Sensitive Colorimetric Detection of MicroRNA Based on Target Catalyzed Double-arm Hairpin DNA Assembling
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1 ANALYTICAL SCIENCES JULY 2016, VOL The Japan Society for Analytical Chemistry Sensitive Colorimetric Detection of MicroRNA Based on Target Catalyzed Double-arm Hairpin DNA Assembling Rui TIAN and Xingwang ZHENG Key Laboratory of Analytical Chemistry for Life Science of Shaanxi Province, School of Chemistry & Chemical Engineering, Shaanxi Normal University, Xi an , Shaanxi, People s Republic of China The common drawbacks of the current colorimetric sensing platform using gold nanoparticles (AuNP) as an indictor is its relatively low sensitivity, which restrict their analytical application for low-level analytes, such as the detection of the microrna (mirna). In the present work, we developed a novel strategy to construct a colorimetric sensing platform for mirna based on target catalyzed hairpin DNA assembling. Unlike a single-stranded DNA probe or a single-arm hairpin structure DNA probe, in our strategy the double-arm hairpin structure DNA probe was first designed, and was further demonstrated to work well in catalysis the of hairpin DNA assembly reaction, which significantly enhanced the sensitivity of the AuNP based colorimetric sensing platform. In addition, compared to other mirna detection schemes reported previously, the proposed strategy is not only enzyme-free, label-free, immobilization-free, but also eliminates the need for any sophisticated instrumentation. The proposed strategy may open a new way to allow mirnas expression to be profiled in a decentralized setting, such as at point-of-care. Keywords Colorimetry, microrna detection, double-arm hairpin DNA, DNA assembly (Received January 21, 2016; Accepted March 22, 2016; Published July 10, 2016) Introduction MicroRNAs (mirnas) are a class of RNAs that play important regulatory roles in cells, such as cell proliferation, differentiation, metabolism and tumorigenesis, viral infection etc. 1 5 Thus the detection of mirnas is crucial for disease diagnosis and screening. Since many important mirnas are in quite low abundance in biological samples, many nucleic acid amplification techniques have been employed, such as RT-PCR, 6,7 ligase chain reaction, 8,9 ribozyme amplification, 10,11 loop-mediated isothermal amplification (LAMP), 12,13 exponential amplification reaction (EXPAR), 14 and rolling circle amplification (RCA). 15,16 These methods indeed have greatly improved the sensitivity of mirnas detection; however, they were highly enzyme dependent and label needed. Therefore, the development of simple, label-free, enzyme-free, and nontarget-amplification methods for mirna analysis is desired. A colorimetric assay based on unmodified AuNP has become an attractive method, since it avoids any complicated chemically modification, allows easy observation by the naked eye, and there is no requirement for sophisticated instruments. 17 Currently, the AuNP based colorimetric detecting systems have been applied to monitor different biological and chemical substances, such as DNA, RNA, proteins, and metal ions etc However, AuNP-based colorimetry suffered from the poor sensitivity. To overcome this shortcoming, many kinds of amplification strategies were introduced into the sensing platform and the detection sensitivity was significantly To whom correspondence should be addressed. zhengxw@snnu.edu.cn improved, but the use of enzymes and tag-labeling procedures of DNA probes still limits their analytical application for an ultra-low level target. In this work, a label-free, enzyme-free, immobilization-free strategy for improving the sensitivity of an unmodified AuNP based colorimetric sensing platform was developed by using a target-catalyzed hairpin DNA assembly. Furthermore, let-7a was selected as the model target to confirm our idea due to its important role in disease diagnosis and screening. Experimental Reagents and chemicals The oligonucleotides and mirnas used in this study were synthesized by Sangon Biotech Company, Ltd. (Shanghai, China). The sequences of all oligonucleotides are listed in Table 1. Chloroauric acid (HAuCl 4 4H 2O), trisodium