Mimicking pH-Gated Ionic Channels by Polyelectrolyte Complex

Mar 27, 2017 - The study of ionic transport through these single nanopores reveals a selectivity on anions and pH-gate properties at low salt concentr...
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Mimicking pH-Gated Ionic Channels by Polyelectrolyte Complex Confinement Inside a Single Nanopore Yixuan Zhao,† Jean-Marc Janot,† Emmanuel Balanzat,‡ and Sébastien Balme*,† †

Institut Européen des Membranes, UMR5635 UM ENSM CNRS, Place Eugène Bataillon, 34095 Montpellier cedex 5, France Centre de recherche sur les Ions, les Matériaux et la Photonique, UMR6252 CEA-CNRS-ENSICAEN, 6 Boulevard du Maréchal Juin, 14050 Caen Cedex 4, France

‡

S Supporting Information *

ABSTRACT: Biological channels have served as inspiration to design stimuli-response artificial nanopores. Here we propose an original approach to design a pH-gate nanopore based on polyethylenimine and chondroitin-4-sulfate (ChS) layer-by-layer self-assembly. This approach is interesting because it is rapid and permits monitoring in real time of functionalization. The study of ionic transport through these single nanopores reveals a selectivity on anions and pH-gate properties at low salt concentration. It is open at pH below 4 or 5 depending on salt concentration. These properties are explained by the modification of both charge and conformation of ChS as well as swelling of the polyelectrolyte complex.

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INTRODUCTION For the past two decades, single nanopore technology has allowed real advancement in the area of biosensing.1 Indeed, using a biological one such α-hemolysin or MspA, it became possible to sequence DNA.2,3 Artificial nanopores drilled inside SiN4 or polymeric film5 are also promising for the development of sensors to detect proteins,6,7 nanoparticles,8 or to identify DNA specific sequences9 or knots.10 Beside these potential applications, a single nanopore can be considered as a basic element of multipore membranes. The main limitation of these artificial nanopores is the unresponsiveness against stimuli without functionalization. In order to improve their properties, biological channels have served as inspiration because they exhibit unique properties in terms of selectivity and response against stimuli. The transposition of such properties to synthetic membranes remains real challenge. To reach this goal, artificial nanopores have to be functionalized by chemical grafting of responsive function.11−13 Based on that, several biological channels have been mimicked, such as nuclear pore complex by grafting a Nups,14 or light-sensitive channel by grafting spiropyrane.15 By inserting specific reconnaissance function (DNA, NTA, biotin, protein) inside a track-etched nanopore, it becomes possible to mimic ligand-responsiveness.9,16−18 The selective ionic channel can also be mimicked using a conical charged nanopore.19,20 The latter presents a real interest to develop membranes to improve separation processes for different applications such as desalination, drug delivery, or “blue” energy production.21−23 A second way consists of the insertion of biological channel. This has been achieved only with α-hemolysin24,25 and gramicidin.26,27 Among biological stimuli-responsive channels, the acid sensitive ones are involved in the perception of pain, memory, © XXXX American Chemical Society

and mechano-sensation. They combine both ionic selectivity and pH-gate. Such properties have been partially transferred to track-etched nanopores. Buchsbaum et al.28 have reported a pH-gated nanopore based on grafting on amino-modified-DNA strength. More recently, we have reported a pH-gated nanopore based on functionalization with PEG-biotin and streptavidin.29 In both of these reports, the nanopores are open at pH greater than 4. The gate mechanism is based on reversible nanopore constriction due to the creation of mesh between the DNA strand for the first example and PEG/streptavidin precipitation for the second one. In terms of selectivity, the pH-gated nanopore based on DNA grafting is selective to cations. Even if these nanopores exhibit very interesting properties, two main points have to be improved. First, due to the mechanism of gating, these nanopores are not responsive to the ion concentration. Second, the nanopore functionalization is based on a multistep chemical grafting, which is timeconsuming. This work aims to design a new pH-gate nanopore that is also sensitive to the ionic concentration. The mechanism of pH activation is inspired by KSCA channel. The gate aperture of this channel is controlled by the organization of 3 residues, which create a network of salt bridge and H-bond. It is open at low pH and closed at high pH due to the protonation/ deprotonation state of Glu118 residue.30 We have chosen to design a nanopore selective to anions since they have been less reported than the nanopore selective to cations. We have also investigated a simple and rapid method to functionalize the Received: February 3, 2017 Revised: March 22, 2017 Published: March 27, 2017 A

