A finite element method to compute three-dimensional equilibrium configurations of fluid membranes: Optimal parameterization, variational formulation and applications

We introduce a finite element method to compute equilibrium configurations of fluid membranes, identified as stationary points of a curvature-dependent bending energy functional under certain geometric constraints. The reparameterization symmetries in the problem pose a challenge in designing parametric finite element methods, and existing methods commonly resort to Lagrange multipliers or penalty parameters. In contrast, we exploit these symmetries by representing solution surfaces as normal offsets of given reference surfaces and entirely bypass the need for artificial constraints. We then resort to a Galerkin finite element method to compute discrete C 1 approximations of the normal offset coordinate.The variational framework presented is suitable for computing deformations of three-dimensional membranes subject to a broad range of external interactions. We provide a systematic algorithm for computing large deformations, wherein solutions at subsequent load steps are identified as perturbations of previously computed ones. We discuss the numerical implementation of the method in detail and demonstrate its optimal convergence properties using examples. We discuss applications of the method to studying adhesive interactions of fluid membranes with rigid substrates and to investigate the influence of membrane tension in tether formation.

[1]  Huajian Gao,et al.  Phase diagrams and morphological evolution in wrapping of rod-shaped elastic nanoparticles by cell membrane: a two-dimensional study. , 2014, Physical review. E, Statistical, nonlinear, and soft matter physics.

[2]  Klaus Kassner,et al.  Phase-field approach to three-dimensional vesicle dynamics. , 2005, Physical review. E, Statistical, nonlinear, and soft matter physics.

[3]  L. R. Scott,et al.  The Mathematical Theory of Finite Element Methods , 1994 .

[4]  Q. Du,et al.  A phase field approach in the numerical study of the elastic bending energy for vesicle membranes , 2004 .

[5]  Warren C W Chan,et al.  Strategies for the intracellular delivery of nanoparticles. , 2011, Chemical Society reviews.

[6]  U. Seifert,et al.  Morphology of vesicles , 1995 .

[7]  M I Bloor,et al.  Method for efficient shape parametrization of fluid membranes and vesicles. , 2000, Physical review. E, Statistical physics, plasmas, fluids, and related interdisciplinary topics.

[8]  Huajian Gao,et al.  Cell entry of one-dimensional nanomaterials occurs by tip recognition and rotation. , 2011, Nature nanotechnology.

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

[10]  Marino Arroyo,et al.  Shape dynamics, lipid hydrodynamics, and the complex viscoelasticity of bilayer membranes [corrected]. , 2012, Physical review. E, Statistical, nonlinear, and soft matter physics.

[11]  L. B. Freund,et al.  The role of binder mobility in spontaneous adhesive contact and implications for cell adhesion , 2004 .

[12]  Ricardo H. Nochetto,et al.  A finite element method for surface diffusion: the parametric case , 2005 .

[13]  A. Shibuya,et al.  Morphology of Axisymmetric Vesicles with Encapsulated Filaments and Impurities , 2002, cond-mat/0207255.

[14]  Jian Zhang,et al.  Adaptive Finite Element Method for a Phase Field Bending Elasticity Model of Vesicle Membrane Deformations , 2008, SIAM J. Sci. Comput..

[15]  Marino Arroyo,et al.  Relaxation dynamics of fluid membranes. , 2009, Physical review. E, Statistical, nonlinear, and soft matter physics.

[16]  Udo Seifert,et al.  Configurations of fluid membranes and vesicles , 1997 .

[17]  Warren C W Chan,et al.  The effect of nanoparticle size, shape, and surface chemistry on biological systems. , 2012, Annual review of biomedical engineering.

[18]  Feng Feng,et al.  Finite element modeling of lipid bilayer membranes , 2006, J. Comput. Phys..

[19]  J. Nitsche,et al.  Boundary value problems for variational integrals involving surface curvatures , 1993 .

[20]  M. Dembo,et al.  Mechanics of neutrophil phagocytosis: experiments and quantitative models , 2006, Journal of Cell Science.

[21]  Mauro Ferrari,et al.  Intravascular Delivery of Particulate Systems: Does Geometry Really Matter? , 2008, Pharmaceutical Research.

[22]  Gustavo C. Buscaglia,et al.  A finite element method for viscous membranes , 2013 .

[23]  Wrapping of a spherical colloid by a fluid membrane , 2002, cond-mat/0212421.

