Mimicking dynamic in vivo environments with stimuli-responsive materials for cell culture

Trends in Biotechnology

Volumn 30, Issue 8, 2012, Pages 426-439

  Kim, Jungwook ^a   Hayward, Ryan C ^a  

^a UNIVERSITY OF MASSACHUSETTS   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CELL FATES; CELL MATRIX INTERACTIONS; COMPLEX CHARACTERISTICS; CONTROL-CELL; DYNAMIC CHARACTERISTICS; EXTRACELLULAR MATRICES; IN-VIVO; LARGE PARTS; MATERIALS CHEMISTRY; REALISTIC CONDITIONS; STIMULI-RESPONSIVE MATERIALS; SYNTHETIC SUBSTRATES; TEMPORAL VARIATION;

BEHAVIORAL RESEARCH; CELL CULTURE; CELLS;

CELL ENGINEERING;

AZOBENZENE; HYDROQUINONE; POLY(N ISOPROPYLACRYLAMIDE);

ADHERENT CELL; CELL ADHESION; CELL CULTURE; CELL FATE; CELL FUNCTION; CELL INTERACTION; CELL MIGRATION; ELECTRIC POTENTIAL; ENDOTHELIUM CELL; EXTRACELLULAR MATRIX; HUMAN; HYDROGEL; IN VIVO CULTURE; ISOMERIZATION; KERATOMETRY; LIGHT; MAGNETIC FIELD; MECHANICAL STRESS; OXIDATION; PH; PHOTOCHEMISTRY; PRIORITY JOURNAL; REVIEW; STIMULATION; TISSUE CULTURE;

ANIMALS; CELL CULTURE TECHNIQUES; CELL PHYSIOLOGICAL PROCESSES; EXTRACELLULAR MATRIX; HUMANS; MODELS, BIOLOGICAL; TISSUE ENGINEERING;

EID: 84863873221     PISSN: 01677799     EISSN: 18793096     Source Type: Journal    
DOI: 10.1016/j.tibtech.2012.04.003     Document Type: Review

References (115)

