Nanocrystalline Cellulose-Assisted Generation of Silver Nanoparticles

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Nanocrystalline Cellulose-Assisted Generation of Silver Nanoparticles for Non-enzymatic Glucose Detection and Antibacterial Agent Shiwen Wang, Jiashu Sun, Yuexiao Jia, Lu Yang, Nuoxin Wang, Yunlei Xianyu, Wenwen Chen, Xiaohong Li, Ruitao Cha, and Xingyu Jiang Biomacromolecules, Just Accepted Manuscript • DOI: 10.1021/acs.biomac.6b00642 • Publication Date (Web): 22 Jun 2016 Downloaded from http://pubs.acs.org on June 24, 2016

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Nanocrystalline Cellulose-Assisted Generation of Silver Nanoparticles for Non-enzymatic Glucose Detection and Antibacterial Agent Shiwen Wang,†,‡ Jiashu Sun,‡,* Yuexiao Jia,‡ Lu Yang,‡ Nuoxin Wang,‡ Yunlei Xianyu,‡ Wenwen Chen,‡ Xiaohong Li,†,* Ruitao Cha,‡ and Xingyu Jiang‡,* †

Key Laboratory of Advanced Technologies of Materials, Ministry of Education of China,

School of Materials Science and Engineering, Southwest Jiaotong University, Chengdu, 610031, China ‡

Beijing Engineering Research Center for BioNanotechnology & CAS Key Laboratory for

Biological Effects of Nanomaterials and Nanosafety, CAS Center for Excellence in Nanoscience, National Center for NanoScience and Technology, 11 Beiyitiao, ZhongGuanCun, Beijing, 100190, China KEYWORDS. Nanocrystalline cellulose; Silver nanoparticles; Glucose; Visual detection; Antibacteria

ABSTRACT. Nanocrystalline cellulose (NCC) is a kind of natural biopolymers with merits of large surface area, high specific strength and unique optical properties. This report shows that NCC can serve as the substrate, allowing glucose to reduce Tollen's reagent to produce silver

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nanoparticles (AgNPs) at room temperature. The generation of AgNPs is affected by the factors such as the concentrations of silver ions, NCC and glucose, as well as the different reaction temperatures. The AgNPs with NCC are applied for the development of a visual, quantitative, non-enzymatic and high-sensitive assay for glucose detection in serum. This assay is also used for monitoring the concentration change of glucose in medium during cell culture. For the antibacterial activity, the minimal inhibitory concentration (MIC) of the generated AgNPs with NCC is much lower than that of commercial AgNPs, attributed to the good dispersion of AgNPs with the presence of NCC. As NCC exhibits unique advantages including green, stable, inexpensive, and abundant, the NCC-based generation of AgNPs may find promising applications in clinical diagnosis, environmental monitoring, and the control of bacteria.

INTRODUCTION Cellulose is one of the most accessible natural biopolymers produced from a variety of organisms (plants, tunicates, algae, or bacteria) and has been applied in many fields, such as paper products, textile industry, pharmaceuticals, and so forth. Nanocrystalline cellulose (NCC) refers to the nanorod-like cellulose of 100-300 nm in length generated by removing the amorphous part of cellulose materials from forest and agricultural crops via hydrolysis or oxidation.1-5 NCC has the merits typically associated with nanorod materials, including large surface area, high specific strength, and unique optical properties. In addition, NCC possesses the following distinct characteristics: (1) NCC is a kind of green material, which is renewable and biodegradable.1, 6, 7 (2) NCC can be manufactured on an industrial scale, and modified with various surface chemistry,8,

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facilitating the applications of NCC in real-world products and

services. (3) NCC has abundant hydroxyl groups as well as the charged surface, making it stable in water.2 Due to these privileged physicochemical properties, NCC has attracted tremendous


