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%\documentclass[aps,pre,twocolumn,amssymb,showpacs,floatfix]{revtex4} |
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\begin{document} |
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%\bibliographystyle{aps} |
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\title{Dipolar Ordering in Molecular-scale Models of the Ripple Phase |
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in Lipid Membranes} |
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\author{Xiuquan Sun and J. Daniel Gezelter} |
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\email[E-mail:]{gezelter@nd.edu} |
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\affiliation{Department of Chemistry and Biochemistry,\\ |
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University of Notre Dame, \\ |
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Notre Dame, Indiana 46556} |
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\date{\today} |
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\begin{abstract} |
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The ripple phase in phosphatidylcholine (PC) bilayers has never been |
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completely explained. |
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\end{abstract} |
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\pacs{} |
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\maketitle |
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\section{Introduction} |
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\label{sec:Int} |
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Fully hydrated lipids will aggregate spontaneously to form bilayers |
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which exhibit a variety of phases depending on their temperatures and |
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compositions. Among these phases, a periodic rippled phase |
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($P_{\beta'}$) appears as an intermediate phase between the gel |
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($L_\beta$) and fluid ($L_{\alpha}$) phases for relatively pure |
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phosphatidylcholine (PC) bilayers. The ripple phase has attracted |
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substantial experimental interest over the past 30 years. Most |
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structural information of the ripple phase has been obtained by the |
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X-ray diffraction~\cite{Sun96,Katsaras00} and freeze-fracture electron |
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microscopy (FFEM).~\cite{Copeland80,Meyer96} Recently, Kaasgaard {\it |
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et al.} used atomic force microscopy (AFM) to observe ripple phase |
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morphology in bilayers supported on mica.~\cite{Kaasgaard03} The |
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experimental results provide strong support for a 2-dimensional |
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hexagonal packing lattice of the lipid molecules within the ripple |
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phase. This is a notable change from the observed lipid packing |
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within the gel phase.~\cite{Cevc87} |
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|
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A number of theoretical models have been presented to explain the |
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formation of the ripple phase. Marder {\it et al.} used a |
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curvature-dependent Landau-de Gennes free-energy functional to predict |
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a rippled phase.~\cite{Marder84} This model and other related continuum |
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models predict higher fluidity in convex regions and that concave |
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portions of the membrane correspond to more solid-like regions. |
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Carlson and Sethna used a packing-competition model (in which head |
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groups and chains have competing packing energetics) to predict the |
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formation of a ripple-like phase. Their model predicted that the |
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high-curvature portions have lower-chain packing and correspond to |
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more fluid-like regions. Goldstein and Leibler used a mean-field |
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approach with a planar model for {\em inter-lamellar} interactions to |
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predict rippling in multilamellar phases.~\cite{Goldstein88} McCullough |
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and Scott proposed that the {\em anisotropy of the nearest-neighbor |
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interactions} coupled to hydrophobic constraining forces which |
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restrict height differences between nearest neighbors is the origin of |
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the ripple phase.~\cite{McCullough90} Lubensky and MacKintosh |
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introduced a Landau theory for tilt order and curvature of a single |
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membrane and concluded that {\em coupling of molecular tilt to membrane |
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curvature} is responsible for the production of |
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ripples.~\cite{Lubensky93} Misbah, Duplat and Houchmandzadeh proposed |
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that {\em inter-layer dipolar interactions} can lead to ripple |
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instabilities.~\cite{Misbah98} Heimburg presented a {\em coexistence |