1. Guillame-Gentil O., et al. Engineering the extracellular environment: strategies for building 2D and 3D cellular structures. Adv. Mater. 2010, 22:5443-5462.
2. Kshitiz, et al. Micro- and nanoengineering for stem cell biology: the promise with a caution. Trends Biotechnol. 2011, 29:399-408.
3. Guillotin B., Guillemot F. Cell patterning technologies for organotypic tissue fabrication. Trends Biotechnol. 2011, 29:183-190.
4. Discher D.E., et al. Tissue cells feel and respond to the stiffness of their substrate. Science 2005, 310:1139-1143.
5. Buxboim A., et al. Matrix elasticity, cytoskeletal forces and physics of the nucleus: how deeply do cells 'feel' outside and in?. J. Cell Sci. 2010, 123:297-308.
6. Nelson C.M. Geometric control of tissue morphogenesis. Biochim. Biophys. Acta 2009, 1793:903-910.
7. Thery M. Micropatterning as a tool to decipher cell morphogenesis and functions. J. Cell Sci. 2010, 123:4201-4213.
8. Lutolf M.P., Hubbell J.A. Synthetic biomaterials as instructive extracellular microenvironments for morphogenesis in tissue engineering. Nat. Biotechnol. 2005, 23:47-55.
9. Tavella S., et al. Regulated expression of fibronectin, laminin and related integrin receptors during the early chondrocyte differentiation. J. Cell Sci. 1997, 110:2261-2270.
10. Young J.L., Engler A.J. Hydrogels with time-dependent material properties enhance cardiomyocyte differentiation in vitro. Biomaterials 2011, 32:1002-1009.
11. Bataller R., Brenner D.A. Liver fibrosis. J. Clin. Invest. 2005, 115:209-218.
12. Jung K.S., et al. Risk assessment of hepatitis B virus-related hepatocellular carcinoma development using liver stiffness measurement (FibroScan). Hepatology 2011, 53:885-894.
13. Georges P.C., et al. Increased stiffness of the rat liver precedes matrix deposition: implications for fibrosis. Am. J. Physiol. Gastrointest. Liver Physiol. 2007, 293:G1147-G1154.
14. Comoglio P.M., Trusolino L. Cancer: the matrix is now in control. Nat. Med. 2005, 11:1156-1159.
15. Huang S., Ingber D.E. Cell tension, matrix mechanics, and cancer development. Cancer Cell 2005, 8:175-176.
16. Lu P., et al. The extracellular matrix: a dynamic niche in cancer progression. J. Cell Biol. 2012, 196:395-406.
17. Anderson R.K., et al. Image analysis of extracellular matrix topography of colon cancer cells. Microsc. Anal. 2006, 20:5-7.
18. Ciba Foundation Symposium: Cell Adhesion and Human Disease 1995, John Wiley & Sons. J. Marsh, J.A. Goode (Eds.).
19. Vleminckx K., et al. Genetic manipulation of E-cadherin expression by epithelial tumor-cells reveals an invasion suppressor role. Cell 1991, 66:107-119.
20. Schroeder A., et al. Treating metastatic cancer with nanotechnology. Nat. Rev. Cancer 2012, 12:39-50.
21. Chan D.D., et al. Mechanostasis in apoptosis and medicine. Prog. Biophys. Mol. Biol. 2011, 106:517-524.
22. Humphrey J.D. Vascular adaptation and mechanical homeostasis at tissue, cellular, and sub-cellular levels. Cell Biochem. Biophys. 2008, 50:53-78.
23. Flaim C.J., et al. An extracellular matrix microarray for probing cellular differentiation. Nat. Methods 2005, 2:119-125.
24. Hynes R.O. Cell adhesion: old and new questions. Trends Biochem. Sci. 1999, 24:M33-M37.
25. Robertus J., et al. Dynamic control over cell adhesive properties using molecular-based surface engineering strategies. Chem. Soc. Rev. 2010, 39:354-378.
26. Mrksich M. Dynamic substrates for cell biology. MRS Bull. 2005, 30:180-184.
27. Cole M.A., et al. Stimuli-responsive interfaces and systems for the control of protein-surface and cell-surface interactions. Biomaterials 2009, 30:1827-1850.
28. Okano T., et al. Mechanism of cell detachment from temperature-modulated, hydrophilic-hydrophobic polymer surfaces. Biomaterials 1995, 16:297-303.
29. Wong J.Y., et al. Electrically conducting polymers can noninvasively control the shape and growth of mammalian cells. Proc. Natl. Acad. Sci. U.S.A. 1994, 91:3201-3204.
30. Jiang X.Y., et al. Electrochemical desorption of self-assembled monolayers noninvasively releases patterned cells from geometrical confinements. J. Am. Chem. Soc. 2003, 125:2366-2367.
