Highly Sensitive Bisphenol-A Electrochemical Aptasensor Based on

Jun 22, 2016 - Given the easy design of the aptasensor, this analytical device constitutes a promising method to monitor the occurrence of BPA in food...
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Highly Sensitive Bisphenol‑A Electrochemical Aptasensor Based on Poly(Pyrrole-Nitrilotriacetic Acid)-Aptamer Film Imen Kazane,†,‡ Karine Gorgy,† Chantal Gondran,† Nicolas Spinelli,† Ali Zazoua,‡ E. Defrancq,† and Serge Cosnier*,† †

Univ. Grenoble Alpes, Département de Chimie Moléculaire, UMR CNRS 5250, 570 rue de la Chimie, CS 40700, 38058 Grenoble cedex 9, France ‡ Université de Jijel, Laboratoire de Matériaux: Elaborations-Propriétés-Applications, BP 98, Ouled Aissa, 18000 Jijel, Algeria

ABSTRACT: An electrochemical highly sensitive aptasensor was developed based on electropolymerized poly(pyrrolenitrilotriacetic) acid film and a new aptamer functionalized by a pentahistidine peptide for the quantification of bisphenol A. A surface coverage of antibisphenol A aptamer of 1.84 × 10−10 mol cm−2 was estimated from the electrochemical signal of the [RuIII(NH3)6]3+ complex bound by electrostatic interactions onto the aptamer-modified electrode. The binding of bisphenol A onto the polymer film was successfully characterized by electrochemical methods as square wave voltammetry and electrochemical impedance spectroscopy measurements. The designed label-free impedimetric aptasensor displayed a wide linear range from 10−11 to 10−6 mol L−1 with a sensitivity of 372 Ω per unit of log of concentration and an excellent specificity toward interfering agents such as 4,4′-dihydroxybiphenyl and bisphenol P.

B

isphenol A (2,2-bis(4-hydroxyphenyl)propane, BPA)1 is an organic monomer widely used in the industry for the production of polycarbonate and epoxy and polystyrene resins especially used for dental sealants and food packaging. This chemical compound has been identified as an endocrine disruptor.2 Because of its ability to mimic both the structure and function of the 17-β estradiol hormone,3−6 it can bind with estrogen receptors and can therefore have negative effects on health.7−9 Because of its toxicity, bisphenol A has received the attention of regulatory laws and despite the fact that bisphenol A is forbidden in baby bottles since 2011 in all European countries,10 this endocrine disrupter can still be found in surface water.11 According to EFSA (European Food Safety Authority), the current tolerable intake of bisphenol A of 4 μg/ kg weight per day is reported.12 As a consequence, it is really important to develop sensitive and easy methods to quantify bisphenol A and to remove it from aqueous solution.13Up until now, different analytical methods have been used successfully for BPA quantification such as liquid or gas chromatography alone or coupled with other techniques such as mass spectrometry.14−17 Although these sensitive techniques allow a low detection limit of BPA, they are expensive, time© 2016 American Chemical Society

consuming, nonadapted to on-site monitoring, and require qualified operators. Among analytical methods, biosensors are of great interest due to their high sensitivity, miniaturization, and low cost.18 Many devices using enzymes19−24 or antibodies25−27 have been designed for the detection of bisphenol A by developing original strategies to immobilize the biomolecules at the surface of the transducer. Some of the papers used advanced materials such as mutiwalled carbon nanotubes, graphene, polymers, or gold nanoparticules to improve sensitivity and detection limit. On the other hand, aptasensors28−33 based on the utilization of synthesized RNA or DNA nucleic acids obtained by systematic evolution of ligands by exponential enrichment (SELEX)34−36 have received these last years great interest; besides the fact that the production of aptamers does not require an immune response in host animals, the synthesized aptamers are stable, can bind the target with high affinity and specificity, and can be easily modified permitting their immobilization over a wide range of transReceived: April 21, 2016 Accepted: June 22, 2016 Published: June 22, 2016 7268

