Bo Kyeong Yoon

Chonnam National University

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Joshua A. Jackman

Sungkyunkwan University

Nam‐Joon Cho

Nanyang Technological University

Tun Naw Sut

Sungkyunkwan University

Soo-Hyun Park

BioMed X Institute

Abdul Rahim Ferhan

Nanyang Technological University

Won‐Yong Jeon

Sungkyunkwan University

Sue Woon Tan

Sungkyunkwan University

Vladimir P. Zhdanov

Boreskov Institute of Catalysis

Hyeonjin Park

Sungkyunkwan University

Gamaliel Junren

Nanyang Technological University

Cooperative Institutions

Nanyang Technological University

Sungkyunkwan University

Universidade Federal de Minas Gerais

Singapore Centre for Environmental Life Sciences Engineering

Government of the Republic of Korea

National University of Singapore

Suwon Research Institute

Hanyang University

Samsung (South Korea)

Agency for Science, Technology and Research

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Correlating Membrane Morphological Responses with Micellar Aggregation Behavior of Capric Acid and Monocaprin

Langmuir (2017)

Bo Kyeong Yoon Joshua A. Jackman Min Chul Kim Tun Naw Sut Nam‐Joon Cho

The interaction of single-chain lipid amphiphiles with phospholipid membranes is relevant to many scientific fields, including molecular evolution, medicine, and biofuels. Two widely studied compounds within this class are the medium-chain saturated fatty acid, capric acid, and its monoglyceride derivative, monocaprin. To date, most studies about these compounds have involved in vitro evaluation of their biological activities, while mechanistic details of how capric acid and monocaprin interact with phospholipid bilayers remain elusive. Herein, we investigated the effect of these two compounds on the morphological and fluidic properties of prefabricated, supported lipid bilayers (SLBs). The critical micelle concentration (CMC) of each compound was determined by fluorescence spectroscopy measurements. At or above its CMC, capric acid induced the formation of elongated tubules protruding from the SLB, as determined by quartz crystal microbalance-dissipation and fluorescence microscopy experiments. By contrast, monocaprin induced the formation of elongated tubules or membrane buds below and above its CMC, respectively. Fluorescence recovery after photobleaching (FRAP) experiments indicated that capric acid increased bilayer fluidity only above its CMC, whereas monocaprin increased bilayer fluidity both above and below its CMC. We discuss these findings in the context of the two compounds' structural properties, including net charge, molecular length and hydrogen-bonding capacity. Collectively, the findings demonstrate that capric acid and monocaprin differentially affect the morphological and fluidic properties of SLBs, and that the aggregation state of the compounds plays a critical role in modulating their interactions with phospholipid membranes.

Capric Acid

Quartz Crystal Microbalance

10.1021/acs.langmuir.6b03944

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Citations (53)

Unraveling How Ethanol-Induced Conformational Changes Affect BSA Protein Adsorption onto Silica Surfaces

Langmuir (2020)

Jia Tan Bo Kyeong Yoon Gamaliel Junren Tun Naw Sut Nam‐Joon Cho

Protein adsorption at solid–liquid interfaces is highly relevant to a wide range of applications such as biosensors, drug delivery, and pharmaceuticals. Understanding how protein conformation in bulk solution impacts adsorption behavior is fundamentally important and could also lead to the development of improved protein-based coatings. To date, relevant studies have been conducted in aqueous solutions, while it remains largely unknown how organic solvents and more specifically solvent-induced conformational changes might influence protein adsorption. Herein, using the quartz crystal microbalance-dissipation (QCM-D) and localized surface plasmon resonance (LSPR) techniques, we systematically investigated the real-time adsorption behavior of bovine serum albumin (BSA) protein onto silica surfaces in different water–ethanol mixtures ranging from 0 to 60% (v/v) ethanol. The results showed that there was greater protein adsorption at higher ethanol fractions in the 10–30% range, while more complex adsorption profiles were observed in the 40–60% range. The combination of QCM-D and LSPR measurements led us to further identify specific cases in water–ethanol mixtures where washing steps caused densification of the adsorbed protein layer as opposed to typical desorption of weakly adsorbed molecules in aqueous conditions. We discuss mechanistic factors that drive these overall adsorption trends by taking into account how ethanol fraction affects BSA conformation in bulk solution. Together, our findings demonstrate that BSA proteins can adsorb onto silica surfaces across a wide range of water–ethanol mixture conditions, while specific adsorption profiles depended on the ethanol fraction in a manner closely linked to solution-phase conformational properties.

