Ru(NH3)62+-Mediated Redox Cycling: Toward

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Ru(NH3)63+/Ru(NH3)62+-Mediated Redox Cycling: Toward Enhanced Triple Signal Amplification for Photoelectrochemical Immunoassay Bing Wang, Yi-Tong Xu, Jing-Lu lv, Tie-Ying Xue, ShuWei Ren, Juntao Cao, Yan Ming Liu, and Wei-Wei Zhao Anal. Chem., Just Accepted Manuscript • DOI: 10.1021/acs.analchem.8b05129 • Publication Date (Web): 21 Feb 2019 Downloaded from http://pubs.acs.org on February 24, 2019

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Analytical Chemistry

Ru(NH3)63+/Ru(NH3)62+-Mediated Redox Cycling: Toward Enhanced Triple Signal Amplification for Photoelectrochemical Immunoassay Bing Wang,1,2,4 Yi-Tong Xu,1,4 Jing-Lu lv,2 Tie-Ying Xue,1 Shu-Wei Ren,3 Jun-Tao Cao,2, Yan-Ming Liu,2 and Wei-Wei Zhao1, 1State

Key Laboratory of Analytical Chemistry for Life Science, School of Chemistry and

Chemical Engineering, Nanjing University, Nanjing 210023, China 2College

of Chemistry and Chemical Engineering, Xinyang Normal University, Xinyang 464000,

China 3Xinyang 4These

Central Hospital, Xinyang 464000, China

authors contributed equally to this work.

* To whom correspondence should be addressed. * E-mail: [email protected] * E-mail: [email protected]

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ABSTRACT: Herein we report an effective Ru(NH3)63+/Ru(NH3)62+-mediated photoelectrochemical-chemical-chemical (PECCC) redox cycling amplification (RCA) strategy toward enhanced triple signal amplification for advanced split-type PEC immunoassay application. Specifically, alkaline phosphatase (ALP) label was confined via a sandwich immunorecognition to convert 4-aminophenyl phosphate to the signal reporter 4-aminophenol (AP), which was then directed to interact with Ru(NH3)62+ as redox mediator and tris (2-carboxyethyl) phosphine (TCEP) as reducing agent in the detection buffer. Upon illumination, the system was then operated upon the oxidation of Ru(NH3)62+ by the photogenerated holes on the Bi2S3/BiVO4 photoelectrode, starting the chain reaction in which the Ru(NH3)62+ was regenerated by Ru(NH3)63+-enabled oxidization of AP to p-quinoneimine, which was simultaneously recovered by TCEP. Exemplified by interleukin-6 (IL-6) as the analyte, the Ru(NH3)63+/Ru(NH3)62+-mediated, AP-involved PECCC RCA coupled with ALP enzymatic amplification could achieve triple signal amplification toward the ultrasensitive PEC IL-6 immunoassay. This protocol can be extended as a general basis for numerous other targets of interest. Besides, we believe this work could offer a new perspective for the further exploration of advanced RCA-based PEC bioanalysis. KEYWORDS: Photoelectrochemical bioanalysis; Triple signal amplification; Redox cycling; Bi2S3/BiVO4; Interleukin-6

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Signal amplification is essential for sensitive photoelectrochemical (PEC) bioanalysis.1-20 This work herein reports Ru(NH3)63+/Ru(NH3)62+-mediated redox cycling toward enhanced triple signal amplification for PEC immunoassay. Previously, we have presented the concept of PEC-chemical-chemical (PECCC) redox cycling amplification (RCA) as effective strategy for sensitive PEC bioanalysis, in which the redox reaction of the ascorbic acid (AA) as signaling species occurred repeatedly upon the coexistence of ferrocenecarboxylic acid as redox mediator and tris (2-carboxyethyl) phosphine (TCEP) as reducing agent at the photoelectrode.21 This proof-of-concept study disclosed the great potential of PECCC RCA in improving the performance of PEC bioanalysis. It is therefore desirable to seek more advanced PECCC RCA strategy with higher efficacy for future PEC bioanalysis development. However, except the aforementioned protocol, no exploration of PECCC RCA in the field has been performed. Achieving innovative PECCC RCA for PEC bioanalysis remains a challenge. Scheme 1. Illustration of the Proposed PECCC RCA-based PEC Immunoassay