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interest from both scientific and industrial communities, and showed great potential in a variety of applications, including drug delivery, bioimaging, tissue engineering,9-17 reinforcement of functional materials,18-21 fabrication of structural color materials,22-27 and so forth.8, 28-30 NCC has also been proposed as a bio-derived matrix for the fabrication of various nanoparticles, such as silver, gold, platinum and palladium nanoparticles in a facile method.28, 3137

NCC could promote the nucleation of metallic nanoparticles from metal salts with the

assistance of reducing agents, while preventing the aggregation of nanoparticles to achieve a narrow size distribution. For example, silver ions could be reduced to silver nanoparticles (AgNPs) using sodium borohydride (NaBH4) as the reducing agent in the presence of NCC.18, 32, 34, 37, 38

NaBH4 is a toxic and hazardous reducing agent that may result in undesired health and

environmental impact. The reduction of Ag+ ions into AgNPs in mild alkaline conditions has also been demonstrated using modified NCC with aldehyde group that serves as the reducing reagent.31 The surface modification of NCC is relatively complicated and involves several chemicals such as periodate. Our previous research applied glucose as the reducing agent, and the negatively charged gold nanorods (AuNRs) as the substrate to generate AgNPs from Tollen's reagent (Ag(NH3)2OH) at 80 oC. The produced AgNPs appeared light yellow, and were used for visual detection of glucose in serum samples. In comparison with AuNRs, NCC has a higher negatively charged surface due to the large amounts of exposed sulfate ester groups, making it desirable as the substrate for the synthesis of AgNPs. The generated nanoparticles assisted by NCC could lead to a variety of interesting applications. The hybrid Pt/NCC nanoparticles exhibited an enhanced electrocatalytic activity towards the reduction of p-nitrophenol.39 The NCC decorated with Cu-Co ferrite yielded magnetic properties and showed the improved thermostability compared with unmodified


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NCC.40 An enzyme/AuNPs/NCC composite revealed high biocatalytic activity and enhanced enzyme stability.41 The generated AgNPs with the assistance of cellulose nanomaterials showed efficient antimicrobial activity against pathogenic bacteria.31, 37, 42, 43 The AgNPs/NCC composite also exhibited a high-quality surface-enhanced Raman scattering activity.38 In this study, we employ glucose as the reducing agent, and NCC as the substrate to generate AgNPs from silver ions in Tollen’s reagent at room temperature. The fabricated AgNPs under different synthetic conditions are characterized by transmission electron microscopy (TEM) and UV/Vis absorbance spectra. The generated AgNPs assisted by NCC are applied for developing a visible, sensitive, and quantitative glucose assay without the use of enzymes. This glucose assay can work at room temperature, and be used for detecting glucose in human blood and cell culture medium. The AgNPs/NCC also exhibits enhanced antibacterial activity in comparison with commercial AgNPs. MATERIALS AND METHODS Materials D-(+)-glucose was from Sigma-Aldrich. All other chemicals were from Beijing Chemical Reagents Co., Ltd.. All chemicals used in the experiment were analytical grade, and milli-Q water (resistivity>18 MΩ cm, Milli-Q) was used throughout the work. Cotton pulp was kindly provided by China International Tourism & Trade Co., Ltd. ACCU-CHEK performa, a personal glucose meter, was purchased from Roche Ltd. A commercial glucose kit (with glucose oxidase) was purchased from Nanjing Jiancheng Bioengineering Institute. AgNPs (10 nm in diameter) were purchased from Sigma-Aldrich with sodium citrate as stabilizer. Preparation of NCC


