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A Glucose Oxidase-Instructed Fluorescence Amplification Strategy for Intracellular Glucose Detection Shanshan Jiang, Yifan Zhang, Yichen Yang, Yan Huang, Gongcheng Ma, Yongxiang Luo, Peng Huang, and Jing Lin ACS Appl. Mater. Interfaces, Just Accepted Manuscript • DOI: 10.1021/acsami.9b00010 • Publication Date (Web): 26 Feb 2019 Downloaded from http://pubs.acs.org on March 6, 2019

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ACS Applied Materials & Interfaces

A Glucose Oxidase-Instructed Fluorescence Amplification Strategy for Intracellular Glucose Detection Shanshan Jiang†, Yifan Zhang†, Yichen Yang, Yan Huang, Gongcheng Ma, Yongxiang Luo, Peng Huang, Jing Lin* Guangdong Key Laboratory for Biomedical Measurements and Ultrasound Imaging, International Cancer Center, Laboratory of Evolutionary Theranostics, School of Biomedical Engineering, Shenzhen University Health Science Center, Shenzhen 518060, China. †Equal

contribution authors.

ABSTRACT: The accurate detection of glucose in the cellular level remains a big challenge. In this study, a signal amplification strategy mediated by silver nanocube (AgNC), glucose oxidase (GOx) and silver ion fluorescence probe (denoted as AgNC-GOx/Ag+-FP) is proposed for amplified intracellular glucose detection. The AgNC is oxidized into Ag+ by H2O2 generated from the GOx-catalyzed glucose oxidation reaction, and Ag+ remarkably enhances the red fluorescence of Ag+-FP. Our results show that the AgNC-GOx/Ag+-FP is highly sensitive and specific to glucose and H2O2. Afterwards, the feasibility of using AgNC-GOx/Ag+-FP to detect intracellular glucose is verified in five different cell lines. In summary, a sensitive and specific fluorescence amplification strategy has been developed for intracellular glucose detection. KEYWORDS: intracellular glucose, silver nanocube, glucose oxidase, fluorescence probe, signal amplification

INTRODUCTION Diabetes mellitus, as a disease of glucose metabolic disorder, is a global health concern which affects almost 10% of the world population.1 The abnormal blood glucose level (hypo- or hyperglycaemic) caused by diabetes can cause severe complications including coma, seizures, and organ damages.2 Accurate detection of blood glucose level is the first step for effective treatment of diabetes mellitus.3-6 In addition to the blood glucose monitoring, intracellular glucose detection is also indicative of many important cellular activities.7 For example, glucose is the main energy source of cells, especially for tumor cells, so the cut-off of glucose uptake is a promising cancer treatment pattern.8-9 Over the years, various noninvasive glucose monitoring methods have been developed, including spectrophotometry10-13, fluorometry14-16 and chemiluminescence17-20. Among these methods, fluorometry detection has drawn increasing research interest due to several distinct merits such as high sensitivity, rapid response, low cost and easy operation.21-23 For example, Song et al. reported a tetraphenylethylene derivative (TPE-HPro) for glucose and H2O2 detection. In the presence of H2O2, the phenylboronic pinacol ester on TPE-HPro is oxidized and the p-quinone methide is released, accompanied with bright yellow fluorescence.24 However, few of these fluorescence probes could detect the changes of intracellular glucose concentration.

in sensing, electronics, photonics and antimicrobial fields.25 As typical noble metal nanoparticles, AgNPs have characteristic surface plasmon resonance (SPR) absorption and high extinction coefficient, which make them suitable for optical sensors. By oxidation of H2O2 and H+, AgNPs could be degraded into Ag+.26 Therefore, the combination of AgNPs and glucose oxidation (GOx) has the potential to be a biodegradable glucose probe.27 For instance, Luo et al synthesized Ag nanoclusters that have an average size of 2 nm and emit blue fluorescence at ~455 nm.28 In combination of GOx, the fluorescence intensity of Ag nanoclusters decreased with the concentration of glucose. However, Ag nanoclusters are instable and the fluorescence turn-off detection strategy has relatively low sensitivity. Furthermore, AgNP-based fluorescence probe for intracellular glucose detection has yet to be developed.