Quartz Crystal Microbalance

Bovine serum albumin

Protein Adsorption

Aqueous two-phase system

10.1021/acs.langmuir.0c01478

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Citations (16)

Versatile formation of supported lipid bilayers from bicellar mixtures of phospholipids and capric acid

Scientific Reports (2020)

Tun Naw Sut Bo Kyeong Yoon Soo-Hyun Park Joshua A. Jackman Nam‐Joon Cho

Originally developed for the structural biology field, lipid bicelle nanostructures composed of long- and short-chain phospholipid molecules have emerged as a useful interfacial science tool to fabricate two-dimensional supported lipid bilayers (SLBs) on hydrophilic surfaces due to ease of sample preparation, scalability, and versatility. To improve SLB fabrication prospects, there has been recent interest in replacing the synthetic, short-chain phospholipid component of bicellar mixtures with naturally abundant fatty acids and monoglycerides, i.e., lauric acid and monocaprin. Such options have proven successful under specific conditions, however, there is room for devising more versatile fabrication options, especially in terms of overcoming lipid concentration-dependent SLB formation limitations. Herein, we investigated SLB fabrication by using bicellar mixtures consisting of long-chain phospholipid and capric acid, the latter of which has similar headgroup and chain length properties to lauric acid and monocaprin, respectively. Quartz crystal microbalance-dissipation, epifluorescence microscopy, and fluorescence recovery after photobleaching experiments were conducted to characterize lipid concentration-dependent bicelle adsorption onto silicon dioxide surfaces. We identified that uniform-phase SLB formation occurred independently of total lipid concentration when the ratio of long-chain phospholipid to capric acid molecules ("q-ratio") was 0.25 or 2.5, which is superior to past results with lauric acid- and monocaprin-containing bicelles in which cases lipid concentration-dependent behavior was observed. Together, these findings demonstrate that capric acid-containing bicelles are versatile tools for SLB fabrication and highlight how the molecular structure of bicelle components can be rationally finetuned to modulate self-assembly processes at solid-liquid interfaces.

Capric Acid

10.1038/s41598-020-70872-8

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Citations (13)

Supported Lipid Bilayer Formation from Phospholipid-Fatty Acid Bicellar Mixtures

Langmuir (2020)

Tun Naw Sut Soo-Hyun Park Bo Kyeong Yoon Joshua A. Jackman Nam‐Joon Cho

Supported lipid bilayers (SLBs) are versatile cell membrane-mimicking biointerfaces for various applications such as biosensors and drug delivery systems, and there is broad interest in developing simple, cost-effective methods to achieve SLB fabrication. One promising approach involves the deposition of quasi-two-dimensional bicelle nanostructures that are composed of long-chain phospholipids and either short-chain phospholipids or detergent molecules. While a variety of long-chain phospholipids have been used to prepare bicelles for SLB fabrication applications, only two short-chain phospholipids, 1,2-dihexanoyl-sn-glycero-3-phosphocholine and 1,2-diheptanoyl-sn-glycero-3-phosphocholine (collectively referred to as DHPC), have been investigated. There remains an outstanding need to identify natural alternatives to DHPC, especially ones that are more affordable, to improve fabrication prospects and application opportunities. Herein, we explored the potential to fabricate SLBs from bicellar mixtures composed of long-chain phospholipids and lauric acid (LA), which is a low-cost, naturally abundant fatty acid that is widely used in soapmaking and various industrial applications. Quartz crystal microbalance-dissipation (QCM-D) experiments were conducted to track bicelle adsorption onto silica surfaces as a function of bicelle composition and lipid concentration, along with time-lapse fluorescence microscopy imaging and fluorescence recovery after photobleaching (FRAP) experiments to further characterize lipid adlayer properties. The results identified optimal conditions where it is possible to efficiently form SLBs from LA-containing bicelles at low lipid concentrations while also unraveling mechanistic insights into the bicelle-mediated SLB formation process and verifying that LA-containing bicelles are biocompatible with human cells for surface coating applications.

