Ligating Dopamine as Signal Trigger onto the Substrate via Metal

Nov 7, 2016 - To the best of our knowledge, a PEC sensing platform for miRNA assay, in which electron donors are introduced and fixed on the substrate...
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Ligating Dopamine as Signal Trigger onto the Substrate via MetalCatalyst-Free Click Chemistry for “Signal-On” Photoelectrochemical Sensing of Ultralow MicroRNA Levels Cui Ye,† Min Qiang Wang,‡ Zhong Feng Gao,† Ying Zhang,† Jing Lei Lei,§ Hong Qun Luo,*,† and Nian Bing Li*,† †

Key Laboratory of Eco−Environments in Three Gorges Reservoir Region (Ministry of Education), School of Chemistry and Chemical Engineering, Southwest University, Chongqing 400715, People’s Republic of China ‡ Institute for Clean Energy & Advanced Materials, Faculty of Materials and Energy, Southwest University, Chongqing 400715, People’s Republic of China § School of Chemistry and Chemical Engineering, Chongqing University, Chongqing 400044, People’s Republic of China S Supporting Information *

ABSTRACT: The efficiency of photon-to-electron conversion is extremely restricted by the electron−hole recombinant. Here, a new photoelectrochemical (PEC) sensing platform has been established based on the signal amplification of click chemistry (CC) via hybridization chain reaction (HCR) for highly sensitive microRNA (miRNA) assay. In this proposal, a preferred electron donor dopamine (DA) was first assembled with designed ligation probe (probe-N3) via amidation reaction to achieve DA-coordinated signal probe (PDA-N3). The PDA-N3 served as a flexible trigger to signal amplification through efficiently suppressing the electron−hole recombinant. Specifically, the PDA-N3 can be successfully ligated into the trapped hairpins (H1 and H2) via the superior ligation method of metal-catalyst-free CC, in which the electron donor DA was introduced into the assay system. Moreover, the enzyme-free HCR, employed as a versatile amplification way, ensures that lots of PDA-N3 can be attached to the substrate. This PEC sensing for miRNA-141 detection illustrated the outstanding linear response to a concentration variation from 0.1 fM to 0.5 nM and a detection limit down to 27 aM, without additional electron donors. The sensor is further employed to monitor miRNA-141 from prostate carcinoma cell (22Rv1), showing good quantitative detection capability. This strategy exquisitely influences the analytical performance and offers a new PEC route to highly selective and sensitive detection of biological molecules.

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resulting from electron excitation and subsequent electron transfer of a photoexcited material. Meanwhile, the photogenerated electron−hole pairs would cause the oxidation− reduction reaction of an electron/hole donor, thus suppressing the electron−hole recombinant and inducing the enhanced signal readout.11,14,15 Among the various kinds of photoexcited materials, bismuth sulfide (Bi2S3) is known to be an attractive material for PEC application.16 The Bi2S3-based composites with specific architectural morphology, via anchoring the 2Dlayered materials molybdenum disulfide (MoS2) to Bi2S3, possess excellent photocatalytic performance,17,18 which are pregnant and urgent to be studied in PEC sensing applications, thus realizing their full potential. To achieve the highly efficient photon-to-electron conversion, an ingenious design of introducing an electron donor into the anodic PEC sensing system is extremely desired. However, the conventional PEC sensing usually directly adds the electron donor into the

icroRNAs (miRNAs) are single-strand and endogenous nonprotein-coding RNAs with approximately 19−23 nucleotides, which mediate post-transcriptional regulation of specific gene expressions.1−3 In this case, miRNA expression and quantitative profiles can be used as biomarkers for the onset and progression of disease states.4,5 Given the low abundance and similar sequences among family members, it is still a challenge to develop an ultrasensitive detection platform for miRNA.6,7 Inspiringly, ever since the photoelectric effect was discovered by Edmond Becquerel in 1839,8 the integration of photoelectrochemical (PEC) process with bioanalysis has inaugurated an innovative field of PEC sensing.9,10 Because of the advantages of the cheap instruments, straightforward operation, high sensitivity, and low background signals, PEC sensing possesses desirable potential in biological analysis compared to conventional electrochemical and optical methods.11,12 Generally, a PEC sensing system is composed of an appropriate PEC transducer referring to photoexcited materials, and an electron/hole donor.13 By the trigger of an applied light, the PEC process involves the photon-to-electricity conversion © 2016 American Chemical Society

