Hydrostatic Pressure Effects on the Lamellar to Gyroid Cubic Phase

Aug 15, 2012 - H. M. G. Barriga , R. V. Law , J. M. Seddon , O. Ces , N. J. Brooks. Physical Chemistry Chemical Physics 2016 18 (1), 149-155 ...
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Hydrostatic Pressure Effects on the Lamellar to Gyroid Cubic Phase Transition of Monolinolein at Limited Hydration T.-Y. Dora Tang,*,† Nicholas J. Brooks,† Christoph Jeworrek,‡ Oscar Ces,† Nick J. Terrill,§ Roland Winter,‡ Richard H. Templer,† and John M. Seddon*,† †

Department of Chemistry, Imperial College London, South Kensington Campus, London SW7 2AZ, United Kingdom Technical University of Dortmund, D-44221 Dortmund, Germany § Diamond Light Source, Harwell Science and Innovation Campus, Didcot, Oxfordshire OX11 0DE, United Kingdom ‡

ABSTRACT: Monoacylglycerol based lipids are highly important model membrane components and attractive candidates for drug encapsulation and as delivery agents. However, optimizing the properties of these lipids for applications requires a detailed understanding of the thermodynamic factors governing the self-assembled structures that they form. Here, we report on the effects of hydrostatic pressure, temperature, and water composition on the structural behavior and stability of inverse lyotropic liquid crystalline phases adopted by monolinolein (an unsaturated monoacylglycerol having cis-double bonds at carbon positions 9 and 12) under limited hydration conditions. Six pressure−temperature phase diagrams have been determined using small-angle X-ray diffraction at water contents between 15 wt % and 27 wt % water, in the range 10−40 °C and 1−3000 bar. The gyroid bicontinuous cubic (QIIG) phase is formed at low pressure and high temperatures, transforming to a fluid lamellar (Lα) phase at high pressures and low temperature via a region of QIIG/Lα coexistence. Pressure stabilizes the lamellar phase over the QIIG phase; at fixed pressure, increasing the water content causes the coexistence region to move to lower temperature. These trends are consistent throughout the hydration range studied. Moreover, at fixed temperature, increasing the water composition increases the pressure at which the QIIG to Lα transition takes place. We discuss the qualitative effect of pressure, temperature, and water content on the stability of the QIIG phase.

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INTRODUCTION Biological amphiphiles, such as lipids, can exhibit complex lyotropic phase behavior when mixed with water. Hydrated lipid systems can form a variety of lamellar and nonlamellar phases and transitions between these phases can be affected by changing factors including the structure of the lipid head or tail group, the hydration, temperature, pressure, or pH. The lamellar phase, which is ubiquitous in the cell membrane, consists of lipid bilayers separated by water; this phase is stabilized by a balance of attractive van der Waals forces and hydration repulsion between the bilayers. Under suitable conditions, rather than assembling into flat sheets, lipid bilayers will prefer to form structures with curved interfaces, for example, the inverse bicontinuous cubic phases. In such curved phases, two lipid monolayers pack tail-to-tail on either side of a periodic minimal surface, which has zero mean curvature and divides space into two equivalent subvolumes. The most wellcharacterized and well-known of these structures are the QIIG, QIID, and QIIP phases1 which are based on the Schoen (G) minimal surface (Figure 1) and the Schwarz D and P minimal surfaces, respectively. The QII phases have important roles in static and dynamic processes within the cell membrane, and in addition, the biocompatibility of lipid based nanostructures and their large surface area to volume ratios make them attractive candidates for drug encapsulation and therapeutic delivery © 2012 American Chemical Society

Figure 1. Schoen (G) minimal surface on which the QIIG phase is based.

devices.2,3 However, the factors which govern the stability of these structures are still not well-understood. Received: June 26, 2012 Revised: August 7, 2012 Published: August 15, 2012 13018

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negligible and it can be assumed that the contribution from packing frustration from the hydrocarbon chains is obtained by 2 multiplying gchain PF by a , where a is the lattice parameter of the bicontinuous cubic phase.6,7

Theoretical modeling of the inverse bicontinuous cubic phases has predicted that their stability arises due to a balance between the curvature elastic energy (gc),4 packing frustration (gPF) (Figure 2), and a third term (ginter) which accounts for

chain gPF = λ (l 2 − l r 2 )

