An electrochemical sensor for high sensitive determination of lysozyme based on the aptamer competition approach
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Open Chemistry 2021; 19: 299–306
Research Article
Kai Song*, Wenwu Chen
An electrochemical sensor for high sensitive
determination of lysozyme based on the aptamer
competition approach
https://doi.org/10.1515/chem-2021-0026
received July 20, 2020; accepted February 3, 2021
1 Introduction
Abstract: Protein is a kind of basic substance that con- The molecular weight of lysozyme is about 14.4 kDa, con-
stitutes a life body. The determination of protein is very taining 129 amino acid residues, and the isoelectric point
important for the research of biology, medicine, and is 11.0. It can destroy the cell wall of bacteria by cata-
other fields. Lysozyme is relatively small and simple in lyzing the hydrolysis of 1,4-β chains between n-acetyl-
structure among all kinds of proteins, so it is often used cell wall acid and N-acetylglucosamine residues in pep-
as a standard target detector in the study of aptamer tidoglycan and between N-acetylglucosamine residues in
sensor for protein detection. In this paper, a lysozyme chitosan [1–4]. Lysozyme is widely found in cell secre-
electrochemical sensor based on aptamer competition tions, such as saliva, tears, and other body fluids. Lyso-
mechanism is proposed. We have successfully prepared zyme is also widely used in pharmaceutical industry and
a signal weakening electrochemical sensor based on the food industry because of its antibacterial property. Lyso-
lysozyme aptamer competition mechanism. The carboxy- zyme molecules are relatively small, and it is often used
lated multi-walled carbon nanotubes (MWCNTs) were as a target detector in the study of aptamer sensors for
modified on the glassy carbon electrode, and the comple- protein detection [5–8].
mentary aptamer DNA with amino group was connected The traditional methods of detecting lysozyme are gel
to MWCNTs. Because of the complementary DNA of dauno- electrophoresis, high-performance liquid chromatography,
mycin into the electrode, the electrochemical signal is
and immunoassay including immunoelectrophoresis and
generated. When there is a target, the aptamer binds to
enzyme-linked immunosorbent assay [9,10]. However,
lysozyme with higher binding power, and the original
although the sensitivity of immunoassay is high, it needs a
complementary chain breaks down, resulting in the loss
long process of protein modification and is limited by the
of daunomycin inserted into the double chain and the
kinds of antibodies. Aptamer chain is easy to synthesize and
weakening of electrochemical signal. Differential pulse
modify and is usually more stable than antibody, so it is
voltammetry was used to determine lysozyme, the response
often used to detect lysozyme in recent years [9–17]. Zou
range was 1–500 nM, the correlation coefficient was 0.9995,
et al. [15] combined the aptamer with 6-carboxyfluorescein
and the detection limit was 0.5 nM. In addition, the pro-
to prepare an efficient lysozyme sensor. In addition, Wang
posed sensor has good selectivity and anti-interference.
et al. [16] obtained a fluorescent sensor using lysozyme
Keywords: differential pulse voltammetry, lysozyme, aptamer. Li and his collaborators [17] fixed DNA comple-
daunomycin, aptamer, multi-walled carbon nanotubes, mentary to lysozyme aptamer on the sensor; one end was
electrochemical analysis modified with ferrocene lysozyme aptamer, and hybridized
to the fixed chain. When there was a target, the aptamer
chain fell off from the electrode surface, resulting in the
weakening of electrical signal, and the detection limit of
the sensor reached 0.1 pM. However, it still takes more
time to modify the electrical signal marker at one end of
* Corresponding author: Kai Song, School of Drug and Food, Xuzhou
DNA [9,10].
Vocational College of Bioengineering, Xuzhou 221006, China,
e-mail: xqyim9@21cn.com
From the end of the last century to the present, it
Wenwu Chen: School of Drug and Food, Xuzhou Vocational College has been found that nanomaterials have the characteris-
of Bioengineering, Xuzhou 221006, China tics that conventional macromaterials do not have in
Open Access. © 2021 Kai Song and Wenwu Chen, published by De Gruyter. This work is licensed under the Creative Commons Attribution 4.0
International License.
