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Cite This: ACS Appl. Mater. Interfaces 2018, 10, 12504−12509

Novel Colorimetric Aptasensor for Zearalenone Detection Based on Nontarget-Induced Aptamer Walker, Gold Nanoparticles, and Exonuclease-Assisted Recycling Amplification Seyed Mohammad Taghdisi,†,‡,¶ Noor Mohammad Danesh,§,¶ Mohammad Ramezani,∥ Ahmad Sarreshtehdar Emrani,⊥ and Khalil Abnous*,∥,#

ACS Appl. Mater. Interfaces 2018.10:12504-12509. Downloaded from pubs.acs.org by UNIV OF SUSSEX on 07/10/18. For personal use only.

†

Targeted Drug Delivery Research Center, Pharmaceutical Technology Institute, ‡Department of Pharmaceutical Biotechnology, School of Pharmacy, ∥Pharmaceutical Research Center, Pharmaceutical Technology Institute, ⊥Cardiovascular Research Center, Faculty of Medicine, and #Department of Medicinal Chemistry, School of Pharmacy, Mashhad University of Medical Sciences, Mashhad 91778-99191, Iran § Research Institute of Sciences and New Technology, Mashhad 91778-99191, Iran S Supporting Information *

ABSTRACT: Zearalenone (ZEN) toxicity is a significant risk for human beings. Thus, it is of high importance to develop sensitive, precise, and inexpensive analytical methods for ZEN detection, especially in human serum. Here, a colorimetric aptasensor is presented for the determination of ZEN based on the nontarget-induced aptamer walker, catalytic reaction of gold nanoparticles (AuNPs), exonuclease III (Exo III) as a signal amplifier, and 4-nitrophenol as a colorimetric agent. Low amount of ZEN requirement and signal amplification are some of the distinct advantages of the proposed aptasensor. In the absence of ZEN, the aptamer (Apt) starts walking on the AuNP surface with the help of Exo III and binds to multiple complementary strands of aptamer, leading to the change of sample color from yellow to colorless. Upon the addition of ZEN, both the Apt and complementary strand exist as single-stranded DNAs on the surface of AuNPs, resulting in less access of 4-nitrophenol to the surface of AuNPs and less catalytic performance of AuNPs. In this situation, the color of the sample remains yellow (the color of 4-nitrophenol). The presented aptasensor was capable to detect ZEN in a wide linear dynamic range, 20−80 000 ng/L, with a detection limit of 10 ng/L. The prepared sensing strategy was successfully used for ZEN determination in the human serum sample. KEYWORDS: aptamer walker, zearalenone, gold nanoparticles, exonuclease III, sensor

1. INTRODUCTION

bodies because of their easy chemical synthesis, satisfactory stability, long-time storage, and inexpensive production.14−16 Among different analytical strategies, an aptamer-based colorimetric sensor has been widely used for routine analysis, owing to its convenience of visual observation, simplicity, and real-time analysis.17,18 Gold nanoparticles (AuNPs) are considered as ideal nanoparticles for colorimetric analysis because of their high extinction coefficient in the visible region, strong dependent optical characteristics, and catalytic activity.19−21 Recently, an electrochemical binding-induced DNA walker sensor was introduced for recognition of thrombin.22 Signal amplification and high sensitivity were advantages of the abovementioned electrochemical sensor. However, needing an electrochemical workstation and split aptamers or two different aptamers for a target limits the application of this sensor, especially for other targets. Moreover, in the mentioned study, walking strand DNA and one of the aptamers existed in one sequence, which could influence the affinity of the aptamer. In

