Effect of surface modification on the peroxidase-like behaviors of carbon dots

Colloids and Surfaces B: Biointerfaces 178 (2019) 163–169

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Effect of surface modification on the peroxidase-like behaviors of carbon dots

T

⁎

Jing Shia, Tianxiang Yina, , Weiguo Shena,b a b

School of Chemistry and Molecular Engineering, East China University of Science and Technology, Shanghai 200237, China Department of Chemistry, Lanzhou University, Lanzhou, Gansu 730000, China

A R T I C LE I N FO

A B S T R A C T

Keywords: Nanoenzyme Peroxidase Carbon dots

Carbon dots (CDs) have drawn much attention in recent decades due to their outstanding biocompatibility and environmental friendliness. In this work, the surface modifications of peroxidase-like carbon dots were carried out to show the influence of surface structure on the catalytic activity. Poly(ethyleneimine) and citric acid modified CDs, i.e. PEI-CDs and CA-CDs, were obtained and used in the catalytic oxidation of two different substrates 3,3',5,5'-tetramethylbenzidine (TMB) and 2,2'-azino-bis(3-ethylbenzothiazoline-6-sulfonic acid) (ABTS). The catalytic activity of CA-CDs for TMB is greater than that of unmodified CDs while the catalytic activity of PEI-CDs for ABTS is greater than that of unmodified CDs. These results may be ascribed to that TMB shows stronger affinity to negatively charged CA-CDs and ABTS shows stronger affinity to positively charged PEI-CDs. These results clearly suggested that the surface charge plays an important role in the catalytic activity of nanoenzyme. Furthermore, the mechanism of peroxidase-like activity of all CDs was investigated and both the generation of hydroxyl radical and enhanced electron transfer were involved in the catalytic process.

1. Introduction Increasing attention has been paid to artificial nanoenzymes and their potential applications since the discovery by Yan and coworkers that iron oxide magnetic nanoparticles showed intrinsic peroxidase-like activity similar to that of natural enzyme [1]. Different kinds of nanomaterials, including V2O5 nanowires [2], Co3O4 nanoparticles [3], CuO nanoparticles [4], MnO2 nanoparticles [5], gold nanoparticles [6], single-wall carbon nanotube [7], graphene oxide [8], Co,N-co-doped porous carbon hydird [9], Fe NPs@Co3O4 hollow nanocage [10], MOFs [11] have been reported to display enzyme-like properties and show potential use in bioanalysis [12–18] and environmental chemistry [19,20]. Comparing with natural enzymes, nanoenzymes possess some advantages, including simple preparation process, low cost, tunable catalytic activity and high stability under stringent conditions et.al. Different researches have been reported to tune the catalytic performance of nanoenzyme by combination with other metals to form hybrid materials like Au@Pt, GO-Fe3O4 or modification of nanoenzymes’ surface [21–27]. Carbon dots (CDs), a new class of nanoenzyme, have drawn much attention due to their easy preparation, chemical inertness, resistant photobleaching, fantastic biocompatibility, low cytotoxicity and environmental-friendliness. Different kinds of carbon dots as well as their ⁎

hybrid materials with metals have been reported in recent years [28–36], whose outstanding properties make them shown great potential for applications in fields like sensors, bio-imaging, and catalysis, et.al. In this work, poly(ethyleneimine) modified CDs (PEI-CDs) and citric acid modified CDs (CA-CDs) were synthesized to show the effect of surface properties on the catalytic activity of CDs. The morphology and surface structure were characterized by transmission electron microscopy (TEM), Fourier transform infrared spectroscopy (FT-IR), X-ray photoelectron spectroscopy (XPS), and zeta potential measurements. The peroxidase like activities of the PEI-CDs and CA-CDs were investigated by catalytic oxidation of 3,3',5,5'-tetramethylbenzidine (TMB) and 2,2'-azino-bis(3-ethylbenzothiazoline -6-sulfonic acid) (ABTS) in the presence of H2O2. Furthermore, catalytic mechanisms of these CDs were studied by means of electron-spin resonance experiment and measurements of electrochemical properties. 2. Experimental section 2.1. Materials Citric acid (≥99.5 wt%), thiourea (≥99 wt%), potassium dihydrogen phosphate (≥99 wt%) and disodium hydrogen phosphate (≥99 wt%) were purchased from Shanghai Runjie Chemical Reagent

Corresponding author. E-mail address: [email protected] (T. Yin).

https://doi.org/10.1016/j.colsurfb.2019.03.012 Received 12 October 2018; Received in revised form 4 March 2019; Accepted 5 March 2019 Available online 06 March 2019 0927-7765/ © 2019 Elsevier B.V. All rights reserved.

