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A Facile Strategy for Electrochemical Analysis of Hydrogen Peroxide Based on Multifunctional Fe3O4@Ag Nanocomposites Zhenzhen Guo, Jun Xu, Jingzhong Zhang, Yayun Hu, Yue Pan, and Peng Miao ACS Appl. Bio Mater., Just Accepted Manuscript • DOI: 10.1021/acsabm.8b00101 • Publication Date (Web): 03 Jul 2018 Downloaded from http://pubs.acs.org on July 4, 2018

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is published by the American Chemical Society. 1155 Sixteenth Street N.W., Washington, DC 20036 Published by American Chemical Society. Copyright © American Chemical Society. However, no copyright claim is made to original U.S. Government works, or works produced by employees of any Commonwealth realm Crown government in the course of their duties.

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ACS Applied Bio Materials

A Facile Strategy for Electrochemical Analysis of Hydrogen

Peroxide Based

on

Multifunctional

Fe3O4@Ag Nanocomposites Zhenzhen Guo,† Jun Xu,‡ Jingzhong Zhang,† Yayun Hu,§ Yue Pan,*,§ and Peng Miao*,† †

Suzhou Institute of Biomedical Engineering and Technology, Chinese Academy of Sciences,

Suzhou 215163, People’s Republic of China ‡

Suzhou Blood Center, Suzhou 215006, People’s Republic of China

§

State and Local Joint Engineering Laboratory for Novel Functional Polymeric Materials,

College of Chemistry, Chemical Engineering and Materials Science, Soochow University, Suzhou 215123, People’s Republic of China

*

Corresponding authors.

E-mail addresses: [email protected] (Y. Pan), [email protected] (P. Miao).

ACS Paragon Plus Environment

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ABSTRACT: The authors are presenting the application of Fe3O4@Ag nanocomposites to highly sensitive and selective analysis of hydrogen peroxide (H2O2). The morphology and structure of the synthesized porous Fe3O4 nanoparticles and Fe3O4@Ag nanocomposites are well characterized by scanning electron microscopy (SEM), X-ray powder diffraction (XRD), UV-vis absorption spectrum, et al. The nanocomposites can be facilely modified on the magnetic glassy carbon electrode, which also exhibit sharp silver stripping peak owning to the loaded Ag nanoparticles. Since autocatalytic oxidation reaction of Ag nanoparticles occurs with the existence of H2O2, the peak current intensity is suitable to track H2O2 levels. The analytical performance is evaluated by the technique of linear sweep voltammetry, which shows a linear range from 0.5 to 20 µM. The limit of detection is as low as 0.16 µM. The detection can be completed in 5 min, which is quite fast and convenient. In addition, electrochemical track of H2O2 released from living cells is also achieved. Therefore, the potential applications in biological studies and disease theranostics are promised.

KEYWORDS: linear sweep voltammetry; porous magnetic nanoparticles; silver nanoparticles; cells; magnetic electrode; solid-state Ag/AgCl reaction.


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INTRODUCTION Hydrogen peroxide (H2O2) is a widely used chemical constituent in certain industrial processes.1 It also belongs to reactive oxygen species, which is distributed in many biological tissues and plays important roles in various biological processes including signalling, tissue damage aging, and carcinogenesis.2-4 An unusual level of H2O2 may result in different diseases such as neurodegeneration, diabetes, tumour and cardiovascular diseases.5-8 Sensitive detection of H2O2 as a molecular alarm is highly desired to monitor the oxidative stress state and to understand related biological mechanisms.9-10 In addition, H2O2 may also be used for the therapy of certain diseases. For instance, Kwon et al. developed antioxidant polymeric nanoparticles for the therapy of peripheral arterial disease, which have H2O2-responsive properties;11 some pro-drugs are studied to deliver H2O2 to certain tissues for therapeutic implications.12 Therefore, development of analytical tools for the determination of H2O2 in biological systems has aroused tremendous interest. Until now, various detection methods have been proposed. For example, Khataee et al. prepared a novel peroxidase mimetic nanozyme for highly sensitive detection of H2O2, which were composed of WS2 nanosheets and silver nanoclusters.13 Shen et al. developed a fluorescent probe with a huge emission shift which targeted mitochondria for the analysis of H2O2.14 Xu et al. constructed a gold nanoparticles and horseradish peroxidase (HRP) composed nanoplasmonic probe to investigate the role of H2O2 in the aggregation of α-Synuclein.15 Zhao et al. fabricated an amperometric biosensor using a peptide/HRP modified electrode.16 Although these methods may have sufficient sensitivity and accuracy, most of them rely on the catalytic reactions by HRP. The low durability and high cost made these methods impractical for widely use. The


