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Real‐Time Detection of Nanoparticles Interaction with Lipid Membranes Using an Integrated Acoustical and Electrical Multimode Biosensor

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Particle & Particle Systems Characterization
Authors:
Yao Lu at Beijing Institute of Technology
Yao Lu
Hao Zhang
Hao Zhang
Hao Zhang
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Zhan Wang
Zhan Wang
Zhan Wang
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Sundo Jeong
Sundo Jeong
Sundo Jeong
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Abstract and Figures

Understanding interactions of nanoparticles with biomembranes is critical in nanomedicine and nanobiotechnology. The underlying mechanisms still remain unclear due to the fact that there are no reliable tools to follow such complex processes. In this work, the interactions between gold nanoparticles (AuNPs) and the supported lipid bilayer (SLB) are monitored in situ by a multimode biosensor integrating a quartz crystal microbalance with dissipation function (QCM‐D) and a field effect transistor (FET). Real‐time responses of frequency shift (Δf), dissipation (ΔD), and ion current (ΔI) are simultaneously recorded to provide complementary information for AuNPs translocation across the SLB. The combined mass loading, mechanical and electrical measurements reveal the dynamics of the particle–membrane interactions as well as the formation of transient pores or permanent defects in the membrane. AuNPs with different diameters, surface charge, and ligand properties are used to study their translocation behaviors, including adsorption on or desorption from the membrane surface, diffusion into or penetration through the lipid bilayer. This multimode sensing approach provides insights into the mechanism of the particle–membrane interactions and suggests a method of label‐free screening of nanomaterials' interaction with model membranes in a real‐time manner.
a) Schematic illustration and b) photograph setup of the integrated biosensor system composed of QCM‐D and FET. The SLB‐coated gold electrode of QCM‐D is connected to the gate electrode of FET and used as the shared working electrode for the biosensor system. A Ag/AgCl reference electrode is immersed into the QCM‐D flow module for electrical measurements of FET. c) Working principles of the multimode sensing system. Changes of frequency shift (Δf), dissipation (ΔD), and ion current (ΔI) are simultaneously and separately recorded to provide information for the adsorption of AuNPs, the deformation of SLB, and the penetration of AuNPs through the SLB.
a) Schematic illustration and b) photograph setup of the integrated biosensor system composed of QCM‐D and FET. The SLB‐coated gold electrode of QCM‐D is connected to the gate electrode of FET and used as the shared working electrode for the biosensor system. A Ag/AgCl reference electrode is immersed into the QCM‐D flow module for electrical measurements of FET. c) Working principles of the multimode sensing system. Changes of frequency shift (Δf), dissipation (ΔD), and ion current (ΔI) are simultaneously and separately recorded to provide information for the adsorption of AuNPs, the deformation of SLB, and the penetration of AuNPs through the SLB.
… 
FRAP experiments of the SLB. a) Fluorescence images of the Texas Red‐labeled SLB before bleaching (top), 5 min later after exposure to high‐intensity laser with the excitation wavelength of 595 nm (middle), and 2 min after the excitation laser was shut down (bottom). b) Fluorescence intensity of Texas Red‐labeled SLB as a function of time during the FRAP experiment.
FRAP experiments of the SLB. a) Fluorescence images of the Texas Red‐labeled SLB before bleaching (top), 5 min later after exposure to high‐intensity laser with the excitation wavelength of 595 nm (middle), and 2 min after the excitation laser was shut down (bottom). b) Fluorescence intensity of Texas Red‐labeled SLB as a function of time during the FRAP experiment.
… 
Characterizations of AuNPs with different sizes and functional groups. a) Chemical structures of AuNPs functionalized with groups of TTMA, TMA, and COOH. TEM images of AuNPs‐TTMA (b: 2 nm, c: 8 nm, d: 17 nm), e) AuNPs‐TMA of 2 nm, and f) AuNPs‐COOH of 2 nm.
Characterizations of AuNPs with different sizes and functional groups. a) Chemical structures of AuNPs functionalized with groups of TTMA, TMA, and COOH. TEM images of AuNPs‐TTMA (b: 2 nm, c: 8 nm, d: 17 nm), e) AuNPs‐TMA of 2 nm, and f) AuNPs‐COOH of 2 nm.
… 
Real‐time QCM‐D and FET responses for a,b) 2 nm, c,d) 8 nm, and e,f) 17 nm AuNPs‐TTMA when interacting with the SLB of POPG. AuNPs‐TTMA and PBS buffer were introduced to the SLB alternately at a flow rate of 100 µL min⁻¹. The frequency and dissipation responses of QCM‐D were the third overtone (f3 and D3). The FET measurements were conducted under a constant drain–source voltage (Vds) of 100 mV.
Real‐time QCM‐D and FET responses for a,b) 2 nm, c,d) 8 nm, and e,f) 17 nm AuNPs‐TTMA when interacting with the SLB of POPG. AuNPs‐TTMA and PBS buffer were introduced to the SLB alternately at a flow rate of 100 µL min⁻¹. The frequency and dissipation responses of QCM‐D were the third overtone (f3 and D3). The FET measurements were conducted under a constant drain–source voltage (Vds) of 100 mV.
… 
Real‐time responses of a) QCM‐D and b) FET for 2 nm AuNPs‐COOH when interacting with the SLB of POPG.