Received: June 28, 2016 Accepted: November 7, 2016 Published: November 7, 2016 11444

DOI: 10.1021/acs.analchem.6b02481 Anal. Chem. 2016, 88, 11444−11449

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Analytical Chemistry electrolytic cell, which hinders the development of PEC living sensing systems due to the lack of electron donors in living cells or organisms.19−21 To meet the demand of simplifying the operation and making the electron donor economical, the electron donor is bound to a specially designed ligation probe, thus obtaining a signal probe. This resultant signal probe was eventually fastened onto the substrate as a signal trigger by virtue of metal-catalystfree click chemistry (CC) as a linker. As a useful tool in the ligation and decoration, CC offers great potential in the development of combinatorial libraries of assembled and scaffolded structure.22,23 Intriguingly, without any metal catalyst, the click chemical ligation proceeds fluently and smoothly between a dibenzocyclooctyne (DBCO)-containing probe and an azide (N3)-containing probe, which is superior to the conventional CC that needs a copper catalyst. Moreover, both DBCO and N3 groups are inert, and thus this novel CC avoids interference from coexisting biomolecules and groups.24 CC becomes an ideal and reliable candidate for developing versatile immobilization platforms, which is preferable to physical adsorption, direct covalent attachment, or noncovalent interaction in terms of practicability and selectivity.24,25 Hybridization chain reaction (HCR) is a simple and efficient amplification strategy, in which two kinetically trapped hairpins (H1 and H2) are designed to trigger a series of DNA polymerization by initiator or target molecules.26−28 Noteworthily, the signal probe binding electron donor can be attached via CC on those dimers with precisely controlled density, which is conducive to the efficiency of signal amplification. To the best of our knowledge, a PEC sensing platform for miRNA assay, in which electron donors are introduced and fixed on the substrate by virtue of a ligation probe as a carrier through CC, has not been reported yet. Herein, we create a new PEC miRNA sensing platform based on Bi2S3@MoS2 nanoflowers coupled with a pithy ligation method of metal-catalyst-free CC and a versatile signal amplification strategy of enzyme-free HCR, as displayed in Scheme 1. Specifically, we aim to design and integrate multiple functional components rationally into a signal probe to create a standalone photoelectric trigger PDA-N3 which can serve as a preferred electron donor to high-efficiently suppress the electron−hole recombinant. For the first time, the electron donor DA assembled with well-designed probe-N3 (PDA-N3) was fastened onto the substrate via CC directly, which is conducive to transport electrical carriers and promote photonto-electron conversion efficiency. Moreover, no additional electron donors were introduced into the PEC sensing system, and the extensive consumption of electron donors was excluded. Flexibly tailoring the electron−hole recombinant is a very promising strategy to perfect this PEC miRNA sensing performance with effectively depressing the electron−hole recombination and significantly accelerating the electron transfer. The success of this work may inspire more rational designs of photoelectric trigger for PEC sensing strategy.

