Skip to main content
Log in

Vertex stability and topological transitions in vertex models of foams and epithelia

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

Abstract.

In computer simulations of dry foams and of epithelial tissues, vertex models are often used to describe the shape and motion of individual cells. Although these models have been widely adopted, relatively little is known about their basic theoretical properties. For example, while fourfold vertices in real foams are always unstable, it remains unclear whether a simplified vertex model description has the same behavior. Here, we study vertex stability and the dynamics of T1 topological transitions in vertex models. We show that, when all edges have the same tension, stationary fourfold vertices in these models do indeed always break up. In contrast, when tensions are allowed to depend on edge orientation, fourfold vertices can become stable, as is observed in some biological systems. More generally, our formulation of vertex stability leads to an improved treatment of T1 transitions in simulations and paves the way for studies of more biologically realistic models that couple topological transitions to the dynamics of regulatory proteins.

Graphical abstract

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

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Similar content being viewed by others

References

  1. J.D. Axelrod, Sem. Cell Dev. Biol. 20, 964 (2009)

    Article  Google Scholar 

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

    Article  Google Scholar 

  3. F. Bosveld, I. Bonnet, B. Guirao, S. Tlili, Z. Wang, A. Petitalot, R. Marchand, P.L. Bardet, P. Marcq, F. Graner et al., Science 336, 724 (2012)

    Article  ADS  Google Scholar 

  4. A. Classen, K. Anderson, E. Marois, S. Eaton, Dev. Cell 9, 805 (2005)

    Article  Google Scholar 

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

    Article  Google Scholar 

  6. E. Assémat, E. Bazelliéres, E. Pallesi-Pocachard, A.L. Bivic, D. Massey-Harroche, Biomembranes 1778, 614 (2008)

    Article  Google Scholar 

  7. A.G. Fletcher, M. Osterfield, R.E. Baker, S.Y. Shvartsman, Biophys. J. 106, 2291 (2014)

    Article  ADS  Google Scholar 

  8. A.G. Fletcher, J.M. Osborne, P.K. Maini, D.J. Gavaghan, Progr. Biophys. Mol. Biol. 113, 299 (2013)

    Article  Google Scholar 

  9. S. Schilling, M. Willecke, T. Aegerter-Wilmsen, O.A. Cirpka, K. Basler, C. von Mering, PLoS Comput. Biol. 7, e1002025 (2011)

    Article  ADS  Google Scholar 

  10. R. Farhadifar, J.C. Röper, B. Algouy, S. Eaton, F. Jülicher, Curr. Biol. 17, 2095 (2007)

    Article  Google Scholar 

  11. P.A. Raymond, S.M. Colvin, Z. Jabeen, M. Nagashima, L.K. Barthel, J. Hadidjojo, L. Popova, V.R. Pejaver, D.K. Lubensky, PLoS ONE 9, e85325 (2014)