DOI: 10.1021/acs.analchem.6b01574 Anal. Chem. 2016, 88, 7268−7273

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Analytical Chemistry ducers. Since the first selection in 2011 of the anti-BPA aptamer,37 many devices and aptasensors38−47 based on optical, spectroscopic, and electrochemical measurements were reported. It was demonstrated that electrochemical transduction can be used to detect the binding process of BPA. For instance, it was reported the use of an electrochemical probe as methylene blue or ferrocene or ferricyanide to investigate the interaction between aptamer and BPA by cyclic voltammetry, differential pulse voltammetry, or by electrochemical impedance spectroscopy. We report here the original synthesis of an anti-BPA aptamer conjugated at its 5′-end with a pentahistidine peptide and its use for the design of an impedimetric BPA aptasensor. Usually, the histidine tag is widely used in recombinant protein purification, and in this paper, the introduction of an histidine tag is dedicated to the noncovalent binding of the aptamer onto electrodes previously modified by polypyrrole nitrilotriacetic films; it constitutes indeed a powerful method of aptamer immobilization onto the transducer surface. This immobilization method, already used by our group48,49 to elaborate immunosensors or aptasensors for HIV DNA or thrombin, occurs via the histidine axial ligation onto Cu complex chelated by the polypyrrole film. This easy procedure and the close proximity at the molecular level between the immobilized probe and the modified electrode surface confers an high sensitivity for the detection of the aptamer/BPA folding. In this work, we have investigated the immobilization of BPA aptamer and the binding of BPA and its analogues by electrochemical impedance spectroscopy and square wave voltammetry.

lithium perchlorate (LiClO4, from Fluka) as supporting electrolyte in the presence or not of perchloric acid. A Pt wire placed in a separated compartment was used as the counter electrode. The Ag/AgNO3 (0.01 mol L−1 in CH3CN + 0.1 mol L−1 LiClO4) electrode served as a reference in organic solution, and the saturated calomel electrode was used in aqueous solutions. The BPA stock solution was first prepared in absolute ethanol at a concentration of 10−4 mol L−1 and kept at 4 °C. The diluted BPA fresh solutions are prepared in phosphate phosphate buffer pH 7.4 with NaCl 10−2 mol L−1, MgCl2 10−3 mol L−1, and KCl 5 × 10−3 mol L−1. The hydroquinone solutions were prepared daily in phosphate buffer, pH = 7.4. Electrodes Preparation. As previously described,49 the poly(pyrrole-NTA) films were electrogenerated by a galvanostatic method (2.5 × 10−3 C cm−2, I = 10 μA, t = 18 s) of pyrrole-NTA (5 × 10−3 mol L−1) in CH3CN + 0.1 mol L−1 LiClO4 containing perchloric acid. Before use, 15 μL of the aptamer 2.9 × 10−7 mol L−1 dissolved in 0.1 mol L−1 phosphate buffer solution are heated during 5 min at 90 °C, cooled at 4 °C during 15 min, and left 5 min at 25 °C before deposition at the surface of the modified polypyrrole-NTA/Cu 2+. After incubation for 45 min at 5 °C, the electrode is rinsed under agitation in a phosphate buffer solution 0.1 mol L−1, pH 7.4. After injection of the desired amount of bisphenol A in the electrochemical cell, the EIS measurement and SWV are registered 30 min later in order to get reproducible results. Apparatus. Electrochemical studies were carried out using a conventional three-electrode potentiostat coupled to a PGSTAT 100. The working electrode was a glassy carbon electrode (diameter 3 mm) thoroughly cleaned using 20 μm diamond paste and rinsed with acetone, ethanol, and distilled water before use. The electrochemical impedance measurements were performed using FRA software, and square wave voltammetry and cyclic voltammetry measurements were performed using GPES software at 25 °C by immersing the electrode into phosphate buffer (pH 7.4) containing hydroquinone (10−3 mol L−1 or 2 × 10−3 mol L−1) as a redox probe. For impedance, the frequency sweep was from 50 000 to 0.01 Hz at a potential of 0.325 V/SCE with an ac amplitude of 5 mVrms. The potential of 0.325 V was chosen to be in the linear part of the stationary curve I = f(E). The ZView software was used to fit the experimental impedance data with the appropriate equivalent electrical circuit. The square wave voltammograms were recorded from 0.00 to 0.80 V with a step potential of 5.1 mV and amplitude of 0.2505 V.



