S. Photo-click living strategy for controlled, reversible exchange of biochemical ligands. Adv. Mater. 26, 2521-2526 (2014).
55. Roberts, M. C., Hanson, M. C., Massey, A. P., Karren, E. A. & Kiser, P. F. Dynamically restructuring hydrogel networks formed with reversible covalent crosslinks. Adv. Mater. 19, 2503-2507 (2007).
56. Hahn, M. S., Miller, J. S. & West, J. L. Three-dimensional biochemical and biomechanical patterning of hydrogels for guiding cell behavior. Adv. Mater. 18, 2679-2684 (2006).
57. Soman, P., Chung, P. H., Zhang, A. P. & Chen, S. Digital microfabrication of user-defined 3D microstructures in cell-laden hydrogels. Biotechnol. Bioeng. 110, 3038-3047 (2013).
58. Wylie, R. G. et al. Spatially controlled simultaneous patterning of multiple growth factors in three-dimensional hydrogels. Nat. Mater. 10, 799-806 (2011).
59. Mosiewicz, K. A. et al. In situ cell manipulation through enzymatic hydrogel photopatterning. Nat. Mater. 12, 1072-1078 (2013).
60. Auernheimer, J., Dahmen, C., Hersel, U., Bausch, A. & Kessler, H. Photoswitched cell adhesion on surfaces with RGD peptides. J. Am. Chem. Soc. 127, 16107-16110 (2005).
61. Li, W. et al. Noninvasive and reversible cell adhesion and detachment via single-wavelength near-infrared laser mediated photoisomerization. J. Am. Chem. Soc. 137, 8199-8205 (2015).
62. Bryant, S. J., Nuttelman, C. R. & Anseth, K. S. Cytocompatibility of UV and visible light photoinitiating systems on cultured NIH/3T3 fibroblasts in vitro. J. Biomater. Sci. Polym. Ed. 11, 439-457 (2000).
63. Liu, B., Liu, Y., Riesberg, J. J. & Shen, W. Dynamic presentation of immobilized ligands regulated through biomolecular recognition. J. Am. Chem. Soc. 132, 13630-13632 (2010).
64. Zhang, Z., Chen, N., Li, S., Battig, M. R. & Wang, Y. Programmable hydrogels for controlled cell catch and release using hybridized aptamers and complementary sequences. J. Am. Chem. Soc. 134, 15716-15719 (2012).
65. Li, S., Gaddes, E. R., Chen, N. & Wang, Y. Molecular encryption and reconfiguration for remodeling of dynamic hydrogels. Angew. Chem. Int. Ed. Engl. 54, 5957-5961 (2015).
66. Zhang, Z., Li, S., Chen, N., Yang, C. & Wang, Y. Programmable display of DNA-protein chimeras for controlling cell-hydrogel interactions via reversible intermolecular hybridization. Biomacromolecules 14, 1174-1180 (2013).
67. Yang, J. et al. A near-infrared light-controlled system for reversible presentation of bioactive ligands using polypeptide-engineered functionalized gold nanorods. Chem. Commun. 51, 2569-2572 (2015).
68. Huebsch, N. et al. Harnessing traction-mediated manipulation of the cell/matrix interface to control stem-cell fate. Nat. Mater. 9, 518-526 (2010).
69. Boekhoven, J., Rubert Pérez, C. M., Sur, S., Worthy, A. & Stupp, S. I. Dynamic display of bioactivity through host-guest chemistry. Angew. Chem. Int. Ed. Engl. 52, 12077-12080 (2013).
70. Neirynck, P. et al. Carborane-β-cyclodextrin complexes as a supramolecular connector for bioactive surfaces. J. Mater. Chem. B 3, 539-545 (2015).
71. HH fragments. J. Am. Chem. Soc. 136, 12675-12681 (2014).
72. Brinkmann, J. et al. About supramolecular systems for dynamically probing cells. Chem. Soc. Rev. 43, 4449-4469 (2014).
73. Seo, J.H. et al. Inducing rapid cellular response on RGD-binding threaded macromolecular surfaces. J. Am. Chem. Soc. 135, 5513-5516 (2013).
74. Kakinoki, S. et al. Mobility of the Arg-Gly-Asp ligand on the outermost surface of biomaterials suppresses integrin-mediated mechanotransduction and subsequent cell functions. Acta Biomater. 13, 42-51 (2015).
