ARTICLE pubs.acs.org/Langmuir
Vesicles in Ionic Liquids Florence Gayet,†,‡,§ Jean-Daniel Marty,†,‡ Annie Br^ulet,|| and Nancy Lauth-de Viguerie*,†,‡ †
Universite de Toulouse, UPS, IMRCP, 118 route de Narbonne, F-31062 Toulouse Cedex 9, France CNRS, IMRCP, F-31062 Toulouse, France § Department of Chemistry, University of Warwick, Coventry, CV4 7AL, United Kingdom Laboratoire Leon Brillouin, UMR12 CEA-CNRS, CEA Saclay, F-91191 GIF/Yvette, France
)
‡
bS Supporting Information ABSTRACT: The formation of vesicles from 1,2-dipalmitoyl-sn-glycero-3phosphatidylcholine (DPPC) in several room-temperature ionic liquids, namely, 1-butyl-3-methylimidazolium tetrafluoroborate (BmimBF4), 1butyl-3-methylimidazolium hexafluorophosphate (BmimPF6), 1-ethyl-3methylimidazolium bis(trifluoromethylsulfonyl)imide (EmimNTf2), and N-benzylpyridinium bis(trifluoromethylsulfonyl)imide (BnPyNTf2), as well as in a water/BmimBF4 mixture, was investigated. In pure ionic liquids, observations by staining transmission electron microscopy demonstrated clearly the formation of spherical structures with diameters of 200400 nm. The morphological characteristics of these vesicles in ionic liquids, in particular, the membrane thicknesses, were first investigated by small-angle neutron scattering measurements. The mean bilayer thickness was found to be ∼63 ( 1 Å in a deuterated ionic liquid (BnPyNTf2-d). This value was similar to that observed in water. The effect of ILs on the modification of the phase physical properties of multilamellar vesicles (MLVs) was then investigated by differential scanning calorimetry. In pure IL as in water, DPPC exhibited an endothermic pretransition followed by the main transition. These transition temperatures and the associated enthalpies in ILs were higher than those in water because of a reduction of the electrostatic repulsion between zwitterionic head groups. To better understand the effect of ionic liquid on the formation of multilamellar vesicles, mixtures of BmimBF4 and water, which are miscible in all proportions, were analyzed (BmimBF4/water ratio from 0% to 100%). SANS and DSC experiments demonstrated that the bilayer structure and stability were strongly modified by the IL content. Moreover, matching SANS experiments showed that BmimBF4 molecules prefer to be located inside the DPPC membrane rather than in water.
’ INTRODUCTION Ionic liquids (ILs) are a class of solvents that are stable over a large range of temperatures and have negligible vapor pressures. Owing to their molecular structures, associating a cation and an anion, their physicochemical properties can easily be modulated by changing one of the ions. Ionic liquids are now widely used in organic synthesis and chemical separations because of their high solvation abilities and tunable natures.1,2 Surfactant organization in ILs could open new research directions toward micellar catalysis in IL media, solvation enhancement for apolar entities, and lyotropic properties.3,4 Indeed, surfactant organization occurs in some nonaqueous solvents and is largely used in aqueous systems for drug vectorization, catalysis, gelification, and other applications.5 Recently, various aggregates such as micelles,6,7 nonaqueous microemulsions,810 and lyotropic phases1113 have been obtained in ILs. Nevertheless, only a few examples of vesicles have been observed in pure ILs.1416 Their formation was first evidenced with a glycolipid L-glutamate derivative15 in two ether-containing ILs, 1-(20 -methoxymethyl)-3-methylimidazolium bromide (Me-Im-C1OC1) and 1-(20 -methoxyethyl)-3methylimidazolium bromide (Me-Im-C2OC1), by differential r 2011 American Chemical Society
scanning calorimetry (DSC) and dark-field optical microscopy. DSC measurements showed an endothermic peak (Tc) at 40 and 51 °C in Me-Im-C2OC1 and in Me-Im-C1OC1, respectively, thus indicating that the phase transition characteristics of glycobilayers are affected by the chemical structure of the IL. In addition, a similar behavior was observed for dialkyldimethylammonium bromides in the same ILs.16 In both studies, bilayer vesicles were claimed to be observed in dark-field optical micrographs only above the transition temperature. Moreover, no aggregate was formed with these surfactants in the conventional IL 1-butyl-3methylimidazolium hexafluorophosphate (BmimPF6). In a more recent study, vesicle structures were obtained with a Zn2+fluorous surfactant ([Zn(OOCCH2C6F13)2]) and a Zn2+fluorous surfactant/zwitterionic surfactant mixture ([Zn(OOC CH2C6F13)2]/C14DMAO) in 1-butyl-3-methylimidazolium tetrafluoroborate (BmimBF4) and BmimPF6.14 The authors determined the size and interlamellar spacing between the bilayers in Received: October 13, 2010 Revised: June 24, 2011 Published: June 30, 2011 9706
