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Modeling the mechanics of cells in the cell-spreading process driven by traction forces

Yuqiang Fang and King W. C. Lai*

  • Department of Mechanical and Biomedical Engineering, City University of Hong Kong, Tat Chee Avenue, Hong Kong

  • *kinglai@cityu.edu.hk
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Phys. Rev. E 93, 042404 – Published 7 April, 2016

DOI: https://doi.org/10.1103/PhysRevE.93.042404

Abstract

Mechanical properties of cells and their mechanical interaction with the extracellular environments are main factors influencing cellular function, thus indicating the progression of cells in different disease states. By considering the mechanical interactions between cell adhesion molecules and the extracellular environment, we developed a cell mechanical model that can characterize the mechanical changes in cells during cell spreading. A cell model was established that consisted of various main subcellular components, including cortical cytoskeleton, nuclear envelope, actin filaments, intermediate filaments, and microtubules. We demonstrated the structural changes in subcellular components and the changes in spreading areas during cell spreading driven by traction forces. The simulation of nanoindentation tests was conducted by integrating the indenting force to the cell model. The force-indentation curve of the cells at different spreading states was simulated, and the results showed that cell stiffness increased with increasing traction forces, which were consistent with the experimental results. The proposed cell mechanical model provides a strategy to investigate the mechanical interactions of cells with the extracellular environments through the adhesion molecules and to reveal the cell mechanical properties at the subcellular level as cells shift from the suspended state to the adherent state.

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References (68)

