Elasticity of cell membranes

A cell membrane defines a boundary between the living cell and its environment. The primary constituent of a membrane is a phospholipid bilayer that forms in a water-based environment due to the hydrophilic nature of the lipid head and the hydrophobic nature of the two tails. In addition there may be other lipids and proteins in the membrane, the latter typically in the form of isolated rafts.

Of the numerous models that have been developed to describe the deformation of cell membranes, a widely accepted model is the fluid mosaic model proposed by Singer and Nicolson in 1972. ^[1] In this model, the cell membrane surface is modeled as a two-dimensional fluid-like lipid bilayer where the lipid molecules can move freely. The proteins are partially or fully embedded in the lipid bilayer. Fully embedded proteins are called integral membrane proteins because they traverse the entire thickness of the lipid bilayer. These communicate information and matter between the interior and the exterior of the cell. Proteins that are only partially embedded in the bilayer are called peripheral membrane proteins. The membrane skeleton is a network of proteins below the bilayer that links with the proteins in the lipid membrane.

Elasticity of closed lipid vesicles

The simplest component of a membrane is the lipid bilayer which has a thickness that is much smaller than the length scale of the cell. Therefore the lipid bilayer can be represented by a two-dimensional mathematical surface. In 1973, based on similarities between lipid bilayers and nematic liquid crystals, Helfrich ^[2] proposed the following expression for the curvature energy per unit area of the closed lipid bilayer

$f_c = \frac{k_c}{2}(2H-c_0)^2+\bar{k}\,K$

(1)

where $k_c,\bar{k}$ are bending rigidities, $c_0$ is the spontaneous curvature of the membrane, and $H$ and $K$ are the mean and Gaussian curvature of the membrane surface, respectively.

The free energy of a closed bilayer under the osmotic pressure $\Delta p$ (the outer pressure minus the inner one) as:

$F_H=\int (f_c+\lambda)\, dA+\Delta p\int dV$

(2)

where dA and dV are the area element of the membrane and the volume element enclosed by the closed bilayer, respectively, and λ is the surface tension of the bilayer. By taking the first order variation of above free energy, Ou-Yang and Helfrich ^[3] derived an equation to describe the equilibrium shape of the bilayer as:

$\Delta p-2\lambda H+k_c(2H+c_0)(2H^2-c_0H-2K)+2k_c\nabla^2 H=0$

(3)

They also obtained that the threshold pressure for the instability of a spherical bilayer was

$\Delta p_{c}\propto k_c/R^3$

(4)

where $R$ being the radius of the spherical bilayer.

Using the shape equation (3) of closed vesicles, Ou-Yang predicted that there was a lipid torus with the ratio of two generated radii being exactly $\sqrt{2}$ . ^[4] His prediction was soon confirmed by the experiment ^[5] Additionally, researchers obtained an analytical solution ^[6] to (3) which explained the classical problem, the biconcave discoidal shape of normal red cells.

Elasticity of open lipid membranes

The opening-up process of lipid bilayers by talin was observed by Saitoh et al. ^[7] arose the interest of studying the equilibrium shape equation and boundary conditions of lipid bilayers with free exposed edges. Capovilla et al., ^[8] Tu and Ou-Yang ^[9] carefully studied this problem. The free energy of a lipid membrane with an edge $C$ is written as

$F_o=\int (f_c+\lambda) dA+\gamma\oint_C ds$

(5)

where $ds$ and $\gamma$ represent the arclength element and the line tension of the edge, respectively. The first order variation gives the shape equation and boundary conditions of the lipid membrane:

$k_{c}(2H+c_{0})(2H^{2}-c_{0}H-2K)-2\lambda H+k_{c}\nabla^{2}(2H)=0$

(6)

$\left. \left[ k_{c}(2H+c_{0})+\bar{k}k_n\right]\right\vert _{C}=0$

(7)

$\left. \left[ -2k_{c}\frac{\partial H}{\partial\mathbf{e}_2}+\gamma k_n+\bar{k}\frac{d\tau_g}{ds}\right]\right\vert _{C}=0$

(8)

$\left. \left[ \frac{k_{c}}{2}(2H+c_{0})^{2}+\bar{k}K+\lambda+\gamma k_{g}\right]\right\vert _{C}=0$

(9)

where $k_n$ , $k_g$ , and $\tau_g$ are normal curvature, geodesic curvature, and geodesic torsion of the boundary curve, respectively. $\mathbf{e}_2$ is the unit vector perpendicular to the tangent vector of the curve and the normal vector of the membrane.