citrate, sodium phosphate, sodium chloride and magnesium chloride were obtained from Sinopharm Chemical Reagent Co. Ltd. (Shanghai, China). Concentrated DNA stock solutions were prepared in a buffer, and were diluted to the reaction concentration before use. Sodium phosphate buffer (PBS, ph 7.4, Na 2HPO 4 NaH 2PO 4 10 mm, NaCl 200 mm, MgCl 2 5 mm) was prepared by dissolving a suitable amount of analytical-grade Na 2HPO 4, NaH 2PO 4, NaCl and MgCl 2 in ultrapure water. All other reagents were of analytical grade and used as received. Apparatus Absorption spectra were recorded on a TU1901 UV-vis spectrophotometer (PUXI optical equipment factory, China)
2 752 ANALYTICAL SCIENCES JULY 2016, VOL. 32 Table 1 Hairpin DNA and other oligonucleotides used in the experiments Name Sequence (5 3 ) H1 H2 L-H1 Target (t) Mis-1(t1) Mis-2(t2) Del-1(t3) AACTATACAACCTACTACCTCACATCGTTGAG- GTAGTAGGTTGTGGCTAG CTAGCCACAACCTACTACCTCAACGATGTGAG- GTAGTAGGTTGT AACTAT(FAM)ACAACCTACTACCTCACATCGT- TGAGGTAGTAGGTTGT(DABCYL)GGCTAG UGA GGU AGU AGG UUG UAU AGUU UGA GGU AGU AGG UUG UAU GGUU UGA GGU AGU AGG UUG UGU GGUU UGA GGU AGU AGG UUG UAU AGU The L-H1 was the fluorophore and quencher labeled H1. From 5 to 3 H1 was consisted of fragment 1, 2, 3, 2* and 4, H2 was consisted of fragment 4*, 2, 3* and 2*. The bold letters means the complementary sequence of the target and H1, the underlined parts means the complementary fragment in the hairpin DNA. at room temperature. Fluorescence spectra were recorded on an F-7000 fluorescence spectrophotometer (Hitachi, Japan). Transmission electron microscopy (TEM) measurements were made on a JEM-2100 transmission electron microscope (Hitachi, Japan). Preparation of gold nanoparticles Gold nanoparticles (~13 nm) were prepared by a citrate reduction of HAuCl In a typical experiment, a 5-mL aqueous solution of sodium citrate (38.8 mm) was added to a boiling solution of HAuCl 4 (50 ml, 1 mm). After the solution color changed to red, the reaction mixture was allowed to reflux for 15 min. Then, the solution was cooled to room temperature, filtered, and stored in a refrigerator at 4 C before use. Measurement procedure In a typical target detection assay, H1 and H2 were heated to 90 C for 2 min, and then allowed to cool to room temperature for 1 h before use; then, target samples were added to a mixture of H1 (100 nm) and H2 (100 nm) and well mixed. Then, 20 μl of the reaction mixture was added into an AuNP solution of 180 μl and incubated at room temperature for 3 h. Subsequently, 10 μl of 0.3 M sodium chloride solutions were added, and the mixed solutions were detected by either visual observations or UV-vis characterizations within 2 min. Results and Discussion Design of the double-arm hairpin DNA probe and verification of its working principle The foundation of the mirna detection principle is shown in Scheme 1. A double-arm hairpin probe DNA (H1) and a singlearm auxiliary probe DNA (H2) were designed. H1 has two overhang sticky regions at its 5 (fragment 1) and 3 (fragment 4) ends; H2 has one overhang sticky region at its 5 (fragment 4*) end; the overhang 5 sticky end (fragment 1) and stem (fragment 2) of H1 are complementary to the target, while the rest fragment of H1 (the overhang 3 sticky end (fragment 4), stem (fragment 2*) and the loop (fragment 3)) are complementary to H2. In the absence of a target, the paired 3 end of H1 (fragment 4) and 5 end of H2 (fragment 4*) can not open the stems of H1 and H2 to form a double-helix H1/H2, because both stems of H1 and H2 were longer than their complementary overhang sticky ends, Scheme 1 Schematic of the target catalyzed hairpin DNA assembly and gold nanoparticle based a colorimetric detection system (in H1 fragment 1, 4 respect to the overhang 5 and 3 end of the DNA line, fragment 3 respect to the loop, 2 and 2* respect to the complementary fragment of the stem; in H2 fragment 4* respect to the overhang 3 end, fragment 3* respect to the loop, 2 and 2* respect to the complementary fragment of the stem. 1-1*, 2-2*, 3-3* and 4-4* were the complementary fragment). and the hybridization power of the sticky ends of H1 and H2 can not open that two stems simultaneously according to the hybridization kinetics. 