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Biophysical Characterization of Bladder Cancer Cells with Different Metastatic Potential

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Abstract

Specific membrane capacitance (SMC) and Young’s modulus are two important parameters characterizing the biophysical properties of a cell. In this work, the SMC and Young’s modulus of two cell lines, RT4 and T24, corresponding to well differentiated (low grade) and poorly differentiated (high grade) urothelial cell carcinoma (UCC), respectively, were quantified using microfluidic and AFM measurements. Quantitative differences in SMC and Young’s modulus values of the high-grade and low-grade UCC cells are, for the first time, reported.

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References

  1. Siegel, R., Naishadham, D., & Jemal, A. (2012). Cancer statistics, 2012. CA: A Cancer Journal for Clinicians, 62, 10–29.

    Article  Google Scholar 

  2. DeGraff, D. J., Clark, P. E., Cates, J. M., et al. (2012). Loss of the urothelial differentiation marker foxa1 is associated with high grade, late stage bladder cancer and increased tumor proliferation. PLoS ONE, 2012(7), e36669.

    Article  Google Scholar 

  3. Jones, T. D., Wang, M., Eble, J. N., et al. (2005). Molecular evidence supporting field effect in urothelial carcinogenesis. Clinical Cancer Research, 11, 6512–6519.

    Article  CAS  PubMed  Google Scholar 

  4. Bubeník, J., Barešová, M., Viklický, V., et al. (1973). Established cell line of urinary bladder carcinoma (t24) containing tumour-specific antigen. International Journal of Cancer, 11, 765–773.

    Article  Google Scholar 

  5. Franks, L., & Rigby, C. (1975). Letter: Hela cells and rt4 cells. Science, 188, 168.

    Article  CAS  PubMed  Google Scholar 

  6. O’Toole, C. M., Tiptaft, R. C., & Stevens, A. (1982). Hla antigen expression on urothelial cells: Detection by antibody-dependent cell-mediated cytotoxicity. International Journal of Cancer, 29, 391–395.

    Article  Google Scholar 

  7. Kim, J., Ji, M., DiDonato, J., et al. (2011). An htert-immortalized human urothelial cell line that responds to anti-proliferative factor. In Vitro Cellular & Developmental Biology—Animal, 47, 2–9.

    Article  CAS  Google Scholar 

  8. Yamada, T., Ueda, T., Shibata, Y., et al. (2010). Trpv2 activation induces apoptotic cell death in human t24 bladder cancer cells: A potential therapeutic target for bladder cancer. Urology, 76, 509.

    Article  PubMed  Google Scholar 

  9. Lokar, M., Perutková, Š., Kralj-Iglič, V., et al. (2009). In A. L. Liu & I. Aleš (Eds.), Advances in planar lipid bilayers and liposomes, vol. 10 (pp. 65–94). Burlington, ON: Academic Press.

    Google Scholar 

  10. van der Heijden, A. G., Jansen, C. F. J., Verhaegh, G., et al. (2004). The effect of hyperthermia on mitomycin-c induced cytotoxicity in four human bladder cancer cell lines. European Urology, 46, 670–674.

    Article  PubMed  Google Scholar 

  11. Bao, J. Z., Davis, C. C., & Schmukler, R. E. (1992). Frequency domain impedance measurements of erythrocytes. Constant phase angle impedance characteristics and a phase transition. Biophysical Journal, 61, 1427–1434.

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  12. Long, Q., & Xing, W. (2006). Detection of the apoptosis of jurkat cell using an electrorotation chip. Frontiers of Biology in China, 1, 208–212.

    Article  Google Scholar 

  13. Arnold, W. M., & Zimmermann, U. (1982). Rotating-field-induced rotation and measurement of the membrane capacitance of single mesophyll-cells of avena-sativa. Zeitschrift Fur Naturforschung Section C: A Journal of Biosciences., 37, 908–915.

    Google Scholar 

  14. Cross, S. E., Jin, Y.-S., Rao, J., et al. (2007). Nanomechanical analysis of cells from cancer patients. Nat Nano., 2, 780–783.

    Article  CAS  Google Scholar 

  15. Gross, L. C. M., Heron, A. J., Baca, S. C., et al. (2011). Determining membrane capacitance by dynamic control of droplet interface bilayer area. Langmuir, 27, 14335–14342.

    Article  CAS  PubMed  Google Scholar 

  16. Iyer, S., Gaikwad, R. M., Subba Rao, V., et al. (2009). Atomic force microscopy detects differences in the surface brush of normal and cancerous cells. Nature Nanotechnology, 2009(4), 389–393.