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The NCC used in this work was prepared by sulfuric acid hydrolysis of cotton pulp. We mechanically stirred 10 g of shredded cotton pulp in 200 mL of sulfuric acid aqueous solution (64% w/w) maintained at 45 oC for 45 min. The hydrolysis was stopped after 45 min stirring by adding 2 L of milli-Q water, followed by standing overnight. The viscous sediment was washed twice with milli-Q water via centrifugation. The obtained suspension was dialyzed against water until the pH value of the outside water remained unchanged. The dialyzed liquid was freezedried and stored in the refrigerator. Preparation of Ag(NH3)2OH (Tollen's reagent) Ammonia (15 M) was added into 6 mL of silver nitrate solution (0.1 M, in milli-Q water) placed in a 50 mL tube with stirring until the brown precipitate just dissolved. 3 mL of KOH solution (0.8 M in milli-Q water) was then added, and the brown precipitate reformed. Ammonia (15 M) was added again to dissolve the precipitate. Milli-Q water was added to reach a final volume of 25 mL. The solution of Ag(NH3)2OH (24 mM) should be prepared just before use and stored in the dark at 4 oC.44 Orthogonal Assay Design for Optimization of AgNPs Generation An orthogonal assay was designed (Table 1) to explore the effects of silver ions, NCC, glucose and temperature on generation of AgNPs. This orthogonal assay was also used to obtain the optimized condition for synthesis of AgNPs. To get predetermined concentrations of silver ions and NCC, we mix Ag(NH3)2OH solution and NCC solution of different amounts in a glass tube. Glucose of different concentrations was added into the mixture and shaken thoroughly, to initiate the reaction for AgNPs generation. The tube was incubated at different temperatures for 30 min. After incubation, the products were dialyzed against milli-Q water in dark for 24 h at room temperature. The morphology of the samples was characterized by a TEM (Tecnai G2 20


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S-TWIN, FEI, USA) with carbon-coated copper support grids (Beijing Xinxing Braim Technology Co. Ltd). More than 200 of nanoparticles from 10 TEM images (130,000 magnification) were counted and sized by Image Pro Plus. The UV/Vis spectra of AgNPs were measured with a spectrophotometer (UV2450, Shimadzu). The absorbance at 410 nm of generated AgNPs was recorded by a microplate spectrophotometer (TECAN, Infinite 200 PRO). NCC-assisted Generation of AgNPs at Room Temperature To study the NCC-assisted generation of AgNPs at room temperature, 20 µL of glucose (500 µM), 20 µL of NCC aqueous solution with different concentrations (0 mg/mL, 0.0001 mg/mL, 0.001 mg/mL, 0.01 mg/mL, 0.1 mg/mL, and 1 mg/mL) and 20 µL of Ag(NH3)2OH (24 mM, diluted by milli-Q water) were sequentially added into milli-Q water to reach a final volume of 200 µL. The reaction was carried out at room temperature for 5 min and the absorbance of solution was measured at 410 nm by a microplate spectrophotometer (TECAN, Infinite 200 PRO). Glucose Detection In all experiments, 1 mL of NCC aqueous solution (10 mg/mL, in milli-Q water) was mixed with 1 mL of Ag(NH3)2OH (12 mM, diluted by milli-Q water) before use within 15 min. 20 µL of glucose and 20 µL of the mixture were sequentially added into milli-Q water to reach a final volume of 200 µL. The reaction was carried out at room temperature for 5 min. After the reaction, the absorbance of the solution was measured at 410 nm by a microplate spectrophotometer. To obtain the calibration curve, a series of glucose concentrations from 0 mM to 2 mM were tested. The UV/Vis spectra of the solution were measured, and the absorbance at 410 nm was recorded with the microplate spectrophotometer.