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model} for ripple formation in which he postulates that fluid-phase |
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line defects cause sharp curvature between relatively flat gel-phase |
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regions.~\cite{Heimburg00} Kubica has suggested that a lattice model of |
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polar head groups could be valuable in trying to understand bilayer |
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phase formation.~\cite{Kubica02} Bannerjee used Monte Carlo simulations |
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of lamellar stacks of hexagonal lattices to show that large headgroups |
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and molecular tilt with respect to the membrane normal vector can |
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cause bulk rippling.~\cite{Bannerjee02} |
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|
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In contrast, few large-scale molecular modelling studies have been |
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done due to the large size of the resulting structures and the time |
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required for the phases of interest to develop. With all-atom (and |
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even unified-atom) simulations, only one period of the ripple can be |
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observed and only for timescales in the range of 10-100 ns. One of |
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the most interesting molecular simulations was carried out by De Vries |
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{\it et al.}~\cite{deVries05}. According to their simulation results, |
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the ripple consists of two domains, one resembling the gel bilayer, |
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while in the other, the two leaves of the bilayer are fully |
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interdigitated. The mechanism for the formation of the ripple phase |
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suggested by their work is a packing competition between the head |
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groups and the tails of the lipid molecules.\cite{Carlson87} Recently, |
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the ripple phase has also been studied by Lenz and Schmid using Monte |
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Carlo simulations.\cite{Lenz07} Their structures are similar to the De |
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Vries {\it et al.} structures except that the connection between the |
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two leaves of the bilayer is a narrow interdigitated line instead of |
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the fully interdigitated domain. The symmetric ripple phase was also |
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observed by Lenz {\it et al.}, and their work supports other claims |
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that the mismatch between the size of the head group and tail of the |
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lipid molecules is the driving force for the formation of the ripple |
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phase. Ayton and Voth have found significant undulations in |
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zero-surface-tension states of membranes simulated via dissipative |
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particle dynamics, but their results are consistent with purely |
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thermal undulations.~\cite{Ayton02} |
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|
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Although the organization of the tails of lipid molecules are |
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addressed by these molecular simulations and the packing competition |
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between headgroups and tails is strongly implicated as the primary |
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driving force for ripple formation, questions about the ordering of |
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the head groups in ripple phase has not been settled. |
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|
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In a recent paper, we presented a simple ``web of dipoles'' spin |
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lattice model which provides some physical insight into relationship |
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between dipolar ordering and membrane buckling.\cite{Sun2007} We found |
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that dipolar elastic membranes can spontaneously buckle, forming |
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ripple-like topologies. The driving force for the buckling in dipolar |
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elastic membranes the antiferroelectric ordering of the dipoles, and |
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this was evident in the ordering of the dipole director axis |
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perpendicular to the wave vector of the surface ripples. A similiar |
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phenomenon has also been observed by Tsonchev {\it et al.} in their |
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work on the spontaneous formation of dipolar peptide chains into |
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curved nano-structures.\cite{Tsonchev04,Tsonchev04II} |
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|
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In this paper, we construct a somewhat more realistic molecular-scale |
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lipid model than our previous ``web of dipoles'' and use molecular |
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dynamics simulations to elucidate the role of the head group dipoles |
