Preservation of Supported Lipid Membrane Integrity from Thermal

Zhu , T.; Jiang , Z.; Nurlybaeva , E. M. R.; Sheng , J.; Ma , Y. Effect of Osmotic Stress on Membrane Fusion on Solid Substrate Langmuir 2013, 29, 637...
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Preservation of Supported Lipid Membrane Integrity from Thermal Disruption: Osmotic Effect Tao Zhu,†,∇ Zhongying Jiang,*,‡,§,∇ Yuqiang Ma,*,†,∥ and Yong Hu⊥ †

Collaborative Innovation Center of Advanced Microstructures and Department of Physics, Nanjing University, Nanjing 210093, China ‡ School of Electronics and Information Engineering, Yi Li Normal University, Yining 835000, China § Laboratory of Solid State Microstructures, Nanjing University, Nanjing 210093, China ∥ Center for Soft Condensed Matter Physics and Interdisciplinary Research, Soochow University, Suzhou 215006, China ⊥ College of Engineering and Applied Sciences, Nanjing University, Nanjing 210093, China S Supporting Information *

ABSTRACT: Preservation of structural integrity under various environmental conditions is one major concern in the development of the supported lipid membrane (SLM)based devices. It is common for SLMs to experience temperature shifts from manufacture, processing, storage, and transport to operation. In this work, we studied the thermal adaption of the supported membranes on silica substrates. Homogenous SLMs with little defects were formed through the vesicle fusion method. The mass and fluidity of the bilayers were found to deteriorate from a heating process but not a cooling process. Fluorescence characterizations showed that the membranes initially budded as a result of heating-induced lipid lateral area expansion, followed by the possible fates including maintenance, retraction, and fission, among which the last contributes to the irreversible compromise of the SLM integrity and spontaneous release of the interlipid stress accumulated. Based on the mechanism, we developed a strategy to protect SLMs from thermal disruption by increasing the solute concentration in medium. An improved preservation of the membrane mass and fluidity against the heating process was observed, accompanied by a decrease in the retraction and fission of the buds. Theoretical analysis revealed a high osmotic energy penalty for the fission, which accounts for the depressed disruption. This osmotic-based protection strategy is facile, solute nonspecific, and long-term efficient and has little impact on the original SLM properties. The results may help broaden SLM applications and sustain the robustness of SLM-based devices under multiple thermal conditions. KEYWORDS: supported lipid membrane, thermal stability, osmotic stress, lipid lateral area, fluidity, fission

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INTRODUCTION Supported lipid membranes (SLMs), sharing the fundamental properties of biological membranes (fluidity, permeability, biocompatibility, and host for membrane proteins), provide a relatively stable, excellent characterization platform for a variety of applications such as biosensors, fouling-resistant coatings, drug deliveries, and basic research on biophysical features of amphiphilic bilayers.1−5 Separated by a thin water layer of ∼1 nm,6 the SLMs and underlying substrates are ideally perfectly coupled and equal in area, while in practice the loss of membrane integrity creates problems to the utilities of the model. Holes in SLMs cause cargo leakage from the internal mesoporous/hydrogel supporting particles, disturbing the target delivery in SLM-based drug systems.1 Undesired molecule adsorptions may occur on the uncovered substrates, leading to failures in fouling resistances and specific biomolecule detections.2,3 Moreover, the high monolayer © XXXX American Chemical Society

curvature and hydrophobic lipid tail exposure at the defects can result in mechanical and affinity changes of the membranes.7 The SLMs containing defects fuse and disrupt far more easily than their intact counterparts.7,8 Earlier works have contributed greatly to the fabrications of complete membranes on supports. Using the common vesicle fusion method, it has been established that the lipid composition, buffer conditions, and substrate physicochemical properties influence the quality of the SLMs.9−12 More attempts have been made to preserve the membrane integrity under regular situations recently. Chief among these includes the constructions of air-stable and physiologically stable SLMs. To date, tethering adhesion-boost,13 polymerization rigidityReceived: December 13, 2015 Accepted: February 17, 2016