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the vesicles through freeze-fracture transmission electron microscopy (FF-TEM) and small-angle X-ray scattering (SAXS) observations. Diameters were ∼3090 and ∼20150 nm in BmimPF6 for [Zn(OOCCH2C6F13)2] and [Zn(OOC CH2C6F13)2]/C14DMAO, respectively. The membrane thickness was about 51.9 Å. Here, the formation of multilamellar vesicles from glycerophospholipids [namely, 1,2-dipalmitoyl-sn-glycero-3-phosphatidylcholine (DPPC)] in BmimBF4, BmimPF6, 1-ethyl-3-methylimidazolium bis(trifluoromethylsulfonyl)imide (EmimNTf2), and N-benzylpyridinium bis(trifluoromethylsulfonyl)imide (BnPyNTf2) was investigated. Lecithins and more specifically DPPC have been extensively studied for their ability to form multilamellar vesicles in water. Hence, there is a great interest in studying their formation in ILs to compare the characteristics of the bilayer structure with that observed in water systems. Toward this end, the resulting DPPC aggregates in ILs were characterized by differential scanning calorimetry (DSC), negative-staining transmission electron microscopy (TEM), freeze-fracture transmission electron microscopy (FF-TEM), freeze-fracture scanning electron microscopy (FF-SEM), and small-angle neutron scattering (SANS). To better assess the role of ILs in the formation of vesicles, aqueous dispersions of DPPC with increasing amounts of IL were also studied.
’ EXPERIMENTAL SECTION Materials. BmimBF4, BmimPF6, and EmimNTf2 (99.9%) were purchased from Solvionic (Varilhes, France). BnPyNTf2 was synthesized as described in the literature.9 All ILs were dried at 60 °C under a vacuum for 3 h prior to use and stored under an inert atmosphere (argon). Their water content, determined by coulometric Karl Fischer titration, was less than 15 ppm. 1,2-Dipalmitoyl-sn-glycero-3-phosphatidylcholine (DPPC) was purchased from Sigma. Multilamellar Vesicle Preparation. A stock solution of DPPC (2 102 mol 3 L1) in chloroform/methanol (9:1, v/v) was prepared and stored at 4 °C. To prepare multilamellar vesicles, 400 μL of this lipid solution was placed in a vial, and solvent was evaporated under a nitrogen stream. Residues were desiccated under a vacuum for 2 h (1 Torr). The dried lipid samples were hydrated in 200 μL of pure IL or IL/water mixture and heated to 80 °C for 20 min. [This temperature is higher than the gel-to-liquid transition temperature (Tm).] The sample was immediately vortexed for 4 min. The vesicle solutions ([DPPC] = 4 102 mol 3 L1, i.e., 2.93% w/v) so prepared were then stored at 4 °C overnight. Differential Scanning Calorimetry. Thermal transitions were measured on a Perkin-Elmer Pyris 1 calorimeter, using heating and cooling rates from 1 to 20 °C/min (1, 2, 5, 10, and 20 °C/min). A 25 μL quantity of each vesicular solution was loaded into a pan and allowed to equilibrate at the initial temperature for 20 min. Data were collected at different rates from 1 to 20 °C/min between 0 and 120 °C. The main transition temperature was determined as the peak maximum of an endothermic transition extrapolated to 0 °C/min. The lipid concentration in the ionic liquids was fixed at 4.2 102 mol 3 L1. Transmission Electronic Microscopy. TEM measurements were performed on a Tecnai Spirit transmission electron microscope operated at an accelerating voltage of 120 kV. Samples were negatively stained with a solution of phosphotungstic acid. Freeze-Fracture Transmission Electron Microscopy (FF-TEM). FF-TEM images were acquired on a JEOL 2010F TEM instrument [200 kV field-emission gun (FEG)] equipped with a Gatan UltraScan 4000 camera and cryogenic sample holder using lacey carbon film grids (300 mesh Cu, Agar Sc. S166-3H). The solutions were preheated in a 40 °C water bath to reduce the viscosity of the ionic liquid samples.
