, TiO 2 and NiO x modified electrode. The SOD-based O 2 biosensors based on. Yan Yang, Jiawan Zhou, Liang Wu, Xiaohua Zhang & Jinhua Chen*
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1 Indian Journal of Chemistry Vol. 51A, August 2012, pp A superoxide anion electrochemical sensor based on the direct electrochemistry of superoxide dismutase assembled layer-by-layer at the L-cysteine modified gold electrode Yan Yang, Jiawan Zhou, Liang Wu, Xiaohua Zhang & Jinhua Chen* State Key Laboratory of Chemo/Biosensing and Chemometrics, College of Chemistry and Chemical Engineering, Hunan University, Changsha, , PR China chenjinhua@hnu.edu.cn Received 1 May 2012; revised and accepted 16 July 2012 A superoxide anion (O 2 ) biosensor has been developed based on layer-by-layer assembled poly-(diallyldimethylammonium) (PDDA) and superoxide dismutase (SOD) on the L-cysteine (Cys) modified gold (Au) electrode. In 25 mm phosphate buffer solution (ph 7.2), the {SOD/PDDA} n /Cys/Au electrode shows a pair of well-defined and nearly reversible peak at ~ 84 mv vs SCE, confirming the direct electrochemistry of SOD. Based on the bifunctional enzymatic catalytic activities of SOD to the oxidation and reduction of O 2, the developed {SOD/PDDA} 5 /Cys/Au electrode exhibits good analytical characteristics in the detection of O 2, such as low detection limit, good stability, reproducibility, selectivity and particularly a wide linear range (0.5 ~ 546 µm). Keywords: Superoxide anion, Superoxide dismutase, Electrochemistry, Poly-(diallyldimethylammonium), Sensors, Modified electrodes, Layer-by-layer assembly Superoxide anion (O 2 ) is the primary species of reactive oxygen species (ROS) related to the damage of proteins, DNA, and lipids in the human body 1,2. The detection of O 2 has become very important in disease diagnosis and management. On the other hand, superoxide dismutase (SOD) is a very important redox protein in aerobic organisms 3, which is involved in cell protection mechanisms against oxidative damage from O 2. It is well-known that SOD protects the organism against oxidative damage by specifically catalyzing the dismutation of O 2 to H 2 O 2 and O 2, which is often used to determine O 2 (Refs 4 6). In the last decade, considerable attention has been paid to direct electrochemistry of copper, zinc-superoxide dismutase (Cu, Zn-SOD) and related O 2 biosensors. For example, Tian et al. 7-9 have systematically studied the direct electron transfer of SOD with self-assembled monolayer (SAM) confined on a gold electrode. Based on the biocompatible microenvironment of the thin silica and sodium alginate sol-gel film, Di et al and Wang et al. 13 have realized the direct electron transfer of SOD. The direct electrochemistry of SOD was also investigated on gold (Au) 14-16, carbon nanotubes (CNTs) 17, ZnO 18, , TiO 2 and NiO x modified electrode. The SOD-based O 2 biosensors based on the direct electron transfer of SOD have good linear response to O 2 in the nanomolar range, although a few papers have reported that the upper limit of the linear response was as high as µm (Refs 16, 19). It is well-known that under normal physiological conditions, O 2 has a rather low concentration ( M). However, in the case of traumatic brain injury ischemia-reperfusion, hypoxia, and environmental stresses, the concentration of O 2 may increase to ca M (Ref. 19). Hence, it is essential to provide quantitative information on O 2 concentration with wider range for tracking the role of O 2 in physiological and pathological processes. The layer-by-layer assembly technique which is based on the alternate adsorption of oppositely charged species from their solutions onto the surface of solid supports has aroused interest 22. It was reported that the layer-by-layer assembly films could provide a suitable microenvironment for the proteins/enzymes to retain their original structure and bioactivity in the films 23 and enhance the direct electron transfer between the proteins and underlying electrodes 24. Therefore, the technique of layer-bylayer assembly has been employed widely to achieve the direct electrochemistry of proteins/enzymes and fabricate related biosensors. Some redox proteins,