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DOI: 10.1021/acsami.5b12153 ACS Appl. Mater. Interfaces XXXX, XXX, XXX−XXX

Research Article

ACS Applied Materials & Interfaces enhancement,14 and protein-binding/obstacle water-trapping strategies15,16 were developed to diminish the damage from air/ water interfacial peel-off force. And PEGylation,17 crosslinking,18 combined with cell membrane coating,19 has been employed to reduce the SLM decomposition by serum components. The ultimate goal of these preservation investigations is to find a simple approach to maintain the bilayer architecture under various conditions, meanwhile reducing the side effect of membrane physical property changes. Yet this has proved to be challenging. For example, though improving stability in air and plasma, cross-linking between monolayers prominently decreases the lipid lateral diffusion.16 Increasing attention has been paid to the search for a novel mechanism to optimize the SLM stabilization from multidisciplinary researchers. Besides the possible changes in specific medium, SLMs inevitably experience thermal perturbations in their applications as well. Supported membranes are generally formed at temperatures above the main transition, kept at 4 °C in storage, and warmed to 37 °C in in vivo/in vitro tests. They are liable to be exposed to room/varied temperatures during numerous operations such as filtration, sonication, and reagent mixing. Nevertheless, the temperature shifts may irreversibly affect the membranes on substrates. Fluorescence microscopy study by Israelachvili et al. showed that large quantities of bright round structures grew from an intact SLM in response to a temperature rise of 10 °C. Cooling of the sample to the original temperature resulted in dark hole formation in the membrane.10 The thermal-history-induced defects were confirmed by atomic force microscopy in the presence of a gel/ fluid lipid phase transition.20,21 And liposomes were observed to form and depart from supported lipid multilayers with the elevation of temperature, indicating the compromise of the membrane integrity.22 The functioning of SLM-based devices was reported to suffer from the thermal disruption of the membranes. Jonkheijm et al. presented that SLM electrophoresis was severely constrained by the bilayer defects generated from the heating in electrical field.4 Membrane-coated colloids were found to aggregate and precipitate owing to the integrity breakdown in thermal oscillation.23 Spectrum measurement displayed profound loss in drug protection in SLM capsules after a temperature increase of 3 °C.5 And for SLM-based biosensors, antifouling could also suffer performance declines from the same membrane failure.2,3 Despite of the significant influences observed, to our knowledge, the disruption mechanism of temperature on supported membranes has not been investigated in detail before. A comprehensive picture of the phenomenon provides the basis for devising strategies to fabricate thermal-stable SLMs. In this work, we studied the impacts of thermal conditions on homogeneous model SLMs. Typically, the membranes were subjected to a heating or cooling process, which consisted of three successive steps of initial heating/cooling, subsequent holding, and final returning. The evolution kinetics and structure transformations of the SLMs were characterized by wide-field and confocal fluorescence microscopies. The membrane integrity loss was quantified by the substrateattached lipid mass change from quartz crystal microbalance with dissipation (QCM-D). We showed that the thermalinduced SLM disruption mainly arises from the membrane fissions driven by lipid lateral area expansion at the raised temperature. Osmotic stress generated spontaneously in budding was demonstrated to play a critical role in the process

from an energetic perspective and can be employed to depress the membrane disruption effectively. The findings may help broaden SLM applications and sustain the robustness of SLMbased devices under multiple thermal conditions.