On the basis of the a Bi2S3/BiVO4 photoelectrode, this work hereby introduces a Ru(NH3)63+/Ru(NH3)62+-mediated, 4-aminophenol (AP)-involved PECCC RCA strategy and its application to enhanced triple signal amplification for PEC immunoassay (see Supporting Information for detailed Experimental Section). As shown in Scheme 1, the signal reporter AP was initially generated from the 4-aminophenyl

phosphate

(APP)

by

alkaline

3


phosphatase

(ALP)

label


(anti-IL-6-SiO2-ALP) in 96-well plate and then steered to interact with Ru(NH3)62+ and TCEP in the detection buffer. Upon illumination, the detection system was then operated upon the oxidation of Ru(NH3)62+ by the photogenerated holes on the Bi2S3/BiVO4 photoelectrode, starting the chain reaction in which the Ru(NH3)62+ was regenerated by Ru(NH3)63+-enabled oxidization of AP to p-quinoneimine (QI), which was simultaneously recovered by TCEP. Exemplified by interleukin-6 (IL-6) as the target, the design, consisting of Ru(NH3)63+/Ru(NH3)62+-mediated, 4-aminophenol (AP)-involved PECCC RCA and ALP enzymatic amplification, achieved the triple signal amplification toward the ultrasensitive PEC IL-6 immunoassay. This work features an innovative Ru(NH3)63+/Ru(NH3)62+-mediated PECCC RCA strategy in PEC bioanalysis and is expected to attract more interest in the exploration of advanced RCA-based PEC bioanalysis. RESULTS AND DISCUSSION

Figure 1. SEM images of (a) BiVO4, (b) Bi2S3, and (c) Bi2S3/BiVO4; (d) TEM image of Bi2S3/BiVO4; (e) XRD results of the samples; (f) PEC tests of BiVO4/ITO (black curve), Bi2S3/ITO (red curve), and Bi2S3/BiVO4/ITO (blue curve) in 0.1 M PBS containing 0.1 M AA. In PEC measurements, the stimulus light was switched on and off every 10 s.

The structural and elemental information of the photoelectrode materials were first studied with scanning electron microscopy (SEM), transmission electron microscope (TEM), X-ray powder diffraction (XRD), Raman spectra, X-ray photoelectron spectroscopy (XPS), and UV-vis diffuse reflectance spectra (DRS). As shown in Figure 1a and 1b, the BiVO4 consisted of irregular particles with sizes over 450 nm, 4


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while the Bi2S3 was composed of nanorod (NR) structure with length and width of about 35-150 nm and about 12-42 nm, respectively. In Figure 1c, the SEM image of Bi2S3/BiVO4 heterojunction displays the deposition of Bi2S3 NRs on the BiVO4 surface, which is confirmed by the corresponding TEM image in Figure 1d. Figure S1 of high-resolution TEM image shows the close contact between the two components, with the spacing values measured to be 0.31 and 0.38 nm that assigned to the 121 lattice plane of BiVO4 and the 101 lattice plane of Bi2S3, respectively.22,23 The element mapping analysis in Figure S2 further evidences the existence of Bi, V and S elements in the heterojunction. Figure 1e of the XRD results exhibits the diffraction patterns of BiVO4 and Bi2S3 were of monoclinic BiVO4 (JCPDS No.14-0688)24 and orthorhombic Bi2S3 (JCPDS No. 17-0320),25,26 respectively, and the pattern of Bi2S3/BiVO4 heterojunction presents the same obvious characteristic peaks of both BiVO4 and Bi2S3. Figure S3 displays the Raman spectra of the samples. The peaks at 820, 367, 324, and 210 cm-1 corresponded to the typical vibrations of monoclinic BiVO4.27 The peak around 820 cm-1 was interpreted as the typical symmetric and antisymmetric stretching modes of V-O bonds,28 while those around 367 and 324 cm-1 were due to the typical symmetric and antisymmetric bending modes of the vanadate anion.29 The Raman spectrum of Bi2S3 presents the bands at 142, 183, 236, and 256 cm-1, matching well with the reported literature.30 These results suggested the successful formation of the Bi2S3/BiVO4 heterojunction. Incidentally, the XPS and UV-vis DRS characterization were presented with Figure S4 and S5, respectively. The PEC responses of the BiVO4/indium tin oxide (ITO), Bi2S3/ITO and Bi2S3/BiVO4/ITO electrodes were then tested with the results shown in Figure 1f. The response of BiVO4/ITO was negligible (curve a),31-33 while that of Bi2S3/ITO was obvious (curve b). In comparison, the Bi2S3/BiVO4/ITO exhibited a fairly high response (curve c), demonstrating the superiority of the as fabricated heterojunction photoelectrode. Besides, the optimum conditions for the heterojunction and the optimum concentration of Ru(NH3)62+ and TCEP for the PECCC redox cycling were also investigated with the results shown in Figure S6. To proof the feasibility of proposed system, as shown in Figure 2a, the cyclic 5