The energetics of the inverse bicontinuous cubic phases can be modeled by constraining the shape of the interface, to either a surface which lies at a uniform distance from the bilayer midplane (parallel interface model, PIM) or a constant mean curvature interface (constant mean curvature model, CMCM). In both of these models, the interface will be subject to frustration and there will be a higher contribution to the energy functional from curvature elasticity energy when considering the PIM and from packing frustration in the CMCM case. However, the exact details of the balance and coupled contributions of the curvature elasticity and packing frustration are still not well-characterized despite recent progress in our understanding of the factors which stabilize the bicontinuous cubics from theory and experiments.8,9 In order to develop a complete and accurate representation of the energetics of the bicontinuous cubic phases, one requires an experimental description of their phase behavior as a function of temperature, pressure, and chemical potential. To date, little research has focused on the effects of hydrostatic pressure on the stability of these curved mesophases under limited hydrated conditions. An understanding of the parameters contributing to the free energy of these mesophases, as a function of pressure and hydration, is crucial to developing a full thermodynamic model of lyotropic phase behavior. This information will be extremely important in rational design of drug delivery systems and novel biocompatible materials,2,3 based on complex lyotropic phases, and may prove significant for deepening our present understanding of membrane stability in deep sea organisms10 and phenomena such as the pressure reversal of anesthesia.11 Increasing pressure often has a qualitatively similar effect as decreasing temperature on the phase behavior of lipid systems. Increasing temperature increases the number of trans-gauche rotamers in the hydrocarbon chain and so increases the chain splay and hence the spontaneous inverse curvature of the monolayers. An increase in hydrostatic pressure is associated with lateral compression of the membrane and a decrease in volume in the hydrocarbon region, which is achieved by

Figure 2. In a symmetric bilayer, there may be a desire for the monolayer leaflets to curve; however, formation of voids is energetically unfavorable. Void formation can be avoided by either (a) the monolayer leaflets lying back to back, which forces the leaflets away from their preferred curvature and introduces stored curvature stress, or (b) the chain extension changing to fill the voids, which forces the chains away from their preferred length and introduces packing frustration.

other interactions such as hydration and electrostatic forces. The third term is assumed to be negligible if the interbilayer spacing is greater than 5 Å; thus, only the curvature elastic energy and the packing frustration are considered to contribute to the free energy of the system. The curvature elastic energy per unit area of a monolayer (gc) is given by eq 1.4 gc = 2κ(H − Ho)2 + κGK

(2)

(1)

where H = 1/2(c1 + c2) and K = c1c2 (H and K are the local mean and Gaussian curvatures respectively defined by the principal curvatures, c1 and c2 of the two principal radii of the surface at a given point),5 H0 is the spontaneous mean curvature (which is zero for a symmetric bilayer), κ is the mean curvature modulus, and κG is the Gaussian curvature modulus. The contribution to the energy functional from packing frustration of the hydrocarbon chain (gchain PF ) in the hydrocarbon region is given by eq 26 where λ is the chain extension modulus, l is the hydrocarbon chain length, and lr is the relaxed length of the hydrocarbon chain. The variance of l in the lipid region is

Figure 3. Plots to show the change in lattice parameter with time at 38.5 °C and 22.2 wt % water and varying pressures. The pressure was increased sequentially, and the time measurement was started after setting each pressure. (a) QIIG phase at 1, 800, 1200, 1800, and 2000 bar. (b) Lamellar phase at 1800, 2000, 2500, and 3000 bar. 13019

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Figure 4. Two-dimensional diffraction patterns and radially integrated diffraction plots from the QIIG phase (a and b) for 20.9 wt % water at 25.6 °C and 1 bar and lamellar phase (c and d) at 22.2 wt % water at 20.4 °C and 1800 bar.

with increasing amounts of water. This anomalous phase sequence has previously been attributed to competition among the hydrophobic effect, hydrocarbon chain entropy, and headgroup hydrogen bond formation, and changes in headgroup volume due to increased hydration.16,17 However, this effect may also be due to competition between the intrinsic preferred curvature of the lipid (Type II) and the amount of water available to fill the aqueous regions in the curved structure. At low hydration (and so low water volume fraction), there may be insufficient water to fill the aqueous channels of a favorable inverse curvature structure, and it becomes more energetically favorable for the lipids to adopt a curvaturestressed lamellar phase. We have used high-pressure synchrotron X-ray diffraction to systematically characterize the effect of pressure, temperature, and water content on the stability of the QIIG phase of monolinolein under limited hydrated conditions from 15 to 27 wt % water. By doing this, we aim to deconvolute the factors that control phase stability in these systems.