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in the formation and morphology of the ripple phase. We describe our |
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model and computational methodology in section \ref{sec:method}. |
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Details on the simulations are presented in section |
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\ref{sec:experiment}, with results following in section |
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\ref{sec:results}. A final discussion of the role of dipolar heads in |
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the ripple formation can be found in section |
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\ref{sec:discussion}. |
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\section{Computational Model} |
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\label{sec:method} |
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\begin{figure}[htb] |
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\centering |
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\includegraphics[width=4in]{lipidModels} |
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\caption{Three different representations of DPPC lipid molecules, |
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including the chemical structure, an atomistic model, and the |
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head-body ellipsoidal coarse-grained model used in this |
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work.\label{fig:lipidModels}} |
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\end{figure} |
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Our simple molecular-scale lipid model for studying the ripple phase |
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is based on two facts: one is that the most essential feature of lipid |
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molecules is their amphiphilic structure with polar head groups and |
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non-polar tails. Another fact is that the majority of lipid molecules |
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in the ripple phase are relatively rigid (i.e. gel-like) which makes |
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some fraction of the details of the chain dynamics negligible. Figure |
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\ref{fig:lipidModels} shows the molecular strucure of a DPPC |
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molecule, as well as atomistic and molecular-scale representations of |
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a DPPC molecule. The hydrophilic character of the head group is |
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largely due to the separation of charge between the nitrogen and |
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phosphate groups. The zwitterionic nature of the PC headgroups leads |
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to abnormally large dipole moments (as high as 20.6 D), and this |
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strongly polar head group interacts strongly with the solvating water |
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layers immediately surrounding the membrane. The hydrophobic tail |
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consists of fatty acid chains. In our molecular scale model, lipid |
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molecules have been reduced to these essential features; the fatty |
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acid chains are represented by an ellipsoid with a dipolar ball |
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perched on one end to represent the effects of the charge-separated |
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head group. In real PC lipids, the direction of the dipole is |
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nearly perpendicular to the tail, so we have fixed the direction of |
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the point dipole rigidly in this orientation. |
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|
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The ellipsoidal portions of the model interact via the Gay-Berne |
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potential which has seen widespread use in the liquid crystal |
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community. Ayton and Voth have also used Gay-Berne ellipsoids for |
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modelling large length-scale properties of lipid |
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bilayers.\cite{Ayton01} In its original form, the Gay-Berne potential |
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was a single site model for the interactions of rigid ellipsoidal |
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molecules.\cite{Gay81} It can be thought of as a modification of the |
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Gaussian overlap model originally described by Berne and |
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Pechukas.\cite{Berne72} The potential is constructed in the familiar |
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form of the Lennard-Jones function using orientation-dependent |
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$\sigma$ and $\epsilon$ parameters, |
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\begin{eqnarray*} |
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V_{ij}({\mathbf{\hat u}_i}, {\mathbf{\hat u}_j}, {\mathbf{\hat |
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r}_{ij}}) = 4\epsilon ({\mathbf{\hat u}_i}, {\mathbf{\hat u}_j}, |
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{\mathbf{\hat r}_{ij}})\left[\left(\frac{\sigma_0}{r_{ij}-\sigma({\mathbf{\hat u}_i}, |
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{\mathbf{\hat u}_j}, {\mathbf{\hat r}_{ij}})+\sigma_0}\right)^{12} |
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-\left(\frac{\sigma_0}{r_{ij}-\sigma({\mathbf{\hat u}_i}, {\mathbf{\hat u}_j}, |
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{\mathbf{\hat r}_{ij}})+\sigma_0}\right)^6\right] |
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\label{eq:gb} |
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\end{eqnarray*} |
