Formation of Supported Lipid Bilayers by Vesicle Fusion: Effect of Deposition Temperature
Abstract

We have investigated the effect of deposition temperature on supported lipid bilayer formation via vesicle fusion. By using several complementary surface-sensitive techniques, we demonstrate that despite contradicting literature on the subject, high-quality bilayers can be formed below the main phase-transition temperature of the lipid. We have carefully studied the formation mechanism of supported DPPC bilayers below and above the lipid melting temperature (Tm) by quartz crystal microbalance and atomic force microscopy under continuous flow conditions. We also measured the structure of lipid bilayers formed below or above Tm by neutron reflection and investigated the effect of subsequent cooling to below the Tm. Our results clearly show that a continuous supported bilayer can be formed with high surface coverage below the lipid Tm. We also demonstrate that the high dissipation responses observed during the deposition process by QCM-D correspond to vesicles absorbed on top of a continuous bilayer and not to a surface-supported vesicular layer as previously reported.
Introduction
Experimental Section
Materials
Small Unilamellar Vesicles (SUVs)
Quartz Crystal Microbalance
Atomic Force Microscopy
Neutron Reflection (NR)
Results and Discussion
Figure 1

Figure 1. (A) Δf (blue) and Δd (red) as a function of vesicle exposure time on a clean silica surface at 25 °C (broken lines) or 50 °C (solid lines). The data shown corresponds to the seventh overtone. At t = 0 s, a solution of SUVs was introduced into the cells. (B) AFM image of the formation of a DPPC bilayer at RT under constant flow conditions. Raster scanning was performed in the direction along the arrow. The numbers correspond to (1) clean mica, before lipids have reached the surface, (2) small lipid bilayer patches formed instantaneously and fused to create a bilayer, and (3) vesicles attached to the bilayer. (C) Imaging during rinsing with water at RT. (D) Image after rinsing and equilibration with hot water (above Tm).
Figure 2

