The Use of Photo-Activatable Materials for the Study of Cell Biomechanics and Mechanobiology

Chapter
Part of the Micro- and Opto-Electronic Materials, Structures, and Systems book series (MOEM)

Abstract

In biomechanical and mechanobiological applications, the ability of photo-activatable materials to change properties in response to a light (photo) stimulus offers key potential advantages over other activatable materials. Not only can photo-activatable materials be used in close contact or proximity to cells and tissues without the cells or tissues being affected by the photostimulus, but photo-activatable materials also offer a level of spatiotemporal control unavailable with many other forms of smart material triggering, such as ambient heating or hydration. This chapter will give an overview of photo-activatable materials that have been developed to study cell biomechanics and mechanobiology and discuss future potential applications for these promising materials.

Keywords

Photo-activatable materials Mechanobiology Cell biomechanics Light Smart Materials Photo-irradiation Shape-memory polymer 

References

  1. 1.
    D.-H. Kim, P.K. Wong, J. Park, A. Levchenko, Y. Sun, Microengineered platforms for cell mechanobiology. Annu. Rev. Biomed. Eng. 11, 203–233 (2009)CrossRefGoogle Scholar
  2. 2.
    J. Wolff, Das Gesetz Der Transformation Der Knochen (A. Hirschwald, Berlin, 1891)Google Scholar
  3. 3.
    J.M. Mitchison, M.M. Swann, The mechanical properties of the cell surface. J. Exp. Biol. 32, 734–750 (1954)Google Scholar
  4. 4.
    R.M. Hochmuth, Micropipette aspiration of living cells. J. Biomech. 33, 15–22 (2000)CrossRefGoogle Scholar
  5. 5.
    K.L. Sung, M.K. Kwan, F. Maldonado, W.H. Akeson, Adhesion strength of human ligament fibroblasts. J. Biomech. Eng. 116, 237–242 (1994)CrossRefGoogle Scholar
  6. 6.
    M. Radmacher, Measuring the elastic properties of biological samples with the AFM. IEEE Eng. Med. Biol. Mag. 16, 47–57 (1997)CrossRefGoogle Scholar
  7. 7.
    H. Haga et al., Elasticity mapping of living fibroblasts by AFM and immunofluorescence observation of the cytoskeleton. Ultramicroscopy 82, 253–258 (2000)CrossRefGoogle Scholar
  8. 8.
    Y.J. Kim et al., A study of compatibility between cells and biopolymeric surfaces through quantitative measurements of adhesive forces. J. Biomater. Sci. Polym. Ed. 14, 1311–1321 (2003)CrossRefGoogle Scholar
  9. 9.
    O. Thoumine, P. Kocian, A. Kottelat, J. Meister, Short-term binding of fibroblasts to fibronectin: Optical tweezers experiments and probabilistic analysis. Eur. Biophys. J. 29, 398–408 (2000)CrossRefGoogle Scholar
  10. 10.
    R.L.Y. Sah et al., Biosynthetic response of cartilage explants to dynamic compression. J. Orthop. Res. 7, 619–636 (1989)CrossRefGoogle Scholar
  11. 11.
    S. Noria et al., Assembly and reorientation of stress fibers drives morphological changes to endothelial cells exposed to shear stress. Am. J. Pathol. 164, 1211–1223 (2004)CrossRefGoogle Scholar
  12. 12.
    R. Yoshida et al., Comb-type grafted hydrogels with rapid deswelling response to temperature changes. Nature 374, 240–242 (1995)CrossRefGoogle Scholar
