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

Similar content being viewed by others
Explore related subjects
Discover the latest articles, news and stories from top researchers in related subjects.References
T. Lecuit, P.F. Lenne, Nat. Rev. Mol. Cell Biol. 8, 633 (2007).
T. Lecuit, P.F. Lenne, E. Munro, Annu. Rev. Cell Dev. Biol. 27, 157 (2011).
D. Bilder, S.L. Haigo, Dev. Cell 22, 12 (2012).
S. Eaton, F. Jülicher, Curr. Opin. Genet. Dev. 21, 747 (2012).
K.E. Kasza, J.A. Zallen, Curr. Opin. Cell Biol. 23, 30 (2011).
M. Nahmad, A.D. Lander, Curr. Opin. Genet. Dev. 21, 726 (2011).
O. Wartlick, M. Gonzalez-Gaitan, Curr. Opin. Genet. Dev. 21, 690 (2011).
F. Graner, Y. Sawada, J. Theor. Biol. 164, 477 (1993).
N.B. Ouchi, J.A. Glazier, J.P. Rieu, A. Upadhyaya, Y. Sawada, Physica A 329, 451 (2003).
J. Käfer, T. Hayashi, A.F.M. Marée, R. Carthew, F. Graner, Proc. Natl. Acad. Sci. U.S.A. 104, 18549 (2007).
R. Farhadifar, J.C. Roper, B. Aigouy, S. Eaton, F. Jülicher, Curr. Biol. 17, 2095 (2007).
M. Krieg, Y. Arboleda-Estudillo, P.-H. Puech, J. Käfer, F. Graner, D.J. Müller, C.-P. Heisenberg, Nat. Cell. Biol. 10, 429 (2008).
S. Hilgenfeldt, S. Erisken, R.W. Carthew, Proc. Natl. Acad. Sci. U.S.A. 105, 907 (2008).
H. Honda, N. Motosugi, T. Nagai, M. Tanemura, T. Hiiragi, Development 135, 1407 (2008).
M. Rauzi, P. Verant, T. Lecuit, P.F. Lenne, Nat. Cell Biol. 10, 1401 (2008).
B. Aigouy, R. Farhadifar, D.B. Staple, A. Sagner, J.C. Roper, F. Jülicher, S. Eaton, Cell 142, 773 (2010).
D.B. Staple, R. Farhadifar, J.-C. Röper, B. Aigouy, S. Eaton, F. Jülicher, Eur. Phys. J. E 33, 117 (2010).
Y. Mao, A.L. Tournier, P.A. Bates, J.E. Gale, N. Tapon, B.J. Thompson, Genes Dev. 25, 131 (2011).
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).
J. Ophir, I. Cespedes, B. Garra, H. Ponnekanti, Y. Huang, N. Maklad, Eur. J. Ultrasound 3, 49 (1996).
U. Nienhaus, T. Aegerter-Wilmsen, C.M. Aegerter, Mech. Dev. 126, 942 (2009).
N. Desprat, W. Supatto, P. Pouille, E. Beaurepaire, E. Farge, Dev. Cell 15, 470 (2008).
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).
A. Peaucelle, S. Braybrook, L.L. Guillou, E. Bron, C. Kuhlemeier, H. Höfte, Curr. Biol. 21, 1720 (2011).
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).
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).
M.S. Hutson, Y. Tokutake, M.S. Chang, J.W. Bloor, S. Venakides, D.P. Kiehart, G.S. Edwards, Science 300, 145 (2003).
M. Stein, R. Gordon, J. Theor. Biol. 97, 625 (1982).
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).
K.K. Chiou, L. Hufnagel, B.I. Shraiman, PLoS Comput. Biol. 8, e1002512 (2012).
S. Ishihara, K. Sugimura, J. Theor. Biol. 313, 201 (2012).
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).
I. Bonnet, P. Marcq, F. Bosveld, L. Fetler, Y. Bellaïche, F. Graner, J. R. Soc. Int. 9, 2614 (2012).
K. Brakke, Exp. Math. 1, 141 (1992).
D. Weaire, S. Hutzler, The Physics of Foams (Clarendon, Oxford, 1999).
H. Honda, Int. Rev. Cytol. 81, 191 (1983).
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).
J. Kaipio, E. Somersalo, Statistical and Computational Inverse Problems (Springer, New York, 2004).
G.K. Batchelor, J. Fluid Mech. 41, 545 (1970).
D’A. Thompson, On Growth and Form (Cambridge University Press, Cambridge, 1917).
K. Sugimura, Y. Bellaiche, F. Graner, P. Marcq, S. Ishihara, Conf. Proc. IEEE Eng. Med. Biol. Soc., in press.
E. Janiaud, F. Graner, J. Fluid Mech. 532, 243 (2005).
V. Kovalevsky, Int. J. Patt. Recognit. Artif. Intell. 15, 1183 (2001).
D. Boal, Mechanics of the Cell (Cambridge University Press, Cambridge, 2002).
E. Bartnik, K. Weber, Eur. J. Cell Biol. 50, 17 (1989).
E. Goldstein, K. Gunawardena, J. Cell Biol. 150, F63 (2000).
Author information
Authors and Affiliations
Corresponding author
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
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
Received:
Revised:
Accepted:
Published:
DOI: https://doi.org/10.1140/epje/i2013-13045-8