EXPERIMENTAL SECTION General Procedures. All reagents used were of analytical grade and were purchased from Sigma-Aldrich. Quantification of antibisphenol A was performed at 260 nm using Cary 400 scan UV−visible spectrometer (ε = 1 026 600 L mol−1 cm−1); ε was estimated according to the nearest neighbor model. Synthesis of the Aptamer. The antibisphenol A aptamer37 conjugated with a polyhistidine tag was synthesized adapting a procedure previously reported in the literature.48 Briefly, the 5′diol antibisphenol A aptamer (5′X GGG CCG TTC GAA CAC GAG CAT GCC GGT GGG TGG TCA GGT GGG ATA GCG TTC CGC GTA TGG CCC AGC GCA TCA CGG GTT CGC ACC AGG ACA GTA CTC AGG TCA TCC TAG3′; X = diol) was synthesized50 at the 0.2 μmol scale using standard β-cyanoethyl phosphoramidite chemistry on a DNA synthesizer (ABI 3400). After elongation, it was cleaved from solid support and deprotected by treatment with 28% ammonia (1.5 mL) for 16 h at 55 °C. After evaporation it was suspended in water (200 μL) and subjected to sodium meta-periodate treatment (0.86 mg, 4 μmol) for 30 min and desalted on Sephadex G-25 cartridges (NAP-10, GE Healthcare). Coupling with aminooxy containing penta-histidine peptide (0.23 mg, 0.3 μmol) was carried out in 500 μL of ammonium acetate buffered solution (0.4 mol L−1, pH 4.5) during 4 h. In total, 50 μg (1.5 nmol) of antibisphenol A aptamer conjugated with pentahistidine was obtained after polyacrylamide gel electrophoresis purification under denaturing conditions. Synthesis of the Monomer. The pyrrole-nitrilotriacetic acid monomer (pyrrole-NTA) has been synthesized as described previously.51 Electrochemical Studies. All electrochemical investigations in organic medium were performed in acetonitrile (CH3CN, HPLC grade, from Rathburn) solutions, using



RESULTS AND DISCUSSION Characterization of the Developed Aptasensor. In order to validate the aptasensor configuration, the postulated successive anchoring of aptamer onto the polymer film and then BPA by aptamer recognition was investigated by cyclic voltammetry measurements. Figure 1 shows the cyclic voltammogram of hydroquinone (2 × 10−3 mol L−1) onto glassy carbon electrode modified by poly(pyrrole-NTA)-Cu2+ (Figure 1a), after incubation during 45 min with the antibisphenol aptamer (Figure 1b) and then in the presence of 10−6 mol L−1 of BPA in solution (Figure 1c). The redox signal of hydroquinone at the modified electrode without aptamer is composed of a couple of anodic and cathodic peaks at 0.345 and −0.151 V (ΔEp = 0.496 V), respectively. After 7269

DOI: 10.1021/acs.analchem.6b01574 Anal. Chem. 2016, 88, 7268−7273

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Analytical Chemistry

To confirm these experimental results, the permeability values were evaluated. The Koutecky−Levich curves were obtained by plotting the current intensities of the redox probe as a function of the inversed square root of the rotation speed. The straight lines obtained successively for the polymer film, the polymer film modified by the aptamer, and in the presence of 10−6 mol L−1 of bisphenol A give a positive intercept whose values allow one to calculate the film’s permeability. The permeability value (Pm) of the material decreases successively from 3.57 × 10−1 cm s−1 to 3.97 × 10−2 cm s−1 after anchoring of the aptamer and reaches a value of 2.72 × 10−2 cm s−1 in the presence of 10−6 mol L−1 BPA in the electrochemical cell. These results associated with the cyclic voltammetry measurements clearly indicate the binding of the aptamer onto the polymer via the histidine tags and then that it is still accessible for the complexation of BPA. They confirm without ambiguity the efficiency of the molecular architecture to detect BPA. In order to determine the amount of aptamer immobilized at the surface of the electrode, the modified electrode was incubated in a solution of [RuIII(NH3)6]3+ 10−2 mol L−1 in phosphate buffer pH = 7.4 (Figure 2A). After rinsing the modified electrode several times under stirring in phosphate buffer, the cyclic voltammogram recorded between 0.00 V and −0.50 V displays a redox system at E1/2 = −0.34 V, characteristic of the RuIII/RuII couple electroactivity, indicating the successful immobilization of the complex onto the aptamer modified electrode (Figure 2B). In addition, it appears that the current intensity of this peak system varies linearly with the scan rate. This corroborates that the process is not controlled by a diffusion process of [RuIII(NH3)6]3+ but ascribed to the immobilization of this redox compound by electrostatic interactions onto the negatively charged aptamer at physiological pH. This immobilization is a result of the compensation of three phosphate residues charged 1− by one Ru complex charged 3+. By integrating the signal under the redox system (Q = 1.44 × 10−5 C), the surface concentration of RuIII was estimated at Γ = 6.63 × 10−9 mol cm−2, by using equation ΓRu