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The range $(\sigma({\bf \hat{u}}_{i},{\bf \hat{u}}_{j},{\bf |
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\hat{r}}_{ij}))$, and strength $(\epsilon({\bf \hat{u}}_{i},{\bf |
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\hat{u}}_{j},{\bf \hat{r}}_{ij}))$ parameters |
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are dependent on the relative orientations of the two molecules (${\bf |
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\hat{u}}_{i},{\bf \hat{u}}_{j}$) as well as the direction of the |
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intermolecular separation (${\bf \hat{r}}_{ij}$). $\sigma$ and |
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$\sigma_0$ are also governed by shape mixing and anisotropy variables, |
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\begin {equation} |
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\begin{array}{rcl} |
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\sigma_0 & = & \sqrt{d_i^2 + d_j^2} \\ \\ |
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\chi & = & \left[ \frac{\left( l_i^2 - d_i^2 \right) \left(l_j^2 - |
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d_j^2 \right)}{\left( l_j^2 + d_i^2 \right) \left(l_i^2 + |
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d_j^2 \right)}\right]^{1/2} \\ \\ |
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\alpha^2 & = & \left[ \frac{\left( l_i^2 - d_i^2 \right) \left(l_j^2 + |
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d_i^2 \right)}{\left( l_j^2 - d_j^2 \right) \left(l_i^2 + |
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d_j^2 \right)}\right]^{1/2}, |
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\end{array} |
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\end{equation} |
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where $l$ and $d$ describe the length and width of each uniaxial |
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ellipsoid. These shape anisotropy parameters can then be used to |
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calculate the range function, |
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\begin {equation} |
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\sigma({\bf \hat{u}}_{i},{\bf \hat{u}}_{j},{\bf \hat{r}}_{ij}) = \sigma_{0} |
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\left[ 1- \left\{ \frac{ \chi \alpha^2 ({\bf \hat{u}}_i \cdot {\bf |
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\hat{r}}_{ij} ) + \chi \alpha^{-2} ({\bf \hat{u}}_j \cdot {\bf |
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\hat{r}}_{ij} ) - 2 \chi^2 ({\bf \hat{u}}_i \cdot {\bf |
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\hat{r}}_{ij} )({\bf \hat{u}}_j \cdot {\bf |
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\hat{r}}_{ij} ) ({\bf \hat{u}}_i \cdot {\bf \hat{u}}_j)}{1 - \chi^2 |
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\left({\bf \hat{u}}_i \cdot {\bf \hat{u}}_j\right)^2} \right\} |
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\right]^{-1/2} |
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\end{equation} |
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Gay-Berne ellipsoids also have an energy scaling parameter, |
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$\epsilon^s$, which describes the well depth for two identical |
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ellipsoids in a {\it side-by-side} configuration. Additionaly, a well |
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depth aspect ratio, $\epsilon^r = \epsilon^e / \epsilon^s$, describes |
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the ratio between the well depths in the {\it end-to-end} and |
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side-by-side configurations. As in the range parameter, a set of |
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mixing and anisotropy variables can be used to describe the well |
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depths for dissimilar particles, |
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\begin {eqnarray*} |
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\epsilon_0 & = & \sqrt{\epsilon^s_i * \epsilon^s_j} \\ \\ |
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\epsilon^r & = & \sqrt{\epsilon^r_i * \epsilon^r_j} \\ \\ |
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\chi' & = & \frac{1 - (\epsilon^r)^{1/\mu}}{1 + (\epsilon^r)^{1/\mu}} |
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\\ \\ |
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\alpha'^2 & = & \left[1 + (\epsilon^r)^{1/\mu}\right]^{-1} |
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\end{eqnarray*} |
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The form of the strength function is somewhat complicated, |
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\begin {eqnarray*} |
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\epsilon({\bf \hat{u}}_{i}, {\bf \hat{u}}_{j},{\bf \hat{r}}_{ij}) & = & |
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\epsilon_{0} \epsilon_{1}^{\nu}({\bf \hat{u}}_{i}.{\bf \hat{u}}_{j}) |
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\epsilon_{2}^{\mu}({\bf \hat{u}}_{i},{\bf \hat{u}}_{j},{\bf |
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\hat{r}}_{ij}) \\ \\ |
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\epsilon_{1}({\bf \hat{u}}_{i},{\bf \hat{u}}_{j}) & = & |
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\left[1-\chi^{2}({\bf \hat{u}}_{i}.{\bf |
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\hat{u}}_{j})^{2}\right]^{-1/2} \\ \\ |
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\epsilon_{2}({\bf \hat{u}}_{i},{\bf \hat{u}}_{j},{\bf \hat{r}}_{ij}) & |
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= & |
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1 - \left\{ \frac{ \chi' \alpha'^2 ({\bf \hat{u}}_i \cdot {\bf |
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\hat{r}}_{ij} ) + \chi' \alpha'^{-2} ({\bf \hat{u}}_j \cdot {\bf |
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\hat{r}}_{ij} ) - 2 \chi'^2 ({\bf \hat{u}}_i \cdot {\bf |
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\hat{r}}_{ij} )({\bf \hat{u}}_j \cdot {\bf |