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To study the specificity of glucose assay, we tested some potentially interfering chemicals such as ascorbic acid, citrate acid, citrate sodium, cysteine, glutathione, peptone, and casein. The original concentrations of peptone and casein were 1 mg/mL, and that of other chemicals was 1 mM. 20 µL of each chemical or glucose (25 µM) was separately added into the solution which contained 20 µL of mixture of NCC (5 mg/mL) and Ag(NH3)2OH (6 mM) and 160 µL of milli-Q water. The reaction was carried out at room temperature for 5 min and the absorbance of the solution was measured at 410 nm. To study the effects of other positively charged ions on the glucose assay, we added 20 µL of NaNO3 water solution (concentrations ([NaNO3]): 0 mM, 31.25 mM, 62.5 mM, 125 mM, 250 mM, 500 mM, and 1000 mM) into the solution which contained 20 µL of mixture of NCC (5 mg/mL) and Ag(NH3)2OH (6 mM), 20 µL of glucose (25 µM) and 140 µL of milli-Q water. The reaction was carried out at room temperature for 5 min and the absorbance of the solution was measured at 410 nm. To detect glucose in human serum by the developed assay, we first prepare the samples by centrifuging the human blood at 3000 g for 10 min, followed by removing the cells and excessive ions in supernatant using a pre-treat ion extraction column (IC-Ag10, Cleaner IC-Ag, Agela Technologies). Cell culture and glucose detection in medium Mouse myoblast cells (C2C12) were obtained from American Type Culture Collection (ATCC, USA). C2C12 cells were cultured in Dulbecco’s Modified Eagle’s medium (DMEM) and supplemented with 10 % of fetal bovine serum (FBS) and 100 U/mL of penicillin/streptomycin at 37 oC in a humidified atmosphere of 5 % CO2. 100 µL of DMEM was


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collected from the petri dishes after cell culture for 24 h and 48 h. The collected DMEM was diluted by 100 times, followed by removing chloridion. 20 µL of treated DMEM was added into the solution which contained 20 µL of mixture of NCC (5 mg/mL), Ag(NH3)2OH (6 mM) and 160 µL of milli-Q water. The reaction was carried out at room temperature and the absorbance of the solution was measured at 410 nm. Antibacterial activity To obtain the calibration curve, a series of glucose concentrations from 0 mM to 2 mM were tested. The UV/Vis spectra of the solution were measured, and the absorbance at 410 nm was recorded with the microplate spectrophotometer. The AgNPs generated with the assistance of NCC for the antibacterial experiments were performed as follows. 50 µM of glucose, 0.5 mg/mL of NCC and 6 mM of silver ions were mixed and shaken thoroughly, to initiate the reaction for AgNPs generation at room temperature (25 oC) for 30 min. After reaction, the products were dialyzed against milli-Q water in dark for 24 h at room temperature. The concentration of the silver ions ([Ag+]) in AgNPs/NCC products was measured by Inductively Coupled Plasma optical emission spectroscopy (ICP-OES, Pekin-Elma, Optima 5300DV). Escherichia coli (E. coli), multi-drug resistance Escherichia coli (MDR E. coli), Staphyloccocus aureus (S. a) and Methicillin-resistant Staphylococcus aureus (MRSA) were selected as model Gram-negative and Gram-positive bacteria to study the antibacterial activity of generated AgNPs with NCC (AgNPs/NCC). Bacteria were cultured in the Luria-Bertani (LB) medium (10 g/L casein tryptone, 5 g/L yeast extract, and 10 g/L NaCl, pH: 7) at 37 oC on a shaker bed at 200 rpm. Ag+ of different concentrations (0 µg/mL-19.55 µg/mL, according to the ICP-OES result) was prepared in each sterilized ﬂask and inoculated with 1 × 106 CFU/mL bacteria suspension for 24 h. Minimum inhibitory concentration (MIC) in this work is defined as


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the minimum [Ag+] at which no bacterial turbid is observed in all three parallel experiments after co-culturing bacteria with AgNPs/NCC for 24 h.45 As the MIC is the [Ag+] which can inhibit the bacterial growth in all three parallels, there is no standard deviation of MIC data.46 The commercial AgNPs (Sigma-Aldrich, 0 µg/mL-23.96 µg/mL, according to the ICP-OES result) were used as control.

