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Redox Recycling-Triggered Peroxidase-Like Activity Enhancement of Bare Gold Nanoparticles for Ultrasensitive Colorimetric Detection of Rare Earth Ce3+ Ion Hao-Hua Deng, Bang-Yue Luo, Shao-Bin He, Ruiting Chen, Zhen Lin, Hua-Ping Peng, Xing-Hua Xia, and Wei Chen Anal. Chem., Just Accepted Manuscript • Publication Date (Web): 22 Feb 2019 Downloaded from http://pubs.acs.org on February 22, 2019

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Analytical Chemistry

Redox Recycling-Triggered Peroxidase-Like Activity Enhancement of Bare Gold Nanoparticles for Ultrasensitive Colorimetric Detection of Rare Earth Ce3+ Ion Hao-Hua Deng,a‡ Bang-Yue Luo,a‡ Shao-Bin He,a Rui-Ting Chen,a Zhen Lin,a Hua-Ping Peng,*a XingHua Xia,b Wei Chen*a a Higher

Educational Key Laboratory for Nano Biomedical Technology of Fujian Province, Department of Pharmaceutical Analysis, Fujian Medical University, Fuzhou 350004, China b State Key Laboratory of Analytical Chemistry for Life Science and Collaborative Innovation Center of Chemistry for Life Sciences, School of Chemistry and Chemical Engineering, Nanjing University, Nanjing 210093, China ABSTRACT: Although it has been demonstrated that rare earth elements (REEs) disturb and alter the catalytic activity of numerous natural enzymes, their effects on nanomaterial-based artificial enzymes (nanozymes) have been seldom explored. In this work, the influence of REEs on the peroxidase-like activity of bare gold nanoparticles (GNPs) is investigated for the first time, and a new type of Ce3+-activated peroxidase mimetic activity of GNPs is obtained. The introduced Ce3+ can be bound to the bare GNP surface rapidly through electrostatic attraction, after which it donates its electron to the bare GNP. As H2O2 is a good electron scavenger, more •OH radicals are generated on the surfaces of the bare GNPs, which can considerably enhance TMB oxidation. Due to its redox cycling ability, the activation effect of Ce3+ is proved to be more efficient than those of the other reported metal ion activators (e.g. Bi3+, Hg2+, and Pb2+). In addition, it is determined that Ce3+ should directly contact with the gold core to trigger its activation effect. When the surface states of the bare GNPs are altered, the Ce3+-stimulated effect is strongly inhibited. Furthermore, a novel colorimetric method for Ce3+ is developed, based on its enhancing effect on the peroxidase mimetic activity of bare GNPs. The sensitivity of this newly developed method for Ce3+ is excellent with a limit of detection as low as 2.2 nM. This study not only provides an effective GNP-based peroxidase mimic, but also contributes in realizing new applications for nanozymes.

Rare earth elements (REEs), which differ from the main group elements and transition metals because of the nature of their 4f orbitals, are playing an increasingly prominent role in industrial development and technical progress. Cerium (Ce3+) is one of the most important REEs and has been extensively used in many fields. Due to its enormous usage, there is an increasing demand to study the biological, medical, and environmental effects of cerium. Consequently, the development of rapid, sensitive and selective methods for the determination of Ce3+ is urgently required. Many analytical techniques, such as X-ray fluorescence,1 inductively coupled plasma atomic emission spectrometry,2 inductively coupled plasma mass spectrometry,3 neutron activation analysis,4 and ion-selective electrode, 5 have been applied for the detection of Ce3+; however, these approaches involve expensive equipment or time-consuming procedures and are unsuitable for on-site monitoring. Colorimetric detection has always been an attractive option because it is direct, simple, and low-cost, and does not require highly trained operators and sophisticated

instruments. Nevertheless, the colorimetric detection of Ce3+ has been rarely reported, and shortcomings such as poor sensitivity and serious interference are often encountered.6,7 Artificial enzyme mimetics, which exhibit better stability than natural enzymes and can be prepared on a large-scale by physical blend and chemical methods at relatively low costs, have gained considerable attention.8 Among the numerous candidates, nanomaterials are particularly interesting because of their unique size, shape, composition, and structuredependent properties.9 In a pioneering work on the intrinsic peroxidase-like activity of Fe3O4 magnetic nanoparticles (NPs),10 a series of organic or inorganic nanomaterials have been demonstrated to be capable of simulating the catalytic functions of naturally occurring horseradish peroxidase (HRP).11-21 These nanomaterial-based artificial enzymes (nanozymes) have shown great promise in many fields, including catalysis, chemo/biosensing, pollutant removal, medical diagnostics, and therapy.