75. Seo, J.-H., Kakinoki, S., Yamaoka, T. & Yui, N. Directing stem cell differentiation by changing the molecular mobility of supramolecular surfaces. Adv. Healthcare Mater. 4, 215-222 (2015).
76. Pierschbacher, M. D. & Ruoslahti, E. Cell attachment activity of fibronectin can be duplicated by small synthetic fragments of the molecule. Nature 309, 30-33 (1984).
77. Hynes, R. O. Integrins: versatility, modulation, and signaling in cell adhesion. Cell 69, 11-25 (1992).
78. Hautanen, A., Gailit, J., Mann, D. M. & Ruoslahti, E. Effects of modifications of the RGD sequence and its context on recognition by the fibronectin receptor. J. Biol. Chem. 264, 1437-1442 (1989).
79. Ruoslahti, E. RGD and other recognition sequences for integrins. Annu. Rev. Cell Dev. Biol. 12, 697-715 (1996).
80. Foley, T. L. & Burkart, M. D. Site-specific protein modification: advances and applications. Curr. Opin. Chem. Biol. 11, 12-19 (2007).
81. West, J. L. & Hubbell, J. A. Polymeric biomaterials with degradation sites for proteases involved in cell migration. Macromolecules 32, 241-244 (1999).
82. Kraehenbuehl, T. P. et al. Three-dimensional extracellular matrix-directed cardioprogenitor differentiation: systematic modulation of a synthetic cell-responsive PEG-hydrogel. Biomaterials 29, 2757-2766 (2008).
83. Kyburz, K. A. & Anseth, K. S. Three-dimensional hMSC motility within peptide-functionalized PEG-based hydrogels of varying adhesivity and crosslinking density. Acta Biomater. 9, 6381-6392 (2013).
84. Patterson, J. & Hubbell, J. A. Enhanced proteolytic degradation of molecularly engineered PEG hydrogels in response to MMP-1 and MMP-2. Biomaterials 31, 7836-7845 (2010).
85. Cameron, A. R., Frith, J. E. & Cooper-White, J. J. The influence of substrate creep on mesenchymal stem cell behaviour and phenotype. Biomaterials 32, 5979-5993 (2011).
86. Chaudhuri, O. et al. Substrate stress relaxation regulates cell spreading. Nat. Commun. 6, 6364 (2015).
87. Wang, H. & Heilshorn, S. C. Adaptable hydrogel networks with reversible linkages for tissue engineering. Adv. Mater. 27, 3717-3736 (2015).
88. Bowman, C. N. & Kloxin, C. J. Covalent adaptable networks: reversible bond structures incorporated in polymer networks. Angew. Chem. Int. Ed. Engl. 51, 4272-4274 (2012).
89. McKinnon, D. D., Domaille, D. W., Cha, J. N. & Anseth, K. S. Bis-aliphatic hydrazone-linked hydrogels form most rapidly at physiological pH: identifying the origin of hydrogel properties with small molecule kinetic studies. Chem. Mater. 26, 2382-2387 (2014).
90. McKinnon, D. D., Domaille, D. W., Cha, J. N. & Anseth, K. S. Hydrogels: biophysically defined and cytocompatible covalently adaptable networks as viscoelastic 3D cell culture systems. Adv. Mater. 26, 865-872 (2014).
91. McKinnon, D. D. et al. Measuring cellular forces using bis-aliphatic hydrazone crosslinked stress-relaxing hydrogels. Soft Matter 10, 9230-9236 (2014).
92. Yan, S. et al. Injectable in situ self-cross-linking hydrogels based on poly(L-glutamic acid) and alginate for cartilage tissue engineering. Biomacromolecules 15, 4495-4508 (2014).
93. Dahlmann, J. et al. Fully defined in situ cross-linkable alginate and hyaluronic acid hydrogels for myocardial tissue engineering. Biomaterials 34, 940-951 (2013).
94. Gurski, L. A., Jha, A. K., Zhang, C., Jia, X. & Farach-Carson, M. C. Hyaluronic acid-based hydrogels as 3D matrices for in vitro evaluation of chemotherapeutic drugs using poorly adherent prostate cancer cells. Biomaterials 30, 6076-6085 (2009).