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\hat{r}}_{ij} ) ({\bf \hat{u}}_i \cdot {\bf \hat{u}}_j)}{1 - \chi'^2 |
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\left({\bf \hat{u}}_i \cdot {\bf \hat{u}}_j\right)^2} \right\}, |
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\end {eqnarray*} |
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although many of the quantities and derivatives are identical with |
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those obtained for the range parameter. Ref. \onlinecite{Luckhurst90} |
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has a particularly good explanation of the choice of the Gay-Berne |
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parameters $\mu$ and $\nu$ for modeling liquid crystal molecules. An |
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excellent overview of the computational methods that can be used to |
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efficiently compute forces and torques for this potential can be found |
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in Ref. \onlinecite{Golubkov06} |
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The choices of parameters we have used in this study correspond to a |
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shape anisotropy of 3 for the chain portion of the molecule. In |
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principle, this could be varied to allow for modeling of longer or |
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shorter chain lipid molecules. For these prolate ellipsoids, we have: |
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\begin{equation} |
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\begin{array}{rcl} |
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d & < & l \\ |
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\epsilon^{r} & < & 1 |
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\end{array} |
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\end{equation} |
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A sketch of the various structural elements of our molecular-scale |
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lipid / solvent model is shown in figure \ref{fig:lipidModel}. The |
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actual parameters used in our simulations are given in table |
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\ref{tab:parameters}. |
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|
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\begin{figure}[htb] |
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\centering |
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\includegraphics[width=4in]{2lipidModel} |
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\caption{The parameters defining the behavior of the lipid |
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models. $l / d$ is the ratio of the head group to body diameter. |
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Molecular bodies had a fixed aspect ratio of 3.0. The solvent model |
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was a simplified 4-water bead ($\sigma_w \approx d$) that has been |
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used in other coarse-grained (DPD) simulations. The dipolar strength |
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(and the temperature and pressure) were the only other parameters that |
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were varied systematically.\label{fig:lipidModel}} |
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\end{figure} |
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|
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To take into account the permanent dipolar interactions of the |
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zwitterionic head groups, we place fixed dipole moments $\mu_{i}$ at |
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one end of the Gay-Berne particles. The dipoles are oriented at an |
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angle $\theta = \pi / 2$ relative to the major axis. These dipoles |
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are protected by a head ``bead'' with a range parameter which we have |
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varied between $1.20 d$ and $1.41 d$. The head groups interact with |
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each other using a combination of Lennard-Jones, |
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\begin{eqnarray*} |
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V_{ij}(r_{ij}) = 4\epsilon_h \left[\left(\frac{\sigma_h}{r_{ij}}\right)^{12} - |
300 |
gezelter |
3195 |
\left(\frac{\sigma_h}{r_{ij}}\right)^6\right], |
301 |
xsun |
3174 |
\end{eqnarray*} |
302 |
gezelter |
3199 |
and dipole-dipole, |
303 |
xsun |
3174 |
\begin{eqnarray*} |
304 |
gezelter |
3200 |
V_{ij}({\bf \hat{u}}_{i},{\bf \hat{u}}_{j},{\bf |
305 |
|
|
\hat{r}}_{ij})) = \frac{|\mu|^2}{4 \pi \epsilon_0 r_{ij}^3} |
306 |
gezelter |
3195 |
\left[ \hat{\bf u}_i \cdot \hat{\bf u}_j - 3 (\hat{\bf u}_i \cdot |
307 |
|
|
\hat{\bf r}_{ij})(\hat{\bf u}_j \cdot \hat{\bf r}_{ij}) \right] |
308 |
xsun |
3174 |
\end{eqnarray*} |
309 |
gezelter |
3195 |
potentials. |
310 |
|
|
In these potentials, $\mathbf{\hat u}_i$ is the unit vector pointing |
311 |
|
|
along dipole $i$ and $\mathbf{\hat r}_{ij}$ is the unit vector |
312 |
gezelter |
3199 |
pointing along the inter-dipole vector $\mathbf{r}_{ij}$. |
313 |
gezelter |
3195 |
|
314 |
|
|
For the interaction between nonequivalent uniaxial ellipsoids (in this |
315 |
gezelter |
3199 |
case, between spheres and ellipsoids), the spheres are treated as |
316 |
|
|
ellipsoids with an aspect ratio of 1 ($d = l$) and with an well depth |
317 |
gezelter |
3200 |
ratio ($\epsilon^r$) of 1 ($\epsilon^e = \epsilon^s$). The form of |
318 |
|
|
the Gay-Berne potential we are using was generalized by Cleaver {\it |
319 |
|
|
et al.} and is appropriate for dissimilar uniaxial |
320 |
|
|
ellipsoids.\cite{Cleaver96} |
321 |
xsun |
3147 |
|
322 |
gezelter |
3199 |
The solvent model in our simulations is identical to one used by |
323 |
|
|
Marrink {\it et al.} in their dissipative particle dynamics (DPD) |
324 |
|
|
simulation of lipid bilayers.\cite{Marrink04} This solvent bead is a single |