300 Kai Song and Wenwu Chen
electromagnetic properties, catalysis, electricity, optics, insert double-stranded DNA specifically and DNM as
and other aspects [16–20]. Therefore, nanomaterials are the electrical signal indicator [47–49]. The carboxylated
more and more widely used in catalysis, sensors, and other multi-walled carbon nanotubes (MWCNTs) were modified
fields [21–25]. By controlling the synthesis conditions, on the glassy carbon electrode (GCE), and the comple-
many kinds of nanomaterials with different morphologies mentary aptamer DNA with amino group was connected
have been successfully prepared, such as nanoparticles to MWCNTs. Because DNM is inserted into complemen-
with tooth shape, strip shape, multilateral shape, and tary DNA on the electrode, electrochemical signals are
empty shell shape. Because of the large specific surface generated [50,51]. When there is a target, the aptamer
area and high reactivity of nanoparticles, the amount of combines with lysozyme with higher binding force, and
DNA modified on the electrode surface can be increased, the original complementary chain breaks down, resulting
thus improving the linear range and detection sensitivity in the falling off of DNM inserted into the double chain, so
of the sensor [26–28]. There is a strong covalent bond the electrical signal is weakened.
between gold particles and sulfhydryl group, and nano-
gold can be used as a probe to detect the target [29–34].
Carbon nanotubes have been widely used in the development
of chemical biosensors because of their good biocompat- 2 Experimental
ibility, effective specific surface, and good conductivity
[23,35–40]. All the reagents were of analytical grade. Nitric acid,
Daunomycin (DNM) is a chemotherapeutic drug potassium ferricyanide, potassium ferrocyanide, concen-
belonging to anthracycline antibiotics, which was first trated sulfuric acid, ethanol, and N,N-dimethylforma-
obtained from Streptomyces peucetius. DNM targets include mide (DMF) were purchased from Macklin Co. Ltd. and
DNA, membrane phospholipid, and protein. DNM has a used without purification (analytical grade). DNM is pro-
planar molecular structure, which can be embedded vided by Shanghai CDC. Lysozyme purchased from CETEC
between adjacent base pairs of complementary DNA Biotechnology (USA) Co., Ltd. DNA and complementary
(dsDNA), interferes with the process of DNA replication DNA are synthesized by Biotechnology (Shanghai) Co.,
and transcription, and induces DNA strand breakage Ltd. The sequence of oligonucleotide used was 5′-HS-
through oxygen-free radicals or top II media. In addition, (CH2)6-ATCTACGAATTCATCAGGGCTAAAGAGTGCAGAGTT
DNM can interact with membrane phospholipids, thus ACTTAG-(CH2)6-NH2-3′. The sequence of dsDNA was 5′-
affecting intracellular information pathways and can also CTAAGTAACTCTGCAGAG-3′. MWCNTs were purchased
react with a variety of proteins to induce apoptosis [41–53]. from Shenzhen Nanotechnology Co., Ltd. 1-Ethyl-3-(3-
Based on the above characteristics, DNM is often used to dimethylaminopropyl)-carbodiimide (EDC) and n-hydroxy-
treat some cancers. succinimide (NHS) were purchased from Sigma. Phosphate-
In this study, the electrochemical sensor of lysozyme buffer solution (PBS) was prepared by mixed stock solutions
based on the mechanism of aptamer competition was of 0.1 M disodium hydrogen phosphate and sodium dihy-
prepared using the characteristics of normycin that can drogen phosphate.
Figure 1: Assembly process of lysozyme sensor.
Electrochemical sensor for lysozyme detection 301
The electrochemical experiment was carried out on the
CHI 760C electrochemical analyzer (Shanghai Chenhua
Instrument Co., Ltd., China). Three electrode system was
adopted: modified electrode as working electrode, platinum
wire electrode as counter electrode, and saturated calomel
electrode as reference electrode (SCE); the solution used in
the electrochemical impedance analysis was 0.1 M KCl con-
taining 10 mM K4[Fe(CN)6] and 10 mm K3[Fe(CN)6]. Both
cyclic voltammetry (CV) and differential pulse voltammetry
(DPV) experiments use 0.1 M PBS as the test solution (con-
taining 0.1 M KCl, pH 6.4).
