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Bridging the Scales to Explore Cellular Adaptation and Remodeling

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Abstract

This short paper presents a multiscale framework to better understand the mechanisms of biological tissue evolution from molecular to tissue scale. For this, a bottom-up strategy is proposed in which mechano-sensitive molecular processes, the evolution of cell architecture and contraction as well as the interaction between cells and the extra-cellular matrix can be integrated in a single framework. Preliminary studies based on this approach suggest that mechano-sensitive feed-back mechanisms at several length-scales may be a key element to understand tissue adaptivity to tis mechanical environment.

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References

  1. Baxter, S. C., Morales, M. O., & Goldsmith, E. C. (2008). Adaptive changes in cardiac fibroblast morphology and collagen organization as a result of mechanical environment. Cell Biochemistry and Biophysics, 51(1), 33–44.

    Article  Google Scholar 

  2. Bell, E., Invarsson, B. & Merrill, C. (1979). Production of a tissue-like structure by contraction of collagen lattices by human fibroblasts of different proliferative potential in vitro. Proceedings of the National Academy of Sciences, 76, 1274–1278.

    Article  Google Scholar 

  3. Bischofs, I. B., & Schwarz, U. S. (2003). Cell organization in soft media due to active mechanosensing. Proceedings of the National Academy of Sciences, 100(16), 9274–9279.

    Article  Google Scholar 

  4. Butcher, D. T., Alliston, T., & Weaver, V. M. (2009). A tense situation: Forcing tumour progression. Nature Reviews Cancer, 9, 108–122.

    Article  Google Scholar 

  5. Chrzanowska-Wodnicka, M., & Burridge, K. (1996). Rhostimulated contractility drives the formation of stress fibers and focal adhesions. Journal of Cell Biology, 133(6), 1403–1415.

    Article  Google Scholar 

  6. Costa, K. D., Lee, E. J., & Holmes, J. W. (2003). Creating alignment and anisotropy in engineered heart tissue: Role of boundary conditions in model three-dimensional culture system. Tissue Engineering, 9(4), 567–577.

    Article  Google Scholar 

  7. Dallon, J. C., & Ehrlich, H. P. (2008). A review of fibroblast-populated collagen lattices. Wound Repair and Regeneration, 16, 472–479.

    Article  Google Scholar 

  8. Discher, D. E., Janmey, P., & Wang, Y. (2005). Tissue cells feel and respond to the stiffness of their substrate. Science, 310(5751), 1139–1143.

    Article  Google Scholar 

  9. Dunn, G. A., & Ebendal, T. (1978). Contact guidance on oriented collagen gels. Experimental Cell Research, 111(2), 475–479.

    Google Scholar 

  10. Eastwood, M., Mudera, V. C., McGrouther, D. A., & Brown, R. A. (1998). Effect of precise mechanical loading on fibroblast populated collagen lattices: Morphological changes. Cell Motility and the Cytoskeleton, 40(1), 13–21.

    Article  Google Scholar 

  11. Ehrlich, H. P., Gabbiani, G., & Meda, P. (2000). Cell coupling modulates the contraction of fibroblast-populated collagen lattices. Journal of Cellular Physiology, 184(1), 86–92.

    Article  Google Scholar 

  12. Geiger, B., & Bershadsky, A. (2002). Exploring the neighborhood: Adhesion-coupled cell mechanosensors. Cell, 110(2), 139–142.

    Article  Google Scholar 

  13. Harris, A. K., Stopak, D., & Warner, P. (1984). Generation of spatially periodic patterns by a mechanical instability: A mechanical alternative to the turing model. Journal of Embryology and Experimental Morphology, 80, 1–20.

    Google Scholar 

  14. Harris, A. K., Stopak, D., & Wild, P. (1980). Fibroblast traction as a mechanism for collagen morphogenesis. Nature, 290, 249–251.

    Article  Google Scholar 

  15. Harris, A. K., Wild, P., & Stopak, D. (1980). Silicone rubber substrata: A new wrinkle in the study of cell locomotion. Science, 208(4440), 177–179.

    Article  Google Scholar 

  16. Haston, W. S., Shields, J. M., & Wilkinson, P. C. (1983). The orientation of fibroblasts and neutrophils on elastic substrata. Experimental Cell Research, 146(1), 117–126.

    Article  Google Scholar 

  17. Hill, A. V. (1938). The heat of shortening and the dynamic constant of muscles. Proceedings of the Royal Society of London, 126(843), 136–195.

    Google Scholar 

  18. Huang, S., & Ingber, D. E. (1999). The structural and mechanical complexity of cell-growth control. Nature Cell Biology, 1(5), E131–E138.