  13. 13.
    S. Dai, P. Ravi, K.C. Tam, pH-responsive polymers: synthesis, properties and applications. Soft Matter 4, 435 (2008)CrossRefGoogle Scholar
  14. 14.
    X. Yin, A.S. Hoffman, P.S. Stayton, Poly( N-isopropylacrylamide- co -propylacrylic acid) copolymers that respond sharply to temperature and pH. Biomacromolecules 7, 1381–1385 (2006)CrossRefGoogle Scholar
  15. 15.
    Y. Osada, H. Okuzaki, H. Hori, A polymer gel with electrically driven motility. Nature 355, 242–244 (1992)CrossRefGoogle Scholar
  16. 16.
    S. Tasoglu et al., Guided and magnetic self-assembly of tunable magnetoceptive gels. Nat. Commun. 5, 4702 (2014)CrossRefGoogle Scholar
  17. 17.
    B. Yang, W.M. Huang, C. Li, L. Li, Effects of moisture on the thermomechanical properties of a polyurethane shape memory polymer. Polymer (Guildf). 47, 1348–1356 (2006)CrossRefGoogle Scholar
  18. 18.
    H. Yamaguchi et al., Photoswitchable gel assembly based on molecular recognition. Nat. Commun. 3, 603 (2012)CrossRefGoogle Scholar
  19. 19.
    A. Lendlein, H. Jiang, O. Jünger, R. Langer, Light-induced shape-memory polymers. Nature 434, 879–882 (2005)CrossRefGoogle Scholar
  20. 20.
    A.M. Kloxin, A.M. Kasko, C.N. Salinas, K.S. Anseth, Photodegradable hydrogels for dynamic tuning of physical and chemcial properties. Science 324, 59–63 (2009)CrossRefGoogle Scholar
  21. 21.
    J. Nakanishi et al., Photoactivation of a substrate for cell adhesion under standard fluorescence microscopes. J. Am. Chem. Soc. 126, 16314–16315 (2004)CrossRefGoogle Scholar
  22. 22.
    A.M. Kloxin, M.W. Tibbitt, A.M. Kasko, J.A. Fairbairn, K.S. Anseth, Tunable hydrogels for external manipulation of cellular microenvironments through controlled photodegradation. Adv. Mater. 22, 61–66 (2010)CrossRefGoogle Scholar
  23. 23.
    S.J. Bryant, C.R. Nuttleman, K.S. Anseth, Cytocompatibility of UV and visible light photoinitiating systems on cultured NIH/3T3 fibroblasts in vitro. J. Biomater. Sci. Polym. Ed. 11, 439–457 (2000)CrossRefGoogle Scholar
  24. 24.
    Biomaterials Science: An Introduction to Materials and Medicine. (Elsevier Academic Press, New York, 2004)Google Scholar
  25. 25.
    K. Han, W.-N. Yin, J.-X. Fan, F.-Y. Cao, X.-Z. Zhang, Photo-activatable substrates for site-specific differentiation of stem cells. ACS Appl. Mater. Interfaces 7, 23679–23684 (2015)CrossRefGoogle Scholar
  26. 26.
    Y.-H. Gong et al., Photoresponsive ‘smart template’ via host-guest interaction for reversible cell adhesion. Macromolecules 44, 7499–7502 (2011)CrossRefGoogle Scholar
  27. 27.
    D. Liu, Y. Xie, H. Shao, X. Jiang, Using azobenzene-embedded self-assembled monolayers to photochemically control cell adhesion reversibly. Angew. Chem. Int. Ed. 48, 4406–4408 (2009)CrossRefGoogle Scholar
  28. 28.
    I. Tomatsu, K. Peng, A. Kros, Photoresponsive hydrogels for biomedical applications. Adv. Drug Deliv. Rev. 63, 1257–1266 (2011)CrossRefGoogle Scholar
  29. 29.
    G.D. Nicodemus, S.J. Bryant, Cell encapsulation in biodegradable hydrogels for tissue engineering applications. Tissue Eng. Part B Rev. 14, 149–165 (2008)CrossRefGoogle Scholar