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2.4. Measurement of peroxidase-like activity

Co.,Ltd. N-hydroxysuccinimide (NHS, 98 wt%), 2,2'-azino-bis(3-ethylbenzothiazoline-6-sulfonic acid) (ABTS, 98 wt%) and 3,3',5,5'Tetramethylbenzidine (TMB, 98 wt%) were supplied by Aladdin. 1Ethyl-3-(3-dimethylaminopropyl) carbodiimide hydrochloride (EDC, 99 wt%) were acquired from J&K Scientific Ltd. Hydrogen peroxide (H2O2, 30 wt%) was obtained from Chinasun Specialty Products Co., Ltd. All reagents were used directly without further purification, and all aqueous solutions were prepared with ultrapure water (18.2 MΩ).

The peroxidase-like activities of the all synthesized nanoenzymes (CDs, CA-CDs, and PEI-CDs) were carried out by the catalytic oxidation of chromogenic substrate (TMB or ABTS) in the presence of H2O2. Typically, a certain amount of chromogenic substrate, H2O2, and the CDs solution were mixed in citrate-phosphate (0.2 M) buffer solution at a certain pH and temperature. The reaction was monitored by recording the absorbance at 652 nm belonged to the oxidation product of TMB (Fig. S1) or at 416 nm belonged to the oxidation product of ABTS (Fig. S2) using UV–vis spectrophotometer. The apparent steady-state kinetic analysis were carried out by using nanoenzyme (1.78 mg L−1) in citrate-phosphate buffer solution (pH 4.0, 0.2 M) at various concentrations of chromogenic substrate and a series of fixed H2O2 concentrations at temperature of 40 ℃. The concentration of TMB-derived or ABTS-derived oxidation product was calculated by the Lambert-Beer Law using a molar absorption coeficient of 39,000 M -1 cm−1 for TMBderived [38] or 36,000 M -1 cm−1 for ABTS-derived [39] oxidation products. Apparent steady-state reaction rates v at different concentrations of substrate were obtained by calculating the slopes of initial absorbance changes with time (A sample of calculation of reaction rate v was shown in Fig. S3 of supporting information).

2.2. Preparation of CDs Unmodified carbon dots: The CDs were firstly synthesized according to a hydrothermal process reported by Zheng et. al [35]. Briefly, 0.630 g citric acid and 0.171 g thiourea were dissolved in 15 ml water, and thereafter the solution was transferred into a hydrothermal autoclave (45 ml), which was heated at a temperature of 180 ℃ for 5 h. The autoclave was cooled down naturally after the reaction. The obtained solution was centrifuged at 13,000 rpm for 20 min to remove the large particles. The transparent CDs solution was stored at 4 ℃ for further use. Poly(ethyleneimine)-modified carbon dots (PEI-CDs): For the preparation of PEI functionalized CDs, PEI (Mw = 1.8 K Da) were chemically bonded on the surface of the as-prepared CDs in the former process by a condensation reaction to obtain PEI-CDs [37]. In a typical procedure for the preparation of PEI-CDs, 6 ml as-prepared CDs in PBS solution was mixed with EDC/NHS (0.99 g/0.60 g) in a 30 ml flask. After stirred for 1 h, 3 ml PBS solution of PEI was injected into the flask. The obtained mixture was kept stirring for 12 h in the dark. Then, it was dialyzed against water for 72 h by using a dialysis bag (3000 Da) to remove residual unreacted molecules. Citric acid-modified carbon dots (CA-CDs): 6 ml citric acid in PBS solution was mixed with EDC/NHS (0.99 g/0.60 g) in a 30 ml flask. After stirring for 1 h, another 3 ml PBS solution of CDs was injected into the flask. The resulting mixture was kept stirring for 12 h in the dark. Then, it was dialyzed against water for 72 h by using a dialysis bag (200 Da) to remove any molecular residual.