325 |
|
|
site that represents four water molecules (m = 72 amu) and has |
326 |
|
|
comparable density and diffusive behavior to liquid water. However, |
327 |
|
|
since there are no electrostatic sites on these beads, this solvent |
328 |
|
|
model cannot replicate the dielectric properties of water. |
329 |
xsun |
3198 |
\begin{table*} |
330 |
|
|
\begin{minipage}{\linewidth} |
331 |
|
|
\begin{center} |
332 |
gezelter |
3199 |
\caption{Potential parameters used for molecular-scale coarse-grained |
333 |
|
|
lipid simulations} |
334 |
|
|
\begin{tabular}{llccc} |
335 |
xsun |
3198 |
\hline |
336 |
gezelter |
3199 |
& & Head & Chain & Solvent \\ |
337 |
xsun |
3198 |
\hline |
338 |
gezelter |
3200 |
$d$ (\AA) & & varied & 4.6 & 4.7 \\ |
339 |
|
|
$l$ (\AA) & & $= d$ & 13.8 & 4.7 \\ |
340 |
gezelter |
3199 |
$\epsilon^s$ (kcal/mol) & & 0.185 & 1.0 & 0.8 \\ |
341 |
|
|
$\epsilon_r$ (well-depth aspect ratio)& & 1 & 0.2 & 1 \\ |
342 |
gezelter |
3200 |
$m$ (amu) & & 196 & 760 & 72.06 \\ |
343 |
gezelter |
3199 |
$\overleftrightarrow{\mathsf I}$ (amu \AA$^2$) & & & & \\ |
344 |
|
|
\multicolumn{2}c{$I_{xx}$} & 1125 & 45000 & N/A \\ |
345 |
|
|
\multicolumn{2}c{$I_{yy}$} & 1125 & 45000 & N/A \\ |
346 |
|
|
\multicolumn{2}c{$I_{zz}$} & 0 & 9000 & N/A \\ |
347 |
|
|
$\mu$ (Debye) & & varied & 0 & 0 \\ |
348 |
xsun |
3198 |
\end{tabular} |
349 |
|
|
\label{tab:parameters} |
350 |
|
|
\end{center} |
351 |
|
|
\end{minipage} |
352 |
|
|
\end{table*} |
353 |
gezelter |
3195 |
|
354 |
gezelter |
3199 |
A switching function has been applied to all potentials to smoothly |
355 |
|
|
turn off the interactions between a range of $22$ and $25$ \AA. |
356 |
gezelter |
3186 |
|
357 |
gezelter |
3200 |
The parameters that were systematically varied in this study were the |
358 |
|
|
size of the head group ($\sigma_h$), the strength of the dipole moment |
359 |
|
|
($\mu$), and the temperature of the system. Values for $\sigma_h$ |
360 |
|
|
ranged from 5.5 \AA\ to 6.5 \AA\ . If the width of the tails is |
361 |
|
|
taken to be the unit of length, these head groups correspond to a |
362 |
|
|
range from $1.2 d$ to $1.41 d$. Since the solvent beads are nearly |
363 |
|
|
identical in diameter to the tail ellipsoids, all distances that |
364 |
|
|
follow will be measured relative to this unit of distance. |
365 |
|
|
|
366 |
gezelter |
3196 |
\section{Experimental Methodology} |
367 |
xsun |
3174 |
\label{sec:experiment} |
368 |
xsun |
3147 |
|
369 |
gezelter |
3196 |
To create unbiased bilayers, all simulations were started from two |
370 |
gezelter |
3200 |
perfectly flat monolayers separated by a 26 \AA\ gap between the |
371 |
gezelter |
3196 |
molecular bodies of the upper and lower leaves. The separated |
372 |
|
|
monolayers were evolved in a vaccum with $x-y$ anisotropic pressure |
373 |
xsun |
3174 |
coupling. The length of $z$ axis of the simulations was fixed and a |
374 |
|
|
constant surface tension was applied to enable real fluctuations of |
375 |
gezelter |
3200 |
the bilayer. Periodic boundary conditions were used, and $480-720$ |
376 |
|
|
lipid molecules were present in the simulations, depending on the size |
377 |
|
|
of the head beads. In all cases, the two monolayers spontaneously |
378 |
|
|
collapsed into bilayer structures within 100 ps. Following this |
379 |
|
|
collapse, all systems were equlibrated for $100$ ns at $300$ K. |
380 |
xsun |
3147 |
|
381 |
gezelter |
3200 |
The resulting bilayer structures were then solvated at a ratio of $6$ |
382 |
gezelter |
3196 |
solvent beads (24 water molecules) per lipid. These configurations |
383 |
gezelter |
3200 |
were then equilibrated for another $30$ ns. All simulations utilizing |
384 |
|
|
the solvent were carried out at constant pressure ($P=1$ atm) with |
385 |
|
|
$3$D anisotropic coupling, and constant surface tension |
386 |
|
|
($\gamma=0.015$ UNIT). Given the absence of fast degrees of freedom in |
387 |
|
|
this model, a timestep of $50$ fs was utilized with excellent energy |
388 |
|
|
conservation. Data collection for structural properties of the |
389 |
|
|
bilayers was carried out during a final 5 ns run following the solvent |
390 |
|
|
equilibration. All simulations were performed using the OOPSE |
391 |
|
|
molecular modeling program.\cite{Meineke05} |
392 |
gezelter |
3196 |
|
393 |
|
|
\section{Results} |
394 |
xsun |
3174 |
\label{sec:results} |
395 |
xsun |
3147 |
|
396 |
xsun |
3174 |
Snapshots in Figure \ref{fig:phaseCartoon} show that the membrane is |
397 |
gezelter |
3200 |
more corrugated with increasing size of the head groups. The surface |
398 |
|
|
is nearly flat when $\sigma_h=1.20 d$. With $\sigma_h=1.28 d$, |
399 |
|
|
although the surface is still flat, the bilayer starts to splay |
400 |
|
|
inward; the upper leaf of the bilayer is connected to the lower leaf |
401 |
|
|
with an interdigitated line defect. Two periodicities with $100$ \AA\ |
402 |
|
|
wavelengths were observed in the simulation. This structure is very |
403 |
|
|
similiar to the structure observed by de Vries and Lenz {\it et |
404 |
|
|
al.}. The same basic structure is also observed when $\sigma_h=1.41 |
405 |
|
|
d$, but the wavelength of the surface corrugations depends sensitively |
406 |
|
|
on the size of the ``head'' beads. From the undulation spectrum, the |
407 |
|
|
corrugation is clearly non-thermal. |
408 |
xsun |
3174 |
\begin{figure}[htb] |
409 |
|
|
\centering |
410 |
gezelter |
3199 |
\includegraphics[width=4in]{phaseCartoon} |
411 |
xsun |
3174 |
\caption{A sketch to discribe the structure of the phases observed in |
412 |
|
|
our simulations.\label{fig:phaseCartoon}} |
413 |
|
|
\end{figure} |
414 |
xsun |
3147 |
|
415 |
gezelter |
3200 |
When $\sigma_h=1.35 d$, we observed another corrugated surface |
416 |
|
|
morphology. This structure is different from the asymmetric rippled |
417 |
xsun |
3174 |
surface; there is no interdigitation between the upper and lower |
418 |
|
|
leaves of the bilayer. Each leaf of the bilayer is broken into several |
419 |
|
|
hemicylinderical sections, and opposite leaves are fitted together |
420 |
|
|
much like roof tiles. Unlike the surface in which the upper |
421 |
|
|
hemicylinder is always interdigitated on the leading or trailing edge |
422 |
gezelter |
3200 |
of lower hemicylinder, this ``symmetric'' ripple has no prefered |
423 |
|
|
