Minimum-energy vesicle and cell shapes calculated using spherical harmonics parameterization

An important open question in biophysics is to understand how mechanical forces shape membrane-bounded cells and their organelles. A general solution to this problem is to calculate the bending energy of an arbitrarily shaped membrane surface, which can include both lipids and cytoskeletal proteins, and minimize the energy subject to all mechanical constraints. However, the calculations are difficult to perform, especially for shapes that do not possess axial symmetry. We show that the spherical harmonics parameterization (SHP) provides an analytic description of shape that can be used to quickly and reliably calculate minimum energy shapes of both symmetric and asymmetric surfaces. Using this method, we probe the entire set of shapes predicted by the bilayer couple model, unifying work based on different computational approaches, and providing additional details of the transitions between different shape classes. In addition, we present new minimum-energy morphologies based on non-linear models of membrane skeletal elasticity that closely mimic extreme shapes of red blood cells. The SHP thus provides a versatile shape description that can be used to investigate forces that shape cells.

[1]  R. Waugh,et al.  Elastic properties of the red blood cell membrane that determine echinocyte deformability , 2004, European Biophysics Journal.

[2]  Evans,et al.  Entropy-driven tension and bending elasticity in condensed-fluid membranes. , 1990, Physical review letters.

[3]  S. Svetina,et al.  Flat and sigmoidally curved contact zones in vesicle–vesicle adhesion , 2007, Proceedings of the National Academy of Sciences.

[4]  S Chien,et al.  Elastic deformations of red blood cells. , 1977, Journal of Biomechanics.

[5]  Douglas W. Jones,et al.  Morphometric analysis of lateral ventricles in schizophrenia and healthy controls regarding genetic and disease-specific factors. , 2005, Proceedings of the National Academy of Sciences of the United States of America.

[6]  E. Hobson The Theory of Spherical and Ellipsoidal Harmonics , 1955 .

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

[8]  Jonathon Howard,et al.  Spherical harmonics-based parametric deconvolution of 3D surface images using bending energy minimization , 2008, Medical Image Anal..

[9]  W. Helfrich,et al.  Red blood cell shapes as explained on the basis of curvature elasticity. , 1976, Biophysical journal.

[10]  R. Heinrich,et al.  Nearly spherical vesicle shapes calculated by use of spherical harmonics : axisymmetric and nonaxisymmetric shapes and their stability , 1992 .

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

[12]  A Iglic,et al.  Membrane skeleton and red blood cell vesiculation at low pH. , 1998, Biochimica et biophysica acta.

[13]  M. McPeek,et al.  Modeling Three-Dimensional Morphological Structures Using Spherical Harmonics , 2009, Evolution; international journal of organic evolution.

[14]  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.

[15]  Reinhard Lipowsky,et al.  The conformation of membranes , 1991, Nature.

[16]  Jorge Nocedal,et al.  An interior algorithm for nonlinear optimization that combines line search and trust region steps , 2006, Math. Program..

[17]  R. Mukhopadhyay,et al.  Echinocyte shapes: bending, stretching, and shear determine spicule shape and spacing. , 2001, Biophysical journal.

[18]  Seifert,et al.  Budding transitions of fluid-bilayer vesicles: The effect of area-difference elasticity. , 1994, Physical review. E, Statistical physics, plasmas, fluids, and related interdisciplinary topics.

[19]  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.

[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]  Guido Gerig,et al.  Parametrization of Closed Surfaces for 3-D Shape Description , 1995, Comput. Vis. Image Underst..

[22]  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.

[23]  W Bosch,et al.  On the computation of derivatives of Legendre functions , 2000 .

[24]  M. Sheetz,et al.  Biological membranes as bilayer couples. A molecular mechanism of drug-erythrocyte interactions. , 1974, Proceedings of the National Academy of Sciences of the United States of America.

[25]  R. Mukhopadhyay,et al.  Stomatocyte–discocyte–echinocyte sequence of the human red blood cell: Evidence for the bilayer– couple hypothesis from membrane mechanics , 2002, Proceedings of the National Academy of Sciences of the United States of America.

[26]  A. Iglič A possible mechanism determining the stability of spiculated red blood cells. , 1997, Journal of biomechanics.

[27]  Primož Ziherl,et al.  Nonaxisymmetric phospholipid vesicles: Rackets, boomerangs, and starfish , 2005 .

[28]  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.

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

[30]  Philip Rabinowitz,et al.  Methods of Numerical Integration , 1985 .

[31]  A. Olson,et al.  Approximation and characterization of molecular surfaces , 1993, Biopolymers.

[32]  W. Helfrich,et al.  Bending energy of vesicle membranes: General expressions for the first, second, and third variation of the shape energy and applications to spheres and cylinders. , 1989, Physical review. A, General physics.

[33]  Thomas F. Coleman,et al.  An Interior Trust Region Approach for Nonlinear Minimization Subject to Bounds , 1993, SIAM J. Optim..

[34]  Jonathon Howard,et al.  Shapes of Red Blood Cells: Comparison of 3D Confocal Images with the Bilayer-Couple Model , 2008, Cellular and molecular bioengineering.