29,30 Thus, both H1 and H2 maintained their hairpin structures and coexisted in solution. In the presence of a target, the target can hybridize with H1 from the overhang 5 sticky end, and open the hairpin through the toehold-mediated strand-displacement interaction to form the target/h1 (fragment 1 2) half duplex structure. The opened H1 then exposes a new single strand fragment (including fragment 3, 2*, 4); this new single-strand fragment can hybridize with H2 from its overhang 5 sticky end (fragment 4*), and opens the hairpin structure of H2 through the toehold-mediated strand-displacement interaction and form the target/h1/h2 complex. The opened H2 expose the new single strand fragment (fragment 2*), which was also complementary to H1 (fragment 2 of H1). Because the H1/H2 duplex has a longer complementary base pairs sequence than that of target/h1, it was more stable than target/h1. Thus, the exposed single strand fragment of H2 (fragment 2*) can replace the target and form the H1/H2 duplex, and then make the target release. The released target then becomes available to trigger another reaction cycle to form more H1/H2 duplexes. When AuNP was added into a solution that did not contain the target, the free sticky ends of H1 and H2 could be closely adsorbed onto the AuNP, and thus prevent any salt-induced AuNP aggregation. On the contrary, when the AuNP was added into the solution which contained the target, since the target can trigger formation of the H1/H2 duplex, and make their negatively charged phosphate backbone exposed. 31,32 Thus, the strong repulsion between double stranded DNA and negatively charged AuNP made the DNA away from the AuNP surface. As a result, AuNP will aggregate and cause the red-to-blue color variation. Based on this, the AuNP based colorimetric can be used to detect the target in solution. To evaluate the target recycle mechanism in the proposed sensing strategy, a fluorescence signal readout method was used to monitor the assembly of the DNA probes. First, a fluorophore and fluorescent quencher double-labeled H1 was designed and named as L-H1 (the structure of L-H1 is shown in Table 1), in the absence of the target, L-H1 form a hairpin structure due to binding of the complementary fragment (the underlined part) of the sequences. Thus the fluorophore was close to the fluorescent quencher and the fluorescence of the fluorophore was quenched,
3 ANALYTICAL SCIENCES JULY 2016, VOL Fig. 1 Fluorescence demonstration of the target catalyzed hairpin DNA assembly (the black bar indicates the initial fluorescence intensity of the systems and the red bar indicates the fluorescence intensity of the systems after 3 h reaction). (A) Fluorescence intensity of the test system contain 100 nm L-H1; (B) fluorescence intensity of the test system contain 100 nm L-H1 and 2 nm target; (C) fluorescence intensity of the test system contain 100 nm L-H1 and 100 nm H2; (D) fluorescence intensity of the test system contain 100 nm L-H1, 100 nm H2 and 2 nm target. and the system showed weak fluorescence; when the target appears, it will hybridize with and open the hairpin structure of L-H1 make the fluorophore away from the quencher and restore its fluorescence. Then, four test systems consisting of L-H1; L-H1 and the target; L-H1 and H2; L-H1, H2 and the target were prepared and their fluorescence intensities were measured to investigate the reactions of the systems. The results showed (Fig. 1) that after incubation for 3 h, the fluorescence intensities of the designed four test systems were different. For test one, its fluorescence intensity showed no change; this was because the hairpin structure of L-H1 had no change in the experiment condition, and L-H1 maintained its hairpin structure and the fluorescence was still quenched. For test two, which contained L-H1 and the target, its fluorescence intensity showed an increase, because the target could hybridize with L-H1 and open the hairpin structure of L-H1 and make the quencher more away from the fluorophore, and thus restore its fluorescence. For the third solution, which contained L-H1 and H2, its fluorescence intensity almost did not present any change, too; this was because L-H1 and H2 can