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MATERIALS AND METHODS

Preparation of Supported Lipid Membranes. SLMs composed of 99.5 mol % 1,2-dimyristoyl-sn-glycero-3-phosphocholine (DMPC) and 0.5 mol % fluorescent probe 1,2-dioleoyl-sn-glycero-3-phosphoethanolamine-N-(7-nitro-2-1,3-benzoxadiazol-4-yl) (NBD-PE) (Avanti Polar Lipids) were prepared by the vesicle fusion method.24 Briefly, a complete dry lipid film was formed by evaporating chloroform solution of lipids under vacuum. The lipid film was hydrated by adding Tris buffer (10 mM tris(hydroxymethyl)aminomethane hydrochloride, given concentration of NaCl, pH = 7.4) with occasional shaking for 3 h. The suspension was then extruded using a miniextruder (Avanti Polar Lipids) with a 100 nm pore polycarbonate membrane. The resulting unilamellar vesicle solution was deposited on silica or borosilicate glass substrates at 37 °C for around 15 min to form complete SLMs. Using a Kalrez 6375 O-ring (Dupont), the substrate area available for a SLM was restricted to a 14 mm diameter circle (Figure 1A). The thermal response of the O-ring is negligible in our study; e.g., it swells < 0.7 vol % at 85 °C in water for 30 days. Excess vesicles were finally removed by buffer rinsing. Only freshly prepared SLMs were used in the subsequent experiments. Quartz Crystal Microbalance with Dissipation Monitoring. QCM-D measurements were performed on a Q-sense E1 system equipped with a flow window chamber and silica-coated quartz crystals (QSense AB). The technique is based on the resonant oscillation of a piezoelectric quartz crystal at a frequency ( f) and energy dissipation (D), which characterize the mass and viscoelasticity of adsorption film, respectively. For a rigid film, the shift in frequency (Δf) is related to the adsorption mass (Δm) by the Sauerbrey relation: Δf = −Δm/C, where C is the mass sensitivity constant.25 Sample solution was delivered to the measurement chamber by a peristaltic pump (Ismatec). And the temperature (T) was controlled by a Peltier element with an accuracy of 0.05 °C. A heating process was imposed using the following steps: Following SLM formation on silica and buffer rinsing (degassed by sonication) at 37 °C, the pumping was stopped to create a quiescent medium for the experiment. The temperature was then raised to 49 °C or other destination temperatures at a rate of 6 °C/min. After being held at the elevated temperate for 1 h, the chamber was cooled back to 37 °C at a rate of −6 °C/min. The sample was left to equilibrate for the next 35 min and finally rinsed with buffer to wash away the free or loosely bound structures on the membrane. A cooling process, where the temperature shifted in the opposite direction, was performed using a similar procedure. Fluorescence Microscopy. The use of the flow window chamber allows simultaneous surface imaging and QCM-D measurement. The fluorescence images of SLMs were captured using a DM6000 upright fluorescence microscopy equipped with a DFC500 CCD (resolution, 2040 × 1536; Lecia). A mercury lamp (Lecia) was used to illuminate and photobleach the samples. Bleaching was done with a 50× lens (NA 0.5) and full lamp power for 20 s, resulting in a rectangular bleached area. Images for recovery were taken at a reduced excitation power with a 20× lens (NA 0.4). Because of the low photobleaching efficiency, quantitive fluorescence recovery after photobleaching (FRAP) studies were not carried out in this experimental setup. Confocal Laser Scanning Microscopy. The fluorescence crosssectional images of SLMs were captured by a LSM 710 inverted confocal microscope equipped with a 25 mW Argon ion laser and 63× (NA 1.4) oil objective (Zeiss). For this characterization, SLMs were formed on 0.17 mm thick borosilicate cover glasses mounted in a RC30 flow chamber (Warner Instruments). A TC-324B heater controller (Warner) was used to control the sample temperature with an accuracy of 0.1 °C. The thermal treatment was applied using the same procedure as the QCM-D experiment except that the cooling was driven by ambient air. The SLM fluidity was determined by FRAP B