longitudinal chain extension and ordering. Consequently, the packing of the lipid molecules becomes denser and the spontaneous curvature at the interface decreases. There may also be an increased energetic contribution from gPF due to an increase in the bending modulus.12 However, it is important to note that increasing temperature and pressure are not quantitatively opposing, as increasing the temperature increases the number of chains that can access higher rotomeric energy levels, while increasing the pressure leads to an increase in the energy gap between the rotomeric levels, thereby reducing occupancy of the higher energy levels. Pressure is an ideal thermodynamic parameter for studying the phase behavior of lyotropic liquid crystalline phases, as it does not significantly disrupt intramolecular bonding below 2 GPa (20 kbar) or affect the solvent properties of the lipid/water mixture. However, high pressure is still relatively under-utilized in studies of biological materials, primarily due to the requirement for specialized instrumentation.13,14 It is usually expected that increasing the water content of a lamellar phase leads to increased hydration and area of the headgroup, so the bilayer curves away from the water giving increased positive curvature and the formation of Type I phases.15 However, the monoacylglycerols form lamellar phases at low water contents and Type II (inverse) phases when mixed

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MATERIALS AND METHODS

Sample Preparation. Monolinolein was tested for sample degradation at the ester linkage using thin layer chromatography (TLC) (silica gel 60, Merck, Hertfordshire, U.K.). This method is 13020

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unlikely to detect oxidation of the hydrocarbon chain double bonds; however, this process will occur significantly slower than degradation of the ester linkage under our experimental and storage conditions. Limited hydration lipid samples were prepared by adding a known volume of HPLC-grade water (VWR, UK) to lyophilized monolinolein (Larodan Fine Chemicals AB, Sweden), the mass of each component being measured to 0.001 mg. To homogenize the hydrated lipid samples, they were centrifuged, mechanically mixed, further centrifuged, and then sealed; and each sample was then subjected to at least 50 freeze−thaw cycles by cycling between −70 and 30 °C. After every 5 freeze−thaw cycles, the samples were centrifuged, and additionally, after every 15 cycles, the samples were mechanically mixed. All samples were stored at −20 °C until use. Prior to SAXS experiments, the samples were transferred to Teflon sample holders which consist of a Teflon O-ring with Mylar windows.14 High-Pressure Synchrotron Small-Angle X-ray Scattering Experiments. Small angle X-ray diffraction (SAXS) experiments were carried out at beamline ID02, European Synchrotron Radiation Facility (ESRF), France, and at beamline I22, Diamond Light Source (DLS), U.K. All experiments utilized a custom-built high-pressure cell13 capable of applying hydrostatic pressures up to 4000 bar with an accuracy of ±10 bar, with the temperature of the cell being controlled to ±0.2 °C using a thermostat jacket connected to an external circulator. Experiments at the ESRF used X-rays with a wavelength of 0.075 nm (16.5 keV), and at DLS, the X-ray wavelength was 0.073 nm (17.0 keV). The pressure was increased from 1 to 3000 bar in 100 bar steps. After each pressure change, 120 s was allowed for equilibration before an image was taken. Our results have shown that the lattice parameter changes by less than 0.02 Å after 90 s of equilibration time when images were acquired every 10 s over a 300 s period (Figure 3). Close to the phase boundaries, the pressure steps were reduced to 50 bar and an additional 60 s of equilibration time was allowed. The uncertainty in the position of the phase boundaries is estimated to be ±50 bar. After a change in temperature, at least 30 min was allowed for the cell and sample temperatures to equilibrate.

