NANO LETTERS
Highly Efficient Biocompatible Single Silicon Nanowire Electrodes with Functional Biological Pore Channels
2009 Vol. 9, No. 3 1121-1126
Julio A. Martinez,†,‡,§ Nipun Misra,†,‡,| Yinmin Wang,‡ Pieter Stroeve,§ Costas P. Grigoropoulos,| and Aleksandr Noy*,‡,⊥ Physical and Life Sciences Directorate, Lawrence LiVermore National Laboratory, LiVermore, California 94551, Department of Chemical Engineering, UniVersity of California, DaVis, DaVis, California 95616, Department of Mechanical Engineering, UniVersity of California, Berkeley, Berkeley, California 94720, and School of Natural Sciences, UniVersity of California, Merced, Merced, California 95344 Received December 3, 2008
ABSTRACT Nanoscale electrodes based on one-dimensional inorganic conductors could possess significant advantages for electrochemical measurements over their macroscopic counterparts in a variety of electrochemical applications. We show that the efficiency of the electrodes constructed of individual highly doped silicon nanowires greatly exceeds the efficiency of flat Si electrodes. Modification of the surfaces of the nanowire electrodes with phospholipid bilayers produces an efficient biocompatible barrier to transport of the solution redox species to the nanoelectrode surface. Incorporating functional r-hemolysin protein pores in the lipid bilayer results in a partial recovery of the Faradic current due to the specific transport through the protein pore. These assemblies represent a robust and versatile platform for building a new generation of highly specific biosensors and nano/bioelectronic devices.
Biological systems have evolved some of the most impressive tools for performing a variety of molecular-level tasks with the levels of sophistication and efficiency that are still unmatched by man-made structures. Living cells are full of proteins that use energy of chemical reactions to perform tasks ranging from mass transport to force generation to multistage information processing.1-3 Nanotechnology has for the first time allowed us to create and manipulate inorganic matter at the scale that is compatible with the biological systems, which opens up a variety of interfacing possibilities.4 Examples of nanomaterials use in biotechnology include nanotube and nanowire biosensors,5,6 quantum dot fluorescent tags,7 nanobarcodes,8 and drug delivery carriers.9 One-dimensional inorganic nanowires, in particular carbon nanotubes and silicon nanowires, possess a unique combination of structural and electrical properties that makes them attractive for electrochemical applications10 and potentially bioelectrochemical use. Specifically, nanoscale electrodes possess higher mass transport rates10,11 and have a smaller contribution of non-Faradic currents that improve signal-to* Corresponding author,
[email protected]. † Equal contribution. ‡ Physical and Life Sciences Directorate, Lawrence Livermore National Laboratory. § Department of Chemical Engineering, University of California, Davis. | Department of Mechanical Engineering, University of California, Berkeley. ⊥ School of Natural Sciences, University of California, Merced. 10.1021/nl8036504 CCC: $40.75 Published on Web 02/09/2009
2009 American Chemical Society
noise ratio10,12 over the macroscale electrodes. Silicon nanowires represent a particularly useful platform system because their size and electronic properties can be controlled with high precision over a significant range. Another advantage of silicon nanowires as a bioelectrochemistry platform is that their surface is “biologically friendly” and allows straightforward functionalization with molecular targets that could detect binding of specific analytes.13-15 However, a large portion of biological functionality is performed by membrane proteins that control the transport of molecules and ions through biological membranes with extremely high precision and specificity. Utilization of these proteins in bioelectrochemical measurements requires the use of biomimetic matrices that could support membrane proteins in their functional form. Phospholipid bilayers represent such universal matrix that mimics the cellular membrane.16,17 Previous work by our group18,19 and others20 showed that onedimensional nanomaterials are compatible with lipid bilayer structures. Here we show that individual silicon nanowires coated with the lipid bilayers shell provide an effective and versatile bioelectrochemistry platform. We demonstrate that highly doped metallic silicon nanowires represent an efficient nanoscale electrode. Lipid bilayer coating on these electrodes provides an effective barrier layer that shields the electrode surface from the solution redox-active species. Finally, we demonstrate that this system is capable of detecting the insertion of the membrane proteins into the lipid matrix.