The assembly process of electrode surface is shown
in Figure 1. MWCNT (5 mg) was dispersed in 5 mL of anhy-
drous DMF for 1 h sonication; 5 μL of them was added to
Figure 2: EIS spectra of bare GCE (blue), MWCNTs/GCE (red), and
the GCE and placed in a drying oven for 24 h. After DMF
dsDNA/Au/GCE (black) at 10 mM [Fe(CN)6]4−/3− solution.
volatilized, a thin layer of MWCNTs was formed on the GCE
(denoted as MWCNTs/GCE). The aptamer DNA with a con-
centration of 20 μM was mixed with complementary DNA, 3 Results and discussion
heated to 94°C, and then cooled slowly at room tempera-
ture. Add 5 mL of mixed solution of 10 mM EDC and 10 mM EIS can reflect the process of electrode modification accord-
NHS on MWCNTs/GCE to activate the carboxyl group on ing to the change of electrode impedance. Figure 2 shows the
carbon nanotubes. After 10 min, take 5 μL of annealed impedance spectrum of the modified electrode in 10 mm
complementary DNA and drop it on MWCNTs/GCE. Cover [Fe(CN)6]4−/3− solution, with the frequency varying from
the electrode with plastic tube to prevent liquid volatiliza- 0.01 Hz to 10 kHz. It can be seen from Figure 2 that compared
tion and let it stand for 1 h. Then rinse with ultra-pure with the bare GCE, the conductivity of MWCNTs/GCE is sig-
water. The electrode was recorded as dsDNA/MWCNTs/ nificantly enhanced, and the semicircle of impedance is sig-
GCE. Finally, 5 μL of DNM solution with a concentration nificantly smaller. When DNA was modified, the impedance
of 10 mM was dropped on dsDNA/MWCNTs/GCE, which reached 8,000 Ω, indicating that DNA was successfully modi-
was left for 5 min at 4°C, and the electrode was washed fied on the electrode surface [51,52].
with ultra-pure water. DNM–dsDNA/MWCNTs/GCE was Figure 3 is a scanning electron micrograph of the
used to represent the modified electrode. surface of the modified electrode. Clean the surface of
bare GCE. After the carbon nanotubes were modified,
Ethical approval: The conducted research is not related to it was clear that the carbon nanotubes were uniformly
either human or animal use. distributed on the surface of the GCE. The length of
Figure 3: SEM images of (a) bare GCE and (b) MWCNTs/GCE.
302 Kai Song and Wenwu Chen
Figure 4: (a) CV of DNM–dsDNA/MWCNTs/GCE in PBS. Enlarged (b) negative scan and (c) positive scan of DNM–dsDNA/MWCNTs/GCE.
the carbon tube is about 1 μm, and the diameter is for 2 h at 25°C. Then put the electrode into PBS solution
50–100 nm. The morphology is beneficial to increase and test the DPV signal. The results are shown in Figure
the specific surface area of the electrode. 5a. The response current of the electrode decreases with
The electrochemical behavior of the DNM–dsDNA/ the increase in lysozyme concentration. Figure 5b shows
MWCNTs/GCE in PBS is shown in Figure 4a. DNM can the linear correction relationship between lysozyme con-
produce two pairs of redox peaks. A pair of peaks in centration and response current. The detection range of
the range of 0.20–0.40 V is produced by the phenolic lysozyme was 1–500 nM, and the detection limit was
structure in DNM molecule. A pair of peaks between 0.5 nM. Under the same conditions, the lysozyme showed
0.60 and 0.70 V is related to the quinone structure. no electrochemical signal on GCE, MWCNTs/GCE, and
Figure 4b and c shows the DPV of the electrode. It can dsDNA/MWCNTs/GCE. Table 1 shows the comparison of
be seen from the figure that there are also two groups of previous report with our result.