At the ESRF, diffraction images were acquired using an imageintensified CCD detector with a typical exposure time of 0.1 s, and at DLS, images were acquired using a RAPID multiwire detector with a typical exposure time of 2 s. Diffraction images were analyzed offline using a custom-written software package, AXcess.18 At both beamlines, the sample to detector distance was calibrated using silver behenate, which has a well-defined layer spacing of 58.38 Å. High-Pressure Density Measurements. The density of the lipid was measured using an Anton Paar DMA 60/512P (Graz, Austria) vibrating tube densitometer at the Technical University of Dortmund. The densitometer consists of a steel U-tube with an internal volume of 2.5 mL. Three × 1 g samples of monolinolein−water mixtures were prepared to approximately 23 wt % water, as described above. To ensure that there were no air bubbles in the U-tube, degassed water was used to prepare the samples and the sample was loaded into the U-tube using a custom-built filling device connected to a high-pressure network. To accurately determine the water content of this mixture, the sample was removed from the U-tube after the experiment, weighed, freeze−dried for 48 h, and weighed again. The sample contained 24 wt % water, and the difference from the expected water content is attributed to lipid loss during mechanical mixing and sample transfer. Determining the Accurate Water Volume Fraction for All Samples. Due to the nature of sample preparation, there is often a small discrepancy between the actual water content of a sample and the water content calculated from the mass of lipid and water mixed. To determine the accurate water contents of the samples used for SAXS experiments, we have used the parallel interface model (eq 3)19,20 and the constant mean curvature model (eq 4)6,8,21,22 to recalculate the water volume fraction from the measured lattice parameter at 1 bar and 30 °C using the density measurement described above (note that the water content of the sample used for density measurements was determined extremely accurately by mass, postexperiment, which affords this method significantly greater accuracy than simply measuring the mass of lipid and water used to make the sample):

⎧ ⎛ ⎞ ⎡⎛ ⎞1/3⎤ ⎛ ⎛ vn ⎞2 ⎛ vn ⎞ ⎛ vn ⎞2 ⎞ ⎟ ⎥ ⎪ ⎜ 5/3 2⎟ ⎢⎜ 3 vn 3 2 2 ⎨−2σ + ⎜2 σ ⎟ /⎢⎜4σ + 9πχ (1 − ϕw ) ⎜ a= ⎟ + 3(1 − ϕw )⎜ ⎟ πχ ⎜⎜8σ + 9πχ (1 − ϕw ) ⎜ ⎟⎟ ⎥ A n × (1 − ϕw) ⎪ ⎝ V ⎠ ⎝ V ⎠ ⎝ V ⎠ ⎟⎠ ⎟⎟ ⎥ ⎜ ⎟ ⎢⎜⎝ ⎝ ⎠ ⎦ ⎩ ⎝ ⎠ ⎣ 1/3⎤⎫ ⎡ ⎞ ⎛ ⎛ ⎛ v ⎞ 2 ⎞ ⎟ ⎥⎪ ⎛ v ⎞2 ⎛ v ⎞ ⎢ ⎜ + ⎢21/3/⎜4σ 3 + 9πχ (1 − ϕw )2 ⎜ n ⎟ + 3(1 − ϕw )⎜ n ⎟ πχ ⎜⎜8σ 3 + 9πχ (1 − ϕw )2 ⎜ n ⎟ ⎟⎟ ⎟ ⎥⎬ ⎜ ⎝ V ⎠ ⎠ ⎟ ⎥⎪ ⎝ V ⎠ ⎝ V ⎠ ⎢ ⎝ ⎠ ⎦⎭ ⎝ ⎣

a=2×

∑ i=0

⎡ σi⎣

Vn V

An V

VnPIM = 609 ± 42 Å3; AnCMCM = 37.5 ± 1.7 Å2, VnCMCM = 592 ± 39 Å3.

⎤2i (1 − ϕw)⎦

( ) ( )(1 − ϕ ) w

(3)

Equation 5 was used to obtain the water contents from the calculated water volume fraction.

(4)

a is the lattice parameter Vn is the molecular volume between the minimal surface and the pivotal surface An is the molecular area at the pivotal surface V is the molecular volume ϕw is the water volume fraction σ is the dimensionless surface area of the minimal surface in the unit cell χ is the Euler characteristic σi are coefficients, tabulated for the QIIG phase in ref 4

ϕw =

Cw Cw + (1 − Cw) ×

() ρw ρl

(5)

cw is the water weight fraction; ρw is the density of water; ρl is the density of lipid. In most instances, there was less than 0.5 wt % difference between the recalculated water contents obtained from the two different models (PIM and CMCM) and a maximum difference of less than 5 wt % between the expected water content and the recalculated water content. The difference between the expected water content and the recalculated water content is attributed to slight loss of water and/or lipid during sample preparation.

