Cellular Membranes, a Versatile Adaptive Composite Material

Abstract

Cellular membranes belong to the most vital yet least understood biomaterials of live matter. For instance, its biomechanical requirements substantially vary across species and subcellular sites, raising the question how membranes manage to adjust to such dramatic changes. Central to its adaptability at the cell surface is the interplay between the plasma membrane and the adjacent cell cortex, forming an adaptive composite material that dynamically adjusts its mechanical properties. Using a hypothetical composite material, we identify core challenges, and discuss how cellular membranes solved these tasks. We further muse how pathological changes in material properties affect membrane mechanics and cell function, before closing with open questions and future challenges arising when studying cellular membranes.

Keywords: adaptive material; cell cortex; composite material; lipid bilayer; plasma membrane.

FIGURE 1

Basic material properties and deformation types. (A) From left to right, membrane exposed to uniform extensional stress σ, which is acting normal to its edges, causes an increase of the area (from A₀ to A). Membrane exposed to forces acting parallel to its surface inducing shear stress τ_yx. Membrane exposed to a point load (F) acting perpendicular to its surface, which is inducing curvature and therefore a bending moment. Viscosity η, the resistance of a fluid against shear stress τ given at a specific shear velocity $\frac{du}{dy}$. (B) Basic properties of a purely elastic (spring, left) and viscous (dashpot, right) material. A purely elastic material always returns to its original state after deformation and exhibits a linear relationship between stress and strain, while a purely viscous material exhibits plastic (permanent) deformations and a linear relationship between stress and shear velocity. (C) Models of viscoelastic materials. Maxwell body (left) consisting of a dashpot and a spring in series displays, like a viscoelastic fluid, permanent deformation after the load is removed. Kelvin body (right) returns, like a viscoelastic solid, to its original state when the load is removed. Images adapted from Seidel et al. (2009) and Kamm and Grodzinsky (2015).

FIGURE 2

Modules of cellular membrane. (A) To the left, hypothetical biomimetic membrane that separates the inside from outside. To the right, the lipid bilayer presents the outermost structure of the cell membrane. Magnification depicts the 5–7 nm thick bilayer composed of individual lipids. (B) To the left, hypothetical composite material composed of a flexible hull associated to a rigid scaffold. To the right, the plasma membrane is tightly coupled to the cell cortex, creating a composite material. Individual actin proteins assemble into filaments that are facing the cell membrane with the growing end. (C) To the left, hypothetical adaptive composite material that changes material properties upon an external stimulus (red). To the right, the membrane/cortex continuum readily responds to external stimuli (red), reminiscent of an adaptive composite material. Note that changes in actin dynamics can also serve as signal (red, dotted line).