2.5. Electron-spin resonance experiment Electron spin resonance (ESR) experiments were performed on EMX-8/2.7 spectrometer (Bruker, Germany) at room temperature. The samples were put in glass capillary tubes and the tubes were inserted into the ESR cavity. ESR parameters settings in the detection of spin adducts using spin trap DMPO were as follows: modulation amplitude 1 G, scan range 3420–3620 G, microwave power 6.4 mW and time constant 163.84 ms. All samples contain DMPO (50 mM), H2O2 (200 mM) and nanoenzymes (CDs) (8.9 mg L−1) in citrate-phosphate buffer solution (pH = 4.0). 2.6. Electrochemical properties The electrochemical properties of CDs were conducted on the CHI 660B electrochemical workstation (ChenHua, China). A typical threeelectrode system was applied, where a saturated calomel electrode was used as reference electrode and a platinum wire was used as auxiliary electrode. A glassy carbon electrode (GCE) was used as working electrode, which was polished by 0.3 mm and 0.05 mm alumina slurry and thus washed by ultrapure water. A drop of CDs solution was added on the surface of GCE and the GCE was air-dried at room temperature to generate modified GCE. In a typical experiment, with the potential being fixed at −1.4 V, the current-time curve was recorded by alternately adding 20 mM H2O2 with an interval of 40 s.

2.3. Characterization of CDs UV-vis absorption spectra of the obtained CDs were recorded by means of a UV2450 spectrophotometer (Hitachi, Japan). The high-resolution transmission electron microscopy (HRTEM) images of CDs were determined using a JEOL-2010 electron microscope (JEOL, Japan) operating at 200 kV. The Fourier transform infrared (FT-IR) spectra of CDs were recorded in the range of 500–4000 cm−1 using a NICOLET iS10 (Thermo Fisher, America) spectrometer to determine the functional groups on the surface of CDs. The X-ray photoelectron spectroscopy (XPS) spectra of the CDs were performed by ESCALAB 250 spectrometer (Thermo Fisher, America) to analysize the surface elemental composition. Zeta potential of CDs in citrate-phosphate buffer (pH = 4.0) was measured to show the surface charge by Malvern Zetasizer NanoZS instrument (Southborough, MA) equipped with a laser Doppler velocimeter at T = 298.15 K using a folded capillary cell with gold electrode as sample cell.

3. Results and discussions 3.1. Characterization of CDs The morphology and structure of the CDs, CA-CDs and PEI-CDs were

Fig. 1. HRTEM images of the (a) CDs, (b) CA-CDs, and (c) PEI-CDs. 164

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Fig. 2. (a) The FT-IR spectra of CA, CDs and CA-CDs. (b) The FT-IR spectra of PEI, CDs and PEI-CDs. Fig. 3. (a) Time-dependent absorbance changes at 652 nm of TMB in different reaction system: (1) TMB/H2O2, (2) PEI/TMB/H2O2 (0.67 mg ml−1 PEI), (3) CA/TMB/H2O2 (1.4 mg ml-1 CA), (4) CA-CDs/TMB/H2O2 (1.78 mg ml-1 CA-CDs), (5) PEI-CDs/TMB/ H2O2 (1.78 mg ml-1 PEI-CDs), (6) CA-CDs/TMB (1.78 mg ml-1 CA-CDs), (7) PEI-CDs/TMB (1.78 mg ml-1 PEI-CDs) and (8) CDs/TMB/ H2O2 (1.78 mg ml−1 CDs). (b) Photos of different reaction systems 1–8. Time-dependent absorbance change at 652 nm of oxide-TMB (black curve) and at 416 nm of oxide-ABTS containing nanoenzyme CDs (c), CA-CDs (d) and PEI-CDs (e). All the experiments are conducted at pH = 4.0 and T = 30 ℃.

Fig. 4. The effect of pH (a and c) and temperature (b and d) on the catalytic activity of the CA-CDs and PEI-CDs with TMB and ABTS as substrates.

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Fig. 5. The steady-state kinetic assay of the CA-CDs (a) and PEI-CDs (b) with concentration of H2O2 fixed at 267 mM and that of TMB or ABTS was varied. (c) to (f) Lineweaver-Burk plots at a series of H2O2 concentration. (g) to (j) plots of the obtained intercepts in plots (c) to (f) against H2O2 concentration.

