Magnetically actuated cell-laden microscale hydrogels for probing strain-induced cell responses in three dimensions

NPG Asia Materials

Volumn 8, Issue 1, 2016, Pages

  Li, Yuhui ^a   Huang, Guoyou ^a   Gao, Bin ^a,b   Li, Moxiao ^a   Genin, Guy M ^a,c,d   Lu, Tian Jian ^a   Xu, Feng ^a  

^a XI'AN JIAOTONG UNIVERSITY   (China)

^b FOURTH MILITARY MEDICAL UNIVERSITY   (China)

^c WASHINGTON UNIVERSITY SCHOOL OF MEDICINE   (United States)

^d WASHINGTON UNIVERSITY IN ST LOUIS   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CYTOLOGY; HYDROGELS; STRAIN; TISSUE HOMEOSTASIS;

CULTURE ENVIRONMENTS; EXTRACELLULAR MATRICES; HOMOGENEOUS DEFORMATION; MECHANOTRANSDUCTION; PATHOPHYSIOLOGICAL; SATURATION BEHAVIOR; THREEDIMENSIONAL (3-D); UNDER EXTERNAL MAGNETIC FIELD;

CELLS;

EID: 85096744406     PISSN: 18844049     EISSN: 18844057     Source Type: Journal    
DOI: 10.1038/am.2015.148     Document Type: Article

References (40)