Zearalenone (ZEN), a kind of resorcylic acid lactone, is a secondary metabolite produced by several Fusarium species.1,2 ZEN has low acute toxicity in most species, and its LD50 in rats and chickens is more than 2 g/kg body weight.3 However, ZEN can be found in most of grain crops, including rice and wheat.4 Chronic exposure to ZEN can cause severe adverse effects, such as neurotoxicity, carcinogenicity, and immunotoxicity.1,5 Also, ZEN as a mycoestrogen can impair reproduction.6,7 Therefore, innovation in the design of analytical techniques for the detection of ZEN is vitally important. Traditional methods for ZEN quantification include liquid chromatography−mass spectrometry, immunochemical approaches, gas chromatography, and high-performance liquid chromatography. The majority of these analytical methods need complicated sample handling procedures and sophisticated instruments.8−10 Aptamers have been broadly applied as recognition probes for various targets with high sensitivity and selectivity.11 Aptamers are short single-chained oligonucleotides isolated by a method known as systematic evolution of ligands by exponential enrichment.12,13 They provide outstanding features over anti© 2018 American Chemical Society

Received: February 7, 2018 Accepted: March 22, 2018 Published: March 22, 2018 12504

DOI: 10.1021/acsami.8b02349 ACS Appl. Mater. Interfaces 2018, 10, 12504−12509

Research Article

ACS Applied Materials & Interfaces this study, a colorimetric aptasensor was proposed for the determination of ZEN based on a nontarget-induced aptamer walker, exonuclease III (Exo III), and optical properties of AuNPs. The proposed sensing strategy exploits the catalytic performance of AuNPs, high sensitivity, and low amount of target requirement of aptamer walker and Exo III-assisted signal amplification. Furthermore, the designed colorimetric aptasensor requires only one aptamer without the addition of any sequence to it which can preserve the high affinity of aptamer toward its target.

The schematic illustration of ZEN detection is displayed in Scheme 1. In the absence of ZEN, the Apt and its CS are into Scheme 1. Representation of the Colorimetric Aptasensor for the Detection of ZEN Based on the Exo III-Assisted Aptamer Walker and Catalytic Reaction of AuNPs

2. MATERIALS AND METHODS 2.1. Reagents. The ZEN aptamer (Apt),23 5′-thiol-AGCAGCACAGAGGTCAGATGTCATCTATCTATGGTACATTACTATCTGTAATGTGATATGCCTATGCGTGCTACCGTGAA-3′, and its partial complementary sequence (CS), 5′-thiol-TTTACGGTAGCACGCATAGGCAT-3′, were synthesized by Bioneer (South Korea) (complementary sections have been shown with the same color). Ochratoxin A (OTA), sodium borohydride (NaBH4), aflatoxin B1 (AFB1), sodium citrate, human serum, aflatoxin M1 (AFM1), ZEN, 4nitrophenol, tris(2-carboxyethyl)phosphine hydrochloride (TCEP), vomitoxin (DON), and gold(III) chloride trihydrate (HAuCl4) were purchased from Sigma-Aldrich (USA). Exo III was obtained from Thermo Fisher Scientific (USA). 2.2. Synthesis of Water Resuspended AuNPs. The water resuspended AuNPs were prepared by a citrate reduction procedure according to our previous reports.24,25 The amount of AuNPs was measured using an extinction coefficient of 2.7 × 108 M−1 cm−1 at 520 nm. The appearance and the size of AuNPs were evaluated by transmission electron microscopy (TEM, CM120, Philips, Netherland) and dynamic light scattering (Malvern, UK). The AuNP solution was kept at 4 °C in the dark. 2.3. Preparation of Apt−CS-Modified AuNPs. The Apt and CS were first treated with 10 mM TCEP buffer (10 mM TCEP, 10 mM TrisHCl, 1 mM ethylenediaminetetraacetic acid, 50 mM NaCl, pH 7.4) for 1 h at 23 °C, separately. The treated CS was added into the AuNP solution to obtain a final concentration of 0.1 μM for CS. After 12 h, the treated Apt (0.03 μM final concentration) was added to the above mixture for 12 h at 23 °C. The mixture was kept at 4 °C in the dark. 2.4. Colorimetric Detection of ZEN. The ZEN detection was carried out in a mixture containing 50 μL of ZEN (0−150 μg/L), 10 μL of Apt−CS-modified AuNPs (the AuNP concentration was 4 nM), and 30 μL of phosphate-buffered saline (2 mM, pH 7.4). The mixtures were incubated for 45 min at 23 °C. Afterward, 8 U Exo III was incubated with each mixture for 60 min at 37 °C. Then, the mixtures were treated with 40 μL of 4-nitrophenol (20 mM) and 40 μL of NaBH4 (1.2 M) for 7 min at 23 °C. Next, the absorbance (400 nm) of each mixture was recorded by a Synergy H4 microplate reader (BioTek, USA). 2.5. Aptasensor Selectivity. To determine the specificity of the aptasensor toward ZEN, other toxins such as OTA, AFM1, AFB1, and DON were examined for their interferences with the colorimetric signal. The amount of each toxin was 80 μg/L, and the incubation time was 45 min. 2.6. Determination of ZEN in the Human Serum Sample. First, various concentrations of ZEN (0−120 μg/L) were spiked into human serum samples. Thereafter, the samples (100 μL) were treated with 3 volumes of acetone/water (4:1) for 3 h at −20 °C, followed by centrifugation at 14 500g for 10 min at 4 °C. After that, 90 μL of each supernatant was collected for ZEN detection by the aptasensor.