Scheme 1. Schematic Illustration of (A) PEC Platform for MiRNA Assay; (B) Principle of Metal-Catalyst-Free Click Chemical Signal Amplification via Hybridization Chain Reaction (The Blue Box Presents the Fabrication Process of PDA-N3); and (C) PEC Response in the Absence and Presence of Target

μM H2 were heated respectively to 95 °C for 5 min, followed by cooling to room temperature for 2 h. After incubation with the target miRNA for 2 h at room temperature, the electrode was rinsed with 0.01 mol L−1 phosphate buffer (pH 7.4) and then incubated with the mixture of 10 μL of H1 and 10 μL of H2 for another 2 h to fulfill the HCR. Finally, the resulted electrode was dipped with 20 μL of PDA-N3 at room temperature for 15 min, allowing the PDA-N3 to hybridize via CC as a linker. The photocurrent intensity of the resulting functionalized electrode was recorded in 0.1 mol L−1 phosphate buffer (pH 7.4) irradiated with a visible-light. The light was switched on and off every 10 s, and the applied potential was 0.2 V. The electrolyte solution was pumped into pure nitrogen for 15 min prior to PEC measurements. Applications for Practical Sample Detection. Human cervical cancer cells (HeLa) and human prostate carcinoma cells (22Rv1) were chosen to execute the practical sample detection. After processing with cell counting, miRNA from the cell samples with diverse amounts were extracted by a column type commercial miRNA extraction kit and then the extracted miRNA was diluted in 30 μL of RNase-free water. As a result, the resulted solutions were applied to miRNA-141 measurement with the PEC sensing.

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RESULTS AND DISCUSSION Morphological and Structural Characterization of Bi2S3@MoS2 Nanoflowers. The morphologies of the asprepared Bi2S3 and Bi2S3@MoS2 nanoflowers were characterized by field emission scanning electron microscopy (FESEM). As displayed in Figure 1a, urchin-shaped Bi2S3 nanoflowers are observed with a diameter of about 2 μm. The high-magnification image (Figure 1b) reveals that each urchin-shaped Bi2S3 nanoflower is composed of nanorods radiating from the center of the nanoflowers. Figure 1c exhibits the morphologies of the as-prepared Bi2S3@MoS2 nanoflowers,

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EXPERIMENTAL SECTION Self-Enhanced PEC Biosensor for MiRNA Assay. MiRNA detection was executed in the sandwich format. Partial experimental details were described minutely in the Supporting Information (SI). With blocked by MCH solution (20 μL, 2 mM) for 1 h to minimize the nonspecific adsorption, 10 μL of the target (miRNA-141 in this work) was first hybridized with TSP (fragments of tetrahedron A). Meanwhile, 1 μM H1 and 1 11445

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The phase structures of the as-prepared Bi2S3 and Bi2S3@MoS2 nanoflowers were characterized by X-ray diffraction (XRD) spectra (Figure 2B). All of the diffraction peaks of prepared Bi2S3 can be indexed to orthorhombic structured Bi2S3 according to JCPDS card no. 17-0320, and the major peaks can be ascribed to the (1 3 0), (3 1 0), (2 1 1), and (2 2 1) crystal planes. The XRD pattern of the Bi2S3@MoS2 nanoflowers matches very well with that of pure Bi2S3, indicating no damage to Bi2S3 nanoflowers by the incorporation of MoS2. This result confirms the feasibility of the synthesis of Bi2S3@ MoS2 nanoflowers. In order to further prove the successful synthesis of Bi2S3@MoS2 nanoflowers, X-ray photoelectron spectroscopy (XPS) was performed for elemental analysis (Figure 2C,D). Apart from the characteristic peaks at 225.8, 162.7, and 161.5 eV, respectively belonging to S 2s, S 2p 1/2, and S 2p 3/2 orbits, other appropriate peaks corresponding to Bi3+ (Bi 4f 5/2:163.6 eV; Bi 4f 7/2:158.3 eV) and Mo4+ (Mo 3d 3/2:235.8 and 231.8 eV; Mo 3d 5/2:232.8 and 228.6 eV) can easily be detected through the XPS spectra. The phenomenon of spin−orbit separation (1.2 eV) between S 2p 1/2 and S 2p 3/2 peaks (Figure 2C) suggests the existence of S2− in the final product, which is in agreement with the previous report.29 The results of XPS are in accordance with that of XRD (as displayed in Figure 2B), which confirms that the composite nanoflowers are composed of Bi2S3 and MoS2. Photoelectrochemical Property of Bi2S3@MoS2 Nanoflowers. The PEC properties of Bi2S3 and Bi2S3@MoS2 nanoflowers were investigated by photocurrent measurement. As indicated in Figure 3A, the photocurrent response of Bi2S3@

