Near-Infrared Light-Driven Photoelectrochemical Aptasensor Based

Sep 14, 2016 - ... of Nano-Tech and Nano-Bionics, Chinese Academy of Sciences, Suzhou 215123, China. ‡School of Pharmacy, Xi'an Jiaotong University,...
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Near-Infrared Light-Driven Photoelectrochemical Aptasensor Based on the Upconversion Nanoparticles and TiO2/CdTe Heterostructure for Detection of Cancer Cells Kewei Wang,†,# Ruihua Zhang,†,‡,# Na Sun,† Xinpan Li,†,‡ Jine Wang,*,† Yi Cao,† and Renjun Pei*,† †

Key Laboratory of Nano-Bio Interface, Division of Nanobiomedicine, Suzhou Institute of Nano-Tech and Nano-Bionics, Chinese Academy of Sciences, Suzhou 215123, China ‡ School of Pharmacy, Xi’an Jiaotong University, Xi’an 710061, China S Supporting Information *

ABSTRACT: A near-infrared-driven photoelectrochemical aptasensor was developed as a new method for the detection of the breast cancer cell MCF-7. The upconversion nanoparticles and TiO2/CdTe heterostructure were combined to prepare the film electrode, and the high-affinity aptamer AS1411 was conjugated to the electrode to recognize MCF-7 cells. In this fabrication, the upconversion nanoparticles transferred the near-infrared light to visible light, which could excite the semiconductor to enhance the current response. As a result, the aptasensor revealed good sensitivity and specificity with MCF-7 cell concentrations ranging from 1 × 103 to 1 × 105 cells/mL. The results presented a favorable determination of MCF-7 cells, which was achieved with the help of the upconversion nanoparticles and the photoelectrochemical interface. KEYWORDS: photoelectrochemical aptasensor, upconversion nanoparticles, TiO2/CdTe heterostructure, aptamer, cancer cells

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INTRODUCTION Photoelectrochemical (PEC) biosensor is a newly developed technique for bioanalysis, which applies the photoelectrical process to enhance the electrochemical signal and shares the same advantage as the electrochemical devices, such as low cost, high sensitivity, and portable instruments.1 In the PEC biosensors, the illumination from the light source directly determines the photon-to-electron conversion efficiency. Recently, UV light has been rarely mentioned because of its high-energy photons which would damage the biological systems. Therefore, using visible light is regarded as a suitable method, which could easily excite the quantum dots2,3 and the sensitized wide band gap semiconductors.4−6 Since a lot of visible-light-driven PEC biosensors have been fabricated in recent years, to the best of our knowledge, there is no report about the near-infrared (NIR) activated PEC interface in the biosensors. The reason is that the NIR irradiation with low energy (>700 nm) cannot provide sufficient energy potential to excite the electron−hole pairs in the common semiconductors (>1.8 eV). Compared with visible-light excitation, bioanalysis under the NIR light presents several advantages, such as minimal photobleaching and low phototoxicity.7 In particular, the NIR excitation can avoid the self-irradiation from the biological tissues and provides the possibility of further development for in vivo applications.8 For this purpose, we first investigated the utilization of the NIR excitation in the solar cell, where the © 2016 American Chemical Society

excess energy of the sub-band gap light is not effectively used by the semiconductor layers and releases as heat.9 To overcome this problem, upconversion nanoparticles (UCNs), or the so-called upconverting phosphors, have been introduced into PEC research and usually act as the back reflectors to convert the NIR light to visible light, which can be reused by the semiconductor layers.10−12 Moreover, the design of composite semiconductors with UCNs has gradually become a new research topic in the field of PEC water splitting.13 In this context, the use of NaYF4:Yb,Er/hematite composite,14 plasmon-assistant upconversion nanostructure,15 and the Y2O3:Yb,Er incorporated TiO2/CdSe heterostructure16 were reported as photoelectrodes. The works above demonstrate the applications of UCNs for broadening the responding light range of the semiconductors, which provides us an exciting opportunity to develop NIR-lightdriven PEC interfaces and devices for the biosensors. Herein, we reported the first NIR-driven PEC biosensor in which the NaYF4:Yb,Er particles were combined with CdTe/ TiO2 heterostructure to form a NIR-light-motivated PEC interface. This hybrid interface used the emission of the visible light from NaYF4:Yb,Er and the absorption of the visible light by CdTe/TiO2 to provide the photogenerated electrons. The Received: August 2, 2016 Accepted: September 14, 2016 Published: September 14, 2016 25834