close proximity and hybridized with each other. With the introduction of Exo III, CS is degraded from its 3′-terminus, whereas Apt remains intact because of its Exo III-resistant 3′ overhanging terminus. The long arm of Apt allows it to walk and bind to another CS, and the procedure continues, leading to unmask most of the AuNP surface, and the size of the modified AuNPs was 16.9 ± 0.8 nm (Figure S1a). Therefore, 4nitrophenol can easily reach the exposed surface of AuNPs and can be reduced to 4-aminophenol by the surface of AuNPs (Figure S2), resulting in the color change of environment from yellow to colorless. Upon the addition of ZEN, Apt interacts with ZEN and is dissociated from its CS because of the stronger binding affinities of aptamers toward their targets.28,29 The resulted Apt/ZEN complex and CS, as single-stranded DNAs on the surface of AuNPs, are resistant to Exo III digestion. In this situation, the size of the modified AuNPs was 19.1 ± 1.2 nm (Figure S1b). Therefore, less amounts of 4-nitrophenol reach the AuNP surface because of the steric hindrance of the Apt/ZEN complex and intact CS on the surface of AuNPs. Therefore, the environment color remains yellow. 3.2. Characterization of AuNPs. Physical characterization of AuNPs by dynamic light scattering showed an average nanoparticle size of 15.2 ± 0.5 nm (Figure S3a). Also, the results of TEM verified that the AuNPs were uniform in shape and size (Figure S3b). 3.3. Optimization of Experimental Conditions. The approach of 4-nitrophenol to the surface of AuNPs is crucial for the high sensitivity of the aptasensor when there is no target in the environment, and it depends on the full function of Exo III for digestion of CS in the dsDNA structure (Apt−CS). To explore the optimum value of Exo III, different amounts of Exo III (0−15 U) were added to the mixture of Apt−CS-modified AuNPs, for 60 min at 37 °C, followed by incubation with 4nitrophenol and NaBH4. According to the experimental principle, the absorbance (400 nm) is reduced gradually with the increase of the concentration of Exo III (in the absence of

3. RESULTS AND DISCUSSION 3.1. ZEN Detection Principle. The detection method of the colorimetric aptasensor relies on the nontarget-induced aptamer walker, catalytic reaction of AuNPs, 4-nitrophenol as a colorimetric probe, and Exo III-aided CS degradation, and signal amplification. Exo III is an enzyme which can specifically digest the 3′-terminus of double-stranded DNAs.26,27 12505

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observed when the ratio of Apt−CS was 3/10. When the ratio of Apt−CS was 1/10, more absorbance was observed because the amount of Apt on the surface of AuNPs was not enough for hybridization with CS and digestion by Exo III, leading to more remained intact CS on the surface of AuNPs. Also, when the ratio of Apt−CS was 5/10, more absorbance was detected because of the high concentration of Apt on the surface of AuNPs which acted as an obstacle for approaching 4-nitrophenol to the AuNP surface. Therefore, the ratio of 3/10 (Apt−CS) was adopted for the next experiments. 3.4. Characterization of Apt−CS-Modified AuNPs and the Function of the Aptasensor. The modification of AuNPs with Apt and CS was investigated by agarose gel electrophoresis (2.5%). As displayed in Figure 2a, the band of CS-modified

target). Results of the experiment (Figure 1a) showed that the optimum level of Exo III was 8 U.