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Over the past few decades, gold nanoparticles (GNPs) have been frequently utilized in various applications owing to their easy fabrication, facile modification, excellent chemical stability, good biocompatibility, and special physical and optical properties.22 Although gold has been considered to be biologically and chemically inert, recently, GNPs have been found to exhibit multiple enzyme-mimicking activities, such as glucose oxidase,23 peroxidase,24 oxidase,25 catalase,26 and superoxide dismutase.27 Particularly, the peroxidase-like activity of GNPs has been extensively investigated and applied for the development of versatile sensors for the detection of various analytes.24,28-32 Nevertheless, compared with HRP and other peroxidase nanomimetics, GNPs possess relatively low catalytic activity. Therefore, the improvement of the peroxidase-like activity of GNPs, which can enable highsensitivity detection, is attracting tremendous interest. As nanozyme-catalyzed reactions occur on the particle surface, surface chemistry control has contributed to the understanding and tuning of its catalytic performance. The surfaces of GNPs can easily adsorb various components due to the strong interaction between the gold atom and the sulfhydryl (−SH) and amino (−NH2) groups, and these adsorbed substances can be readily replaced. Of late, several reports are focusing on the surface chemistry of GNPs, and certain activating compounds including melamine,33 adenosine triphosphate,34 and DNA,35 have been identified to enhance the native peroxidase-like activity of GNPs by accelerating the decomposition of H2O2, stabilizing the oxidized species, improving the colloidal stability, or increasing the surface charge. However, the precise regulation of the peroxidase-like activity of GNPs by chemical molecules remains a challenge, and there has been no noteworthy efficiency enhancement thus far, mainly because of their complicated effects on the GNP surface state. For instance, the absorption of single-stranded DNA (ssDNA) on the GNP surface can facilitate substrate binding and strengthen their stability due to electrostatic interaction,35 which is conductive for nanozyme-catalyzed reactions. On the other hand, the bound ssDNA can potentially block the surface active sites of the GNPs, and affect the accessibility of the reactants to GNP surface, inactivating the enzyme mimic function.32 As an alternative, metal ions have been proven to be efficient modulators for enhancing the performance of GNP-based artificial catalytic systems.36-39 The introduced metal ions can be deposited on the GNP surface through aurophilic interactions and change the surface properties of the GNPs, while having negligible influence on the substrate accessibility. Although a remarkable improvement in the peroxidase-mimicking activity of GNPs has been achieved based on this strategy, the use of toxic metal ions such as Hg2+ and Pb2+ would definitely hinder their further biological and environmental application.40 The determination of a new metal ion/GNP pair with high catalytic activity and good compatibility remains challenging. REEs have been shown to affect certain biological progresses by disturbing or altering the functions of enzymes and proteins.41 Biological investigations have indicated that the enzyme activity of HRP is very sensitive to REEs, and the biochemical behavior of REEs toward HRP is very different. For example, Huang et al. found that a low concentration of La3+ can stimulate the catalytic activity of HRP, while a high concentration has an inhibiting effect, known as the “hormesis effect”.42 Ge et al. compared the valence state of cerium (Ce) and the HRP activity, and demonstrated that both Ce3+ and