Model lipid bilayer

Quartz Crystal Microbalance

10.1021/acs.langmuir.0c00675

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Citations (18)

Indirect Nanoplasmonic Sensing Platform for Monitoring Temperature-Dependent Protein Adsorption

Analytical Chemistry (2017)

Joshua A. Jackman Abdul Rahim Ferhan Bo Kyeong Yoon Jae Hyeon Park Vladimir P. Zhdanov

The development of highly surface-sensitive measurement approaches to monitor protein adsorption across different temperatures would advance understanding of how thermally activated processes contribute to the denaturation of adsorbed proteins. Herein, we established an indirect nanoplasmonic sensing approach to monitor the temperature-dependent adsorption and denaturation of bovine serum albumin (BSA) protein onto a silica-coated array of plasmonic gold nanodisks. A theoretical model was developed to explain how the denaturation of an individual, adsorbed protein molecule influences the localized surface plasmon resonance (LSPR) measurement response and provided an analytical framework to estimate the effect of temperature-dependent protein denaturation on the corresponding adsorption kinetics. The sensing performance of this measurement platform was also characterized across the tested range of temperatures. With increasing temperature (up to 50 °C), it was observed that adsorbed proteins undergo greater denaturation. Circular dichroism spectroscopy and dynamic light scattering experiments verified that individual BSA monomers in bulk solution had increasingly lower conformational stability at higher temperatures within this range, which correlated with the extent of denaturation in the adsorbed state. At higher temperatures, distinct kinetic profiles arising from multilayer/aggregate formation on the sensor surface were also detected. Taken together, our findings identify that the high surface sensitivity and temperature stability of LSPR sensors make them broadly useful analytical tools for monitoring thermally activated biomacromolecular interaction processes.

Denaturation (fissile materials)

Bovine serum albumin

Protein Adsorption

10.1021/acs.analchem.7b03921

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Citations (40)

Graphene Oxide Mimics Biological Signaling Cue to Rescue Starving Bacteria

Advanced Functional Materials (2021)

Joshua A. Jackman Bo Kyeong Yoon Natalia Mokrzecka Gurjeet S. Kohli Elba R. Valle‐González

Abstract There is extensive debate about how 2D nanomaterials such as graphene oxide (GO) affect bacteria. Various effects of GO are proposed, including bacterial growth inhibition or enhancement, killing, and no activity. Herein, we report that GO protects Staphylococcus aureus bacterial cells from death in starvation conditions with up to a 1000‐fold improvement in cell viability. Transcriptomic profiling reveals that bacterial cells in starvation conditions generally shut down metabolic activity, while only cells incubated with GO increase production of specific enzymes involved in the glyoxalase detoxification pathway along with repressed autolysis. The oxygen‐containing functional groups of GO resemble the molecular structure of methylglyoxal, which bacteria produce to adapt to nutrient imbalances and is detoxified by glyoxalase enzymes. The ability of GO to enable bacterial cell survival in starvation conditions and accompanying cellular responses support that bacterial cells perceive GO as a methylglyoxal‐mimicking nanomaterial cue to reshuffle cellular metabolism and defenses.

Autolysis (biology)

Microbial Metabolism

10.1002/adfm.202102328

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Citations (5)

Membrane adaptation limitations inEnterococcus faecalisunderlie sensitivity and the inability to develop significant resistance to conjugated oligoelectrolytes

RSC Advances (2018)

Gayatri Shankar Chilambi Iris H. Gao Bo Kyeong Yoon Soo-Hyun Park Lisa M. Kawakami

The growing problem of antibiotic resistant bacteria, along with a dearth of new antibiotics, has redirected attention to the search for alternative antimicrobial agents. Conjugated oligoelectrolytes (COEs) are an emerging class of antimicrobial agents which insert into bacterial cell membranes and are inhibitory against a range of Gram-positive and Gram-negative bacteria. In this study, the extent of COE resistance that Enterococcus faecalis could achieve was studied. Enterococci are able to grow in hostile environments and develop resistance to membrane targeting antibiotics such as daptomycin in clinical settings. Herein we expand our knowledge of the antimicrobial mechanism of action of COEs by developing COE-resistant strains of E. faecalis OG1RF. Evolution studies yielded strains with a moderate 4-16 fold increase in antimicrobial resistance relative to the wild type. The resistant isolates accumulated agent-specific mutations associated with the liaFSR operon, which is a cell envelope-associated stress-response sensing and regulating system. The COE resistant isolates displayed significantly altered membrane fatty acid composition. Subsequent, exogenous supplementation with single fatty acids, which were chosen based on those dominating the fatty acid profiles of the mutants, increased resistance of the wild-type E. faecalis to COEs. In combination, genetic, fatty acid, and uptake studies support the hypothesis that COEs function through insertion into and disruption of membranes and that the mechanism by which this occurs is specific to the disrupting agent. These results were validated by a series of biophysical experiments showing the tendency of COEs to accumulate in and perturb adapted membrane extracts. Collectively, the data support that COEs are promising antimicrobial agents for targeting E. faecalis, and that there is a high barrier to the emergence of severely resistant strains constrained by biological limits of membrane remodeling that can occur in E. faecalis.