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employment of nonenzymatic mimetics may overcome the above disadvantages, nevertheless, the reaction time is too long. Facile and rapid detection of H2O2 is still in great demand. In this report, we develop a facile method for the synthesis of magnetic Fe3O4@Ag nanocomposites, which can be used for electrochemical detection of H2O2 from biological samples. Due to the multifunctions of the nanocomposites, the biosensor may meet the demands of fast response, high sensitivity and selectivity. Porous Fe3O4 core not only provides a large space for the immobilization of Ag nanoparticles, but also helps the modification of the nanomaterials on the magnetic electrode surface firmly and quickly. Autocatalytic oxidation reaction of Ag nanoparticles with the existence of H2O2 could reflect the level of H2O2. A limit of detection (LOD) as low as 0.16 µM is obtained, which is superior to most current methods. EXPERIMENTAL SECTION Synthesis of Fe3O4@Ag Nanocomposites. Pristine porous Fe3O4 nanoparticles were prepared as follows. First, 1.3 g of FeCl3, 4.7 g of sodium citrate dehydrate and 1.44 g of urea were added to 160 mL of pure water successively and then vigorously stirred for 20 min. Next, 1.2 g of polyacrylamide was slowly spiked into the solution of FeCl3, sodium citrate dehydrate and urea, coupled with vigorous stirring. The blended solution was further transferred into a 200 mL Teflon-lined autoclave and heated to 200 °C for half a day. Finally, the obtained product was washed with ethanol and then water, each for three times. The formed porous Fe3O4 nanoparticles were dried at 60°C before further use. To synthesize Fe3O4@Ag nanocomposites, the following experiments were conducted. First, 20 mg of pristine Fe3O4 and 1.2 g of polyacrylamide were added to 150 mL of pure water, followed by ultrasonication for 0.5 h. Meanwhile, AgNO3 solution was prepared by spiking 10.8


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mg of AgNO3 to 2 mL of pure water. The prepared AgNO3 solution was then added to the mixture of Fe3O4 and polyacrylamide solution under stirring. After that, it was ultrasonicated for 30 min. Subsequently, 2 mL of ascorbic acid (44 mg/mL) was slowly added to the above solution and the resulted solution was placed in the oven at 60°C for 30 min. Next, the formed Fe3O4@Ag nanocomposites were washed with ethanol and then water, each for three times. Finally, the nanocomposites were dried at 60°C before further use. Polyacrylamide used in the synthesis procedure could not only increase the water solubility of the nanomaterials,17 but also prevent the oxidation of Fe3O4 by H2O2.18 Therefore, the level of comprehensive H2O2 could be reflected by the consumption of Ag nanoparticles. Electrode Treatment. The substrate magnetic glassy carbon electrode was treated according to a previous work.19 Briefly, the electrode was incubated in piranha solution (98% H2SO4 : 30% H2O2 = 3 : 1) for 5 min. After the electrode was rinsed with pure water, it was polished to a mirror-like surface on P3000 silicon carbide paper. Next, the electrode was sonicated in ethanol and then water for 10 min. Finally, the cleaned electrode was dried with nitrogen. Quantitative Detection. The cleaned magnetic glassy carbon electrode was immersed in the Fe3O4@Ag nanocomposites solution (0.5 mg/mL) for 2 min. H2O2 standard solutions with a series of concentrations (0.5, 2, 10, 20, 40, 80, 160 µM) were freshly prepared. After modified with Fe3O4@Ag nanocomposites, the electrode was further incubated with different H2O2 solutions for another 2 min. Afterward, it was carefully rinsed before electrochemical measurement. In order to investigate the selectivity of the method, uric acid, glucose, ascorbic acid, dopamine, and acetaminophen (1 mM) were added to interact with the modified electrode for 2 min. After the reaction, the electrochemical responses were recorded for comparison.