95. Yang, B. et al. Facilely prepared inexpensive and biocompatible self-healing hydrogel: a new injectable cell therapy carrier. Polym. Chem. 3, 3235-3238 (2012).
96. Tan, H., Chu, C. R., Payne, K. A. & Marra, K. G. Injectable in situ forming biodegradable chitosan-hyaluronic acid based hydrogels for cartilage tissue engineering. Biomaterials 30, 2499-2506 (2009).
97. Weng, L., Romanov, A., Rooney, J. & Chen, W. Non-cytotoxic, in situ gelable hydrogels composed of N-carboxyethyl chitosan and oxidized dextran. Biomaterials 29, 3905-3913 (2008).
98. Zhao, X., Huebsch, N., Mooney, D. J. & Suo, Z. Stress-relaxation behavior in gels with ionic and covalent crosslinks. J. Appl. Phys. 107, 063509 (2010).
99. Rodell, C. B., Wade, R. J., Purcell, B. P., Dusaj, N. N. & Burdick, J. A. Selective proteolytic degradation of guest-host assembled, injectable hyaluronic acid hydrogels. ACS biomater. Sci. Eng. 1, 277-286 (2015).
100. Liao, X., Chen, G. & Jiang, M. Hydrogels locked by molecular recognition aiming at responsiveness and functionality. Polym. Chem. 4, 1733-1745 (2013).
101. Park, K. M. et al. In situ supramolecular assembly and modular modification of hyaluronic acid hydrogels for 3D cellular engineering. ACS Nano 6, 2960-2968 (2012).
102. Dankers, P. Y. W., Harmsen, M. C., Brouwer, L. A., Van Luyn, M. J. A. & Meijer, E. W. A modular and supramolecular approach to bioactive scaffolds for tissue engineering. Nat. Mater. 4, 568-574 (2005).
103. Wong Po Foo, C. T. S., Lee, J. S., Mulyasasmita, W., Parisi-Amon, A. & Heilshorn, S. C. Two-component protein-engineered physical hydrogels for cell encapsulation. Proc. Natl Acad. Sci. USA 106, 22067-22072 (2009).
104. Cai, L., Dewi, R. E. & Heilshorn, S. C. Injectable hydrogels with in situ double network formation enhance retention of transplanted stem cells. Adv. Funct. Mater. 25, 1344-1351 (2015).
105. Sathaye, S. et al. Engineering complementary hydrophobic interactions to control β-hairpin peptide self-assembly, network branching, and hydrogel properties. Biomacromolecules 15, 3891-3900 (2014).
106. Glassman, M. J., Chan, J. & Olsen, B. D. Reinforcement of shear thinning protein hydrogels by responsive block copolymer self-assembly. Adv. Funct. Mater. 23, 1182-1193 (2013).
107. Lee, K. Y. & Mooney, D. J. Alginate: properties and biomedical applications. Prog. Polym. Sci. 37, 106-126 (2012).
108. McBeath, R., Pirone, D. M., Nelson, C. M., Bhadriraju, K. & Chen, C. S. Cell shape, cytoskeletal tension, and RhoA regulate stem cell lineage commitment. Dev. Cell 6, 483-495 (2004).
109. Kilian, K. A., Bugarija, B., Lahn, B. T. & Mrksich, M. Geometric cues for directing the differentiation of mesenchymal stem cells. Proc. Natl Acad. Sci. USA 107, 4872-4877 (2010).
110. Ito, F. et al. Reversible hydrogel formation driven by protein-peptide-specific interaction and chondrocyte entrapment. Biomaterials 31, 58-66 (2010).
111. Lu, H. D., Charati, M. B., Kim, I. L. & Burdick, J. A. Injectable shear-thinning hydrogels engineered with a self-assembling dock-and-lock mechanism. Biomaterials 33, 2145-2153 (2012).
112. Shen, W., Kornfield, J. A. & Tirrell, D. A. Dynamic properties of artificial protein hydrogels assembled through aggregation of leucine zipper peptide domains. Macromolecules 40, 689-692 (2007).
113. Um, S. H. et al. Enzyme-catalysed assembly of DNA hydrogel. Nat. Mater. 5, 797-801 (2006).
114. Lampe, K. J., Antaris, A. L. & Heilshorn, S. C. Design of three-dimensional engineered protein hydrogels for tailored control of neurite growth. Acta Biomater. 9, 5590-5599 (2013).