The surface structure of CA-CDs and PEI-CDs was investigated by Fourier transform infrared (FT-IR). As shown in Fig. 2a, The FT-IR spectrum of CA-CDs displays a broad peak at 3211 cm−1 which is attributed to the stretching vibration of eOH. Moreover, compared with the FT-IR spectra of citric acid and CDs, the FT-IR spectrum of CA-CDs exhibited a strong peak at 1572 cm-1 (attributed to the bending

studied by high-resolution transmission electron microscopy (HRTEM). It is found from Fig. 1a and b that the CDs and CA-CDs exhibited excellent mono-dispersed spherical structures with an average diameter of 3.8 ± 0.4 nm and 5.0 ± 0.9 nm, respectively. However, PEI-CDs exhibited irregular shape with apparent size being about 13.6 ± 2.6 nm (Fig. 1c). 166

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absorbance at 652 nm is caused by peroxidase-like activity of CA-CDs, PEI-CDs or CDs. Moreover, the absorbance at 652 nm in PEI-CDs/TMB/ H2O2 system is much weaker than that of CA-CDs/TMB/H2O2 system at the same reaction time. This may be ascribed to the fact that TMB contains two amino groups which likely results in stronger affinity to a negatively charged CA-CDs surface. Therefore, the CA-CDs showed higher catalytic activity toward oxidation of TMB in the presence of H2O2 than that of PEI-CDs. In order to further confirm this speculation, another substrate ABTS, containing two sulfonic acid group and showing higher affinity to a positively charged surface, was used in the catalytic oxidation reaction. As shown in Fig. 3d and e, the catalytic activity of CA-CDs with TMB (black curve) as reaction substrate was higher than that of ABTS (red curve), while the opposite occurred for PEI-CDs. However, compared with CA-CDs and PEI-CDs, CDs showed similar catalytic activity toward oxidation of TMB and ABTS in the presence of H2O2 as shown in Fig. 3c, which may be ascribed to that the Zeta potential of CDs is close to zero (0.5 mV), i.e. CDs are nearly neutral. These results indicate that the peroxidase-like activity of CDs varies with the surface modification. Cationic amino-modified CDs (PEI-CDs) show weak catalytic activity toward TMB due to their low affinity toward the positively charged substrate. In contrast, citratecapped CDs (CA-CDs), which are negatively charged, tend to attract amino groups of TMB electrostatically and show strong catalytic activity toward TMB. It is generally accepted that pH and temperature are important factors to influence the catalytic activity of natural enzyme. Therefore, we first investigated the effect of pH and temperature on the catalytic activity of CA-CDs and PEI-CDs based on the relative activity Ai /Am, where Ai is the absorbance at 652 nm for TMB (or 416 nm for ABTS) at different reaction conditions and Am is the maximum one. The plots of Ai/Am against pH and temperature are displayed in Fig. 4. It's noteworthy that the effect of pH and temperature on the catalytic activity of PEI-CDs (CA-CDs) on the oxidation of TMB and ABTS was similar. The results suggest that the optimal experimental conditions of CA-CDs and PEI-CDs are pH of 4.0 and temperature of 40 ℃. Moreover, the resistance of CA-CDs on the change of pH and temperature is better than that of PEI-CDs. The relative activity is higher than 60% in the whole studied temperature range for CA-CDs, much higher than HRP (5% at 55 ℃), which indicates good stability of CA-CDs. In order to shed deeper insight on the catalytic oxidation, quantitative steady-state kinetic analysis with Michaelis-Menten equation is conducted:

Table 1 Michaelis-Menten parameters of K mTMB (or K mABTS ), and vmax. Nanoenzyme

a

CDs PEI-CDs CA-CDs a

TMB

ABTS

TMB Km (mmol/L)

vmax (10−8 M/s)

ABTS Km (mmol/L)

vmax (10−8 M/s)

0.470 0.957 0.152

4.72 3.54 4.90

0.685 0.198 0.708

4.34 5.99 4.16

experimental results for CDs are shown in supporting information (Fig. S6).

