Viscous regularization and r-adaptive remeshing for finite element analysis of lipid membrane mechanics

As two-dimensional fluid shells, lipid bilayer membranes resist bending and stretching but are unable to sustain shear stresses. This property gives membranes the ability to adopt dramatic shape changes. In this paper, a finite element model is developed to study static equilibrium mechanics of membranes. In particular, a viscous regularization method is proposed to stabilize tangential mesh deformations and improve the convergence rate of nonlinear solvers. The augmented Lagrangian method is used to enforce global constraints on area and volume during membrane deformations. As a validation of the method, equilibrium shapes for a shape-phase diagram of lipid bilayer vesicle are calculated. These numerical techniques are also shown to be useful for simulations of three-dimensional large deformation problems: the formation of tethers (long tube-like extensions); and Ginzburg-Landau phase separation of a two lipid-component vesicle. To deal with the large mesh distortions of the two-phase model, modification of viscous regularization is explored to achieve r-adaptive mesh optimization.

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

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

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

[4]  R. Lipowsky,et al.  The Structure and Conformation of Amphiphilic Membranes , 1992 .

[5]  Q. Du,et al.  Modelling and simulations of multi-component lipid membranes and open membranes via diffuse interface approaches , 2006, Journal of Mathematical Biology.

[6]  E. Evans,et al.  Bending resistance and chemically induced moments in membrane bilayers. , 1974, Biophysical journal.

[7]  R. Mahajan,et al.  The Landau theory of phase transitions: A mechanical analog , 2009 .

[8]  J. Nocedal,et al.  A Limited Memory Algorithm for Bound Constrained Optimization , 1995, SIAM J. Sci. Comput..

[9]  Heinrich,et al.  Nonaxisymmetric vesicle shapes in a generalized bilayer-couple model and the transition between oblate and prolate axisymmetric shapes. , 1993, Physical review. E, Statistical physics, plasmas, fluids, and related interdisciplinary topics.

[10]  R. Waugh,et al.  Role of lamellar membrane structure in tether formation from bilayer vesicles. , 1992, Biophysical journal.

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

[12]  S. Svetina,et al.  THEORETICAL ANALYSIS OF THE FORMATION OF MEMBRANE MICROTUBES ON AXIALLY STRAINED VESICLES , 1997 .

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

[14]  David Andelman,et al.  Phase transitions and shapes of two component membranes and vesicles II : weak segregation limit , 1993 .

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

[16]  J. Lippincott-Schwartz,et al.  Formation of stacked ER cisternae by low affinity protein interactions , 2003, The Journal of cell biology.

[17]  S. Svetina,et al.  Membrane bending energy and shape determination of phospholipid vesicles and red blood cells , 1989, European Biophysics Journal.

[18]  Stephen J. Wright,et al.  Numerical Optimization , 2018, Fundamental Statistical Inference.

[19]  S Svetina,et al.  Bilayer couple hypothesis of red cell shape transformations and osmotic hemolysis. , 1983, Biomedica biochimica acta.

[20]  Seifert,et al.  Vesicular instabilities: The prolate-to-oblate transition and other shape instabilities of fluid bilayer membranes. , 1995, Physical review. E, Statistical physics, plasmas, fluids, and related interdisciplinary topics.

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

[22]  S. Svetina,et al.  Membrane bending energy in relation to bilayer couples concept of red blood cell shape transformations. , 1982, Journal of theoretical biology.

[23]  Bruce Alberts,et al.  Essential Cell Biology , 1983 .

[24]  Aaas News,et al.  Book Reviews , 1893, Buffalo Medical and Surgical Journal.

[25]  Jemal Guven,et al.  Deformations of the geometry of lipid vesicles , 2002 .

[26]  Hiroshi Noguchi,et al.  Dynamics of fluid vesicles in shear flow: effect of membrane viscosity and thermal fluctuations. , 2005, Physical review. E, Statistical, nonlinear, and soft matter physics.