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Ce4+ can shield the catalytic activity of HRP in the entire concentration range, with Ce4+ being more effective than Ce3+.43 To the best of our knowledge, there are no reports on the evaluation of rare earth ions on the catalytic activity of peroxidase nanomimetics. Based on the above, in this study, we assessed the effect of rare earth ions on the peroxidase-like activity of GNPs, for the first time. Surprisingly, in contrast to the traditional feature of Ce3+ with respect to the HRP, a new type of Ce3+-activated peroxidase mimetic activity was observed in the GNPs. Other rare earth ions, including Ce4+, did not exhibit a similar stimulating catalytic effect. It was found that the activation effect of Ce3+ relied on its electron donating capability and redox recycling ability. This mechanism is completely different from those of other metal ions, wherein the stimulated effect is based on the deposition of metal ions on the GNP surface for changing the GNP surface properties.36-39 Based on the enhancing effect of Ce3+, a colorimetric Ce3+ sensor was established. This REE-mediated surface engineering method can be extended to other nanozymes, as well (may not be Ce3+ in all cases). EXPERIMENTAL SECTION Reagents and Materials. All the used reagents and chemicals were at least analytical grade and were commercially available. Deionized water was used in all the experiments. HAuCl4·4H2O, 3,3’,5,5’-tetramethylbenzidine (TMB), NaBH4, 2,2’-azino-bis(3-ethylbenzothiazoline-6sulfonic acid) diammonium salt (ABTS), N-ethyl-N-(3sulfopropyl)-3-methylaniline sodium salt (TOPS), ophenylenediamine (OPD), Ce2(SO4)3·8H2O, Ce(SO4)2, ScCl3·6H2O, YCl3·6H2O, Eu(NO3)3·6H2O, TbCl3·6H2O, SmCl3, TmCl3, LuCl3·6H2O, NdCl3, LaCl3, GdCl3,Yb(NO3)3·5H2O, Er2(SO4)3·8H2O, PrCl3, HoCl3, and Dy2(SO4)3 were purchased from Aladdin Reagent Co. (Shanghai, China). Sodium acetate, acetate acid, H2O2 (30%, wt.), and 4-aminoantipyrine (4-AAP) were obtained from Sinopharm Chemical Reagent Co. Ltd. (Shanghai, China). Instrumentation. All the ultraviolet–visible (UV–vis) absorption spectra were recorded using a Cary 60 UV–vis spectrophotometer (Agilent). A 1 mL-capacity cuvette with a 1 cm path length was used for measuring the absorbance, and deionized water was employed as the reference solution in the entire colorimetric procedure. The photoluminescence spectra and transmission electron microscopy (TEM) images were obtained using Cary eclipse fluorescence spectrophotometer (Agilent) and JEM-2100 microscope (JEOL), respectively. Synthesis of Bare GNPs. Bare GNPs was prepared according to our previous report.29 The wine-red bare GNP solution was stored at 4 °C before use. Bare GNPs can maintain relative stability in aqueous solution against aggregation for at least two months. Ce3+-Stimulated Peroxidase Mimetic Activity of the Bare GNPs. 0.2 mL of 1 μM Ce3+ solution was added to a 1.5 mL vial containing 0.05 mL bare GNP solution. Further, 0.65 mL of acetate buffer (0.1 M, pH 5.0), 0.05 mL of 5 M H2O2, and 0.05 mL of 8 mM TMB were added. After incubating at 25 °C for 10 min, the resulting solution was measured by naked-eye observation or a Cary 60 UV–vis spectrophotometer (Agilent) at 652 nm.


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Figure 1. (A) UV-vis absorption spectrum of the bare GNPs. Inset: Corresponding photograph of the bare GNPs. (B) Top: Photographs of (a) 0.25 M H2O2 + 0.4 mM TMB, (b) bare GNPs + 0.25 M H2O2 + 0.4 mM TMB, (c) 200 nM Ce3+ + 0.25 M H2O2 + 0.4 mM TMB, and (d) bare GNPs + 200 nM Ce3+ + 0.25 M H2O2 + 0.4 mM TMB; Bottom: Bare GNP-catalyzed reaction of TMB with H2O2. (C) UV-vis absorption spectra of (a) 0.25 M H2O2 + 0.4 mM TMB, (b) bare GNPs + 0.25 M H2O2 + 0.4 mM TMB, (c) 200 nM Ce3+ + 0.25 M H2O2 + 0.4 mM TMB, and (d) bare GNPs + 200 nM Ce3+ + 0.25 M H2O2 + 0.4 mM TMB.

Electron Spin Resonance Measurements. Electron spin resonance (ESR) spectroscopy with a spin trap 5,5-dimethyl-1pyrroline N-oxide (DMPO) was used for detecting hydroxyl radical (•OH) generation in the form of spin adduct DMPO/•OH. Data collection commenced after sample mixing for 1 min, and the ESR spectra were recorded on a Bruker ESR 300E at ambient temperature using the following settings: 0.998 mW microwave power, 1 G field modulation, and 100 G scan range. Colorimetric Assay for Ce3+. 0.2 mL of standard Ce3+ solution with different concentrations were added to a 1.5 mL vial containing 0.05 mL bare GNP solution. Further, 0.65 mL of acetate buffer (0.1 M, pH 5.0), 0.05 mL of 5 M H2O2, and 0.05 mL of 8 mM TMB were added. After incubating at 25 °C for 10 min, the resulting solutions were measured using a Cary 60 UV–vis spectrophotometer (Agilent) at 652 nm. The selectivity test of the proposed sensing system for Ce3+ detection was performed similarly. RESULTS AND DISCUSSION The GNPs used in our study were prepared using the borohydride reduction method. The as-synthesized bare GNPs displayed a distinct wine-red color with an absorption peak at 515 nm (Figure 1A). These GNPs were very stable in aqueous solution due to the electrostatic repulsion invoked by the AuCl4-/AuCl2- ions adsorbed on the particle surface.44 To investigate the peroxidase-like activity of the bare GNPs, we used 3,3’,5,5’-tetramethylbenzidine (TMB) as the substrate. TMB is a promising substrate, which has been extensively applied in immunohistochemistry and enzyme-linked immunosorbent assays because of its high sensitivity, low cost, nontoxicity, and ease of unaided visual detection. As seen in the inset of Figure 1B, the mixture of TMB and H2O2 is colorless. After introducing bare GNPs, only a small fraction of TMB was oxidized and a light blue color was observed, suggesting that bare GNPs possess relatively low catalytic activity. Surprisingly, with the addition of a trace amount of Ce3+ (200 nM), the catalytic activity of the bare GNPs drastically increased, and the deep blue color of the oxidized TMB (oxTMB) was observed immediately. In the control experiments, we used Ce3+ to catalyze the H2O2mediated TMB chromogenic reaction, which showed no catalytic activity for Ce3+. Therefore, Ce3+ functioned as a promoter for the bare GNPs. The UV-vis absorption spectra of