31. Qiu Y., Park K. Environment-sensitive hydrogels for drug delivery. Adv. Drug Deliv. Rev. 2001, 53:321-339.
32. Bajpai A.K., et al. Responsive polymers in controlled drug delivery. Prog. Polym. Sci. 2008, 33:1088-1118.
33. He C., et al. In situ gelling stimuli-sensitive block copolymer hydrogels for drug delivery. J. Control. Release 2008, 127:189-207.
34. Auernheimer J., et al. Photoswitched cell adhesion on surfaces with RGD peptides. J. Am. Chem. Soc. 2005, 127:16107-16110.
35. Liu D., et al. Using azobenzene-embedded self-assembled monolayers to photochemically control cell adhesion reversibly. Angew. Chem. Int. Ed. 2009, 48:4406-4408.
36. Edahiro J., et al. In situ control of cell adhesion using photoresponsive culture surface. Biomacromolecules 2005, 6:970-974.
37. Edahiro J.I., et al. Analysis of photo-induced hydration of a photochromic poly(N-isopropylacrylamide)-spiropyran copolymer thin layer by quartz crystal microbalance. Eur. Polym. J. 2008, 44:300-307.
38. Kim M.S., Diamond S.L. Photocleavage of o-nitrobenzyl ether derivatives for rapid biomedical release applications. Bioorg. Med. Chem. Lett. 2006, 16:4007-4010.
39. Nakanishi J., et al. Spatiotemporal control of cell adhesion on a self-assembled monolayer having a photocleavable protecting group. Anal. Chim. Acta 2006, 578:100-104.
40. Nakanishi J., et al. Spatiotemporal control of migration of single cells on a photoactivatable cell microarray. J. Am. Chem. Soc. 2007, 129:6694-6695.
41. Kaneko S., et al. Photocontrol of cell adhesion on amino-bearing surfaces by reversible conjugation of poly(ethylene glycol) via a photocleavable linker. Phys. Chem. Chem. Phys. 2011, 13:4051-4059.
42. Wirkner M., et al. Triggered cell release from materials using bioadhesive photocleavable linkers. Adv. Mater. 2011, 23:3907-3910.
43. Ohmuro-Matsuyama Y., Tatsu Y. Photocontrolled cell adhesion on a surface functionalized with a caged arginine-glycine-aspartate peptide. Angew. Chem. Int. Ed. 2008, 47:7527-7529.
44. Kim M., et al. Addressable micropatterning of multiple proteins and cells by microscope projection photolithography based on a protein friendly photoresist. Langmuir 2010, 26:12112-12118.
45. Pasparakis G., et al. Laser-induced cell detachment and patterning with photodegradable polymer substrates. Angew. Chem. Int. Ed. 2011, 50:4142-4145.
46. Benoit D.S.W., et al. Small functional groups for controlled differentiation of hydrogel-encapsulated human mesenchymal stem cells. Nat. Mater. 2008, 7:816-823.
47. DeForest C.A., et al. Sequential click reactions for synthesizing and patterning three-dimensional cell microenvironments. Nat. Mater. 2009, 8:659-664.
48. Wylie R.G., et al. Spatially controlled simultaneous patterning of multiple growth factors in three-dimensional hydrogels. Nat. Mater. 2011, 10:799-806.
49. Kloxin A.M., et al. Photodegradable hydrogels for dynamic tuning of physical and chemical properties. Science 2009, 324:59-63.
50. San Miguel V., et al. Wavelength-selective caged surfaces: how many functional levels are possible?. J. Am. Chem. Soc. 2011, 133:5380-5388.
51. Yeo W.S., et al. Dynamic interfaces between cells and surfaces: electroactive substrates that sequentially release and attach cells. J. Am. Chem. Soc. 2003, 125:14994-14995.
52. Chan E.W.L., et al. An electroactive catalytic dynamic substrate that immobilizes and releases patterned ligands, proteins, and cells. Angew. Chem. Int. Ed. 2008, 47:6267-6271.
53. Luo W., Yousaf M.N. Tissue morphing control on dynamic gradient surfaces. J. Am. Chem. Soc. 2011, 133:10780-10783.
54. Lamb B.M., Yousaf M.N. Redox-switchable surface for controlling peptide structure. J. Am. Chem. Soc. 2011, 133:8870-8873.
55. Jiang X.Y., et al. Directing cell migration with asymmetric micropatterns. Proc. Natl. Acad. Sci. U.S.A. 2005, 102:975-978.
56. Raghavan S., et al. Micropatterned dynamically adhesive substrates for cell migration. Langmuir 2010, 26:17733-17738.
57. West J.L., Hubbell J.A. Polymeric biomaterials with degradation sites for proteases involved in cell migration. Macromolecules 1999, 32:241-244.