DOI: 10.1021/acsami.5b12153 ACS Appl. Mater. Interfaces XXXX, XXX, XXX−XXX

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ACS Applied Materials & Interfaces using the microscopy. For 1.5 s 100% laser intensity was used to bleach a circular spot of 20 μm diameter. The recovery kinetics was recorded with a delay of 3 s between each frame. The diffusion coefficient (DC) was estimated following the approach by Soumpasis: DC = 0.224w2 /t1/2, where w is the radius of bleach spot and t1/2 is the time to half fluorescence intensity recovery obtained by the singleexponential fit to the recovery curve. The mobile fraction (Rmobile) was determined using the following equation: Rmobile = (I∞ − I0)/(Ibef − I0), where Ibef, I0, and I∞ are the fluorescence intensities before bleaching, after bleaching, and after full recovery, respectively.26 Atomic Force Microscopy and Dynamic Light Scattering. Atomic force microscopy (AFM) experiments were conducted on a NanoWizard atomic force microscope (JPK) equipped with a temperature-controlled BioCell sample chamber (JPK) and silicon nitride cantilevers (DNP-S10, Bruker). SLMs were formed and imaged (contact mode, scan rate of 1.7 Hz) on borosilicate glasses mounted in the chamber at 37 °C. A first-order polynomial was subtracted from each line to compensate for sample tilt. The root-mean-square roughness (Rq) of the bare silica and glass substrates was determined in air. Dynamic light scattering (DLS) sizing and ζ potential analyses of liposomes were performed by a BI-9000 AT instrument (Brookhaven) with a wavelength of 633 nm at room temperature.

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RESULTS AND DISCUSSION Characterization of SLMs. We first characterized the SLMs prepared by the vesicle fusion method. The fluorescentlabeled DMPC unilamellar vesicles, having an average hydrodynamic size of 112 nm and ζ potential of −2.1 mV in 150 mM NaCl Tris buffer, were pumped into a QCM-D flow window chamber at 37 °C to initiate the SLM formation on silica substrate. QCM-D measurement showed first an increase and then decrease of −Δf and ΔD (Figure 1A), indicating the adhesion of the highly dissipative vesicles to substrate, followed by the rupture of the vesicles above critical adsorption coverage.24 The equilibria Δf and ΔD were approximately −26.5 Hz and 0.2 × 10−6, consistent with the typical values for a complete supported lipid membrane.9,27 The low ΔD (8 h (Figure 5C). This presents that the low Cs facilitates an efficient release of the membrane stress accumulated in heating, while the high Cs inhibits the action. Since the SLM stress is released through fissions, which are the origin of membrane disruption, we examined the buds with closed fission pore near the end of the elevated temperature period (t = 55 min) using the confocal microscopy (Figure 6). It is discovered that a decreasing proportion of around 98%, 65%, and 6% of the buds possessed the fission structure in 1.5, 150, and 1500 mM NaCl mediums, thus bridging between the results in QCM-D and FRAP about the Cs effect on SLM disruption and in fluorescence imaging about the Cs effect on the spontaneous interlipid stress release. We can obtain insight into the origin of this medium impacts by considering the SLM thermal response using a simplified model, in which a growing relative area mismatch between the membrane and substrate, mimicking the heating effect and modeled by substrate contraction, generates the budding and fission of a circular area of lipid bilayer with a diameter L. Figure 7A defines the curvature of bud (C) and half the central angle (θ). It may be derived that LC = 4 sin(θ/2) following Lipowsky, while LC = 0, 0−4, and 4 denote the planar bilayer, unfissioned bud, and fissioned bud, respectively.36 The contributions from elastic, adhesion, and osmotic energies thereby give the following: E = πkb(LC)2/2 + πL2wa/4 + πNRTL3 [LC − (LC)3/24]/64, where kb is the bending rigidity (∼10−20 J), wa is the adhesion potential (∼10−4 J/m2), and N is the osmolarity disparity across membrane.27,36 Note that the temperature dependence of the former two parameters is negligible in the present research.37−39 Figure 7B displays the plots of E as a function of LC under various Cs calculated for a typical bud with 7 μm L. It is shown that the energy barrier for the mismatch, corresponding to the stretching energy, to overcome in 1500 mM is one and three order(s) of magnitude higher than that in 150 and 1.5 mM NaCl buffers, respectively. The high energy cost implies the strong resistance against fission for the high Cs. A further estimated energy barrier shift produced by the varied bud size in our research does not influence the validation of this result. Table 1 manifests the dominant role of the osmosis in the energy barrier. Generally, the osmotic energy exceeds the adhesion and elastic energies by a factor of more than 102. And

