Photo-Dimerization Induced Dynamic Viscoelastic Changes in ABA Triblock Copolymer-Based Hydrogels for 3D Cell Culture

Chemistry of Materials

Volumn 28, Issue 17, 2016, Pages 6401-6408

  Tamate, Ryota ^a   Ueki, Takeshi ^b   Kitazawa, Yuzo ^c   Kuzunuki, Morinobu ^c   Watanabe, Masayoshi ^c   Akimoto, Aya Mizutani ^a   Yoshida, Ryo ^a  

^a UNIVERSITY OF TOKYO   (Japan)

^b NATIONAL INSTITUTE FOR MATERIALS SCIENCE   (Japan)

^c YOKOHAMA NATIONAL UNIVERSITY   (Japan)

Author keywords

[No Author keywords available]

Indexed keywords

ACRYLIC MONOMERS; BIOCOMPATIBILITY; BLOCK COPOLYMERS; CELL CULTURE; CROSSLINKING; ELASTICITY; ETHYLENE; IRRADIATION; POLYETHYLENE OXIDES; STRESS RELAXATION; VISCOELASTICITY;

ABA TRIBLOCK COPOLYMER; BIOCHEMICAL SIGNAL; CHEMICAL CROSS-LINKING; CROSS-LINKED HYDROGELS; N- ISOPROPYLACRYLAMIDE; RHEOLOGICAL PROPERTY; UV-LIGHT IRRADIATION; VISCOELASTIC PROPERTIES;

HYDROGELS;

EID: 84987644121     PISSN: 08974756     EISSN: 15205002     Source Type: Journal    
DOI: 10.1021/acs.chemmater.6b02839     Document Type: Article

References (60)