Figure 1. FESEM images of (a, b) Bi2S3 and (c, d) Bi2S3@MoS2 nanoflowers. The corresponding elemental mappings of the region shown in (c) framed with the blue line for the (e) merged; (f) Mo; (g) Bi; and (h) S.

in which the whole Bi2S3 nanoflowers are densely coated by the 2D MoS2 nanosheets. A high-magnification image (Figure 1d) further discloses that the MoS2 nanosheets compactly grow on the surface of Bi2S3 nanoflowers. To verify the composition of as-prepared Bi2S3@MoS2 nanoflowers, the corresponding elemental mappings were carried out and displayed for the region c framed with the blue line (Figure 1e−h). The elemental mapping analysis confirms the coexistence and the homogeneous dispersion of Mo, Bi, and S elements in the urchin-shaped nanoflowers. These results indicate that the building units of the urchin-shaped nanoflowers are packed in a highly ordered manner, and the distinctive structure implies potential application in photoelectrochemistry. Figure 2A shows a low- and (inset) high-magnification transmission electron microscopy (TEM) image of Bi2S3@ MoS 2 nanoflowers, indicating that the surface of Bi 2 S3 nanoflowers was uniformly coated with 2D MoS2 nanosheets.

Figure 3. (A) Photocurrent responses of (a) MoS2, (b) Bi2S3, and (c) Bi2S3@MoS2 nanoflowers in 0.1 M Na2SO4 electrolyte (pH 7.0) at 0.2 V under visible-light illumination [inset: photographs of (a) MoS2, (b) Bi2S3, and (c) Bi2S3@MoS2]. (B) Schematic illustration of the proposed photocurrent−transducer mechanism.

MoS2 nanoflowers modified electrode (curve c) is higher than that of Bi2S3 modified electrode (curve b) and MoS2 modified electrode (curve a), demonstrating that the Bi2S3@MoS2 nanoflowers can efficiently enhance the photocurrent response. Following the onset of irradiation, the prompt rise of the signal to the stable value illustrates the fast electrical carriers excitation, separation, and transfer in the Bi2 S 3 @MoS 2 nanoflowers. The proposed photocurrent-transducer mechanism is illustrated in Figure 3B. Under a visible-light illumination, the electron−hole pairs are generated from the Bi2S3@MoS2 nanoflowers. The conduction band (CB) and the valence band (VB) of Bi2S3 are more negative than that of MoS2. This thermodynamic condition facilitates the facile injection of photogenerated electrons from the CB of Bi2S3 to the CB of MoS2, and photogenerated holes from the VB of MoS2 to the VB of Bi2S3. Such a synergy effect in the designed Bi2S3@MoS2 nanoflowers can hasten the spatial charge

Figure 2. (A) Low- and (inset) high-magnification TEM images of Bi2S3@MoS2 nanoflowers; (B) XRD patterns simulated from the X-ray crystal diffraction file for Bi2S3, prepared Bi2S3, and Bi2S3@MoS2 nanoflowers; XPS spectra of Bi 4f (C) and Mo 3d (D) orbits in the sample of Bi2S3@MoS2 nanoflowers. 11446

