An Integrated Redox Cycling for Electrochemical Enzymatic Signal

Nov 22, 2017 - Highly sensitive analytical methods for the detection of proteins are still an urgent demand in early medical diagnosis and the discove...
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Article Cite This: Anal. Chem. 2017, 89, 13480−13486

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An Integrated Redox Cycling for Electrochemical Enzymatic Signal Enhancement Md. Rajibul Akanda† and Huangxian Ju* State Key Laboratory of Analytical Chemistry for Life Science, School of Chemistry and Chemical Engineering, Nanjing University, Nanjing 210023, P. R. China S Supporting Information *

ABSTRACT: Highly sensitive analytical methods for the detection of proteins are still an urgent demand in early medical diagnosis and the discovery of biomarkers with ultralow abundance. Here an integrated electrochemical− chemical−enzymatic redox cycling is designed for significant enhancement of electrochemical enzymatic signal in biorecognition. This strategy efficiently utilizes the high specificity of the outersphere to innersphere redox reaction to mediate the enzymatic redox cycling with the nonenzymatic redox cycling. The oxygenation activity of tyrosinase as a label of the biorecognition event ensures low background and generates outersphere-reaction-philic/innersphere-reactionphilic redox couples, which leads to 13 300× amplification of electrochemical signal. The mediation of nonenzymatic redox cycling in the integrated system produces a 14-fold improved ratio of signal to background. The practicality of the proposed approach with clinical samples demonstrates its potential in clinical diagnostic and therapeutic monitoring. This work opens a new avenue to design novel signal amplification strategies for ultrasensitive bioanalysis.

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ples,25 a signal enhancement concept has also been presented for ECC redox cycling.23 Obviously, the participation of the nonenzymatic redox system in enzymatic redox strategies and the specificity of the OSR-philic/ISR-philic controlled redox system can efficiently amplify enzymatic signal and improve the biosensing performance of enzymatic assays. Thus, the integration of a highly ISR-philic redox enzyme, a highly OSR-philic mediator, and an OSR-philic/ISR-philic enzyme product on an OSR-philic electrode as a redox enzyme triggered electrochemical enzymatic redox scheme can achieve an outersphere to innersphere redox reaction to significantly enhance enzymatic signal. The highly ISR-philic redox enzyme ensures slow electron transfer on the OSR-philic electrode, which leads to low background. The OSR-philic/ISR-philic enzyme product brings about both the outersphere reaction with a highly OSR-philic mediator and the innersphere reaction with a highly ISR-philic redox enzyme, and the highly OSRphilic mediator ensures fast electron transfer between the OSRphilic electrode and enzyme redox couple, which leads to a high electrochemical response. The oxygenation of tyrosinase (Tyr), a representative enzymatic reaction, shows low background when using lowly electroactive phenol as the substrate to generate highly electroactive catechol for Tyr responsive nonenzymatic EC redox cycling.22,26 The formed catechol and the enzymatic

mplified measurement technology for proteins or genes is highly challenging in both bioelectronics1 and early medical diagnosis.2 Although the electron transfer properties of enzymes have shown great promise in amplified biosensors, bioreactors, and biomedical devices,3,4 insufficient enzymatic readout in the electrochemical measurements of a biological recognition event in conventional direct sandwich ELISA limits the compatibility and broad utility of this technology. Thus, some strategies have been designed to improve the sensing performances of redox enzyme labeled assays by incorporating multiple enzymes5 or nanocatalysts6 in a single recognition event and increasing enzyme concentration on the nanocatalyst.7,8 The wiring of an active center of redox enzymes has also been achieved to enhance the enzymatic readout by using nanomaterials such as gold nanoparticles,9 carbon nanotube,10,11 graphene,12 and quantum dots,13 hybrid organic− inorganic film,14 room temperature ionic liquid,15 and electron mediators such as pyrroloquinolinoquinone,16 1,2-naphthoquinone-4-sulfonate,17 and Fe(CN)62+/3+18 to increase electron hopping distance.19 However, the sensitivity improvement of these methods is still insatiable in bioanalysis of biomarkers with ultralow abundance. Recently, some redox cycling strategies have been designed in an electrochemical system for acquiring additional signal amplification.20 Among these strategies, the coupling of nonenzymatic redox cycling, such as electrochemical−chemical (EC)21,22 and electrochemical−chemical−chemical (ECC) cycling,23,24 with immunosensors shows improved biosensing performance. By introducing the outersphere-reaction-philic/ innersphere-reaction-philic (OSR-philic/ISR-philic) redox cou© 2017 American Chemical Society