[27]  Taniguchi,et al.  Shape deformation and phase separation dynamics of two-component vesicles. , 1996, Physical review letters.

[28]  T G Frey,et al.  The internal structure of mitochondria. , 2000, Trends in biochemical sciences.

[29]  Deborah Kuchnir Fygenson,et al.  Mechanics of Microtubule-Based Membrane Extension , 1997 .

[30]  Seifert,et al.  Shape transformations of vesicles: Phase diagram for spontaneous- curvature and bilayer-coupling models. , 1991, Physical review. A, Atomic, molecular, and optical physics.

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

[33]  J. Ho,et al.  Simulations of Fluid Self-Avoiding Membranes , 1990 .

[34]  R Skalak,et al.  Mechanics and thermodynamics of biomembranes: part 1. , 1979, CRC critical reviews in bioengineering.

[35]  R. Lipowsky,et al.  Shape transformations of vesicles with intramembrane domains. , 1996, Physical review. E, Statistical physics, plasmas, fluids, and related interdisciplinary topics.

[36]  Reinhard Lipowsky,et al.  Gravity-induced shape transformations of vesicles , 1995 .

[37]  Gregory A Voth,et al.  Coupling field theory with continuum mechanics: a simulation of domain formation in giant unilamellar vesicles. , 2005, Biophysical journal.

[38]  Jorge Nocedal,et al.  Algorithm 778: L-BFGS-B: Fortran subroutines for large-scale bound-constrained optimization , 1997, TOMS.

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

[40]  Watt W. Webb,et al.  Imaging coexisting fluid domains in biomembrane models coupling curvature and line tension , 2003, Nature.

[41]  Saxena,et al.  Phase separation and shape deformation of two-phase membranes , 2000, Physical review. E, Statistical physics, plasmas, fluids, and related interdisciplinary topics.

[42]  R. Lipowsky,et al.  Domain-induced budding of vesicles. , 1993, Physical review letters.

[43]  I. S. Sokolnikoff,et al.  Tensor Analysis: Theory and Applications , 1952 .

[44]  Manfredo P. do Carmo,et al.  Differential geometry of curves and surfaces , 1976 .

[45]  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.

[46]  John Sullivan,et al.  Minimizing the Squared Mean Curvature Integral for Surfaces in Space Forms , 1992, Exp. Math..

[47]  Michael Ortiz,et al.  Fully C1‐conforming subdivision elements for finite deformation thin‐shell analysis , 2001, International Journal for Numerical Methods in Engineering.

[48]  W. Helfrich,et al.  Budding of lipid bilayer vesicles and flat membranes , 1992 .

[49]  M. Ortiz,et al.  Subdivision surfaces: a new paradigm for thin‐shell finite‐element analysis , 2000 .

[50]  Udo Seifert,et al.  Budding transition for bilayer fluid vesicles with area-difference elasticity , 1992 .

[51]  Petra Schwille,et al.  Sterol structure determines the separation of phases and the curvature of the liquid-ordered phase in model membranes. , 2005, Proceedings of the National Academy of Sciences of the United States of America.

[52]  Robert W. Balluffi,et al.  Kinetics Of Materials , 2005 .

[53]  Reinhard Lipowsky,et al.  Budding of membranes induced by intramembrane domains , 1992 .

[54]  Gerhard Gompper,et al.  Network models of fluid, hexatic and polymerized membranes , 1997 .

[55]  U. Seifert,et al.  Pulling tethers from adhered vesicles. , 2004, Physical review letters.

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

[57]  V. Heinrich,et al.  Vesicle deformation by an axial load: from elongated shapes to tethered vesicles. , 1999, Biophysical journal.

[58]  Hiroshi Noguchi,et al.  Meshless membrane model based on the moving least-squares method. , 2006, Physical review. E, Statistical, nonlinear, and soft matter physics.

[59]  W. Webb,et al.  Membrane elasticity in giant vesicles with fluid phase coexistence. , 2005, Biophysical journal.