1. Fletcher, D. A. & Mullins, R. D. Cell mechanics and the cytoskeleton. Nature 463, 485–492 (2010).
2. Elson, E. L. & Genin, G. M. The role of mechanics in actin stress fiber kinetics. Exp. Cell. Res. 319, 2490–2500 (2013).
3. Li, Y. H., Huang, G. Y., Zhang, X. H., Wang, L., Du, Y. A., Lu, T. J. & Xu, F. Engineering cell alignment in vitro. Biotechnol. Adv. 32, 347–365 (2014).
4. Wang, L., Li, Y. H., Huang, G. Y., Zhang, X. H., Pingguan-Murphy, B., Gao, B., Lu, T. J. & Xu, F. Hydrogel-based methods for engineering cellular microenvironment with spatiotemporal gradients. Crit. Rev. Biotechnol. 0, 1–13 (2015).
5. Cui, Y., Hameed, F. M., Yang, B., Lee, K., Pan, C. Q., Park, S. & Sheetz, M. Cyclic stretching of soft substrates induces spreading and growth. Nat. Commun. 6, 6333 (2015).
6. Discher, D. E., Janmey, P. & Wang, Y. L. Tissue cells feel and respond to the stiffness of their substrate. Science 310, 1139–1143 (2005).
7. Livne, A., Bouchbinder, E. & Geiger, B. Cell reorientation under cyclic stretching. Nat. Commun. 5, 3938 (2014).
8. Fu, J., Wang, Y. K., Yang, M. T., Desai, R. A., Yu, X., Liu, Z. & Chen, C. S. Mechanical regulation of cell function with geometrically modulated elastomeric substrates. Nat. Meth. 7, 733–736 (2010).
9. Trepat, X., Wasserman, M. R., Angelini, T. E., Millet, E., Weitz, D. A., Butler, J. P. & Fredberg, J. J. Physical forces during collective cell migration. Nat. Phys. 5, 426–430 (2009).
10. Cukierman, E., Pankov, R., Stevens, D. R. & Yamada, K. M. Taking cell–matrix adhesions to the third dimension. Science 294, 1708–1712 (2001).
11. Bellas, E. & Chen, C. S. Forms, forces, and stem cell fate. Curr. Opin. Cell. Biol. 31, 92–97 (2014).
12. Hassan, W., Dong, Y. & Wang, W. Encapsulation and 3D culture of human adiposederived stem cells in an in situ crosslinked hybrid hydrogel composed of PEG-based hyperbranched copolymer and hyaluronic acid. Stem. Cell. Res. Ther. 4, 32 (2013).
13. Legant, W. R., Pathak, A., Yang, M. T., Deshpande, V. S., McMeeking, R. M. & Chen, C. S. Microfabricated tissue gauges to measure and manipulate forces from 3D microtissues. Proc. Natl. Acad. Sci. USA 106, 10097–10102 (2009).
14. Legant, W. R., Miller, J. S., Blakely, B. L., Cohen, D. M., Genin, G. M. & Chen, C. S. Measurement of mechanical tractions exerted by cells in three-dimensional matrices. Nat. Meth. 7, 969–971 (2010).
15. Rodriguez, M. L., McGarry, P. J. & Sniadecki, N. J. Review on cell mechanics: experimental and modeling approaches. Appl. Mech. Rev. 65, 1–41 (2013).
16. Wakatsuki, T., Kolodney, M. S., Zahalak, G. I. & Elson, E. L. Cell mechanics studied by a reconstituted model tissue. Biophys. J. 79, 2353–2368 (2000).
17. Foolen, J., Deshpande, V. S., Kanters, F. M. & Baaijens, F. P. The influence of matrix integrity on stress-fiber remodeling in 3D. Biomaterials 33, 7508–7518 (2012).
18. Sniadecki, N. J., Anguelouch, A., Yang, M. T., Lamb, C. M., Liu, Z., Kirschner, S. B., Liu, Y., Reich, D. H. & Chen, C.S. Magnetic microposts as an approach to apply forces to living cells. Proc. Natl. Acad. Sci. USA 104, 14553–14558 (2007).
19. Zhao, R. G., Boudou, T., Wang, W. G., Chen, C. S. & Reich, D. H. Decoupling cell and matrix mechanics in engineered microtissues using magnetically actuated microcantilevers. Adv. Mater. 25, 1699–1705 (2013).
20. Zhao, R. G., Chen, C. S. & Reich, D. H. Force-driven evolution of mesoscale structure in engineered 3D microtissues and the modulation of tissue stiffening. Biomaterials 35, 5056–5064 (2014).
21. Li, Y. H., Poon, C. T., Li, M., Pingguan-Murphy, B., Lu, T. J. & Xu, F. Chinese-noodleinspired muscle myofiber fabrication. Adv. Funct. Mater. 25, 5999–6008 (2015).
22. Krishnamurthy, G., Itoh, A., Bothe, W., Swanson, J. C., Kuhl, E., Karlsson, M., Craig Miller, D. & Ingels, N. B. Jr. Stress–strain behavior of mitral valve leaflets in the beating ovine heart. J. Biomech. 42, 1909–1916 (2009).
23. Guccione, J. M., Costa, K. D. & McCulloch, A. D. Finite element stress analysis of left ventricular mechanics in the beating dog heart. J. Biomech. 28, 1167–1177 (1995).
24. Scott, A., Khan, K. M., Heer, J., Cook, J. L., Lian, O. & Duronio, V. High strain mechanical loading rapidly induces tendon apoptosis: an ex vivo rat tibialis anterior model. Br. J. Sports. Med. 39, e25 (2005).
25. Appleby-Thomas, G. J., Hazell, P. J., Sheldon, R. P., Stennett, C., Hameed, A. & Wilgeroth, J. M. The high strain-rate behaviour of selected tissue analogues. J. Mech. Behav. Biomed. Mater. 33, 124–135 (2014).
26. Prevost, T. P., Balakrishnan, A., Suresh, S. & Socrate, S. Biomechanics of brain tissue. Acta Biomater. 7, 83–95 (2011).
27. 4 nanoparticles and their biomedical applications. Biomaterials 26, 729–738 (2005).
28. Nichol, J. W., Koshy, S. T., Bae, H., Hwang, C. M., Yamanlar, S. & Khademhosseini, A. Cell-laden microengineered gelatin methacrylate hydrogels. Biomaterials 31, 5536–5544 (2010).
29. Tai, H., Howard, D., Takae, S., Wang, W., Vermonden, T. & Hennink, W. E. Photo-cross-linked hydrogels from thermoresponsive PEGMEMA-PPGMA-EGDMA copolymers containing multiple methacrylate groups: mechanical property, swelling, protein release, and cytotoxicity. Biomacromolecules 10, 2895–2903 (2009).
30. Fairbanks, B. D., Schwartz, M. P., Bowman, C. N. & Anseth, K. S. Photoinitiated polymerization of PEG-diacrylate with lithium phenyl-2,4,6-trimethylbenzoylphosphinate: polymerization rate and cytocompatibility. Biomaterials 30, 6702–6707 (2009).
31. Schmittgen, T. D. & Livak, K. J. Analyzing real-time PCR data by the comparative C (T) method. Nat. Protoc. 3, 1101–1108 (2008).
32. Xu, F., Inci, F., Mullick, O., Gurkan, U. A., Sung, Y., Kavaz, D., Li, B., Denkbas, E. B. & Demirci, U. Release of magnetic nanoparticles from cell-encapsulating biodegradable nanobiomaterials. ACS Nano 6, 6640–6649 (2012).
33. Huang, G. Y., Zhang, X. H., Xiao, Z. P., Zhang, Q. C., Zhou, J. X., Xu, F. & Lu, T. J. Cellencapsulating microfluidic hydrogels with enhanced mechanical stability. Soft Matter 8, 10687–10694 (2012).
34. Nakayama, A., Kakugo, A., Gong, J. P., Osada, Y., Takai, M., Erata, T. & Kawano, S. High mechanical strength double-network hydrogel with bacterial cellulose. Adv. Funct. Mater. 14, 1124–1128 (2004).
35. Li, Y. H., Huang, G. Y., Zhang, X. H., Li, B. Q., Chen, Y. M., Lu, T. L., Lu, T. J. & Xu, F. Magnetic hydrogels and their potential biomedical applications. Adv. Funct. Mater. 23, 660–672 (2013).
36. Schaffer, E., Norrelykke, S. F. & Howard, J. Surface forces and drag coefficients of microspheres near a plane surface measured with optical tweezers. Langmuir 23, 3654–3665 (2007).
37. Lee, S. L., Nekouzadeh, A., Butler, B., Pryse, K. M., Mc Connaughey, W. B., Nathan, A. C., Legant, R.W.,Schaefer, M.P.,Pless, B.R., Elson, E.L.& Genin, G.M. Physicallyinduced cytoskeleton remodeling of cells in three-dimensional culture. PloS ONE 7, e45512 (2012).
38. Yeh, J., Ling, Y., Karp, J. M. & Khademhosseini, A. Micromolding of shape-controlled, harvestable cell-laden hydrogels. Biomaterials 27, 5391–5398 (2006).
39. Du, Y., Lo, E. & Khademhosseini, A. Directed assembly of cell-laden microgels for fabrication of 3D tissue constructs. Proc. Natl. Acad. Sci. USA 105, 9522–9527 (2008).
40. Madden, L., Juhas, M., Kraus, W. E., Truskey, G. A. & Bursac, N. Bioengineered human myobundles mimic clinical responses of skeletal muscle to drugs. eLife 4, e04885 (2015).