Scheme 1. Schematic illustration of fluorescence amplification strategy of glucose detection mediated by AgNC-GOx/Ag+-FP.

Silver nanoparticles (AgNPs) have unique electronic, optical and antibacterial properties, which are widely used

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To address these issues, we have synthesized GOxconjugated Ag nanocube (AgNC-GOx) and an ultrasensitive Ag+ fluorescence probe (3', 6'-bis (diethylamino)-2-(2-iodoethyl) spiro[isoindoline-1, 9'xanthen]-3-one (Ag+-FP) (Scheme 1).29 In the existence of glucose, GOx can catalyze the glucose oxidation reaction to produce H+ and H2O2. The generated H2O2 could further degrade AgNC into Ag+. The generated Ag+ would turn on the fluorescence of Ag+-FP. The chemical equations of chain reactions among glucose, GOx and AgNC are as follows: Glucose + O2 + H2O (1)

𝐺𝑂𝑥

Gluconic acid + H2O2

2Ag + H2O2 + 2H+ → 2Ag+ + 2H2O (2) In the chain reactions above, one molar H2O2 could produce two molar Ag+, and then Ag+ increases the fluorescence of Ag+-FP molecule. Therefore, our probe AgNC-GOx/Ag+-FP could remarkably amplify the fluorescence signal and achieve high sensitivity. This new amplification strategy for glucose detection is of high specificity and selectivity toward glucose and H2O2. The fluorescence detection of intracellular glucose using AgNC-GOx/Ag+-FP is also investigated in both normal and tumor cells. EXPERIMENTAL SECTION Materials. Ethylene glycol (EG), Silver trifluoroacetate (CF3COOAg), Thioctic acid (TA), Rhodamine B, 2aminoethanol, acetone, glucose, mannose, fructose, maltose, sucrose, galactose, lactose, Nhydroxysuccinimide (NHS) and carbodiimides (EDC) were obtained from JK Chemical. H2O2 Assay Kit, Glucose oxidase (GOx) and poly(vinyl pyrrolidone) (PVP, MW ≈ 55 000) were purchased from Sigma-Aldrich. Xylose was obtained from MCE. Apparatus. Fluorescence intensity was measured by Synergy H1 microplate reader (BioTek, USA). Fluorescence spectra were taken on a Thermo Scientific Lumina fluorescence spectrophotometer (Thermo Fisher Scientific Co., USA). UV-Vis absorption spectra were taken on a Cary 60 UV–vis spectrophotometer (Agilent Technologies, Santa Clara, CA, USA). Transmission electron microscopy (TEM) images were captured on a JEM-1230 TEM (JEOL, Tokyo, Japan). Zeta potential was recorded by a Malven model Zetasizer 2000 zeta potential analyzer. FT-IR spectra were collected on an attenuated total reflectance FTIR spectrometer (Spectrum Two™, PerkinElmer). The H2O2 concentration was detected by a H2O2 Assay Kit (Biyotime, Shanghai, China). Fluorescence imaging was performed on an IVIS Spectrum system (Caliper Life Sciences, Hopkinton, MA).

