Nonlinear mechanics of hybrid polymer networks that mimic the complex mechanical environment of cells

Nature Communications

Volumn 8, Issue , 2017, Pages

  Jaspers, Maarten ^a   Vaessen, Sarah L ^a   Van Schayik, Pim ^a   Voerman, Dion ^a   Rowan, Alan E ^a,b   Kouwer, Paul H J ^a  

^a RADBOUD UNIVERSITY NIJMEGEN   (Netherlands)

^b UNIVERSITY OF QUEENSLAND   (Australia)

Author keywords

[No Author keywords available]

Indexed keywords

BIOPOLYMER; FIBRIN; GRAPHENE; ACRYLIC ACID RESIN; BIOMIMETIC MATERIAL; CARBON NANOTUBE; POLYACRYLAMIDE;

BIOLOGY; CELLS AND CELL COMPONENTS; CONCENTRATION (COMPOSITION); CYTOPLASM; POLYMER;

AQUEOUS SOLUTION; ARTICLE; CELL ACTIVITY; CHEMICAL STRUCTURE; DISPERSION; EXTRACELLULAR MATRIX; FLOW MEASUREMENT; HYBRID; HYDROGEL; MECHANICS; MOLECULAR DYNAMICS; RIGIDITY; BIOLOGICAL MODEL; BIOMECHANICS; CHEMICAL MODEL; CHEMISTRY; FLOW KINETICS; NONLINEAR SYSTEM; SYNTHETIC BIOLOGY; YOUNG MODULUS;

ACRYLIC RESINS; BIOMECHANICAL PHENOMENA; BIOMIMETIC MATERIALS; BIOPOLYMERS; ELASTIC MODULUS; FIBRIN; HYDROGELS; MODELS, BIOLOGICAL; MODELS, CHEMICAL; NANOTUBES, CARBON; NONLINEAR DYNAMICS; RHEOLOGY; SYNTHETIC BIOLOGY;

EID: 85019743911     PISSN: None     EISSN: 20411723     Source Type: Journal    
DOI: 10.1038/ncomms15478     Document Type: Article

References (54)