Figure 1. (A) TEM image of a highly doped Si nanowire showing the core/shell structure of the wire. Insert shows the diffraction pattern of the core indicating nanowire crystallinity. (B) Schematics of the measurement setup used for two-electrode voltammetry. The sourcemeter (S-M) and reference electrode are connected to common ground point. (C) Scanning electron microscopy image of the SiNWE in the LOR-3A/Si3N4 trench. (D) Current response of a single SiNWE (black curve) recorded during the anodic voltage sweep in redox solution vs Ag/AgCl reference electrode. Red curve represents the current response obtained for a similar device without SiNWs (i.e., just metal contacts protected with silicon nitride and LOR-3A with a trench in the vicinity).
Silicon Nanowire Electrode Fabrication and Characterization. Our devices were fabricated using metallic highly doped p-type silicon nanowires (SiH4:B2H6 ) 200:1) grown using catalytic vapor-liquid-solid synthesis with an average diameter of 87 nm, range 43-130 nm (see Materials and Methods in Supporting Information for details). Transmission electron microscopy (TEM) images of these wires (Figure 1A) show that they possess a core-shell structure that resulted from the in situ lateral growth of the silicon nanowire (SiNW) induced by the large concentration of diborane.21 Nanowires were deposited from solution onto the silicon wafer surface using a flow alignment technique and conventional photolithographic steps were used to define metal contacts to the nanowires (20 nm of Ti followed by 80 nm of Pt) (Figure 1B) Electrical characterization of silicon nanowire electrodes (SiNWEs) yielded resistivities between 0.007 and 0.08 Ω cm, Ohmic SiNWE/metal contacts, and mobilities of ∼0.2 cm2/(V s) which are comparable to previously reported values for SiNWs at similar doping levels21,22 and substantially different from the typical values reported for heavily doped amorphous p-type silicon.21 Effective protection of the metal electrodes is critical for the use of SiNW devices in solution; therefore our device electrodes were covered by an 80 nm overlayer of plasma 1122
enhanced chemical vapor deposition (PECVD) silicon nitride. Previous studies demonstrated that PECVD silicon nitride coating could be used to shield metal-nanowire contacts from the solutions species.4 Unfortunately, we found that this approach alone did not reduce the leakage current observed in our devices below 50 pA which was still too large for the electrochemical measurements. To obtain more effective shielding, we have developed a combined approach that utilized a second fabrication step where we covered the wafer surface with a 400 nm thick LOR-3A layer and used another photolithography step to open up trenches that exposed 5-7 µm long segments of the nanowire surfaces (Figure 1C). The resulting devices exhibited leakage currents of less than 5 pA, which ensured optimal detection conditions for our experiments. Our design also allowed us to interrogate single and multiple nanowires using the same chip. Cyclic voltammetry was performed using a two-electrode approach with the SiNW functioning as the working electrode (Figure 1B) and a leak-free Ag/AgCl electrode functioning as a reference electrode; this configuration is similar to the setup used by LeMay, Dekker, and co-workers to characterize the performance of single carbon nanotube electrodes. Anodic potential sweeps in the presence of the Fe(CN)64species in solution show a characteristic electrochemical Nano Lett., Vol. 9, No. 3, 2009
Table 1. Summary of the Oxidation Rate Constant (k0) and Transfer Coefficients β Obtained from Fitting the Measured Current Response of Single (16 Devices) and Multiple (4 Devices) Si Nanowire, and Flat Si (5 Devices) Electrodes to Equation 1 k0 (cm/s)
electrode
β -3
single Si NW (1.2 ( 1.0) × 10 0.28 ( 0.13 multiple Si NW (1.6 ( 1.0) × 10-3 0.24 ( 0.08 a -9 flat Si (6.5 ( 3.9) × 10 0.4 ( 0.02 flat gold (1 mMFe(CN)641.5 × 10-2 0.57 in 0.5 M KCl)26 a 0 k and β for flat silicon are obtained by the fitting of experimental data to the Tafel equation (eq 3).