Figure 4. 3D reconstitution of the SLM transformations during the heating process by confocal microscopy. (A) Z plane view of the three types of budding: (i) retraction at the elevated temperature; (ii) retraction with the temperature return; (iii) irreversible fission at high temperature. The z-heights of the images are 14.1, 15.2, and 11.1 μm, respectively. (B) Cross-sectional images displaying the coexistence of the fissioned and unfissioned buds near the end of the 49 °C period (t = 55 min, 150 mM NaCl Tris buffer).

96%, 93%, and 100% by the alteration of Cs from 1.5 to 1500 mM. This displays that the SLM disruption from the heating process may be depressed or enhanced by the increase or decrease of salt in the medium, respectively. The SLM transformation kinetics was parallelly acquired by the fluorescence microscopy (Figure 5A). Generally, bright objects generated with the rise of temperature. And the budding entered a transient or prolonged stable stage at 12 ± 2 min irrespective of the medium. Assuming a semispherical shape, the statistics give Gaussian peaks at 9.7, 7.5, and 5.1 μm for the area-equivalent-circle diameter (L) of these buds in 1.5, 150, and 1500 mM NaCl buffers (estimation error of the method, 29%; Figure 5B). The buds become smaller with the increase of Cs, possibly due to their larger surface/volume ratio, which decreases the higher osmotic energy penalty introduced

Table 1. SLM Property Changes from the Heating Treatment (ΔT = 12 °C) and Disruption Energy Barrier Analysis under Different Csa before treatment

a

2

after treatment 2

2

energy scale at the barrier (J) 2

Cs (mM)

m (ng/cm )

Rmobile (%)

DC (μm /s)

M (ng/cm )

Rmobile (%)

DC (μm /s)

bending

adhesion

osmotic

1.5 150 1500

473.4 ± 3.5 469.1 ± 1.8 471.6 ± 2.4

94 94 95

1.7 ± 0.2 1.7 ± 0.1 1.8 ± 0.1

424.0 ± 9.4 439.0 ± 7.1 469.7 ± 3.0

67 78 93

0.9 ± 0.2 1.3 ± 0.2 1.8 ± 0.1

10−19 10−19 10−19

10−15 10−15 10−15

10−13 10−11 10−10

Mean and standard deviations were obtained from three measurements. F

DOI: 10.1021/acsami.5b12153 ACS Appl. Mater. Interfaces XXXX, XXX, XXX−XXX

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ACS Applied Materials & Interfaces

Figure 5. Effect of Cs on SLM transformation kinetics upon heating to 49 °C. (A) Fluorescence microscopy images of the membranes at typical time points. (B) Statistical distribution of L. (C) Time profile of Nb in the ROI. The rapid decrease of Nb at low Cs after the initial increase reflects the ease of spontaneous release of the interlipid stress built from the heating.

