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Investigation of effect of fullerenol on viscoelasticity properties of human hepatocellular carcinoma by AFM-based creep tests

Published online by Cambridge University Press:  19 June 2017

Xinyao Zhu Open the ORCID record for Xinyao Zhu [Opens in a new window] ,
Zuobin Wang  and
Xianping Liu
Xinyao Zhu
Affiliation:
School of Engineering, University of Warwick, Coventry CV4 7AL, U.K.
Zuobin Wang
Affiliation:
International Research Centre for Nano Handling and Manufacturing of China, Changchun University of Science and Technology, Changchun 130022, China
Xianping Liu*
Affiliation:
School of Engineering, University of Warwick, Coventry CV4 7AL, U.K.
*
a) Address all correspondence to this author. e-mail: [email protected]
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Abstract

Cellular elasticity is frequently measured to investigate the biomechanical effects of drug treatment, diseases, and aging. In light of the cellular viscosity property exhibited by filament actin networks, this study investigates the viscoelasticity alterations of the human hepatocellular carcinoma (SMMC-7721) cell subjected to fullerenol treatment by means of creep tests realized by atomic force microscopy indentation. An SMMC-7721 cell was first modeled as a sphere and then as a flattened layer with finite thickness. Both Sneddon’s solutions and the Dimitriadis model have been modified to adapt to the viscoelastic situation, which are used to fit the same indentation depth–time curves obtained by creep tests. We find that the SMMC-7721 cell’s creep behavior is well described by the two modified models and the divergence of parameters determined by the two models is justified. By fullerenol treatment, the SMMC-7721 cell exhibits a significant decrease of elastic modulus and viscosity, which is presumably due to the disruption of actin filaments. This work represents a new attempt to understand the alternation of the viscoelastic properties of cancerous cells under the treatment of fullerenol, which has the significance of comprehensively elucidating the biomechanical effects of anticancer agents (such as fullerenol) on cancer cells.

Keywords

viscoelasticitynanoindentationbiofilm
Type
Articles
Information
Journal of Materials Research , Volume 32 , Issue 13 , 14 July 2017 , pp. 2521 - 2531
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Copyright
Copyright © Materials Research Society 2017 