Enterococcus faecalis

Daptomycin

Cell envelope

10.1039/c7ra11823f

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Citations (14)

Influence of NaCl Concentration on Bicelle-Mediated SLB Formation

Langmuir (2019)

Tun Naw Sut Joshua A. Jackman Bo Kyeong Yoon Soo-Hyun Park Kavoos Kolahdouzan

The deposition of two-dimensional bicellar disks on hydrophilic surfaces is an emerging approach to fabricate supported lipid bilayers (SLBs) that requires minimal sample preparation, works at low lipid concentrations, and yields high-quality SLBs. While basic operating steps in the fabrication protocol mimic aspects of the conventional vesicle fusion method, lipid bicelles and vesicles have distinct architectural properties, and understanding how experimental parameters affect the efficiency of bicelle-mediated SLB formation remains to be investigated. Herein, using the quartz crystal microbalance-dissipation and localized surface plasmon resonance techniques, we investigated the effect of bulk NaCl concentration on bicelle-mediated SLB formation on silicon dioxide surfaces. For comparison, similar experiments were conducted with vesicles as well. In both cases, SLB formation was observed to occur rapidly provided that the NaCl concentration was sufficiently high (>50 mM). Under such conditions, the effect of NaCl concentration on SLB formation was minor in the case of bicelles and significant in the case of vesicles where it is expected to be related primarily to osmotic pressure. At lower NaCl concentrations, bicelles also formed SLBs but slowly, whereas adsorbed vesicles remained intact. These findings were complemented by time-lapsed fluorescence microscopy imaging and fluorescence recovery after photobleaching measurements that corroborated bicelle-mediated SLB formation across the range of tested NaCl concentrations. The results are discussed by comparing the architectural properties of bicelles and vesicles along with theoretical analysis of the corresponding adsorption kinetics.

Model lipid bilayer

Quartz Crystal Microbalance

Vesicle fusion

10.1021/acs.langmuir.9b01644

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Citations (30)

Controlling adsorption and passivation properties of bovine serum albumin on silica surfaces by ionic strength modulation and cross-linking

Physical Chemistry Chemical Physics (2017)

Jae Hyeon Park Tun Naw Sut Joshua A. Jackman Abdul Rahim Ferhan Bo Kyeong Yoon

Understanding the physicochemical factors that influence protein adsorption onto solid supports holds wide relevance for fundamental insights into protein structure and function as well as for applications such as surface passivation.

Passivation

Bovine serum albumin

Protein Adsorption

Modulation (music)

10.1039/c7cp01310h

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Citations (62)

pH-Modulated Nanoarchitectonics for Enhancement of Multivalency-Induced Vesicle Shape Deformation at Receptor-Presenting Lipid Membrane Interfaces

Langmuir (2023)

Hyeonjin Park Tun Naw Sut Abdul Rahim Ferhan Bo Kyeong Yoon Vladimir P. Zhdanov

Multivalent ligand–receptor interactions between receptor-presenting lipid membranes and ligand-modified biological and biomimetic nanoparticles influence cellular entry and fusion processes. Environmental pH changes can drive these membrane-related interactions by affecting membrane nanomechanical properties. Quantitatively, however, the corresponding effects on high-curvature, sub-100 nm lipid vesicles are scarcely understood, especially in the multivalent binding context. Herein, we employed the label-free localized surface plasmon resonance (LSPR) sensing technique to track the multivalent attachment kinetics, shape deformation, and surface coverage of biotin ligand-functionalized, zwitterionic lipid vesicles with different ligand densities on a streptavidin receptor-coated supported lipid bilayer under varying pH conditions (4.5, 6, 7.5). Our results demonstrate that more extensive multivalent interactions caused greater vesicle shape deformation across the tested pH conditions, which affected vesicle surface packing as well. Notably, there were also pH-specific differences, i.e., a higher degree of vesicle shape deformation was triggered at a lower multivalent binding energy in pH 4.5 than in pH 6 and 7.5 conditions. These findings support that the nanomechanical properties of high-curvature lipid membranes, especially the membrane bending energy and the corresponding responsiveness to multivalent binding interactions, are sensitive to solution pH, and indicate that multivalency-induced vesicle shape deformation occurs slightly more readily in acidic pH conditions relevant to biological environments.

Membrane Curvature

10.1021/acs.langmuir.3c00777

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Citations (2)