58. Lutolf M.R., et al. Repair of bone defects using synthetic mimetics of collagenous extracellular matrices. Nat. Biotechnol. 2003, 21:513-518.
59. Straley K.S., Heilshorn S.C. Dynamic, 3D-pattern formation within enzyme-responsive hydrogels. Adv. Mater. 2009, 21:4148-4152.
60. Ulijn R.V., et al. Bioresponsive hydrogels. Mater. Today 2007, 10:40-48.
61. Todd S.J., et al. Enzyme-triggered cell attachment to hydrogel surfaces. Soft Matter 2007, 3:547-550.
62. Perlin L., et al. Cell adhesive hydrogels synthesised by copolymerisation of Arg-protected Gly-Arg-Gly-Asp-Ser methacrylate monomers and enzymatic deprotection. Chem. Commun. 2008, 5951-5953.
63. Liu B., et al. Dynamic presentation of immobilized ligands regulated through biomolecular recognition. J. Am. Chem. Soc. 2010, 132:13630-13632.
64. Yambe M., et al. Arterial stiffening as a possible risk factor for both atherosclerosis and diastolic heart failure. Hypertens. Res. 2004, 27:625-631.
65. Discher D.E., et al. Growth factors, matrices, and forces combine and control stem cells. Science 2009, 324:1673-1677.
66. Chowdhury F., et al. Material properties of the cell dictate stress-induced spreading and differentiation in embryonic stem cells. Nat. Mater. 2010, 9:82-88.
67. Frey M.T., Wang Y.-l. A photo-modulatable material for probing cellular responses to substrate rigidity. Soft Matter 2009, 5:1918-1924.
68. Kloxin A.M., et al. Tunable hydrogels for external manipulation of cellular microenvironments through controlled photodegradation. Adv. Mater. 2010, 22:61-66.
69. Tibbitt M.W., et al. Controlled two-photon photodegradation of PEG hydrogels to study and manipulate subcellular interactions on soft materials. Soft Matter 2010, 6:5100-5108.
70. Yoshikawa H.Y., et al. Quantitative evaluation of mechanosensing of cells on dynamically tunable hydrogels. J. Am. Chem. Soc. 2011, 133:1367-1374.
71. Li Y., et al. A molecular mechanisms-based biophysical model for two-phase cell spreading. Appl. Phys. Lett. 2010, 96:043703.
72. Khetan S., et al. Sequential crosslinking to control cellular spreading in 3-dimensional hydrogels. Soft Matter 2009, 5:1601-1606.
73. Khetan S., Burdick J.A. Patterning network structure to spatially control cellular remodeling and stem cell fate within 3-dimensional hydrogels. Biomaterials 2010, 31:8228-8234.
74. Gillette B.M., et al. Dynamic hydrogels: switching of 3D microenvironments using two-component naturally derived extracellular matrices. Adv. Mater. 2010, 22:686-691.
75. Engler A.J., et al. Matrix elasticity directs stem cell lineage specification. Cell 2006, 126:677-689.
76. Lin D.C., et al. Inducing reversible stiffness changes in DNA-crosslinked gels. J. Mater. Res. 2005, 20:1456-1464.
77. Jiang F.X., et al. Effect of dynamic stiffness of the substrates on neurite outgrowth by using a DNA-crosslinked hydrogel. Tissue Eng. A 2010, 16:1873-1889.
78. Jiang F.X., et al. The relationship between fibroblast growth and the dynamic stiffnesses of a DNA crosslinked hydrogel. Biomaterials 2010, 31:1199-1212.
79. Storm C., et al. Nonlinear elasticity in biological gels. Nature 2005, 435:191-194.
80. Winer J.P., et al. Non-linear elasticity of extracellular matrices enables contractile cells to communicate local position and orientation. PLoS ONE 2009, 4:e6382.
81. Brown T.D. Techniques for mechanical stimulation of cells in vitro: a review. J. Biomech. 2000, 33:3-14.
82. Kim D.-H., et al. Microengineered platforms for cell mechanobiology. Annu. Rev. Biomed. Eng. 2009, 11:203-233.
83. Moraes C., et al. Microfabricated arrays for high-throughput screening of cellular response to cyclic substrate deformation. Lab. Chip 2010, 10:227-234.
84. Moraes C., et al. A microfabricated platform for high-throughput unconfined compression of micropatterned biomaterial arrays. Biomaterials 2010, 31:577-584.
85. Kamotani Y., et al. Individually programmable cell stretching microwell arrays actuated by a Braille display. Biomaterials 2008, 29:2646-2655.
86. Shimizu K., et al. Development of a biochip with serially connected pneumatic balloons for cell-stretching culture. Sens. Actuators B 2011, 156:486-493.