direction. The corresponding structures are shown in Figure |
424 |
xsun |
3174 |
\ref{fig:phaseCartoon} for elucidation of the detailed structures of |
425 |
gezelter |
3200 |
different phases. The top panel in figure \ref{fig:phaseCartoon} is |
426 |
|
|
the flat phase, the middle panel shows the asymmetric ripple phase |
427 |
|
|
corresponding to $\sigma_h = 1.41 d$ and the lower panel shows the |
428 |
|
|
symmetric ripple phase observed when $\sigma_h=1.35 d$. In the |
429 |
|
|
symmetric ripple, the bilayer is continuous over the whole membrane, |
430 |
|
|
however, in asymmetric ripple phase, the bilayer domains are connected |
431 |
|
|
by thin interdigitated monolayers that share molecules between the |
432 |
|
|
upper and lower leaves. |
433 |
xsun |
3174 |
\begin{table*} |
434 |
|
|
\begin{minipage}{\linewidth} |
435 |
|
|
\begin{center} |
436 |
gezelter |
3200 |
\caption{Phases, ripple wavelengths and amplitudes observed as a |
437 |
|
|
function of the ratio between the head beads and the diameters of the |
438 |
|
|
tails. All lengths are normalized to the diameter of the tail |
439 |
|
|
ellipsoids.} |
440 |
xsun |
3174 |
\begin{tabular}{lccc} |
441 |
|
|
\hline |
442 |
gezelter |
3200 |
$\sigma_h / d$ & type of phase & $\lambda / d$ & $A / d$\\ |
443 |
xsun |
3174 |
\hline |
444 |
|
|
1.20 & flat & N/A & N/A \\ |
445 |
gezelter |
3200 |
1.28 & asymmetric ripple or flat & 21.7 & N/A \\ |
446 |
xsun |
3174 |
1.35 & symmetric ripple & 17.2 & 2.2 \\ |
447 |
|
|
1.41 & asymmetric ripple & 15.4 & 1.5 \\ |
448 |
|
|
\end{tabular} |
449 |
|
|
\label{tab:property} |
450 |
|
|
\end{center} |
451 |
|
|
\end{minipage} |
452 |
|
|
\end{table*} |
453 |
xsun |
3147 |
|
454 |
gezelter |
3200 |
The membrane structures and the reduced wavelength $\lambda / d$, |
455 |
|
|
reduced amplitude $A / d$ of the ripples are summarized in Table |
456 |
|
|
\ref{tab:property}. The wavelength range is $15~21$ molecular bodies |
457 |
|
|
and the amplitude is $1.5$ molecular bodies for asymmetric ripple and |
458 |
|
|
$2.2$ for symmetric ripple. These values are consistent to the |
459 |
|
|
experimental results. Note, that given the lack of structural freedom |
460 |
|
|
in the tails of our model lipids, the amplitudes observed from these |
461 |
|
|
simulations are likely to underestimate of the true amplitudes. |
462 |
xsun |
3174 |
|
463 |
gezelter |
3195 |
\begin{figure}[htb] |
464 |
|
|
\centering |
465 |
gezelter |
3199 |
\includegraphics[width=4in]{topDown} |
466 |
gezelter |
3195 |
\caption{Top views of the flat (upper), asymmetric ripple (middle), |
467 |
|
|
and symmetric ripple (lower) phases. Note that the head-group dipoles |
468 |
|
|
have formed head-to-tail chains in all three of these phases, but in |
469 |
|
|
the two rippled phases, the dipolar chains are all aligned |
470 |
|
|
{\it perpendicular} to the direction of the ripple. The flat membrane |
471 |
|
|
has multiple point defects in the dipolar orientational ordering, and |
472 |
|
|
the dipolar ordering on the lower leaf of the bilayer can be in a |
473 |
|
|
different direction from the upper leaf.\label{fig:topView}} |
474 |
|
|
\end{figure} |
475 |
|
|
|
476 |
gezelter |
3200 |
Figure \ref{fig:topView} shows snapshots of bird's-eye views of the |
477 |
|
|
flat ($\sigma_h = 1.20 d$) and rippled ($\sigma_h = 1.41, 1.35 d$) |
478 |
|
|
bilayers. The directions of the dipoles on the head groups are |
479 |
|
|
represented with two colored half spheres: blue (phosphate) and yellow |
480 |
|
|
(amino). For flat bilayers, the system exhibits signs of |
481 |
|
|
orientational frustration; some disorder in the dipolar chains is |
482 |
|
|
evident with kinks visible at the edges between different ordered |
483 |
|
|
domains. The lipids can also move independently of lipids in the |
484 |
|
|
opposing leaf, so the ordering of the dipoles on one leaf is not |
485 |
|
|
necessarily consistant with the ordering on the other. These two |
486 |
|
|
factors keep the total dipolar order parameter relatively low for the |
487 |
|
|
flat phases. |
488 |
xsun |
3147 |
|
489 |
gezelter |
3200 |
With increasing head group size, the surface becomes corrugated, and |
490 |
|
|
the dipoles cannot move as freely on the surface. Therefore, the |
491 |
|
|
translational freedom of lipids in one layer is dependent upon the |
492 |
|
|
position of lipids in the other layer. As a result, the ordering of |
493 |
|
|
the dipoles on head groups in one leaf is correlated with the ordering |
494 |
|
|
in the other leaf. Furthermore, as the membrane deforms due to the |
495 |
|
|
corrugation, the symmetry of the allowed dipolar ordering on each leaf |
496 |
|
|
is broken. The dipoles then self-assemble in a head-to-tail |
497 |
|
|
configuration, and the dipolar order parameter increases dramatically. |
498 |
|
|
However, the total polarization of the system is still close to zero. |
499 |
|
|
This is strong evidence that the corrugated structure is an |
500 |
|
|
antiferroelectric state. It is also notable that the head-to-tail |
501 |
|
|
arrangement of the dipoles is in a direction perpendicular to the wave |
502 |
|
|
vector for the surface corrugation. This is a similar finding to what |
503 |
|
|
we observed in our earlier work on the elastic dipolar |
504 |
|
|
membranes.\cite{Sun07} |
505 |
|
|
|
506 |
|
|
The $P_2$ order parameters (for both the molecular bodies and the head |
507 |
|
|
group dipoles) have been calculated to quantify the ordering in these |
508 |
|
|
phases. $P_2 = 1$ implies a perfectly ordered structure, and $P_2 = 0$ |
509 |
|
|
implies complete orientational randomization. Figure \ref{fig:rP2} |
510 |
|
|
shows the $P_2$ order parameter for the head-group dipoles increasing |
511 |
|
|
with increasing head group size. When the heads of the lipid molecules |
512 |
|
|
are small, the membrane is nearly flat. The dipolar ordering exhibits |
513 |
|
|
frustrated orientational ordering in this circumstance. |
514 |
|
|
|
515 |
xsun |
3174 |
The ordering of the tails is essentially opposite to the ordering of |
516 |
gezelter |
3200 |
the dipoles on head group. The $P_2$ order parameter {\it decreases} |
517 |
|
|
with increasing head size. This indicates that the surface is more |
518 |
|
|
curved with larger head / tail size ratios. When the surface is flat, |
519 |
|
|
all tails are pointing in the same direction (parallel to the normal |
520 |
|
|