Received: September 17, 2017 Accepted: November 22, 2017 Published: November 22, 2017 13480

DOI: 10.1021/acs.analchem.7b03802 Anal. Chem. 2017, 89, 13480−13486

Article

Analytical Chemistry

Figure 1. Schematic illustration of (A) the integration of EC and CN redox cycling containing mediator RI and its oxidized form OI, oxidant Q and its reduced form P, and oxidant of enzyme OII and its reduced form RII; and B) example of the integrated ECN redox cycling for electrochemical enzymatic signal enhancement in the immunosensing of protein.

reaction product o-benzoquinone can act as an OSR-philic/ ISR-philic redox couple (Q/P) to specifically combine with a highly OSR-philic redox mediator (RI), which leads to a RI mediated chemical−enzymatic (CN) redox cycling (Figure 1A). As a proof of concept, an integrated redox cycling, called electrochemical−chemical−enzymatic (ECN) redox cycling, was designed by combining the oxygenation of Tyr with a classical highly OSR-philic ferrocene redox couple (FcA+/ FcA)27 (Figure 1B). Compared to the previous ECC redox cycling,23 the integrated system achieved 1000-fold amplification of the electrochemical signal in a single biorecognition event on an OSR-philic glassy carbon electrode (GCE) due to the presence of two enzymatic reactions. Moreover, the low electroactivity of phenol on GCE and the negligible reaction between phenol and FcA maintains a negligible background. This work opened a new avenue to design amplified biosensing strategies for analysis of biomolecules with ultralow abundance.

(Beijing, China). Sulfosuccinimidyl-4-[N-maleimidomethyl] cyclohexane-1-carboxylate (sulfo-SMCC) and N-succinimidylS-acetylthiopropionate (SATP) were obtained from Thermo Scientific Inc. (U.S.A.). Ethylenediaminetetraacetic acid (EDTA), phosphate buffer saline (PBS, pH 7.4, 10 mM), and phosphate buffer saline containing bovine serum albumin (PBSB, pH 7.4, 10 mM) were obtained from Sigma-Aldrich Co. (U.S.A.). Washing buffer contained PBS and 0.05% tween-20, and blocking buffer contained PBS and 5% BSA. All other reagents were of analytical grade. All aqueous solutions were prepared using ultrapure water (≥18 MΩ, Milli-Q, Millipore). Apparatus. Electrochemical measurements were carried out using CHI 660B (CH Instruments, Inc., Austin, TX, U.S.A.). All electrochemical experiments were carried out in a cell containing 10 mL of 10 mM PBS (pH 5.5) and using a platinum wire as the auxiliary, an Ag/AgCl (3 M NaCl) electrode as the reference, and GCE as the working electrode. The GCE (3 mm in diameter) was polished to a mirror-like finish with 0.3 and 0.05 mm alumina slurry (Beuhler) followed by rinsing thoroughly with ultrapure water. The electrode was successively sonicated in 1:1 nitric acid, acetone, and ultrapure water, and then allowed to dry at room temperature. The UV− vis absorption spectra were carried out with a UV-3600 spectrophotometer (UV−vis−NIR spectrophotometer, Shimadzu, Japan). Preparation of Tyr-anti-CEA. Tyr-conjugated anti-CEA (Tyr-anti-CEA) was prepared by cross-linking between the −NH2 group of detection anti-CEA and the −NH2 group of Tyr. After 1 mL of 100 μg/mL Tyr in pH 7.4 PBS and 50 μL of 1 mg/mL sulfosuccinimidyl-4-[N-maleimidomethyl] cyclohexane-1-carboxylate (sulfo-SMCC) in pH 7.4 PBS were mixed to incubate for 30 min at room temperature, the sulfo-SMCC conjugated Tyr was filtered through a 50 K centrifuge filter, purchased from Merck Millipore Ltd. (Tullagreen, Ireland), at