V was determined from the density measurements described previously. An and Vn were obtained by fitting lattice parameter swelling data, measured at atmospheric pressure using a Bede Microscource X-ray system at Imperial College London;23 data were fitted to both the parallel interface model and the constant mean curvature model to obtain AnPIM = 37.1 ± 1.8 Å2 and

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RESULTS AND DISCUSSION High-pressure X-ray diffraction experiments at a range of temperatures showed two distinct phases. At atmospheric 13021

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Figure 5. Pressure−temperature phase diagrams constructed from SAXS data for limited hydrated monolinolein from 15.75 wt % water to 26.9 wt % water. The gray areas indicate the estimated uncertainty in the phase boundaries.

Characterizing the pressure−temperature phase behavior of monolinolein as a function of water content allows us to experimentally deconvolute the effects of pressure, temperature, and water content on the spontaneous curvature of the QIIG phase, and these different effects are discussed below. An increase in temperature leads to a more negative spontaneous curvature and stabilization of the QIIG phase, while increasing the pressure has the opposite effect: the volume occupied by the hydrocarbon chain decreases and the magnitude of the spontaneous mean curvature decreases (Figure 6). These trends are consistent with previous experiments and theoretical predictions.12,24,25 The phase diagrams in Figure 5 show that, with increasing hydration, the QIIG phase occupies a larger region in the phase diagram, and there is also a shift of the coexistence region to higher pressures and lower temperatures as the water content increases. The increase in the pressure range over which the lamellar and QIIG phases coexist with increasing hydration is

pressure and high temperatures, 8 distinct Bragg reflections with characteristic position ratios of √6:√8:√14:√16:√20:√22:√24:√26 (Figure 4a,b) led to the unambiguous assignment of the QIIG phase, where the diffraction peaks correspond to the Miller indices: 211, 220, 321, 400, 420, 332, 422 and 431/510, respectively. The second phase observed was a fluid lamellar (Lα) phase with characteristic peak positions in the ratio 1:2 which correspond to the Miller indices 100 and 200, respectively (Figure 4c,d). Pressure−temperature phase diagrams were constructed for each sample from the obtained X-ray diffraction data (Figure 5), and these show three distinct phase regions, pure QIIG, Lα and QIIG coexistence, and pure Lα. The accuracy of each point is limited by the equilibration time, uncertainty in the pressure (±10 bar), and uncertainty in the temperature (±0.2 °C); the combined estimated uncertainty in the phase boundary is indicated by the gray area around each phase boundary line. 13022

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volume. The QIIG phase forms with a large negative interfacial curvature, and as the water volume fraction increases, the interfacial curvature becomes less negative. Figure 7 shows the pressure−composition phase diagram, at constant temperature (30 °C) for the 20.9 wt % water sample. For monolinolein, at low pressures, the QIIG phase is stable, and increasing the pressure causes a slight increase in the lattice parameter. This is due to a decrease in the magnitude of the spontaneous curvature of the lipids caused by an increase in chain extension at elevated pressures. On increasing the pressure further, the system reaches a biphasic region where the QIIG phase coexists with the Lα phase, and the relative amounts of these phases can be determined using the lever rule from the tie-lines in the pressure−composition phase diagram. As the pressure increases, the QIIG phase will seek to increase its water content (as shown by the positive gradient of the phase boundary). Under limited hydration conditions, this can only be achieved by a concomitant change in the relative amounts of Lα and QIIG phases; at atmospheric pressure, the Lα phase is stable at lower water content than the QIIG phase. An increase in the lattice parameter of both the Lα and QIIG phases is permitted by a change in the relative proportions of the Lα and QIIG phases and is described by moving perpendicular to the tie-lines within the phase diagram.

Figure 6. Effect of increasing temperature, pressure, and water volume fraction on the preferred monolayer curvature of monolinolein. Increasing temperature increases the number of trans-gauche rotamers in the hydrocarbon chain, increasing the chain splay; increasing pressure decreases the volume of the hydrocarbon chain, which is achieved by ordering the chains, decreasing the chain splay; increasing the water volume fraction has a more complex effect on the bilayer structure, qualitatively similar to increasing temperature.