DOI: 10.1021/acsami.6b09614 ACS Appl. Mater. Interfaces 2016, 8, 25834−25839

Research Article

ACS Applied Materials & Interfaces Scheme 1. Illustration of the NIR-Light-Excited PEC Interface and the MCF-7 Cell Detection Principle

The oligonucleotide AS1411 was synthesized and purified by Sangon Biotechnology (Shanghai, China). The 5′ end of AS1411 was modified by the NH2 group and the sequence was (5′ to 3′) NH2-GGT GGT GGT GGT TGT GGT GGT GGT GG. Before use, this oligonucleotide was stored at −20 °C and diluted to the required concentration with 10 mM PBS. Scanning electron microscopy (SEM) with FEI Quanta 400F was used to observe the morphology of samples. The structure characterization was performed on a diffractometer (D8 Advance, Bruker AXS, Germany) employing Cu Kα radiation (λ = 0.15406 nm), with a scanning rate of 5°/min in the 2θ angle ranged from 20° to 70°. UV−vis spectroscopy measurement was carried out on a Jasco V-660 spectrophotometer. Photoelectrochemical measurements were operated with CHI660D electrochemical workstation (Shanghai Chenhua). Fabrication of the PEC Aptasensor. The NaYF4:Yb,Er/TiO2 film was prepared by a modified doctor blade method according to the previous report.19 Typically, 1.2 g of NaYF4:Yb,Er/TiO2 mixture was grinded in a mortar and was wet by some drops of acetic acid. Then 1 mL of water and 6 mL of ethanol were added subsequently drop by drop under milling. After that, the paste was transferred to a flask by 20 mL of ethanol, and then stirring and ultrasonicating were carried out to perform a homogeneous suspension. Terpineol (4 g) and ethyl cellulose (0.6 g) were slowly added into the flask with vigorous stirring. After the cellulose was dissolved, the ethanol was removed by rotary evaporation. The paste was coated on the FTO glass with 3M tape (Scotch 810) as spacer to control the thickness as ∼50 μm. The as-prepared NaYF4:Yb,Er/TiO2 film was annealed at 450 °C for 1 h to remove the residual organics. CdTe was grown on the NaYF4:Yb,Er/TiO2 electrode via an electrochemical deposition method to construct the TiO2/CdTe heterojunction.20 Commonly, CdTe was cathodically deposited using NaYF4:Yb,Er/TiO2 as the working electrode, Ag/AgCl as the reference electrode, and Pt foil electrode as the counter electrode with the potential as −0.4 V at 85 °C. The electrolyte consisted of 0.1 M CdSO4 and 0.1 mM TeO2, which was adjusted to pH 1.4 by the diluted H2SO4. After the deposition, the resulting electrode was cooled down to room temperature and carefully washed with water. At last, the electrode was dried at room temperature and stored in the dark. The CdTe-modified NaYF4:Yb,Er/TiO2 electrode was incubated with 25 mM thioglycolic acid (TGA) in ethanol over 12 h at room temperature. After that, the electrode was rinsed with ethanol and water,

detailed principle is as shown in Scheme 1, where the CdTe nanoparticles can absorb the upconversion emissions of the NaYF4:Yb,Er, such as the main peaks in the visible-light region at 520 nm (2H11/2 → 4I15/2), 550 nm (4S3/2 → 4I15/2), and 670 nm (4F9/2 → 4I15/2) (Figure S1).14,15 Moreover, we chose the cancer cell MCF-7 and its aptamer AS1411 as a recognition system to evaluate the PEC interface. Since the first report of the PEC biosensor for cancer cell detection,17 aptamer obtained by SELEX (Systematic Evolution of Ligands by Exponential Enrichment) is a more attractive alternative because of its small size and high binding affinity to different target molecules.18 In this work, the amino-modified AS1411 was immobilized on the electrode through the bridge of the mercaptoacid ester. After incubation, the binding of the MCF7 cells caused the steric hindrance effect to block the charge transfer and decreased the amounts of the sacrificial agents near the electrode surface. Thus, the photocurrent response presented obvious decrement depending on the concentrations of the cells. The rapid sensitive determination method could be presented as an efficient detection of the breast cancer cells.

