Skip to main content
SpringerLink
Log in

Investigation of the Effects of Extracellular Osmotic Pressure on Morphology and Mechanical Properties of Individual Chondrocyte

  • Original Paper
  • Published:
Cell Biochemistry and Biophysics Aims and scope Submit manuscript

Abstract

It has been demonstrated that most cells of the body respond to osmotic pressure in a systematic manner. The disruption of the collagen network in the early stages of osteoarthritis causes an increase in water content of cartilage which leads to a reduction of pericellular osmolality in chondrocytes distributed within the extracellular environment. It is therefore arguable that an insight into the mechanical properties of chondrocytes under varying osmotic pressure would provide a better understanding of chondrocyte mechanotransduction and potentially contribute to knowledge on cartilage degeneration. In this present study, the chondrocyte cells were exposed to solutions with different osmolality. Changes in their dimensions and mechanical properties were measured over time. Atomic force microscopy (AFM) was used to apply load at various strain-rates and the force–time curves were logged. The thin-layer elastic model was used to extract the elastic stiffness of chondrocytes at different strain-rates and at different solution osmolality. In addition, the porohyperelastic (PHE) model was used to investigate the strain-rate-dependent responses under the loading and osmotic pressure conditions. The results revealed that the hypo-osmotic external environment increased chondrocyte dimensions and reduced Young’s modulus of the cells at all strain-rates tested. In contrast, the hyper-osmotic external environment reduced dimensions and increased Young’s modulus. Moreover, using the PHE model coupled with inverse FEA simulation, we established that the hydraulic permeability of chondrocytes increased with decreasing extracellular osmolality which is consistent with previous work in the literature. This could be due to a higher intracellular fluid volume fraction with lower osmolality.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5
Fig. 6
Fig. 7
Fig. 8
Fig. 9

Similar content being viewed by others

References

  1. Bao, G., & Suresh, S. (2003). Cell and molecular mechanics of biological materials. Nature Materials, 2, 715–725.

    Article  CAS  PubMed  Google Scholar 

  2. Huang, H., Kamm, R. D., & Lee, R. T. (2004). Cell mechanics and mechanotransduction: pathways, probes, and physiology. American Journal of Physiology-Cell Physiology, 287, C1–C11.

    Article  CAS  PubMed  Google Scholar 

  3. Lim, C. T., Zhou, E. H., & Quek, S. T. (2006). Mechanical models for living cells–a review. Journal of Biomechanics, 39(2), 195–216.

    Article  CAS  PubMed  Google Scholar 

  4. Suresh, S., et al. (2005). Connections between single-cell biomechanics and human disease states: gastrointestinal cancer and malaria. Acta Biomaterialia, 1(1), 15–30.

    Article  CAS  PubMed  Google Scholar 

  5. Guilak, F., & Mow, V. C. (2000). The mechanical environment of the chondrocyte: a biphasic finite element model of cell-matrix interactions in articular cartilage. Journal of Biomechanics, 33(12), 1663–1673.

    Article  CAS  PubMed  Google Scholar 

  6. Oloyede, A., & Broom, N. D. (1991). Is classical consolidation theory applicable to articular cartilage deformation? Clinical Biomechanics, 6(4), 206–212.

    Article  CAS  PubMed  Google Scholar 

  7. Oloyede, A., Flachsmann, R., & Broom, N. D. (1992). The dramatic influence of loading velocity on the compressive response of articular cartilage. Connective Tissue Research, 27, 211–224.

    Article  CAS  PubMed  Google Scholar 

  8. Nguyen, T. D., & Gu, Y. T. (2014). Exploration of mechanisms underlying the strain-rate-dependent mechanical property of single chondrocytes. Applied Physics Letters, 104, 1–5.

    Google Scholar 

  9. Simon, B. R., et al. (1998). Porohyperelastic finite element analysis of large arteries using ABAQUS. ASME Journal of Biomechanical Engineering, 120, 296–298.

    Article  CAS  Google Scholar 

  10. Ayyalasomayajula, A., Vande Geest, J. P., & Simon, B. R. (2010). Porohyperelastic finite element modeling of abdominal aortic aneurysms. Journal of Biomechanical Engineering, 132(10), 104502.

    Article  PubMed  Google Scholar 

  11. Nguyen, T. D., et al. (2015). Microscale consolidation analysis of relaxation behavior of single living chondrocytes subjected to varying strain-rates. Journal of the Mechanical Behavior of Biomedical Materials, 49, 343–354.