RESULTS AND DISCUSSION NCC-Assisted Generation of AgNPs We first investigate the generation of AgNPs from Tollen's reagent (Ag(NH3)2OH) using NCC as the substrate and glucose as the reducing agent. We prepare NCC by the previously reported method.13 The fabricated NCC has an average size of 10 nm wide and ~ 100 nm long (Figure 1D and Table S1). The water solution of NCC is transparent, with no characteristic absorbance from 300 to 700 nm measured by a UV2450 spectrophotometer (Figure S1). After mixing NCC solution with glucose and Ag(NH3)2OH, a visible color change from transparent to yellow is observed in a few minutes. The solution exhibits a characteristic absorption peak at 410 nm, indicating the production of AgNPs of surface plasmon resonance properties (Figure 2).37,47 To investigate the role of NCC for AgNPs generation in redox reaction, we use the following experimental parameters: 0.6 mM of silver ions, 0.1 mg/mL of NCC, 50 µM of glucose, and room temperature. The growth of AgNPs attached onto the surface of NCC is clearly observed (Figure 1E and Figure S2). We speculate that the negatively charged NCC could absorb Ag+ from Ag(NH3)2OH solution by electrostatic interactions, serving as the substrate to facilitate the nucleation of AgNPs in the presence of glucose.


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Figure 1. The NCC-assisted generation of AgNPs. (A) The schematic illustration and photograph of NCC (0.5 mg/mL) well dispersed in aqueous solution. (B) The schematic illustration and photograph of silver ions absorbed onto the surface of NCC based on electrostatic interactions after adding Ag(NH3)2OH solution (0.6 mM of silver ions) into NCC solution. (C) The schematic illustration and photograph of AgNPs generated from redox reaction between glucose (50 µM) and silver ions (0.6 mM). (D) TEM image of dispersed NCC (negative stained by uranyl acetate). (E) TEM image of generated AgNPs assisted by NCC at room temperature. The red arrow points to NCC, and the yellow arrow points to the generated AgNPs.

To systemically investigate the generation of AgNPs reduced from silver ions, we design an orthogonal assay including nine experiments for four parameters ([Ag+]: the concentration of silver ions, [NCC]: the concentration of NCC, [glucose]: the concentration of glucose, and temperature) with three levels (Table 1). The products from nine experiments are named as T1 to


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T9 (Table 1). The UV/Vis absorbance spectra and TEM images of T1 to T9 are shown in Figure 2. There is no absorbance at 410 nm for samples T3, T5, T7 and T9, neither the generated AgNPs from TEM images due to the lack of glucose or NCC (Table 1 and Figure 2). The UV/Vis absorbance of sample T1 at 410 nm is significant, and the solution appears to be dark yellow (Figure 2A). This phenomenon is attributed to a high concentration of silver ions (2.4 mM) which results in the production of a large amount of AgNPs (> 120 nm). The UV/Vis absorbance of T8 at 410 nm is negligible due to the small amount of generated AgNPs (~ 5 nm) at a low concentration of silver ions (0.15 mM). The absorption peak of T6 is shifted from 410 to 439 nm as a result of irregularly shaped AgNPs (Figure 2B and C). The AgNPs in T2 and T4 are ~ 25 nm in diameter with the absorption peak at 410 nm (Figure S3). These results indicate that we could fabricate AgNPs of different sizes by modulating the experimental parameters including [Ag+], [NCC], [glucose], and temperature.

Table 1. The design of orthogonal array and characterization of produced AgNPs. #

Ag+

NCC

Glucose

Temperature Mean

Standard

UV/Vis

(mM)

(mg/mL)

(µM)

(oC)

diameter

deviation

absorbance

(nm)

(SD)

at 410 nm

T1

2.4

5

500

25

126.1

59.6

1.34

T2

2.4

0.5

50

60

25.1

5.4

0.45

T3

2.4

0

0

90

/

/

0.014

T4

0.6

5

50

90

22.6

9.3

0.49

T5

0.6

0.5

0

25

/

/

0.053


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T6

0.6

0

500

60

51.7

11.6

0.33

T7

0.15

5

0

60

/

/

0.025

T8

0.15

0.5

500

90

5.6

5.7

0.093

T9

0.15

0

50

25

/

/

0.036

“/” indicates that no AgNPs are observed.