due to the coupled effects of water and pressure on the bilayer; increasing the pressure reduces the magnitude of the spontaneous curvature of the bilayer and formation of a lamellar phase is favored. As the lamellar phase contains less water than the QIIG phase,16,23 there is more water available to the QIIG phase to relieve curvature frustration which is induced by increased pressure. The observation that increasing hydration in the lamellar phase (zero curvature) leads to the stabilization of the QIIG phase (negative curvature) is counterintuitive15 since an increase in water content in the lamellar phase is expected to increase the water packing around the headgroup and lead to an increase in positive curvature. This anomalous phase sequence is thought to be due to the intrinsic desire of monolinolein to form inverse curved structures which is determined by the structural properties of the lipid molecules. We believe that, at low hydration, there is insufficient water to fill the aqueous channels of the QIIG phase, and so the lipids must adopt a lamellar phase. Within the lamellar bilayer stacks, the lipid hydrocarbon chains are laterally compressed relative to their preferred volume, leading to curvature stress in the bilayer. Addition of water to the system relieves the curvature stress by allowing the QIIG phase to form with an increased aqueous

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CONCLUSIONS By systematically investigating the effect of three fundamental thermodynamic variables, pressure, temperature, and water content, on the bilayer phase behavior of limited hydrated monolinolein, we have been able to qualitatively deconvolute the factors which stabilize curved mesophases. These results are consistent with other monoacylglyceride experiments previously conducted at atmospheric pressure and with theoretical predictions. Our results suggest that water plays a crucial role in stabilizing the QIIG phase by relieving curvature frustration, which is required for the bilayer to attain its desired curvature. Experimental phase behavior data are a vital prerequisite for quantitative modeling of lipid bilayer mechanics, and we hope the results presented here will stimulate further work in this area. Indeed, the effect of pressure and temperature on the free energy of inverse bicontinuous cubic phases determined using the constant mean curvature and the parallel interface model is the subject of a forthcoming article.

Figure 7. (a) Pressure−composition phase diagram at 30 °C, where the horizontal lines represent tie lines in the coexistence region. (b) Plot of lattice parameter against pressure for the 20.9 wt % water sample at 30 °C, where the filled black squares show the lattice parameter of the lamellar phase and the hollow circles show the lattice parameter of the QIIG phase. 13023

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studies of liquid crystal transitions in lipids. Philos. Trans. R. Soc. A: Math. Phys. Eng. Sci. 2006, 364 (1847), 2635−2655. (19) Templer, R. H.; Seddon, J. M.; Warrender, N. A.; Syrykh, A.; Huang, Z.; Winter, R.; Erbes, J. Inverse Bicontinuous Cubic Phases in 2:1 Fatty Acid/Phosphatidylcholine Mixtures. The Effects of Chain Length, Hydration, and Temperature. J. Phys. Chem. B 1998, 102 (37), 7251−7261. (20) Hyde, S. T. Microstructure of bicontinuous surfactant aggregates. J. Phys. Chem. 1989, 93 (4), 1458−1464. (21) Brakke, K. A. The Surface Evolver. Exp. Math. 1992, 1, 141. (22) Grosse-Brauckmann, K. On Gyroid Interfaces. J. Colloid Interface Sci. 1997, 187 (2), 418−428. (23) Kulkarni, C. V.; Tang, T.-Y.; Seddon, A. M.; Seddon, J. M.; Ces, O.; Templer, R. H. Engineering bicontinuous cubic structures at the nanoscale-the role of chain splay. Soft Matter 2010, 6 (14), 3191− 3194. (24) Czeslik, C.; Winter, R.; Rapp, G.; Bartels, K. TemperatureDependent and Pressure-Dependent Phase-Behavior of Monoacylglycerides Monoolein and Monoelaidin. Biophys. J. 1995, 68 (4), 1423− 1429. (25) Reis, O.; Winter, R. Pressure and temperature effects on conformational and hydrational properties of lamellar and bicontinuous cubic phases of the fully hydrated monoacylglyceride monoelaidin - A Fourier transform infrared spectroscopy study using the diamond anvil technique. Langmuir 1998, 14 (10), 2903−2909.

AUTHOR INFORMATION

Notes

The authors declare no competing financial interest.

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ACKNOWLEDGMENTS This work was supported by EPSRC Platform Grant EP/ G00465X and by an EPSRC DTA studentship awarded to TYDT. We acknowledge Diamond Light Source (UK) and the European Synchrotron Radiation Facility (Grenoble, France) for the provision of synchrotron radiation facilities and we would like to thank Dr. Claire Pizzey (beamline I22, DLS) and Dr. Michael Sztucki (beamline ID02, ESRF) for their assistance during the synchrotron experiments.