DOI: 10.1021/acs.langmuir.7b00377 Langmuir XXXX, XXX, XXX−XXX

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Figure 1. Chemical structure of branched PEI (a) and ChS (b). (c) Illustration of the experimental protocol of nanopore functionalization. Typical current trace recorded during the functionalization by PEI (d) and ChS (e). These examples were recorded for NP dtip = 15 nm under pH 8 at NaCl 100 mM, TRIS 5 mM, and EDTA 1 mM; the applied voltage is −1 V (for PEI) or 1 V (for ChS). a value of several hundred picoamperes, the etching process was stopped by the replacement of the etching solution by the stop one. The conical nanopores are characterized as follows. The base diameter (D) is calculated from total etch time t (min) using D = 2.5t as relationship. The value 2.5 was determined from multipore membranes produced under the same condition as a single pore at different etch times (t). The measurements of D were performed by MEB. The tip diameter (d) was calculated, assuming a bulk-like ionic conductivity inside the nanopores, from the dependence of the conductance G to the NaCl concentration (eq 1).35 In order to correct the conductivity at high salt concentration, the diameter is calculated using the ionic conductivity of solution κ. The latter was measured using a conductimeter (Hanna HI 255 combined meter with conductivity and electrode HI 76310) after preparation.

nanopore, the layer-by-layer (LbL) deposition of polyelectrolyte. This method, which is commonly used to functionalize surfaces, was investigated in the case of a single nanopore. Ali et al. have used the poly(allylamine hydrochloride)/poly(styrenesulfonate) (PSS) couple to modify the ionic transport of a nanopore in order to determine with a mathematical model its exact shape.31 In this work, the authors have also pointed out that the bilayers grown inside the nanopore induce a decrease of surface charge. More recently, Lepoitevin et al. have reported that poly-L-lysine (PLL) could be used for reversible functionalization in order to design biosensors.32 Here, we were interested to another polyelectrolyte system base on branched polyethylenimine (PEI) and chondroitin-4-sulfate (ChS). On one hand, the PEI was chosen because it permits a strong attachment of the polyelectrolyte; on the other, the ChS was chosen because it presents two acid functions: one sulfonate (pKa 1.5−2) and one carboxylate (pKa 3−5). In addition, it permits the formation of a strong polyelectolyte complex with a polyamine such as poly(amino-serinate).33 Besides the possibility to design a new biomimetic channel, this work also investigates the behavior of a ChS/PEI layer under confinement.

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G = κπDd /L

(1)

where L is the nanopore length. Current−Voltage Measurements. Electrical measurements were achieved by a patch-clamp amplifier (EPC10 HEKA electronics, Germany). The current was measured by Ag/AgCl, 1 M KCl electrodes connected to the cell chamber by agar−agar bridges. A single nanopore was mounted in the chemical Teflon cell containing an electrolyte solution. One electrode was plugged to the working end of the amplifier (trans chamber, base side), and the other electrode was connected to the ground (cis chamber, tip side). Recorded currents were analyzed by a Fitmaster (Heka Elektronik, Germany). For I−V curves, the currents data were recorded as a function of time under constant voltage from −1 to 1 V by 100 mV steps. All current traces were recorded for 60 s at a frequency of 4 kHz. These measurements were performed three times. The conductance G was extracted from the linear zone of I−V curves from −75 mV to 75 mV. These IV curves were recorded using a voltage ramp from −75 mV to 75 mV for 60 s. These measurements were repeated five times.

MATERIALS AND METHODS

Materials. Poly(ethylene terephthalate) (PET) film (thickness 13 μm, biaxial orientation) was purchased from Goodfellow (ES301061). Sodium chloride (71380), sodium hydroxide (30603), hydrogen chloride (30721), ethylenediaminetetraacetic acid (EDTA) (E5513), (243051), polyethylenimine, branched (PEI) Mw 25 kDa (408727), chondroitin 4-sulfate sodium salt from bovine trachea (27042), trizma hydrochloride (T3253), and CAPS (C2632) were purchased from Sigma-Aldrich. Potassium chloride (POCL-00A) was purchased from LabKem. Ultrapure water was produced from a Q-grad-1 Milli-Q system (Millipore). Track-Etching Nanopores and Characterization. Single tracks were produced by Xe irradiation (8.98 MeV) in the PET membrane (13 μm) (GANIL, SEM line, Caen, France). Before the chemical etching process, the PET film was exposed to UV light for 24 h per side to activate the track (Fisher bioblock; VL215.MC, λ = 302 nm). The etching of the conical nanopore was performed under dissymmetric conditions by electrostopping methods.34 The PET foil was mounted between two compartments of a chemical cell in Teflon. The etchant solution (NaOH 9M, 1.6 mL) was added on the base side, and the stopping solution (KCl 1 M and acetic acid 1M, 1.6 mL) was added on tip side. A potential of 1 V was applied across the membrane; the reference electrode is immersed in the stop solution, and the working one in the etchant solution. When the current reaches

