ARTICLE pubs.acs.org/JPCC
Investigation of Ion Transport Traversing the “Ion Channels” by Scanning Electrochemical Microscopy (SECM) Xiaoquan Lu,* Tianxia Wang, Xibing Zhou, Yao Li, Bowan Wu, and Xiuhui Liu Key Laboratory of Bioelectrochemistry & Environmental Analysis of Gansu Province, College of Chemistry & Chemical Engineering, Northwest Normal University, Lanzhou, 730070, China ABSTRACT: In the nervous system, ion channels are essential for all processes. The highly ordered porous anodic aluminum oxide (AAO) was modified at the interface between two immiscible electrolyte solutions (ITIES) to recover the process of ion transfer through the ion channels. The study on dynamic process of ion transfer through the ion channels obtained for DKþ0 is 1.40 10-8 cm2 s-1 and DNaþ0 is 2.74 10-7 cm2 s-1. The result offers tremendous advantages for linear relationship between the half-wave potential and concentration of Kþ and Naþ. In addition, it will be helpful to understand both the mechanism about the dynamics and thermodynamics processes of ion transfer through the ion channels and the role about ionic concentration in nerve conduction.
’ INTRODUCTION The role of ion channels in cell physiology was regulated by processes occurring after protein biosynthesis, which are critical for both channel function and targeting of channels to appropriate cell compartments.1-5 Hodgkin and Huxley first brought forward the concept in 1952.6,7 Neher and Sakmann provided the means for directly visualizing ion current through a single channel. Further literature relevant to this topic may be found in reviews and handbooks of the structure and function of voltagegated ion channels in general.8-11 In 2003, Rod Mackinnon made a groundbreaking work for discovering the structures of potassium and chloride channels.7 On the basis of main work about ion channel engineering by the groups of Mutter,12,13 Montal,14 Armentrout,15-21 Schwarz,22-24 Kevan,25 ion-channel proteins and ion-channel-forming peptides have received increasing attention for sensing applications. Ion channels are supramolecular structures embedded in biological membranes. Ion channel-controlled transport through biological membrane is an extremely important aspect of the electrophysiology of living cells. Different kinds of channels can open and close synchronously, resulting in electric signals and responses of the nervous system. The opened highly selective ion channels allow some kinds of ions to enter along the electrochemical gradient.26,27 Their activation, or opening, permits an ion-specific flow of a few hundred to many thousands of ionic charges to rush through the channel before its closure.28 With the development in the molecular biology and X-ray diffraction techniques, many experiments regarding the structural details of ion channels have been done.29 Many models were developed to describe the ionic channels, with either theoretical or experimental purposes. Simulation techniques were applied to the study of these systems recently,29-31 such as anion-doped carbon nanotube,32 computer-aided design,33 and hydration r 2011 American Chemical Society
structure of the ions and nuclear magnetic resonance.34 Many biological methods could also provide effective means to make clear the structure of ion channels,1,6,26,35-38 but the details of both the process and the energy of ion through the ion channels cannot be obtained at the same time. To address these issues, we have developed the L/L-AAO interface. The L/L interface has been suggested as a simple model for biological and artificial membranes.39,40 More important is that in virtue of the interface not only can the life-likeness of ion channels be recurred easily but also both the process and the energy of ion through the ion channels are obtained commendably simultaneously. Furthermore, the experimental results show the relationship between the rate constant and the driving force. The constant of the ion controlled how the ion channels open or closed. The driving force is an important factor of how fast the ion is through the ion channels. To sum up the above arguments, studies of artificial ion channels must have received much attention because they both contribute to the fundamental understanding of natural ion channels and may lead to applications such as drug discovery and sensors.4,41