Figure 2. Neutron reflectivity curves. (A) dDPPC measured at 50 °C (red) and after cooling to 25 °C (gray). Data points in solid circles were measured in D2O (SLD = 6.35 × 10–6 Å–2), while data points in open circles were measured in H2O (SLD = −0.56 × 10–6 Å–2). (B) hDPPC membrane deposited and measured at 25 °C. The gray data points and the solid line correspond to reflectivity measured in D2O and the best fit to the data. This fit includes an additional lipid layer on top of the membrane, separated by a layer of water. The additional layer has a coverage of 14 ± 1 v/v% and is believed to stem from attached vesicles. The red data is measured in CM4 (contrast matched to SLD = 4 × 10–6 Å–2). The broken lines give the corresponding fits for a model without an additional lipid layer for comparison. Note that the data has been plotted as RQ (4) versus Q in order to highlight the difference between the fits. (C) Model (not to scale) of the effect of cooling the membrane to 25 °C. (D) Model of the membrane including attached vesicles, which would give rise an additional layer aligned with the membrane. dr denotes the repeat distance which is consistent with the dr of multilamellar vesicles of DPPC (Supporting Information Figure S2). The clean surfaces were measured in D2O and H2O, but the data and fits have been omitted for clarity in both A and B.
| sample | deposition temp/°C | measured temp/°C | layer | d/Å | ϕ/% | Awet/Å2 | Amol/A2 | Γ/mg m–2 | d/Å |
|---|---|---|---|---|---|---|---|---|---|
| 1 | 50 | 50 | head | 6.8 | 70 | 69 ± 11 | 64 ± 3 | 3.5 ± 0.5 | 41.6 ± 6 |
| tail | 28 | 91 | 70 ± 4 | ||||||
| head | 6.8 | 70 | 69 ± 11 | ||||||
| 25 | head | 6.6 | 72 | 69 ± 11 | 47 ± 2 | 3.5 ± 0.6 | 50.7 ± 6 | ||
| tail | 37.5 | 68 | 70 ± 4 | ||||||
| head | 6.6 | 72 | 69 ± 11 | ||||||
| 2 | 25 | 25 | head | 6.8 | 86 | 55 ± 8 | 48 ± 2 | 4.4 ± 0.7 | 50.1 ± 6 |
| tail | 37 | 87 | 55 ± 4 | ||||||
| head | 6.8 | 86 | 55 ± 8 | ||||||
| water | 14 | 100 | 14 ± 2 | ||||||
| bilayer | 50 | 14 | 347 ± 126 | 49 ± 18 | 0.7 ± 0.3 | 50 ± 3 |
The parameters used for fitting neutron reflectivity data were d = thickness, φ = surface coverage of the layer, Awet = wet area per lipid molecule, Amol = area per lipid molecule, Γ = surface density. In sample 1, the SiO2 layer was 10 ± 1 Å thick, 4 ± 1 Å rough, and contained 12 ± 1 v/v% water (due to porosity) while in sample 2 the numbers were 6 ± 1 Å, 5 ± 1 Å, and 0 v/v%, respectively. The lipid heads and tails were assumed to have molecular volumes of Vhead = 326.3 Å2 and Vtails = 889.2 Å2, respectively, obtained from molecular dynamics simulations. (28) The fitting errors of the headgroup and tail thicknesses are ±1 Å, while the errors in ϕ are ±3 v/v% as determined by the quality of the fits. (24) The molecular scattering length density of the headgroups was 1.85 × 10–6 for both samples while for the tails the values were 6.89 × 10–6 Å–2 (dDPPC) for sample 1 and −0.35 × 10–6 Å–2 for sample 2 (hDPPC). The SLD of the extra layer of hDPPC in sample 2 was fitted to 0.3 × 10–6 Å–2, which is an average of the SLDs of the components of a bilayer.
Outlook
Supporting Information
QCM-D traces for the deposition of DPPC bilayers in buffer and in pure water at 25 and at 50 °C. Additional information on neutron reflection measurements, fitting procedures, and models. SAXS data of multilamellar DPPC vesicles used to obtain the lamellar repeat distance. This material is available free of charge via the Internet at http://pubs.acs.org.
Terms & Conditions
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Acknowledgment
We thank Pierre-Yves Chapuis and Kell Mortensen for access to the SAXS instrument. M.C. gratefully acknowledges financial support from the Center for Synthetic Biology at Copenhagen University funded by the UNIK research initiative of the Danish Ministry of Science, Technology and Innovation, the DANSCATT Centre funded by the Danish government, and the Swedish Research Council. T.K.L thanks the European Spallation Source, ESS AB for funding her Ph.D. We thank neutron scattering facilities Institut Laue Langevin (Grenoble, France) and ISIS (Didcot, U.K.) for allocated beam time and Robert Barker (ILL) and Maximilian Skoda (ISIS) for local support.
References
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- 29Seantier, B.; Breffa, C.; Félix, O.; Decher, G. In situ investigations of the formation of mixed supported lipid bilayers close to the phase transition temperature Nano Lett. 2004, 4, 5– 10
- 30Leonenko, Z. V.; Finot, E.; Ma, H.; Dahms, T. E. S.; Cramb, D. T. Investigation of temperature-induced phase transitions in DOPC and DPPC phospholipid bilayers using temperature-controlled scanning force microscopy Biophys. J. 2004, 86, 3783– 3793[Crossref], [PubMed], [CAS], Google Scholar30https://chemport.cas.org/services/resolver?origin=ACS&resolution=options&coi=1%3ACAS%3A528%3ADC%252BD2cXltlGlt7g%253D&md5=938caa38378da8ff2acd4a47fb7587a8Investigation of temperature-induced phase transitions in DOPC and DPPC phospholipid bilayers using temperature-controlled scanning force microscopyLeonenko, Z. V.; Finot, E.; Ma, H.; Dahms, T. E. S.; Cramb, D. T.Biophysical Journal (2004), 86 (6), 3783-3793CODEN: BIOJAU; ISSN:0006-3495. (Biophysical Society)Under physiol. conditions, multicomponent biol. membranes undergo structural changes which help define how the membrane functions. An understanding of biomembrane structure-function relations can be based on knowledge of the phys. and chem. properties of pure phospholipid bilayers. Here, we have investigated phase transitions in dipalmitoylphosphatidylcholine (DPPC) and dioleoylphosphatidylcholine (DOPC) bilayers. We demonstrated the existence of several phase transitions in DPPC and DOPC mica-supported bilayers by both at. force microscopy imaging and force measurements. Supported DPPC bilayers show a broad Lβ-Lα transition. In addn. to the main transition we obsd. structural changes both above and below main transition temp., which include increase in bilayer coverage and changes in bilayer height. Force measurements provide valuable information on bilayer thickness and phase transitions and are in good agreement with at. force microscopy imaging data. A De Gennes model was used to characterize the repulsive steric forces as the origin of supported bilayer elastic properties. Both electrostatic and steric forces contribute to the repulsive part of the force plot.
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Abstract