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EXPERIMENTAL SECTION

Reagents and Instruments. 1-(3-(Dimethylamino)propyl)-3ethylcarbodiimide hydrochloride (EDC) and N-hydroxysuccinimide (NHS) were purchased from Sigma-Aldrich (St. Louis). Anatase-phase TiO2 was received from Alfa Aesar (Haverhill, MA). The NaYF4:Yb,Er powder was obtained from Shanghai Huaming Gona Rare Earth New Materials Co. Ltd. Fluorine-doped tin oxide (FTO) glass was purchased from Nippon Sheet Glass (Tokyo) with the resistance of 14 Ω and the transmittance ≥90%. All other reagents were purchased from Sinopharm Chemical Reagent Co. Ltd. (Shanghai, China). Except the chemically pure terpineol, all of the reagents were analytical grade and used as received without further purification. All other reagents were purchased from Sinopharm Chemical Reagent Co. Ltd. All solutions were prepared by Milli-Q pure water. The 0.1 M phosphate buffered saline (PBS) was obtained by mixing 0.1 M NaH2PO4 and 0.1 M Na2HPO4 to pH 7.4. 10 mM PBS was prepared by diluting the 0.1 M PBS. 25835

DOI: 10.1021/acsami.6b09614 ACS Appl. Mater. Interfaces 2016, 8, 25834−25839

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ACS Applied Materials & Interfaces respectively, and then blown dry by nitrogen. Subsequently, 20 μL of 10 mM PBS containing 10 mM EDC and 20 mM NHS was dropped on the electrode surface to activate the carboxyl group of TGA for 1 h. Then the electrode was rinsed with 10 mM PBS and incubated with 20 μL of 20 μM AS1411 at 4 °C overnight. After incubation, the electrode was rinsed with PBS several times and treated with PBS containing 1% BSA for 1 h to decrease the nonspecific binding. The prepared electrode was kept at 4 °C until use. PEC Detection of the MCF-7 Cells. The MCF-7 cells were centrifuged and collected at 1000 rpm for 4 min to separate the culture medium and then were carefully redispersed into the PBS with different concentrations. The electrode was incubated with the cell solution at 37 °C for 60 min, and followed to clean out the nonspecifically bound cells. A three-electrode system was used for the detection in which the prepared photoelectrode was applied as work electrode. The illuminated area of the work electrode was around 5 mm2. A saturated Ag/AgCl and a Pt foil electrode were served as the reference electrode and counter electrode, respectively. The measurement method was i−t curve and the applied potential was 0 V. The electrolyte was 0.01 M PBS containing 10 mM ascorbic acid (AA). A 300 mW 980 nm laser was employed as the light source. After the current was stabilized, the responses were recorded at the “turn on” and “turn off” states of the laser.

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RESULTS AND DISCUSSION Characterization of the Materials. The morphologies of the raw materials and the as-prepared electrodes were observed by SEM. As shown in Figure 1A,B, the TiO2 nanoparticles were homogeneous with the diameter around 30 nm and the NaYF4:Yb,Er powder had the size from hundreds of nanometers to several micrometers. After casting onto the FTO glass by the doctor blade method, the NaYF4:Yb,Er/TiO2 composites (80:20, w/w) formed a rough film with good dispersion (Figure 1C). Moreover, they kept the same morphologies as the precursors and the large pores between the NaYF4:Yb,Er particles were fulfilled with the small TiO2 nanoparticles as shown in Figure 1D. Figure 1E shows that the CdTe nanoparticles prepared by the electrochemical deposition method covered almost the surface of the film and tended to aggregate as microspheres, which consisted of large amounts of nanoparticles (Figure 1F). As a result of the in situ growth by the electrochemical deposition, the interfaces between TiO2 and CdTe and the interface between NaYF4:Yb,Er and CdTe are shown in Figure S2. The XRD patterns of the materials are shown in Figure 2. The F-doped SnO2 substrate (FTO glass) showed obvious SnO2 peaks (JSPDS PDF 46-1088) in all of the patterns, which became slightly weaker after the films were fabricated. The curve (b) displayed diffraction peaks which could be indexed to the characteristic planes of the anatase TiO2 (JSPDS PDF 71-1166) and the β-phase NaYF4 with a hexagonal structure (JSPDS PDF 28-1192), where the peaks belonging to NaYF4:Yb,Er were very strong and the TiO2 only had two weaker peaks. The reason was not only the ratio between them but also the large scale and good crystallinity of the NaYF4:Yb,Er particles. After the electrochemical deposition, the NaYF4:Yb,Er/TiO2/CdTe electrode presented similar XRD patterns with curve (b) except a very weaker peak, which might belong to the (111) plane of the CdTe (JSPDS PDF 75-2086). In this cathodic deposition, the dissolved TeO2 powders were transformed to HTeO2+ in the H2SO4 solution, and had been reduced on the surface of the electrode, where they could quickly react with Cd2+ to form a compact layer of the CdTe nanoparticles.20 The formula could be

Figure 1. SEM graphs of the TiO2 nanoparticles (A), the NaYF4:Yb,Er powder (B), the NaYF4:Yb,Er/TiO2 (C, D), and the NaYF4:Yb,Er/ TiO2/CdTe (E, F) electrodes.