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Synthesis of GOx-conjugated silver nanocube (AgNC-GOx). Fisrtly, 0.4 mL trifluoroacetate (CF3COOAg) (282 mM in ethylene glycol) reacted with NaHS (3 mM in EG) and poly(vinyl pyrrolidone) (20 mg/mL in EG) at 150 °C for 20 min. Afterwards, the mixture was centrifuged (9000 g, 10 min) to obtain AgNC and dispersed in deionized water. To conjugate AgNC with thioctic acid (TA), NaOH (0.5 M) was added to 5 mL AgNC solution. Subsequently, TA (15 mM in ethanol) was slowly added to the solution and stirred for 2 h. After centrifugation at 9000 g for 10 min, the AgNC-TA was obatined and dispersed in deionized water. To conjugate AgNC-TA with GOx, NHS and EDC reacted with the as-prepared AgNC-TA solution (5 mL) for 0.5 h. Then 3 mg of GOx was added into the solution above under stirring for 1 h. After centrifugation at 9000 g for 10 min, the AgNC-TA was obatined and dispersed in deionized water. Synthesis of Rhodamine B-based Ag+ fluorescence probe (Ag+-FP). The Ag+ fluorescence probe 3', 6'bis(diethylamino)-2-(2-iodoethyl)spiro[isoindoline-1, 9'xanthen]-3-one (Ag+-FP) was synthesized according to the previous method. First, 2-aminoethanol was dissolved in ethanol reacted with Rhodamine B at 120 °C for 2 days to obtain 3', 6'-bis(diethylamino)-2-(2-hydroxyethyl)-3', 9'dihydrospiro[isoi-ndoline-1, 9'-xanthen]-3-one (product 1). The product 1 reacted with methanesulfonyl chloride and sodium iodide to obtain the Ag+-FP by a cascade reaction: methanesulfonyl reaction and iodide reaction. Ag+-FP was characterized by 1H NMR spectra (Figure S1, S2, Supporting Information). Detection of glucose in aqueous solutions. 50 μL AgNC-GOx (200 nM in PB buffer) was added into each 96well plates, and 50 µL different concentrations of glucose solution (in PB buffer) were added. The mixture was incubated for 2 h at room temperature. 100 µL Ag+-FP solution (20 µM) comprised of 20% ethanolic was then added and incubated at room temperature for 1 h. Afterwards, the fluorescence intensity of each well was measured. Detection of glucose in living cells. MCF-10a, HeLa, MCF-7, A375 and 4T1 cells were cultured in Dulbecco’s modified Eagle’s medium (DMEM) supplemented with 10% fetal bovine serum (FBS) and 1% penicillin / streptomycin at 37 ºC. The cells were seeded into 6-well plates at a density of 2x105 cells per well. After incubation for 24 h, the culture medium was replaced and the different cells were incubated with AgNC-GOx (50 nM, 2 mL) with no glucose. After 2 h, the cells were washed three times with PB buffer and added Ag+-FP (10 μM, 1 mL). Then the fluorescence intensity of Ag+-FP was measured by using a fluorescence microscope, a microplate reader and a flow cytometry.

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RESULTS AND DISCUSSION To prepare the GOx-conjugated AgNC (AgNC-GOx), thioctic acid (TA) was firstly conjugated to the surface of AgNC through Ag-S bond. TA could offer carboxyl groups for further conjugation with GOx via amide bonds. As shown in Figure 1a, the as-prepared AgNC-GOx solution was light yellow green, while the natural AgNC was light yellow. The UV-vis spectrum of AgNC-GOx is similar to that of AgNC, which peaked at ~435 nm. During the conjugation process, AgNC remained a cubic shape with a narrow size distribution at ~45 nm, further confirming its stability (Figure 1b). The zeta potential of AgNC-TA was about -28.1 ± 0.87 mV, which was significantly lower than that of AgNC (-19.47 ± 0.96 mV) due to the abundant carboxyl groups of TA on its surface (Figure 1c). After conjugation with GOx, the zeta potential increased to -23.2 ± 0.75 mV due to the high negative surface charge of GOx. The Fourier-transform infrared spectroscopy (FTIR) spectra of AgNC, GOx and AgNC-GOx were also examined (Figure 1d). In Figure 1d, the characteristic band of both GOx and AgNC-GOx at 1640−1660 cm−1 were principally attributed to the C=O stretching mode in the amid I, which further indicated the existence of GOx in AgNC-GOx. The as-prepared AgNC-GOx was stable in PBS for more than 2 h (Figure S3, Supporting Information).