current that results from the oxidation process on the SiNW surface (Figure 1D). Anodic Faradic current from p-type SiNWEs is largely dominated by the transfer of holes from the valence band to Fe(CN)64- in solution, but a minimal contribution of electron injection from solution to the conductance band is also possible.23,24 An anodic sweep of silicon electrodes in pure water solutions often leads to the growth of silicon oxide (anodic oxide),23 and a similar effect is also expected for SiNWE. In absence of redox species in solution, this oxide layer would continuously grow in thickness until hole tunneling will no longer be possible; however, solution Fe(CN)64- can stabilize the formation of anodic oxide, making voltammetric applications in such conditions possible.25 Notably, the contribution to the total observed current is negligible (Figure 1D) due to the small dimensions of the SiNWE. The sigmoid shape of the curve in Figure 1D is characteristic of surface-limited electrochemical processes with mass transport contribution at large bias, and it can be modeled by the classical Butler-Volmer equation for onestep single charge exchange imt
i) -f(E-E0)
1+e
+
imt AFk0C0
(1) -βf(E-E0)
e
where imt is the mass transport limiting current, A is the NW electrode area, F is the Faraday constant, k0 is the standard
first-order oxidation rate constant, C0 is the bulk concentration of Fe(CN)64-, β is the anodic transfer coefficient, f is equal to F/(R T) (38.9 V-1 at 25 °C), E is the applied potential, and E0 is the standard redox potential for Fe(CN)64(0.24 V vs Ag/AgCl electrode). Fitting of the measured electrochemical response provides estimates of the two main electrode parameters (k0 and β) for single and multiple SiNW electrodes (Table 1). A striking feature of the SiNWEs is that their efficiency (as measured by the k0 value) is almost 6 orders of magnitude higher than the efficiency that we measured for flat heavily doped p-type Si electrodes (Figure 2A and Table 1). Moreover, the measured value of the kinetic constant of the single SiNWEs was approaching the values reported for a flat gold electrode (Table 1). The first clue for understanding the origins of the highly efficient transport on the SiNWEs comes from the analysis of the measured anodic transfer coefficient, β. β values measured for the SiNWEs were significantly lower than typical values for metal electrodes (degenerate semiconductors behave like a metal and show β ≈ 0.5; semiconductor electrodes have β ≈ 1).27 Researchers reported that redox reactions on electrodes with thin nonuniform insulating coating films can show large variations in local rates because electron tunneling is more efficient in places where the coating film is disordered or defective.28,29 As a consequence, fitting experimental electrochemical data with simple models such as eq 1 could artificially lower the transfer coefficient as a way to compensate for the large distribution of k0. A likely possibility is that our SiNW electrodes are covered with a very thin or highly defective anodic oxide that causes the observed high efficiency of the electrochemical reactions. This conclusion is supported by the TEM images of the SiNWs that show either a very thin layer of oxide or almost no oxide layer at all (Figure 1A). Additional verification for this explanation comes from the quantitative comparison of the values of kinetic constant for the SiNWEs and flat Si electrodes. Faradic current for the flat
Figure 2. (A) Faradic current density for a SiNWE and flat silicon electrode. Note the additional scaling factor for the current measured flat silicon. Solid lines represent a fit to eq 1 for the single SiNWE data and a fit to eq 3 for the flat Si electrode data. (B) Faradic current as a function of the electrode area for multiple and single SiNWE (as indicated in the legend). Faradic currents are normalized to a single redox probe concentration of 50 mM. A solid line represents the linear regression forced to go through the origin. Nano Lett., Vol. 9, No. 3, 2009
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Figure 3. (A) Schematic of a Si nanowire coated by the lipid bilayer that incorporates R-hemolysin biological pore channel. (B) Faradic current response recoded before and after lipid bilayer formation onto SiNWE. (C) Tafel plot of the electrochemical response of a single SiNWE before and after bilayer formation and after subsequent R-hemolysin incubation. (D) Electrochemical response of a multiple SiNWE (same conditions and measurement sequence as used to record the data shown in (C). Solid lines in (C) and (D) represent best fits of the experimental data to eq 3.