2 1058 INDIAN J CHEM, SEC A, AUGUST 2012 such as myoglobin 25,26, glucose oxidase (GOD) 27,28, hemoglobin 29,30, horseradish peroxidase (HRP) 31,32, etc. have been investigated by layer-by-layer assembly methods. However, to the best of our knowledge, there is only one study focused on the layer-by-layer assembly of SOD and related O 2 electrochemical biosensors 33. In the present work, a new strategy for fabricating O 2 electrochemical biosensors is developed based on the layer-by-layer assembly of Cu, Zn-SOD and poly-(diallyldimethylammonium) (PDDA) on the L-cysteine (Cys) modified Au electrode. Also, the direct electrochemistry of SOD has been investigated. Herein, Cys was used as the promoter to improve the direct electron transfer between redox sites of SOD and the electrode as reported previously 4,7-9. The formation of {SOD/PDDA} n layer-by-layer film was monitored by cyclic voltammetry (CV). Based on the bifunctional enzymatic catalytic activities of the SOD to the oxidation and reduction of O 2, the developed {SOD/PDDA} 5 /Cys/Au electrode exhibited good analytical characteristics in the detection of O 2, such as low detection limit (0.1 µm), good stability, reproducibility and selectivity, and particularly a wide linear range, up to 546 µm. Materials and Methods SOD from bovine erythrocytes (Cu, Zn-SOD, EC ) was purchased from Sigma and used without further purification. The SOD stock solution at a concentration of 2 mg ml -1 was prepared with 25 mm phosphate buffer solution (PBS, ph 7.2) and stored at 4 C. Cys was supplied by Bio Basic Inc, Canada. Aqueous solution of Cys was freshly prepared. KO 2 was purchased from Alfa Aesar. A stock solution of KO 2 was prepared by adding KO 2 to dimethyl sulfoxide (DMSO) (water was removed by 4 Å molecular sieves), ultrasonicating the solution for 5 min, and then adding 4 Å molecular sieves to remove water. PDDA (MW , 20 wt. %) was from Aldrich. All other chemicals were of analytical grade. All aqueous solutions were prepared with ultra pure water obtained from Millipore system (resistivity >18 MΩ cm). Electrochemical measurements were performed on a CHI 660B electrochemical workstation (Chenhua Instrument Company of Shanghai, China). A conventional three-electrode cell was used with an Au electrode (dia. 2 mm) as the working electrode, a platinum wire as the counter electrode and a saturated calomel electrode (SCE) as the reference electrode. Amperometric measurements of O 2 were carried out in gently stirred (100 rpm) phosphate buffer solution (25 mm, ph 7.2) at the applied potential. Unless mentioned otherwise, the electrochemical measurements were carried out at room temperature (25 ± 2 C). All the potentials herein are referred to SCE. Preparation of the modified electrode The Au electrode was carefully polished to a mirror-like surface with 0.5 and 0.05 µm alumina slurries, followed by ultrasonication in ultra pure water and methanol. Subsequently, Au electrode was pretreated electrochemically in 0.5 M H 2 SO 4 aqueous solution by potential cycling in the potential range of 300 to 1500 mv at a potential scan rate of 100 mv s -1 until the cyclic voltammogram characteristic of a clean Au electrode was obtained. Then, the Au electrode was washed thoroughly with copious amounts of ultra pure water and dried under nitrogen gas. The surface of the Au electrode was modified with SOD/PDDA multilayer films by layer-by-layer assembly technique; the related procedure is shown in Scheme 1. Firstly, a precursor layer of the negatively charged Cys monolayer was adsorbed on the surface of Au electrode by immersing the Au electrode into Cys aqueous solution (1 mm, ph 5.5) for 30 min at room temperature 34 (step 1 in Scheme 1). Prior to the layer-by-layer assembly, the preparation conditions were optimized. It was found that the immersing time of 60 min was reasonable and optimal for the assembly of positively charged PDDA and negatively charged SOD, respectively. Based on the optimal preparation conditions, the positively charged polycation was first adsorbed by dipping the negatively charged Cys/Au electrode in PDDA solution for 60 min (step 2 in Scheme 1). Then the Schematic description for the layer-by-layer assembly procedure of {SOD/PDDA} n /Cys/Au electrode Scheme 1