Figure 1. (a) UV-Vis-NIR spectra of AgNC and AgNC-GOx. (b) TEM image of AgNC-GOx. (c) Zeta potentials of AgNC, AgNCTA and AgNC-GOx. (d) FTIR spectra of AgNC (black), GOx (blue) and AgNC-GOx (red).

Figure 2. (a) TEM images of AgNC-GOx before and 1, 2 h after incubation with glucose solution. Scale bar: 20 nm. (b) UVVis-NIR spectra of AgNC during the incubation with H2O2 solution. (c) Absorbance changes of AgNC-GOx at 435 nm after 2 h incubation with glucose. The insets are digital photos of AgNC-GOx in different concentrations of glucose solution. (d) H2O2 concentration and (e) pH value of GOx or AgNCGOx solution after 2 h incubation with glucose at different concentrations. n=3, Mean ± SD.

The chain reactions between AgNC-GOx and glucose was then investigated in vitro. As shown in Figure 2a, the morphology of AgNC gradually changed from cube to round after incubation with glucose solution. The characteristic absorbance peak of AgNC also gradually decreased in the H2O2 solution, which further demonstrated the dissolution of AgNC into Ag+ (Figure 2b). In Figure 2c, the absorption decrease of AgNC-GOx at 435 nm was positively correlated with the concentration of glucose. The digital photos of AgNC-GOx also showed that the yellow green color of AgNC-GOx became paled to colorless during the dissolution of AgNC. A large number of gluconic acid (reflected by the value of pH) and H2O2 were generated during the glucose decomposition reaction catalyzed by GOx (Figure 2d, e), which indicated that AgNC was oxidized into Ag+ by H2O2 and H+ produced from GOx-catalyzed glucose decomposition. Compared to traditional fluorescence probes for glucose that detect H2O2 concentration or pH, detection of Ag+ generated by the oxidation reaction of AgNP and H2O2 is supposed to further amplify the signal. The Ag+ fluorescence probe (Ag+-FP) was synthesized according to the literature, and its structure was confirmed using 1H NMR spectrum.30 There was an exponential relationship



between the fluorescence intensity of Ag+-FP and the concentration of Ag+ (Figure S4, Supporting Information). The fluorescence increase of Ag+-FP was highly specific to Ag+ (Figure S5, Supporting Information). As shown in Figure 3, the fluorescence intensity of Ag+-FP that incubated with AgNC-GOx increased with the concentration of glucose. A good exponential correlation between the fluorescence intensity and the glucose concentration ranging from 0.05 to 5 mM was observed (R2 = 0.9913). The limit of detection (LOD) of Ag+-FP for glucose was determined to be 50 μM (S N-1 = 3). The interferences of H2O2, GOx, AgNC and gluconic acid on the fluorescence of Ag+-FP had been excluded (Figure S6, Supporting Information). Therefore, our results showed that the fluorescence amplification strategy mediated by AgNC-GOx/Ag+-FP can detect glucose with high sensitivity.

Figure 3. (a) Fluorescence spectra of Ag+-FP (10 μM) in the presence of AgNC-GOx (50 nM) and different concentrations of glucose (0, 0.05, 0.1, 0.2, 0.6, 1, 2 and 5 mM). (b) Calibration curves of fluorescence intensity versus the concentrations of glucose (ex: 530 nm; em: 585 nm), R = 0.996. (c) Fluorescence images of Ag+-FP incubated with AgNC-GOx and different concentrations of glucose (0, 0.005, 0.05, 0.1, 0.3, 0.5, 1, 2, 5 and 10 mM).