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was also investigated since the reaction time for CC can directly affect and decide the dominance of the PEC assay (Figure 4C). When the incubation time varied from 5 to 20 min, the photocurrent response for the reaction of metal-catalyst-free CC augments gradually, and then flattens out, demonstrating an equilibrium state for this sensing system. Thus, incubation for 20 min to achieve CC reaction is employed for the PEC assay. To clarify the contribution of HCR to signal amplification, a control experiment has been executed by using H1 only for miRNA detection (see the SI for more experimental details). In this work, the photocurrent mainly derives from the CC reaction to introduce DA as a highly efficient electron donor. Thus, the DA concentration of PDA-N3 in the sensing system is expected to affect the response signal. Figure 4D depicts a correlation between DA concentration and photocurrent intensity. With increasing DA concentration, the photocurrent increases rapidly and then levels off after 10 mM. So, 10 mM is employed as the optimal DA concentration. Apart from the above-mentioned DA concentration, the effect of different introduction methods, such as CC and covalent bonding, of the electron donor were studied. Two kinds of trapped hairpins (H1, H2 and H1′, H2′) were designed. H1 and H2 modified DBCO can ligate PDA-N3 via CC to efficiently introduce DA. H1′ and H2′ modified COOH can introduce DA via covalent bonding. After HCR, those two trapped hairpins were incubated, respectively. As shown in the inset of Figure 4D, the photocurrent intensity of fastening PDA-N3 via CC is much larger than that of immobilizing DA via covalent bonding, thus achieving the efficient “signal-on” strategy. The reason might be the fact that the metal-catalyst-free CC, as a linker in developing versatile immobilization platforms, proceeds fluently and quickly without any additional aid. However, the method of covalent bonding needs a chemical covalent cross-linking agent to immobilize DA, which is complicated to operate and easy to introduce interference. Therefore, the electron donor DA assembled with a well-designed probe-N3 (PDA-N3) is fastened onto the substrate via CC directly. The amount of TSP immobilized onto the surface of electrodes was optimized. The rational design of conduct CC after HCR was also certified (see the SI for more experimental details). Analytical Performance of the PEC Biosensor. The response signal of the PEC biosensor relied on the fixation amount of PDA-N3, which was connected with the concentration of miRNA. Under the optimized experimental conditions, the quantitative range of this PEC biosensor for miRNA-141 detection was assessed by incubating different concentrations of miRNA based on the developed PEC strategy. Figure 5A depicts that the photocurrent increases gradually with increasing concentration of miRNA. A linear relationship between photocurrent response and the logarithm of miRNA concentration is achieved in the range of 0.1 fM to 0.5 nM (Figure 5B). The linear regression equation is i = 11.4 lg c + 60.9 (R2 = 0.992) with a limit of detection 27 aM. The prepared PEC biosensor shows a lower limit of detection and wider linear response range for miRNA detection compared to the previous reports (Table S2). Such outstanding analytical performance is ascribed to the excellent signal-amplification ability of HCR synthesized enzyme-free reactor and the fantastic introduction of DA via CC as a linker. To validate the selectivity of the prepared PEC biosensor, miRNA-200 family members are employed to challenge the system, including 5 nM miRNA-429, 5 nM miRNA-200c, 5 nM

separation and suppress the electron−hole recombination, and hence increase the excitation and conversion efficiency. Because of the matched energy band, the recombination of photoinduced electron−hole pairs is suppressed and the lifetime of photoinduced electron−hole pairs is prolonged, which is favorable to ameliorate the PEC performance for subsequent miRNA assay. Optimal Conditions for the Fabrication of PEC Assay. The fabrication process of the PEC biosensor was studied by CV and PEC characterizations, and the results demonstrated the successful fabrication of the PEC biosensor (see more detail in the SI). To achieve an optimal analytical performance of the PEC biosensor, several experimental conditions were investigated (see the SI for more experimental details). As a PEC detection protocol, we first screened electron donors that affect the electron−hole recombinant. We selected these substances, including dopamine (DA), L-cysteine (L-cys), histidine (His), and L-glutathione oxidized (GSSG), as alternatives, because those substances have amino group which ensures they can be immobilized onto well-designed probe-N3, thus obtaining signal probe PX-N3 (X = DA, L-cys, His, and GSSG). As shown in Figure 4A, a doughty photocurrent is generated only when DA

