Dynamics of surface of lipid membranes: theoretical considerations and the ESR experiment

Eur Biophys J Dynamics of surface of lipid membranes: theoretical considerations and the ESR experiment Dariusz Man 0 Ryszard Olchawa 0 0 Institute of Physics, Opole University , Oleska 48, 45-052 Opole , Poland The effect of the surface layer of model membranes on their physical properties was discussed in this paper. The research involved a physical ESR experiment with the use of spin probes and computer simulation based on the Monte Carlo technique. Liposomes formed during the process of sonication of lecithin were scanned in an ESR spectrometer. The membrane surface layer model, represented by the system of electric dipoles arranged in rectangular or hexagonal matrices, was studied. The final states of computer simulations were presented as textures. It was found that in the gel phase some ordered domain structures are formed, while in the liquid-crystal phase we got complex textures comprising a plurality of gaps. The process of forming domain structures during the changing of the temperature and the phase transitions taking place in a dipole system as a function of dipole mobility (k-parameter) was presented. The results obtained imply that the head groups (represented by electric dipoles in the computer model) of the surface layer play a key role in membranes, affecting the properties of the entire membrane, which is particularly essential for transport processes. It also modified the characteristics of the membrane gel-liquid crystalline transition phase. Lipid membrane; Membrane fluidity; Monte Carlo simulation; ESR probe - Biological membranes play a fundamental role in the functioning of all living organisms. They have a complex and dynamic structure (Singer and Nicolson 1972) whose elements are constantly moving (McConnell 1976; Sackmann 1978). Because of the considerable complexity of these systems, developing a mathematical model covering all interactions is very difficult; therefore the proposed models of membranes concentrate on selected groups of physical interactions. The basic structure of a biological membrane is a lipid bilayer, which constitutes its core. It serves as a foundation to which other elements determining individual properties of the membrane are attached. Learning about mechanisms affecting the properties of the lipid bilayer (the structural core of membranes) will allow for a better understanding of processes occurring in the actual biological membrane. Liposomes provide a good model for studying the physical properties of real biological membranes. Both their molecular composition and geometric dimension can be precisely controlled, meaning that the studied objects are well defined, whilst at the same time, being complex enough to reflect the properties of natural biological membranes. In order to understand better the processes taking place in the lipid bilayer, in parallel to the physical experiment, other studies have focused on using mathematical models. One of the earliest was the model presented in 1980 and 1998 by Pink et al. 1998 who assumed that the area determining the dynamic properties of the membrane is their hydrophobic interior, comprising long hydrocarbon chains. The properties of the surface layer were not taken into consideration. Because of the specificity of the object, the computer-based techniques have become an extraordinarily helpful tool in imaging and providing a better understanding of the processes occurring in the membranes. The computer-based models can be divided into two groups: deterministic (e.g., implemented in biomolecular codes: GROMACS, CHARMM), which are based on numerical solutions of movement equations of a system, e.g., molecular dynamic simulations, which illustrate time-dependent phenomena (Pasenkiewicz-Gierula et al. 1999; Lopez et al. 2002; Berendsen and Tieleman 2014), and the Monte Carlo method, which in its broadest meaning introduces an element of randomness into the algorithms of calculations. The Monte Carlo method is most often applied in those cases where the deterministic methods are not appropriate because of the large degree of freedom in a given system. One example of the application of this method is when generating a large set of configurations of the examined system, which meet preset physical conditions (of an ensemble) and then calculating the mean of this group of states. This model, applied to lipid membranes, can be found in the following studies on: gel-fluid transitions (Mouritsen et al. 1983; Kubica 1997), acyl density fluctuations (Ipsen et al. 1990), the binding energy of a lipid surface (Man et al. 2004, 2007, 2010, 2013a), the effects of cholesterol (Ipsen et al. 1989, 1990), influence of membrane modifiers on membrane properties (Jorgensen et al. 1991a), partitioning of membrane intruders (Jorgensen et al. 1991b), membrane heterogeneity, lateral distribution of proteins in membranes, and on membrane electroporation (Kotulska et al. 2007). The Monte Carlo method enables one also to simulate (...truncated)