Figure 2. XRD patterns of (a) the FTO glass, (b) the NaYF4:Yb,Er/ TiO2, and (c) the NaYF4:Yb,Er/TiO2/CdTe electrodes. The above black, red, and blue marks indicated the planes of the TiO2, NaYF4:Yb,Er, and CdTe, respectively, and the triangle was the FTO substrate. The below vertical lines were the standard PDF card of the materials.

Photocurrent Response of the As-Prepared Electrode. The variation of the photocurrent of NaYF4:Yb,Er/TiO2/CdTe

3H+ + 2Cd2 + + HTeO2+ + 6e− → CdTe + 2H 2O 25836

DOI: 10.1021/acsami.6b09614 ACS Appl. Mater. Interfaces 2016, 8, 25834−25839

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ACS Applied Materials & Interfaces film during the fabrication is shown in Figure 3. As expected, though the NaYF4:Yb,Er could harvest the low-energy NIR light

Figure 3. Photocurrent response of the electrodes. (a) NaYF4:Yb,Er/ TiO2; (b) TiO2/CdTe; (c) NaYF4:Yb,Er/CdTe; (d) NaYF4:Yb,Er/ TiO2 /CdTe; (e) NaYF 4 :Yb,Er/TiO 2 /CdTe/AS1411; (f) NaYF4:Yb,Er/TiO 2/CdTe/AS1411/MCF-7; (g) NaYF4:Yb,Er/TiO 2/ CdTe + MCF-7. The electrolyte was 0.01 M PBS (pH = 7.4).

and emit high-energy light, there was no photocurrent at the NaYF4:Yb,Er/TiO2 electrode after the irradiation (curve (a)) because the visible light could not excite TiO2. Similarly, TiO2/ CdTe could not absorb the NIR light, which resulted in no photocurrent response generation (curve (b)). Then in the NaYF4:Yb,Er/CdTe electrode, the CdTe was excited by the NaYF4:Yb,Er and shows a reasonable photocurrent response (curve (c)). Moreover, the introduction of TiO2 enhanced the photocurrent by the conformation of the heterostructure between TiO2 and CdTe (curve (d)). After that, conjunction of the AS1411 resulted in the photocurrent slightly changing compared with the NaYF4:Yb,Er/TiO2/CdTe electrode (curve (e)). At last, the photocurrent decreased sharply with the incubation of MCF-7 cells at the concentration of 105 cell/mL (curve (f)) because the layer of cancer cells greatly blocked the charge transfer and impeded the diffusion of AA to the electrode surface. We also incubated the NaYF4:Yb,Er/TiO2/CdTe electrode with the same MCF-7 cells, and the photocurrent response (curve (g)) was slightly decreased due to weak adsorption. Compared with the big decrement of the photocurrent, it was considered that the nonspecific adsorption of the cells could not affect the sensitivity of the sensor. These results confirmed the mechanism of the NIR-driven PEC interface and the magnificent response to the cancer cells with reasonable selectivity. Optimization of the Detection. Though the UCNs have been applied in the aptasensors as NIR excited detection systems,21−23 there has been no report about the fabrication of PEC biosensor, so the parameters in the construction and the detection process should be investigated prior to use. First, one of the critical factors is the ratio of the NaYF4:Yb,Er and TiO2. Here, the NaYF4:Yb,Er converted the NIR light to visible light, indicating that more NaYF4:Yb,Er could generate more visible light emission. As shown in Figure 4A, various mass ratio NaYF4:Yb,Er/TiO2 electrodes gave great differences after being electrodeposited with CdTe for 60 min. Though more NaYF4:Yb,Er could excite more CdTe to generate higher photocurrent, the results suggested that 20% TiO2 was suitable to form the heterostructure with CdTe. The composition with TiO2 not only enhanced the photocurrent but also reduced the

Figure 4. (A) Photocurrent response of the NaYF4:Yb,Er/TiO2/CdTe electrodes with different mass ratio of NaYF4:Yb,Er in the paste of NaYF4:Yb,Er/TiO2. (B) Photocurrents of the NaYF4:Yb,Er/TiO2/ CdTe electrodes with different deposition times of CdTe. (C) Photocurrent decrements of the NaYF4:Yb,Er/TiO2/CdTe electrodes after incubation with different times of MCF-7 cells. The electrolyte was 0.01 M PBS (pH = 7.4).