    Google Scholar 

  19. Lambert, A., Nusgens, B. V., & Lapiere, M. (1998). Mechano-sensing and mechano-reaction of soft connective tissue cells. Advances in Space Research, 21(8/9), 1081–1091.

    Article  Google Scholar 

  20. Makale, M. (2007). Cellular mechanobiology and cancer metastasis. Birth Defects Research (Part C), 81, 329–343.

    Article  Google Scholar 

  21. Martin, P. (1997). Wound healing: Aiming for perfect skin regeneration. Science, 276, 75–81.

    Article  Google Scholar 

  22. Paszek, M., Zahir, N., Johnson, K., Lakins, J., Rozenberg, G., Gefen, A., et al. (2005). Tensional homeostasis and the malignant phenotype. Cancer Cell, 8, 241–254.

    Article  Google Scholar 

  23. Pelham, R. J., & Wang, Y. L. (1997). Cell locomotion and focal adhesions are regulated by substrate flexibility. Proceedings of the National Academy of Sciences of the United States of America, 94, 13661–13665.

  24. Rome, L. C., Cook, C., Syme, D. A., Connaughton, M. A., Ashley-Ross, M., Klimov, B., et al. (1999). Trading force for speed: Why superfast crossbridge kinetics leads to superlow forces. Proceedings of the National Academy of Sciences, 96, 5826–5831.

    Article  Google Scholar 

  25. Sawhney, R. K., & Howard, J. (2002). Slow local movements of collagen fibers by fibroblasts drive the rapid global self organization of collagen gels. The Journal of Cell Biology, 157(6), 1083–1091.

    Article  Google Scholar 

  26. Semesh, T., Geiger, B., Bershadsky, A. D., & Kozlov, M. (2005). Focal adhesions as mechanosensors: a physical mechanism. Proceedings of the National Academy of Sciences, 102(35), 12383–12388.

    Article  Google Scholar 

  27. Smith, R. C., Cande, W. Z., Craig, R., Tooth, P. J., Scholey, J. M., & Kendrick-Jones, J. (1983). Regulation of myosin filament assembly by light-chain phosphorylation. Philosophical Transactions of the Royal Society of London, 302(1108),73–82.

    Article  Google Scholar 

  28. Solon, J., Levental, I., Sengupta, K., Georges, P. C., & Janmey, P. A. (2007). Fibroblast adaptation and stiffness matching to soft elastic substrates. Biophysical journal, 93(12), 4453–4461.

    Google Scholar 

  29. Sun, D. N., Gu, W. Y., Guo, X. E., Lai, W. M., & Mow, V. C. (2008). A mixed finite element formulation of triphasic mechano-electrochemical theory for charged, hydrated biological soft tissues. International Journal for Numerical Methods in Engineering, 45, 1375–1402.

    Article  Google Scholar 

  30. Tamariz, E., & Grinnell, F. (2002). Modulation of fibroblast morphology and adhesion during collagen matrix remodeling. Molecular Biology of the Cell, 13, 3915–3929.

    Article  Google Scholar 

  31. Vernerey, F. J. (2011). Advances in cell mechanics, on the application of multiphasic theories to the problem of cell-substrate mechanical interactions. New York: Springer.

    Google Scholar 

  32. Vernerey, F. J., & Farsad, M. (2011). A constrained mixture approach to mechano-sensing and force generation in contractile cells. Journal of the Mechanical Behavior of Biomedical Materials. doi:10.1016/j.jmbbm.2011.05.022.

  33. Vernerey, F. J., & Farsad, M. (2011). An eulerian/xfem formulation for the large deformation of cortical cell membrane. Computer Methods in Biomechanics and Biomedical Engineering, 14(5), 433–445.

    Article  Google Scholar 

  34. Weiss, P., & Garber, B. (1952). Shape and movement of mesenchyme cells as functions of the physical structure of the medium contributions to a quantitative morphology. Proceedings of the National Academy of Sciences of the United States of America, 38(3), 264–280.

  35. Weiss, P., & Garber, B. (1952). Shape and movement of mesenchyme cells as functions of the physical struture of the medium contributions to a quantitative morphology. Proceedings of the National Academy of Sciences, 38, 264–280.

    Article  Google Scholar 

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Acknowledgement

FJV gratefully acknowledges the University of Colorado CRCW Seed Grant in support of this research.

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Correspondence to Franck J. Vernerey.

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Vernerey, F.J., Foucard, L. & Farsad, M. Bridging the Scales to Explore Cellular Adaptation and Remodeling. BioNanoSci. 1, 110–115 (2011). https://doi.org/10.1007/s12668-011-0013-6

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  • DOI: https://doi.org/10.1007/s12668-011-0013-6

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