these samples were recorded (Figure 1C). The oxTMB has a remarkable absorption peak at around 652 nm, whose height is approximately 10 times more with Ce3+, than without it. As can be seen from Figure S1, bare GNPs cannot catalyze TMB chromogenic reaction in the absence of H2O2, and the ultrafiltrate of bare GNPs ( 0.375 M). This may be due to the competitive binding between H2O2 and Ce3+ on the surfaces of bare GNPs. The time-dependent curve indicates that ΔA increases on increasing the reaction time up to 10 min, above which, it increases slowly (Figure S8). Based on these results, the experimental conditions for Ce3+ detection were employed as follows: a solution pH of 5, incubation temperature of 25 °C, TMB concentration of 0.4 mM, H2O2 concentration of 0.25 M, and reaction time of 10 min. Under optimal conditions, the sensitivity of this method for the detection of Ce3+ was evaluated. As shown in Figure 5, the absorbance increased on increasing the concentration of Ce3+. In the calibration graph, the ΔA value versus Ce3+ concentration was linear in the 10160 nM range. The regression equation is ΔA = 0.01252 [Ce3+] (nM) − 0.08547, r2 = 0.99873. The limit of detection (LOD) was calculated to be 2.2 nM, based on the 3σ/slope (σ = standard deviation of the blank signal). The relative standard deviation (RSD) was 2.8% for the detection of 50 nM Ce3+ (n = 9). The proposed method

was compared to the analytical methods previously published in the literature. As seen in Table 1, the proposed method is highly sensitive, facile, and simple without any surface modification steps, trained operators, toxic reagents, and complicated or time-consuming detection processes. It is to be noted that the sensitivity of this method was 23 orders of magnitude higher than those of the colorimetric detection methods based on the Ce3+-induced SPR peak shift of the GNPs and Ce3+-binding to the chromogenic reagent.6,7

Figure 5. Relationship between A652 and the concentration of Ce3+. Inset: Linear relationship between ∆A and the concentration of Ce3+. The error bars represented the standard deviation across three repetitive experiments.

Further, the selectivity of this assay against those of the other ions was estimated. Figure 6A shows that only Ce3+ ions can significantly stimulate the peroxidase-like activity of bare GNPs. Other rare earth ions, including Sc3+, Y3+, La3+, Ce4+, Pr3+, Nd3+, Sm3+, Eu3+, Gd3+, Tb3+, Dy3+, Ho3+, Er3+, Tm3+,


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Yb3+, and Lu3+, did not exhibit any distinct activation effect. Moreover, we tested the system with 20 types of cations and 21 types of anions. All the tested cations and anions showed nearly negligible changes in the absorbance of the sensing system (Figure 6B and 6C). Very slight absorbance enhancement was found in the presence of Bi3+, Hg2+, and Pb2+, which is in accordance with the phenomenon observed in citrate-capped GNPs.36-38 The calculation results show that the enhancing efficiency of Ce3+ is 8.5, 27.8, and 18.0 times higher than those of Bi3+, Hg2+, and Pb2+, respectively. This is probably because of the recycling ability of Ce3+/Ce4+, which provides sustained effect on the bare GNPs. Fe3+ was also found to boost the peroxidase-mimicking activity of bare GNPs as it can catalyze H2O2 resulting in •OH, however, a higher concentration is needed (Figure S9). Other molecules at certain concentrations exhibit negligible influence on the testing system (Figure S10). These data sufficiently indicate that this sensor is highly specific for quantification of Ce3+.