voltammogram (CV) behaviors of the bare ITO electrode in different tris buffer solutions were studied. The oxidation peak of Ru(NH3)62+ appeared at approximately 0.09 V (curve a), whereas the oxidation peak of AP could not be observed (curve b), indicating the easier oxidation of Ru(NH3)62+ than AP. For the Ru(NH3)62+/AP system, the broad oxidation peak with higher current intensity revealed that Ru(NH3)62+ could be regenerated from its oxidative product Ru(NH3)63+ by a small portion of AP, while the enhanced reduction peak may be due to the reduction of the generated QI from AP along with the reduction of Ru(NH3)63+ (curve c).34 Such a phenomenon was also observed in a recent ferrocene-phenol electrochemical cycling system.35 By comparing the CV results of the Ru(NH3)62+/TCEP and the Ru(NH3)62+/AP/TCEP (curves d and e), the existence of AP led to the higher current, and the oxidation peaks occurred at the lower potential of ~ 0.01 V. The reaction process of Ru(NH3)62+/AP/TCEP system on the ITO electrode were further studied with CV at different scan rates, as shown in Figure S7-9 and Table S1-2, the results indicated that the electrode reaction was quasi-reversible. All these results strongly revealed that Ru(NH3)62+ could be rapidly regenerated by the double-cycle redox cycling, and the reaction between Ru(NH3)63+ and AP was accelerated by the reaction between QI and TCEP. To investigate the photocurrent behaviors of these solutions on the Bi2S3/BiVO4 photoelectrode, PEC tests were then performed as shown in Figure 2b. It could be seen that the photoelectrode exhibited obvious PEC response in both Ru(NH3)62+ (curve a) and AP (curve b) solutions, indicating the two materials could be oxidized by the photogenerated holes on the electrode. Since Ru(NH3)62+ could be regenerated from the reduction of Ru(NH3)63+ by AP, the photocurrent of Ru(NH3)62+/AP system was higher than that of Ru(NH3)62+ or AP (curve c). Comparatively, Ru(NH3)62+/TCEP exhibited a relatively weaker response (curve d). Remarkably, the Ru(NH3)62+/AP/TCEP system exhibited much high signal among all systems (curve e). These results demonstrated that the Ru(NH3)63+/Ru(NH3)62+-mediated, AP-involved PECCC redox cycling could achieve the as-expected signal amplification. 6


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Figure 2. (a) CV at bare ITO electrode (at a scan rate of 0.20 V/s), and (b) PEC signals measured on Bi2S3/BiVO4/ITO electrode in different tris buffer solutions (pH 8.9) after argon treatment. Curves (a-e) are Ru(NH3)62+, AP, Ru(NH3)62+/AP, Ru(NH3)62+/TCEP, and Ru(NH3)62+/AP/TCEP, respectively. The concentrations of Ru(NH3)62+, AP, and TCEP used in the experiment are 1.0, 1.0, and 2.0 mM, respectively. In the PEC measurements, the stimulus light was switched on and off every 10 s.