Figure 2. The fabrication of AgNPs under different experimental conditions listed in Table 1. (A) Photograph, (B) UV/Vis absorbance spectra, and (C) TEM images of samples (T1-T9) from orthogonal array.

As NCC shows a high negative surface charge that can enrich Ag+ from Ag(NH3)2OH, we next investigate if the existence of NCC could trigger the production of AgNPs at room temperature. We mix different concentrations of NCC ([NCC]: 0 mg/mL, 0.0001 mg/mL, 0.001


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mg/mL, 0.01 mg/mL, 0.1 mg/mL, 1 mg/mL) with 2.4 mM of silver ions and 50 µM of glucose. After reaction at room temperature for 5 min, we measure the absorbance of solution at 410 nm which is the characteristic signal of AgNPs (Figure 3). When [NCC] is lower than 0.1 mg/mL, the solution is transparent and the absorbance at 410 nm is below 0.25, indicating that no AgNPs are generated. With [NCC] increasing to 0.1 mg/mL or 1 mg/mL, the solution appears to be dark yellow, and the absorbance at 410 nm is above 0.35, revealing that AgNPs are reduced from Ag+ at room temperature. This might be due to the high local concentration of Ag+ around the well dispersed NCC of negative surface charge via electrostatic interactions, thus promoting the nucleation of AgNPs with NCC serving as the substrate.47, 48 Previous investigations also prove that the negatively charged nanomaterials such as AuNRs could facilitate the generation of AgNPs at a high temperature by increasing the local concertation of Ag+.47 In our study, nanorod-shaped NCC of higher negative surface charge (zeta potential ~ - 46 mV) could attract more Ag+ than AuNRs, leading to the production of AgNPs at room temperature.


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Figure 3. The generation of AgNPs from Ag+ at room temperature with the assistance of NCC at different concentrations ranging from 0 mg/mL to 1 mg/mL. The concentrations of Ag+ and glucose are 2.4 mM and 50 µM. (A) Photograph, and (B) UV/Vis absorbance at 410 nm of solutions after 5-min reaction at room temperature. The error bars represent the standard deviation of three replicate measurements (SD, n=3).

Colorimetric Glucose Assay We next develop a colorimetric, quantitative and non-enzymatic glucose assay based on the NCC-assisted generation of AgNPs. The solution of generated AgNPs exhibits a yellow color with a characteristic absorbance at 410 nm, the intensity of which is related to the concentration of glucose.49 The optimal [NCC] and [Ag+] are determined by an orthogonal array with [NCC] ranging from 0.05 mg/mL to 2 mg/mL, [Ag+] from 0.24 mM to 2.4 mM, and [glucose] of 50 µM (Figure 4). After a 5-min reaction at room temperature, we find that the absorbance at 410 nm has a maximum value for [NCC] of 0.5 mg/mL and [Ag+] of 0.6 mM (Figure 4B). These parameters are adapted for the following glucose detection.


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Figure 4. The optimization of concentrations of NCC and Ag+ for glucose detection. (A) Photograph, and (B) the absorbance at 410 nm of solutions after 5-min reaction at room temperature with different concentrations of NCC and glucose.

To evaluate the sensitivity and linear range of this glucose assay, we spike different concentrations of glucose into solution composed of 0.5 mg/mL of NCC and 0.6 mM of Ag(NH3)2OH. After a 5-min reaction at room temperature, the color of solution changes gradually from transparent to dark yellow with the increased [glucose] from 0 µM to 25 µM, which could be discriminated by naked eyes (Figure 5A). The absorption of solution at 410 nm indicates a good linear response (R2=0.998) for different concentrations of glucose from 0 µM to 35 µM (Figure 5). The limit of detection of this assay is 0.116 µM according to the equation: 3×SD(0)+Abs(0), in which SD(0) is the standard deviation of absorption of blank sample, and Abs(0) is the absorption value of blank sample.