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RESULTS AND DISCUSSION Single conical nanopores were obtained in PET film (thickness 13 μm) by the track-etched method. The first step is the irradiation with Xe 8.98 MeV u−1. The second one is a chemical etching process under dissymmetrical conditions using etchant solution (NaOH 9 M) and stop solution (KCl 1 M, Acetic Acid 1 M). In this work we have used two types of nanopores depending on the range of tip diameter (d), typically 15 nm < d < 30 nm for the small ones and d ≈ 90 nm for the large ones. After the etching process, the carboxylate groups cover the internal surface of the nanopore. Thus, the latter exhibits a negative surface charge at pH 8. The recorded I−V curves show a current rectification, which can be characterized by the rectification factor ( f rec) calculated from f rec = |I(1V)|/|I(−1V)|. B

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Figure 2. Evolution of nanopore conductance and rectification factor for two nanopores: d = 15 nm (a,b) and d = 90 nm (c,d). The experiments were done at pH 8, NaCl 100 mM, Tris 5 mM and EDTA 1 mM (Raw nanopore - blue triangle, after PEI - black square, and after ChS deposition red circle). The conductance was extracted from the linear zone of the I−V curve (between −75 mV and 75 mV).

According to our experimental conditions (Figure SI-1), the current rectification is lower than 1 when the nanopore wall is negatively charged. The nanopore functionalization was done by alternative deposition of PEI and ChS (Figure 1c). Typically 16 μL of polyelectrolyte solution (1 mg mL−1) was added on the tip chamber, which contained 1.6 mL of buffer (NaCl 100 mM, TRIS 5 mM, and EDTA 1 mM). A voltage of −1 V for the PEI or of 1 V for the ChS was applied on the base side to favor the polymer entrance inside the pore. This voltage also permits characterization in real time of the polyelectrolyte adsorption on the nanopore wall, as previously shown in the case of the PLL/PSS LbL functionalization.32 Typical current traces recorded during the functionalization process for the PEI and the ChS are reported in Figures 1d,e. It permits in situ monitoring of the self-assembly of each polyelectrolyte layers. As expected, after the polyelectrolyte addition, we observed a decrease of current due to the modification of the charge at the nanopore entrance. Regarding the short time required to observe the current decrease, we cannot consider a full functionalization along the nanopore length by polyelectrolyte.32 We can assume those polyelectrolytes are adsorbed at the region close to the narrow opening only. In order to confirm that the polyelectrolytes are loaded inside the nanopore, the I−V dependence was recorded at pH 8, NaCl 0.1 M, after each layer adsorption. The current rectification and the conductance G, are reported on Figure 2 for a small pore (d = 15 nm) functionalized with (PEI/ChS)4/ PEI and a large one (d = 90 nm) functionalized with (PEI/ ChS)9/PEI. Whatever the nanopore diameter, we can observe a strong decrease of the ionic conductance after adsorption of the first layer of PEI. The following layers induce a weak decrease of conductance. This could suggest a random coil form of the first layer of PEI, which significantly reduced the nanopore

diameter. However, it is difficult to claim that, since the conformation of PEI inside a single nanopore cannot be characterized. The current rectification is also modified after each layer; it increases after the PEI loading and decreases after the ChS. These results of current rectification and ionic conductance confirm that polyelectrolyte adsorption really occurs. However, regarding previous works, we could expect a modification of the charge of the nanopore entrance for each addition of polyelectrolyte and thus an inversion of the current rectification. This should be translated into a f rec value greater than 1 after the PEI loading and lower than 1 after the ChS loading. This inversion occurs only after the first PEI/ChS bilayer adsorption. Then the f rec values are greater than 1 even after ChS adsorption. Two assumptions can be done to explain this result. The first one suggests that the charge at the nanopore entrance is positive because compensation of charge between PEI and ChS layer may be not total. The second one suggest that the charge at the nanopore entrance is negative due to the ChS addition In this case, the value of current rectification may result from in-homogeneous surface charge patterns between the region close to the narrow opening where the polyelectrolyte layers are located and the rest of the nanopore where the carboxylate groups are located due to the chemical etching process. In previous reports, the rectification factor tends to 1 with the increase of number of polyelectrolyte bilayers. This was explained by the structural reorganization and the generation of both charges and ion pairs, which impact the charge overcompensation.31,36 In our case, the f rec values tend to a constant value around 4 and 3, which depends on the nanopore. After nanopore functionalization, the evolution of the conductance of NaCl solutions from 10−4 M to 1 M was studied at pH 7. It should be noted that the polyelectrolyte C