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EXPERIMENTAL SECTION Materials and Reagents. Catechol, phenol, glutaraldehyde, and tyrosinase (Tyr, ≥1000 unit/mg) from mushrooms were purchased from Sigma-Aldrich Co. (U.S.A.). Chitosan was obtained from KAYON (Shanghai, China). Nitric acid, acetone, hydroxylamine·HCl, and ethylenediaminetetraacetic acid (EDTA) (CAS 6381−92−8) were purchased from Nanjing Chemical Reagent Co. Ltd. (Nanjing, China). Acetic acid was purchased from Sinopharm Chemical Reagent Co. Ltd. (Nanjing, China). Bovine serum albumin (BSA) was obtained from KeyGEN Biotech. O. Ltd. (Nanjing, China). Ferrocenemonocarboxylic acid (FcA, CAS 1271−42−7) was purchased from TCI (Shanghai, China). Carcinoembryonic antigen (CEA, calibrator grade), capture antibody of CEA (capture anti-CEA, clone: D3C), and detection antibody of CEA (detection antiCEA, clone: M5B) were purchased from Keybiotech Co. Ltd. 13481

DOI: 10.1021/acs.analchem.7b03802 Anal. Chem. 2017, 89, 13480−13486

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Analytical Chemistry

Figure 2. (A,B) Cyclic voltammograms of 10 mM PBS (pH 5.5) containing marked species at GCE at 20 mV/s and (C,D) chronocoulograms of 10 mM PBS (pH 5.5) containing marked species at GCE at +0.08 V. The concentrations for FcA, catechol, and Tyr are 1.0 mM, 0.5 mM, and 50 μg/ mL, respectively.

10 000 rpm for 30 min, and then dissolved in 1 mL of PBS. Meanwhile, 1 mL of 100 μg/mL detection anti-CEA in PBS and 10 μL of 2 mg/mL N-succinimidyl-S-acetylthiopropionate (SATP) in PBS were mixed to incubate for 30 min at room temperature. Afterward, 20 μL of PBS (pH 7.4) containing 0.012 g/mL ethylenediaminetetraacetic acid and 0.044 g/mL hydroxylamine·HCl was added in the mixture to incubate for 2 h at room temperature, which was then filtered through a 50 K centrifuge filter at 10 000 rpm for 30 min to obtain SATP conjugated anti-CEA, which was dissolved in 1 mL of PBS. Finally, the sulfo-SMCC conjugated Tyr solution and the SATP conjugated anti-CEA solution were mixed at a molar ratio of 1:1 for 2 h at room temperature. The unconjugated ingredients were removed by centrifugation through a 50 K centrifuge filter at 10 000 rpm for 30 min, and the obtained Tyr-anti-CEA was dissolved in 1 mL of PBSB and diluted to 50 μg/mL. Functionalization of Chitosan Matrix on GCE. After GCE was subsequently polished with 3.0 and 0.05 mm alumina slurries, followed by ultrasonication in ethanol and deionized water (1:1 v/v) for 5 min, and drying using N2 gas, 7 μL of 0.25 mg/mL chitosan (CS) solution in 0.1 M acetic acid was drop cast onto its surface and dried at room temperature for 1 h, and the obtained CS/GCE was dipped in 0.25% glutaraldehyde (GA) (in 10 mM pH 7.4 PBS) for 2 h to activate the chitosan film (GA-CS/GCE) for further functionalization. The GA-CS/ GCE was washed with ultrapure water repeatedly to remove unreacted GA. After the GA-CS/GCE was incubated in 20 μL of capture anti-CEA (50 μg/mL) for 3 h at 4 °C in a moisture-saturated environment, the anti-CEA terminated surface (anti-CEA-CS/ GCE) was washed with washing buffer to remove unbound captured anti-CEA. The immunosensor was then obtained by dropping 20 μL of blocking buffer on anti-CEA-CS/GCE and by incubating for 60 min at 4 °C in a moisture-saturated

environment, which was used to block the remaining active sites from nonspecific adsorption. Electrochemical Immunoassay. The immunosensing procedure was performed by incubating 20 μL of target CEA at different concentrations on the immunosensors for 30 min at 4 °C, rinsing the immunosensors with washing buffer, dropping 20 μL of Tyr-anti-CEA (50 μg/mL) to incubate at 4 °C for 30 min, rinsing the surface with washing buffer, and dipping the immunosensors in detection solution containing 1.0 mM FcA and 5.0 mM phenol to measure the electrochemical responses at room temperature (25 °C) with electrochemical workstation CHI 660B (CH Instruments, Inc., Austin, TX, U.S.A.).