Figure 4. Effects of (A) the screening of the electron donor, (B) HCR hybridization time, (C) CC reaction time, and (D) DA concentration, inset: PEC response for the different introduction methods of the electron donor (a, b, and c depict the results of three parallel measurements).

acts as an electron donor. Undoubtedly, the existence of DA can effectively suppress the electron−hole recombination via scavenging the photogenerated holes, leading to the photocurrent enhancement. When L-cys is presented, the photocurrent increases slightly. The reason may be that the SH groups of L-cys are mildly oxidized to form SS bonds, and the ability to suppress the electron−hole recombinant is limited. Thus, DA is chosen as the optimized electron donor for subsequent miRNA assay. The hybridization time of HCR was evaluated by using the photocurrent response. As shown in Figure 4B, the photocurrent increases with increasing incubation time and levels off after 2 h. Hence, 2 h is chosen as the optimized hybridization time for HCR. Under this condition, the reaction time of CC 11447

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22Rv1 cells rather than HeLa cells, which are in accordance with the previous report.30,31 The number of copies of miR-141 per cell was determined using our proposed method in 22Rv1 cell and HeLa cell (seen in Figure S6), which is in accordance with the previous reports.32,33 Therefore, the prepared PEC biosensor possesses a great potential for monitoring miRNAs in cancer cells for early diagnosis of cancers.

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CONCLUSIONS In summary, a preferred electron donor DA assembled with a well-designed probe-N3 (PDA-N3) is first fastened onto the substrate via metal-catalyst-free CC and applied in the PEC sensing platform for ultrasensitively HCR-based miRNA assay. Significantly, the PDA-N3 can not only be exponentially ligated onto the substrate through the enzyme-free HCR amplification strategy but also serve as a flexible trigger dramatically enhancing photocurrent through efficiently suppressing the electron−hole recombinant. Furthermore, because of the introduction pattern of electron donor DA, Bi2S3@MoS2 nanoflowers yield high photoactivity under visible-light illumination with effective consumption of DA electron donor. Meanwhile, the SPR effect of GNPs increases the light absorption and enhances the photoinduced charge separation, thus resulting in high photon-to-electron conversion efficiency. As expected, the well-established sensing platform presents outstanding PEC performance with an ultralow limit of detection and is successfully employed to detect miRNA-141 with highly specific response in practical analysis of tumor cells. This work paves a new pattern to introduce an electron donor as a flexible trigger, which promotes the effective consumption of the electron donor, resulting in an enhanced signal, and hints great potential for further application in early clinical diagnostics and biomedical research.

Figure 5. (A) Photocurrent responses of the PEC biosensor toward various concentrations of miRNA; (B) the relevant calibration curve; (C) selectivity of the PEC biosensor with different targets: 5 nM miRNA-429, 5 nM miRNA-200c, 5 nM miRNA-200b, 5 nM miRNA200a, 0.5 nM miRNA-141, and 0.5 nM miRNA-141 in mixed solution; and (D) application of the PEC sensing in various tumor cell lines: (a) blank, (b) 102 cells, (c) 103 cells, (d) 104 cells, (e) 105 cells, and (f) 106 cells of 22Rv1 and HeLa, respectively.