Additional experiments were conducted to evaluate the generality, effectivity, and applicability of this osmotic-based SLM protection strategy. First, we changed the major solute in SLM medium from NaCl to sucrose or PEG 200 (the later two also contained 1.5 mM NaCl). The measurements at ∼3 M osmolarity all exhibited similar suppression against the thermalinduced disruption (Figure 8B). This demonstrates that the strategy is not salt specific and may be employed in situations where a certain buffer component cannot be modified, i.e., ionic concentration in SLM electrophoresis, by adding a second solute. Next, SLMs were exposed to consecutive heating circles, where the temperature was temporarily raised by 12 °C for 1 h and for 5 times with 1 h interval. It is shown that the SLM integrity at the low Cs continued to deteriorate with the circles, while the SLM at the high Cs was not obviously affected (Figure 8B), supporting the long-term effectivity of the strategy in thermal fluctuation. Lastly, in contrast to the previous constancy, the solution above the supported membranes was exchanged to higher/lower Cs buffer after preparation, which presents a preservation/destruction effect on the bilayer integrity upon heating (Supporting Information). This reveals that the strategy can be applied to the SLM-based products already manufactured. Difference between SLMs and Liposomes. Efforts have been devoted to revealing the correlation between lipid

it undergoes the most dramatic change in response to the alternation of Cs. As portrayed in Figure 8A, the origin of the osmotic penalty can schematically be attributed to the cavity formed between membrane and substrate in budding. Because of the semipermeability of the lipid bilayer,27 confirmed by the osmotic-induced bud swelling/shrinking, water may diffuse freely across the membrane to fill the cavity whereas ions cannot. The emerging internal and external solute concentration difference results in an osmotic stress across the membrane and unfavorable energy contribution to the fission process. Accordingly, the budding-out in high Cs is greatly hindered by its resulting large concentration disparity and osmotic stress. By contrast, the osmotic resistance in low Cs is small, and hence membrane curving and fission may efficiently carry out to release the interlipid stress accumulated in heating, which compromises the SLM integrity. Besides that, it should be noted that the adhesion and elastic energies may also increase with Cs owing to the ionic screening of lipid−substrate electrical repulsion and lipid repacking. However, the adhesion potential was reported to be on the scale of 10−4 J/m2 in both low (0 mM) and high (2 M) ionic strength conditions.11,12 And the salt-induced bilayer rigidification is generally insignificant with controversies about its presence in all zwitterionic phospholipids.40,41 The contributions from these two factors are therefore minor in the present research. G

DOI: 10.1021/acsami.5b12153 ACS Appl. Mater. Interfaces XXXX, XXX, XXX−XXX

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ACS Applied Materials & Interfaces

Figure 7. Estimation of the energy cost in SLM disruption using a simplified fission model. (A) Fission driven by the relative membrane/ substrate area change. (B) Plot of E versus LC (insert: logarithmic scale). Generally, higher Cs leads to larger energy barrier. The gray dotted line illustrates the energy calculated for L two times larger than the typical 7 μm, Cs = 1.5 mM. The small E shift with large L change demonstrates that the bud size disparity in our study does not influence the former result.

Figure 6. Confocal microscopy images of the SLMs under different Cs near the end of the 49 °C period (t = 55 min). (A) Cs = 1.5 mM; (B) Cs = 1500 mM. The proportion of the buds exhibiting closed fission pore decreased with the increase of Cs.

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CONCLUSION In this research, the impacts of the thermal condition changes on supported lipid membranes have been comprehensively studied. For a start, we characterized the SLM integrity using QCM-D and FRAP and found conspicuous mass and fluidity losses after a heating process. Fluorescence reconstitution indicated fissions as the origin of the membrane disruption, which is driven by the heating-induced lipid lateral area expansion. Next, we discovered that the SLM integrity loss from the treatment can be regulated by the salt added in the medium. High salt concentration depressed the spontaneous release of the interlipid stress accumulated in heating by decreasing the fissions of the membrane. Theoretical analysis exhibited that the budding-related osmotic energy penalty dominates the fission process. The penalty becomes manifest with the increase of the bulk salt concentration as a result of the semipermeability of lipid bilayer, which breaks the osmotic balance across the membrane during the budding. Finally, we presented that the osmotic-based SLM protection strategy is solute nonspecific and long-term effective and is not limited by the SLM preparation condition. Our study remarks on the significance of temperature in influencing SLM integrity. The thermal protection approach proposed is facile with low side effect on the membrane properties including mass and fluidity.