  30. 30.
    M.T. Frey, Y. Wang, A photo-modulatable material for probing cellular responses to substrate rigidity. Soft Matter 5, 1918–1924 (2009)CrossRefGoogle Scholar
  31. 31.
    A.M. Rosales, K.M. Mabry, E.M. Nehls, K.S. Anseth, Photoresponsive elastic properties of azobenzene-containing poly(ethylene-glycol)-based hydrogels. Biomacromolecules 16, 798–806 (2015)CrossRefGoogle Scholar
  32. 32.
    M. Behl, A. Lendlein, Shape-memory polymers. Mater. Today 10, 20–28 (2007)CrossRefGoogle Scholar
  33. 33.
    M. Behl, M.Y. Razzaq, A. Lendlein, Multifunctional shape-memory polymers. Adv. Mater. 22, 3388–3410 (2010)CrossRefGoogle Scholar
  34. 34.
    C. Liu, H. Qin, P.T. Mather, Review of progress in shape-memory polymers. J. Mater. Chem. 17, 1543 (2007)CrossRefGoogle Scholar
  35. 35.
    P.T. Mather, X. Luo, I.A. Rousseau, Shape memory polymer research. Annu. Rev. Mater. Res. 39, 445–471 (2009)CrossRefGoogle Scholar
  36. 36.
    A. Lendlein, R. Langer, Biodegradable, elastic shape-memory polymers for potential biomedical applications. Science 296, 1673–1676 (2002)CrossRefGoogle Scholar
  37. 37.
    W. Small IV, P. Singhal, T.S. Wilson, D.J. Maitland, Biomedical applications of thermally activated shape memory polymers. J. Mater. Chem. 20, 3356–3366 (2010)CrossRefGoogle Scholar
  38. 38.
    K.A. Davis, X. Luo, P.T. Mather, J.H. Henderson, Shape memory polymers for active cell culture. J. Vis. Exp. (2011).  https://doi.org/10.3791/2903
  39. 39.
    R.M. Baker, J.H. Henderson, P.T. Mather, Shape memory poly(ε-caprolactone)-co-poly(ethylene glycol) foams with body temperature triggering and two-way actuation. J. Mater. Chem. B 1, 4916–4920 (2013)CrossRefGoogle Scholar
  40. 40.
    L.F. Tseng, P.T. Mather, J.H. Henderson, Shape-memory-actuated change in scaffold fiber alignment directs stem cell morphology. Acta Biomater. 9, 8790–8801 (2013)CrossRefGoogle Scholar
  41. 41.
    H. Lv, J. Leng, Y. Liu, S. Du, Shape-memory polymer in response to solution. Adv. Eng. Mater. 10, 592–595 (2008)CrossRefGoogle Scholar
  42. 42.
    H. Koerner, G. Price, N.A. Pearce, M. Alexander, R.A. Vaia, Remotely actuated polymer nanocomposites—Stress-recovery of carbon-nanotube-filled thermoplastic elastomers. Nat. Mater. 3, 115–120 (2004)CrossRefGoogle Scholar
  43. 43.
    N.G. Sahoo, Y.C. Jung, J.W. Cho, Electroactive shape memory effect of polyurethane composites filled with carbon nanotubes and conducting polymer. Mater. Manuf. Process. 22, 419–423 (2007)CrossRefGoogle Scholar
  44. 44.
    D.J. Maitland, M.F. Metzger, D. Schumann, A. Lee, T.S. Wilson, Photothermal properties of shape memory polymer micro-actuators for treating stroke. Lasers Surg. Med. 30, 1–11 (2002)CrossRefGoogle Scholar
  45. 45.
    W. Small IV, T.S. Wilson, W.J. Benett, J.M. Loge, D.J. Maitland, Laser-activated shape memory polymer intravascular thrombectomy device. Opt. Express 13, 8204–8213 (2005)CrossRefGoogle Scholar
  46. 46.
