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Review
. 2000 Nov 10;1469(3):159-95.
doi: 10.1016/s0304-4157(00)00016-2.

Structure of lipid bilayers

J F Nagle  1 , S Tristram-Nagle
Affiliations
Review

Structure of lipid bilayers

J F Nagle et al. Biochim Biophys Acta. .

Abstract

The quantitative experimental uncertainty in the structure of fully hydrated, biologically relevant, fluid (L(alpha)) phase lipid bilayers has been too large to provide a firm base for applications or for comparison with simulations. Many structural methods are reviewed including modern liquid crystallography of lipid bilayers that deals with the fully developed undulation fluctuations that occur in the L(alpha) phase. These fluctuations degrade the higher order diffraction data in a way that, if unrecognized, leads to erroneous conclusions regarding bilayer structure. Diffraction measurements at high instrumental resolution provide a measure of these fluctuations. In addition to providing better structural determination, this opens a new window on interactions between bilayers, so the experimental determination of interbilayer interaction parameters is reviewed briefly. We introduce a new structural correction based on fluctuations that has not been included in any previous studies. Updated measurements, such as for the area compressibility modulus, are used to provide adjustments to many of the literature values of structural quantities. Since the gel (L(beta)') phase is valuable as a stepping stone for obtaining fluid phase results, a brief review is given of the lower temperature phases. The uncertainty in structural results for lipid bilayers is being reduced and best current values are provided for bilayers of five lipids.

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Figures

Fig. 1
Fig. 1
Summary of published areas for fluid phase DPPC at 50°C (black) and gel phase DPPC (grey) at 20°C. References: aSun et al. [4], bPace and Chan [9], cBüldt et al. [10], dSchindler and Seelig [11], eNagle et al. [3], fLewis and Engelman [12], gRand and Parsegian [1] and Janiak et al. [13], hDeYoung and Dill [14], iLis et al. [15], jThurmond et al. [16].
Fig. 2
Fig. 2
Three representations of structure of DPPC bilayers in the Lα fluid phase. (a) Probability distribution functions p for different component groups from simulations [20] and the downward pointing arrows show the peak locations determined by neutron diffraction with 25% water [10]. The equality of the areas denoted α and β locates the Gibbs dividing surface for the hydrocarbon region determined by the simulation. (b) Electron density profile ρ* from X-ray studies (solid line) [3] and from simulations (dots) (contributed by Scott Feller). (c) Two volumetric pictures. The version on the left monolayer is a simple three compartment representation. The version on the right monolayer is a more realistic representation of the interfacial headgroup region [26]. DC is the experimentally determined Gibbs dividing surface for the hydrocarbon region. The x-axis is in Å along the bilayer normal with the same scale for a, b and c. The y-axis in c shows a lateral dimension along the surface of the bilayer. Values for the parameters in c are taken from Table 6.
Fig. 3
Fig. 3
Schematic view of MLVs with defect regions of excess water. Figure reproduced from [63] with permission of the authors.
Fig. 4
Fig. 4
Snapshot of fluctuations from a non-atomic level Monte Carlo simulation [91].
Fig. 5
Fig. 5
Example of hidden diffuse scattering under h = 3 peak in DOPC. The solid line is the fit that is determined by the first three orders of diffraction. The dashed horizontal line shows the background corrected baseline, drawn at zero counts. There is a large integrated intensity in the tails that extend halfway to the next peak which is located at Δq = 0.1 Å−1. The dotted line shows the resolution function.
Fig. 6
Fig. 6
The solid line shows the continuous transform F(q) for fully hydrated gel phase DPPC. The data points show the discrete form factors Fh for h = 1−10 for five different values of D from 58.7 Å to fully hydrated 63.2 Å. The phase factors are indicated by the signs under each lobe. The first five phase factors are obvious. The next five require more detailed analysis [39,49].
Fig. 7
Fig. 7
Dependence of A versus ADWP for DOPC at 30°C [38]. The solid line is the best fit with slope −1/KA corresponding to KA = 188 dyn/cm. The dotted line is the best fit using KA = 265 dyn/cm from [17].
Fig. 8
Fig. 8
Osmotic pressure P versus steric water space DW′. Various lines show contributions from various interactions, with the bold solid curve showing the fitted total P.
Fig. 9
Fig. 9
Functional form of fluctuation free energy versus water spacing is represented by an exponential with decay length λfl = 5.9 Å = 3λh (solid line).
Fig. 10
Fig. 10
Schematic of two sections of a fluctuating bilayer (plus associated water) in an MLV. The left section has its local normal along the average normal N and the right section is tilted by angle θ. A local unit cell is drawn in each section. The local thickness DB+DW is given by Dcosθ.
Fig. 11
Fig. 11
Electron density map obtained using X-ray phases from [147] and intensity data from [146] for the ripple thermodynamic phase of DMPC with 25% water (nW = 13) at 18°C. The rippling repeat period is 142 Å (length of unit cell) and the lamellar repeat is 58 Å (height of unit cell). The profiles show a major M side (across A) that has the same thickness as the gel phase and a thinner minor m side (across B). The presence of a thin water layer between bilayers (across C) indicates complete inner shell hydration of the headgroups.
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