115. Rodell, C. B., Kaminski, A. L. & Burdick, J. A. Rational design of network properties in guest-host assembled and shear-thinning hyaluronic acid hydrogels. Biomacromolecules 14, 4125-4134 (2013).
116. Parisi-Amon, A., Mulyasasmita, W., Chung, C. & Heilshorn, S. C. Protein-engineered injectable hydrogel to improve retention of transplanted adipose-derived stem cells. Adv. Healthcare Mater. 2, 428-432 (2013).
117. Haines-Butterick, L. et al. Controlling hydrogelation kinetics by peptide design for three-dimensional encapsulation and injectable delivery of cells. Proc. Natl Acad. Sci. USA 104, 7791-7796 (2007).
118. Zhang, J. et al. Physically associated synthetic hydrogels with long-term covalent stabilization for cell culture and stem cell transplantation. Adv. Mater. 23, 5098-5103 (2011).
119. Rodell, C. B. et al. Shear-thinning supramolecular hydrogels with secondary autonomous covalent crosslinking to modulate viscoelastic properties in vivo. Adv. Funct. Mater. 25, 636-644 (2015).
120. Newcomb, C. J. et al. Cell death versus cell survival instructed by supramolecular cohesion of nanostructures. Nat. Commun. 5, 3321 (2014).
121. Baker, B. M. et al. Cell-mediated fibre recruitment drives extracellular matrix mechanosensing in engineered fibrillar microenvironments. Nat. Mater. 14, 1262-1268 (2015).
122. Yang, C., Tibbitt, M. W., Basta, L. & Anseth, K. S. Mechanical memory and dosing influence stem cell fate. Nat. Mater. 13, 645-652 (2014).
123. Balestrini, J. L., Chaudhry, S., Sarrazy, V., Koehler, A. & Hinz, B. The mechanical memory of lung myofibroblasts. Integr. Biol. 4, 410-421 (2012).
124. Levental, K. R. et al. Matrix crosslinking forces tumor progression by enhancing integrin signaling. Cell 139, 891-906 (2009).
125. Liu, Z. et al. Spatiotemporally controllable and cytocompatible approach builds 3D cell culture matrix by photo-uncaged-thiol michael addition reaction. Adv. Mater. 26, 3912-3917 (2014).
126. Guvendiren, M. & Burdick, J. A. Stiffening hydrogels to probe short- and long-term cellular responses to dynamic mechanics. Nat. Commun. 3, 792 (2012).
127. He, M., Li, J., Tan, S., Wang, R. & Zhang, Y. Photodegradable supramolecular hydrogels with fluorescence turn-on reporter for photomodulation of cellular microenvironments. J. Am. Chem. Soc. 135, 18718-18721 (2013).
128. Jiang, F. X., Yurke, B., Schloss, R. S., Firestein, B. L. & Langrana, N. A. The relationship between fibroblast growth and the dynamic stiffnesses of a DNA crosslinked hydrogel. Biomaterials 31, 1199-1212 (2010).
129. Jiang, F. X., Yurke, B., Schloss, R. S., Firestein, B. L. & Langrana, N. A. Effect of dynamic stiffness of the substrates on neurite outgrowth by using a DNA-crosslinked hydrogel. Tissue Eng. Part A 16, 1873-1889 (2010).
130. Peng, L. et al. Macroscopic volume change of dynamic hydrogels induced by reversible DNA hybridization. J. Am. Chem. Soc. 134, 12302-12307 (2012).
131. Lin, D. C., Yurke, B. & Langrana, N. A. Inducing reversible stiffness changes in DNA-crosslinked gels. J. Mater. Res. 20, 1456-1464 (2005).
132. Lin, D. C., Yurke, B. & Langrana, N. A. Mechanical properties of a reversible, DNA-crosslinked polyacrylamide hydrogel. J. Biomech. Eng. 126, 104-110 (2004).
133. Murphy, W. L. Emerging area: biomaterials that mimic and exploit protein motion. Soft Matter 7, 3679-3688 (2011).
134. Ehrick, J. D. et al. Genetically engineered protein in hydrogels tailors stimuli-responsive characteristics. Nat. Mater. 4, 298-302 (2005).