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Footnotes

Contributing Editor: Jinju Chen

References

REFERENCES

Chen, Z., Ma, L., Liu, Y., and Chen, C.: Applications of functionalized fullerenes in tumor theranostics. Theranostics 2, 238 (2012).CrossRefGoogle ScholarPubMed
Partha, R. and Conyers, J.L.: Biomedical applications of functionalized fullerene-based nanomaterials. Int. J. Nanomed. 4, 261 (2009).Google ScholarPubMed
Bosi, S., Da, R.T., Spalluto, G., and Prato, M.: Fullerene derivatives: An attractive tool for biological applications. Eur. J. Med. Chem. 38, 913 (2003).CrossRefGoogle ScholarPubMed
Li, J., Takeuchi, A., Ozawa, M., Li, X.H., Saigo, K., and Kitazawa, K.: C-60 fullerol formation catalyzed by quaternary ammonium hydroxides. J. Chem. Soc., Chem. Commun. 23, 1784 (1993).CrossRefGoogle Scholar
Jin, J., Dong, Y., Wang, Y., Xia, L., and Gu, W.: Fullerenol Nanoparticles with structural activity induce variable intracellular actin filament morphologies. J. Biomed. Nanotechnol. 12, 1234 (2016).CrossRefGoogle ScholarPubMed
Zhou, Y.T., Guy, G.R., and Low, B.C.: BNIP-Sa induces cell rounding and apoptosis by displacing p50RhoGAP and facilitating RhoA activation via its unique motifs in the BNIP-2 and Cdc42GAP homology domain. Oncogene 25, 2393 (2006).CrossRefGoogle ScholarPubMed
Johnson-Lyles, D.N., Peifley, K., Lockett, S., Neun, B.W., Hansen, M., Clogston, J., Stern, S.T., and McNeil, S.E.: Fullerenol cytotoxicity in kidney cells is associated with cytoskeleton disruption, autophagic vacuole accumulation, and mitochondrial dysfunction. Toxicol. Appl. Pharmacol. 248, 249 (2010).CrossRefGoogle ScholarPubMed
Zhu, J.D., Ji, Z.Q., W, J., Sun, R.H., Zhang, X., Gao, Y., Sun, H., Liu, Y., Wang, Z., Li, A., Ma, J., Wang, T., Jia, G., and Gu, Y.: Tumor-inhibitory effect and immunomodulatory activity of fullerol C60(OH) x . Small. 4, 1168 (2008).CrossRefGoogle ScholarPubMed
Lu, L.H., Lee, Y.T., Chen, H.W., Long, Y.C., and Huang, H.C.: The possible mechanisms of the antiproliferative effect of fullerenol, polyhydroxylated C60, on vascular smooth muscle cells. Br. J. Pharmacol. 123, 1097 (1998).CrossRefGoogle ScholarPubMed
Paraskar, A., Soni, S., Mashelkar, R.A., and Sengupta, S.: Fullerenol–cytotoxic conjugates for cancer chemotherapy. ACS Nano 3, 2505 (2009).Google Scholar
Iyer, S., Gaikwad, R.M., Subba Rao, V., Woodworth, C.D., and Sokolov, I.: Atomic force microscopy detects differences in the surface brush of normal and cancerous cells. Nat. Nanotechnol. 4, 389 (2009).CrossRefGoogle ScholarPubMed
Hawkins, T., Mirigian, M., Yasar, M.S., and Ross, J.L.: Mechanics of microtubules. J. Biomech. 43, 23 (2010).CrossRefGoogle ScholarPubMed
Mrdanović, J., Solajić, S., Bogdanović, V., Stankov, K., Bogdanovicć, G., and Djordjevic, A.: Effects of fullerenol C60(OH)24 on the frequency of micronuclei and chromosome aberrations in CHO-K1 cells. Mutat. Res., Genet. Toxicol. Environ. Mutagen. 680, 25 (1999).CrossRefGoogle Scholar
Siamantouras, E., Hills, C.E., Younis, M.Y., Squire, P.E., and Liu, K.K.: Quantitative investigation of calcimimetic R568 on beta cell adhesion and mechanics using AFM single-cell force spectroscopy. FEBS Lett. 588, 1178 (2014).CrossRefGoogle ScholarPubMed
Thomas, G., Burnham, N.A., Camesano, T.A., and Wen, Q.: Measuring the mechanical properties of living cells using atomic force microscopy. J. Visualized Exp. 76, e50497 (2013).Google Scholar
Rianna, C. and Radmacher, M.: Cell mechanics as a marker for diseases: Biomedical applications of AFM. AIP Conf. Proc. 1760, 020057 (2016).CrossRefGoogle Scholar
Starodubtseva, M.N.: Mechanical properties of cells and ageing. Ageing Res. Rev. 10, 16 (2011).CrossRefGoogle ScholarPubMed
Mahaffy, R.E., Park, S., Gerde, E., Käs, J., and Shih, C.K.: Quantitative analysis of the viscoelastic properties of thin regions of fibroblasts using atomic force microscopy. Biophys. J. 86, 1777 (2004).CrossRefGoogle ScholarPubMed
Bremmell, K.E., Evans, A., and Prestidge, C.A.: Deformation and nano-rheology of red blood cells: An AFM investigation. Colloids Surf., B 50, 43 (2006).CrossRefGoogle ScholarPubMed
Zhao, M. and Srinivasan, C.: Rate- and depth-dependent nanomechanical behavior of individual living Chinese hamster ovary cells probed by atomic force microscopy. J. Mater. Res. 21, 1906 (2006).CrossRefGoogle Scholar
Li, Q.S., Lee, G.Y.H., Ong, C.N., and Lim, C.T.: AFM indentation study of breast cancer cells. Biochem. Biophys. Res. Commun. 374, 609 (2008).CrossRefGoogle ScholarPubMed
Darling, E.M., Zauscher, S., and Guilak, F.: Viscoelastic properties of zonal articular chondrocytes measured by atomic force microscopy. Osteoarthritis Cartilage 14, 571 (2006).CrossRefGoogle ScholarPubMed
Koay, E.J., Shieh, A.C., and Athanasiou, K.A.: Creep indentation of single cells. J. Biomech. Eng. 125, 334 (2003).CrossRefGoogle ScholarPubMed
Leipzig, N.D. and Athanasiou, K.A.: Unconfined creep compression of chondrocytes. J. Biomech. 38, 77 (2005).CrossRefGoogle ScholarPubMed
