Skip to main content
Log in

Comparative study of non-invasive force and stress inference methods in tissue

  • Regular Article
  • Published:
The European Physical Journal E Aims and scope Submit manuscript

Abstract

In the course of animal development, the shape of tissue emerges in part from mechanical and biochemical interactions between cells. Measuring stress in tissue is essential for studying morphogenesis and its physical constraints. For that purpose, a possible new approach is force inference (up to a single prefactor) from cell shapes and connectivity. It is non-invasive and can provide space-time maps of stress in a whole tissue, unlike existing methods. To validate this approach, three force-inference methods, which differ in their approach of treating indefiniteness in an inverse problem between cell shapes and forces, were compared. Tests using two artificial and two experimental data sets consistently indicate that our Bayesian force inference, by which cell-junction tensions and cell pressures are simultaneously estimated, performs best in terms of accuracy and robustness. Moreover, by measuring the stress anisotropy and relaxation, we cross-validated the force inference and the global annular ablation of tissue, each of which relies on different prefactors. A practical choice of force-inference methods in different systems of interest is discussed.

Graphical abstract

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

Access this article

Subscribe and save

Springer+ Basic
€32.70 /Month
  • Get 10 units per month
  • Download Article/Chapter or eBook
  • 1 Unit = 1 Article or 1 Chapter
  • Cancel anytime
Subscribe now

Buy Now

Price includes VAT (Finland)

Instant access to the full article PDF.

Similar content being viewed by others

Explore related subjects

Discover the latest articles, news and stories from top researchers in related subjects.

References

  1. T. Lecuit, P.F. Lenne, Nat. Rev. Mol. Cell Biol. 8, 633 (2007).

    Article  Google Scholar 

  2. T. Lecuit, P.F. Lenne, E. Munro, Annu. Rev. Cell Dev. Biol. 27, 157 (2011).

    Article  Google Scholar 

  3. D. Bilder, S.L. Haigo, Dev. Cell 22, 12 (2012).

    Article  Google Scholar 

  4. S. Eaton, F. Jülicher, Curr. Opin. Genet. Dev. 21, 747 (2012).

    Article  Google Scholar 

  5. K.E. Kasza, J.A. Zallen, Curr. Opin. Cell Biol. 23, 30 (2011).

    Article  Google Scholar 

  6. M. Nahmad, A.D. Lander, Curr. Opin. Genet. Dev. 21, 726 (2011).

    Article  Google Scholar 

  7. O. Wartlick, M. Gonzalez-Gaitan, Curr. Opin. Genet. Dev. 21, 690 (2011).

    Article  Google Scholar 

  8. F. Graner, Y. Sawada, J. Theor. Biol. 164, 477 (1993).

    Article  Google Scholar 

  9. N.B. Ouchi, J.A. Glazier, J.P. Rieu, A. Upadhyaya, Y. Sawada, Physica A 329, 451 (2003).

    Article  MathSciNet  ADS  MATH  Google Scholar 

  10. J. Käfer, T. Hayashi, A.F.M. Marée, R. Carthew, F. Graner, Proc. Natl. Acad. Sci. U.S.A. 104, 18549 (2007).

    Article  ADS  Google Scholar 

  11. R. Farhadifar, J.C. Roper, B. Aigouy, S. Eaton, F. Jülicher, Curr. Biol. 17, 2095 (2007).

    Article  Google Scholar 

  12. M. Krieg, Y. Arboleda-Estudillo, P.-H. Puech, J. Käfer, F. Graner, D.J. Müller, C.-P. Heisenberg, Nat. Cell. Biol. 10, 429 (2008).

    Article  Google Scholar 

  13. S. Hilgenfeldt, S. Erisken, R.W. Carthew, Proc. Natl. Acad. Sci. U.S.A. 105, 907 (2008).

    Article  ADS  Google Scholar 

  14. H. Honda, N. Motosugi, T. Nagai, M. Tanemura, T. Hiiragi, Development 135, 1407 (2008).

    Article  Google Scholar 

  15. M. Rauzi, P. Verant, T. Lecuit, P.F. Lenne, Nat. Cell Biol. 10, 1401 (2008).

    Article  Google Scholar 

  16. B. Aigouy, R. Farhadifar, D.B. Staple, A. Sagner, J.C. Roper, F. Jülicher, S. Eaton, Cell 142, 773 (2010).

    Article  Google Scholar 

  17. D.B. Staple, R. Farhadifar, J.-C. Röper, B. Aigouy, S. Eaton, F. Jülicher, Eur. Phys. J. E 33, 117 (2010).

    Article  Google Scholar 

  18. Y. Mao, A.L. Tournier, P.A. Bates, J.E. Gale, N. Tapon, B.J. Thompson, Genes Dev. 25, 131 (2011).

    Article  Google Scholar 

  19. F. Bosveld, I. Bonnet, B. Guirao, S. Tlili, Z. Wang, A. Petitalot, R. Marchand, P.-L. Bardet, P. Marcq, F. Graner, Y. Bellaïche, Science 336, 724 (2012).