not hybridize spontaneously in the test condition and both maintain their hairpin structures, respectively, the fluorescence of L-H1 was still quenched. However, for a system that contained the target, L-H1 and H2, its fluorescence intensity had a significantly increase, because the hybridization of the target and L-H1 could open the hairpin structure of L-H1 and restore its fluorescence. More importantly, the opened L-H1 can hybridize with H2 through the toeholdmediated strand-displacement interaction, and further replace and release the target. Then, the released target can cyclic catalytze the assemblies of L-H1 and H2, and cause more L-H1 to open, and restore their fluorescence; thus, the fluorescence intensities of the system increased significantly. Those results clearly indicate that the target can cyclic catalyze assembling of the designed DNA probes of H1 and H2. Colorimetric readout of the target catalyzed hairpin DNA assembly In order to demonstrate that the proposed reaction of a mirna-catalyzed hairpin DNA assembly could be used to detect mirna by a label-free AuNP-based colorimetric assay. Fig. 2 Absorption spectra of the H1/H2/AuNP system in the absence (curve 1) and presence (curve 2) of let-7a. The absorption spectra of the H1/H2/AuNP systems were recorded, the results (Fig. 2) of which showed that: in the absence of let-7a, the maximum absorption band of H1/H2/AuNP system was in about 520 nm, and the color of the solution appeared to be pink after the addition of salt (Fig. 2, inset, centrifuge tube 1). However, when same amount of salt was add to a system that contained let-7a, the absorbance peak at 520 nm showed a decrease, and a new absorption band at about 630 nm appeared (Fig. 2, curve 2). This corresponded to the color of the solution turned to blue violet (Fig. 2, inset, centrifuge tube 2). The reason was that, in the absence of let-7a, H1 and H2 could maintain their hairpin structure, and their hanging arms could be adsorbed onto the AuNP surface to stabilize the AuNP to against salt-induced aggregation. Thus, the color of the AuNP system remained pink. Conversely, in the presence of let-7a, it can catalyze the assembling of H1 and H2, because the produced H1/H2 duplex provides little stabilization to the AuNP against salt-induced aggregation. Thus, the aggregation states of AuNP were formed, and the color of the AuNP system changed to blue-violet. In addition, the TEM values were also used to investigate these AuNP-based reactions. The TEM images (Fig. S1, Supporting Information) showed that the AuNP were nearly monodispersed in the absent of let-7a. However, irregular gathered AuNP were observed in the presence of let-7a. These results suggested that the designed DNA probes could be used to detect mirna based on a labelfree AuNP-based colorimetric assay. Investigation into the stability ability of the single and doublearm hairpin DNA towards gold nanoparticles For an AuNP-based colorimetric sensing platform, the protection ability of the DNA probes to AuNP was very important, because it strongly affected the ratio of the signal to noise of this sensing platform. Compared to previously report hairpin DNA probes, the probe DNA in this work has a doublearm structure, so the protecting ability of the single-arm and double-arm DNA probes to AuNP were investigated. The same amounts of H1 and H2 were firstly added to the two AuNP solutions, respectively, and incubated for 30 min. Then, suitable concentration salt solutions were added to the above H1/AuNP and H2/AuNP solutions. Our results showed that, along with the adding the salt, the color of the H1/AuNP and H2/AuNP both began to change, but the color of H2/AuNP showed a more obvious change than that of H1/AuNP (Fig. S2, Supporting Information). This result indicated that H1 has a stronger