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CHI660D electrochemical analyzer was employed for electrochemical measurements. A three-electrode system was constructed by an Ag/AgCl reference electrode, a platinum wire counter electrode and the modified glassy carbon electrode as the working electrode. Linear sweep voltammetry (LSV) was conducted in a potential scan range from -0.1 to 0.3 V using an electrolyte of 0.1 M KCl. 0.1 V / s was set as the scanning rate. Cell Culture and Cadmium-Induced H2O2 Generation. HeLa cells were cultured in DMEM medium with 10% (v/v) FBS. After the cells reach a confluence of 80%, they were firstly washed with phosphate buffered saline and then detached by trypsin. Finally, they were resuspended in DMEM medium containing cadmium (10 and 20 µg/mL) for 5 min.

RESULTS AND DISCUSSION Principles of Synthesis and Sensing. The synthesis of magnetic nanomaterials has attracted great interest due to their potential applications in ferrofluids, catalysis, biomedical diagnosis, magnetic resonance imaging and drug delivery technology.20-22 Fe3O4 based nanoparticles and nanocomposites are among the most important magnetic materials. Herein, we have prepared novel Fe3O4@Ag nanocomposites and applied them to facile electrochemical detection of H2O2. Detailed procedures are shown in Scheme 1. Fe3O4@Ag nanocomposites are synthesized by the reduction of AgNO3 under ultrasonication in the presence of ascorbic acid. Due to the porous structure, Fe3O4 nanoparticles have a relatively larger specific surface area. Besides, there is a physical 3D space as well. These factors can enhance the loading of numerous Ag nanoparticles.23 Since the inner space of porous Fe3O4 can be used for in-situ growth of Ag nanoparticles, the nanocomposites are superior to materials with surface loading only. The


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mechanism for H2O2 sensing is as follows. The Fe3O4@Ag nanocomposites are adsorbed on the electrode due to the magnetic property of the electrode. The Ag nanoparticles can be used as electrochemical probes, which exhibit highly characteristic solid-state Ag/AgCl reaction.24 Traditional modification technique may result in the agglomeration of Ag nanoparticles on the surface of electrode, which may affect the electrochemical response.25 However, the porous Fe3O4 nanoparticles may solve the problem by forming uniform distribution of Ag nanoparticles. The large number of loaded Ag nanoparticles thus exhibit significant silver stripping signals.26 In the presence of H2O2, Ag nanoparticles are oxidized and dissolved with the reaction as follows:24 Agn (solid) + 3H2O2 + 2H+ Agn-2 (solid) + 2Ag+ + O2 + 4H2O

(1)

Therefore, the decreased silver stripping peak current could be used to reflect the level of H2O2. The

synthesized

nanocomposites

show

multifunctions

including

magnetic

electrode

modification, dispersivity enhancement, signal generation and amplification. Note that the durations of electrode modification and the reaction with H2O2 are all 2 min, making the H2O2 biosensor quite convenient and time-saving. In addition, the analytical performances are also excellent. Therefore, the proposed method is supposed to have great potential utility challenging biological samples.


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Scheme 1. Illustrations of (a) preparation process of Fe3O4@Ag nanocomposites, (b) electrochemical detection of H2O2 based on LSV. Characterization of the Nanomaterials. From Figure 1a, the scanning electron microscope (SEM) image of the Fe3O4 nanoparticles are observed. The diameter of the coarse nanospheres is around 250 nm and the cracks on the surface evidence the porous structure. In the SEM image of Fe3O4@Ag, the bright dots coated on the surface of Fe3O4 are attributed to Ag nanoparticles (Figure 1b). In addition, transmission electron microscope (TEM) images clearly indicate that the inner color of Fe3O4@Ag nanocomposites is much darker than Fe3O4 nanoparticles, which demonstrates the diffusion of Ag+ in the porous Fe3O4 nanoparticles and subsequent reduction inside Fe3O4 nanoparticles (Figure S1). Furthermore, Figure 1c and d show the X-ray powder diffraction (XRD) patterns of the two materials. The peaks are well indexed to Fe3O4 and Ag, confirming the successful synthesis of the nanocomposites.