  1. D. Di Carlo, J. Lab. Autom. 17, 32 (2012).
  2. N. Wang, J. P. P. Butler, and D. E. E. Ingber, Science 260, 1124 (1993).
  3. D. A. Fletcher and R. D. Mullins, Nature 463, 485 (2010).
  4. K. J. Van Vliet, G. Bao, and S. Suresh, Acta Mater. 51, 5881 (2003).
  5. M. Plodinec, M. Loparic, C. A. Monnier, E. C. Obermann, R. Zanetti-Dallenbach, P. Oertle, J. T. Hyotyla, U. Aebi, M. Bentires-Alj, R. Y. H. Lim, and C.-A. Schoenenberger, Nat. Nanotechnol. 7, 757 (2012).
  6. L. Trichet, J. Le Digabel, R. J. Hawkins, S. R. K. Vedula, M. Gupta, C. Ribrault, P. Hersen, R. Voituriez, and B. Ladoux, Proc. Natl. Acad. Sci. USA 109, 6933 (2012).
  7. F. Chowdhury, S. Na, D. Li, Y.-C. Poh, T. S. Tanaka, F. Wang, and N. Wang, Nat. Mater. 9, 82 (2010).
  8. A. Vaziri and A. Gopinath, Nat. Mater. 7, 15 (2008).
  9. G. T. Charras and M. A. Horton, Biophys. J. 83, 858 (2002).
  10. C. M. Nelson, R. P. Jean, J. L. Tan, W. F. Liu, N. J. Sniadecki, A. A. Spector, and C. S. Chen, Proc. Natl. Acad. Sci. USA 102, 11594 (2005).
  11. F. P. T. Baaijens, W. R. Trickey, T. A. Laursen, and F. Guilak, Ann. Biomed. Eng. 33, 494 (2005).
  12. J. P. Mills, L. Qie, M. Dao, C. T. Lim, and S. Suresh, Mech. Chem. Biosyst. 1, 169 (2004).
  13. D. Stamenović and D. E. Ingber, Biomech. Model. Mechanobiol. 1, 95 (2002).
  14. M. F. Coughlin and D. Stamenović, Biophys. J. 84, 1328 (2003).
  15. K. Wang and D. Sun, J. Biomech. 45, 1900 (2012).
  16. Y. Ujihara, M. Nakamura, H. Miyazaki, and S. Wada, Ann. Biomed. Eng. 38, 1530 (2010).
  17. J. Li, M. Dao, C. T. Lim, and S. Suresh, Biophys. J. 88, 3707 (2005).
  18. I. V. Pivkin and G. E. Karniadakis, Phys. Rev. Lett. 101, 118105 (2008).
  19. L. Lamalice, F. Le Boeuf, and J. Huot, Circ. Res. 100, 782 (2007).
  20. N. Q. Balaban, U. S. Schwarz, D. Riveline, P. Goichberg, G. Tzur, I. Sabanay, D. Mahalu, S. Safran, A. Bershadsky, L. Addadi, and B. Geiger, Nat. Cell Biol. 3, 466 (2001).
  21. V. Vogel and M. Sheetz, Nat. Rev. Mol. Cell Biol. 7, 265 (2006).
  22. J. M. Dong, T. Leung, E. Manser, and L. Lim, J. Biol. Chem. 273, 22554 (1998).
  23. M.-C. Kim, C. Kim, L. Wood, D. Neal, R. D. Kamm, and H. H. Asada, Integr. Biol. 4, 1386 (2012).
  24. B. Maurin, P. Cañadas, H. Baudriller, P. Montcourrier, and N. Bettache, J. Biomech. 41, 2036 (2008).
  25. M. Dao, J. Li, and S. Suresh, Mater. Sci. Eng. C 26, 1232 (2006).
  26. F. Rivero, B. Köppel, B. Peracino, S. Bozzaro, F. Siegert, C. J. Weijer, M. Schleicher, R. Albrecht, and A. A. Noegel, J. Cell Sci. 109, 2679 (1996).
  27. V. M. Laurent, E. Planus, R. Fodil, and D. Isabey, Biorheology 40, 235 (2003).
  28. K. A. Barbee, P. F. Davies, and R. Lal, Circ. Res. 74, 163 (1994).
  29. A. R. Bausch, F. Ziemann, A. A. Boulbitch, K. Jacobson, and E. Sackmann, Biophys. J. 75, 2038 (1998).
  30. S. Deguchi, K. Maeda, T. Ohashi, and M. Sato, J. Biomech. 38, 1751 (2005).
  31. N. Caille, O. Thoumine, Y. Tardy, and J. J. Meister, J. Biomech. 35, 177 (2002).
  32. M. M. Nava, M. T. Raimondi, and R. Pietrabissa, Biomech. Model. Mechanobiol. 13, 929 (2014).
  33. A. J. Maniotis, C. S. Chen, and D. E. Ingber, Proc. Natl. Acad. Sci. USA 94, 849 (1997).
  34. J. D. Pajerowski, K. N. Dahl, F. L. Zhong, P. J. Sammak, and D. E. Discher, Proc. Natl. Acad. Sci. 104, 15619 (2007).
  35. J. R. Sims, S. Karp, and D. E. Ingber, J. Cell Sci. 103, 1215 (1992).