    Article  PubMed  Google Scholar 

  12. Nguyen, T. D., & Gu, Y. T. (2014). Determination of strain-rate-dependent mechanical behavior of living and fixed osteocytes and chondrocytes using atomic force microscopy and inverse finite element analysis. Journal of Biomechanical Engineering, 136(10), 101004.

    Article  PubMed  Google Scholar 

  13. Crowley, L. V. (2013). An introduction to human disease: Pathology and pathophysiology correlations. Sudbury: Jones & Bartlett Publishers.

    Google Scholar 

  14. Sarkadi, B., & Parker, J. C. (1991). Activation of ion transport pathways by changes in cell volume. Biochimica et Biophysica Acta (BBA)-Reviews on Biomembranes, 1071(4), 407–427.

    Article  CAS  Google Scholar 

  15. Maroudas, A. (1979). Physicochemical properties of articular cartilage. Adult articular cartilage, 2, 215–290.

    Google Scholar 

  16. Maroudas, A., et al. (1985). Studies of hydration and swelling pressure in normal and osteoarthritic cartilage. Biorheology, 22(2), 159–169.

    CAS  PubMed  Google Scholar 

  17. McGann, L. E., et al. (1988). Kinetics of osmotic water movement in chondrocytes isolated from articular cartilage and applications to cryopreservation. Journal of Orthopaedic Research, 6(1), 109–115.

    Article  CAS  PubMed  Google Scholar 

  18. Ateshian, G. A., Costa, K. D., & Hung, C. T. (2007). A theoretical analysis of water transport through chondrocytes. Biomechanics and Modeling in Mechanobiology, 6, 91–101.

    Article  CAS  PubMed  Google Scholar 

  19. Oswald, E. S., et al. (2008). Dependence of zonal chondrocyte water transport properties on osmotic environment. Cellular and Molecular Bioengineering, 1(4), 339–348.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  20. Oloyede, A., & Broom, N. (1993). Stress-sharing between the fluid and solid components of articular cartilage under varying rates of compression. Connective Tissue Research, 30(2), 127.

    CAS  PubMed  Google Scholar 

  21. Lai, W. M., & Mow, V. C. (1980). Drag-induced compression of articular cartilage during a permeation experiment. Biorheology, 17(1–2), 111–123.

    CAS  PubMed  Google Scholar 

  22. Lai, W. M., Mow, V. C., & Roth, V. (1981). Effects of non-linear strain-dependent permeability and rate of compression on the stress behavior of articular cartilage. Journal of Biomechanical Engineering, 103, 61–66.

    Article  CAS  PubMed  Google Scholar 

  23. Oloyede, A., & Broom, N. D. (1994). The generalized consolidation of articular cartilage: an investigation of its near-physiological response to static load. Connective Tissue Research, 31(1), 75–86.

    Article  CAS  PubMed  Google Scholar 

  24. Moeendarbary, E., et al. (2013). The cytoplasm of living cells behaves as a poroelastic material. Nature Materials, 12(3), 253–261.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  25. Shin, D., & Athanasiou, K. (1997). Biomechanical Properties of the Individual Cell. In 43rd Annual Meeting, Orthopaedic Research Society. San Francisco, California.

  26. Shin, D., & Athanasiou, K. (1999). Cytoindentation for obtaining cell biomechanical properties. Journal of Orthopaedic Research, 17(6), 880–890.

    Article  CAS  PubMed  Google Scholar 

  27. Nguyen, T. D., Oloyede, A., & Gu, Y. T. (2014). Stress relaxation analysis of single chondrocytes using porohyperelastic model based on AFM experiments. Theoretical and Applied Mechanics Letters, 4(5), 054001.

    Article  Google Scholar 

  28. Singh, S., et al. (2008). Characterization of a mesenchymal-like stem cell population from osteophyte tissue. Stem cells and development, 17(2), 245–254.

    Article  CAS  PubMed  Google Scholar 

  29. Logisz, C. C., & Hovis, J. S. (2005). Effect of salt concentration on membrane lysis pressure. Biochimica et Biophysica (BBA)-Biomembranes, 1717(2), 104–108.

    Article  CAS  Google Scholar 

  30. Guilak, F., Erickson, G. R., & Ting-Beall, H. P. (2002). The effects of osmotic stress on the viscoelastic and physical properties of articular chondrocytes. Biophysical Journal, 82, 720–727.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  31. Ladjal, H., et al. (2009). Atomic force microscopy-based single-cell indentation: experimentation and finite element simulation. In: IEEE/RSJ international conference on intelligent robots and systems. St. Louis, MO: Univted States.