4 754 ANALYTICAL SCIENCES JULY 2016, VOL. 32 Fig. 3 UV-vis spectra of the AuNP solution in the presence of different concentrations of target (A), the concentration of target from bottom to top was 0, 0.005, 0.01, 0.05, 0.1, and 2.0 nm, respectively. (Inset: solution color after the addition of salt) and plot of target concentration vs. A 630/A 520 ratio for the target DNA assay (B) (Inset: linear calibration curve of the A 630/A 520 ratio change to logarithm of target concentration). protecting ability to AuNP than that of H2. The reason may be imaged by observing Fig. S3 in Supporting Information, since both the two arm of H1 could simultaneously adsorb onto the AuNP, and it provide stronger protecting ability to the AuNP to against salt-induced aggregation. In contrast, as for H2, since it only has one arm to be adsorbed to the AuNP, and it thus has poor protection ability to the AuNP. Optimization of experimental conditions To optimize the chemical conditions for the colorimetric sensing of mirna, various factors, such as the incubation time of the H1/H2/AuNP detection system, the concentration of the probe DNA, AuNP and the salt concentration were examined in detail, respectively. The effects of the incubation time of H1/H2/AuNP detection system were examined by detecting the absorbance ratio (A 630/A 520) of the detection system. The results showed (Fig. S4, Supporting Information) that from 0 to 2.5 h, the signal-to-noise ratio of the system increased continuously; after that, the signal-to-noise ratio was almost constant. Taking into account the signal-to-noise ration of the system, 3 h of incubation time was selected for further experiments. The concentration of AuNP, the probe DNA and the salt concentration will sharply influence this colorimetric assay, so the influence of the concentration of the AuNP, probe DNA and salt to the colorimetric assay were all studied (Fig. S5, Supporting Information). According to our results, the concentration of the AuNP, DNA probe and NaCl were chosen to be 1.4 nm, 100 nm, and 0.3 M, respectively. Analytical performance To quantitatively detect let-7a with the developed method, the absorption spectra of the detection system in the presence of different concentrations of let-7a were recorded. The results showed (Fig. 3A) that the absorbance of AuNP at 520 nm gradually decreased, the absorbance at 630 nm showed a gradual increase with the increase of let-7a. Also, there was a good linear correlation between the absorbance ratio of A 630/A 520 and the logarithm (lg) of the let-7a concentration in the range of to 2 nm (Fig. 3B). The linear-regression equation was A 630/A 520 = log c (R = ), and the detection limit that was taken to be three-times the standard derivation in a blank solution is 3 pm, which is lower than that of the Fig. 4 UV-vis absorption spectra for the colorimetric detection of various targets (concentration of mirna was 2 nm, insert colorimetric responses photograph of the solution after addition of various mirna: (1) H1/H2 with salt; (2) H1/H2/t1 with salt; (3) H1/H2/t3 with salt; (4) H1/H2/t2 with salt; (5) H1/H2/t with salt). colorimetric detection of DNA previously reported. 33 This may be because the double-arm hairpin probe DNA could protect AuNP from aggregation more efficiently, and thus reduce the background signal, besides, that the length of the sticky ends of the obtained double-stranded DNA may also influence the detection sensitivity. To test the selectivity of the proposed colorimetric sensing method, three let-7 mirna family members (let-7b (t1), let-7c (t2) and let-7g (t3)) were selected as the potential interference, and tested using the same method of let-7a. As shown in Fig. 4, upon the addition of salt, there was only a slight spectral change in the presence of let-7b, let-7c and let-7g. This means that the mismatched mirna is difficult to initialize the hairpin DNA assembling and induce aggregation of AuNP; only the matched target triggered the reaction obviously. The sequence specificity of the target assay is attributed to the requirement of full complementarity between the trigger and the probe hairpin DNA (H1) in the target-triggered hairpin DNA assembling system. The results indicated that the method has high specificity for let-7a detection.
