Modelling cell motility and chemotaxis with evolving surface finite elements

We present a mathematical and a computational framework for the modelling of cell motility. The cell membrane is represented by an evolving surface, with the movement of the cell determined by the interaction of various forces that act normal to the surface. We consider external forces such as those that may arise owing to inhomogeneities in the medium and a pressure that constrains the enclosed volume, as well as internal forces that arise from the reaction of the cells' surface to stretching and bending. We also consider a protrusive force associated with a reaction–diffusion system (RDS) posed on the cell membrane, with cell polarization modelled by this surface RDS. The computational method is based on an evolving surface finite-element method. The general method can account for the large deformations that arise in cell motility and allows the simulation of cell migration in three dimensions. We illustrate applications of the proposed modelling framework and numerical method by reporting on numerical simulations of a model for eukaryotic chemotaxis and a model for the persistent movement of keratocytes in two and three space dimensions. Movies of the simulated cells can be obtained from http://homepages.warwick.ac.uk/∼maskae/CV_Warwick/Chemotaxis.html.

[1]  G. G. Stokes "J." , 1890, The New Yale Book of Quotations.

[2]  H. Piaggio Differential Geometry of Curves and Surfaces , 1952, Nature.

[3]  N. Rashevsky,et al.  Mathematical biology , 1961, Connecticut medicine.

[4]  I. Prigogine,et al.  Symmetry Breaking Instabilities in Dissipative Systems. II , 1968 .

[5]  W. Ramsey Analysis of individual leucocyte behavior during chemotaxis.. , 1972, Experimental cell research.

[6]  W. Helfrich Elastic Properties of Lipid Bilayers: Theory and Possible Experiments , 1973, Zeitschrift fur Naturforschung. Teil C: Biochemie, Biophysik, Biologie, Virologie.

[7]  C. Gardiner Handbook of Stochastic Methods , 1983 .

[8]  G. Dziuk,et al.  An algorithm for evolutionary surfaces , 1990 .

[9]  Dennis Bray,et al.  Cell Movements: From Molecules to Motility , 1992 .

[10]  T. Willmore Riemannian geometry , 1993 .

[11]  W Alt,et al.  Cytoplasm dynamics and cell motion: two-phase flow models. , 1999, Mathematical biosciences.

[12]  H. Meinhardt Orientation of chemotactic cells and growth cones: models and mechanisms. , 1999, Journal of cell science.

[13]  E. Platen An introduction to numerical methods for stochastic differential equations , 1999, Acta Numerica.

[14]  Thomas D Pollard,et al.  Cellular Motility Driven by Assembly and Disassembly of Actin Filaments , 2003, Cell.

[15]  T. Pollard,et al.  Cellular Motility Driven by Assembly and Disassembly of Actin Filaments , 2003, Cell.

[16]  Timothy A. Davis,et al.  Algorithm 832: UMFPACK V4.3---an unsymmetric-pattern multifrontal method , 2004, TOMS.

[17]  Kunibert G. Siebert,et al.  Design of Adaptive Finite Element Software - The Finite Element Toolbox ALBERTA , 2005, Lecture Notes in Computational Science and Engineering.

[18]  C. M. Elliott,et al.  Computation of geometric partial differential equations and mean curvature flow , 2005, Acta Numerica.

[19]  J. M. Oliver,et al.  Thin-film theories for two-phase reactive flow models of active cell motion. , 2005, Mathematical medicine and biology : a journal of the IMA.

[20]  R. Grima Directed cell migration in the presence of obstacles , 2007, Theoretical Biology and Medical Modelling.

[21]  Kamila Larripa,et al.  Transport of a 1D viscoelastic actin-myosin strip of gel as a model of a crawling cell. , 2006, Physica A.

[22]  R. Kay,et al.  Possible roles of the endocytic cycle in cell motility , 2007, Journal of Cell Science.

[23]  Mingming Wu,et al.  A hydrogel-based microfluidic device for the studies of directed cell migration. , 2007, Lab on a chip.

[24]  Micah Dembo,et al.  Traction force microscopy in Dictyostelium reveals distinct roles for myosin II motor and actin-crosslinking activity in polarized cell movement , 2007, Journal of Cell Science.