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Figure 1. SEM images of (a) porous Fe3O4 nanoparticles and (b) Fe3O4@Ag nanonocomposites. XRD patterns of (c) porous Fe3O4 nanoparticles and (d) Fe3O4@Ag nanocomposites. Qualitative Verification. Figure 2 depicts the UV-vis absorption spectra of Fe3O4 nanoparticles and Fe3O4@Ag nanocomposites before and after treatment with H2O2, respectively. In the curve of Fe3O4 nanoparticles, no absorption peak is observed. After treated with H2O2, the spectrum is barely changed. While in the curve of Fe3O4@Ag, a typical absorption peak around 420 nm emerges, which indicates the surface plasmon resonance of Ag nanoparticles. However, after reacted with H2O2, autocatalytic oxidation reaction occurs and Ag nanoparticles are dissolved, which could be reflected by the disappearance of the peak in the spectrum.


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Figure 2. UV-vis absorption spectra of (a) porous Fe3O4 nanoparticles, (b) after reacted with H2O2 (200 µM); (c) Fe3O4@Ag nanocomposites, (d) after reacted with H2O2 (200 µM). We have then employed LSV to further study this phenomenon. As shown in Figure 3a, a flat curve is observed on Fe3O4 nanoparticles modified electrode. Few changes occur after the reaction with H2O2. Due to the highly characteristic solid-state Ag/AgCl reaction in the presence Ag nanoparticles, a significant silver stripping peak is observed for Fe3O4@Ag nanocomposites modified electrode. After the addition of H2O2, the curve is found to be flat, which exhibits the consumption of Ag nanoparticles.


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Figure 3. LSV curves of (a) porous Fe3O4 nanoparticles modified electrode, (b) after reacted with H2O2 (200 µM); (c) Fe3O4@Ag nanocomposites modified electrode, (d) after reacted with H2O2 (200 µM). Quantitative Analysis of H2O2. In order to study the kinetics of autocatalytic oxidation reaction with the existence of 200 µM H2O2, the reaction time is optimized to be 2 min before the electrochemical analysis of H2O2 (Figure S2). The peak intensity of LSV is then used to characterize the level of H2O2. As shown in Figure 4a, with the increase of the amount of H2O2, the LSV peak drops gradually. The relationship between the decreased peak current and H2O2 concentration is depicted in Figure 4b, which shows that the ∆peak current is proportional to H2O2 concentration and the linear range is from 0.5 to 20 µM. The fitting equation is y = 2.69 + 1.61 x (n = 3, R2 = 0.99), in which y stands for the decreased peak current value of LSV (µA) and x is the concentration of used H2O2 (µM). LOD is calculated to be 0.16 µM (S/N = 3). H2O2 with low concentrations can be successfully distinguished (Figure S3). This method shows high


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sensitivity compare with recent developed H2O2 sensors (Table 1). The used materials are also much convenient, which promises its potential practical utility. In addition, since the modification of the glassy carbon electrode is facile, we have performed repeated detection of H2O2 after electrode cleaning and modification. The results of different concentrations of H2O2 show good consistency (Figure S4).

Figure 4. (a) LSV curves for the detection of H2O2 with the concentrations of 0.5, 2, 10, 20, 40, 80, 160 µM (from bottom to top). (b) Calibration curve of the H2O2 detection method. Inset


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shows the linear range. Error bars stand for standard deviations of three independent measurements. Table 1. Comparison of analytical performances of recent H2O2 biosensors.

Technique

Detection

LOD

range (µM)

(µM)

Materials

Ref

colorimetry

FePt-Au ternary metallic nanocomposites

20 to 700

12.33

27

colorimetry

Au@Ag nanorods

0 to 100

3.2

28

fluorescence

aggregation induced emission fluorogen

2.5 to 5000

2.5

29

amperometry

silver nanoparticles

20 to 5000

1.4

30

colorimetry

silver and gold nanoparticles

1.25 to 1250

1.2

31

0.8 to 12780

0.5

32

1 to 300

0.3

33

cuprous oxide, polyaniline and reduced amperometry graphene oxide nanocomposites Pd-Pt