’ EXPERIMENTAL SECTION Materials. Sodium chloride (NaCl, AR), Potassium chloride (KCl, AR), and 1,2-dichloroethane (DCE, 99.8%, AR) were purchased from Beijing Chemical, China. Tetrabutylammonium tetraphenylborate (TBATPB, 99%, Aldrich), tetrabutylammonium chloride (TBACl, 99%, Aldrich), tetramethyammonium chloride (TMACl, 99%, Aldrich), and dibenzo-18-crown-6 (DB18C6, 98%, Aldrich) were used without purification. The AAO templates were Received: December 15, 2010 Revised: January 27, 2011 Published: February 25, 2011 4800
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Scheme 1. (A) Ions through the Ion Channels; (B) Simple Model for Single Ion through the Ion Channel; (C) Model for a ThreeElectrode to Investigation of Ion Transport Traversing the “Ion Channels” by (SECM); (D) Scanning Electron Micrographs of AAO
made according to the literature.42,43 The aqueous and organic phases were prepared with doubly distilled water (made by our laboratory) and DCE, respectively. DCE was washed several times with deionized water before use. Special precautions were taken for dealing with DCE and other hazardous chemicals. Apparatus and Electrochemical Measurements. A CHI900 electrochemical workstation (CH Instruments) was connected to a personal computer, which was employed to record approach curves and cyclic voltammograms. In this work, the nanopipets employed as the SECM tips were fabricated from borosilicate glass capillaries (o.d. = 2.0 mm, i.d. = 1.16 mm, L = 10 cm) using a laserbased puller (made by our laboratory). The pipets were filled with the aqueous solutions from the back using a small syringe (5 μL). Before each experiment, the nanopipet was checked up by an Olympus optical microscope to ensure that there was no trapped bubble. As shown in Scheme 1, a three-electrode setup was employed with a nanopipet as the SECM tip, a Ag wire coated with AgTPBCl served as the reference electrode, and a Pt wire served as the counter electrode. A silver wire coated with AgCl was inserted into the pipet as the reference electrode in the aqueous phase. The tip was filled with x mM NaCl or x mM KCl aqueous solution from the back by using a small syringe and biased at the potential where the facilitated Naþ or Kþ transfer reaction was diffusion-controlled. The approach curves (iT-d curves) were obtained by moving the tip toward the bottom L/L interface and recording the tip current (iT) as the function of the tip interface separation distance (d). The coordinate of the L/L interface (d0) was decided from the sharp increase in iT that occurred when the tip touched the bottom DCE/W interface. Then, the droplet electrodes were for the cyclic voltammograms. A drop of a certain volume of aqueous solution containing the KCl, FeCl3, and FeCl2 was transferred to the surface of a freshly polished platinum disk electrode (d = 2 mm) with a small syringe. The aqueous solution spread spontaneously across the surface of this platinum electrode and covered it completely. Then, the electrode was turned over and immersed immediately in a DCE solution (of a certain volume) containing DB18C6 and TBATPB salt. All of the experiments were carried out at room temperature (22 ( 2 °C).