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RESULTS AND DISCUSSION Construction of ECN Redox Cycling. The integrated ECN redox cycling depends on the OSR-philic electrode surface, the highly OSR-philic redox couple FcA+/FcA, the highly ISR-philic oxidase, and the OSR-philic/ISR-philic redox couple. Thus, the related natures and feasibility were first evaluated. At the bare GCE, FcA in PBS showed a reversible cyclic voltammogram (CV) (Figure 2A), indicating a fast outersphere reaction of the highly OSR-philic FcA. The mixture of FcA and Tyr showed the same CV response as that of FcA (Figure 2B). Thus, the reaction between FcA and Tyr could be excluded, though they possess different redox potentials, which verified the ISR-philic nature of Tyr. Both the fast response of FcA and the negligible CV signal of Tyr demonstrated the OSR-philic electrode surface. At the GCE, the highly electroactive catechol showed slow electron transfer (blue curve, Figure 2A), indicating the ISRphilic nature of catechol. Thus, it could be oxidized by the ISRphilic Tyr to trigger a fast enzymatic reduction of highly ISRphilic O2, which led to the formation of o-benzoquinone and was demonstrated by the characteristic adsorption peak at 385 nm (Figure S1A). The o-benzoquinone produced from both 13482

DOI: 10.1021/acs.analchem.7b03802 Anal. Chem. 2017, 89, 13480−13486

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Analytical Chemistry electro-oxidation and enzymatic reaction showed a reduction peak around +0.13 V (blue and green curves, Figure 2A). The o-benzoquinone also significantly increased the redox peaks of highly OSR-philic FcA through an electro-reduction-based EC redox cycling at pH 5.5 (red curve, Figure 2A), indicating the OSR-philic nature of o-benzoquinone. The OSR/ISR natures of the o-benzoquinone/catechol redox couple efficiently linked the chemical and enzymatic reactions for the construction of CN redox cycling. In this cycling, the enzymatic product obenzoquinone could oxidize OSR-philic FcA to generate FcA+ (Figure 1A). Thus, the characteristic adsorption peak of FcA+ occurred at 622 nm (Figure S1B). The generation of FcA+ through CN redox cycling was further confirmed electrochemically by the decreased oxidation response of FcA and increased reduction peak of FcA+ (green curve, Figure 2A) as well as the reduction current in the chronoamperogram (Figure S2), which underwent an electro-reduction-based ECN redox cycling for significant signal amplification (Figure 2C,D). Feasibility Confirmation of ECN Redox Cycling. The feasibility of electro-reduction-based ECN redox cycling is also decided by the formal potentials (E0′) of these redox couples. In this integrated system, the E0′ of O2/H2O at pH 5.5 was +0.682 V (vs Ag/AgCl). The fast enzymatic oxidation of catechol by O2 (Figure S1A) indicated that the E0′ of Tyr2+/ Tyr+ should be between the E0′ values of the O2/H2O and obenzoquinone/catechol redox couples, though it did not show the CV response in the potential window due to the high overpotential of the enzyme at the solid electrode and its highly ISR-philic nature (Figure 2B). The E0′ of the o-benzoquinone/ catechol redox couple at pH 5.5 was measured to be +0.254 V, while the E0′ of FcA+/FcA was calculated from the CV peak potentials to be +0.289 V (blue and pink curves, Figure 2A). Although the E0′ value of o-benzoquinone/catechol was more negative than that of FcA+/FcA, the complete oxidation of catechol by dissolved O2 in the presence of Tyr led to a much higher surface concentration of o-benzoquinone than catechol. Thus, the practical electrode potential of the o-benzoquinone/ catechol couple was more positive than that of the FcA+/FcA couple in the presence of excessive FcA, which resulted in the feasibility of the oxidation of FcA by enzymatic product obenzoquinone. The whole ECN redox cycling at GCE could be expressed in Figure 3A. The difference of the OSR-philic/ISRphilic natures suppressed some theoretically possible reactions (Figure 3B), which led to low background in the conventional direct sandwich ELISA platform. In the ECN redox cycling, the signal enhancement depended on the specific reactions among the redox couples, following the outersphere to innersphere reaction mechanism. The fast innersphere reaction of CN redox cycling was achieved at the optimized Tyr concentration of 50 μg/mL (Figure S3). Compared to the oxidation signal of catechol at +0.08 V, the addition of Tyr led to a 426-fold amplified signal due to the presence of EN redox cycling (blue curves in Figure 2C,D, and Table 1). Also, after FcA was added into the PBS containing catechol and Tyr, the electrochemical signal from the proposed ECN system increased by 1175-fold (red curve, Figure 2D). In the absence of Tyr, both the EN and ECN redox cycling could not be achieved, and the electrochemical signal of catechol showed only a 3× increase upon the addition of FcA (red curve, Figure 2C). Thus, Tyr played a key role in the designed ECN redox cycling system, which led to extensive application of the electrochemical enzymatic signal enhancement system in Tyr-related biosensing.