Elasticity of cell membranes

A cell membrane is simplified as lipid bilayer plus membrane skeleton. The skeleton is a cross-linking protein network and joints to the bilayer at some points. Assume that each proteins in the membrane skeleton have similar length which is much smaller than the whole size of the cell membrane, and that the membrane is locally 2-dimensional uniform and homogenous. Thus the free energy density can be expressed as the invariant form of $2H$ , $K$ , $\mathrm{tr}(\varepsilon)$ and $\det(\varepsilon)$ :

$f_{cm}=f(2H,K,\mathrm{tr}(\varepsilon),\det(\varepsilon))$

(10)

where $\varepsilon$ is the in-plane strain of the membrane skeleton. Under the assumption of small deformations, and invariant between $\mathrm{tr}\varepsilon$ and $-\mathrm{tr}\varepsilon$ , (10) can be expanded up to second order terms as:

$f_{cm}=\frac{k_c}{2}(2H-c_0)^2+\bar{k}K+\lambda+\frac{k_d}{2}(\mathrm{tr}\varepsilon)^2-2\mu (\det\varepsilon)$

(11)

where $k_d$ and $\mu$ are two elastic constants. In fact, the first two terms in (11) are the bending energy of the cell membrane which contributes mainly from the lipid bilayer. The last two terms come from the entropic elasticity of the membrane skeleton.

References

↑ Singer, S. Jonathan; Nicolson, Garth L. (1972), "The fluid mosaic model of the structure of cell membranes", Science 175 (23): 720–731., doi:10.1126/science.175.4023.720, PMID 4333397
↑ Helfrich, Wolfgang (1973), "Elastic properties of lipid bilayers: theory and possible experiments", Zeitschrift für Naturforschung. Teil C: Biochemie, Biophysik, Biologie, Virologie 28 (11): 693.
↑ Zhong-Can, Ou-Yang; Helfrich, Wolfgang (1987), "Instability and deformation of a spherical vesicle by pressure", Physical Review Letters 59 (21): 2486., doi:10.1103/physrevlett.59.2486
↑ Zhong-Can, Ou-Yang (1990), "Anchor ring-vesicle membranes", Physical Review A 41 (8): 4517., doi:10.1103/physreva.41.4517
↑ Mutz, M.; Bensimon, D. (1991), "Observation of toroidal vesicles", Physical Review A 43 (8): 4525., doi:10.1103/physreva.43.4525
↑ Naito, Hiroyoshi; Okuda, Masahiro; Zhong-Can, Ou-Yang (1993), "Counterexample to some shape equations for axisymmetric vesicles", Physical Review E 48: 2304–2307., doi:10.1103/physreve.48.2304
↑ Saitoh, Akihiko; Takiguchi, Kingo; Tanaka, Yohko; Hotani, Hirokazu (1998), "Opening-up of liposomal membranes by talin", Proceedings of the National Academy of Sciences 95 (3): 1026–1031., doi:10.1073/pnas.95.3.1026
↑ Capovilla, R.; Guven, J.; Santiago, J. A. (2002), "Lipid membranes with an edge", Physical Review E 66 (2): 021607., doi:10.1103/physreve.66.021607
↑ Tu, Z. C.; Z. C., Ou-Yang (2003), "Lipid membranes with free edges", Physical Review E 68 (6): 061915., doi:10.1103/physreve.68.061915

Bibliography

Reviews on configurations of lipid vesicles

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[3] Z. C. Ou-Yang, J. X. Liu and Y. Z. Xie, Geometric Methods in the Elastic Theory of Membranes in Liquid Crystal Phases (World Scientific, Singapore, 1999).