intracellular and extracellular ions and permeability of biomembrane. Because ion channels are embedded in lecithin bilayer of protein molecules, the ions, especially the Kþ and Naþ passing the biomembrane, must traverse the ion channels. Through these channels, cells could exchange the ions with outside. The model in the discussion was used to embellish the L/L interface, which has the high similarity with biological membranes. AAO membranes with nanochannels in the experiment have been successfully fabricated via a two-step annodization method. According to the literature,42,43 the cylindrical uniformly sized holes range from 20 to 40 nm in diameter, and the film thickness varies from 0.1 to 300 μm. The nanopores are so thick and fast that the ions are just through the AAO pores, not the other aperture. Before the experiment, the improvement of experimental device was that the AAO membrane could completely cover the measuring L/L interface. The transmembrane behavior of ions gave rise to a concentration gradient between the in and out of cell, the same as the transmembrane voltage; therefore, the concentration of Mþ in the tip (cMþw) should be higher than that of DB18C6 in the DCE phase (cO DB18C6). In view of this, the biomembrane could be simulated veritably and compactly by the new system. Kþ and Naþ Transfer through the Ion Channels at the Modified W/DCE Interface. Evaluation of Mechanism. The ways that a cell releases or takes up ions might be considered chemically as follows: (1) active transport: ions pass through the biomembrane directly; (2) passive transport: ions pass through the biomembrane facilitated by ionophores; and (3) ion pathway: certain ions pass the biomembrane through the ion channels immobilized in the biomembrane.44,45 Therefore, we could consider that ions traversing the ion channels belong to the third way. The following electrochemical cell(I) is employed for investigation of alkali metal ion transfer at the modified W/DCE interface facilitated by DB18C6. AgjAgClj5 mM TBACl j5 mM TBATPBCl þ 0:5 mM DB18C6j
rsf
organic phase TBA þ ISE
rsf 1, 2 - DEC
jxMMCl þ 10 mM TBAClj AgAgCl
rsf rsf
’ RESULTS AND DISCUSSION: TRANSMEMBRANE DELIVERY System Setup. The transmembrane delivery of ions was caused by the inhomogeneous concentrations between the
H2 O
Re f
cellðIÞ
where M is Naþ or Kþ. The first process is the alkali metal ion (Mþ) transfer facilitated by DB18C6 from water to DCE at the tip, and its mechanism could be considered chemically as a transfer by 4801
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Scheme 2. Schematic Diagram of the Electrochemical Cell (II) Employed for the Study of Facilitated M (Kþ and Naþ) Ion Transfer Across the L/L-AAO interface
of DB18C6 in DCE, the current is limited by diffusion of DB18C6 to the pipet orifice. Assuming that the pipet orifice is disk-shaped, one can calculate the steady-state diffusion limiting current as50-53 id ¼ 4nfaDc
Figure 1. Experimental approach curves fit with theoretical values for the facilitated (a) Kþ and (b) Naþ transfer reactions. For curves from bottom to top, the concentrations of Kþ and Naþ are 10, 20, 30, 40, and 50 mM, respectively, and concentration of DB18C6 is 0.25 mM. Sweep rate is 50 mV/s.
where D is the diffusion coefficient of species in the outer solution responsible for the interfacial charge-transfer reaction, a is the inner pipet radius, F is the Faraday constant, and n is the transferred charge. Equation 1 should be equally applicable to ion-transfer processes.53-55 The following cell(II) is employed to investigate the Kþ and Naþ transfer through the ion channel at the modified W/DCE interface facilitated by DB18C6 (shown in Scheme 2). Ptj1 mM FeCl2 þ 1 mM FeCl3 þ x mM MCl þ x mM TMACljj10 mM TBATPBjAgTPBCljAg
interfacial complexation (TIC) process45-47 kb
Mþ ðwÞ þ DB18C6ðDCEÞ f s ½M - DB18C6þ ðDCEÞ ðat the tipÞ
The second process is transfer by interfacial dissociation (TID) at the bottom W/DCE interface. kf
½M - DB18C6þ ðDCEÞ f s M þ ðwÞ þ DB18C6ðDCEÞ ðat the ITIESÞ