Figure 1. (a) Negative-staining TEM of vesicles of DPPC in BmimBF4. Sodium phosphotungstate was used as the negatively charged dye. (b) Freeze-fracture transmission electron microscopy of vesicles of DPPC in BmimBF4. [DPPC] = 1% (w/v), scale bar = 200 nm. Samples were prepared in the following way: A small droplet of each solution was placed on an ionized grid, and the excess solution was blotted with a piece of filter paper. The thus-obtained thin film of solution spanning the grid was quickly plunged into liquid ethane (∼90 K) that was cooled by liquid nitrogen. The samples were then kept in liquid nitrogen before transfer by a cryogenic sample holder to the microscope and imaged at 178 °C. Adequate phase contrast was obtained at a nominal underfocus of 315 μm.
Freeze-Fracture Scanning Electron Microscopy (FF-SEM). FF-SEM was performed on a Zeiss SUPRA 55-VP instrument equipped with a cold stage and a sample preparation chamber. The accelerating voltage was set to 13 kV to avoid burning the sample. For FF-SEM sample preparation, typically, the specimen stub was tapped on the surface of the solution to take the sample by capillary action until the stub was filled. It was then rapidly frozen in solid nitrogen (less than 210 °C), which was obtained from liquid nitrogen (196 °C) under a vacuum. The sample was stabilized on the prefrozen stub adaptor and transferred under a vacuum to the cold stage of the preparation chamber, which was mounted on the SEM chamber. Both the anticontaminate plates in the chamber and the microscope were cooled to 186 °C, and 9707
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Table 1. Thermodynamic Parameters of the Phase Transitions of DPPC MLV in BmimBF4, BmimPF6, EmimNTf2, and Water Determined by DSC Measurements Lβ0 f Pβ0
Figure 2. (a) Freeze-fracture scanning electron microscopy of vesicles of DPPC in BnPyNTf2-d. (b) SANS curves of DPPC solutions in (b) D2O and (0) BnPyNTf2-d. [DPPC] = 1% (w/v). both cold stages were set to 130 °C. The stub adaptor was subsequently transferred under a vacuum into the SEM chamber where it was easily located on the cold stage specifically tailored to the SEM instrument. Small-Angle Neutron Scattering (SANS) Experiments. SANS experiments were performed with the PACE spectrometer at the Orphee reactor (Laboratoire Leon Brillouin, Saclay, France). DPPCILwater mixtures were placed inside quartz cells with a gap of 1 or 2 mm and measured at 20 °C ([DPPC] = 1% w/v). Three spectrometer configurations were used: a neutron wavelength (λ) of 7 Å with a sample-todetector distance of 3 m, the same wavelength with a distance of 1 m, and a wavelength of 17 Å with a distance of 4.8 m. The scattering vector range was thus 0.0025 < q (Å1) < 0.35. Scattering intensities were also normalized by the incoherent signal delivered by a 1-mm-gap water sample to account for the efficiency of the detector cells.17 Absolute values of the scattering intensity, I(q) in cm1, were obtained from the direct determination of the number of neutrons in the incident beam and the detector cell solid angle.18 No background was subtracted from the sample scattering; thus, a flat incoherent signal was observed at high q values.
