Advertisement

Annals of Biomedical Engineering

, Volume 46, Issue 7, pp 1026–1037 | Cite as

Experimental Verification of the Elastic Formula for the Aspirated Length of a Single Cell Considering the Size and Compressibility of Cell During Micropipette Aspiration

  • YongSheng Li
  • Jing Chen
  • LiLi Wang
  • Yuan Guo
  • JiLing Feng
  • WeiYi Chen
Article

Abstract

In this study, an aspiration system for elastic spheres was developed to verify the approximate elastic formula for the aspirated length of a single solid-like cell undergoing micropipette aspiration (MPA), which was obtained in our previous study by theoretical analysis and numerical simulation. Using this system, foam silicone rubber spheres with different diameters and mechanical properties were aspirated in a manner similar to the MPA of single cells. Comparisons between the approximate elastic formula and aspiration experiments of spheres indicated that the predictions of the formula agreed with the experimental results. Additionally, combined with the MPA data of rabbit chondrocytes, differences in terms of the elastic parameters derived from the half-space model, incompressible sphere model, and compressible sphere model were explored. The results demonstrated that the parameter ξ (ξ = R/a, where R is the radius of the cell and a is the inner radius of the micropipette) and Poisson’s ratio significantly influenced the determination of the elastic modulus and bulk modulus of the cell. This work developed for the first time an aspiration system of elastic spheres to study the elastic responses of the MPA of a single cell and provided new evidence supporting the use of the approximate elastic formula to determine cellular elastic parameters from the MPA data.

Keywords

Cell mechanics Micropipette aspiration Cell model Mechanical properties Experimental verification 

Notes

Acknowledgments

Supports from the National Natural Science Foundation of China (Grant Nos. 11572213, 11632013, 11702184 and 11472185), the Natural Science Foundation of Shanxi Province, China (Grant No. 2014021013), and the Youth Funds of Taiyuan University of Technology (No. 2013T079) are acknowledged.

Conflict of interest

None of the authors have any competing financial interests related to this paper.