When the tip approaches the ITIES, Mþ is released from the complex and transferred through the AAO pores into the aqueous solution, and DB18C6 is regenerated to its neutral form by interfacial dissociation and diffuses back to the tip to produce the enhancement. Dynamics and Thermodynamics of Ions Transport. A family of approach curves calculated for different concentrations is shown in Figure 1 clearly. In this study, the L/L-modified interface is different from the previous research, but there is no better way for fitting the experimental SECM approach curves in the theory, so we use the Bard’s formula.48 The steady-state current obtained is consistent with the asymmetric diffusion regime formed at the interface due to the specific shape of the micropipet and the mechanism of the facilitated ion transfer.46,49 The voltage applied between the micropipet and the reference electrode provides the driving force for the IT process. With the concentration of KCl and NaCl inside a pipet higher than the concentration
ð1Þ
2þ
cellðIIÞ
3þ
When the concentration of the Fe /Fe redox couple in the aqueous phase was in excess, the platinum-water interface was unpolarizable and acted as a reference/counter electrode for the aqueous phase. The current is then limited by the ion transfer reactions at the ITIES. The system of alkali metal ions transport facilitated by DB18C6 is a classical FIT process, and its mechanism has already been explained.50,56,57 Here the Kþ and Naþ through ion channels at the “biomembrane” had the similar mechanism, so the half-wave potentials of facilitated Kþ and Naþ transfer were evaluated in accordance with the TBATPB assumption in the form 0
1=2
Δwo φ0i - Δwo φi
0
0
1=2
¼ Δwo φ0TMA þ - Δwo φTMAþ
Δwo G0o f w ¼ nFΔwo φ0i
0
ð2Þ ð3Þ
0
where Δwo φi0 is the transfer potential of Kþ and Naþ, Δwo φi1/2 is the half-wave potential of Kþ and Naþ, Δwo φTMAþ1/2 is the formal transfer potential of TMAþ (199 mV), and Δwo 0φTMAþ1/2 is the half-wave potential of TMAþ (240 mV). Δwo G0ofw is the Gibbs energies of ion transfer, and F is the Faraday constant.58,59 Figures 2 and 3 show the cyclic voltammograms for Kþ and Naþ transfer through the ion channels at the W/DCE interface with different concentrations. It is obvious that the 4802
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Figure 2. Cyclic voltammograms of the transfer of Kþ facilitated by DB18C6 through ion channels on the Pt electrode. The concentrations of Kþ are 10, 20, 30, 40, and 50 mM, respectively, and the concentration of DB18C6 is 0.25 mM. Sweep rate is 50 mV/s. Inset: Concentration of Kþ is 10 mM; the DCE contains TBATPBCl but without DB18C6.
Figure 4. Relationship between the half-wave potential of the FIT of the Mþ system and the logarithm of Kr (Kr = CMþ/cDB18C6; CMþ is concentration of the Kþ or Naþ ion in the aqueous phase and cDB18C6 is concentration of the DB18C6 in the DCE).
Table 1. Kinetic Parameters for Facilitated Transfer of Kþ and Naþ with DB18C6 through the Ion Channels at the Bionic Membrane
half-wave potentials for ion transfer shift negatively with increasing concentration of alkali metal ion. At half-wave potentials of ∼0.45 V, the voltammogram is very well-shaped with a peak. The relationship between the anodic peak currents and the root of sweep rates obeys the Randles/Sevcik equation60-63 ip ¼ 0:4463 10-3 n3=2 F 3=2 AðRTÞ-1=2 DMþ cMþ v1=2 1=2
ð4Þ
where ip is the anodic peak current of the anodic polarization, A is the area of the micro-L/L interface, cMþ is the metal ion diffusion coefficient in aqueous solution, and the other parameters have been defined as above. The kinetic parameters can be found from the literature for given values ΔE1/4 andΔE3/4; the standard rate constant (κ0) is given by k0 ¼
λD0 a
ð5Þ
0
Kr
Na
20
0.464
0.251
24.2
0.049
40 80
0.446 0.431
0.232 0.217
22.4 20.9
0.082 0.122
120
0.428
0.215
20.7
0.152
160
0.408
0.194
18.8
0.167
20
0.509
0.295
28.5
0.002
40
0.474
0.260
25.1
0.003
80
0.444
0.230
22.3
0.006
120
0.428
0.214
20.7
0.007
160
0.413
0.199
19.3
0.008
K
Figure 3. Cyclic voltammograms of the transfer of Naþ facilitated by DB18C6 through ion channels on the Pt electrode. The concentrations of Naþ are 10, 20, 30, 40, and 50 mM, respectively, and the concentration of DB18C6 is 0.25 mM. Sweep rate is 50 mV/s. Inset: Cyclic voltammogram obtained with TMAþ ion transfer across the AAO-W/ DCE interface.