+2
Real‐time responses of a) QCM‐D and b) FET for 2 nm AuNPs‐COOH when interacting with the SLB of POPG.
… 
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FULL PAPER
1800370 (1 of 9) © 2018 WILEY-VCH Verlag GmbH & Co. KGaA, Weinheim
www.particle-journal.com
Real-Time Detection of Nanoparticles Interaction with Lipid
Membranes Using an Integrated Acoustical and Electrical
Multimode Biosensor
Yao Lu, Hao Zhang, Zhan Wang, Sundo Jeong, Min-Chul Jo, Myoung-Hwan Park,*
and Xuexin Duan*
Dr. Y. Lu, Prof. H. Zhang, Z. Wang, Prof. X. Duan
State Key Laboratory of Precision Measuring Technology & Instruments
Tianjin University
Tianjin 300072, China
E-mail: xduan@tju.edu.cn
S. Jeong, M.-C. Jo, Prof. M.-H. Park
Department of Chemistry
Sahmyook University
Seoul 01795, South Korea
E-mail: mpark@syu.ac.kr
The ORCID identification number(s) for the author(s) of this article
can be found under https://doi.org/10.1002/ppsc.201800370.
DOI: 10.1002/ppsc.201800370
nanoparticles in human health and eco-
systems are still not clear and require to
be addressed to ensure their sustainable
use and development. For example, some
ultrafine particulate matters, normally
considered as “nuisance dusts” from the
industrial emission, exhibit toxic biological
effects on human respiratory systems.[14]
The integration of nanoparticles into con-
sumer products induces unforeseeable
biological responses to living organisms
when contacting with human skin.[15,16]
Whether applied as nanomedicines or
concerned toxicity effects, the interactions
between nanoparticles and the cell mem-
branes, including the adsorption on the
membrane surface or the internalization
into the cell interior, are of central impor-
tance. Due to the great complexity of
native cell membranes, the supported
lipid bilayer (SLB) is commonly used as
a model system to investigate the particle–
membrane interactions since it exhibits
many of the properties of biological mem-
branes, such as lateral fluidity and imper-
meability to ionic species.[17,18]
Different sensors and surface characterization tools have
been applied to probe the interactions between nanoparti-
cles and the lipid membrane including atomic force micro-
scopy (AFM),[19–23] electrochemical impedance spectroscopy
(EIS),[24,25] and fluorescence microscopy.[26] Although these
methods can provide the information regarding the membrane
integrity upon attachment with the nanoparticles and express
the spatial distributions of these particles in lipids, it is still
challenging to monitor the complex translocation process of
nanoparticles across the lipid membrane.[27] For instance, the
EIS measurements can determine the configuration changes of
the lipid membrane by monitoring the variation of membrane
capacitance but in lack of kinematic information on the trans-
location process. Quartz crystal microbalance with dissipation
function (QCM-D), which is sensitive to the mass acoustically
coupled to the oscillatory motion of the sensor, provides a label-
free approach of monitoring nanoparticles interactions with the
lipid membranes in real time.[28–32] The interaction of nanopar-
ticles with the lipid membrane usually starts with their adsorp-
tion on the surface, which can be readily detected by QCM-D
Understanding interactions of nanoparticles with biomembranes is critical
in nanomedicine and nanobiotechnology. The underlying mechanisms still
remain unclear due to the fact that there are no reliable tools to follow such
complex processes. In this work, the interactions between gold nanoparticles
(AuNPs) and the supported lipid bilayer (SLB) are monitored in situ by
a multimode biosensor integrating a quartz crystal microbalance with
dissipation function (QCM-D) and a field effect transistor (FET). Real-time
responses of frequency shift (Δf), dissipation (ΔD), and ion current (ΔI) are
simultaneously recorded to provide complementary information for AuNPs
translocation across the SLB. The combined mass loading, mechanical and
electrical measurements reveal the dynamics of the particle–membrane
interactions as well as the formation of transient pores or permanent defects
in the membrane. AuNPs with different diameters, surface charge, and
ligand properties are used to study their translocation behaviors, including
adsorption on or desorption from the membrane surface, diffusion into or
penetration through the lipid bilayer. This multimode sensing approach
provides insights into the mechanism of the particle–membrane interactions
and suggests a method of label-free screening of nanomaterials’ interaction
with model membranes in a real-time manner.
Nanoparticle–Membrane Interactions
1. Introduction
Nanoparticles have been successfully applied for various bio-
medical applications such as imaging contrast agents,[1–3]
phototherapy agents,[4–6] biomarkers,[7–9] and drug delivery
carriers.[10–13] However, the potential risks of the engineered
Part. Part. Syst. Charact. 2019, 36, 1800370
... Water chemical analyses are performed to determine water quality, pollution, and hydrology via expensive and cumbersome facilities using complex pretreatment methods [1][2][3][4][5] . Recently, the availability of electronic nose technology for detection and characterization, through mimicking the human olfaction system, may offer a more rapid and simpler technique for monitoring changes in water [6][7][8][9] . More recently, colorimetric determinations of trace toxicants have become another alternative due to the ability of the technique to coordinate metalresponsive dyes such as porphyrin, terpyridine, and rhodamine [10][11][12] . ...
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