References

  1. 1.
    Ahmad, I. L., and M. R. Ahmad. Trends in characterizing single cell’s stiffness properties. Micro Nano Syst. Lett. 2:8, 2014.  https://doi.org/10.1186/s40486-014-0008-5.CrossRefGoogle Scholar
  2. 2.
    Baaijens, F. P. T., W. R. Trickey, T. A. Laursen, and F. Guilak. Large deformation finite element analysis of micropipette aspiration to determine the mechanical properties of the chondrocyte. Ann. Biomed. Eng. 33:494–501, 2005.CrossRefPubMedGoogle Scholar
  3. 3.
    Bidhendi, A. J., and R. K. Korhonen. A finite element study of micropipette aspiration of single cells: Effect of compressibility. Comput. Math. Methods Med. 2012.  https://doi.org/10.1155/2012/192618.PubMedGoogle Scholar
  4. 4.
    Boudou, T., J. Ohayon, Y. Arntz, G. Finet, C. Picart, and P. Tracqui. An extended modeling of the micropipette aspiration experiment for the characterization of the Young’s modulus and Poisson’s ratio of adherent thin biological samples: numerical and experimental studies. J. Biomech. 39:1677–1685, 2006.CrossRefPubMedGoogle Scholar
  5. 5.
    Charras, G. T., P. P. Lehenkari, and M. A. Horton. Atomic force microscopy can be used to mechanically stimulate osteoblasts and evaluate cellular strain distributions. Ultramicroscopy 86:85–95, 2001.CrossRefPubMedGoogle Scholar
  6. 6.
    Chaudhuri, O., and D. J. Mooney. Stem-cell differentiation: anchoring cell-fate cues. Nat. Mater. 11:568–569, 2012.CrossRefPubMedGoogle Scholar
  7. 7.
    Fung, Y. C. Biomechanics: Mechanical Properties of Living Tissues. New York: Springer, p. 788, 1993.CrossRefGoogle Scholar
  8. 8.
    Galbraith, C. G., and M. P. Sheetz. Forces on adhesive contacts affect cell function. Curr. Opin. Cell Biol. 10:566–571, 1998.CrossRefPubMedGoogle Scholar
  9. 9.
    Guilak, F., G. Erickson, and H. Ting-Beall. The effects of osmotic stress on the viscoelastic and physical properties of articular chondrocytes. Biophys. J. 82:720–727, 2002.CrossRefPubMedPubMedCentralGoogle Scholar
  10. 10.
    Guz, N., M. Dokukin, V. Kalaparthi, and I. Sokolov. If cell mechanics can be described by elastic modulus: study of different models and probes used in indentation experiments. Biophy. J. 107:564–575, 2014.CrossRefGoogle Scholar
  11. 11.
    Haider, M. A., and F. Guilak. An axisymmetric boundary integral model for incompressible linear viscoelasticity: application to the micropipette aspiration contact problem. ASME J. Biomech. Eng. 122:236–244, 2000.CrossRefGoogle Scholar
  12. 12.
    Haider, M. A., and F. Guilak. An axisymmetric boundary integral model for assessing elastic cell properties in the micropipette aspiration contact problem. ASME J. Biomech. Eng. 124:586–595, 2002.CrossRefGoogle Scholar
  13. 13.
    Hochmuth, R. M. Micropipette aspiration of living cells. J. Biomech. 33:15–22, 2000.CrossRefPubMedGoogle Scholar
  14. 14.
    Hu, W. J., H. Chen, K. Zhang, and X. Chen. Effect of porosity on the properties of open cell silicone rubber foam materials. China Rubber Ind. 45:647–651, 1998; ((In Chinese)).Google Scholar
  15. 15.
    Jones, W. R., H. P. Ting-Beall, G. M. Lee, S. S. Kelly, R. M. Hochmuch, and F. Guilak. Alterations in the Young’s modulus and volumetric properties of chondrocytes isolated from normal and osteoarthritic human cartilage. J. Biomech. 32:119–127, 1999.CrossRefPubMedGoogle Scholar
  16. 16.
    Khani, M.-M., M. Tafazzoli-Shadpour, Z. Goli-Malekabadi, and N. Haghighipour. Mechanical characterization of human mesenchymal stem cells subjected to cyclic uniaxial strain and TGF-β1. J. Mech. Behav. Biomed. 43:18–25, 2015.CrossRefGoogle Scholar
  17. 17.
    Kinney, J. H., G. W. Marshall, S. J. Marshall, and D. L. Haupt. Three-dimensional imaging of large compressive deformations in elastomeric foams. J. Appl. Polym. Sci. 80:1746–1755, 2001.CrossRefGoogle Scholar
  18. 18.
    Lee, G. Y. H., and C. T. Lim. Biomechanics approaches to studying human diseases. Trends Biotechnol. 25:111–118, 2007.CrossRefPubMedGoogle Scholar
  19. 19.
    Lekka, M., and P. Laidler. Applicability of AFM in cancer detection. Nat. Nanotechnol. 4:72–73, 2009.CrossRefPubMedGoogle Scholar
  20. 20.
    Li, Y. S. Study on the mechanical models for micropipette aspiration of cells. Thesis for the Doctor Degree of Taiyuan University of Technology, pp. 51–52, 2014 (In Chinese).Google Scholar
  21. 21.
    Li, Y. S., and W. Y. Chen. Finite element analysis of micropipette aspiration considering finite size and compressibility of cells. Sci. China Phys. Mech. 56:2208–2215, 2013.CrossRefGoogle Scholar
  22. 22.
    Li, J., M. Dao, and S. Suresh. Spectrin-level modeling of the cytoskeleton and optical tweezers stretching of the erythrocyte. Biophys. J. 88:3707–3719, 2005.CrossRefPubMedPubMedCentralGoogle Scholar