Figure 3. (A) Relative formal potentials (vs Ag/AgCl) of redox couples in the integrated system. (B) Suppressed reactions due to the different OSR-philic/ISR-philic natures: (i) electro-oxidation of phenol and (ii) oxygen reduction at GCE at +0.08 V, (iii) chemical reaction of phenol with FcA, and (iv) enzymatic oxidation of FcA by O 2.

Table 1. Charges at 100 s from Figure 2C,D components PBS PBS + catechol PBS + FcA PBS + FcA + catechol PBS + Tyr PBS + Tyr + catechol PBS + FcA + Tyr PBS + FcA + Tyr + catechol

charge (μC) 0.125 0.391 0.232 1.013

change upon addition of catechol (μC)

amplification factor

0.266 0.781

3

0.287 113.6

113.3

426

0.316 313.0

312.7

1175

Optimization of Applied Potential for ECN Redox Cycling. To achieve the highest sensitivity of the ECN redoxcycling-related biosensing strategies, using the appropriate applied potential was important for obtaining the maximum ratio of electrochemical signal to background (S/B). In the biosensing system, FcA and phenol were generally added in detection solution, and Tyr was used as a label to produce the biorecognition-related detection signal. Thus, the response of FcA and phenol mixed in the detection solution could be considered as the electrochemical background. With the increasing applied potential around a feasible range for electro-reduction of FcA+, the chronocoulometric response of the mixture increased, while the response of PBS containing FcA, phenol, and Tyr slightly increased and then decreased (Figure S4). At the applied potential of +0.08 V, this biosensing system showed a maximum S/B ratio of 755. Thus following experiments for chronocoulometric measurements were performed at +0.08 V. Suitability of Phenol as Substrate for ECN Redox Cycling. When using phenol as the enzyme substrate, the electro-reduction-based ECN redox cycling showed greater superiority than the electro-reduction-based EN redox cycling, though phenol could keep a very low background (compared to catechol) for both EN and ECN redox cycling at +0.08 V 13483

DOI: 10.1021/acs.analchem.7b03802 Anal. Chem. 2017, 89, 13480−13486

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Figure 4. (A) Cyclic voltammograms of the marked solutions in 10 mM PBS (pH 5.5) at 20 mV/s, (B) chronocoulograms of the marked solutions in 10 mM PBS (pH 5.5) at +0.08 V, and (C) charge responses of phenol + FcA as ECN redox cycling and phenol as EN redox cycling in presence (as signal, cyan column) and absence (as background, black column) of Tyr and schematic representation of ECN and EN redox cycling. Inset in B: a magnification of the curves for phenol and mixture of FcA and phenol. The concentrations of phenol, FcA and Tyr are 5.0 mM, 1.0 mM and 50 μg/mL, respectively.

Figure 5. (A) Chronocoulograms of immunosensors in 10 mM PBS (pH 5.5) containing 1.0 mM FcA and 5.0 mM phenol at +0.08 V after incubation with CEA at marked concentrations for 30 min and then Tyr-anti-CEA for 30 min at 4 °C. (B) Plot of the response at 100 s vs logarithm of CEA concentration. The inset represents a magnification of the plot at low concentrations of CEA.

(Figure 4A,B). In the presence of Tyr in phenol solution, catechol was first generated via the oxygenation of Tyr to undergo the EN and ECN redox cycling (Figure 4C), which led to the amplification factors of 516 and 13 300 for the signals at 100 s, respectively (Table S1). The further enzymatic oxidation of catechol produced an obvious reduction peak of obenzoquinone (blue and violet curves, Figure 4A), as observed in PBS containing catechol with or without FcA and Tyr (Figure 2A). Compared to EN redox cycling, the much greater signal amplification of ECN redox cycling led to a higher sensitivity and S/B ratio for electrochemical biosensing of the enzymatic signal enhancement system. The S/B ratio of 755 for the ECN redox cycling was 14-fold greater than the ratio of 54 for EN redox cycling (Figure 4B,C) due to the mediation of nonenzymatic redox cycling in the integrated system. Evaluation of Immunosensing Performance. As an application example of the designed integrated redox cycling