Subsequently, the selectivity of AgNC-GOx/Ag+-FP toward glucose was tested. Under the same condition, there was no obvious fluorescence increase of Ag+-FP to mannose, fructose, maltose, sucrose, galactose and lactose, while glucose induced a significant increase of fluorescence, indicating the good selectivity of our detection method (Figure. 4a). The feasibility of using our probe to detect intracellular glucose was then investigated. AgNC-GOx could be efficiently incorporated into cells (Figure S7, Supporting Information), so the intracellular glucose could be oxidized into H2O2 and H+ by AgNC-GOx. After removing the extracellular AgNC-GOx, Ag+-FP was added into the cell medium to detect the concentration of Ag+. The fluorescence signals of Ag+-FP in five cell lines were detected, including MCF-10a, MCF-7, 4T1, HeLa and A375. As shown in Figure 4b and 4c, after incubation of AgNC-GOx/Ag+-FP for 2 h, red fluorescence could be observed inside the cells. Comparatively, AgNC/Ag+-FP

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caused much lower intracellular fluorescence increase, which indicated that the interference of intracellular H2O2 (Figure S8, Supporting Information). The subtraction of the fluorescence increase induced by AgNC/Ag+-FP could be a feasible choice to eliminate the interference of intracellular H2O2. Notably, the fluorescence increase of Ag+-FP in the four tumor cell lines was higher than that in the normal cells (MCF-10a), which indicated a relatively higher glucose concentration in the tumor cells than normal cells. This result was consistent with the reports that tumor cells consumed a higher amount of glucose than normal cells.31 AgNC at the detection concentration had no obvious toxicity to five different cells, demonstrating a good biocompatibility of the probe (Figure S9, Supporting Information). Further quantification of intracellular glucose is not allowed due to the fluctuation of intracellular glucose concentration.

Figure 4. (a) Selectivity of the detection for glucose. [Ag+FP]=10 μM, [AgNC-GOx]=50 nM. The final concentrations of Glucose and other saccharides: 2.5 mM. (b) Fluorescence intensity and (c) fluorescence images of Ag+-FP in different cell lines incubated sequentially with AgNC-GOx and Ag+-FP. Scale bar: 100 μm. (d) Flow cytometry analysis of different cell lines sequentially incubated with AgNC-GOx and Ag+-FP. n=3, mean ± SD, ****P < 0.0001, two-sided Student’s t-test.

CONCLUSIONS In summary, we have developed a highly specific and selective fluorescence amplification approach based on silver nanoparticles for intracellular glucose detection (AgNC-GOx/Ag+-FP). The AgNC can be oxidized into Ag+ by H2O2 and gluconic acid generated from the GOxcatalyzed glucose decomposition. Each Ag+ can increase the fluorescence intensity of one Ag+-FP molecule, thus largely amplifying the signals. This signal amplification strategy provides a novel method for sensitive glucose detection in the cellular level. Moreover, this system that combines AgNC-enzyme and Ag+ probes can be easily


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extended to other enzyme-substrate catalysis reactions generating H2O2 and H+, such as choline-choline oxidase, lactic acid-lactate oxidase), and oxalic acid-oxalic oxidase, etc.

ASSOCIATED CONTENT Supporting Information The Supporting Information is available free of charge on the ACS Publications website at DOI: Synthetic method and 1H NMR spectrum of Ag+-FP, the stability of the AgNC-GOx, H2O2 and pH values produced by the reaction between GOx and glucose, fluorescence spectra of Ag+-FP in the different concentrations of Ag+, selectivity of the Ag+-FP for metal cations, the fluorescence intensity of Ag+-FP in glucose and AgNC or GOx, confocal laser scanning microscopy (CLSM) images of AgNC-5-AF, fluorescence intensity of Ag+-FP in different cell lines incubated sequentially with AgNC and Ag+-FP and the viability of different cells incubated with AgNC (PDF)

AUTHOR INFORMATION Corresponding Author E-mail: [email protected] Notes The authors declare no competing financial interest.

ACKNOWLEDGMENTS This work is financially supported by the National Natural Science Foundation of China (31771036, 51573096, 51703132), the Basic Research Program of Shenzhen (JCYJ20170412111100742), Guangdong Province Natural Science Foundation of Major Basic Research and Cultivation Project (2018B030308003), Fok Ying-Tong Education Foundation for Young Teachers in the Higher Education Institutions of China (161032), and China Postdoctoral Science Foundation (2018M633139).

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