1. Lu, P.; Weaver, V. M.; Werb, Z. The Extracellular Matrix: A Dynamic Niche in Cancer Progression J. Cell Biol. 2012, 196, 395-406 10.1083/jcb.201102147
2. Watt, F. M.; Huck, W. T. S. Role of the Extracellular Matrix in Regulating Stem Cell Fate Nat. Rev. Mol. Cell Biol. 2013, 14, 467-473 10.1038/nrm3620
3. Bonnans, C.; Chou, J.; Werb, Z. Remodelling the Extracellular Matrix in Development and Disease Nat. Rev. Mol. Cell Biol. 2014, 15, 786-801 10.1038/nrm3904
4. Hoffman, A. S. Hydrogels for Biomedical Applications Adv. Drug Delivery Rev. 2012, 64, 18-23 10.1016/j.addr.2012.09.010
5. Drury, J. L.; Mooney, D. J. Hydrogels for Tissue Engineering: Scaffold Design Variables and Applications Biomaterials 2003, 24, 4337-4351 10.1016/S0142-9612(03)00340-5
6. Lutolf, M. P.; Hubbell, J. A. Synthetic Biomaterials as Instructive Extracellular Microenvironments for Morphogenesis in Tissue Engineering Nat. Biotechnol. 2005, 23, 47-55 10.1038/nbt1055
7. Seliktar, D. Designing Cell-Compatible Hydrogels for Biomedical Applications Science 2012, 336, 1124-1128 10.1126/science.1214804
8. Thiele, J.; Ma, Y.; Bruekers, S. M. C.; Ma, S.; Huck, W. T. S. 25th Anniversary Article: Designer Hydrogels for Cell Cultures: A Materials Selection Guide Adv. Mater. 2014, 26, 125-148 10.1002/adma.201302958
9. Pelham, R. J.; Wang, Y. L. Cell Locomotion and Focal Adhesions Are Regulated by Substrate Flexibility Proc. Natl. Acad. Sci. U. S. A. 1997, 94, 13661-13665 10.1073/pnas.94.25.13661
10. Engler, A. J.; Griffin, M. A.; Sen, S.; Bönnemann, C. G.; Sweeney, H. L.; Discher, D. E. Myotubes Differentiate Optimally on Substrates with Tissue-like Stiffness: Pathological Implications for Soft or Stiff Microenvironments J. Cell Biol. 2004, 166, 877-887 10.1083/jcb.200405004
11. Engler, A. J.; Sen, S.; Sweeney, H. L.; Discher, D. E. Matrix Elasticity Directs Stem Cell Lineage Specification Cell 2006, 126, 677-689 10.1016/j.cell.2006.06.044
12. Klein, E. A.; Yin, L.; Kothapalli, D.; Castagnino, P.; Byfield, F. J.; Xu, T.; Levental, I.; Hawthorne, E.; Janmey, P. A.; Assoian, R. K. Cell-Cycle Control by Physiological Matrix Elasticity and in Vivo Tissue Stiffening Curr. Biol. 2009, 19, 1511-1518 10.1016/j.cub.2009.07.069
13. Banerjee, A.; Arha, M.; Choudhary, S.; Ashton, R. S.; Bhatia, S. R.; Schaffer, D. V.; Kane, R. S. The Influence of Hydrogel Modulus on the Proliferation and Differentiation of Encapsulated Neural Stem Cells Biomaterials 2009, 30, 4695-4699 10.1016/j.biomaterials.2009.05.050
14. Saha, K.; Keung, A. J.; Irwin, E. F.; Li, Y.; Little, L.; Schaffer, D. V.; Healy, K. E. Substrate Modulus Directs Neural Stem Cell Behavior Biophys. J. 2008, 95, 4426-4438 10.1529/biophysj.108.132217
15. Tibbitt, M. W.; Anseth, K. S. Hydrogels as Extracellular Matrix Mimics for 3D Cell Culture Biotechnol. Bioeng. 2009, 103, 655-663 10.1002/bit.22361
16. Baker, B. M.; Chen, C. S. Deconstructing the Third Dimension: How 3D Culture Microenvironments Alter Cellular Cues J. Cell Sci. 2012, 125, 3015-3024 10.1242/jcs.079509
17. Huebsch, N.; Arany, P. R.; Mao, A. S.; Shvartsman, D.; Ali, O. A.; Bencherif, S. A.; Rivera-Feliciano, J.; Mooney, D. J. Harnessing Traction-Mediated Manipulation of the Cell/matrix Interface to Control Stem-Cell Fate Nat. Mater. 2010, 9, 518-526 10.1038/nmat2732