135. Murphy, W. L., Dillmore, W. S., Modica, J. & Mrksich, M. Dynamic hydrogels: translating a protein conformational change into macroscopic motion. Angew. Chem. Int. Ed. Engl. 46, 3066-3069 (2007).
136. Yuan, W., Yang, J., Kopečková, P. & Kopeček, J. Smart hydrogels containing adenylate kinase: translating substrate recognition into macroscopic motion. J. Am. Chem. Soc. 130, 15760-15761 (2008).
137. Tang, S., Glassman, M. J., Li, S., Socrate, S. & Olsen, B. D. Oxidatively responsive chain extension to entangle engineered protein hydrogels. Macromolecules 47, 791-799 (2014).
138. Kong, N., Peng, Q. & Li, H. Rationally designed dynamic protein hydrogels with reversibly tunable mechanical properties. Adv. Funct. Mater. 24, 7310-7317 (2014).
139. Rosales, A. M., Mabry, K. M., Nehls, E. M. & Anseth, K. S. Photoresponsive elastic properties of azobenzene-containing poly(ethylene-glycol)-based hydrogels. Biomacromolecules 16, 798-806 (2015).
140. Tamesue, S., Takashima, Y., Yamaguchi, H., Shinkai, S. & Harada, A. Photoswitchable supramolecular hydrogels formed by cyclodextrins and azobenzene polymers. Angew. Chem. Int. Ed. Engl. 49, 7461-7464 (2010).
141. Gillette, B. M., Jensen, J. A., Wang, M., Tchao, J. & Sia, S. K. Dynamic hydrogels: switching of 3D microenvironments using two-component naturally derived extracellular matrices. Adv. Mater. 22, 686-691 (2010).
142. Stowers, R. S., Allen, S. C. & Suggs, L. J. Dynamic phototuning of 3D hydrogel stiffness. Proc. Natl Acad. Sci. USA 112, 1953-1958 (2015).
143. Seiffert, S. & Weitz, D. A. Microfluidic fabrication of smart microgels from macromolecular precursors. Polymer 51, 5883-5889 (2010).
144. Shah, R. K., Kim, J.-W., Agresti, J. J., Weitz, D. A. & Chu, L.Y. Fabrication of monodisperse thermosensitive microgels and gel capsules in microfluidic devices. Soft Matter 4, 2303-2309 (2008).
145. Das, M., Zhang, H. & Kumacheva, E. Microgels: old materials with new applications. Annu. Rev. Mater. Res. 36, 117-142 (2006).
146. Panda, P. et al. Stop-flow lithography to generate cell-laden microgel particles. Lab. Chip 8, 1056-1061 (2008).
147. Xu, S. et al. Generation of monodisperse particles by using microfluidics: control over size, shape, and composition. Angew. Chem. Int. Ed. Engl. 44, 724-728 (2005).
148. Shen, Q. et al. Specific capture and release of circulating tumor cells using aptamer-modified nanosubstrates. Adv. Mater. 25, 2368-2373 (2013).
149. Deng, Y. et al. An integrated microfluidic chip system for single-cell secretion profiling of rare circulating tumor cells. Sci. Rep. 4, 7499 (2014).
150. Zhao, W. et al. Bioinspired multivalent DNA network for capture and release of cells. Proc. Natl Acad. Sci. USA 109, 19626-19631 (2012).
151. Liu, H. et al. Dual-responsive surfaces modified with phenylboronic acid-containing polymer brush to reversibly capture and release cancer cells. J. Am. Chem. Soc. 135, 7603-7609 (2013).
152. Ouyang, J. et al. Morphology controlled poly(aminophenylboronic acid) nanostructures as smart substrates for enhanced capture and release of circulating tumor cells. Adv. Funct. Mater. 25, 6122-6130 (2015).
153. Pan, G. et al. Dynamic introduction of cell adhesive factor via reversible multicovalent phenylboronic acid/cis-diol polymeric complexes. J. Am. Chem. Soc. 136, 6203-6206 (2014).
154. Li, W., Wang, J., Ren, J. & Qu, X. 3D graphene oxide-polymer hydrogel: near-infrared light-triggered active scaffold for reversible cell capture and on-demand release. Adv. Mater. 25, 6737-6743 (2013).