’ RESULTS AND DISCUSSION Formation of Vesicles in Ionic Liquids. Preliminary measurements showed that, in the different ILs (BmimBF4, BmimPF6, EmimNTf2, BnPyNTf2), DPPC reduces the surface tension in a manner analogous to aqueous surfactant solutions (Figure S1 in the Supporting Information). This indicates that DPPC molecules can adsorb at the surface of the ILs and lead to organized systems. Multilamellar vesicles (MLVs) were prepared following a classical method usually used in water.19 Initial observations by negativestaining TEM, FF-TEM, and FF-SEM clearly demonstrated the formation of spherical aggregates (Figures 1 and 2a) in all ionic liquids. As expected considering the method of preparation leading to multilamellar vesicles, these structures presented a rather large
Pβ0 f LR
solvent
T (°C)
ΔH (kJ/mol)
T (°C)
ΔH (kJ/mol)
BmimBF4
55.9
0.5 ( 0.1
61.7
85 ( 2
BmimPF6
48.5
0.4 ( 0.1
57.5
85 ( 2
EmimNTf2
50.5
7.1 ( 1.8
56.5
92 ( 6
BnPyNTf2
52.0
0.3 ( 0.2
56.3
89 ( 2
H2O
36.9
1.6 ( 0.7
44.1
42 ( 2
size distribution, with diameters ranging from 30 to 300 nm (Figure 1a and Figure S2 in the Supporting Information). The observed aggregates could be either large unilamellar vesicles (LUVs) or MLVs. To assess vesicle formation, the morphological characteristics of the aggregates in ILs were further investigated by DSC and SANS experiments and compared to the results obtained in water. In water, DPPC exhibited an endothermic pretransition at 36.9 °C that corresponds to the transition from the lamellar gel phase (Lβ0 ) to the ripple gel phase (Pβ0 ). This first transition was followed by the main gel-to-liquid crystalline phase (LR) transition at 44.1 °C (see Table 1). As mentioned above, the preparation method used here involved the formation of vesicles with a large size dispersity. Thus, the transitions observed were broad and induced a slightly overestimated value of those transitions compared to that given in the literature (i.e., 41.3 ( 1.8 °C).20 The SANS curve (Figure 2b) exhibited a huge decrease (q4 dependence) and a Bragg peak at large q, characteristic of a randomly oriented lamellar phase.21,22 The Bragg peak with a maximum at q ≈ 0.098 Å1 resulted from the organization of lipid bilayers in a one-dimensional periodic lattice of periodicity d ≈ 64 Å, which is a typical repeat distance of fully hydrated DPPC multibilayers at T ≈ 5060 °C.2327 In pure ILs, both transitions were also detected. They were at higher temperature than in water (61.7, 57.5, 56.5, and 56.3 °C in BmimBF4, BmimPF6, EmimNTf2, and BnPyNTf2, respectively, for the Pβ0 f LR transition). The significant increases of the transition temperatures and associated enthalpies can be ascribed to a reduction of the electrostatic repulsion between zwitterionic head groups.16 Considering that the molecular alignment of DPPC molecules in bilayers is determined by the balance of electrostatic and van der Waals forces, it is reasonable to assume that the decreased repulsion between head groups leads to an increase of the thermal stability of crystalline-state bilayers. SANS experiments were then performed with hydrogenated DPPC in a deuterated IL (BnPyNTf2-d), which was synthesized as described previously.9 The strong absorption properties of BmimBF4 and, to a smaller extent, of the other ILs did not allow SANS studies to be performed accurately in the other ILs. The curve for hydrogenated DPPC in BnPyNTf2-d was slightly different from that observed in water (Figure 2b): At low q, it flattens, as expected for the typical q2 dependence characteristic of large-vesicle flat membranes, whereas a small bump (more visible in the enlargement in the inset of Figure 2b) is observed at large q. From the latter, we deduced a repeat distance assimilated to a mean bilayer thickness (DPPC and solvent) of d ≈ 63 ( 1 Å. This distance, within error bars, shows that the DPPC bilayer was not significantly affected by using BnPyNTf2-d instead of water. 9708
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Figure 3. Tmax extrapolated to 0 °C/min as a function of IL content deduced from DSC thermograms obtained for the DPPCwater/ BmimBF4 system. Vertical bar lengths are proportional to the width of the peak measured at 10 °C/min (lengths represent one-half of the real values).