miRNA-200b, and 5 nM miRNA-200a. As depicted in Figure 5C, the contrast experiments were executed via replacing 0.5 nM miRNA-141 with above sequences, respectively. The biosensor shows negligible cross-reactivity to miRNA-429, miRNA-200c, miRNA-200b, miRNA-200a, and the mixture containing miRNA-141 and above sequences, indicating that only the perfectly matched sequence can trigger the amplification strategies and the designed protocol possesses good selectivity toward target against other control sequences. The matrix effect was studied. The photocurrent response of the proposed biosensor toward miRNA in buffer solution and in lysates was measured. As shown in Figure S5, the photocurrent signal responding to lysates was similar to that in TM buffer solution, certifying no matrix effect of the proposed method. The repeatability of the PEC biosensor is expressed in terms of values for a within-batch (intra-assay) and a between-batch (interassay) relative standard deviation (RSD). The resulting electrode incubated with 0.5 nM miRNA-141 is repeatedly determined six times, giving an intra-assay RSD of 4.5%. The interassay RSD on six modified electrodes is 6.3%. The results suggest a good repeatability of the developed PEC biosensor. To further evaluate the capacity of the PEC biosensor applied in tumor cell extractions analysis, HeLa (a human cervical cancer cell line with low miRNA-141 expression) and 22Rv1 (a human prostate carcinoma cell line with high miRNA141 expression29) were chosen to perform a PEC assay and survey miRNA-141 expression. As demonstrated in Figure 5D, when the cell concentration increases, the lysates from HeLa cells cause insignificant photocurrent enhancement compared to the blank buffer, suggesting the low expression of miRNA141 in HeLa cells. However, in the presence of lysates from 22Rv1 cells, obvious photocurrent response is observed in a concentration variation from 102 to 106 cells. The comparison results demonstrate the overexpression of miRNA-141 in

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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/acs.analchem.6b02481. Experimental details for reagents, apparatus, the preparation of Bi2S3@MoS2 nanoflowers, TSP and signal probe, the CV and PEC characterization, optimization, supplementary figures, tables, and references (PDF)

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AUTHOR INFORMATION

Corresponding Authors

*Tel: +86 23 68253237; Fax: +86 23 68253237; E-mail: [email protected] (H.Q.L.). *Tel: +86 23 68253237; Fax: +86 23 68253237; E-mail: linb@ swu.edu.cn (N.B.L.). Notes

The authors declare no competing financial interest.

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ACKNOWLEDGMENTS This work was financially supported by the National Natural Science Foundation of China (No. 21273174, 21675131), the Municipal Science Foundation of Chongqing City (No. CSTC2013jjB00002, CSTC-2015jcyjB50001), the Fund Project of Sichuan Provincial Academician (Expert) Workstation (No. 2015YSGZZ03), the Opening Project of Key Laboratory of Green Catalysis of Sichuan Institutes of High Education (No. LYJ1501, LYJ1402), the Fundamental Research Funds for the 11448

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(31) Yin, B. C.; Liu, Y. Q.; Ye, B. C. J. Am. Chem. Soc. 2012, 134, 5064−5067. (32) Liu, Y. Q.; Zhang, M.; Yin, B. C.; Ye, B. C. Anal. Chem. 2012, 84, 5165−5169. (33) He, X. W.; Zeng, T.; Li, Z.; Wang, G. L.; Ma, N. Angew. Chem., Int. Ed. 2015, 54, 1−5.

Central Universities of China (No. XDJK2016E054), and the Innovation Foundation of Chongqing City for Postgraduate (No. CYB14052).