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Figure 5. The sensitivity and linear range of glucose detection by NCC-assisted generation of AgNPs. (A) Photographs of different concentrations of glucose in milli-Q water after 5 min reaction. (B) Characterization curve for glucose detection (absorbance at 410 nm), and the linear fit for glucose concentration from 0 µM to 35 µM (absorbance at 410 nm, insert). (C) The UV/Vis spectra of various concentrations of glucose from 0 µM to 25 µM. The error bars represent the standard deviation of three replicate measurements (SD, n=3).

We next investigate the effects of potentially interfering substances (including ascorbic acid, citrate acid, citrate sodium, cysteine, glutathione, peptone, casein) on glucose detection. The concentrations of peptone and casein are 0.1 mg/mL, and those of other chemicals are 100 mM. We find that ascorbic acid yields a detectable signal at 410 nm, the intensity of which is 25 % of that from 25 µM of glucose, indicating that ascorbic acid may potentially affect the readout of glucose detection (Figure 6). However, the concentration of glucose in human whole blood is ~ 50 times higher than that of ascorbic acid, and thus the influence of ascorbic acid is negligible.47 In addition, peptone or casein of high concentration (0.1 mg/mL) does not result in the absorbance at 410 nm. We also investigate the effects of positively charged cations such as


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Na+ that may compete with Ag+ for absorption onto the surface of NCC. Na+ with a highest concentration of 100 mM cannot interfere the absorption of solution (composed of 0.5 mg/mL of NCC, 0.6 mM of Ag+, and 25 µM of glucose) at 410 nm (Figure 6B). These investigations indicate that the developed assay is suitable for assaying glucose in human blood samples.

Figure 6. The effects of potentially interfering substances on glucose detection. (A) The absorbance of ascorbic acid, citrate acid, citrate sodium, cysteine, glutathione, peptone, casein at 410 nm. (B) The absorbance of NaNO3 at 410 nm. The original solution contains 0.5 mg/mL of NCC, 0.6 mM of Ag+, and 25 µM of glucose. The error bars represent the standard deviation of three replicate measurements (SD, n=3).

The developed assay is used for glucose detection in human serum. The measured concentrations of glucose in two human blood samples are 5.511 mM and 4.810 mM by our method, and 5.5 mM and 4.7 mM by ACCU-CHEK (Roche). Compared with ACCU-CHEK, our assay exhibits a lower limit of detection and a wider detective range, without the using of any enzyme (Table 2). In addition, our methods allows for room temperature detection, while many other nanomaterials-based glucose detections require a high temperature to initiate the reaction. 47


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Table 2. Comparison of commercially available method (ACCU-CHEK) and the nonenzyme glucose detection based on AuNRs or NCC.

ACCU-CHEK AuNRs 47 NCC

Linear range

Enzyme

Temperature

0.6 mM–33.33 mM

Yes

25 oC

0.07 µM–4 µM

No

80 oC

0.116 µM–0.4 mM

No

25 oC

We also use this NCC-based assay to monitor the change of [glucose] in DMEM medium during the culture of mouse myoblast cells, C2C12. This type of assay is critical for many processes of biomanufacturing, such as cell culture and microbial fermentation. The measured [glucose] in DMEM by our assay decreases from 24.6 mM to 18.4 mM after culturing C2C12 cells for two days, while the commercial glucose kit (Sigma) shows the similar result (Figure 7). For measuring 25 mM of glucose in fresh DMEM, our method and commercial kit yield the [glucose] of 24.6 mM and 23.9 mM, respectively. These assays indicate that the developed method could detect [glucose] in different settings.

Figure 7. The concentrations of glucose in fresh DMEM medium (marked with 0) and in


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DMEM after culturing C2C12 cells for 1 and 2 days. [Glucose] in DMEM is measured by our assay (AgNPs/NCC) and the commercial glucose kit (Commercial Kit). The error bars represent the standard deviation of three replicate measurements (SD, n=3).