The peak intensity was much smaller than in the mixture with D2O, and its width was much greater. The correlation length of the bilayer structure was estimated from the full width at halfmaximum to be ca. 20 nm in the case of water, and it decreased significantly (by a factor 3) when water was replaced by BnPyNTf2-d. Both correlation lengths are compatible with a multilamellar structure. Self-assembly of DPPC in BnPyNTf2-d could be a mixture of polydisperse vesicles with some multilamellar membrane vesicles. Nevertheless, the precise nature of the bilayer structure in ILs has not yet been fully characterized and will be the subject of forthcoming studies. Formation of Vesicles in Mixtures of Water and BmimBF4. The effect of solvent composition on the formation of vesicles was studied by using mixtures of water and BmimBF4, which are miscible in all proportions. Figure 3 shows the evolution of the phase transition temperatures as a function of IL content. (See Figure S3 in the Supporting Information for the corresponding DSC thermograms.) Upon addition of small quantities of ILs (below 5%), the stability of the bilayer structure was significantly increased from 44 to 60 °C. In addition, scattering curves obtained from SANS measurements (Figure 4a) showed no modification of the layer thickness, which remained around 64.0 Å. It can be noticed that the scattering curves change mainly at low q, but it is quite difficult to quantify such structural changes at large distances without a precise structural model. Both results suggest an increase of the packing density of the DPPC molecules in the bilayer. This can be ascribed to a modification to some extent of the structure of water around the head groups of DPPC. ILs induce a screening effect of the polar head groups and thus reduce the electrostatic repulsion between them. This effect was similar to that observed upon salt addition to DPPC vesicles in water.16 Supplementary addition of IL (up to 75%) induced a slight decrease of the transition temperature (from 60 to 52 °C for 10% IL). This change was associated with the appearance of a shoulder on the main transition peak (see Figure S3 in the Supporting Information), as well as a small decrease of the associated enthalpy variation (see Table S4 in the Supporting Information). This suggests a modification of the bilayer structure. Hence, the Bragg peak observed on SANS scattering curves shifted toward the small q values: The corresponding membrane thickness, reported
Figure 4. (a) Logarithmic plot of SANS data for DPPC-D2O/ BmimBF4 mixtures. (2% shifted by a factor of 5; 10%, a factor of 40; and 25%, a factor of 60 for the sake of clarity). (b) SANS data of DPPCwater/BmimBF4 mixtures obtained under the matching conditions for DPPC (25% shifted down).