vibration of NeH bonds) and a weak peak at 1643 cm-1 (attributed to the stretching vibrations of amide C]O [40,41], suggesting successful amidation on the surface of CA-CDs. The FT-IR spectrum of PEI-CDs (Fig. 2b) shows a peak at 1643 cm −1 which can be ascribed to the stretching vibrations of amide C]O of the PEI-CDs, and the strong peak at 1563 cm-1 was assigned to the bending vibration of N−H bonds, indicating successful amidation on the surface of PEI-CDs. The composites of PEI-CDs, CA-CDs and CDs were further explored by XPS. As shown in Fig. S4, the CDs (Fig. S4a), PEI-CDs (Fig. S4b) and CA-CDs (Fig. S4c) are composed of carbon, nitrogen and oxygen elements. It can be seen from Fig. S4d, S4e and S4f that three main peaks at 284.8, 285.9 and 288.5 eV are presented in the fine structure spectra of C1s, which are attributed to graphitic, nitrous and oxygenated carbon atoms, respectively [42]. The two peaks for N1s (Fig. S4g, S4h and S4i) are ascribed to two kinds of N atoms in amide group and amine one [43]. The fine spectra of O1s shown in Fig. S4j, k, and l displayed two peaks belonged to the CeO and C]O [43]. The content of each element is given in Table S1. It is clearly shown that the content of N in PEI-CDs is greater than that of CDs while the content of O in CA-CDs is greater than that of CDs. Therefore, it is appropriate to speculate from the above results that PEI and CA are chemically bonded on the surface of CDs through amidation reaction, which is consistent with HRTEM and FT-IR measurements. In addition, zeta potential of PEI-CDs and CA-CDs in citrate-phosphate buffer (pH = 4.0) were determined to be 12.7 mV and −10.8 mV, respectively, which further supported that PEI and CA were successfully bound on CDs. 3.2. Peroxidase-like activity and kinetic analysis of PEI-CDs and CA-CDs The peroxidase-like behaviors of the CA-CDs and PEI-CDs were examined by using 3,3’,5,5’-tetramethylbenzidine (TMB) and 2,2’-azinobis(3-ethyl -benzothiazoline-6-sulfonic acid) diammonium salt (ABTS) as chromogenic substrates. A series of control experiments were carried out to investigate the enzymic activity of CA-CDs and PEI-CDs as shown in Fig. 3a. It is clearly suggested that only mixed solutions of TMB, H2O2 and CA-CDs (or PEI-CDs or CDs) show blue color (bottles No. 4, 5, and 8 in Fig. 3b). For systems of CA-CDs/TMB/H2O2 (black curve), PEI-CDs/ TMB/ H2O2 (green curve) or CDs/TMB/H2O2 (red curve), the absorbance at maximum wavelength of 652 nm is increased with time as shown in Fig. 3a. The above results indicate that the change of

v=

vmax [S ][H2 O2] K mS [H2 O2] + K mH2O2 [S ] + [S ][H2 O2]

(1)

where Michealis constant Km is an indicator of the affinity of enzyme with the substrate and S refers to the substrate TMB or ABTS. Under the optimal condition (pH = 4.0 and T = 40 ℃), steady-state kinetics experiments were performed by changing one substrate concentration with that of the other substrate being fixed. Typical curves obtained at a fixed H2O2 concentration (267 mM) and at various TMB/ABTS concentrations are shown in Fig. 5a and b. The curves at other H2O2 concentrations are displayed in supporting information (Fig. S5).

Fig. 6. DMPO spin-trapping ESR spectra in PBS solution (pH 4.0) in the presence of CDs (a), CA-CDs (b) and PEI-CDs (c) with H2O2 (200 mM) and DMPO (50 mM). 167

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Fig. 7. Current—time curves of bared GCE system (black line) and CDs-modified systems (red line) in buffer solution (pH = 4) with alternately addition of H2O2: (a) CDs, (b) CACDs, and (c) PEI-CDs.