155. Hyun, J., Lee, W.-K., Nath, N., Chilkoti, A. & Zauscher, S. Capture and release of proteins on the nanoscale by stimuli-responsive elastin-like polypeptide "switches". J. Am. Chem. Soc. 126, 7330-7335 (2004).
156. Mabry, K. M., Lawrence, R. L. & Anseth, K. S. Dynamic stiffening of poly(ethylene glycol)-based hydrogels to direct valvular interstitial cell phenotype in a three-dimensional environment. Biomaterials 49, 47-56 (2015).
157. Tsien, R. Y. Constructing and exploiting the fluorescent protein paintbox (Nobel lecture). Angew. Chem. Int. Ed. Engl. 48, 5612-5626 (2009).
158. Dean, K. M. & Palmer, A. E. Advances in fluorescence labeling strategies for dynamic cellular imaging. Nat. Chem. Biol. 10, 512-523 (2014).
159. Legant, W. R. et al. Measurement of mechanical tractions exerted by cells in three-dimensional matrices. Nat. Meth 7, 969-971 (2010).
160. Schultz, K. M. & Anseth, K. S. Monitoring degradation of matrix metalloproteinases-cleavable PEG hydrogels via multiple particle tracking microrheology. Soft Matter 9, 1570-1579 (2013).
161. Bloom, R. J., George, J. P., Celedon, A., Sun, S. X. & Wirtz, D. Mapping local matrix remodeling induced by a migrating tumor cell using three-dimensional multiple-particle tracking. Biophys. J. 95, 4077-4088 (2008).
162. Watt, F. M. & Huck, W. T. S. Role of the extracellular matrix in regulating stem cell fate. Nat. Rev. Mol. Cell Biol. 14, 467-473 (2013).
163. Grashoff, C. et al. Measuring mechanical tension across vinculin reveals regulation of focal adhesion dynamics. Nature 466, 263-266 (2010).
164. Manduca, A. et al. Magnetic resonance elastography: non-invasive mapping of tissue elasticity. Med. Image Anal. 5, 237-254 (2001).
165. Othman, S. F., Xu, H., Royston, T. J. & Magin, R. L. Microscopic magnetic resonance elastography (μMRE). Magn. Reson. Med. 54, 605-615 (2005).
166. Othman, S. F., Xu, H. & Mao, J. J. Future role of MR elastography in tissue engineering and regenerative medicine. J. Tissue Eng. Regener. Med. 9, 481-487 (2015).
167. Ranga, A. & Lutolf, M. P. High-throughput approaches for the analysis of extrinsic regulators of stem cell fate. Curr. Opin. Cell Biol. 24, 236-244 (2012).
168. Zanella, F., Lorens, J. B. & Link, W. High content screening: seeing is believing. Trends Biotechnol. 28, 237-245 (2010).
169. Megason, S. G. & Fraser, S. E. Imaging in systems biology. Cell 130, 784-795 (2007).
170. Chen, W. L. K., Likhitpanichkul, M., Ho, A. & Simmons, C. A. Integration of statistical modeling and high-content microscopy to systematically investigate cell-substrate interactions. Biomaterials 31, 2489-2497 (2010).
171. Highley, C. B., Rodell, C. B. & Burdick, J. A. Direct 3D printing of shear-thinning hydrogels into self-healing hydrogels. Adv. Mater. 27, 5075-5079 (2015).
172. Kolesky, D. B. et al. 3D bioprinting of vascularized, heterogeneous cell-laden tissue constructs. Adv. Mater. 26, 3124-3130 (2014).
173. Culver, J. C. et al. Three-dimensional biomimetic patterning in hydrogels to guide cellular organization. Adv. Mater. 24, 2344-2348 (2012).
174. Tumbleston, J. R. et al. Continuous liquid interface production of 3D objects. Science 347, 1349-1352 (2015).
175. Appel, E. A., del Barrio, J., Loh, X. J. & Scherman, O. A. Supramolecular polymeric hydrogels. Chem. Soc. Rev. 41, 6195-6214 (2012).
176. Cheng, E. et. al. A pH-triggered, fast-responding DNA hydrogel. Angew. Chem. Int. Ed. Engl. 48, 7660-7663 (2009).