    Q. Shou, K. Uto, M. Iwanaga, M. Ebara, T. Aoyagi, Near-infrared light-responsive shape-memory poly(ε-caprolactone) films that actuate in physiological temperature range. Polym. J. 46, 492–498 (2014)CrossRefGoogle Scholar
  47. 47.
    Y. Yu, T. Ikeda, Photodeformable polymers: A new kind of promising smart material for micro- and nano-applications. Macromol. Chem. Phys. 206, 1705–1708 (2005)CrossRefGoogle Scholar
  48. 48.
    A. Lendlein, M. Behl, B. Hiebl, C. Wischke, Shape-memory polymers as a technology platform for biomedical applications. Expert Rev. Med. Dev. 7, 357–379 (2010)CrossRefGoogle Scholar
  49. 49.
    K.A. Davis, K.A. Burke, P.T. Mather, J.H. Henderson, Dynamic cell behavior on shape memory polymer substrates. Biomaterials 32, 2285–2293 (2011)CrossRefGoogle Scholar
  50. 50.
    R.M. Baker, L.F. Tseng, M.T. Iannolo, M.E. Oest, J.H. Henderson, Self-deploying shape memory polymer scaffolds for grafting and stabilizing complex bone defects: A mouse femoral segmental defect study. Biomaterials 76, 388–398 (2016)CrossRefGoogle Scholar
  51. 51.
    X. Xu et al., Shape memory RGD-containing networks: Synthesis, characterization, and application in cell culture. Macromol. Symp. 309–310, 162–172 (2011)CrossRefGoogle Scholar
  52. 52.
    P. Yang, R.M. Baker, J.H. Henderson, P.T. Mather, In vitro wrinkle formation via shape memory dynamically aligns adherent cells. Soft Matter 9, 4705–4714 (2013)CrossRefGoogle Scholar
  53. 53.
    R.M. Baker, M.E. Brasch, M.L. Manning, J.H. Henderson, Automated, contour-based tracking and analysis of cell behaviour over long time scales in environments of varying complexity and cell density. J. R. Soc. Interface 11, 20140386 (2014)CrossRefGoogle Scholar
  54. 54.
    M. Ebara et al., Focus on the interlude between topographic transition and cell response on shape-memory surfaces. Polym. (United Kingdom) 55, 5961–5968 (2014)Google Scholar
  55. 55.
    T. Gong et al., The control of mesenchymal stem cell differentiation using dynamically tunable surface microgrooves. Adv. Healthc. Mater. 3, 1608–1619 (2014)CrossRefGoogle Scholar
  56. 56.
    P.Y. Mengsteab et al., Spatiotemporal control of cardiac anisotropy using dynamic nanotopographic cues. Biomaterials 86, 1–10 (2016)CrossRefGoogle Scholar
  57. 57.
    S.A. Turner, J. Zhou, S.S. Sheiko, V.S. Ashby, Switchable micropatterned surface topographies mediated by reversible shape memory. ACS Appl. Mater. Interfaces 6, 8017–8021 (2014)CrossRefGoogle Scholar
  58. 58.
    D.M. Le, M.A. Tycon, C.J. Fecko, V.S. Ashby, Near-infrared activation of semi-crystalline shape memory polymer nanocomposites. J. Appl. Polym. Sci. 130, 4551–4557 (2013)Google Scholar
  59. 59.
    Q. Shou, K. Uto, W.-C. Lin, T. Aoyagi, M. Ebara, Near-infrared-irradiation-induced remote activation of surface shape-memory to direct cell orientations. Macromol. Chem. Phys. 215, 2473–2481 (2014)CrossRefGoogle Scholar
  60. 60.
    C.A. Goubko, S. Majumdar, A. Basak, X. Cao, Hydrogel cell patterning incorporating photocaged RGDS peptides. Biomed. Microdev. 12, 555–568 (2010)CrossRefGoogle Scholar
  61. 61.
    J. Nakanishi et al., Spatiotemporal control of cell adhesion on a self-assembled monolayer having a photocleavable protecting group. Anal. Chim. Acta 578, 100–104 (2006)CrossRefGoogle Scholar