18. Georges, P. C.; Hui, J. J.; Gombos, Z.; McCormick, M. E.; Wang, A. Y.; Uemura, M.; Mick, R.; Janmey, P. A.; Furth, E. E.; Wells, R. G. Increased Stiffness of the Rat Liver Precedes Matrix Deposition: Implications for Fibrosis Am. J. Physiol. Gastrointest. Liver Physiol. 2007, 293, G1147-G1154 10.1152/ajpgi.00032.2007
19. Levental, K. R.; Yu, H.; Kass, L.; Lakins, J. N.; Egeblad, M.; Erler, J. T.; Fong, S. F. T.; Csiszar, K.; Giaccia, A.; Weninger, W.; Yamauchi, M.; Gasser, D. L.; Weaver, V. M. Matrix Crosslinking Forces Tumor Progression by Enhancing Integrin Signaling Cell 2009, 139, 891-906 10.1016/j.cell.2009.10.027
20. Samuel, M. S.; Lopez, J. I.; McGhee, E. J.; Croft, D. R.; Strachan, D.; Timpson, P.; Munro, J.; Schröder, E.; Zhou, J.; Brunton, V. G.; Barker, N.; Clevers, H.; Sansom, O. J.; Anderson, K. I.; Weaver, V. M.; Olson, M. F. Actomyosin-Mediated Cellular Tension Drives Increased Tissue Stiffness and β-Catenin Activation to Induce Epidermal Hyperplasia and Tumor Growth Cancer Cell 2011, 19, 776-791 10.1016/j.ccr.2011.05.008
21. Yoshikawa, H. Y.; Rossetti, F. F.; Kaufmann, S.; Kaindl, T.; Madsen, J.; Engel, U.; Lewis, A. L.; Armes, S. P.; Tanaka, M. Quantitative Evaluation of Mechanosensing of Cells on Dynamically Tunable Hydrogels J. Am. Chem. Soc. 2011, 133, 1367-1374 10.1021/ja1060615
22. Yamaki, K.; Harada, I.; Goto, M.; Cho, C.-S.; Akaike, T. Regulation of Cellular Morphology Using Temperature-Responsive Hydrogel for Integrin-Mediated Mechanical Force Stimulation Biomaterials 2009, 30, 1421-1427 10.1016/j.biomaterials.2008.11.036
23. 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. 2010, 22, 686-691 10.1002/adma.200902265
24. Kloxin, A. M.; Kasko, A. M.; Salinas, C. N.; Anseth, K. S. Photodegradable Hydrogels for Dynamic Tuning of Physical and Chemical Properties Science 2009, 324, 59-63 10.1126/science.1169494
25. Yang, C.; Tibbitt, M. W.; Basta, L.; Anseth, K. S. Mechanical Memory and Dosing Influence Stem Cell Fate Nat. Mater. 2014, 13, 645-652 10.1038/nmat3889
26. Khetan, S.; Katz, J. S.; Burdick, J. A. Sequential Crosslinking to Control Cellular Spreading in 3-Dimensional Hydrogels Soft Matter 2009, 5, 1601-1606 10.1039/b820385g
27. Guvendiren, M.; Burdick, J. A. Stiffening Hydrogels to Probe Short- and Long-Term Cellular Responses to Dynamic Mechanics Nat. Commun. 2012, 3, 792 10.1038/ncomms1792
28. Khetan, S.; Guvendiren, M.; Legant, W. R.; Cohen, D. M.; Chen, C. S.; Burdick, J. A. Degradation-Mediated Cellular Traction Directs Stem Cell Fate in Covalently Crosslinked Three-Dimensional Hydrogels Nat. Mater. 2013, 12, 458-465 10.1038/nmat3586
29. McKinnon, D. D.; Domaille, D. W.; Cha, J. N.; Anseth, K. S. Biophysically Defined and Cytocompatible Covalently Adaptable Networks as Viscoelastic 3D Cell Culture Systems Adv. Mater. 2014, 26, 865-872 10.1002/adma.201303680
30. Cameron, A. R.; Frith, J. E.; Cooper-White, J. J. The Influence of Substrate Creep on Mesenchymal Stem Cell Behaviour and Phenotype Biomaterials 2011, 32, 5979-5993 10.1016/j.biomaterials.2011.04.003