Figure 2. Confirmation of the formation and the function of the developed sensing method. (a) Evaluation of Apt−CS-modified AuNP formation using agarose gel electrophoresis (2.5%). Lane 1: Apt, lane 2: CS, lane 3: CS-modified AuNPs, and lane 4: Apt−CS-modified AuNPs. (b) Absorbance spectra of the presented aptasensor in the absence (blue curve) and presence of ZEN (red curve).

Figure 1. Optimum concentration of Exo III (a), the incubation time of 4-nitrophenol (b), and the ratio of Apt−CS (c) (n = 4).

AuNPs (Figure 2a, lane 3) migrated less than the band of free CS (Figure 2a, lane 2), confirming the immobilization of CS on the AuNP surface via a Au−S bond. Following the addition of Apt to the CS-modified AuNPs, the mobility of the band of Apt was retarded (Figure 2a, lane 4), showing the immobilization of Apt on the surface of AuNPs. Optical measurement was applied to verify the performance of the sensing platform. The results showed that when 4nitrophenol and NaBH4 were mixed with the Apt−CS-modified AuNPs treated with ZEN and Exo III, the color of the environment was yellow (Figure 2b, red curve), confirming the presence of the Apt/ZEN complex and CS on the AuNP surface, lack of walking of Apt on the surface of AuNPs, and so, lack of reduction of 4-nitrophenol by AuNPs. Without the introduction of ZEN, the environment color changes from yellow to colorless (Figure 2b, blue curve), following the addition of 4-nitrophenol and NaBH4 to the Apt−CS-modified AuNPs treated with Exo III,

In this sensor, the colorimetric signal is also based on the reduction of 4-nitrophenol to 4-aminophenol by the AuNP surface. Therefore, it is vital to confirm the optimum time of reduction of 4-nitrophenol in the absence of target in which 4nitrophenol reaches more to the AuNP surface compared to the presence of ZEN. 4-Nitrophenol and NaBH4 were transferred to the mixture containing Exo III-treated Apt−CS-modified AuNPs and incubated for different times (0−12 min). The colorimetric signal was reduced with the reduction of 4-nitrophenol by the AuNP surface. As displayed in Figure 1b, the optimum incubation time of 4-nitrophenol was 7 min. Also, the ratio of Apt−CS captured on the surface of AuNPs could significantly affect the performance of the proposed aptasensor. To find the optimum ratio of Apt−CS, various ratios of Apt−CS were immobilized on the AuNP surface, followed by the introduction of Exo III and 4-nitrophenol (Figure 1c). On the basis of the experimental results, the minimum absorbance was 12506

DOI: 10.1021/acsami.8b02349 ACS Appl. Mater. Interfaces 2018, 10, 12504−12509

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ACS Applied Materials & Interfaces verifying the digestion of CSs on the surface of AuNPs by Exo III because of the formation of the dsDNA structure (Apt−CS) on the surface of AuNPs through walking of the Apt and high access of 4-nitrophenol, as a colorimetric agent, to the AuNP surface. 3.5. Aptasensor Sensitivity. The colorimetric aptasensor was applied for sensitive quantification of ZEN (Figure 3a). As displayed in Figure 3b, there is a linear fitting between the log concentration of ZEN and the relative colorimetric signal, in a dynamic range from 20 to 80 000 ng/L. The limit of detection (LOD) for ZEN was 10 ng/L (S/N = 3).