    Article  Google Scholar 

  17. Discher, D. E., Janmey, P., & Wang, Y.-L. (2005). Tissue cells feel and respond to the stiffness of their substrate. Science, 310, 1139–1143.

    Article  CAS  PubMed  Google Scholar 

  18. Rotsch, C., & Radmacher, M. (2000). Drug-induced changes of cytoskeletal structure and mechanics in fibroblasts: An atomic force microscopy study. Biophysical Journal, 78, 520–535.

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  19. Guck, J., Schinkinger, S., Lincoln, B., et al. (2005). Optical deformability as an inherent cell marker for testing malignant transformation and metastatic competence. Biophysical Journal, 88, 3689–3698.

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  20. Suresh, S., Spatz, J., Mills, J. P., et al. (2005). Connections between single-cell biomechanics and human disease states: Gastrointestinal cancer and malaria. Acta Biomaterialia, 1, 15–30.

    Article  CAS  PubMed  Google Scholar 

  21. Yamaguchi, H., & Condeelis, J. (2007). Regulation of the actin cytoskeleton in cancer cell migration and invasion. Biochimica et Biophysica Acta, 1773, 642–652.

    Article  CAS  PubMed  Google Scholar 

  22. Tan, Q. Y., Ferrier, G. A., Chen, B. K., et al. (2012). Quantification of the specific membrane capacitance of single cells using a microfluidic device and impedance spectroscopy measurement. Biomicrofluidics, 2012, 6.

    Google Scholar 

  23. Kydd, W. L. (1960). Toxicity evaluation of diethylenetriamine. Journal of Dental Research, 39, 46–48.

    Article  CAS  PubMed  Google Scholar 

  24. Kapsimalis, P. (1960). Toxicity studies of cured epoxy resins. Journal of Dental Research, 39, 1072.

    Article  CAS  PubMed  Google Scholar 

  25. Costa, K. D., & Yin, F. C. (1999). Analysis of indentation: Implications for measuring mechanical properties with atomic force microscopy. Journal of Biomechanical Engineering, 121, 462–471.

    Article  CAS  PubMed  Google Scholar 

  26. Harris, A. R., & Charras, G. T. (2011). Experimental validation of atomic force microscopy-based cell elasticity measurements. Nanotechnology, 2011(22), 345102.

    Article  Google Scholar 

  27. Akhremitchev, B. B., & Walker, G. C. (1999). Finite sample thickness effects on elasticity determination using atomic force microscopy. Langmuir, 15, 5630–5634.

    Article  CAS  Google Scholar 

  28. Liu, H. J., Sun, Y., & Simmons, C. A. (2013). Determination of local and global elastic moduli of valve interstitial cells cultured on soft substrates. Journal of Biomechanics. doi:10.1016/j.jbiomech.2013.05.001.

  29. Ohler, B. (2007). Cantilever spring constant calibration using laser Doppler vibrometry. Review of Scientific Instruments, 2007(78), 063701.

    Article  Google Scholar 

  30. Wang, X.-B., Huang, Y., Gascoyne, P. R. C., et al. (1994). Changes in friend murine erythroleukaemia cell membranes during induced differentiation determined by electrorotation. Biochimica et Biophysica Acta, 1193, 330–344.

    Article  CAS  PubMed  Google Scholar 

  31. Kabaso, D., Lokar, M., Kralj-Iglič, V., et al. (2011). Temperature and cholera toxin b are factors that influence formation of membrane nanotubes in rt4 and t24 urothelial cancer cell lines. International Journal of Nanomedicine, 6, 495–509.

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  32. Mazurek, S., Grimm, H., Wilker, S., et al. (1998). Metabolic characteristics of different malignant cancer cell lines. Anticancer Research, 18, 3275–3282.

    CAS  PubMed  Google Scholar 

  33. Ben-Ze’ev, A. (1997). Cytoskeletal and adhesion proteins as tumor suppressors. Current Opinion in Cell Biology, 9, 99–108.

    Article  PubMed  Google Scholar 

  34. Rao, K. M. K., & Cohen, H. J. (1991). Actin cytoskeletal network in aging and cancer. Mutation Research/DNAging, 256, 139–148.

    Article  CAS  Google Scholar 

  35. Gumińska, M., Ignacak, J., Kedryna, T., et al. (1997). Tumor-specific pyruvate kinase isoenzyme m2 involved in biochemical strategy of energy generation in neoplastic cells. Acta Biochimica Polonica, 44, 711–724.