Table 2. Bilayer Thickness in IL/Water Mixtures: dDPPC in D2O and dBmimBF4 in D2O/H2O Mixtures, Matching DPPC BmimBF4 content (% v/v)
dDPPC (Å)
dBmimBF4
0
63.6 ( 0.2
1
64.0 ( 0.2
64.0 ( 0.7
2 10
64.0 ( 0.2 71.8 ( 0.2
66 ( 1 74.7 ( 0.5
25
74.4 ( 0.2
74.3 ( 0.3
in Table 2, increased from 63.6 to 74.4 Å for an increase in BmimBF4 content from 0% to 25%. Because of the absorption of neutrons by B atoms, we could not explore higher fractions of BmimBF4 in the DPPCwater system than 25%. To understand why such a modification occurred, further SANS experiments were performed under matching conditions for DPPC17 to observe the scattering by BmimBF4 molecules (Figure 4b). For this purpose, a 29%/71% (v/v) D2O/H2O mixture was used. Typical curves are shown in Figure 4b. In this figure, one clearly see a weak Bragg peak, the intensity of which increases with increasing BmimBF4 content. This signal is due to periodic fluctuations of BmimBF4. The dBmimBF4 periods are listed in Table 2: They are similar to those observed under full-contrast conditions. Hence, when the BmimBF4 content was increased from 2% to 25%, DPPC was partially solubilized in the bilayer structure, as shown by matching experiments. Both the increase of the bilayer thickness and the decrease of the thermal stability of the bilayer structure can be ascribed to the weakening of van 9709
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Langmuir der Waals interaction between the DPPC molecules due to the presence of the IL molecules.16 For IL contents above 75%, the transition temperature increased to 62 °C and remained roughly constant (Figure 3). Interestingly, at the same time, a strong modification of the enthalpy variation associated with this transition was observed. Thus, the corresponding enthalpy variation increased from 1 to 85 kJ 3 mol1 when the IL content increased from 90% to 100% (see Table S4 in the Supporting Information). As shown in the first part of this article, vesicles are formed in pure ILs. Therefore, addition of a small quantity of water strongly disturbed the membrane organization and almost disrupted it for a water content of 10%. This organization was strongly modified by further addition of water, whereas the enthalpy variation increased to 40 kJ 3 mol1.
’ CONCLUSIONS The formation of vesicles from DPPC in several roomtemperature ionic liquids (BmimBF4, BmimPF6, EmimNTf2, BnPyNTf2) and in water/BmimBF4 mixtures was demonstrated by TEM, SANS, and DSC experiments. In pure ILs, the formation of spherical structures with diameters of 200400 nm was clearly observed by TEM. Moreover, SANS experiments allowed a mean bilayer thickness of around 63 ( 1 Å to be evaluated in a deuterated ionic liquid (BnPyNTf2-d). This value was similar to that observed in water. Finally, the thermal behaviors obtained from DSC measurements were found to be similar in pure ILs and in water: In both cases, an endothermic pretransition was followed by the main transition. Nevertheless, these transition temperatures and the associated enthalpies were higher in ILs than in water because of a reduction of the electrostatic repulsion between the zwitterionic head groups. To better understand the effects of ILs on the formation of MLVs, mixtures of BmimBF4 and water were analyzed (BmimBF4/water ratio ranging from 0% to 100% ). SANS and DSC experiments demonstrated that the bilayer structure and stability were strongly modified by the IL content. These modifications were shown to be strongly dependent on the ionic liquid content. ’ ASSOCIATED CONTENT
bS
Supporting Information. Additional characterization data (surface tension measurements, freeze fracture transmission electron microscopy, thermograms, and enthalpy variations) are available free of charge via the Internet at http://pubs.acs.org.