Figure 1

Figure 1. (A) Δf (blue) and Δd (red) as a function of vesicle exposure time on a clean silica surface at 25 °C (broken lines) or 50 °C (solid lines). The data shown corresponds to the seventh overtone. At t = 0 s, a solution of SUVs was introduced into the cells. (B) AFM image of the formation of a DPPC bilayer at RT under constant flow conditions. Raster scanning was performed in the direction along the arrow. The numbers correspond to (1) clean mica, before lipids have reached the surface, (2) small lipid bilayer patches formed instantaneously and fused to create a bilayer, and (3) vesicles attached to the bilayer. (C) Imaging during rinsing with water at RT. (D) Image after rinsing and equilibration with hot water (above Tm).
Figure 2

Figure 2. Neutron reflectivity curves. (A) dDPPC measured at 50 °C (red) and after cooling to 25 °C (gray). Data points in solid circles were measured in D2O (SLD = 6.35 × 10–6 Å–2), while data points in open circles were measured in H2O (SLD = −0.56 × 10–6 Å–2). (B) hDPPC membrane deposited and measured at 25 °C. The gray data points and the solid line correspond to reflectivity measured in D2O and the best fit to the data. This fit includes an additional lipid layer on top of the membrane, separated by a layer of water. The additional layer has a coverage of 14 ± 1 v/v% and is believed to stem from attached vesicles. The red data is measured in CM4 (contrast matched to SLD = 4 × 10–6 Å–2). The broken lines give the corresponding fits for a model without an additional lipid layer for comparison. Note that the data has been plotted as RQ (4) versus Q in order to highlight the difference between the fits. (C) Model (not to scale) of the effect of cooling the membrane to 25 °C. (D) Model of the membrane including attached vesicles, which would give rise an additional layer aligned with the membrane. dr denotes the repeat distance which is consistent with the dr of multilamellar vesicles of DPPC (Supporting Information Figure S2). The clean surfaces were measured in D2O and H2O, but the data and fits have been omitted for clarity in both A and B.
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- 30Leonenko, Z. V.; Finot, E.; Ma, H.; Dahms, T. E. S.; Cramb, D. T. Investigation of temperature-induced phase transitions in DOPC and DPPC phospholipid bilayers using temperature-controlled scanning force microscopy Biophys. J. 2004, 86, 3783– 3793[Crossref], [PubMed], [CAS], Google Scholar30https://chemport.cas.org/services/resolver?origin=ACS&resolution=options&coi=1%3ACAS%3A528%3ADC%252BD2cXltlGlt7g%253D&md5=938caa38378da8ff2acd4a47fb7587a8Investigation of temperature-induced phase transitions in DOPC and DPPC phospholipid bilayers using temperature-controlled scanning force microscopyLeonenko, Z. V.; Finot, E.; Ma, H.; Dahms, T. E. S.; Cramb, D. T.Biophysical Journal (2004), 86 (6), 3783-3793CODEN: BIOJAU; ISSN:0006-3495. (Biophysical Society)Under physiol. conditions, multicomponent biol. membranes undergo structural changes which help define how the membrane functions. An understanding of biomembrane structure-function relations can be based on knowledge of the phys. and chem. properties of pure phospholipid bilayers. Here, we have investigated phase transitions in dipalmitoylphosphatidylcholine (DPPC) and dioleoylphosphatidylcholine (DOPC) bilayers. We demonstrated the existence of several phase transitions in DPPC and DOPC mica-supported bilayers by both at. force microscopy imaging and force measurements. Supported DPPC bilayers show a broad Lβ-Lα transition. In addn. to the main transition we obsd. structural changes both above and below main transition temp., which include increase in bilayer coverage and changes in bilayer height. Force measurements provide valuable information on bilayer thickness and phase transitions and are in good agreement with at. force microscopy imaging data. A De Gennes model was used to characterize the repulsive steric forces as the origin of supported bilayer elastic properties. Both electrostatic and steric forces contribute to the repulsive part of the force plot.
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Supporting Information
ARTICLE SECTIONSQCM-D traces for the deposition of DPPC bilayers in buffer and in pure water at 25 and at 50 °C. Additional information on neutron reflection measurements, fitting procedures, and models. SAXS data of multilamellar DPPC vesicles used to obtain the lamellar repeat distance. This material is available free of charge via the Internet at http://pubs.acs.org.
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