5 ANALYTICAL SCIENCES JULY 2016, VOL Table 2 Detection of let-7a in synthetic samples Sample Application of the method In order to evaluate the application of this assay for the detection of let-7a in a biological system, this assay was used to detect let-7a in synthetic samples. The total RNA samples were isolated from the human breast adenocarcinoma cells using Trizol Reagent and a dispersed PBS buffer solution (10 mm, ph 7.4, 0.1 M NaCl). 34 Then let-7a was added for the detection of let-7a by the standard-addition method. The results are given in Table 2, which show that the method has high accuracy. Conclusions In conclusion, we have developed a simple, label-free, enzymefree, immobilization-free target catalyzed hairpin DNA assembling-based colorimetric method for mirna detection. The key feature of the proposed method is the design of the double-arm hairpin DNA probe. Also, in the target catalytic hairpin DNA assembly, the design of the double-arm hairpin probe can decrease the background signal of the AuNP based colorimetric assay, and the target recycles have a signal amplifying ability. According to this idea, the design of the new functional DNA probe may open a new way to detect analytes with an AuNP colorimetric sensing platform. Acknowledgements This work was financially supported by the National Natural Foundation of China (Grant ), and the Fundamental Research Funds for the Central Universities (Grant ). Supporting Information TEM images of the H1/H2/AuNP system and protection of hairpin DNA to the unmodified gold nanoparticle etc. were provided as Supporting Information. This material is available free of charge on the Web at References Amount added/pm Amount detected/pm RSD, % (n = 3) Recovery, % B. D. Aguda, Y. Kima, M. G. Piper-Hunter, A. Friedmana, and C. B. Marsh, Proc. Natl. Acad. Sci. U. S. A., 2008, 105, J. R. Buchan and R. Parker, Science, 2007, 318, G. A. Calin and C. M. Croce, Nat. Rev. Cancer, 2006, 6, C. S. Sullivan and D. Ganem, Mol. Cell, 2005, 20, C. M. Croce and G. A. Calin, Cell, 2005, 122, C. Chen, D. A. Ridzon, A. J. Broomer, Z. Zhou, D. H. Lee, J. T. Nguyen, M. Barbisin, N. L. Xu, V. R. Mahuvakar, M. R. Andersen, K. Q. Lao, K. J. Livak, and K. J. Guegler, Nucl. Acids Res., 2005, 33, e C. K. Raymond, B. S. Roberts, P. Garrett-Engele, L. P. Lim, and J. M. Johnson, RNA, 2005, 11, J. L. Yan, Z. P. Li, C. H. Liu, and Y. Q. Cheng, Chem. Commun., 2010, 46, Z. Yuan, Y. Zhou, S. Gao, Y. Cheng, and Z. Li, ACS Appl. Mater. Interfaces, 2014, 6, J. S. Hartig, I. Grüne, S. H. Najafi-Shoushtari, and M. Famulok, J. Am. Chem. Soc., 2004, 126, D. M. Zhou, W.-F. Du, Q. Xi, J. Ge, and J.-H Jiang, Anal. Chem., 2014, 86, C. Li, Z. Li, H. Jia, and J. Yan, Chem. Commun., 2011, 47, Y. Yu, Z. Chen, L. Shi, F. Yang, J. Pan, B. Zhang, and D. Sun, Anal. Chem., 2014, 86, G. Wang and C. Zhang, Anal. Chem., 2012, 84, H. Liu, L. Li, L. Duan, X. Wang, Y. Xie, L. Tong, Q. Wang, and B. Tang, Anal. Chem., 2013, 85, Y. Wen, Y. Xu, X. Mao, Y. Wei, H. Song, N. Chen, Q. Huang, C. Fan, and D. Li, Anal. Chem., 2012, 84, N. L. Rosi and C. A. Mirkin, Chem. Rev., 2005, 105, M. C. Daniel and D. Astruc, Chem. Rev., 2004, 104, K. Saha, S. S. Agasti, C. Kim, X. Li, and V. M. Rotello, Chem. Rev., 2012, 112, H. Li and L. Rothberg, Proc. Natl. Acad. Sci. U. S. A., 2004, 101, F. Xia, X. Zuo, R. Yang, Y. Xiao, D. Kang, A. Vallée- Bélisle, X. Gong, J. D. Yuen, B. B. Y. Hsu, A. J. Heegera, and K. W. Plaxco, Proc. Natl. Acad. Sci. U. S. A., 2010, 107, X. Xu, J. Zhang, F. Yang, and X. Yang, Chem. Commun., 2011, 47, E. Tan, J. Wong, D. Nguyen, Y. Zhang, B. Erwin, L. K. Van Ness, S. M. Baker, D. J. Galas, and A. Niemz, Anal. Chem., 2005, 77, J. Zhao, T. Liu, Q. Fan, and G. Li, Chem. Commun., 2011, 47, J. Li, H. Fu, L. Wu, A. Zheng, G. Chen, and H. Yang, Anal. Chem., 2012, 84, L. Ou, P. Jin, X. Chu, J. Jiang, and R. Yu, Anal. Chem., 2010, 82, C. Yan, C. Jiang, J. Jiang, and R. Yu, Anal. Sci., 2013, 29, J. J. Storhoff, R. Elghanian, R. C. Mucic, C. A. Mirkin, and R. L. Letsinger, J. Am. Chem. Soc., 1998, 120, D. Y. Zhang and E. Winfree, J. Am. Chem. Soc., 2009, 131, A. J. Genot, D. Y. Zhang, J. Bath, and A. J. Turberfield, J. Am. Chem. Soc., 2011, 133, H. Li and L. Rothberg, J. Am. Chem. Soc., 2004, 126, R. Kanjanawarut and X. Su, Anal. Chem., 2009, 81, P. Liu, X. Yang, S. Sun, Q. Wang, K. Wang, J. Huang, J. Liu, and L. He, Anal. Chem., 2013, 85, P. Zhang, J. Zhang, C. Wang, C. Liu, H. Wang, and Z. Li, Anal. Chem., 2014, 86, 1076.
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