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Figure 3. I−V dependence as a function of NaCl concentration (from 10−4 M to 2 M) at pH 7 for small nanopores d = 25 nm (a) and d = 15 nm (b) functionalized with (PEI/ChS)4PEI. (c) NaCl conductance as a function of NaCl Concentration (pH 7) for small nanopores functionalized with (PEI/ChS)4PEI: black square, d = 25 nm; red circle, d = 15 nm. The conductances were extracted from linear zone of the I−V curve (between −75 mV and 75 mV).

Figure 4. I−V curve recorded for NaCl concentration (10−3 M, 5 × 10−2 M and 1 M) of small nanopores d = 25 nm (a,b,c), d = 15 nm (d,e,f) functionalized with (PEI/ChS)4PEI, and large nanopore d = 90 nm (g,h,i) functionalized with (PEI/ChS)9PEI at pH 3 (black square), 4 (red circle), 5 (green triangle), 7 (blue triangle), and 8 (magenta diamond).

becomes constant at low salt concentration. The plateau of conductance is attributed to the mobile counterions, which ensure the electroneutrality inside the nanopore. These two regimes were also reported in the case of an uncharged nanopore.37 Interestingly, for the nanopore functionalized with PEI/ChS, we do not observe the plateau at low concentration while it is charged. This could be the case if we assume a perfect compensation of the charge between the nanopore surface, PEI

layers are not stable for a NaCl concentration greater than 1 M. The I−V curves obtained for two small nanopores (d = 15 nm and d = 25 nm) functionalized with (PEI/ChS)4PEI and for a large one (d = 90 nm) functionalized with (PEI/ChS)9PEI are reported in Figure 3 as well as the evolution of the conductance as a function of the NaCl concentration for a small nanopore. Usually, in the case of a charged nanopore, the conductance follows two regimes: it increases at high salt concentration and D

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Figure 5. Rectification factor as a function of pH at different NaCl concentrations 10−3 M (black square), 5 × 10−3 M (red circle) and 1 M (blue triangle) of small nanopores d = 25 nm (a) and d = 15 nm (b) functionalized with (PEI/ChS)4PEI, and large nanopore d = 90 nm (c). (d) Illustration of PEI/ChS swelling induced by pH at low salt concentration.

the nanopore can be considered close at pH greater 4, and thus the pH-gate properties is maintained. This displacement of pH is likely due to the increase of pKaCOOH in the nanopore. This is in good agreement with the experimental result reported by Yameen et al.41 and the theoretical model reported by Tagliazucchi et al.40 At high salt concentration (1 M), the pH-gated phenomenon disappears. In order to confirm the role of ChS, a control experiment with PEI/PAA LbL was performed. The I−V curves (see Figure SI-3) show an inversion of current rectification with the pH but not a pH-gate. To go further in our investigation, the current rectification as a function of pH is reported for all nanopores as a function of concentration (Figure 5). For all nanopores, the value of f rec increases at pH lower than 4. The NaCl concentration also plays a role since at 10−3 M the rectification factors f rec are 1625, 201, and 512 for the small (d = 15 nm and d = 25 nm functionalized with (PEI/ChS)4PEI and large nanopores (d = 90 nm functionalized with (PEI/ ChS) 9 PEI, respectively. These high values of current rectification suggested that the position of the depletion zone is close to the nanopore tip entrance as predicted by Constantin et al.42 This is in good agreement with a location of polyelectrolyte layer at the region close to the narrow opening. The values of current rectification decrease to around 100 at 5 × 10−2 M NaCl. It has been reported in the case of conical nanopores that the rectification factor tends to 1 with the increase of concentration. This has been explained by the thickness of electrical double layer.43 In our case, to interpret the ionic transport, the influence of both pH and the NaCl concentration on the structure of polyeletrolyte layers should be taken into account. It can be explained as follows. When the pH is greater than the pKa of the COOH groups, a compensation of charge occurs between both the polymers and the additional counterion (Cl−). At low salt concentration, the polyelectrolytes adopt a linear conformation. The compression of the layers traps and immobilizes the counter-