Antibacterial Activity The antibacterial activity of AgNPs generated with the assistance of NCC (AgNPs/NCC) is evaluated, and compared with commercial AgNPs (Sigma-Aldrich). To determine the MIC, we select E. coli, multi-drug resistance MDR E. coli, S. a and MRSA as model Gram-negative and Gram-positive bacteria. AgNPs/NCC exhibits a lower MIC for both Gram-negative and Gram-positive bacteria than commercial AgNPs (Figure 8). The MIC for MRSA decreases from 1.50 µg/mL of Ag+ in commercial AgNPs to 0.16 µg/mL of Ag+ in AgNPs/NCC. The enhanced antibacterial activity of AgNPs/NCC is attributed to the good dispersion of AgNPs with the presence of NCC. The stability/diversity of AgNPs/NCC or AgNPs in physiological condition (LB culture medium) is evaluated using the UV/Vis absorbance spectra and the sedimentation experiments (Figure S4). We first added 200 µL of AgNPs/NCC (40 µg/mL) or 150 µL of commercial AgNPs (47 µg/mL) into 200 µL of LB culture medium at room temperature, and allowed the solution to stand for 5 h at room temperature. The UV/Vis absorbance of AgNPs/NCC in LB culture medium is peaked at 410 nm, revealing the good dispersion of AgNPs (Figure 2B and Figure 5C). Moreover, no sedimentation of nanoparticles is observed by naked eyes (Figure S4). In comparison, the sedimentation of commercial AgNPs in LB culture medium after 5 h is significant (Figure S4, pointed by the red arrow), so that no absorbance at 410 nm is detected. This experiment indicates that the stability/dispersity of AgNPs/NCC in physiological condition is much better than that of commercial AgNPs. We should note that


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previous study has prepared AgNPs using nano-wood materials as both the reducing and supporting agents at 100 °C. The obtained AgNPs exhibited sustained antibacterial activity against the model bacteria E. coli.42 In this study, we could fabricate AgNPs/NCC at room temperature, which show antibacterial activity against both Gram-negative and Gram-positive bacteria.

Figure 8. The MIC of the AgNPs/NCC and commercial AgNPs. AgNPs/NCC exhibits a lower MIC for both Gram-negative and Gram-positive bacteria in comparison with the commercial AgNPs.

CONCLUSION In this work, we employ NCC to facilitate the synthesis of AgNPs with different sizes from the redox reaction between Ag+ and glucose at room temperature, by exploiting the large surface-to-volume ratio and negatively charged surface of NCC. Based on the NCC-assisted generation of AgNPs, we develop a colorimetric and non-enzymatic assay for glucose detection


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at room temperature, with a low limit of detection of 0.116 µM, and a wide linear range from 0.116 µM to 0.4 mM. This glucose assay is further applied for monitoring the concentration change of glucose in medium during cell culture. The AgNPs/NCC also exhibits an enhanced antibacterial activity for both Gram-negative and Gram-positive bacteria in comparison with the commercial AgNPs, attributed to the good dispersion of AgNPs with the presence of NCC. NCC-based generation of AgNPs thus shows great promise in a variety of applications such as clinical diagnosis, biomanufacturing, and antibacterial action.

ASSOCIATED CONTENT Supporting Information. This material is available free of charge via the Internet at http://pubs.acs.org. Details about the properties of NCC (Table S1) and characterizations of AgNPs/NCC and AgNPs (Figures S1-S4). AUTHOR INFORMATION Corresponding Author X. Jiang, [email protected], J. Sun, [email protected], X. Li, [email protected] ACKNOWLEDGMENT We acknowledge financial support from MOST (2013AA032204, and 2013YQ190467), NSFC (21475028, 21025520, and 51073045), and the Independent Innovation and Achievement Transformation Project in Shandong Province (2014CGZH0303). REFERENCES


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