1. Pritchard, R. H., Huang, Y. Y. & Terentjev, E. M. Mechanics of biological networks: from the cell cytoskeleton to connective tissue. Soft Matter 10, 1864-1884 (2014).
2. Discher, D. E., Janmey, P. & Wang, Y. L. Tissue cells feel and respond to the stiffness of their substrate. Science 310, 1139-1143 (2005).
3. Engler, A. J., Sen, S., Sweeney, H. L. & Discher, D. E. Matrix elasticity directs stem cell lineage specification. Cell 126, 677-689 (2006).
4. Place, E. S., Evans, N. D. & Stevens, M. M. Complexity in biomaterials for tissue engineering. Nat. Mater. 8, 457-470 (2009).
5. 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. 26, 125-148 (2014).
6. Huber, F., Boire, A., Lopez, M. P. & Koenderink, G. H. Cytoskeletal crosstalk: when three different personalities team up. Curr. Opin. Cell Biol. 32, 39-47 (2015).
7. Gong, J. P., Katsuyama, Y., Kurokawa, T. & Osada, Y. Double-network hydrogels with extremely high mechanical strength. Adv. Mater. 15, 1155-1158 (2003).
8. Nakajima, T. et al. A universal molecular stent method to toughen any hydrogels based on double network concept. Adv. Funct. Mater. 22, 4426-4432 (2012).
9. Gong, J. P. Why are double network hydrogels so tough Soft Matter 6, 2583-2590 (2010).
10. Haraguchi, K. & Takehisa, T. Nanocomposite hydrogels: A unique organicinorganic network structure with extraordinary mechanical, optical, and swelling/de-swelling properties. Adv. Mater. 14, 1120-1124 (2002).
11. Okay, O. & Oppermann, W. Polyacrylamide-clay nanocomposite hydrogels: Rheological and light scattering characterization. Macromolecules 40, 3378-3387 (2007).
12. Wang, Q. et al. High-water-content mouldable hydrogels by mixing clay and a dendritic molecular binder. Nature 463, 339-343 (2010).
13. Liu, M. J. et al. An anisotropic hydrogel with electrostatic repulsion between cofacially aligned nanosheets. Nature 517, 68-72 (2015).
14. Storm, C., Pastore, J. J., MacKintosh, F. C., Lubensky, T. C. & Janmey, P. A. Nonlinear elasticity in biological gels. Nature 435, 191-194 (2005).
15. Gardel, M. L. et al. Elastic behavior of cross-linked and bundled actin networks. Science 304, 1301-1305 (2004).
16. Lin, Y. C. et al. Origins of elasticity in intermediate filament networks. Phys. Rev. Lett. 104, 058101 (2010).
17. Piechocka, I. K., Bacabac, R. G., Potters, M., MacKintosh, F. C. & Koenderink, G. H. Structural hierarchy governs fibrin gel mechanics. Biophys. J. 98, 2281-2289 (2010).
18. Motte, S. & Kaufman, L. J. Strain stiffening in collagen I networks. Biopolymers 99, 35-46 (2013).
19. Winer, J. P., Oake, S. & Janmey, P. A. Non-linear elasticity of extracellular matrices enables contractile cells to communicate local position and orientation. PLoS ONE 4, e6382 (2009).
20. Wen, Q. & Janmey, P. A. Effects of non-linearity on cell-ECM interactions. Exp. Cell Res. 319, 2481-2489 (2013).
21. Gillette, B. M., Jensen, J. A., Wang, M. X., Tchao, J. & Sia, S. K. Dynamic hydrogels: switching of 3D microenvironments using two-component naturally derived extracellular matrices. Adv. Mater. 22, 686-691 (2010).
22. Gillette, B. M. et al. In situ collagen assembly for integrating microfabricated three-dimensional cell-seeded matrices. Nat. Mater. 7, 636-640 (2008).
23. Jensen, M. H., Morris, E. J., Goldman, R. D. & Weitz, D. A. Emergent properties of composite semiflexible biopolymer networks. BioArchitecture 4, 138-143 (2014).
24. Lin, Y. C., Koenderink, G. H., MacKintosh, F. C. & Weitz, D. A. Control of non-linear elasticity in F-actin networks with microtubules. Soft Matter 7, 902-906 (2011).
25. Huisman, E. M., Heussinger, C., Storm, C. & Barkema, G. T. Semiflexible filamentous composites. Phys. Rev. Lett. 105, 118101 (2010).
26. Kouwer, P. H. J. et al. Responsive biomimetic networks from polyisocyanopeptide hydrogels. Nature 493, 651-655 (2013).
27. Jaspers, M. et al. Ultra-responsive soft matter from strain-stiffening hydrogels. Nat. Commun. 5, 5808 (2014).