Si electrodes did not show saturation within the range of applied anodic potentials, indicating that surface oxidation of Fe(CN)64represented the limiting reaction step (Figure 2A). Values of the transfer coefficient β obtained for flat silicon electrode also fall within the expected range of values for metallic electrodes; however the values of the standard kinetic constant were almost 6 orders of magnitude lower than the values observed for the SiNW electrodes (Table 1). This observation leads us to conclude that the redox reactions on the surface of the flat Si electrode were impeded by a uniform layer of anodic oxide formed on flat silicon wafers. A recent study reported a similar type of discrepancy between the dielectric properties of thermal oxide on SiNW surfaces and flat silicon surfaces.30 The barrier for the hole tunneling through the oxide layer leads to a decrease of the first-order kinetic constant through a simple relationship k ) k ′ e-θt
(2)
where k′ is the kinetic constant at the surface of the electrode in absence of tunneling barrier, t is the oxide thickness, and θ is the decay constant factor.27 Our flat Si electrodes were covered by 7 Å thick layer of oxide, as measured by ellipsometry; therefore, if we assume that the values of the kinetic constant obtained for SiNWEs represent the transport efficiency in absence of the anodic oxide, k′, then eq 2 predicts the value of the decay constant factor, θ, of 1.7 Å-1. 1124
This value compares favorably with the literature value of 0.9 Å-1 reported for mercury/2 nm thermal silicon oxide/ p-type Si semiconductor diodes31 and 0.8-1.5 Å-1 reported for saturated self-assembled monolayers on gold electrode in solution.32-34 Our previous work35 established the feasibility of covering the surface of SiNWs with a continuous lipid bilayer layer that could act as a barrier for solution species transport. To realize this one-dimensional bilayer concept in a functional electrochemical device and to quantify the shielding behavior of the lipid layers, we deposited a dioleoylphosphatidylcholine (DOPC) lipid layer onto the SiNW electrodes using vesicle fusion. Surface plasmon resonance measurements on flat PECVD SiO2 surfaces showed that the thickness of the final lipid membrane was 4.4 nm, as expected for a DOPC bilayer.36 Notably, lipid-shielded electrodes show a markedly weaker electrochemical response: after DOPC coating the current on a SiNWE decreased by 90% (as measured at 0.6 V relative to Ag/AgCl electrode) (Figure 3B). Note also that the current versus voltage characteristics for the coated SiNWE does not show the classical sigmoidal shape predicted by eq 1; most likely because the mass transfer of Fe(CN)64- is slowed down by the lipid bilayer. Since the shape of the i-E curves recorded for the lipid-coated and uncoated (bare) electrode devices is different, a better way Nano Lett., Vol. 9, No. 3, 2009
Table 2. Tafel Equation Parameters for Lipid-Bilayer-Coated Silicon Electrodes parameter
SiNW electrode
k0BL (cm/s) (6.3 ( 5.8) × 10-5 β 0.11 ( 0.09 k0BL/k0barea 0.10 ( 0.09 iBL/ibare (0.6 V) 0.13 ( 0.08 a 0 k bare calculated from eq 1 for SiNW.