  62. 62.
    J. Nakanishi et al., Spatiotemporal control of migration of single cells on a photoactivatable cell microarray. J. Am. Chem. Soc. 129, 6694–6695 (2007)CrossRefGoogle Scholar
  63. 63.
    J. Nakanishi, H. Nakayama, K. Yamaguchi, A.J. Garcia, Y. Horiike, Dynamic culture substrate that captures a specific extracellular matrix protein in response to light. Sci. Technol. Adv. Mater. 12, 44608 (2011)CrossRefGoogle Scholar
  64. 64.
    Y. Kikuchi et al., Grafting poly(ethylene glycol) to a glass surface via a photocleavable linker for light-induced cell micropatterning and cell proliferation control. Chem. Lett. 37, 1062–1063 (2008)CrossRefGoogle Scholar
  65. 65.
    Y. Kikuchi et al., Arraying heterotypic single cells on photoactivatable cell-culturing substrates. Langmuir 24, 13084–13095 (2008)CrossRefGoogle Scholar
  66. 66.
    S. Kaneko 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. 13, 4051–4059 (2011)CrossRefGoogle Scholar
  67. 67.
    M. Kamimura et al., Facile preparation of a photoactivatable surface on a 96-well plate: A versatile and multiplex cell migration assay platform. Phys. Chem. Chem. Phys. 17, 14159–14167 (2015)CrossRefGoogle Scholar
  68. 68.
    S. Petersen et al., Phototriggering of cell adhesion by caged cyclic RGD peptides. Angew. Chem. Int. Ed. 47, 3192–3195 (2008)CrossRefGoogle Scholar
  69. 69.
    J. Nakanishi et al., Precise patterning of photoactivatable glass coverslip for fluorescence observation of shape-controlled cells. Supramol. Chem. 22, 396–405 (2010)CrossRefGoogle Scholar
  70. 70.
    Y. Shimizu, H. Boehm, K. Yamaguchi, J.P. Spatz, J. Nakanishi, A photoactivatable nanopatterned substrate for analyzing collective cell migration with precisely tuned cell-extracellular matrix ligand interactions. PLoS One 9(3), e91875 (2014).  https://doi.org/10.1371/journal.pone.0091875 CrossRefGoogle Scholar
  71. 71.
    Y. Ohmuro-Matsuyama, Y. Tatsu, Photocontrolled cell adhesion on a surface functionalized with a caged arginine-glycine-aspartate peptide. Angew. Chem. Int. Ed. 47, 7527–7529 (2008)CrossRefGoogle Scholar
  72. 72.
    M.D. Pierschbacher, E. Ruoslahti, Cell attachment activity of fibronectin can be duplicated by small synthetic fragments of the molecule. Nature 309, 30–33 (1984)CrossRefGoogle Scholar
  73. 73.
    G.S. Nowakowski et al., A specific heptapeptide from a phage display peptide library homes to bone marrow and binds to primitive hematopoietic stem cells. Stem Cells 22, 1030–1038 (2004)CrossRefGoogle Scholar
  74. 74.
    F.-Y. Cao, W.-N. Yin, J.-X. Fan, R.-X. Zhuo, X.-Z. Zhang, A novel function of BMHP1 and cBMHP1 peptides to induce the osteogenic differentiation of mesenchymal stem cells. Biomater. Sci. 3, 345–351 (2015)CrossRefGoogle Scholar
  75. 75.
    M.W. Tibbitt, A.M. Kloxin, K.U. Dyamenahalli, K.S. Anseth, Controlled two-photon photodegradation of PEG hydrogels to study and manipulate subcellular interactions on soft materials. Soft Matter 6, 5100 (2010)CrossRefGoogle Scholar
  76. 76.