    Article  ADS  Google Scholar 

  12. M. Rauzi, P.F. Lenne, T. Lecuit, Nature 468, 1110 (2010)

    Article  ADS  Google Scholar 

  13. A.M. Greiner, H. Chen, J.P. Spatz, R. Kemkemer, PLoS ONE 8, e77328 (2013)

    Article  ADS  Google Scholar 

  14. D. Weaire, S. Hutzler, The Physics of Foams (Clarendon Press, 1999)

  15. H. Honda, H. Yamanaka, M. Dan-Sohkawa, J. Theor. Biol. 106, 423 (1984)

    Article  Google Scholar 

  16. H. Honda, H. Yamanaka, G. Eguchi, J. Embryol. Exp. Morphol. 98, 1 (1986)

    Google Scholar 

  17. T. Okuzono, K. Kawasaki, Phys. Rev. E 51, 1246 (1995)

    Article  ADS  Google Scholar 

  18. H. Frost, C. Thompson, C. Howe, J. Whang, Scr. Metall. 22, 65 (1988)

    Article  Google Scholar 

  19. Y. Ishimoto, Y. Morishita, Phys. Rev. E 90, 052711 (2014)

    Article  ADS  Google Scholar 

  20. G. Salbreux, L.K. Barthel, P.A. Raymond, D.K. Lubensky, PLoS Comput. Biol. 8, e1002618 (2012)

    Article  ADS  Google Scholar 

  21. K. Sherrard, F. Robin, P. Lemaire, E. Munro, Curr. Biol. 20, 1499 (2010)

    Article  Google Scholar 

  22. H. Chen, G. Brodland, J. Biomech. Engin. Trans. ASME 122, 394 (2000)

    Article  Google Scholar 

  23. E. Hannezo, J. Prost, J.F. Joanny, Proc. Natl. Acad. Sci. U.S.A. 111, 27 (2014)

    Article  ADS  Google Scholar 

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

    Article  Google Scholar 

  25. J.T. Blankenship, S.T. Backovic, J.S.P. Sanny, O. Weitz, J.A. Zallen, Dev. Cell 11, 459 (2006)

    Article  Google Scholar 

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

    Article  Google Scholar 

  27. R.P. Simone, S. DiNardo, Development 137, 1385 (2010)

    Article  Google Scholar 

  28. P.L. Bardet, B. Guirao, C. Paoletti, F. Serman, V. Léopold, F. Bosveld, Y. Goya, V. Mirouse, F. Graner, Y. Bellaiche, Dev. Cell 25, 534 (2013)

    Article  Google Scholar 

  29. G. Trichas, A.M. Smith, N. White, V. Wilkins, T. Watanabe, A. Moore, B. Joyce, J. Sugnaseelan, T.A. Rodriguez, D. Kay et al., PLoS Biol. 10, e1001256 (2012)

    Article  Google Scholar 

  30. M. Tamada, J.A. Zallen, Dev. Cell 35, 151 (2015)

    Article  Google Scholar 

  31. M.J. Harding, H.F. McGraw, A. Nechiporuk, Development 141, 2549 (2014)

    Article  Google Scholar 

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

    Article  Google Scholar 

  33. T. Nagai, H. Honda, Philos. Mag. B 81, 699 (2001)

    Article  ADS  Google Scholar 

  34. S. Ishihara, K. Sugimura, S.J. Cox, I. Bonnet, Y. Bellaiche, F. Graner, Eur. Phys. J. E 36, 9859 (2013)

    Article  Google Scholar 

  35. P. Spahn, R. Reuter, PLoS ONE 8, e75051 (2013)

    Article  ADS  Google Scholar 

  36. X. Du, M. Osterfield, S.Y. Shvartsman, Phys. Biol. 11, 066007 (2014)

    Article  ADS  Google Scholar 

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

    Article  Google Scholar 

  38. D. Bi, J.H. Lopez, J.M. Schwarz, M.L. Manning, Nat. Phys. 11, 1074 (2015)

    Article  Google Scholar 

  39. K.T. Sakurai, T. Kojima, T. Aigaki, S. Hayashi, Dev. Biol. 309, 126 (2007)

    Article  Google Scholar 

  40. K. Kawasaki, T. Nagai, K. Nakashima, Philos. Mag. B 60, 399 (1989)

    Article  ADS  Google Scholar 

  41. G. Odell, G. Oster, P. Alberch, B. Burnside, Dev. Biol. 85, 446 (1981)

    Article  Google Scholar 

  42. W. Karush, PhD Thesis, Univ. of Chicago (1939)

  43. H. Kuhn, A. Tucker, Proc. Second Berkeley Symp. Math. Stat. Probab, pp. 481--492 (1951)

  44. P. Campinho, M. Behrndt, J. Ranft, T. Risler, N. Minc, C.P. Heisenberg, Nat. Cell Biol. 15, 65 (2013)

    Article  Google Scholar 

  45. M. Zajac, G. Jones, J. Glazier, Phys. Rev. Lett. 85, 2022 (2000)

    Article  ADS  Google Scholar 

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

    Article  Google Scholar 

  47. Y. Mao, A.L. Tournier, A. Hoppe, L. Kester, B.J. Thompson, N. Tapon, EMBO J. 32, 2790 (2013)

    Article  Google Scholar 

  48. M. Durand, H.A. Stone, Phys. Rev. Lett. 97, 226101 (2006)

    Article  ADS  Google Scholar 

Download references

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Meryl A. Spencer.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Spencer, M.A., Jabeen, Z. & Lubensky, D.K. Vertex stability and topological transitions in vertex models of foams and epithelia. Eur. Phys. J. E 40, 2 (2017). https://doi.org/10.1140/epje/i2017-11489-4

Download citation

  • Received:

  • Accepted:

  • Published:

  • DOI: https://doi.org/10.1140/epje/i2017-11489-4

Keywords

Navigation