The analytical performance of the designed system was analyzed by different concentrations of IL-6. As shown in Figure 3a, the signal increased proportionally to the concentration of IL-6 in logarithmic scale ranged from 5.0 × 10-15 to 1.0 × 10-9 g/mL. The reason for this is that the enhanced concentration of IL-6 could promote the enzymatic formation of AP and thus accelerated the regeneration of Ru(NH3)62+, facilitating PECCC RCA for intensified signal. Figure 3b shows the linear relationship between the PEC response and logarithm of IL-6 concentration, which follows the correlation equation I = 39.27 + 2.05log C (R2 = 0.998). The limit of detection (LOD) is found to be 2.0 × 10-15 g/mL experimentally. Impressively, this immunoassay shows relatively lower LOD compared with some IL-6 detection methods in Table S3.36-39 To evaluate the selectivity, the interfering substances were analyzed including human serum albumin (HSA), human IgG (hIgG), and the mixture of above two proteins plus the target. As shown in Figure 3c, both the IL-6 and mixture exhibited high responses, while the results of HSA and hIgG were similar to that of the blank test, demonstrating the good selectivity of this system. To evaluate the practical application of this method, the immunoassay was applied for the IL-6 measurement in five human serum samples provided by Xinyang Central Hospital, with the results tabulated in Table S4. The relative standard deviations (RSDs) of the 7



proposed method are no more than 7.0%. Additionally, the recovery of IL-6 was measured by the standard addition method in human serums. As listed in Table S5, the recoveries range from 84.9 to 110.3% with RSDs of less than 7.6%, which proved that the method presented here possessed the acceptable accuracy for human samples.

Figure 3. (a) Photocurrents of the immunosensor in response to different concentrations; (b) the linear relationship between the PEC response and the logarithm of IL-6 concentration; (c) selectivity test with HSA, hIgG, and IL-6 concentrations corresponding to 4.0 × 10-2, 1.0 × 10-2, and 1.0 × 10-11 g/mL, respectively.

CONCLUSION In conclusion, we have presented a new Ru(NH3)63+/Ru(NH3)62+-mediated, AP-involved PECCC RCA strategy and its application toward enhanced triple signal amplification for PEC immunoassay. The bridging between the ALP-enabled AP production from a sandwich immunoassay and PECCC RCA on the Bi2S3/BiVO4 photoelectrode is crucial to the operation of the system, based on which a sensitive PEC immunoassay was exemplified by protein IL-6. This work features the first use of Ru(NH3)63+/Ru(NH3)62+ electron mediator for the construction of advanced PECCC RCA strategy and enhanced amplification effect is thus achieved. Based on this protocol, general PEC bioanalysis toward numerous other targets of interest can be envisioned by its integration with specific biorecognition or biocatalytic events. Its desirable properties and potentials determine this protocol main strength in current armory of advanced RCA-based PEC bioanalysis.

ASSOCIATED CONTENT Supporting Information 8


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Experimental section, high-resolution TEM image and elemental mapping of Bi2S3/BiVO4, Raman spectra, XPS spectra and UV-Vis DRS for prepared samples, the optimization of experimental conditions, the study results of reaction process of the bare ITO electrode in Ru(NH3)62+/AP/TCEP system, the table of performance comparison of the proposed method and references, and the tables of analytical results in human serum samples and the recovery of target. AUTHOR INFORMATION Corresponding Authors * E-mail: [email protected] * E-mail: [email protected] ORCID Jun-Tao Cao: 0000-0002-8983-4655 Yan-Ming Liu: 0000-0003-3381-2307 Wei-Wei Zhao: 0000-0002-8179-4775 Notes The authors declare no competing financial interest. ACKNOWLEDGMENTS We gratefully appreciate the support from the National Natural Science Foundation of China (21874115, 21675080, and 21675136), Plan for Scientific Innovation Talent of Henan Province (2017JR0016), the Natural Science Foundation of Jiangsu Province (grant BK20170073), Science & Technology Innovation Talents in Universities of Henan Province (grant 18HASTIT003), and the Nanhu Young Scholar Supporting Program of XYNU.

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spectroscopy. ACS Appl. Mater. Interfaces 2016, 8, 22032-22038.

14


fluorescence

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15


Ru(NH3)62+-Mediated Redox Cycling: Toward

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