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

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

[1]  Christian von Mering,et al.  Cell-Sorting at the A/P Boundary in the Drosophila Wing Primordium: A Computational Model to Consolidate Observed Non-Local Effects of Hh Signaling , 2011, PLoS Comput. Biol..

[2]  Alexandra M. Greiner,et al.  Cyclic Tensile Strain Controls Cell Shape and Directs Actin Stress Fiber Formation and Focal Adhesion Alignment in Spreading Cells , 2013, PloS one.

[3]  A. Le Bivic,et al.  Polarity complex proteins. , 2008, Biochimica et biophysica acta.

[4]  H. Honda,et al.  Transformation of a polygonal cellular pattern during sexual maturation of the avian oviduct epithelium: computer simulation. , 1986, Journal of embryology and experimental morphology.

[5]  Bubbly vertex dynamics: A dynamical and geometrical model for epithelial tissues with curved cell shapes. , 2014, Physical review. E, Statistical, nonlinear, and soft matter physics.

[6]  H. Honda Geometrical models for cells in tissues. , 1983, International review of cytology.

[7]  Y. Bellaïche,et al.  PTEN controls junction lengthening and stability during cell rearrangement in epithelial tissue. , 2013, Developmental cell.

[8]  Katsuya Nakashima,et al.  Vertex models for two-dimensional grain growth , 1989 .

[9]  T. Aigaki,et al.  Differential control of cell affinity required for progression and refinement of cell boundary during Drosophila leg segmentation. , 2007, Developmental biology.

[10]  J. Axelrod,et al.  Progress and challenges in understanding planar cell polarity signaling. , 2009, Seminars in cell & developmental biology.

[11]  David K. Lubensky,et al.  Coupling Mechanical Deformations and Planar Cell Polarity to Create Regular Patterns in the Zebrafish Retina , 2012, PLoS Comput. Biol..

[12]  Philippe Marcq,et al.  Mechanical Control of Morphogenesis by Fat/Dachsous/Four-Jointed Planar Cell Polarity Pathway , 2012, Science.

[13]  D. Lubensky,et al.  Patterning the Cone Mosaic Array in Zebrafish Retina Requires Specification of Ultraviolet-Sensitive Cones , 2014, PloS one.

[14]  R. Reuter,et al.  A Vertex Model of Drosophila Ventral Furrow Formation , 2013, PloS one.

[15]  E. Munro,et al.  Sequential Activation of Apical and Basolateral Contractility Drives Ascidian Endoderm Invagination , 2010, Current Biology.

[16]  P. Gennes The Physics Of Foams , 1999 .

[17]  Philip K Maini,et al.  Implementing vertex dynamics models of cell populations in biology within a consistent computational framework. , 2013, Progress in biophysics and molecular biology.

[18]  H Honda,et al.  A computer simulation of geometrical configurations during cell division. , 1984, Journal of theoretical biology.

[19]  M. Tamada,et al.  Square Cell Packing in the Drosophila Embryo through Spatiotemporally Regulated EGF Receptor Signaling. , 2015, Developmental cell.

[20]  S. Shvartsman,et al.  Computational analysis of three-dimensional epithelial morphogenesis using vertex models , 2014, Physical biology.

[21]  Frank Jülicher,et al.  Cell Flow Reorients the Axis of Planar Polarity in the Wing Epithelium of Drosophila , 2010, Cell.

[22]  Jacques Prost,et al.  Theory of epithelial sheet morphology in three dimensions , 2013, Proceedings of the National Academy of Sciences.

[23]  S. Eaton,et al.  Hexagonal packing of Drosophila wing epithelial cells by the planar cell polarity pathway. , 2005, Developmental cell.

[24]  Pierre-François Lenne,et al.  Planar polarized actomyosin contractile flows control epithelial junction remodelling , 2010, Nature.

[25]  Pierre-François Lenne,et al.  Force generation, transmission, and integration during cell and tissue morphogenesis. , 2011, Annual review of cell and developmental biology.

[26]  G W Brodland,et al.  Cell-level finite element studies of viscous cells in planar aggregates. , 2000, Journal of biomechanical engineering.

[27]  J. Glazier,et al.  Model of convergent extension in animal morphogenesis. , 1999, Physical review letters.

[28]  Stephen P. Boyd,et al.  Convex Optimization , 2004, Algorithms and Theory of Computation Handbook.

[29]  P. Alberch,et al.  The mechanical basis of morphogenesis. I. Epithelial folding and invagination. , 1981, Developmental biology.

[30]  Frank Jülicher,et al.  The Influence of Cell Mechanics, Cell-Cell Interactions, and Proliferation on Epithelial Packing , 2007, Current Biology.

[31]  C. Heisenberg,et al.  Tension-oriented cell divisions limit anisotropic tissue tension in epithelial spreading during zebrafish epiboly , 2013, Nature Cell Biology.

[32]  Howard A Stone,et al.  Relaxation time of the topological T1 process in a two-dimensional foam. , 2006, Physical review letters.

[33]  Yanlan Mao,et al.  Planar polarization of the atypical myosin Dachs orients cell divisions in Drosophila. , 2011, Genes & development.

[34]  Ruth E Baker,et al.  Vertex models of epithelial morphogenesis. , 2014, Biophysical journal.

[35]  Lennart Kester,et al.  Differential proliferation rates generate patterns of mechanical tension that orient tissue growth , 2013, The EMBO journal.

[36]  Okuzono,et al.  Intermittent flow behavior of random foams: A computer experiment on foam rheology. , 1995, Physical review. E, Statistical physics, plasmas, fluids, and related interdisciplinary topics.

[37]  Pierre-François Lenne,et al.  Nature and anisotropy of cortical forces orienting Drosophila tissue morphogenesis , 2008, Nature Cell Biology.

[38]  Molly J. Harding,et al.  The roles and regulation of multicellular rosette structures during morphogenesis , 2014, Development.

[39]  S. DiNardo,et al.  Actomyosin contractility and Discs large contribute to junctional conversion in guiding cell alignment within the Drosophila embryonic epithelium , 2010, Development.

[40]  Dapeng Bi,et al.  A density-independent rigidity transition in biological tissues , 2014, Nature Physics.

[41]  S. Eaton,et al.  Mechanics and remodelling of cell packings in epithelia , 2010, The European physical journal. E, Soft matter.

[42]  C. V. Thompson,et al.  A two-dimensional computer simulation of capillarity-driven grain growth: Preliminary results , 1988 .

[43]  Tatsuzo Nagai,et al.  A dynamic cell model for the formation of epithelial tissues , 2001 .

[44]  Ruth E. Baker,et al.  Multi-Cellular Rosettes in the Mouse Visceral Endoderm Facilitate the Ordered Migration of Anterior Visceral Endoderm Cells , 2012, PLoS biology.

[45]  Jennifer A Zallen,et al.  Multicellular rosette formation links planar cell polarity to tissue morphogenesis. , 2006, Developmental cell.

[46]  F Graner,et al.  Comparative study of non-invasive force and stress inference methods in tissue , 2013, The European physical journal. E, Soft matter.