[25]  Alberto Aliseda,et al.  Spatio-temporal analysis of eukaryotic cell motility by improved force cytometry , 2007, Proceedings of the National Academy of Sciences.

[26]  Charles M. Elliott,et al.  Finite elements on evolving surfaces , 2007 .

[27]  Harald Garcke,et al.  Parametric Approximation of Willmore Flow and Related Geometric Evolution Equations , 2008, SIAM J. Sci. Comput..

[28]  Gerhard Dziuk,et al.  Computational parametric Willmore flow , 2008, Numerische Mathematik.

[29]  Charles M. Elliott,et al.  Eulerian finite element method for parabolic PDEs on implicit surfaces , 2008 .

[30]  Liu Yang,et al.  Modeling cellular deformations using the level set formalism , 2008, BMC Systems Biology.

[31]  Julie A. Theriot,et al.  Mechanism of shape determination in motile cells , 2008, Nature.

[32]  P. V. van Haastert,et al.  Navigation of Chemotactic Cells by Parallel Signaling to Pseudopod Persistence and Orientation , 2009, PloS one.

[33]  Alex Mogilner,et al.  Mathematics of Cell Motility: Have We Got Its Number? , 2022 .

[34]  Till Bretschneider,et al.  Analysis of cell movement by simultaneous quantification of local membrane displacement and fluorescent intensities using Quimp2. , 2009, Cell motility and the cytoskeleton.

[35]  Matthew P. Neilson,et al.  Use of the parameterised finite element method to robustly and efficiently evolve the edge of a moving cell. , 2010, Integrative biology : quantitative biosciences from nano to macro.

[36]  Ricardo H. Nochetto,et al.  Parametric FEM for geometric biomembranes , 2010, J. Comput. Phys..

[37]  Wouter-Jan Rappel,et al.  Computational model for cell morphodynamics. , 2010, Physical review letters.

[38]  Axel Voigt,et al.  A multigrid finite element method for reaction-diffusion systems on surfaces , 2010, Comput. Vis. Sci..

[39]  Charles M. Elliott,et al.  Modeling and computation of two phase geometric biomembranes using surface finite elements , 2010, J. Comput. Phys..

[40]  Robert H. Insall,et al.  Understanding eukaryotic chemotaxis: a pseudopod-centred view , 2010, Nature Reviews Molecular Cell Biology.

[41]  Eshel Ben-Jacob,et al.  Activated Membrane Patches Guide Chemotactic Cell Motility , 2011, PLoS Comput. Biol..

[42]  Alexandra Jilkine,et al.  A Comparison of Mathematical Models for Polarization of Single Eukaryotic Cells in Response to Guided Cues , 2011, PLoS Comput. Biol..

[43]  Falko Ziebert,et al.  Model for self-polarization and motility of keratocyte fragments , 2012, Journal of The Royal Society Interface.

[44]  Steven D. Webb,et al.  Modeling Cell Movement and Chemotaxis Using Pseudopod-Based Feedback , 2011, SIAM J. Sci. Comput..

[45]  J. Sethian,et al.  The Voronoi Implicit Interface Method for computing multiphase physics , 2011, Proceedings of the National Academy of Sciences.

[46]  C. M. Elliott,et al.  The surface finite element method for pattern formation on evolving biological surfaces , 2011, Journal of mathematical biology.

[47]  E. Ben-Jacob,et al.  “Self-Assisted” Amoeboid Navigation in Complex Environments , 2011, PloS one.

[48]  John A. Mackenzie,et al.  Chemotaxis: A Feedback-Based Computational Model Robustly Predicts Multiple Aspects of Real Cell Behaviour , 2011, PLoS biology.

[49]  P. Maini,et al.  Modeling parr-mark pattern formation during the early development of Amago trout. , 2011, Physical review. E, Statistical, nonlinear, and soft matter physics.

[50]  Pravin Madhavan,et al.  Biomembranes report , 2012, 1212.1641.

[51]  O. Lakkis,et al.  Global existence for semilinear reaction–diffusion systems on evolving domains , 2010, Journal of Mathematical Biology.

[52]  Charles M. Elliott,et al.  L2-estimates for the evolving surface finite element method , 2012, Math. Comput..

[53]  Charles M. Elliott,et al.  Computation of Two-Phase Biomembranes with Phase Dependent Material Parameters Using Surface Finite Elements , 2013 .