and ChS. This assumption is unlikely because the I−V curves exhibit a current rectification (f rec > 1), which proves the inhomogeneous surface charges the nanopore. Actually, to explain the lack of a residual current, the modification of the polyelectrolyte structure with the salt concentration should be considered. It has been shown that at low salt concentration, the polyelectrolytes are linearly arranged.38,39 In this case, the polyelectrolytes are compressed, and thus the counterions that ensure the charge compensation are trapped inside the polyelectrolyte layer and are not mobile. In this case, the observed conductance is due to the mobile ion outside the polyelectrolyte layer, which mainly depends to the reservoir concentration. With the increase of concentration, the polyelectrolyte layers swell due to the entrance of mobile ion and water. This induces the increase of conductance. As previously mentioned, the ChS presents two anionic functions at pH 7: one sulfonate (pKaSO3H 1.5−2) and one carboxylate (pKaCOOH 4−5). Beside these functions, the carbohydrate chain contains −OH, which could contribute to polymer organization via H-bond. The influence of the pH on the ionic conductivity was studied at low, medium, and high NaCl concentrations (10−3, 5 × 10−2 and 1 M respectively). The I−V dependences are reported in Figure 4. For all nanopores, the pH activates the anionic transport at low and medium salt concentrations. At NaCl 10−3 M, we can consider that the nanopore is closed for pH greater than 4 and open for pH lower than 4. Actually, we could expect to observe this gate at higher pH, typically around the pKaCOOH. However, it has been shown in the case of a conical nanopore functionalized with a zwitterionic polymer that a shift between the pKa in bulk and the pKa in the nanopore occurs.40 This shift to the lower pH was interpreted by the charge regulation, which is a displacement of base-acid equilibrium toward the uncharged segment to minimize the local electrostatic repulsion. With the increase of the salt concentration (NaCl 5 × 10−2 M) weak ionic transport at pH greater than 4 can be observed. However, E

DOI: 10.1021/acs.langmuir.7b00377 Langmuir XXXX, XXX, XXX−XXX

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ions inside the layers, which ensures electroneutrality. Thus, the concentration of mobile ions inside the nanopore depends on that in the reservoir. With the increase of salt concentration, the swelling of polyelectrolyte layers permits the entrance of water, and the counterions become mobile. Additionally, the decrease of Debye screening length permits the nanopore filling with the counterions and the co-ions from the reservoir. This interpretation is in good agreement with the dependence between the conductance and the salt concentration reported at pH 7. When the pH is lower than the COOH pKa in the nanopore (typically at pH 3−4), the protonation of the carboxylate groups breaks in the electroneutrality, which has to be counterbalanced by the entrance of counterions inside the nanopore. In other words, the decrease of pH should behave like a pump of Cl− to ensure the electroneutrality inside the nanopore. In addition, this partial protonation of ChS has an influence on the layer organization. It is well-known that a weak polyanion such as PAA swells at pH below pKa.44 The swelling of ChS can explain the anionic transport at low pH. In this case, the polyelectrolyte layer is charged in counterions and water to ensure their transport. At low concentration, there are only mobile anions inside the nanopore, which can explain the gate and the high value of the rectification factor. With the increase of the salt concentration, the nanopore is filled by the counters and co-ions from the reservoir and thus the current rectification decreases and the gated phenomenon disappears.

Sébastien Balme: 0000-0003-0779-3384 Notes

The authors declare no competing financial interest.

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ACKNOWLEDGMENTS Single tracks have been produced in GANIL (Caen, France) in the framework of an EMIR project.

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CONCLUSION This work aimed to design an anionic pH-gated nanopore. To do it, several nanopores were functionalized by LbL selfassembly of (PEI/ChS)nPEI. To sum up our results, the nanopores are selective to anion. Interestingly, at low salt concentrations the nanopore is practically closed at pH > 4 and only opens for the anions at pH < 4. With the increase of the salt concentration, the pH-gate phenomenon disappears and the current rectification tends to 1. The results have been interpreted by the swelling PEI/ChS and the modification of the conformation due to the protonation of the COOH groups of ChS. Globally, these results are particularly interesting from a fundamental point of view because they allow one to study the influence of confinement on polyelectrolyte self-assembly. Indeed, the conductance experiments permit characterization of the swelling by the mobility of the counterion inside the polyelectrolyte layer. Additionally, a single track-etched nanopore can be considered as the basic element of a multipore membrane obtained using the same methods of preparation. Thus, we can easily upscale these properties obtained for the single nanopore to a multipore membrane. The latter should be used in processes that require regulation of anionic flux with pH and by ionic concentration.

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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.langmuir.7b00377.

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DOI: 10.1021/acs.langmuir.7b00377 Langmuir XXXX, XXX, XXX−XXX

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DOI: 10.1021/acs.langmuir.7b00377 Langmuir XXXX, XXX, XXX−XXX