Figure 1. Cyclic voltammograms of hydroquinone (2 × 10−3 mol L−1) in 0.1 mol L−1 phosphate buffer solutions, pH = 7.4 until a switching potential of 0.65 V. Scan rate 100 mV s−1: (a) for the modified polymer electrode, (b) after anchoring of the aptamer, and (c) in the presence of 10−6 mol L−1 of BPA. Reference electrode: SCE.

incubation of the modified electrode with the aptamer, these peaks are shifted, respectively, to 0.400 and −0.185 V (ΔEp = 0.585 V) indicating the formation of a barrier for diffusion and/ or electron transfer of the electrochemical probe. This phenomenon reflects the anchoring of the aptamer via the coordination of its histidine groups onto the Cu2+ complex chelated by the polymerized NTA groups. In the presence of 10−6 mol L−1 of BPA in electrolyte solution, the diffusion associated with the electron transfer of hydroquinone are slowed, as can be proved by the decrease of both anodic and cathodic peak intensities associated with an ΔEp increase from 0.585 to 0.738 V. These results suggest a rearrangement of the conformation52 of the aptamer to detect BPA, which is less favorable for the hydroquinone diffusion toward the underlying electrode surface.

Figure 2. (A) Schematic representation of the immobilization of [RuIII(NH3)6]3+ at the surface of the aptamer modified electrode in order to determine the Ru III surface coverage. (B) Cyclic voltammogram of the aptamer modified electrode registered at 50 mV s−1 (a) before and (b) after incubation of the electrode in a solution of phosphate buffer 0.1 mol L−1 containing [RuIII(NH3)6]3+ 10−2 mol L−1 and after rinsing of the electrode under agitation. Reference electrode: SCE. 7270

DOI: 10.1021/acs.analchem.6b01574 Anal. Chem. 2016, 88, 7268−7273

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Analytical Chemistry = Q/(nFS) where Γ is the surface coverage, n the number of exchanged electron which is equal to 1, F the Faraday’s constant, and S the surface of the electrode. This value allows calculating the DNA surface coverage (ΓDNA = 3 × ΓRu/108) at 1.84 × 10−10 mol cm−2 by considering that all the 108 phosphate groups of the aptamer are available to interact electrostatically with the ruthenium cation. Electrochemical Impedance Spectroscopy (EIS) and Square Wave Voltammetry (SWV) Measurements. The electrochemical impedance spectroscopy (EIS) measurements were carried out at 0.325 V by using the redox probe hydroquinone in 0.1 mol L−1 phosphate buffer (pH 7.4). Figure 3A shows the spectra without BPA (curve a) and in the

(j0) as a function of the logarithm of BPA concentration, a linear range between 10−10 and 10−6 mol L−1 is obtained (Figure 4) with a sensitivity of 12.32 μA cm−2 per order of magnitude. The calibration curve was compared thereafter with the one obtained with the EIS.

Figure 4. Calibration curve for the BPA biosensor corresponding to the changes in SWV of the electrode upon detection of different BPA concentrations. Experimental (dots) and linear regression (lines) are presented. Experimental conditions are the same as Figure 3B.