3 YANG et al.: SUPEROXIDE ANION BIOSENSOR BASED ON {SOD/PDDA} 5 /Cys/Au ELECTRODE 1059 obtained PDDA/Cys/Au electrode was immersed into a superoxide dismutase solution (2 mg ml 1 at ph 7.4) for 60 min, where the negatively charged SOD (pi = 4.9) was adsorbed to the positively charged PDDA surface through electrostatic interaction 19. The loosely attached SOD molecules were removed from the surface by a thorough rinse with ultrapure water to obtain the SOD/PDDA/Cys/Au electrode (step 3 in Scheme 1). The desired number of bilayers (n) for {SOD/PDDA} n films on the Cys/Au electrode was controlled by repeating the above steps (step 4 in Scheme 1). After each step, the electrode was rinsed thoroughly with ultra pure water. The electrode was washed thoroughly with ultra pure water and stored in 4 C for future use. Results and Discussion Direct electrochemistry of SOD at different modified electrode Figure 1A shows the cyclic voltammograms of the Cys/Au (dashed line) and PDDA/Cys/Au (solid line) electrodes in 25 mm PBS (ph 7.2) at the scan rate of 100 mv s -1. No redox peaks are observed on both Cys/Au and PDDA/Cys/Au electrodes in the applied potential window. Poly-(diallyldimethylammonium) (PDDA) is a polycation, while SOD (the isoelectric point at ph 4.9) 18 has considerable negative surface charge at ph 7.2. Thus, based on the electrostatic interaction between PDDA and SOD, layer-by-layer films of PDDA and SOD could be assembled on the Cys/Au electrode surface by alternate adsorption of PDDA in water and SOD in PBS (ph 7.2). The obtained film was designated as {SOD/PDDA} n, where n is the cycle number of the SOD/PDDA bilayer. Figure 1B shows the cyclic voltammograms of the {SOD/PDDA} n /Cys/Au (n = 1-6) electrodes in 25 mm PBS (ph 7.2). It can be observed that the anodic peak potential (E p a ) and cathodic peak potential (E p c ) are at ~188 mv and 20 mv respectively with a peak potential separation ( E p ) of 208 mv, implying a quasi-reversible process of the immobilized SOD. Additionally, the formal potential (E 0 = (E p a + E p c )/2) is found to be ca. 84 mv. This is consistent with the value reported previously for the direct electron transfer of SOD in the neutral PBS 4,5, These results imply that a good electron transfer between the redox center of SOD and the electrode can be achieved for all {SOD/PDDA} n /Cys/Au (n = 1 ~ 6) electrodes. In addition, it may be noted that the redox peak current of SOD increases with increase in the number of bilayers (n) due to the increase of the immobilized SOD. At n > 5, the increase of the redox peak currents is not obvious, indicating that the optimum value of the assembly number is 5 which has been adopted in the following experiments. According to Γ = Q/nFA (where Q is the charge, Γ is the amount of electroactive SOD, n is the electron transfer number, F is the Faraday constant and A is the geometric area of the working electrode) 35, the amount of electroactive SOD (Γ, mol cm -2 ) on the {SOD/PDDA} 5 /Cys/Au electrode was estimated from curve e in Fig. 1B to be mol cm -2. This value is higher than that on the SOD-CNT/GC 17 ( mol cm -2 ), SOD/TiO 2 /ITO 20 ( mol cm -2 ) and SOD/Au-NP 16 ( mol cm -2 ) electrodes. This Fig. 1 (A) Cyclic voltammograms obtained at the (1) Cys/Au (dashed line) and (2) PDDA/Cys/Au (solid line) electrodes in 25 mm PBS (ph 7.2). (B) Cyclic voltammograms of the {SOD/PDDA} n /Cys/Au electrode in 25 mm PBS (ph 7.2) at a scan rate of 100 mv s -1, for varying assembly number(n) from a f: 1-6.