geometry and membrane structural dynamics at the molecular and macroscopic levels.42,43 Temperature shift was reported to generate membrane fissions in freestanding giant liposomes, attributed to the thermal-induced area−volume incompatibility.44,45 Compared to the liposome volume, the budding-related water transport across the membrane is commonly small. Thus, the osmotic change from the budding is negligible in this system. However, given the small volume encapsulated inside SLM (∼1 nm confined water layer),6 the budding-related volume change can greatly interfere with the original osmotic balance between the internal and external. Thus, osmosis may be employed to regulate the latter process. And our study does not involve the gel/fluid transition of lipids (the main transition temperature of DMPC is 24 °C), which has been adopted by many thermal researches on liposomes.10,21,45 The main transition produces a sudden change of the lipid lateral area by 20−25% within 2−4 °C,32 amplifying the thermal effects. We observed that even without passing through the transition, temperature can significantly affect the lipid bilayer integrity. Therefore, caution must be taken in modulating the temperature during SLM operations. H

DOI: 10.1021/acsami.5b12153 ACS Appl. Mater. Interfaces XXXX, XXX, XXX−XXX

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ACS Applied Materials & Interfaces Author Contributions ∇

T.Z. and Z.J. contributed equally to this work.

Notes

The authors declare no competing financial interest.

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ACKNOWLEDGMENTS We thank the Center for Biological Imaging (CBI), Institute of Biophysics, Chinese Academy of Science for part of our AFM work, and we are grateful to Dr. Yanxia Jia for her help in image capture and analysis. This work was supported by the National Basic Research Program of China (Grant No. 2012CB821500) and the National Natural Science Foundation of China (Grant Nos. 91427302, 11474155, and 21264016).

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(1) Liu, J.; Jiang, X.; Ashley, C.; Brinker, C. J. Electrostatically Mediated Liposome Fusion and Lipid Exchange with a NanoparticleSupported Bilayer for Control of Surface Charge, Drug Containment, and Delivery. J. Am. Chem. Soc. 2009, 131, 7567−7569. (2) Hinman, S. S.; Ruiz, C. J.; Drakakaki, G.; Wilkop, T. E.; Cheng, Q. On-Demand Formation of Supported Lipid Membrane Arrays by Trehalose-Assisted Vesicle Delivery for SPR Imaging. ACS Appl. Mater. Interfaces 2015, 7, 17122−17130. (3) Persson, F.; Fritzsche, J.; Mir, K. U.; Modesti, M.; Westerlund, F.; Tegenfeldt, J. O. Lipid-Based Passivation in Nanofluidics. Nano Lett. 2012, 12, 2260−2265. (4) van Weerd, J.; Krabbenborg, S. O.; Eijkel, J.; Karperien, M.; Huskens, J.; Jonkheijm, P. On-Chip Electrophoresis in Supported Lipid Bilayer Membranes Achieved Using Low Potentials. J. Am. Chem. Soc. 2014, 136, 100−103. (5) Wu, X.; Wang, Z.; Zhu, D.; Zong, S.; Yang, L.; Zhong, Y.; Cui, Y. pH and Thermo Dual-Stimuli-Responsive Drug Carrier Based on Mesoporous Silica Nanoparticles Encapsulated in a Copolymer-Lipid Bilayer. ACS Appl. Mater. Interfaces 2013, 5, 10895−10903. (6) Kim, J.; Kim, G.; Cremer, P. S. Investigations of Water Structure at the Solid/Liquid Interface in the Presence of Supported Lipid Bilayers by Vibrational Sum Frequency Spectroscopy. Langmuir 2001, 17, 7255−7260. (7) Van Lehn, R. C.; Ricci, M.; Silva, P. H. J.; Andreozzi, P.; Reguera, J.; Voitchovsky, K.; Stellacci, F.; Alexander-Katz, A. Lipid Tail Protrusions Mediate the Insertion of Nanoparticles into Model Cell Membranes. Nat. Commun. 2014, 5, 4482. (8) Chen, E. H.; Olson, E. N. Unveiling the Mechanisms of Cell-Cell Fusion. Science 2005, 308, 369−373. (9) Jackman, J. A.; Tabaei, S. R.; Zhao, Z.; Yorulmaz, S.; Cho, N. J. Self-Assembly Formation of Lipid Bilayer Coatings on Bare Aluminum Oxide: Overcoming the Force of Interfacial Water. ACS Appl. Mater. Interfaces 2015, 7, 959−968. (10) Anderson, T. H.; Min, Y.; Weirich, K. L.; Zeng, H.; Fygenson, D.; Israelachvili, J. N. Formation of Supported Bilayers on Silica Substrates. Langmuir 2009, 25, 6997−7005. (11) Jackman, J. A.; Choi, J. H.; Zhdanov, V. P.; Cho, N. J. Influence of Osmotic Pressure on Adhesion of Lipid Vesicles to Solid Supports. Langmuir 2013, 29, 11375−11384. (12) Schonherr, H.; Johnson, J. M.; Lenz, P.; Frank, C. W.; Boxer, S. G. Vesicle Adsorption and Lipid Bilayer Formation on Glass Studied by Atomic Force Microscopy. Langmuir 2004, 20, 11600−11606. (13) Deng, Y.; Wang, Y.; Holtz, B.; Li, J.; Traaseth, N.; Veglia, G.; Stottrup, B. J.; Elde, R.; Pei, D.; Guo, A.; Zhu, X. Y. Fluidic and AirStable Supported Lipid Bilayer and Cell-Mimicking Microarrays. J. Am. Chem. Soc. 2008, 130, 6267−6271. (14) Ross, E. E.; Bondurant, B.; Spratt, T.; Conboy, J. C.; O’Brien, D. F.; Saavedra, S. S. Formation of Self-Assembled, Air-Stable Lipid Bilayer Membranes on Solid Supports. Langmuir 2001, 17, 2305− 2307.