Research papers on closed vesicles

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[2] O.-Y. Zhong-Can and W. Helfrich, Instability and Deformation of a Spherical Vesicle by Pressure, Phys. Rev. Lett. 59 (1987) 2486-2488.

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Research papers on open membranes

[1] A. Saitoh, K. Takiguchi, Y. Tanaka, and H. Hotani, Opening-up of liposomal membranes by talin, Proc. Natl. Acad. Sci. 95 (1998) 1026-1031.

[2] R. Capovilla, J. Guven, and J.A. Santiago, Lipid membranes with an edge, Phys. Rev. E 66 (2002) 021607.

[3] R. Capovilla and J. Guven, Stresses in lipid membranes, J. Phys. A 35 (2002) 6233-6247.

[4] Z. C. Tu and Z. C. Ou-Yang, Lipid membranes with free edges, Phys. Rev. E 68, (2003) 061915.

[5] T. Umeda, Y. Suezaki, K. Takiguchi, and H. Hotani, Theoretical analysis of opening-up vesicles with single and two holes, Phys. Rev. E 71 (2005) 011913.

Numerical solutions on lipid membranes

[1] J. Yan, Q. H. Liu, J. X. Liu and Z. C. Ou-Yang, Numerical observation of nonaxisymmetric vesicles in fluid membranes, Phys. Rev. E 58 (1998) 4730-4736.

[2] J. J. Zhou, Y. Zhang, X. Zhou, Z. C. Ou-Yang, Large Deformation of Spherical Vesicle Studied by Perturbation Theory and Surface Evolver, Int J Mod Phys B 15 (2001) 2977-2991.

[3] Y. Zhang, X. Zhou, J. J. Zhou and Z. C. Ou-Yang, Triconcave Solution to the Helfrich Variation Problem for the Shape of Lipid Bilayer Vesicles is Found by Surface Evolver, In. J. Mod. Phys. B 16 (2002) 511-517.

[4] Q. Du, C. Liu and X. Wang, Simulating the deformation of vesicle membranes under elastic bending energy in three dimensions, J. Comput. Phys. 212 (2006) 757.

[5] X. Wang and Q. Du, physics/0605095.

Selected papers on cell membranes

[1] Y. C. Fung and P. Tong, Theory of the Sphering of Red Blood Cells, Biophys. J. 8 (1968) 175-198.

[2] S. K. Boey, D. H. Boal, and D. E. Discher, Simulations of the Erythrocyte Cytoskeleton at Large Deformation. I. Microscopic Models, Biophys. J. 75 (1998) 1573-1583.

[3] D. E. Discher, D. H. Boal, and S. K. Boey, Simulations of the Erythrocyte Cytoskeleton at Large Deformation. II. Micropipette Aspiration, Biophys. J. 75 (1998) 1584-1597.

[4] E. Sackmann, A.R. Bausch and L. Vonna, Physics of Composite Cell Membrane and Actin Based Cytoskeleton, in Physics of bio-molecules and cells, Edited by H. Flyvbjerg, F. Julicher, P. Ormos And F. David (Springer, Berlin, 2002).

[5] G. Lim, M. Wortis, and R. Mukhopadhyay, Stomatocyte–discocyte–echinocyte sequence of the human red blood cell: Evidence for the bilayer–couple hypothesis from membrane mechanics, Proc. Natl. Acad. Sci. 99 (2002) 16766-16769.

[6] Z. C. Tu and Z. C. Ou-Yang, A Geometric Theory on the Elasticity of Bio-membranes, J. Phys. A: Math. Gen. 37 (2004) 11407-11429.

[7] Z. C. Tu and Z. C. Ou-Yang, Elastic theory of low-dimensional continua and its applications in bio- and nano-structures,arxiv:0706.0001.