For this purpose, the impedance experimental values were fitted to a standard Randles equivalent circuit: this circuit is composed by the ohmic resistance Rel of the electrolyte solution and film, the charge transfer resistance Rct, in series with the diffusion-limited Warburg impedance and in parallel to a constant phase element (CPE) instead of a classic double layer capacitance Cdl in order to take in account the inhomogeneity of the surface. The curve passing through the data points in Figure 3A represents the fitting curve using this equivalent circuit described below. As can be seen, its superposition on the data points indicated a good match of the model with the measured data. The values of the equivalent circuit elements obtained by the experimental data fitting are reported in Table 1. The charge transfer resistance, Rct, increases strongly with the addition of BPA, which means that the BPA binding hinders the efficient electron transfer between the electrode and the redox probe. These data corroborate the preceding results obtained both by SWV and CV measurements. Besides, the configuration change of the aptamer has a direct impact on two other parameters listed in Table 1, which are the double layer capacitance, Cdl, and the parameter of the homogeneity of the interface, n. The double layer capacitance is about 10 μF cm−2, which is standard in aqueous solution, and it decreases with increasing the concentration of BPA. This decrease certainly indicates an increase of the thickness of the double layer. In regards to the parameter n, it increases with increasing the concentration of BPA indicating better homogeneity of the interface. Finally, the low frequency impedance loop provides the diffusion resistance, Rdiff. Besides, in Table 1, we see that diffusion resistance increases with the concentration of BPA. Proportionally, this increase is less than that of charge transfer resistance. Diffusion is thus less affected by the presence of BPA than the charge transfer. A calibration curve demonstrating BPA detection was established by plotting Rct as a function of the logarithm of BPA concentration. As can be seen in Figure 5, a linear section is obtained between 10−11 and 10−6 mol L−1, with a sensitivity of 372 ± 6 Ω per order of magnitude demonstrating the

Figure 3. (A) Nyquist plot of impedance spectra obtained at different concentrations of BPA on polypyrrole-NTA/Cu2+/aptamer electrode: (a) 0, (b) 10−11, (c) 10−10, (d) 10−9, (e) 10−8, (f) 10−7, and (g) 10−6 mol L−1. Impedance measurements were performed at 0.325 V vs SCE using hydroquinone 10−3 mol L−1 in 0.1 mol L−1 phosphate buffer, pH 7.4. Reference electrode: SCE. Experimental (dots) and fitted data (lines) are presented. The three red points on a spectrum, correspond to 59.3, 7.7, and 0.25 Hz. (B) Square wave voltammetry (SWV) obtained at different concentrations of BPA on polypyrrole-NTA/ Cu2+/aptamer electrode: (a) 0, (b) 10−11, (c) 10−10, (d) 10−9, (e) 10−8, (f) 10−7, and (g) 10−6 mol L−1. SWV measurements were performed until a switching potential of 0.65 V using hydroquinone 10−3 mol L−1 in 0.1 mol L−1 phosphate buffer pH 7.4. Reference electrode: SCE.

presence of increased concentration of BPA (curves b to g) in the range l0−11 mol L−1 to 10−6 mol L−1. As expected, the increase of the EIS spectra with BPA concentration is in a good agreement with the efficient recognition of different concentrations of BPA by the aptamer. These results were confirmed by square wave measurements, (Figure 3B). The anodic peak current decreases continuously with the increasing concentrations of BPA from l0−11 mol L−1 to 10−6 mol L−1 while the peak potential increases from 0.365 to 0.386 V vs SCE. This clearly indicates that the rearrangement of the aptamer configuration induced by the BPA recognition generates new steric hindrances to the hydroquinone diffusion toward the electrode surface. Moreover, a shoulder is detected on SWV curves for a concentration of 10−7 mol L−1 BPA at Epa = 0.615 V vs SCE whose intensity increases at a higher concentration. This system is attributed to the oxidation of BPA53 entrapped in the aptamer at the surface of the electrode. By plotting the difference Δj = (j − j0) between the current density measured in the presence of BPA (j) and without BPA 7271

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Table 1. Values of Impedance Modulus at 7.7 Hz and Values of Equivalent Circuit Elements (Rct, Cdl, n, and Rdiff) Obtained for Fitting of the Experimental Data Corresponding to the Changes in Impedance of the Aptamer Modified Electrode upon Detection of Different BPA Concentrations bisphenol A concn −11

−1

10 mol L 10−10 mol L−1 10−9 mol L−1 10−8 mol L−1 10−7 mol L−1 10−6 mol L−1 a

Rct/Ω 3350 3880 4230 4530 4830 5320

± ± ± ± ± ±

50 60 70 70 80 80

Cdl/μF cm−2a

n

10.5 ± 0.2 9.7 ± 0.2 9.3 ± 0.2 9.1 ± 0.2 8.9 ± 0.2 8.8 ± 0.2

0.912 0.928 0.934 0.939 0.941 0.943

Rdiff/Ω 1310 1400 1440 1520 1590 1756

± ± ± ± ± ±

Z at 7.7 Hz/Ω

20 30 30 30 30 30

3582 4103 4441 4743 5074 5589

Values calculated from the CPE obtained by fitting.