of the surface). This simplified model appears to be exhibiting a |
521 |
|
|
smectic A fluid phase, similar to the real $L_{\beta}$ phase. We have |
522 |
|
|
not observed a smectic C gel phase ($L_{\beta'}$) for this model |
523 |
|
|
system. Increasing the size of the heads, results in rapidly |
524 |
|
|
decreasing $P_2$ ordering for the molecular bodies. |
525 |
gezelter |
3199 |
|
526 |
xsun |
3174 |
\begin{figure}[htb] |
527 |
|
|
\centering |
528 |
|
|
\includegraphics[width=\linewidth]{rP2} |
529 |
gezelter |
3200 |
\caption{The $P_2$ order parameter as a function of the ratio of |
530 |
|
|
$\sigma_h$ to $d$. \label{fig:rP2}} |
531 |
xsun |
3174 |
\end{figure} |
532 |
xsun |
3147 |
|
533 |
xsun |
3174 |
We studied the effects of the interactions between head groups on the |
534 |
|
|
structure of lipid bilayer by changing the strength of the dipole. |
535 |
|
|
Figure \ref{fig:sP2} shows how the $P_2$ order parameter changes with |
536 |
|
|
increasing strength of the dipole. Generally the dipoles on the head |
537 |
|
|
group are more ordered by increase in the strength of the interaction |
538 |
|
|
between heads and are more disordered by decreasing the interaction |
539 |
|
|
stength. When the interaction between the heads is weak enough, the |
540 |
|
|
bilayer structure does not persist; all lipid molecules are solvated |
541 |
|
|
directly in the water. The critial value of the strength of the dipole |
542 |
|
|
depends on the head size. The perfectly flat surface melts at $5$ |
543 |
xsun |
3182 |
$0.03$ debye, the asymmetric rippled surfaces melt at $8$ $0.04$ |
544 |
|
|
$0.03$ debye, the symmetric rippled surfaces melt at $10$ $0.04$ |
545 |
|
|
debye. The ordering of the tails is the same as the ordering of the |
546 |
|
|
dipoles except for the flat phase. Since the surface is already |
547 |
|
|
perfect flat, the order parameter does not change much until the |
548 |
|
|
strength of the dipole is $15$ debye. However, the order parameter |
549 |
|
|
decreases quickly when the strength of the dipole is further |
550 |
|
|
increased. The head groups of the lipid molecules are brought closer |
551 |
|
|
by stronger interactions between them. For a flat surface, a large |
552 |
|
|
amount of free volume between the head groups is available, but when |
553 |
|
|
the head groups are brought closer, the tails will splay outward, |
554 |
|
|
forming an inverse micelle. When $\sigma_h=1.28\sigma_0$, the $P_2$ |
555 |
|
|
order parameter decreases slightly after the strength of the dipole is |
556 |
|
|
increased to $16$ debye. For rippled surfaces, there is less free |
557 |
|
|
volume available between the head groups. Therefore there is little |
558 |
|
|
effect on the structure of the membrane due to increasing dipolar |
559 |
|
|
strength. However, the increase of the $P_2$ order parameter implies |
560 |
|
|
the membranes are flatten by the increase of the strength of the |
561 |
|
|
dipole. Unlike other systems that melt directly when the interaction |
562 |
|
|
is weak enough, for $\sigma_h=1.41\sigma_0$, part of the membrane |
563 |
|
|
melts into itself first. The upper leaf of the bilayer becomes totally |
564 |
|
|
interdigitated with the lower leaf. This is different behavior than |
565 |
|
|
what is exhibited with the interdigitated lines in the rippled phase |
566 |
|
|
where only one interdigitated line connects the two leaves of bilayer. |
567 |
xsun |
3174 |
\begin{figure}[htb] |
568 |
|
|
\centering |
569 |
|
|
\includegraphics[width=\linewidth]{sP2} |
570 |
|
|
\caption{The $P_2$ order parameter as a funtion of the strength of the |
571 |
|
|
dipole.\label{fig:sP2}} |
572 |
|
|
\end{figure} |
573 |
xsun |
3147 |
|
574 |
xsun |
3174 |
Figure \ref{fig:tP2} shows the dependence of the order parameter on |
575 |
|
|
temperature. The behavior of the $P_2$ order paramter is |
576 |
|
|
straightforward. Systems are more ordered at low temperature, and more |
577 |
|
|
disordered at high temperatures. When the temperature is high enough, |
578 |
xsun |
3182 |
the membranes are instable. For flat surfaces ($\sigma_h=1.20\sigma_0$ |
579 |
|
|
and $\sigma_h=1.28\sigma_0$), when the temperature is increased to |
580 |
|
|
$310$, the $P_2$ order parameter increases slightly instead of |
581 |
|
|
decreases like ripple surface. This is an evidence of the frustration |
582 |
|
|
of the dipolar ordering in each leaf of the lipid bilayer, at low |
583 |
|
|
temperature, the systems are locked in a local minimum energy state, |
584 |
|
|
with increase of the temperature, the system can jump out the local |
585 |
|
|
energy well to find the lower energy state which is the longer range |
586 |
|
|
orientational ordering. Like the dipolar ordering of the flat |
587 |
|
|
surfaces, the ordering of the tails of the lipid molecules for ripple |
588 |
|
|
membranes ($\sigma_h=1.35\sigma_0$ and $\sigma_h=1.41\sigma_0$) also |
589 |
|
|
show some nonthermal characteristic. With increase of the temperature, |
590 |
|
|
the $P_2$ order parameter decreases firstly, and increases afterward |
591 |
|
|
when the temperature is greater than $290 K$. The increase of the |
592 |
|
|
$P_2$ order parameter indicates a more ordered structure for the tails |
593 |
|
|
of the lipid molecules which corresponds to a more flat surface. Since |
594 |
|
|
our model lacks the detailed information on lipid tails, we can not |
595 |
|
|
simulate the fluid phase with melted fatty acid chains. Moreover, the |
596 |
|
|
formation of the tilted $L_{\beta'}$ phase also depends on the |
597 |
|
|
organization of fatty groups on tails. |
598 |
xsun |
3174 |
\begin{figure}[htb] |
599 |
|
|
\centering |
600 |
|
|
\includegraphics[width=\linewidth]{tP2} |
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\caption{The $P_2$ order parameter as a funtion of |
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temperature.\label{fig:tP2}} |
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\end{figure} |
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\section{Discussion} |
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\label{sec:discussion} |
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gezelter |
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\newpage |
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\bibliography{mdripple} |
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\end{document} |