peaks in DPV, which is consistent with the result of CV The effect of different scanning speeds on the oxida-
chart. The peak current of a pair of peaks of 0.60–0.70 V tion peak current of DNM–dsDNA/MWCNTs/GCE in PBS
related to quinone structure is larger, and the peak cur- solution (Figure 6) before and after lysozyme (Figure 7)
rent increases rapidly with the increase in DNM inserted detection was investigated. The oxidation peak current
into DNA double helix. Therefore, we choose DPV signal increases with the increase in sweep rate, while the
of the oxidation peak of this group of peaks for quantita- peak potential is basically unchanged. The sweep speed
tive determination. is in the range of 100–600 mV/s, and the peak current
Add 20 μL lysozyme solution with different concen- has a good linear relationship with the sweep speed. This
trations on DNM–dsDNA/MWCNTs/GCE, respectively, shows that the electrochemical reaction is controlled by
and wash the electrode with PBS solution after standing adsorption [57]. In addition, when the sensor detects
Figure 5: (a) DPV curves of the DNM–dsDNA/MWCNTs/GCE toward to different concentrations of lysozyme. (b) Plots of concentrations of
lysozyme with the peak current.
Electrochemical sensor for lysozyme detection 303
Table 1: Comparison of previous reports with the dsDNA/MWCNTs/ 10 nM lysozyme, there is a good linear relationship
GCE toward lysozyme determination between peak current and scanning speed in the range
of scanning speed of 100–600 mV/s. It suggested the
Method Limit of detection (nM) Reference electrochemical reaction is controlled by adsorption
Electrochemical 0.45 [52] as well.
Electrochemical 35 [53] The effective area of the electrode can reflect whether
Electrochemical 36 [54] the layer by layer modification is successful. The effective
Electrochemical 350 [55]
area data of the electrode can be obtained by chronocoulo-
Electrochemical 7 [56]
Optical 2 [57]
metry in 0.1 M KCl + 10 mM K3[Fe(CN)6] solution. Figure 8
Optical 0.5 [58] shows the timing Coulomb data of bare GCE and
ECL 7 [59] MWCNTs/GCE. The slope can be obtained by plotting
Electrochemical 0.5 This work the square of time (t) with current (I). The electroche-
mical effective surface areas of bare GCE and MWCNTs/
GCE modified electrodes can be calculated as 0.00052
Figure 6: CVs of DNM–dsDNA/MWCNTs/GCE in the absence of the lysozyme with different scan rate (100, 150, 200, 250, 300, 350, 400, 450,
500, 550, and 600 mV/s).
Figure 7: CVs of DNM–dsDNA/MWCNTs/GCE in the presence of 10 nM lysozyme with different scan rate (50, 100, 150, 200, 250, 300, 350,
400, 450, 500, 550, and 600 mV/s).
304 Kai Song and Wenwu Chen
The relative standard deviation of 5 nM lysozyme was
5.2%, which indicated that DNM–dsDNA/MWCNTs/GCE
sensor had good reproducibility. When the sensor needs
to be stored, it can be placed in a humid environment of
4°C. After 1 week of storage, the current response of the
electrode is 95% of the current response value when the
preparation is finished, which proves that the sensor has
good stability.
4 Conclusion
The DNM–dsDNA/MWCNTs/GCE sensor developed in this
Figure 8: Linear relationship between Q and t1/2 of GCE and
work is a new type of unmarked lysozyme detector. The
MWCNTs/GCE.
sensor uses DNM as the active substance of electrical
signal, which has the characteristics of strong signal
and high stability. The response range was 1–500 nM,
the correlation coefficient was 0.9995, and the detection
limit was 0.5 nM. Compared with the traditional electro-
chemical method, the sensor prepared in this chapter has
a wide linear range, strong anti-interference, high sensi-
tivity, and strong practicability.
Funding information: This work was supported by Xuzhou
science and technology plan project KC16SG274.
Author contributions: K. S.: conceptualization, metho-
dology, and review and editing; K. S. and W. C.: data
curation, formal analysis, and writing – original draft.
Figure 9: Anti-interference property of the proposed DNM–dsDNA/
MWCNTs/GCE. Conflict of interest: The authors declare no conflict of
interest.
and 0.00124 cm2, respectively. The experimental results Data availability statement: The datasets generated during
are in accordance with the expectation that the effective and/or analyzed during the current study are available
area of the electrode is increased and the sensitivity of the from the corresponding author on reasonable request.
electrode is improved [41].
Nonspecific adsorption often interferes with the
determination of target by biosensors. To verify the selec-
tivity of the sensor to the target, 20 μL of 100 nM glucose
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