  23. 23.
    Loh, O., A. Vaziri, and H. D. Espinosa. The potential of MEMS for advancing experiments and modeling in cell mechanics. Exp. Mech. 49:105–124, 2010.CrossRefGoogle Scholar
  24. 24.
    Maksym, G. N., B. Fabry, J. P. Butler, D. Navajas, D. J. Tschumperlin, J. D. Laporte, and J. J. Fredberg. Mechanical properties of cultured human airway smooth muscle cells from 0.05 to 0.4 Hz. J. Appl. Physiol. 89:1619–1632, 2000.CrossRefPubMedGoogle Scholar
  25. 25.
    Mills, J. P., L. Qie, M. Dao, C. T. Lim, and S. Suresh. Nonlinear elastic and viscoelastic deformation of the human red blood cell with optical tweezers. Mech. Chem. Biosyst. 1:169–180, 2004.PubMedGoogle Scholar
  26. 26.
    Nash, G. B., E. O’Brien, and J. A. Dormandy. Abnormalities in the mechanical properties of red blood cells caused by Plasmodium falciparum. Blood. 74:855–861, 1989.PubMedGoogle Scholar
  27. 27.
    Pachenari, M., S. M. Seyedpour, M. Janmaleki, S. B. Shayan, S. Taranejoo, and H. Hosseinkhani. Mechanical properties of cancer cytoskeleton depend on actin filaments to microtubules content: investigating different grades of colon cancer cell lines. J. Biomech. 47:373–379, 2014.CrossRefPubMedGoogle Scholar
  28. 28.
    Paszek, M. J., N. Zahir, and V. M. Weaver. Tensional homeostasis and the malignant phenotype. Cancer Cell. 8:241–254, 2005.CrossRefPubMedGoogle Scholar
  29. 29.
    Roduit, C., S. Sekatski, G. Dietler, S. Catsicas, F. Lafont, and S. Kasas. Stiffness to mography by atomic force microscopy. Biophys. J. 97:674–677, 2009.CrossRefPubMedPubMedCentralGoogle Scholar
  30. 30.
    Sato, M., D. P. Theret, L. T. Wheeler, N. Ohshima, and R. M. Nerem. Application of the micropipette technique to the measurement of cultured porcine aortic endothelial cell viscoelastic properties. ASME J. Biomech. Eng. 112:263–268, 1990.CrossRefGoogle Scholar
  31. 31.
    Seyedpour, S. M., M. Pachenari, M. Janmaleki, M. Alizadeh, and H. Hosseinkhani. Effects of an antimitotic drug on mechanical behaviours of the cytoskeleton in distinct grades of colon cancer cells. J. Biomech. 48:1172–1178, 2015.CrossRefPubMedGoogle Scholar
  32. 32.
    Sliogeryte, K., S. D. Thorpe, Z. Wang, C. L. Thompson, N. Gavara, and M. M. Knight. Differential effects of LifeAct-GFP and actin-GFP on cell mechanics assessed using micropipette aspiration. J. Biomech. 49:310–317, 2016.CrossRefPubMedPubMedCentralGoogle Scholar
  33. 33.
    Theret, D. P., M. J. Levesque, M. Sato, R. M. Nerem, and L. T. Wheeler. The application of a homogeneous half-space model in the analysis of endothelial cell micropipette measurements. ASME J. Biomech. Eng. 110:190–199, 1988.CrossRefGoogle Scholar
  34. 34.
    Timoshenko, S. P., and J. N. Goodier. Theory of Elasticity (3rd edition). New York: McGraw-Hill Book Company, 1970.Google Scholar
  35. 35.
    Vogel, V., and M. Sheetz. Local force and geometry sensing regulate cell functions. Nat. Rev. Mol. Cell Biol. 7:265–275, 2006.CrossRefPubMedGoogle Scholar
  36. 36.
    Wang, Z., A. K. T. Wann, C. L. Thompson, A. Hassen, W. Wang, and M. M. Knight. IFT88 influences chondrocyte actin organization and biomechanics. Osteoarthr. Cartil. 24:544–554, 2016.CrossRefPubMedPubMedCentralGoogle Scholar
  37. 37.
    Xie, J. J., W. J. Hu, and J. L. Tao. Quasi-static experimental study on the energy dissipation performance of foam rubber based on quasi static. China Meas. Test. Technol. 38:29–32, 2012; ((In Chinese)).Google Scholar
  38. 38.
    Zhang, Q. Y. Mechanical properties of chondrocytes from normal and osteoarthritic rabbit knee cartilage. Dissertation for the Master Degree of Taiyuan University of Technology, 2006 (In Chinese)Google Scholar
  39. 39.
    Zhang, Q. Y., X. H. Wang, X. C. Wei, and W. Y. Chen. Characterization of viscoelastic properties of normal and osteoarthritic chondrocytes in experimental rabbit model. Osteoarthr. Cartil. 16:837–840, 2008.CrossRefPubMedGoogle Scholar
  40. 40.
    Zhou, E. H., C. T. Lim, and S. T. Quek. Finite element simulation of the micropipette aspiration of a living cell undergoing large viscoelastic deformation. Mech. Adv. Mater. Struct. 12:501–512, 2005.CrossRefGoogle Scholar

Copyright information

© Biomedical Engineering Society 2018

Authors and Affiliations

  • YongSheng Li
    • 1
  • Jing Chen
    • 1
  • LiLi Wang
    • 2
  • Yuan Guo
    • 2
  • JiLing Feng
    • 3
  • WeiYi Chen
    • 2
  1. 1.Department of Mechanics and Engineering ScienceTaiyuan University of TechnologyTaiyuanChina
  2. 2.Institute of Applied Mechanics and Biomedical EngineeringTaiyuan University of TechnologyTaiyuanChina
  3. 3.Department of Design, Manufacture, and Engineering ManagementUniversity of StrathclydeGlasgowScotland, UK

Personalised recommendations