Palmer, A., Mason, T.G., Xu, J., Kuo, S.C., and Wirtz, D.: Diffusing wave spectroscopy microscopy of actin filament networks. Biophys. J. 76, 1063 (1999).CrossRefGoogle Scholar
Ketene, A.N., Roberts, P.C., Shea, A.A., Schmelz, E.M., and Agah, M.: Actin filaments play a primary role for structural integrity and viscoelastic response in cells. Integr. Biol. 4, 540 (2012).CrossRefGoogle ScholarPubMed
Ngan, A.H.W. and Tang, B.: Response of power-law-viscoelastic and time-dependent materials to rate jumps. J. Mater. Res. 24, 853 (2009).CrossRefGoogle Scholar
Tang, B. and Ngan, A.H.W.: Nanoindentation using an atomic force microscope. Philos. Mag. 91, 1329 (2011).CrossRefGoogle Scholar
Tang, B. and Ngan, A.H.W.: Investigation of viscoelastic properties of amorphous selenium near glass transition using depth-sensing indentation. Soft Mater. 2, 125 (2004).CrossRefGoogle Scholar
Dimitriadis, E.K., Horkay, F., Maresca, J., Kachar, B., and Chadwick, R.S.: Determination of elastic moduli of thin layers of soft material using the atomic force microscope. Biophys. J. 82, 2798 (2002).CrossRefGoogle ScholarPubMed
Zhu, X.Y., Zhang, N., Wang, Z.B., and Liu, X.P.: Investigation of work of adhesion of biological cell (human hepatocellular carcinoma) by AFM nanoindentation. J. Micro-Bio Rob. 11, 47 (2016).CrossRefGoogle ScholarPubMed
Neumann, T.: Determining the elastic modulus of biological samples using atomic force microscopy. JPK Instruments Application Report (2008).Google Scholar
Liu, Y., Wang, Z.B., and Wang, X.Y.: AFM-based study of fullerenol (C60(OH)24)-induced changes of elasticity in living SMCC-7721 cells. J. Mech. Behav. Biomed. Mater. 45, 65 (2015).CrossRefGoogle Scholar
King, R.B.: Elastic analysis of some punch problems for a layered medium. Int. J. Solids Struct. 23, 1657 (1987).CrossRefGoogle Scholar
Antunes, J.M., Menezes, L.F., and Fernandes, J.V.: Three-dimensional numerical simulation of Vickers indentation tests. Int. J. Solids Struct. 43, 784 (2006).CrossRefGoogle Scholar
Ward, I.M. and Hadley, D.W.: An introduction to the mechanical properties of solid polymers, 2nd ed. (John Wiley & Sons Ltd, New York, 1993).Google Scholar
Findley, W.N., Lai, J.S., and Onaran, K.: Creep and Relaxation of Nonlinear Viscoelastic Materials with an Introduction to Linear Viscoelasticity, 3rd ed. (Dover Publications, Inc, New York, 1989).Google Scholar
Hills, C.E., Younis, M.Y., Bennett, J., Siamantouras, E., Liu, K.K., and Squires, P.E.: Calcium-sensing receptor activation increases cell–cell adhesion and β-cell function. Cell. Physiol. Biochem. 30, 575 (2012).CrossRefGoogle ScholarPubMed
Chen, J.: Nanobiomechanics of living cells: A review. J. R. Soc., Interface 4, 20130055 (2014).Google ScholarPubMed
Sneddon, I.N.: The relation between load and penetration in the axisymmetric Boussinesq problem for a punch of arbitrary profile. Int. J. Eng. Sci. 3, 47 (1965).CrossRefGoogle Scholar
Lee, E.H. and Radok, J.R.M.: The contact problem for viscoelastic bodies. J. Appl. Mech. 27, 438 (1960).CrossRefGoogle Scholar
Ting, T.C.T.: The contact stresses between a rigid indenter and a viscoelastic half-space. J. Appl. Mech. 33, 845 (1966).CrossRefGoogle Scholar
Yu, H.L., Li, Z., and Wang, Q.J.: Viscoelastic-adhesive contact modeling: Application to the characterization of the viscoelastic behavior of materials. Mech. Mater. 60, 55 (2013).CrossRefGoogle Scholar
Chen, J. and Lu, G.: Finite element modelling of nanoindentation based methods for mechanical properties of cells. J. Biomech. 45, 2810 (2012).CrossRefGoogle ScholarPubMed
Chen, J.: Understanding the nanoindentation mechanisms of a microsphere for biomedical applications. J. Phys. D: Appl. Phys. 46, 495303 (2013).CrossRefGoogle Scholar
Sanchez-Adams, J., Wilusz, R.E., and Guilak, F.: Atomic force microscopy reveals regional variations in the micromechanical properties of the pericellular and extracellular matrices of the meniscus. J. Orthop. Res. 31, 1218 (2013).CrossRefGoogle ScholarPubMed
Gavara, N. and Chadwick, R.S.: Determination of the elastic moduli of thin samples and adherent cells using conical atomic force microscope tips. Nat. Nanotechnol. 7, 733 (2012).CrossRefGoogle ScholarPubMed
Vadillo-Rodriguez, V., Beveridge, T.J., and Dutcher, J.R.: Surface viscoelasticity of individual Gram-negative bacterial cells measured using atomic force microscopy. J. Bacteriol. 190, 4225 (2008).CrossRefGoogle ScholarPubMed
Zhou, Z.L., Ngan, A.H.W., Tang, B., and Wang, A.X.: Reliable measurement of elastic modulus of cells by nanoindentation in an atomic force microscope. J. Mech. Behav. Biomed. Mater. 8, 134 (2012).CrossRefGoogle Scholar
Sirghi, L., Ponti, J., Broggi, F., and Rossi, F.: Probing elasticity and adhesion of live cells by atomic force microscopy indentation. Eur. Biophys. J. 37, 935 (2008).CrossRefGoogle ScholarPubMed
Zhu, X.Y., Siamantouras, E., Liu, K.K., and Liu, X.P.: Determination of work of adhesion of biological cell under AFM bead indentation. J. Mech. Behav. Biomed. Mater. 56, 77 (2015).CrossRefGoogle ScholarPubMed