nanocages

and

SnO2/graphene

amperometry nanosheets amperometry

concave Ag nanosheets

5 to 6000

0.17

34

fluorescence

polydopamine-glutathione nanoparticles

0.5 to 6

0.15

35


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this LSV

Fe3O4@Ag nanocomposites

0.5 to 20

0.16 work

Selectivity Investigation and Cells Analysis. Since Ag shows reactive behavior towards many materials, we have researched the selectivity of the proposed H2O2 biosensor by challenging a series of potential interfering substances including uric acid, glucose, ascorbic acid, dopamine, and acetaminophen. The decreased peak currents for the detection of H2O2 (10 and 100 µM) and the interfering substances (1 mM) are compared in Figure 5. All these interfering substances only result in negligible current response with much higher concentration. After mixing these molecules with H2O2, the obtained electrochemical result is similar to that of single H2O2. Therefore, the high selectivity of Fe3O4@Ag nanocomposites toward H2O2 detection is confirmed.


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Figure 5. Selectivity investigation of the H2O2 biosensor against a range of interfering substances (1 mM). The mixture sample contains H2O2 (100 µM) and the other interfering substances (1 mM). Consequently, the proposed method is applied to detect H2O2 released from living cells. Cadmium solution is used as the stimulating agent to induce the generation of H2O2.36 The cell states before and after treatment with different amount of cadmium can be observed in the inset of Figure 6. The untreated cells attach to the culture flask and show fusiform. However, after the treatment of 10 µg/mL cadmium, the shape changes and the cells gradually detach from the culture flask. As to the cells treated with 20 µg/mL cadmium, nearly all the cells are detached with round morphology. These changes may ascribed to cell damage caused by the released H2O2. We have then applied the proposed method for the detection of H2O2 in the medium of these cells. As shown in Figure 6, bare cadmium solution and DMEM of control cells generate negligible variations of peak currents, demonstrating the inexistence of H2O2. On the other hand, the culture mediums of the cells treated with cadmium show significant decreased LSV peaks. We have employed a commercial hydrogen peroxide assay kit to further demonstrate the cadmium-induced H2O2 release. The detected values of H2O2 in medium of cadmium-treated cells (10 and 20 µg/mL) are 4.5 and 6.7 times larger than that of control cells. There results indicate the proposed electrochemical method is suitable for practical utility with biological samples.


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Figure 6. Comparison of decreased current peaks of Fe3O4@Ag nanocomposites modified electrodes which have been incubated with (a) cadmium solution (20 µg/mL), (b) DMEM of control cells, DMEM of cells treated with (c) 10 and (d) 20 µg/mL cadmium for 5 min. Inset shows corresponding bright-field images of the cells. CONCLUSIONS In summary, we have prepared Fe3O4@Ag nanocomposites and fabricated a convenient biosensor for the detection H2O2 secreted from biological samples. The nanomaterials not only provide intense electrochemical signals, but also facilitate the sensing interface construction and the uniform distribution of Ag nanoparticles. Compared with other H2O2 sensors, this method exhibits high sensitively, selectivity, convenient operation and fast response, which may be a promising candidate for nonenzymatic H2O2 analysis for biological studies and disease theranostics. ASSOCIATED CONTENT


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Supporting Information The Supporting Information is available free of charge on the ACS Publications website. Materials and instruments, TEM images of the nanomaterials, optimization of reaction time, LSV analysis of H2O2 with low concentrations, repeatability investigation (PDF) AUTHOR INFORMATION Corresponding Author * Tel.: +86-512-69588279. E-mail: [email protected]. * E-mail: [email protected] Author Contributions All authors have given approval to the final version of the manuscript. ORCID Peng Miao: 0000-0003-3993-4778 Yue Pan: 0000-0001-7709-0508 Notes The authors declare no competing financial interest. ACKNOWLEDGMENT This work was supported by the National Natural Science Foundation of China (81771929, 51402203), the Key Research and Development Program of Jiangsu Province (BE2017669), the Science and Technology Program of Suzhou (SYG201736) and Science and Education Program of Health and Family Planning Commission of Suzhou (GWZX201504).


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Tang, L.; Mo, S.; Liu, S. G.; Li, N.; Ling, Y.; Li, N. B.; Luo, H. Q. Preparation of Bright

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