Figure 6. Selectivity test of the newly developed method for the detection of Ce3+. (A) Rare earth ions. Samples marked as 1−17 correspond to Ce3+, Sc3+, Y3+, La3+, Ce4+, Pr3+, Nd3+, Sm3+, Eu3+, Gd3+, Tb3+, Dy3+, Ho3+, Er3+, Tm3+, Yb3+, and Lu3+. (B) Cations. Samples marked as 1−21 correspond to Ce3+, Sn2+, Bi3+, Cr3+, Cu2+, Ag+, Zn2+, Fe3+, Na+, K+, Mg2+, Mn2+, NH4+, Pb2+, Co2+, Ba2+, Ni2+, Al3+, Cd2+, Hg2+, and Ca2+. (C) Anions. Samples marked as 1−22 correspond to Ce3+, S2O32-, OAc-, BrO3-, EDTA2-, ClO4-, NO2-, C4O6H42-, HCO3-, SO32-, Cr2O72-, HPO42-, S2O82-, Mo2O72-, F-, IO3-, I-, MnO4-, SCN-, B4O72-, IO4-, and S2-. The concentration of all the tested ions was 200 nM. The error bars represent the standard deviation across three repetitive experiments.

Table 2. Results of the Determination of Ce3+ in Tap Water Added value (nM) 100 200 400

Found value (nM) 97.4 185.0 384.8

Recovery (%) 97.4 92.5 96.2

RSD (%, n = 3) 1.9 6.4 4.9

In view of its excellent sensitivity and high selectivity, the feasibility of this newly developed method for practical application was confirmed by measuring the Ce3+ concentration in tap water samples. It was found that Ce3+ was not detectable in tap water using this approach. Therefore, using the standard addition method, different amounts of Ce3+ were respectively spiked in the tap water samples and analyzed. As seen from Table 2, the recovery for the sample was in the range of 92.597.4%, proving that there were no significant differences between the determined and added values. This result validates the application of the proposed Ce3+ sensor for real samples.

CONCLUSIONS

In summary, we have reported a new mechanism for improving the peroxidase-like activity of GNPs by Ce3+mediated surface engineering, in this work. The introduced Ce3+ can be absorbed on the bare GNP surface rapidly by electrostatic force, and accelerate the decomposition of H2O2 into •OH by donating its electron to the bare GNPs. As more •OH radicals are generated on the surfaces of the bare GNPs, the oxidation of TMB is considerably enhanced. Due to its redox recycling ability, the activation effect of Ce3+ is prominently higher than those of the other ions. This work enables better understanding of the chemical regulation of the catalytic activity of nanozymes. The newly recognized bare GNP/Ce3+ system has great potential in analytical and bioanalytical applications. As a demonstration, we developed a colorimetric sensor for the detection of Ce3+. Compared to the other approaches based on absorbance, this detecting system exhibited high sensitivity and excellent selectivity.

ASSOCIATED CONTENT Supporting Information



Additional information as noted in text. This material is available free of charge on the ACS Publications website. Catalytic activities of bare GNPs and their ultrafiltrate for TMB chromogenic reaction, the oxidation of other chromogenic reagents, UV-vis spectra of bare GNPs and bare GNPs + Ce3+, effect of the adding sequences of H2O2 and Ce3+ on the observed peroxidase-like activity enhancement of bare GNPs, effect of incubation time on the assay system for the detection of Ce3+, effect of Fe3+ on the bare GNPs-catalyzed TMB-H2O2 reporting system, and the selectivity of this assay against those of other

molecules.

AUTHOR INFORMATION Corresponding Author *E-mail address: [email protected] (W. Chen), [email protected] (H.P. Peng). Tel./fax: +86 591 22862016. ORCID Xing-Hua Xia: 0000-0001-9831-4048 Wei Chen: 0000-0003-3233-8877 Author Contributions ‡These authors contributed equally.

Notes The authors declare no competing financial interest.

ACKNOWLEDGMENT The authors gratefully acknowledge the financial support from the National Natural Science Foundation of China (21675024, 21804021), the Program for Innovative Leading Talents in Fujian Province (2016B016), the Joint Funds for the Innovation of Science and Technology, Fujian Province (2016Y9056), the Natural Science Foundation of Fujian Province (2017J01575), and the Science and Technology Project of Fujian Province (2018L3008), and Startup Fund for scientific research, Fujian Medical University (2017XQ1014).

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