  36. K. D. Costa, W. J. Hucker, and F. C. P. Yin, Cell Motil. Cytoskeleton 52, 266 (2002).
  37. D. E. Discher, D. H. Boal, and S. K. Boey, Biophys. J. 75, 1584 (1998).
  38. J. F. Marko and E. D. Siggia, Macromolecules 28, 8759 (1995).
  39. O. Chaudhuri, S. H. Parekh, and D. A. Fletcher, Nature 445, 295 (2007).
  40. N. Mücke, L. Kreplak, R. Kirmse, T. Wedig, H. Herrmann, U. Aebi, and J. Langowski, J. Mol. Biol. 335, 1241 (2004).
  41. A. Vaziri, H. Lee, and M. R. K. Mofrad, J. Mater. Res. 21, 2126 (2006).
  42. M. Dao, C. T. Lim, and S. Suresh, J. Mech. Phys. Solids 51, 2259 (2003).
  43. B. Wickstead and K. Gull, J. Cell Biol. 194, 513 (2011).
  44. N. Wang and D. Stamenović, Am. J. Physiol. - Cell Physiol. 279, C188 (2000).
  45. F. Gittes, J. Cell Biol. 120, 923 (1993).
  46. C. P. Brangwynne, F. C. MacKintosh, S. Kumar, N. A. Geisse, J. Talbot, L. Mahadevan, K. K. Parker, D. E. Ingber, and D. A. Weitz, J. Cell Biol. 173, 733 (2006).
  47. C. T. Skau and C. M. Waterman, Annu. Rev. Biophys. 44, 285 (2015).
  48. M. Jean, Comput. Methods Appl. Mech. Eng. 177, 235 (1999).
  49. S. E. Cross, Y.-S. Jin, J. Rao, and J. K. Gimzewski, Nat. Nanotechnol. 2, 780 (2007).
  50. C. Rotsch and M. Radmacher, Biophys. J. 78, 520 (2000).
  51. M. Radmacher, M. Fritz, C. M. Kacher, J. P. Cleveland, and P. K. Hansma, Biophys. J. 70, 556 (1996).
  52. T. T. Hormel, S. Q. Kurihara, M. K. Brennan, M. C. Wozniak, and R. Parthasarathy, Phys. Rev. Lett. 112, 188101 (2014).
  53. Y. Li, A. F. Bushnell, C.-M. Lee, L. S. Perlmutter, and S. K.-F. Wong, Brain Res. 738, 196 (1996).
  54. Y. Fang, C. Y. Y. Iu, C. N. P. Lui, Y. Zou, C. K. M. Fung, H. W. Li, N. Xi, K. K. L. Yung, and K. W. C. Lai, Sci. Rep. 4, 7074 (2014).
  55. N. P. B. Au, Y. Fang, N. Xi, K. W. C. Lai, and C. H. E. Ma, Nanomed. Nanotech. Biol. Med. 10, 1323 (2014).
  56. J. L. Tan, J. Tien, D. M. Pirone, D. S. Gray, K. Bhadriraju, and C. S. Chen, Proc. Natl. Acad. Sci. USA 100, 1484 (2003).
  57. L. Luo, Annu. Rev. Cell Dev. Biol. 18, 601 (2002).
  58. J. P. Califano and C. A. Reinhart-King, Cell. Mol. Bioeng. 3, 68 (2010).
  59. C. M. Lo, H. B. Wang, M. Dembo, and Y. L. Wang, Biophys. J. 79, 144 (2000).
  60. L. K. Wrobel, T. R. Fray, J. E. Molloy, J. J. Adams, M. P. Armitage, and J. C. Sparrow, Cell Motil. Cytoskeleton 52, 82 (2002).
  61. D. E. Ingber, Annu. Rev. Physiol. 59, 575 (1997).
  62. J. Sleep, D. Wilson, R. Simmons, and W. Gratzer, Biophys. J. 77, 3085 (1999).
  63. A. Kis, S. Kasas, B. Babić, A. J. Kulik, W. Benoît, G. A. D. Briggs, C. Schönenberger, S. Catsicas, and L. Forró, Phys. Rev. Lett. 89, 248101 (2002).
  64. Y. M. Sirenko, M. A. Stroscio, and K. W. Kim, Phys. Rev. E 53, 1003 (1996).
  65. T. D. Pollard and M. S. Mooseker, J. Cell Biol. 88, 654 (1981).
  66. I. Schwaiger, A. Kardinal, M. Schleicher, A. A. Noegel, and M. Rief, Nat. Struct. Mol. Biol. 11, 81 (2003).
  67. M. L. Gardel, J. H. Shin, F. C. MacKintosh, L. Mahadevan, P. Matsudaira, and D. A. Weitz, Science 304, 1301 (2004).
  68. J. S. Palmer and M. C. Boyce, Acta Biomater. 4, 597 (2008).

Outline

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Phys. Rev. E 93, 042404– Published 7 April, 2016
  • Received 4 June 2015
  • Revised 9 March 2016

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