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’ REFERENCES (1) Ranke, J.; Stolte, S.; Stormann, R.; Arning, J.; Jastorff, B. Chem. Rev. 2007, 107, 2183–2206. (2) Dupont, J.; de Souza, R. F.; Suarez, P. A. Z. Chem. Rev. 2002, 102, 3667–3691. (3) Greaves, T. L.; Drummond, C. J. Chem. Soc. Rev. 2008, 37, 1709–1726. (4) Hao, J. C.; Zemb, T. Curr. Opin. Colloid Interface Sci. 2007, 12, 129–137. (5) Lindstrom, U. M. Chem. Rev. 2002, 102, 2751–2771. (6) Anderson, J. L.; Pino, V.; Hagberg, E. C.; Sheares, V. V.; Armstrong, D. W. Chem. Commun. 2003, 2444–2445. (7) (a) Patrascu, C.; Gauffre, F.; Nallet, F.; Bordes, R.; Oberdisse, J.; de Lauth-Viguerie, N.; Mingotaud, C. ChemPhysChem 2006, 7, 99–101. (b) Gayet, F.; Patrascu, C.; Marty, J.-D.; Lauth-de Viguerie, N. Int. J. Chem. React. Eng. 2010, 8, A38. (8) Gao, H. X.; Li, J. C.; Han, B. X.; Chen, W. N.; Zhang, J. L.; Zhang, R.; Yan, D. D. Phys. Chem. Chem. Phys. 2004, 6, 2914–2916. (9) Gayet, F.; El Kalamouni, C.; Lavedan, P.; Marty, J. D.; Brulet, A.; Lauth-de Viguerie, N. Langmuir 2009, 25, 9741–9750. (10) Eastoe, J.; Gold, S.; Rogers, S. E.; Paul, A.; Welton, T.; Heenan, R. K.; Grillo, I. J. Am. Chem. Soc. 2005, 127, 7302–7303. (11) Evans, D. F.; Kaler, E. W.; Benton, W. J. J. Phys. Chem. 1983, 87, 533–535. (12) Araos, M. U.; Warr, G. G. J. Phys. Chem. B 2005, 109, 14275–14277. (13) Wang, L. Y.; Chen, X.; Chai, Y. C.; Hao, J. C.; Sui, Z. M.; Zhuang, W. C.; Sun, Z. W. Chem. Commun. 2004, 2840–2841. (14) Hao, J. C.; Song, A. X.; Wang, J. Z.; Chen, X.; Zhuang, W. C.; Shi, F.; Zhou, F.; Liu, W. M. Chem.—Eur. J. 2005, 11, 3936–3940. (15) Kimizuka, N.; Nakashima, T. Langmuir 2001, 17, 6759–6761. (16) Nakashima, T.; Kimizuka, N. Chem. Lett. 2002, 1018–1019. (17) Br^ulet, A.; Lairez, D.; Lapp, A.; Cotton, J.-P. J. Appl. Crystallogr. 2007, 40, 165–177. (18) Cotton, J.-P. In Neutron, X-ray and Light Scattering; Lindner, P., Zemb, Th., Eds.; Elsevier: New York, 1991. (19) Lasic, D. D. Biochem. J. 1988, 256, 1–11. (20) Koynova, R.; Caffrey, M. Biochim. Biophys. Acta, Rev. Biomembr. 1998, 1376, 91–145. (21) Herve, P.; Roux, D.; Bellocq, A. M.; Nallet, F.; Gulikkrzywicki, T. J. Phys. II 1993, 3, 1255–1270. (22) Nallet, F.; Laversanne, R.; Roux, D. J. Phys. II 1993, 3, 487–502. (23) Chen, S. C.; Sturtevant, J. M.; Gaffney, B. J. Proc. Natl. Acad. Sci. U.S.A. 1980, 77, 5060–5063. (24) Katsaras, J. J. Phys. Chem. 1995, 99, 4141–4147. (25) Nagle, J. F.; Tristram-Nagle, S. Biochim. Biophys. Acta, Rev. Biomembr. 2000, 1469, 159–195. (26) Uhrikova, D.; Kucerka, N.; Teixeira, J.; Gordeliy, V.; Balgavy, P. Chem. Phys. Lipids 2008, 155, 80–89. (27) Worcester, D. L.; Franks, N. P. J. Mol. Biol. 1976, 100, 359–378.
’ AUTHOR INFORMATION Corresponding Author
*Tel.: +33 5 61 55 61 35. Fax: 00 33 5 61 55 81 55. E-mail:
[email protected].
’ ACKNOWLEDGMENT The authors thank the University of Warwick and Professor D. Haddleton for facilities access supported by the Innovative Uses for Advanced Materials in the Modern World (AM2) with support from Advantage West Midlands (AWM) and partial funding by the European Regional Development Fund (ERDF). We also give grateful thanks to Ian Portman (School of Life Sciences, University of Warwick) for help with FF-TEM analysis and Thomas Skelhon for his help for FF-SEM measurements. 9710
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