4 1060 INDIAN J CHEM, SEC A, AUGUST 2012 indicates that by layer-by-layer assembly technology, more SOD molecules can be immobilized on the {SOD/PDDA} 5 /Cys/Au electrode, which is significant for improvement of the analytical performance of the modified electrode. In order to investigate the direct electron transfer process of SOD on the modified electrode, the electrochemical performance of the {SOD/PDDA} 5 /Cys/Au electrode was investigated at varying potential scan rate (from 10 to 1000 mv s -1 ) (Fig. 2(A)). It is noted that the redox peak currents of SOD increase with increase of scan rate. This can be observed clearly in the relationship between the redox peak currents and the potential scan rate (Fig. 2B). From Fig. 2B, it can be seen that the anodic and cathodic peak currents (I p a and I p c ) increase linearly with the increase of the scan rate from 10 to 1000 mv s 1. This demonstrates that the redox reaction of SOD at the {SOD/PDDA} 5 /Cys/Au electrode is a surfacecontrolled process and not a diffusion-controlled process 8,9,19. In addition, no obvious change of the cyclic voltammograms is observed on consecutive potential scanning for 100 cycles at the sweep rate of 100 mv s -1, indicating that SOD is stably immobilized in the layer-by-layer films. Determination of O 2 at the {SOD/PDDA} 5 /Cys/Au electrode Figure 3 shows the cyclic voltammograms obtained at the PDDA/Cys/Au electrode and {SOD/PDDA} 5 /Cys/Au electrode in the absence and Fig. 2 (A) Cyclic voltammograms of the {SOD/PDDA} 5 /Cys/Au electrode with different scan rates [a m: 10, 20, 50, 100, 200, 300, 400, 500, 600, 700, 800, 1000 mv s -1 ]. (B) Relationship between anodic and cathodic peak currents of the {SOD/PDDA} 5 /Cys/Au electrode and potential scan rate. Fig. 3 Cyclic voltammograms obtained at the (A) PDDA/Cys/Au electrode, and, (B) {SOD/PDDA} 5 /Cys/Au electrode in the absence (1, solid line) and presence (2, dashed line) of 300 µm O 2 in 25 mm PBS (ph 7.2) at a scan rate of 100 mv s -1. [Inset plot: The currenttime responses of {SOD/PDDA} 5 /Cys/Au electrode in 25 mm PBS at (a) 300 mv, and, (b) 200 mv. The arrows represent the addition of KO 2 (10 µm O 2 ) and SOD (3000 U) to the solution].
5 YANG et al.: SUPEROXIDE ANION BIOSENSOR BASED ON {SOD/PDDA} 5 /Cys/Au ELECTRODE 1061 presence of 300 µm O 2. There is almost no change in the current at the PDDA/Cys/Au electrode before and after adding O 2 (Fig. 3A). However, at the {SOD/PDDA} 5 /Cys/Au electrode (Fig. 3B), it can be observed that both oxidation and reduction peak currents increase obviously after adding O 2. On the other hand, a typical current-time response of the {SOD/PDDA} 5 /Cys/Au electrode is observed after adding O 2 and SOD (Fig. 3B inset). It may be noted that a large anodic current is present at 300 mv when 10 µm O 2 is added to the PBS and the current is quickly reduced after introducing SOD into the solution. At 200 mv, the catholic current increases obviously after injecting O 2 and decreases when SOD is added into the solution similarly. These results indicate that the redox peak currents resulting from the direct electron transfer of SOD can be enhanced by the addition of O 2, as reported in the literatures 4,7,8. The following reaction mechanism (Scheme 2) is proposed to explain these phenomena. The results in Fig. 3 indicate that the {SOD/PDDA} 5 /Cys/Au electrode can be used to fabricate a third-generation biosensor for O 2 detection. In order to find the optimum potential for O 2 determination, the potential dependence of the response of {SOD/PDDA} 5 /Cys/Au electrode toward O 2 was investigated (Fig. 4). The anodic response current of O 2 increases from 0 to 0.81 na with the positive increase of the applied potential from 0 to 500 mv and the cathodic response current increases from 0 to 0.67 na with the negative increase of the applied potential from 0 to 300 mv. This current- potential profile gives the experimental basis for choosing the operating potential suitable for the measurement of O 2 using {SOD/PDDA} 5 /Cys/Au electrode. It is considered that the interference of the co-existing compounds in the physiological conditions may be more obvious at the higher potential. To meet the requirements of the selectivity and sensitivity of the present O 2 biosensor, the anodic and cathodic optimum potentials of modified electrode was typically polarized at 300 mv and 200 mv, respectively. It has been reported that in vivo formation of physiologically inappropriate levels of free radical occurs in response to low blood flow, low oxygen levels, and low ph 19. Therefore, the effect of ph on the response of O 2 was studied. It is observed that only slight ph dependence is observed for both anodic and cathodic O 2 response at the {SOD/PDDA} 5 /Cys/Au electrode within a ph range of Herein, ph 7.2, which is close to physiological ph value, has been selected as the optimum ph value for the determination of O 2. Under the optimum conditions, the amperometric response of {SOD/PDDA} 5 /Cys/Au electrode to the successive addition of O 2 at the applied potential of 300 mv and 200 mv was studied (Fig. 5A). A side-step-like current response can be observed both at 300 mv and 200 mv; the currents increases stepwise with successive additions of O 2. In order to express clearly the relationship between response current and the concentration of O 2, the calibration plots are show in Fig. 5B. It can be observed that the response current changes linearly with the O 2 concentration in the range of µm at the applied potential of 300 mv, and in the range of µm at the applied potential of 200 mv. It is noted that the upper limit of the linear response range is much higher than that obtained at SOD/Au-NS/ITO (207 µm at 250 mv and 147 µm at 300 mv) 16 and Fig. 4 The Potential dependence of the response of the {SOD/PDDA} 5 /Cys/Au electrode toward 10 µm O 2 in 25 mm PBS (ph 7.2).