0
Δwo φ1/2 (V) Δwo φi0 (V) Δw0 G0tr,i,wfo (kJ 3 mol-1) Kf (cm 3 s-1)
ion
where κ0, D°, and R have been defined in the context. This method64 has been successfully taken to evaluate the standard rate constant of Kþ and Naþ transport across bionic membrane. As shown in Figure 4, Δowφi1/2 linearly depends on the logarithm of the concentration of Naþ (log Kr), Kr is ratio of concentration of Naþ and DB18C6, and the slope was found to be -0.07465. Kþ is the same as Naþ, and the slope was found to be -0.13793. The result offers tremendous advantages for linear relationship between the half-wave potential and concentration of Kþ and Naþ. In other words, the half-wave potential increases with the concentrations of alkali metals ion increasing. Effect of AAO on the Ion Transfer at the Bionic Membrane. Figures 2 and 3 present steady-state voltammograms for the transfer of Kþ and Naþ through the ion channel at the W/DCE interface facilitated by DB18C6 with different concentrations. As described by Stewart et. al,65,66 simple IT reactions at a micropipet are characterized by an asymmetric diffusion regime. It is obvious that the peak currents for facilitated ion transfer increase and the peak currents for Kþ transfer increase with increasing concentrations of alkali metals ion. (See the inset in Figure 3.) Table 1 shows the kinetic rate constants of the FIT at the different potentials added externally under various concentrations of the redox couple in the water droplet. These results are in 4803
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The Journal of Physical Chemistry C good agreement with the theoretical simulation developed by Stewart et al. The value obtained for DKþ0 is 1.40 10-8 cm2 s-1 and DNaþ0 is 2.74 10-7 cm2 s-1, which is smaller than the value of 1.5 10-5 cm2 s-1 from the previous research.60,67 From the experimental results, we can conclude that the AAO plays a block effect. To investigate the effect of the AAO on the rate constant, we further researched its structure. The serrated structures initiate to form at the bottom of nanochannels during the growth of the oxide membranes. The periodic serrated channels are aligned along the same direction with an inclination angle of 20-30° to the stem channel. The current density is concentrated around the bubble42,68-71 so that ion transport is suppressed through the bubble region. Therefore, it should be rather easy to understand why the AAO has a block on the electron transfer. The first process at the tip is the alkali ion (Mþ) transfer facilitated by DB18C6 from water to DCE; the second process is the interfacial dissociation reaction at the bottom W/DCE interface. When the tip approaches the substrate (aqueous) phase, Mþ is released from the complex and transferred to the aqueous solution, and DB18C6 is regenerated to its neutral form by interfacial dissociation and diffuses back to the tip to produce the current enhancement. Here the kinetic parameters for facilitated transfer of Kþ are a little smaller than Naþ, which may be caused by the radii of Kþ (1.38 Å) larger than the Naþ (1.02 Å) . This indicated that the resistance of Kþ is larger than that of Naþ when they through the ion channels. The L/L interface modified by the AAO is not quite flat, which leads to the experimental approach curves not being smooth.
’ CONCLUSIONS In this Article, the new method is described for investigating ion transport traversing the “ion channels” by SECM, which has the same trend of change on relationship between the half-wave potential and concentration with traditional L/L interface. Using this method, the lively process of ions traversing the bionic membrane can be monitored simply. The dynamics and thermodynamics processes have been determined using SECM, and the result indicates a tremendous advantage for a linear relationship between the half-wave potential and concentration of Kþ and Naþ. Moreover, the L/L-AAO interface not only has the advantages of traditional biomimetics but also has better research of process of ions traversing the bionic membrane. The L/LAAO interface could provide a simple and feasible method to study the ion transfer reaction for the future, which contributes to the biochemical applications such as drug discovery and sensors. ’ AUTHOR INFORMATION Corresponding Author
*Tel: þ86-931-7971276. Fax: þ86-931-7971323. E-mail: luxq@ nwnu.edu.cn.
’ ACKNOWLEDGMENT This work was supported by the Natural Science Foundation of China (nos. 20775060, 20927004, 20875077) and the Key Laboratory of Polymer Materials of Gansu Province. ’ REFERENCES (1) Schmalhofer, W. A.; Sanchez, M.; Dai, G.; Dewan, A.; Secades, L.; Hanner, M.; Knaus, H. G.; McManus, O. B.; Kohler, M.; Kaczorowski, G. J.; Garcia, M. L. Biochemistry 2005, 44, 10135–10144.
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dx.doi.org/10.1021/jp111915y |J. Phys. Chem. C 2011, 115, 4800–4805