    Article  ADS  Google Scholar 

  20. J. Ophir, I. Cespedes, B. Garra, H. Ponnekanti, Y. Huang, N. Maklad, Eur. J. Ultrasound 3, 49 (1996).

    Article  Google Scholar 

  21. U. Nienhaus, T. Aegerter-Wilmsen, C.M. Aegerter, Mech. Dev. 126, 942 (2009).

    Article  Google Scholar 

  22. N. Desprat, W. Supatto, P. Pouille, E. Beaurepaire, E. Farge, Dev. Cell 15, 470 (2008).

    Article  Google Scholar 

  23. V. Fleury, A. Al-Kilani, O.P. Boryskina, A.J.M. Cornelissen, T. Nguyen, M. Unbekandt, L. Leroy, G. Baffet, F.L. Noble, O. Sire, E. Lahaye, V. Burgaud, Phys. Rev. E 81, 021920 (2010).

    Article  ADS  Google Scholar 

  24. A. Peaucelle, S. Braybrook, L.L. Guillou, E. Bron, C. Kuhlemeier, H. Höfte, Curr. Biol. 21, 1720 (2011).

    Article  Google Scholar 

  25. D.T. Tambe, C.C. Hardin, T.E. Angelini, K. Rajendran, C.Y. Park, X. Serra-Picamal, E.H. Zhou, M.H. Zaman, J.P. Butler, D.A. Weitz, J.J. Fredberg, X. Trepat, Nat. Mater. 10, 469 (2011).

    Article  ADS  Google Scholar 

  26. A.R. Harris, L. Peter, J. Bellis, B. Baum, A.J. Kabla, G.T. Charras, Proc. Natl. Acad. Sci. U.S.A. 109, 16449 (2012).

    Article  ADS  Google Scholar 

  27. M.S. Hutson, Y. Tokutake, M.S. Chang, J.W. Bloor, S. Venakides, D.P. Kiehart, G.S. Edwards, Science 300, 145 (2003).

    Article  ADS  Google Scholar 

  28. M. Stein, R. Gordon, J. Theor. Biol. 97, 625 (1982).

    Article  Google Scholar 

  29. G.W. Brodland, V. Conte, P.G. Cranston, J. Veldhuis, S. Narasimhan, M.S. Hutson, A. Jacinto, F. Ulrich, B. Baum, M. Miodownik, Proc. Natl. Acad. Sci. U.S.A. 107, 22111 (2010).

    Article  ADS  Google Scholar 

  30. K.K. Chiou, L. Hufnagel, B.I. Shraiman, PLoS Comput. Biol. 8, e1002512 (2012).

    Article  Google Scholar 

  31. S. Ishihara, K. Sugimura, J. Theor. Biol. 313, 201 (2012).

    Article  Google Scholar 

  32. I. Cantat, S. Cohen-Addad, F. Elias, F. Graner, R. Höhler, O. Pitois, F. Rouyer, A. Saint-Jalmes, Les Mousses---Structure et Dynamique (Belin, Paris, 2010).

  33. I. Bonnet, P. Marcq, F. Bosveld, L. Fetler, Y. Bellaïche, F. Graner, J. R. Soc. Int. 9, 2614 (2012).

    Article  Google Scholar 

  34. K. Brakke, Exp. Math. 1, 141 (1992).

    Article  MathSciNet  MATH  Google Scholar 

  35. D. Weaire, S. Hutzler, The Physics of Foams (Clarendon, Oxford, 1999).

  36. H. Honda, Int. Rev. Cytol. 81, 191 (1983).

    Article  Google Scholar 

  37. H. Akaike, in Bayesian Statistics, edited by J.M. Bernardo, M.H. DeGroot, D.V. Lindley, A.F.M. Smith (Valencia University Press, Valencia, 1980).

  38. J. Kaipio, E. Somersalo, Statistical and Computational Inverse Problems (Springer, New York, 2004).

  39. G.K. Batchelor, J. Fluid Mech. 41, 545 (1970).

    Article  MathSciNet  ADS  MATH  Google Scholar 

  40. D’A. Thompson, On Growth and Form (Cambridge University Press, Cambridge, 1917).

  41. K. Sugimura, Y. Bellaiche, F. Graner, P. Marcq, S. Ishihara, Conf. Proc. IEEE Eng. Med. Biol. Soc., in press.

  42. E. Janiaud, F. Graner, J. Fluid Mech. 532, 243 (2005).

    Article  ADS  MATH  Google Scholar 

  43. V. Kovalevsky, Int. J. Patt. Recognit. Artif. Intell. 15, 1183 (2001).

    Article  Google Scholar 

  44. D. Boal, Mechanics of the Cell (Cambridge University Press, Cambridge, 2002).

  45. E. Bartnik, K. Weber, Eur. J. Cell Biol. 50, 17 (1989).

    Google Scholar 

  46. E. Goldstein, K. Gunawardena, J. Cell Biol. 150, F63 (2000).

    Article  Google Scholar 

Download references

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to S. Ishihara.

Additional information

Contribution to the Topical Issue “Physical constraints of morphogenesis and evolution”, edited by Vincent Fleury, Paul François and Marie Christine Ho Ba Tho.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Ishihara, S., Sugimura, K., Cox, S.J. et al. Comparative study of non-invasive force and stress inference methods in tissue. Eur. Phys. J. E 36, 45 (2013). https://doi.org/10.1140/epje/i2013-13045-8

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • DOI: https://doi.org/10.1140/epje/i2013-13045-8

Keywords

Navigation