The sensitivity of the aptasensor for ZEN detection was significantly enhanced compared with that of most of other analytical techniques which are listed in Table S1.1,8,23,30 Also, the designed aptasensor had a wider linear range relative to the most of these approaches. Among these analytical techniques, the electrochemical indirect competitive immunoassay1 showed better LOD and linear range compared to our aptasensor. However, this method needed 3.5 h analysis time and two kinds of antibodies, leading to the increase of the cost of analytical method, whereas the analysis time of our aptasensor was less than 2 h and the sensing agent was aptamer, leading to the decrease of the cost of sensing platform. 3.6. Specificity of the Aptasensor. The selectivity of the sensor is an important criterion for its operational capability. The selectivity of the presented aptasensor was evaluated by incubation of the aptasensor with different toxins, including OTA, AFM1, AFB1, and DON. All of the concentrations of interferents were 80 μg/L. As depicted in Figure 3c, none of these interferents could induce great changes of the relative colorimetric signal, verifying that the aptasensor has high specificity for ZEN detection. 3.7. Real Sample Analysis. To investigate the practical utility of the proposed aptasensor, the aptasensor response in a complex system such as human serum was measured (Figure 4). The sensing platform exhibited a low detection limit of 40 ng/L for ZEN in human serum, which is much lower than LD50 of ZEN in most species. The results verified the practicality of the

Figure 3. (a) Absorbance spectra of the aptasensor in the presence of increasing concentrations of ZEN (0−150 000 ng/L from bottom to top). (b) Calibration curve of the ZEN aptasensor. A0 and A are the absorbance at 400 nm before and after the addition of various concentrations of ZEN, respectively. (c) Relative responses of the aptasensor toward ZEN and other toxins (the concentration of each toxin was 80 μg/L). A0 and A are the absorbance at 400 nm before and after the addition of each toxin, respectively (n = 4).

Figure 4. (a) Absorbance spectra of the aptasensor in the presence of increasing concentrations of ZEN (0−120 000 ng/L from bottom to top) in serum. (b) Calibration curve of the ZEN aptasensor in serum. A0 and A are the absorbance at 400 nm before and after the addition of various concentrations of ZEN, respectively (n = 4). 12507

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colorimetric analytical method for determination of ZEN in serum.

a

added ZEN (μg/L)

found (μg/L)

recovery (%)

RSD (%, n = 4)

1 2 3

2.0 15.0 60.0

1.9 15.2 61.8

95 101.3 103

7.1 6.4 2.6

Data are mean ± relative RSD.

Furthermore, the feasibility of the aptasensor was estimated in the spiked human serum using the recovery assay. The recoveries for ZEN in spiked serum samples were in the range of 95−103% with relative standard deviations (RSDs) equal or less than 7.1% (Table 1), exhibiting that the presented analytical technique could be applied to accurately detect the ZEN concentration in the biological sample.

4. CONCLUSIONS In conclusion, we demonstrated a colorimetric aptasensor for ZEN detection based on the nontarget-induced aptamer walker, Exo III, and AuNPs. The developed aptasensor showed excellent selectivity toward ZEN. The aptasensor significantly improved the ZEN detection sensitivity relative to other sensing platforms with a LOD of 10 ng/L. Such an excellent sensing performance can be attributed to the Exo III-assisted signal amplification and prohibition of the aptamer walker in the presence of ZEN. The application of the aptasensor for the detection of ZEN in the serum sample further proved its reliability. All of these characteristics indicate that the designed aptasensor is a promising analytical technique for the detection of ZEN.

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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.8b02349. Reaction scheme of 4-nitrophenol; size of synthesized AuNPs; TEM image of synthesized AuNPs; and comparison of the present work with other reported ZEN sensing platforms (PDF)

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REFERENCES

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Table 1. Recovery of ZEN from Spiked Human Serum Samples (n = 4)a serum samples

Research Article

AUTHOR INFORMATION

Corresponding Author

*E-mail: [email protected]. Phone: +98 513 1801535. Fax: +98 513 882 3251. ORCID

Seyed Mohammad Taghdisi: 0000-0001-9836-2189 Khalil Abnous: 0000-0001-6314-0164 Author Contributions ¶

These authors contributed equally to the work.

Notes

The authors declare no competing financial interest.

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ACKNOWLEDGMENTS Financial support of this study was provided by Mashhad University of Medical Sciences. 12508

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DOI: 10.1021/acsami.8b02349 ACS Appl. Mater. Interfaces 2018, 10, 12504−12509