an original triple-signaling strategy reporting a limit of detection at 1.9 × 10−13 mol L−1, but this sensor exhibits a linearity range of only 2 orders of magnitude whereas our sensor exhibits a linearity of 5 orders of magnitude, the linearity range being a key parameter in the design of biosensor. The specificity of the proposed aptasensor was also examined by evaluating the Rct change in the presence of 10−6 mol L−1 of two interfering agents: 4,4′-dihydroxybiphenyl (DHB) and bisphenol P (BPP). Without BPA, an increase of 3.6% charge transfer resistance was observed for DHB while an increase of 12.3% for BPP was determined. The comparison of these two values with the 18.8% achieved for the lowest concentration of BPA (10−11 mol L−1) shows the selectivity of this aptasensor. For the impedance modulus at 7.7 Hz, an increase of 3.5% was observed for the DHB while it is 11% for the BPP. The comparison of these two values with the 14.5% achieved for the lowest concentration of BPA (10−11 mol L−1) is in agreement with results obtained with charge transfer resistance.

Figure 5. Calibration curve for the BPA biosensor corresponding to the changes in impedance of the electrode upon detection of different BPA concentrations: (a) RCT, charge transfer resistance obtained by fitting of experimental data; (b) Z 7.7 Hz, impedance modulus obtained at 7.7 Hz. Experimental (dots) and linear regression (lines) are presented. Experimental conditions are the same as Figure 3A.



CONCLUSION We have synthesized and characterized by electrochemical methods a bisphenol A aptasensor. A very competitive detection limit of 10−11 mol L−1 was determined associated with a large linearity range of 5 orders of magnitude, which is a key parameter for the design of an aptasensor. Given the easy design of the aptasensor, this analytical device constitutes a promising method to monitor the occurrence of BPA in food, drinking water, or the environment and to understand its effects toward living organisms.

efficient characteristics of the designed biosensor (R2 = 0.991). The linear dynamic range is greater than 1 order of magnitude than the one obtained by SWV showing the efficiency of the impedimetric method. In order to simplify the electrochemical impedimetric measurements that are registered over a wide frequency range and that require both time and the modeling of the data, measuring the change of the impedance modulus, Z, at a single frequency is an attractive easier alternative. The frequency of 7.7 Hz was chosen since a high variation of the impedance modulus is obtained at this frequency (Figure 3A). This strategy has been previously used and constitutes an easier and faster way to get the calibration curve.54 As expected, a similar linear relationship was obtained in the concentration range from 10−11 to 10−6 mol L−1 with an almost identical sensitivity (slope = 379 ± 6 Ω per order of magnitude with R2 = 0.991, Figure 5). This new impedimetric aptasensor provides a very competitive limit 10−11 mol L−1 with a higher linearity range (5 orders of magnitude) compared to recent electrochemical aptasensors described in the literature. Up until now, only a few examples of aptasensors reported lower limit. In 2013, Xue et al.47 designed an aptasensor with a limit of detection of 1.24 × 10−12 mol L−1 and a linearity range of 4 orders of magnitude using the intercalator methylene blue. The principle is based on competitive recognition of BPA and a complementary DNA. Although the limit of detection is very competitive, it is based on a “signal off” whereas our impedimetic sensor is based on a “signal on” with an increase of the impedance modulus. The most recent “signal on” electrochemical aptasensor46 based on



AUTHOR INFORMATION

Corresponding Author

*E-mail: [email protected]. Author Contributions

The manuscript was written through contributions of all authors. All authors have given approval to the final version of the manuscript. Notes

The authors declare no competing financial interest.



ACKNOWLEDGMENTS The authors thank the Nanobio-ICMG platforms (FR2607) “Functionalization of surfaces and transduction” and “Biomolecules Synthesis” of the scientific structure “Nanobio campus” for providing the facilities. The authors thank the platform “Functionalization of surfaces and transduction”. The authors wish to acknowledge the support from the LabEx ARCANE (ANR-11-LABX-0003-01). Arielle Lepellec should especially be acknowledged for her helpful and fruitful 7272

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Analytical Chemistry

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discussions. The authors gratefully acknowledge the algerian gouvernment for the support to provide a PNE fellowship to Imen Kazane.



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DOI: 10.1021/acs.analchem.6b01574 Anal. Chem. 2016, 88, 7268−7273