with the exciting signal enhancement and sensitivity improvement, carcinoembryonic antigen (CEA), a colorectal cancer biomarker,28,29 was used as a model analyte of Tyr-related biosensing. The immunosensor for CEA was prepared by covalently immobilizing capture antibody anti-CEA on chitosan (CS) modified GCE30−32 and blocking the active sites with blocking buffer containing 5% bovine serum albumin (BSA) to exclude the nonspecific binding.22 Considering the good immunosensing performance for the redox-cycling-based assay,23 chronocoulometry was used to collect the detection signal, which showed negligible nonspecific binding (Figure S5). The background signals from seven immunosensors in PBS containing FcA and phenol showed a relative standard deviation (RSD) of 4.9% (Figure S6), indicating a good preparation reproducibility. With the increasing CEA concentration, the chronocoulometric curve of the immunosensor after incubation with CEA and then Tyr-anti-CEA showed an 13484

DOI: 10.1021/acs.analchem.7b03802 Anal. Chem. 2017, 89, 13480−13486

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Analytical Chemistry increasing response at +0.08 V (Figure 5A). The plot of the charge response at 100 s vs the logarithm of CEA concentration from 1.0 pg/mL to 50 μg/mL showed a good linearity with an ultralow limit of detection (1.0 fg/mL) at 3SD (Figure 5B), indicating the excellent performance of the proposed integrated strategy. Practicality of the Integrated Strategy in Clinical Diagnosis. To demonstrate the practicality of the developed protocol, five clinical real samples with various concentrations of CEA were tested. Each test was conducted three times with three different immunosensors and the calibration plot in Figure 5B. During the test of clinical real samples containing various concentrations of CEA, the immunosensors experienced several washing steps before being finally dipped to the detection solution. From the electrochemical point of view, the interfering chemicals in the real sample could not affect the ECN redox system due to having a different E0′ from that of catechol. Thus, both the reproducibility of the proposed immunoassay and acceptable relative errors compared to commercial technique (Table S2) indicated its superior suitability in clinical diagnosis.

Huangxian Ju: 0000-0002-6741-5302 Present Address †

M.R.A.: Department of Chemistry, Jagannath University, Dhaka 1100, Bangladesh

Notes

The authors declare no competing financial interest.

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ACKNOWLEDGMENTS This work was financially supported by the National Natural Science Foundation of China (21635005, 21361162002).

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CONCLUSION This work introduces an integrated ECN redox cycling for significantly enhancing the electrochemical enzymatic signal. The high specificity of the outersphere to innersphere redox reaction and the mediation of the enzymatic redox cycling by nonenzymatic redox cycling led to a signal amplification factor of 3 orders of magnitude. When using phenol as the substrate of Tyr to produce catechol, a key species to form the OSRphilic/ISR-philic redox couple in the cycling, the amplification factor reaches 4 orders of magnitude, and the S/B ratio is increased by 755 times. Using the Tyr-labeled antibody to perform the biomolecular recognition through conventional direct sandwich ELISA, the designed strategy shows ultrahigh sensitivity for protein detection with an fg/mL-leveled limit of detection. The practicability of the developed approach in a biomarker assay has also been demonstrated. The electrochemical enzymatic signal enhancement system possesses extensive applications in Tyr-related biosensing and opens a new avenue to design amplified biosensing strategies for analysis of biomolecules with ultralow abundance.

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ASSOCIATED CONTENT

S Supporting Information *

The Supporting Information is available free of charge on the ACS Publications website at DOI: 10.1021/acs.analchem.7b03802. Formal potential evaluation of O2/H2O and Tyr2+/ Tyr+redox couples, spectroscopic and chronoamperometric evaluation of redox cycling, optimization of Tyr concentration, electrochemical S/B ratio, nonspecific binding and reproducibility of immunosensor preparation, amplification factor, and comparison of detection results (PDF)

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AUTHOR INFORMATION

Corresponding Author

*Phone/Fax: +86-25-89683593; E-mail: [email protected] (H.X.J.) ORCID

Md. Rajibul Akanda: 0000-0002-9529-0578 13485

DOI: 10.1021/acs.analchem.7b03802 Anal. Chem. 2017, 89, 13480−13486

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DOI: 10.1021/acs.analchem.7b03802 Anal. Chem. 2017, 89, 13480−13486