Micro-, nano- and meso-scale heterogeneity of iipid bilayers and its influence on macroscopic membrane properties

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Abstract
The lipid-bilayer component of cell membranes is a mesoscopic system consisting typically of the order of 108-1010 interacting particles. In its capacity as an interacting many-particle system, the membrane sustains correlated dynamical modes and it may display co-operative phenomena such as static global phase separation and dynamic local heterogeneity. These phenomena, which are highly non-trivial collective consequences of the molecular interactions, cannot be understood or described in terms of the properties of individual molecules alone. The microscopic manifestation of the co-operative modes consists in the formation of micro- and nano-scale heterogeneous structures, such as Iipid domains, that are dynamically maintained. The Iipid domains may be seen as either lateral density fluctuations or compositional fluctuations. The macroscopic consequences of these fluctuations are anomalies in response functions, such as the specific heat and the lateral compressibility. The dynamic heterogeneity corresponds to a specific lateral organization of the molecular constituents of the membrane. On the basis of recent experimental and theoretical progress in the study of the physical properties of lipid-bilayer membranes, in particular detailed pictures derived from computer simulations on models of bilayer membranes, it is proposed that the dynamically heterogeneous membrane states, which are induced by thermal density fluctuations and lateral compositional fluctuations, are important for passive and active membrane functions such as transmembrane permeability, enzymatic activity, and the in-plane aggregation of protein subunits to functioning protein complexes. Membrane-associated functions may be manipulated by changes in the heterogeneous membrane structure that can be significantly altered in response to changes in compositional, thermodynamic and environmental conditions. The diverse physical effects, and possibly some physiological effects of a variety of molecular compounds interacting with membranes such as cholesterol and drugs like anaesthetics, may be understood in terms of the ability of these compounds to affect and modulate the dynamic membrane heterogeneity.

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