KS

1

1

K H2 O2

1

4. Conclusions

1

× [H O ] + v ) at a Lineweaver-Burk plots ( v = v m × [S] + vm max max 2 2 max series of fixed H2O2 concentration with different substrates and nanoenzymes are presented in Fig. 5c–f, where the parallel lines clearly indicate the ping-pang mechanism of the catalytic oxidation of TMB/ ABTS by CA-CDs/PEI-CDs [1,44,45]. Further plots of the obtained inK H2 O2

1

To sum up, in this work, poly(ethyleneimine) (PEI) and citric acid (CA) modified CDs, i.e. PEI-CDs and CA-CDs, were synthesized by using a simple method. The peroxidase-like activities of PEI-CDs and CA-CDs are explored and were found to be dependent on the surface charge of modified nanoparticles. The catalytic activity of CDs was similar toward TMB and ABTS in the presence of H2O2. However, since CA-CDs showed higher affinity than PEI-CDs toward TMB, CA-CDs exhibited greater catalytic activity in TMB/H2O2 system. Conversely, PEI-CDs presented high affinity toward ABTS and thus showed enhanced catalytic activity with ABTS as substrate. Moreover, the catalytic activity of CA-CDs in TMB system and that of PEI-CDs in ABTS system are both better than the corresponding behavior of unmodified CDs. The peroxidase-like catalytic mechanism of PEI-CDs and CA-CDs could be ascribed to the dual contributions from generation of hydroxyl radical and the promotion of electron transfer by PEI-CDs/CA-CDs during the catalytic procedure. The results presented herein suggest that surface modification is an effective way to tune the catalytic activity of nanoenzymes. Besides, the results also indicate that CDs based nanoenzymes may have potential applications in harsh environments, for instance, determination of H2O2 in acid rain, due to their good stabilities in relative high temperature and low pH.

1

× [H O ] + v ) against H2O2 concentration, showing in tercepts ( vm max 2 2 max Fig. 5g–j, give the values of K m , and vmax, which are presented in Table 1. A comparison of the kinetic parameters of PEI-CDs and CA-CDs with CDs listed in Table 1 demonstrates that the CA-CDs display better affinity to TMB than that of PEI-CDs while PEI-CDs display better affinity to ABTS than that of CA-CDs. This is due to that TMB is more leaning to a negatively charged surface (CA-CDs) while a positive charged surface (PEI-CDs) is more favorable for ABTS. However, the Michaelis-Menten parameters of unmodified CDs for TMB and ABTS are much closer, which suggested their similar catalytic activity toward oxidation of TMB and ABTS.

3.3. Mechanism of peroxidase-like activity of PEI-CDs and CA-CDs Although complicated, the surface properties may influence the catalytic behavior of nanoparticles. For instance, it has been shown by Huang et al. that the chitosan coated Ag NPs showed peroxidase-like behavior while citrate coated Ag NPs displayed no catalytic activity for TMB because it cannot decompose H2O2 into %OH. [46] However, results reported by Yang et al. [27]. suggested that different types of coating structures for iron oxide nanoparticles all showed peroxidaselike behaviors for both TMB and ABTS with various catalytic activity. Generally, the peroxidase-like catalytic mechanism of nanoenzymes can be ascribed to different contributions such as generation of reactive oxygen species like •OH, enhanced electron transfer process etc [44,47]. In this work, combination of spin trapping technique and electron spin resonance (ESR) spectroscopy was used to probe hydroxyl radical in the enzyme catalysis process. DMPO was used as spin trap material that reacts with %OH to generate the stable DMPO/%OH spin adduct, which has a typical four lines ESR spectrum with relative intensity being 1:2:2:1. As shown in Fig. 6, the presence of typical spectrum of DMPO/%OH spin adduct suggests that the generation of hydroxyl radical is involved in the catalytic oxidation of substrates TMB or ABTS by nanoenzymes CDs, CA-CDs or PEI-CDs. In addition, we further conducted amperometric measurements to investigate the electron transfer performance in the catalytic process. The obtained current—time curve is shown in Fig. 7. A sharp increase of reduction current followed by a plateau is clearly shown when a certain amount of H2O2 was added with modified GCE being used as working electrode. However, almost no change occurs when bare GCE was used. This may suggest that the electron transfer between the electrode and H2O2 is greatly enhanced with the help of CDs. Therefore, we may speculate that both the generation of hydroxyl radical and the promotion of the electron transfer process may be involved in the catalysis mechanism for CDs, PEI-CDs, and CA-CDs, i.e. surface modifications didn’t change the catalytic mechanism of CDs.

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