6 1062 INDIAN J CHEM, SEC A, AUGUST 2012 Fig. 5 (A) Amperometric responses of the {SOD/PDDA} 5 /Cys/Au electrode to the successive addition of 10 µm O 2 at (1) 300 mv, and, (2) 200 mv in 25 mm PBS (ph 7.2). (B) Calibration plots obtained at the {SOD/PDDA} 5 /Cys/Au electrode at (1) 300 mv, and, (2) 200 mv. [ i is the value of the steady-state current minus the initial current]. SOD/ZnO/ITO (180 µm at 300 mv and 250 µm at 0 mv) electrodes 19. Such high upper limit of the linear response range is very important in some unusual cases where the concentration of O 2 may increase to ca M, such as traumatic brain injury ischemiareperfusion, hypoxia and environmental stresses. The detection limit (S/N=3) is 0.1 µm at the applied potential of 300 mv (0.24 µm at the applied potential of 200 mv) and the response time is as short as 5 s, which is comparable to that reported previously 16,19. To the best of our knowledge, the O 2 electrochemical sensors based on the direct electrochemistry of SOD with low detection limit and wide linear range have rarely been reported. It is well known that the possible co-existing compounds in the biological system may result in the interference for electrochemical determination of O 2. Herein, the interferences from AA, UA and H 2 O 2 were investigated. At 300 mv, 3.2 and 4.5 % current responses were obtained for respectively 15 µm AA and 20 µm UA, relative to 5 µm O 2. However, no obvious interference was observed at 200 mv. On the other hand, the interferences of H 2 O 2 were small (~2.5 %) at both 300 and 200 mv. These results indicate that the {SOD/PDDA} 5 /Cys/Au electrode has a satisfactory selectivity. Further, the reproducibility was investigated by testing ten enzyme electrodes prepared sincerlarly. The relatively standard deviation does not exceed 8 % for the determination of 10 µm O 2. To examine the storage stability of the electrode, the response current of the electrode was investigated after stored at 4 C, which remained 92 % of its initial response towards O 2 after two weeks. This indicates that the biosensor developed herein has satisfactory analytical characteristics and may have promising applications in O 2 determination and the evaluation of antioxidants. Conclusions A biosensor for O 2 detection based on SOD has been developed via layer-by-layer assembly technique. The fabricated {SOD/PDDA} 5 /Cys/Au electrode possesses good analytical performance, such as low detection limit (0.1 µm), wide linear range ( µm), good reproducibility, stability and selectivity. Such high upper limit of the linear response range makes {SOD/PDDA} 5 /Cys/Au electrode suitable for application in the determination of unusual O 2 levels and the evaluation of antioxidants. Acknowledgement This work was financially supported by National Natural Science Foundation of China, ( ) and Program for Changjiang Scholars and Innovative Research Team in University (PCSIRT), China. References 1 Auchère F & Rusnak F, J Biol Inorg Chem, 7 (2002) Beissenhirtz M K, Scheller F W, Viezzoli M S & Lisdat F, Anal Chem, 78 (2006) Fridovich I, Acc Chem Res, 5 (1972) Ohsaka T, Tian Y, Shioda M, Kasahara S & Okajima T, Chem Commun, 9 (2002) Prieto-Simón B, Cortina M, Campàs M & Calas-Blanchard C, Sens Actuat B, 129 (2008) 459.
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