Figure 8. Effect of solute on SLM disruption in heating treatment. (A) Schematic illustrations of the generation of solute concentration disparity across the semipermeable lipid bilayer during the budding for fission. The high bulk solute concentration results in a large osmotic imbalance and energy penalty. (B) Membrane mass loss from the multiheating cycles (ΔT = 12 °C). “Control”, “PEG″, “sucrose”, and “NaCl” represent the experiments performed in 1.5 mM NaCl, 3000 mM PEG 200 + 1.5 mM NaCl, 3000 mM sucrose +1.5 mM NaCl, and 1500 mM NaCl Tris buffers. The first and the latter three solutions have osmolarities of ∼13 mM and 3 M, respectively. The average values from three measurements are shown.

The results may help extend SLM applications to the areas where the experience of temperature shifts is required, for example, the heating and annealing of multicomponent membrane to form desirable functional phase separated domains.46 Novel SLM capsulated cargo release systems may be developed based on the disparity in membrane disruption as well.

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ASSOCIATED CONTENT

* Supporting Information S

The Supporting Information is available free of charge on the ACS Publications website at DOI: 10.1021/acsami.5b12153. Details of effects of a cooling process on SLM integrity, osmotic response and retraction of buds in the heating process, and examples for the osmotic-based protection strategy applied after SLM formation (PDF)

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REFERENCES

AUTHOR INFORMATION

Corresponding Authors

*(Z.J.) Tel.: +86 13813955964. E-mail: [email protected]. *(Y.M.) Tel.: +86 025 83592900. E-mail: [email protected]. I

DOI: 10.1021/acsami.5b12153 ACS Appl. Mater. Interfaces XXXX, XXX, XXX−XXX

Research Article

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DOI: 10.1021/acsami.5b12153 ACS Appl. Mater. Interfaces XXXX, XXX, XXX−XXX