87. Steward R.L., et al. Probing cell structure responses through a shear and stretching mechanical stimulation technique. Cell Biochem. Biophys. 2010, 56:115-124.
88. Young E.W.K., Simmons C.A. Macro- and microscale fluid flow systems for endothelial cell biology. Lab. Chip 2010, 10:143-160.
89. Kurpinski K., et al. Anisotropic mechanosensing by mesenchymal stem cells. Proc. Natl. Acad. Sci. U.S.A. 2006, 103:16095-16100.
90. Cheng C.-M., et al. Probing cell structure by controlling the mechanical environment with cell-substrate interactions. J. Biomech. 2009, 42:187-192.
91. Ahmed W.W., et al. Myoblast morphology and organization on biochemically micro-patterned hydrogel coatings under cyclic mechanical strain. Biomaterials 2010, 31:250-258.
92. Gopalan S.M., et al. Anisotropic stretch-induced hypertrophy in neonatal ventricular myocytes micropatterned on deformable elastomers. Biotechnol. Bioeng. 2003, 81:578-587.
93. Huh D., et al. Reconstituting organ-level lung functions on a chip. Science 2010, 328:1662-1668.
94. Sniadecki N.J., et al. Magnetic microposts as an approach to apply forces to living cells. Proc. Natl. Acad. Sci. U.S.A. 2007, 104:14553-14558.
95. Wang N., et al. Mechanotransduction across the cell-surface and through the cytoskeleton. Science 1993, 260:1124-1127.
96. Huang H.D., et al. Cell mechanics and mechanotransduction: pathways, probes, and physiology. Am. J. Physiol. Cell Physiol. 2004, 287:C1-C11.
97. Lin Y.-W., et al. Understanding sensory nerve mechanotransduction through localized elastomeric matrix control. PLoS ONE 2009, 4:e4293.
98. Cheng C.-M., et al. Probing localized neural mechanotransduction through surface-modified elastomeric matrices and electrophysiology. Nat. Protoc. 2010, 5:714-724.
99. Yamaki K., et al. Regulation of cellular morphology using temperature-responsive hydrogel for integrin-mediated mechanical force stimulation. Biomaterials 2009, 30:1421-1427.
100. Kim-Kaneyama J., et al. Uni-axial stretching regulates intracellular localization of Hic-5 expressed in smooth-muscle cells in vivo. J. Cell Sci. 2005, 118:937-949.
101. Kim J., et al. Dynamic display of biomolecular patterns through an elastic creasing instability of stimuli-responsive hydrogels. Nat. Mater. 2010, 9:159-164.
102. Chen C.S., et al. Geometric control of cell life and death. Science 1997, 276:1425-1428.
103. Gao L., et al. Stem cell shape regulates a chondrogenic versus myogenic fate through Rac1 and N-cadherin. Stem Cells 2010, 28:564-572.
104. Kulangara K., Leong K.W. Substrate topography shapes cell function. Soft Matter 2009, 5:4072-4076.
105. Chou L.S., et al. Substratum surface-topography alters cell-shape and regulates fibronectin messenger-RNA level, messenger-RNA stability, secretion and assembly in human fibroblasts. J. Cell Sci. 1995, 108:1563-1573.
106. Brunette D.M., Chehroudi B. The effects of the surface topography of micromachined titanium substrata on cell behavior in vitro and in vivo. J. Biomech. Eng. 1999, 121:49-57.
107. Lam M.T., et al. Reversible on-demand cell alignment using reconfigurable microtopography. Biomaterials 2008, 29:1705-1712.
108. Zhu X.Y., et al. Fabrication of reconfigurable protein matrices by cracking. Nat. Mater. 2005, 4:403-406.
109. Liu C., et al. Review of progress in shape-memory polymers. J. Mater. Chem. 2007, 17:1543-1558.
110. Le D.M., et al. Dynamic topographical control of mesenchymal stem cells by culture on responsive poly(epsilon-caprolactone) surfaces. Adv. Mater. 2011, 23:3278-3283.
111. Davis K.A., et al. Dynamic cell behavior on shape memory polymer substrates. Biomaterials 2011, 32:2285-2293.
112. Ebara M., et al. Shape-memory surface with dynamically tunable nano-geometry activated by body heat. Adv. Mater. 2012, 24:273-278.
113. Jiang W., et al. Nanoparticle-mediated cellular response is size-dependent. Nat. Nanotechnol. 2008, 3:145-150.
114. Oh S., et al. Stem cell fate dictated solely by altered nanotube dimension. Proc. Natl. Acad. Sci. U.S.A. 2009, 106:2130-2135.
115. Kim D.-H., et al. Nanoscale cues regulate the structure and function of macroscopic cardiac tissue constructs. Proc. Natl. Acad. Sci. U.S.A. 2010, 107:565-570.