    PubMed  Google Scholar 

  36. Janmey, P. A. (1998). The cytoskeleton and cell signaling: Component localization and mechanical coupling. Physiological Reviews, 78, 763–781.

    CAS  PubMed  Google Scholar 

  37. Glass-Marmor, L., & Beitner, R. (1997). Detachment of glycolytic enzymes from cytoskeleton of melanoma cells induced by calmodulin antagonists. European Journal of Pharmacology, 328, 241–248.

    Article  CAS  PubMed  Google Scholar 

  38. Tsai, M. A., Waugh, R. E., & Keng, P. C. (1998). Passive mechanical behavior of human neutrophils: Effects of colchicine and paclitaxel. Biophysical Journal, 74, 3282–3291.

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  39. Li, Q. S., Lee, G. Y. H., Ong, C. N., et al. (2008). Afm indentation study of breast cancer cells. Biochemical and Biophysical Research Communications, 374, 609–613.

    Article  CAS  PubMed  Google Scholar 

  40. Lekka, M., Laidler, P., Gil, D., et al. (1999). Elasticity of normal and cancerous human bladder cells studied by scanning force microscopy. European Biophysics Journal, 28, 312–316.

    Article  CAS  PubMed  Google Scholar 

  41. Lekka, M., Laidler, P., Ignacak, J., et al. (2001). The effect of chitosan on stiffness and glycolytic activity of human bladder cells. Biochimica et Biophysica Acta, 1540, 127–136.

    Article  CAS  PubMed  Google Scholar 

  42. MacQueen, L. A., Thibault, M., Buschmann, M. D., et al. (2012). Electromechanical deformation of mammalian cells in suspension depends on their cortical actin thicknesses. Journal of Biomechanics, 45, 2797–2803.

    Article  PubMed  Google Scholar 

  43. Ananthakrishnan, R., Guck, J., Wottawah, F., et al. (2006). Quantifying the contribution of actin networks to the elastic strength of fibroblasts. Journal of Theoretical Biology, 242, 502–516.

    Article  CAS  PubMed  Google Scholar 

  44. Laurent, V. M., Fodil, R., Canadas, P., et al. (2003). Partitioning of cortical and deep cytoskeleton responses from transient magnetic bead twisting. Annals of Biomedical Engineering, 31, 1263–1278.

    Article  PubMed  Google Scholar 

  45. Trask, D. K., Band, V., Zajchowski, D. A., et al. (1990). Keratins as markers that distinguish normal and tumor-derived mammary epithelial cells. Proceedings of the National Academy of Sciences, 87, 2319–2323.

    Article  CAS  Google Scholar 

  46. Beil, M., Micoulet, A., von Wichert, G., et al. (2003). Sphingosylphosphorylcholine regulates keratin network architecture and visco-elastic properties of human cancer cells. Nature Cell Biology, 5, 803–811.

    Article  CAS  PubMed  Google Scholar 

Download references

Acknowledgments

This work was financially supported by the Natural Sciences and Engineering Research Council of Canada through a Strategic Projects Grant and the Canada Research Chairs Program.

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Authors and Affiliations

  1. Department of Mechanical and Industrial Engineering, University of Toronto, Toronto, ON, M5S 3G8, Canada

    Haijiao Liu, Qingyuan Tan, Craig A. Simmons & Yu Sun

  2. Institute of Biomaterials and Biomedical Engineering, University of Toronto, Toronto, ON, M5S 3G9, Canada

    Haijiao Liu, Craig A. Simmons & Yu Sun

  3. Department of Laboratory Medicine and Pathobiology, University of Toronto, Toronto, ON, M5G 2C4, Canada

    William R. Geddie

  4. Department of Surgical Oncology, Princess Margaret Hospital, Toronto, ON, M5G 2M9, Canada

    Michael A. S. Jewett

  5. Bioniche Life Sciences Inc, Montreal, QC, H4P 2R2, Canada

    Nigel Phillips & Danbing Ke

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  1. Haijiao Liu
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Corresponding author

Correspondence to Yu Sun.

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Haijiao Liu and Qingyuan Tan contributed equally to this work.

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Liu, H., Tan, Q., Geddie, W.R. et al. Biophysical Characterization of Bladder Cancer Cells with Different Metastatic Potential. Cell Biochem Biophys 68, 241–246 (2014). https://doi.org/10.1007/s12013-013-9702-9

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  • DOI: https://doi.org/10.1007/s12013-013-9702-9

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