photocorrosion of the CdTe, leading to a more stable response due to the improvement of the separation between photogenerated electrons and holes. Next, the amount of the CdTe nanoparticles was considered, which was attributed to the different deposition time. As shown in Figure 4B, increasing the time could greatly increase the photocurrent response of the electrode. When the visible light from the NaYF4:Yb,Er was emitted, more CdTe nanoparticles could absorb more photons and generate more photoelectrons. However, the film after 120 min deposition brought a very unstable response due to a loose thick film which might drop from the electrode in the detection. Thus, we chose 60 min as the favorable deposition time. At last, the incubation time of the cancer cells was also examined. In Figure 4C, ΔI = |I0 − I|, where I0 and I are the photocurrents of the electrode before and after incubation with MCF-7 cells, respectively. The photocurrent response decreased 25837

DOI: 10.1021/acsami.6b09614 ACS Appl. Mater. Interfaces 2016, 8, 25834−25839

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ACS Applied Materials & Interfaces

semiconductor heterostructure to detect the MCF-7 cells. The matched photoconversion interface could efficiently absorb the NIR light and generate photoelectrons to enhance the detection signal. Moreover, the high affinity of the aptamer AS1411 improved the sensitivity and the selectivity of the cancer cell detection. Also, the low toxicity of the electrode guaranteed the activity of the cell and maintained the sensing performance. So, the prepared NIR driven PEC aptasensor would have potential to be extended for the detection of other cancer cells with the wide linear range and low detection limit.

quickly after 10 min incubation, indicating the high affinity of the aptamer. With the increase of the incubation time, the photocurrent increased gently and reached a plateau at 60 min. The result confirmed that increasing incubation time could lead to many more cells adsorbing on the electrode. Considering the efficiency of the detection, the incubation of 60 min was selected to detect MCF-7 cells. Detection of the MCF-7 Cells. The cell detection exploited the affinity interaction between the immobilized aptamers and the target cells (Figure S3), where the resulted photocurrent intensity was related directly with the number of cells. Figure 5

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ASSOCIATED CONTENT

S Supporting Information *

The Supporting Information is available free of charge on the ACS Publications website at DOI: 10.1021/acsami.6b09614. The fluorescence emission spectrum of the NaYF4Yb,Er and the absorption of the electrode, the specificity of the aptasensor toward two other cancer cells (PDF)

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AUTHOR INFORMATION

Corresponding Authors

*E-mail: [email protected] (R.P.). *E-mail: [email protected] (J.W.). Author Contributions #

Kewei Wang and Ruihua Zhang contributed equally to this work.

Figure 5. Photocurrent decrements of the AS1411 immobilized NaYF4:Yb,Er/TiO2/CdTe electrodes after incubating with different concentrations of the MCF-7 cells. The electrolyte was 0.01 M PBS (pH = 7.4).

Notes

The authors declare no competing financial interest.

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ACKNOWLEDGMENTS This work was financially supported by the Natural Science Foundation of Jiangsu Province (BK20130349, BK20130351), the National Natural Science Foundation of China (21305154, 21575154), and the State Key Laboratory of Electroanalytical Chemistry (SKLEAC201410).

shows the spots of the photocurrent decrement upon the concentration of MCF-7 cells, which indicated that more and more cells reacted with the aptamers and led to the enhance of suppression to photocurrent. Furthermore, it could be observed that the decrements had a linear ralation with the logarithm of MCF-7 cell concentrations ranging from 1 × 103 to 1 × 105 cells/ mL, the equation of which was Y = −1.20 + 0.41X (R = 0.989). The detection limit was estimated to be 400 cells/mL at a S/N of 3. Compared with previous studies (Table S1), our results also presented a favorable examination of the MCF-7 cells with a large detection range and a comparable detection limit was achieved with the help of the UCNs and the PEC interface. In addition, we also investigated the specificity of this aptasensor toward two cancer cells (Figure S4), including leukemia cell (CCRF-CEM) and fibrosarcoma cell (HT1080). Even though the concentration ratios between the MCF-7 cells and the two cells were 1:100, the aptasensor exhibited good specificity. The results might indicate this PEC system is very promising for the applications in the cancer cell dectection. Besides, the cytotoxicity of the electrode was conducted to ensure the viability of the cells in the experiment, which deterimine the performance of sensing sensitivity. WST assay was performed with MCF-7 cells. After culture with the electrode for 4h, the MCF-7 cells exhibited 92−112% viability, indicating favorable cell viability and possibly a boosting by the nanomaterials. With the low toxicity, our electrode may become a promising candidate in the PEC biosensor.

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REFERENCES

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CONCLUSIONS In conclusion, we prepared a photoelectrochemical aptasensor combining the NaYF4:Yb,Er upconversion material and the 25838

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DOI: 10.1021/acsami.6b09614 ACS Appl. Mater. Interfaces 2016, 8, 25834−25839