31. Cameron, A. R.; Frith, J. E.; Gomez, G. A.; Yap, A. S.; Cooper-White, J. J. The Effect of Time-Dependent Deformation of Viscoelastic Hydrogels on Myogenic Induction and Rac1 Activity in Mesenchymal Stem Cells Biomaterials 2014, 35, 1857-1868 10.1016/j.biomaterials.2013.11.023
32. Chaudhuri, O.; Gu, L.; Darnell, M.; Klumpers, D.; Bencherif, S. A.; Weaver, J. C.; Huebsch, N.; Mooney, D. J. Substrate Stress Relaxation Regulates Cell Spreading Nat. Commun. 2015, 6, 6365 10.1038/ncomms7365
33. Chaudhuri, O.; Gu, L.; Klumpers, D.; Darnell, M.; Bencherif, S. A.; Weaver, J. C.; Huebsch, N.; Lee, H. P.; Lippens, E.; Duda, G. N.; Mooney, D. J. Hydrogels with Tunable Stress Relaxation Regulate Stem Cell Fate and Activity Nat. Mater. 2015, 15, 326-334 10.1038/nmat4489
34. Frantz, C.; Stewart, K. M.; Weaver, V. M. The Extracellular Matrix at a Glance J. Cell Sci. 2010, 123, 4195-4200 10.1242/jcs.023820
35. Monnier, V. M.; Mustata, G. T.; Biemel, K. L.; Reihl, O.; Lederer, M. O.; Zhenyu, D.; Sell, D. R. Cross-Linking of the Extracellular Matrix by the Maillard Reaction in Aging and Diabetes: An Update On "a Puzzle Nearing Resolution" Ann. N. Y. Acad. Sci. 2005, 1043, 533-544 10.1196/annals.1333.061
36. Bailey, A. Molecular Mechanisms of Ageing in Connective Tissues Mech. Ageing Dev. 2001, 122, 735-755 10.1016/S0047-6374(01)00225-1
37. Cellesi, F.; Tirelli, N.; Hubbell, J. A. Materials for Cell Encapsulation via a New Tandem Approach Combining Reverse Thermal Gelation and Covalent Crosslinking Macromol. Chem. Phys. 2002, 203, 1466-1472 10.1002/1521-3935(200207)203:10/11<1466::AID-MACP1466>3.0.CO;2-P
38. Cellesi, F.; Tirelli, N.; Hubbell, J. A. Towards a Fully-Synthetic Substitute of Alginate: Development of a New Process Using Thermal Gelation and Chemical Cross-Linking Biomaterials 2004, 25, 5115-5124 10.1016/j.biomaterials.2003.12.015
39. Sanabria-DeLong, N.; Crosby, A. J.; Tew, G. N. Photo-Cross-Linked PLA-PEO-PLA Hydrogels from Self-Assembled Physical Networks: Mechanical Properties and Influence of Assumed Constitutive Relationships Biomacromolecules 2008, 9, 2784-2791 10.1021/bm800557r
40. Kadam, V.; Nicolai, T.; Nicol, E.; Benyahia, L. Structure and Rheology of Self-Assembled Telechelic Associative Polymers in Aqueous Solution before and after Photo-Cross-Linking Macromolecules 2011, 44, 8225-8232 10.1021/ma201097s
41. Gu, Y.; Zhang, S.; Martinetti, L.; Lee, K. H.; McIntosh, L. D.; Frisbie, C. D.; Lodge, T. P. High Toughness, High Conductivity Ion Gels by Sequential Triblock Copolymer Self-Assembly and Chemical Cross-Linking J. Am. Chem. Soc. 2013, 135, 9652-9655 10.1021/ja4051394
42. Zhao, Y. Light-Responsive Block Copolymer Micelles Macromolecules 2012, 45, 3647-3657 10.1021/ma300094t
43. Ueki, T.; Nakamura, Y.; Lodge, T. P.; Watanabe, M. Light-Controlled Reversible Micellization of a Diblock Copolymer in an Ionic Liquid Macromolecules 2012, 45, 7566-7573 10.1021/ma3016008
44. Siegert, A. J. F. On the Fluctuations in Signals Returned by Many Independent Scatterers MIT Rad. Lab. Rep. 1943, 465, 1-14
45. Koppel, D. E. Analysis of Macromolecular Polydispersity in Intensity Correlation Spectroscopy: The Method of Cumulants J. Chem. Phys. 1972, 57, 4814-4820 10.1063/1.1678153