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REFERENCES

(1) Dong, H.; Lei, J.; Ding, L.; Wen, Y.; Ju, H.; Zhang, X. Chem. Rev. 2013, 113, 6207−6233. (2) Yates, L. A.; Norbury, C. J.; Gilbert, R. J. Cell 2013, 153, 516− 519. (3) Esteban-Fernández de Avila, B. E.; Martín, A.; Soto, F.; LopezRamirez, M. A.; Campuzano, S.; Vásquez-Machado, G. M.; Gao, W. W.; Zhang, L. F.; Wang, J. ACS Nano 2015, 9, 6756−6764. (4) Whatley, S. D.; Mason, N. G.; Rhodes, J. M.; Stewart, M. F.; Reed, P.; Crowley, V.; Darby, C. M.; Badminton, M. N. Clin. Chem. 2013, 59, 1123−1125. (5) George, S.; Chaudhery, V.; Lu, M.; Takagi, M.; Amro, N.; Pokhriyal, A.; Tan, Y.; Ferreira, P.; Cunningham, B. T. Lab Chip 2013, 13, 4053−4064. (6) Jia, H.; Li, Z.; Liu, C.; Cheng, Y. Angew. Chem., Int. Ed. 2010, 49, 5498−5501. (7) Hong, C.; Baek, A.; Hah, S. S.; Jung, W.; Kim, D. E. Anal. Chem. 2016, 88, 2999−3003. (8) Becquerel, A. E. C R Acad. Sci. 1839, 9, 145−149. (9) Willner, I.; Patolsky, F.; Wasserman. Angew. Chem., Int. Ed. 2001, 40, 1861−1864. (10) Li, J.; Tu, W.; Li, H.; Bao, J.; Dai, Z. Chem. Commun. 2014, 50, 2108−2110. (11) Zhao, W. W.; Xu, J. J.; Chen, H. Y. Chem. Soc. Rev. 2015, 44, 729−741. (12) Zhao, W. W.; Xu, J. J.; Chen, H. Y. Chem. Rev. 2014, 114, 7421− 7441. (13) Wu, S.; Song, H.; Song, J.; He, C.; Ni, J.; Zhao, Y.; Wang, X. Anal. Chem. 2014, 86, 5922−5928. (14) Li, G. S.; Wu, L.; Li, F.; Xu, P. P.; Zhang, D. Q.; Li, H. X. Nanoscale 2013, 5, 2118−2125. (15) Shen, Q.; Han, L.; Fan, G.; Zhang, J. R.; Jiang, L.; Zhu, J. J. Anal. Chem. 2015, 87, 4949−4956. (16) Tahir, A. A.; Ehsan, M. A.; Mazhar, M.; Wijayantha, K. G. U.; Zeller, M.; Hunter, A. D. Chem. Mater. 2010, 22, 5084−5092. (17) Wang, S.; Li, X.; Chen, Y.; Cai, X.; Yao, H.; Gao, W.; Zheng, Y.; An, X.; Shi, J.; Chen, H. Adv. Mater. 2015, 27, 2775−2782. (18) Weng, B.; Zhang, X.; Zhang, N.; Tang, Z. R.; Xu, Y. J. Langmuir 2015, 31, 4314−4322. (19) Qian, C. G.; Zhu, S.; Feng, P. J.; Chen, Y. L.; Yu, J. C.; Tang, X.; Liu, Y.; Shen, Q. D. ACS Appl. Mater. Interfaces 2015, 7, 18581− 18589. (20) Zhuang, J.; Tang, D.; Lai, W.; Xu, M.; Tang, D. Anal. Chem. 2015, 87, 9473−9480. (21) Zhao, W. W.; Wang, J.; Zhu, Y. C.; Xu, J. J.; Chen, H. Y. Anal. Chem. 2015, 87, 9520−9531. (22) Thirumurugan, P.; Matosiuk, D.; Jozwiak, K. Chem. Rev. 2013, 113, 4905−4979. (23) Choi, J. Y.; Kim, Y. T.; Seo, T. S. ACS Nano 2013, 7, 2627− 2633. (24) Kato, D.; Oishi, M. ACS Nano 2014, 8, 9988−9997. (25) Chakrabarty, R.; Stang, P. J. J. Am. Chem. Soc. 2012, 134, 14738−14741. (26) Wang, F.; Lu, C. H.; Willner, I. Chem. Rev. 2014, 114, 2881− 2941. (27) Kahn, J. S.; Trifonov, A.; Cecconello, A.; Guo, W.; Fan, C.; Willner, I. Nano Lett. 2015, 15, 7773−7778. (28) Li, C.; Wang, H.; Shen, J.; Tang, B. Anal. Chem. 2015, 87, 4283−4291. (29) Zhang, H.; Huang, J.; Zhou, X.; Zhong, X. Inorg. Chem. 2011, 50, 7729−7734. (30) Liu, Y. Q.; Zhang, M.; Yin, B. C.; Ye, B. C. Anal. Chem. 2012, 84, 5165−5169. 11449

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