  32. Hertz, H. (1881). Ueber den kontakt elastischer koerper. J. fuer die Reine Angewandte Mathematik, 92, 156.

    Google Scholar 

  33. Sneddon, I. N. (1965). The relation between load and penetration in the axisymmetric Boussinesq problem for a punch of arbitrary profile. International Journal of Engineering Science, 3(1), 47–57.

    Article  Google Scholar 

  34. Johnson, K. L. (1987). Contact mechanics. Cambridge: Cambridge University Press.

    Google Scholar 

  35. Dimitriadis, E. K., et al. (2002). Determination of elastic moduli of thin layers of soft material using the atomic force microscope. Biophysical Journal, 82, 2798–2810.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  36. Biot, M. A. (1941). General theory of three-dimensional consolidation. Journal of Applied Physics, 12, 155–164.

    Article  Google Scholar 

  37. Terzaghi, K. (1943). Theoritical soil mechanics. New York: Wiley.

    Book  Google Scholar 

  38. Simon, B. R., & Gaballa, M. A. (1989). Total Lagrangian ‘porohyperelastic’ finite element models of soft tissue undergoing finite strain.pdf. In B. Rubinsky (ed.), 1989 advances in bioengineering (BED-vol 15, pp. 97–98). New York: ASME.

  39. Sherwood, J. D. (1993). Biot poroelasticity of a chemically active shale. Proceedings of the Royal Society of London, Series A: Mathematical and Physical Sciences, 440, 365–377.

    Article  CAS  Google Scholar 

  40. Simon, B. R. (1992). Multiphase poroelastic finite element models for soft tissue structures. Applied Mechanics Reviews, 45(6), 191–219.

    Article  Google Scholar 

  41. Meroi, E. A., Natali, A. N., & Schrefler, B. A. (1999). A porous media approach to finite deformation behaviour in soft tissues. Computer Methods in Biomechanics and Biomedical Engineering, 2, 157–170.

    Article  PubMed  Google Scholar 

  42. Nguyen, T. C. (2005). Mathematical modelling of the biomechanical properties of articular cartilage, in school of mechanical, manufacturing and medical engineering. Brisbane: Queensland University of Technology.

    Google Scholar 

  43. Olsen, S., & Oloyede, A. (2002). A finite element analysis methodology for representing the articular cartilage functional structure. Computer Methods in Biomechanics and Biomedical Engineering, 5(6), 377–386.

    Article  CAS  PubMed  Google Scholar 

  44. Simon, B. R., et al. (1996). A poroelastic finite element formulation including transport and swelling in soft tissue structures. Journal of Biomechanical Engineering, 118, 1–9.

    Article  CAS  PubMed  Google Scholar 

  45. Simon, B. R., et al. (1998). Identification and determination of material properties for porohyperelastic analysis of large arteries. ASME Journal of Biomechanical Engineering, 120, 188–194.

    Article  CAS  Google Scholar 

  46. Kaufmann, M. V. (1996). Porohyperelastic analysis of large arteries including species transport and swelling effects, in mechanical engineering. Tucson: The University of Arizona.

    Google Scholar 

Download references

Acknowledgments

This research was funded by ARC Future Fellowship project (FT100100172) and QUT Postgraduate Research Scholarship. The authors would like to thank Central Analytical Research Facility (CARF) at QUT for experimental support. The work was performed in part at the Queensland node of the Australian National Fabrication Facility (ANFF), a company established under the National Collaborative Research Infrastructure Strategy to provide nano and micro-fabrication facilities for Australia’s researchers. The authors would also thank Ms. Sarah Barns for her suggestions to improve the paper’s quality.

Author information

Authors and Affiliations

  1. School of Chemistry, Physics and Mechanical Engineering, Science and Engineering Faculty, Queensland University of Technology, GPO Box 2434, Brisbane, QLD, 4001, Australia

    Trung Dung Nguyen, Adekunle Oloyede, Sanjleena Singh & YuanTong Gu

Authors
  1. Trung Dung Nguyen
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Adekunle Oloyede
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Sanjleena Singh
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. YuanTong Gu
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to YuanTong Gu.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Nguyen, T.D., Oloyede, A., Singh, S. et al. Investigation of the Effects of Extracellular Osmotic Pressure on Morphology and Mechanical Properties of Individual Chondrocyte. Cell Biochem Biophys 74, 229–240 (2016). https://doi.org/10.1007/s12013-016-0721-1

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s12013-016-0721-1

Keywords

Search

Navigation