46. Jiang, J.; Qi, B.; Lepage, M.; Zhao, Y. Polymer Micelles Stabilization on Demand through Reversible Photo-Cross-Linking Macromolecules 2007, 40, 790-792 10.1021/ma062493j
47. Trenor, S. R.; Shultz, A. R.; Love, B. J.; Long, T. E. Coumarins in Polymers: From Light Harvesting to Photo-Cross-Linkable Tissue Scaffolds Chem. Rev. 2004, 104, 3059-3077 10.1021/cr030037c
48. Kaur, G.; Johnston, P.; Saito, K. Photo-Reversible Dimerisation Reactions and Their Applications in Polymeric Systems Polym. Chem. 2014, 5, 2171-2186 10.1039/C3PY01234D
49. Woodward, R. B.; Hoffmann, R. Stereochemistry of Electrocyclic Reactions J. Am. Chem. Soc. 1965, 87, 395-397 10.1021/ja01080a054
50. Danpure, H. J.; Tyrrell, R. M. Oxygen-Dependence of Near UV (365 nm) Lethality and the Interaction of Near UV and X-Rays in Two Mammalian Cell Lines Photochem. Photobiol. 1976, 23, 171-177 10.1111/j.1751-1097.1976.tb07238.x
51. Kitazawa, Y.; Ueki, T.; Niitsuma, K.; Imaizumi, S.; Lodge, T. P.; Watanabe, M. Thermoreversible High-Temperature Gelation of an Ionic Liquid with Poly(benzyl Methacrylate-b-Methyl Methacrylate-b-Benzyl Methacrylate) Triblock Copolymer Soft Matter 2012, 8, 8067-8074 10.1039/c2sm25375e
52. He, J.; Yan, B.; Tremblay, L.; Zhao, Y. Both Core- and Shell-Cross-Linked Nanogels: Photoinduced Size Change, Intraparticle LCST, and Interparticle UCST Thermal Behaviors Langmuir 2011, 27, 436-444 10.1021/la1040322
53. Zhang, J.; Jiang, X.; Zhang, Y.; Li, Y.; Liu, S. Facile Fabrication of Reversible Core Cross-Linked Micelles Possessing Thermosensitive Swellability Macromolecules 2007, 40, 9125-9132 10.1021/ma071564r
54. Li, C.; Tang, Y.; Armes, S. P.; Morris, C. J.; Rose, S. F.; Lloyd, A. W.; Lewis, A. L. Synthesis and Characterization of Biocompatible Thermo-Responsive Gelators Based on ABA Triblock Copolymers Biomacromolecules 2005, 6, 994-999 10.1021/bm049331k
55. Kirkland, S. E.; Hensarling, R. M.; McConaughy, S. D.; Guo, Y.; Jarrett, W. L.; McCormick, C. L. Thermoreversible Hydrogels from RAFT-Synthesized BAB Triblock Copolymers: Steps toward Biomimetic Matrices for Tissue Regeneration Biomacromolecules 2008, 9, 481-486 10.1021/bm700968t
56. O'Lenick, T. G.; Jin, N.; Woodcock, J. W.; Zhao, B. Rheological Properties of Aqueous Micellar Gels of a Thermo- and pH-Sensitive ABA Triblock Copolymer J. Phys. Chem. B 2011, 115, 2870-2881 10.1021/jp2001332
57. Zhang, S.; Lee, K. H.; Sun, J.; Frisbie, C. D.; Lodge, T. P. Viscoelastic Properties, Ionic Conductivity, and Materials Design Considerations for Poly(styrene-b-Ethylene Oxide-b-Styrene)-Based Ion Gel Electrolytes Macromolecules 2011, 44, 8981-8989 10.1021/ma201356j
58. Zhao, X.; Huebsch, N.; Mooney, D. J.; Suo, Z. Stress-Relaxation Behavior in Gels with Ionic and Covalent Crosslinks J. Appl. Phys. 2010, 107, 63509 10.1063/1.3343265
59. O'Brien, J.; Wilson, I.; Orton, T.; Pognan, F. Investigation of the Alamar Blue (Resazurin) Fluorescent Dye for the Assessment of Mammalian Cell Cytotoxicity Eur. J. Biochem. 2000, 267, 5421-5426 10.1046/j.1432-1327.2000.01606.x
60. Yoshioka, H.; Mikami, M.; Mori, Y.; Tsuchida, E. A Synthetic Hydrogel with Thermoreversible Gelation. I. Preparation and Rheological Properties J. Macromol. Sci., Part A: Pure Appl.Chem. 1994, 31, 113-120 10.1080/10601329409349722