28. Jaspers, M., Rowan, A. E. & Kouwer, P. H. J. Tuning hydrogel mechanics using the hofmeister effect. Adv. Funct. Mater. 25, 6503-6510 (2015).
29. Jaspers, M. et al. Bundle formation in biomimetic hydrogels. Biomacromolecules 17, 2642-2649 (2016).
30. Kasza, K. E. et al. The cell as a material. Curr. Opin. Cell Biol. 19, 101-107 (2007).
31. van Buul, A. M. et al. Stiffness versus architecture of single helical polyisocyanopeptides. Chem. Sci. 4, 2357-2363 (2013).
32. Mandal, S. et al. Therapeutic nanoworms: Towards novel synthetic dendritic cells for immunotherapy. Chem. Sci. 4, 4168-4174 (2013).
33. Das, R. K., Gocheva, V., Hammink, R., Zouani, O. F. & Rowan, A. E. Stressstiffening-mediated stem-cell commitment switch in soft responsive hydrogels. Nat. Mater. 15, 318-325 (2016).
34. Ajayan, P. M. & Tour, J. M. Materials science-nanotube composites. Nature 447, 1066-1068 (2007).
35. Weisel, J. W. & Litvinov, R. I. Mechanisms of fibrin polymerization and clinical implications. Blood 121, 1712-1719 (2013).
36. Kurniawan, N. A., Grimbergen, J., Koopman, J. & Koenderink, G. H. Factor XIII stiffens fibrin clots by causing fiber compaction. J. Thromb. Haemost. 12, 1687-1696 (2014).
37. Janmey, P. A., Winer, J. P. & Weisel, J. W. Fibrin gels and their clinical and bioengineering applications. J. R. Soc. Interface 6, 1-10 (2009).
38. Frantz, C., Stewart, K. M. & Weaver, V. M. The extracellular matrix at a glance. J. Cell Sci. 123, 4195-4200 (2010).
39. Bruekers, S. M. et al. Fibrin-fiber architecture influences cell spreading and differentiation. Cell Adh. Migr. 10, 495-504 (2016).
40. Broedersz, C. P. et al. Measurement of nonlinear rheology of cross-linked biopolymer gels. Soft Matter 6, 4120-4127 (2010).
41. Gard, D. L. & Kirschner, M. W. Microtubule assembly in cytoplasmic extracts of xenopus oocytes and eggs. J. Cell Biol. 105, 2191-2201 (1987).
42. Shah, K., Vasileva, D., Karadaghy, A. & Zustiak, S. P. Development and characterization of polyethylene glycol-carbon nanotube hydrogel composite. J. Mater. Chem. B 3, 7950-7962 (2015).
43. Shin, S. R. et al. Carbon nanotube reinforced hybrid microgels as scaffold materials for cell encapsulation. ACS Nano 6, 362-372 (2012).
44. Lee, C. K. et al. Tough supersoft sponge fibres with tunable stiffness from a DNA self-assembly technique. Angew. Chem. Int. Ed. 48, 5116-5120 (2009).
45. Head, D. A., Levine, A. J. & MacKintosh, F. C. Deformation of cross-linked semiflexible polymer networks. Phys. Rev. Lett. 91, 4 (2003).
46. Onck, P. R., Koeman, T., van Dillen, T. & van der Giessen, E. Alternative explanation of stiffening in cross-linked semiflexible networks. Phys. Rev. Lett. 95, 178102 (2005).
47. Bustamante, C., Marko, J. F., Siggia, E. D. & Smith, S. Entropic elasticity of [lgr]-phage DNA. Science 265, 1599-1600 (1994).
48. Mosesson, M. W. Fibrinogen gamma chain functions. J. Thromb. Haemost. 1, 231-238 (2003).
49. Chen, R. & Doolittle, R. F. Lambda-lambda cross-linking sites in human and bovine fibrin. Biochemistry 10, 4486-4491 (1971).
50. Deshpande, S. R. et al. DNA-responsive polyisocyanopeptide hydrogels with stress-stiffening capacity. Adv. Funct. Mater. 26, 9075-9082 (2016).
51. Calvet, D., Wong, J. Y. & Giasson, S. Rheological monitoring of polyacrylamide gelation: importance of cross-link density and temperature. Macromolecules 37, 7762-7771 (2004).
52. MacKintosh, F. C., Kas, J. & Janmey, P. A. Elasticity of semiflexible biopolymer networks. Phys. Rev. Lett. 75, 4425-4428 (1995).
53. Jansen, K. A., Bacabac, R. G., Piechocka, I. K. & Koenderink, G. H. Cells actively stiffen fibrin networks by generating contractile stress. Biophys. J. 105, 2240-2251 (2013).
54. Koepf, M. et al. Preparation and characterization of non-linear poly(ethylene glycol) analogs from oligo(ethylene glycol) functionalized polyisocyanopeptides. Eur. Polym. J. 49, 1510-1522 (2013).