    B. Wildt, D. Wirtz, P.C. Searson, Programmed subcellular release for studying the dynamics of cell detachment. Nat. Methods 6, 211–213 (2009)CrossRefGoogle Scholar
  77. 77.
    A.J. Ridley et al., Cell migration: Integrating signals from front to back. Science 302, 1704–1709 (2003)CrossRefGoogle Scholar
  78. 78.
    P. Friedl, B. Weigelin, Interstitial leukocyte migration and immune function. Nat. Immunol. 9, 960–969 (2008)CrossRefGoogle Scholar
  79. 79.
    P.L. Ryan, R.A. Foty, J. Kohn, M.S. Steinberg, Tissue spreading on implantable substrates is a competitive outcome of cell-cell vs. cell-substratum adhesivity. Proc. Natl. Acad. Sci. 98, 4323–4327 (2001)CrossRefGoogle Scholar
  80. 80.
    J. Bourget, M. Guillemette, T. Veres, F.A. Auger, L. Germain, Alignment of cells and extracellular matrix within tissue-engineered substitutes. Adv. Biomater. Sci. Biomed. Appl. Ref., 365–390 (2013).  https://doi.org/10.5772/54142
  81. 81.
    C.M. Kirschner, D.L. Alge, S.T. Gould, K.S. Anseth, Clickable, photodegradable hydrogels to dynamically modulate valvular interstitial cell phenotype. Adv. Healthc. Mater. 3, 649–657 (2014)CrossRefGoogle Scholar
  82. 82.
    F. Guilak et al., Control of stem cell fate by physical interactions with the extracellular matrix. Cell Stem Cell 5, 17–26 (2009)CrossRefGoogle Scholar
  83. 83.
    S. Tavella et al., Regulated expression of fibronectin, laminin and related integrin receptors during the early chondrocyte differentiation. J. Cell Sci. 110, 2261–2270 (1997)Google Scholar
  84. 84.
    A.M. Kloxin, J.A. Benton, K.S. Anseth, In situ elasticity modulation with dynamic substrates to direct cell phenotype. Biomaterials 31, 1–8 (2010)CrossRefGoogle Scholar
  85. 85.
    H. Wang, S.M. Haeger, A.M. Kloxin, L.A. Leinwand, K.S. Anseth, Redirecting valvular myofibroblasts into dormant fibroblasts through light-mediated reduction in substrate modulus. PLoS One 7 (2012)Google Scholar
  86. 86.
    C. Yang, M.W. Tibbitt, L. Basta, K.S. Anseth, Mechanical memory and dosing influence stem cell fate. Nat. Mater. 13, 645–652 (2014)CrossRefGoogle Scholar
  87. 87.
    S. Dupont et al., Role of YAP/TAZ in mechanotransduction. Nature 474, 179–183 (2011)CrossRefGoogle Scholar
  88. 88.
    G. Halder, S. Dupont, S. Piccolo, Transduction of mechanical and cytoskeletal cues by YAP and TAZ. Nat. Publ. Gr. 13, 591–600 (2012)Google Scholar
  89. 89.
    M.J. Salierno, A.J. Garcia, A. Del Campo, Photo-activatable surfaces for cell migration assays. Adv. Funct. Mater. 23, 5974–5980 (2013)CrossRefGoogle Scholar
  90. 90.
    R.M. Pope, E.S. Fry, Absorption spectrum (340–640 nm) of pure water. I. Photothermal measurement. Appl. Opt. 36, 8710–8723 (1997)CrossRefGoogle Scholar
  91. 91.
    H. Zhang, H. Xia, Y. Zhao, Optically triggered and spatially controllable shape-memory polymer–gold nanoparticle composite materials. J. Mater. Chem. 22, 845–849 (2012)CrossRefGoogle Scholar

Copyright information

© Springer International Publishing AG, part of Springer Nature 2018

Authors and Affiliations

  1. 1.Syracuse UniversitySyracuseUSA

Personalised recommendations