[24]  Huajian Gao,et al.  Role of nanoparticle geometry in endocytosis: laying down to stand up. , 2013, Nano letters.

[25]  Robert E. Rudd,et al.  On the variational theory of cell-membrane equilibria , 2003 .

[26]  D. Steigmann,et al.  Boundary-value problems in the theory of lipid membranes , 2009 .

[27]  Markus Deserno,et al.  Elastic deformation of a fluid membrane upon colloid binding. , 2004, Physical review. E, Statistical, nonlinear, and soft matter physics.

[28]  T. Hughes,et al.  Isogeometric analysis of the Cahn–Hilliard phase-field model , 2008 .

[29]  J. Israelachvili Intermolecular and surface forces , 1985 .

[30]  Marino Arroyo Balaguer,et al.  Shape dynamics, lipid hydrodynamics, and the complex viscoelasticty of bilayer membranes , 2012 .

[31]  Libchaber,et al.  Buckling microtubules in vesicles. , 1996, Physical review letters.

[32]  P. Canham The minimum energy of bending as a possible explanation of the biconcave shape of the human red blood cell. , 1970, Journal of theoretical biology.

[33]  Huajian Gao,et al.  Mechanics of receptor-mediated endocytosis. , 2005, Proceedings of the National Academy of Sciences of the United States of America.

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

[35]  P. Mattila,et al.  Filopodia: molecular architecture and cellular functions , 2008, Nature Reviews Molecular Cell Biology.

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

[37]  T. Hughes,et al.  Isogeometric analysis : CAD, finite elements, NURBS, exact geometry and mesh refinement , 2005 .

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

[39]  Huajian Gao,et al.  Graphene microsheets enter cells through spontaneous membrane penetration at edge asperities and corner sites , 2013, Proceedings of the National Academy of Sciences.

[40]  Greg Huber,et al.  Fluid-membrane tethers: minimal surfaces and elastic boundary layers. , 2002, Physical review. E, Statistical, nonlinear, and soft matter physics.

[41]  J. C. Luke A Method for the Calculation of Vesicle Shapes , 1982 .

[42]  M Ferrari,et al.  The receptor-mediated endocytosis of nonspherical particles. , 2008, Biophysical journal.

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

[44]  Xiaopeng Xu,et al.  Numerical simulations of fast crack growth in brittle solids , 1994 .

[45]  Raluca E. Rusu An algorithm for the elastic flow of surfaces , 2005 .

[46]  T. Healey,et al.  Existence of Global Symmetry-Breaking Solutions in an Elastic Phase-Field Model for Lipid Bilayer Vesicles , 2014, 1402.2314.

[47]  Lin Ma,et al.  Viscous regularization and r-adaptive remeshing for finite element analysis of lipid membrane mechanics , 2007, J. Comput. Phys..

[48]  Michael P. Sheetz,et al.  Laser tweezers in cell biology , 1998 .

[49]  Qiang Du,et al.  Simulating the deformation of vesicle membranes under elastic bending energy in three dimensions , 2006, J. Comput. Phys..

[50]  Subra Suresh,et al.  Size‐Dependent Endocytosis of Nanoparticles , 2009, Advanced materials.

[51]  Huajian Gao,et al.  Probing mechanical principles of cell–nanomaterial interactions , 2014 .

[52]  James T. Jenkins,et al.  The Equations of Mechanical Equilibrium of a Model Membrane , 1977 .

[53]  J. Jenkins,et al.  Static equilibrium configurations of a model red blood cell , 1977, Journal of mathematical biology.

[54]  David J. Steigmann,et al.  Fluid Films with Curvature Elasticity , 1999 .

[55]  Huajian Gao,et al.  Two-dimensional model of vesicle adhesion on curved substrates , 2006 .

[56]  P. Bassereau,et al.  Bending lipid membranes: experiments after W. Helfrich's model. , 2014, Advances in colloid and interface science.

[57]  A. Rosolen,et al.  An adaptive meshfree method for phase-field models of biomembranes. Part I: Approximation with maximum-entropy basis functions , 2013, J. Comput. Phys..

[58]  Carl de Boor,et al.  A Practical Guide to Splines , 1978, Applied Mathematical Sciences.

[59]  Hamilton's equations for a fluid membrane , 2005, cond-mat/0505631.

[60]  Frank Jülicher,et al.  Formation and interaction of membrane tubes. , 2002, Physical review letters.