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REFERENCES

(1) Templer, R. H. Thermodynamic and theoretical aspects of cubic mesophases in nature and biological amphiphiles. Curr. Opin. Colloid Interface Sci. 1998, 3 (3), 255−263. (2) Drummond, C. J.; Fong, C. Surfactant self-assembly objects as novel drug delivery vehicles. Curr. Opin. Colloid Interface Sci. 1999, 4 (6), 449−456. (3) Shah, J. C.; Sadhale, Y.; Chilukuri, D. M. Cubic phase gels as drug delivery systems. Adv. Drug Delivery Rev. 2001, 47 (2−3), 229−250. (4) Helfrich, W. Elastic properties of lipid bilayers - Theory and possible experiments. Z. Naturforsch., C: J. Biosci. 1973, C 28, (11−1), 693−703. (5) Andersson, S.; Hyde, S. T.; Larsson, K.; Lidin, S. Minimal surfaces and structures: from inorganic and metal crystals to cell membranes and biopolymers. Chem. Rev. 1988, 88 (1), 221−242. (6) Anderson, D. M.; Gruner, S. M.; Leibler, S. Geometrical aspects of the frustration in the cubic phases of lyotropic liquid crystals. Proc. Natl. Acad. Sci. U.S.A. 1988, 85 (15), 5364−5368. (7) Templer, R. H.; Seddon, J. M.; Duesing, P. M.; Winter, R.; Erbes, J. Modeling the Phase Behavior of the Inverse Hexagonal and Inverse Bicontinuous Cubic Phases in 2:1 Fatty Acid/Phosphatidylcholine Mixtures. J. Phys. Chem. B 1998, 102 (37), 7262−7271. (8) Shearman, G. C.; Khoo, B. J.; Motherwell, M.-L.; Brakke, K. A.; Ces, O.; Conn, C. E.; Seddon, J. M.; Templer, R. H. Calculations of and Evidence for Chain Packing Stress in Inverse Lyotropic Bicontinuous Cubic Phases. Langmuir 2007, 23 (13), 7276−7285. (9) Shearman, G.; Ces, C.; Templer, O. R. H. Towards an understanding of phase transitions between inverse bicontinuous cubic lyotropic liquid crystalline phases. Soft Matter 2010, 6, 256−262. (10) Bartlett, D. H. Pressure effects on in vivo microbial processes. Biochim. Biophys. Acta 2002, 1595 (1−2), 367−381. (11) Johnson, F. H.; Flagler, E. A. Hydrostatic Pressure Reversal of Narcosis in Tadpoles. Science 1950, 112 (2899), 91−92. (12) Duesing, P. M.; Seddon, J. M.; Templer, R. H.; Mannock, D. A. Pressure effects on the lamellar and Inverse Curved Phases of fully hydrated dialkyl Phosphatidylethanolamines and beta-D-Xylopyranosyl-sn-glycerols. Langmuir 1997, 13, 2655−2664. (13) Woenckhaus, J. High pressure-jump apparatus for kinetic studies of protein folding reactions using the small-angle synchrotron x-ray scattering technique. Rev. Sci. Instrum. 2000, 71 (10), 3895−3899. (14) Brooks, N. J.; Gauthe, B.; Terrill, N. J.; Rogers, S. E.; Templer, R. H.; Ces, O.; Seddon, J. M. Automated high pressure cell for pressure jump x-ray diffraction. Rev. Sci. Instrum. 2010, 81 (6), 10. (15) Charvolin, J. Crystals of Interfaces: The Cubic phase of Amphiphile/Water systems. J. Phys. 1985, 46, C3 173−C3 190. (16) Lee, W. B.; Mezzenga, R.; Fredrickson, G. H. Anomalous Phase Sequences in Lyotropic Liquid Crystals. Phys. Rev. Lett. 2007, 99 (18), 187801. (17) Kocherbitov, V. Driving forces of phase transitions in surfactant and lipid systems. J. Phys. Chem. B 2005, 109 (13), 6430−6435. (18) Seddon, J. M.; Squires, A. M.; Conn, C. E.; Ces, O.; Heron, A. J.; Mulet, X.; Shearman, G. C.; Templer, R. H. Pressure-jump X-ray 13024

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