flat Si electrode (1.4 ( 0.6) × 10-9 0.22 ( 0.05 0.20 ( 0.05 0.012 ( 0.001
to characterize the shielding efficiency of the lipid bilayer coating would be to consider its effects on the electrode parameters as defined by the Tafel equation (the Butler-Volmer equation reduces to the Tafel equation in the case of mass transfer limitations) ln i ) ln(FAk0C0) + fβ(E - E0)
(3)
Comparison of the Tafel equation fit parameters (Figure 3C and Table 2) for the coated and uncoated electrodes shows that the formation of the lipid bilayer on top of the nanowire reduced the k0 by approximately an order of magnitude. We can safely discard the hole tunneling through the lipid bilayer as the reason for this decrease, as the bilayer is too thick to support efficient tunneling. Current reduction could also be caused by an increasing thickness of anodic oxide on the electrode. However, at least for the flat silicon electrode, the formation of an extra layer of oxide would reduce k0 (eq 2), but the β value should remain unchanged because of the good quality of anodic oxide on flat Si. Yet, the data show (Table 2) that lipid coating leads to a significant shift in the β values. Therefore, we suggest that the reduction of k0 and β is indeed caused by the lipid bilayer blocking of the transport of the redox species to the NW electrode surface. A similar effect and comparable decrease of k0 and β have been observed in voltammetric studies of lipid bilayers deposited onto selfassembled monolayers.37,38 The relative decreases of k0 and β after lipid bilayer fusion are comparable for SiNWE and flat silicon electrode which could indicate that both systems have similar bilayer shielding capacity. However, the flat silicon electrode shows a reduction of the Faradic current at 0.6 V applied potential of about 1 order of magnitude larger relative to SiNW electrodes. It is tempting to assign this discrepancy to the lower shielding capacity of the lipid layers on SiNW electrodes due to the higher defect density in the highly curved bilayer. Indeed, Roiter et al. observed39 that the formation of lipid bilayer onto silica nanoparticles larger than 22 nm in diameter was size dependent and could produce a discontinuous lipid bilayer due to nonuniformities on the surface with high curvature. However, we believe that the most likely explanation for this discrepancy comes from the different regimes of the mass transport characteristic for these two types of electrodes. The small dimension of SiNW electrodes ensures a high mass transfer rate of Fe(CN)64-, which can sustain large Faradic current in the mass transfer dominated regime. We also observed that bare SiNWE has a large k0, which allows it to reach the mass transfer dominated regime at low applied overpotentials. In that regime, the current no longer can grow exponentially with the increase in the applied potential. When the SiNW electrode is covered by a lipid bilayer, it reduces the efficiency of the electrode reaction and the mass transfer-dominated limit is not reached; Nano Lett., Vol. 9, No. 3, 2009
therefore the ratio of currents observed at 0.6 V applied potential underestimates the true shielding effect of the lipid bilayer. In contrast, a bare flat Si electrode does not reach the masstransport-dominated regime. Therefore the ratio of heterogeneous standard rate constants observed between the bare and lipid-coated electrodes provides a better estimate of the bilayer shielding ability. Note also that multiple SiNWE (Figure 3D) behaves as a single SiNWE which suggests that the proximity (sometimes less than 1 µm separation) does not substantially affect the shielding characteristics of the lipid bilayer (LB) formed onto SiNWEs. One of the most important properties of the lipid bilayers is their ability to serve as a matrix for a variety of biological ion channels. If the lipid-coated SiNWE incorporates functional biological pores, then specific transport through the pore could modulate the electrochemical response of the electrode. To provide a proof-of-concept demonstration of such integration, we doped the lipid bilayers with bacterium exotoxin R-hemolysin (R-HL) from Staphylococcus aureus. R-Hemolysin is a self-inserting polypeptide that forms a welldefined heptameric pore of 1.4 nm in diameter at the narrowest point in lipid membranes that can pass small electroactive molecules.40-43 Significantly, we observed that protein insertion into the lipid bilayer produces an increase in the Faradic current due to the unimpeded transport of the Fe(CN)64- ions through the R-HL pores (Figure 3C,D). The incorporation of R-HL into the lipid bilayer resulted in k0R-HL/ k0bare ) 0.7 ( 0.4 and 0.2 ( 0.1 for SiNW and flat silicon electrodes, respectively. We suggest that the larger standard rate constant observed for SiNW electrodes could indicate better insertion of R-HL in the supported bilayer. One possibility is that the region between the SiNWE and the silicon oxide substrate underneath it may provide a small span where the LB is suspended over a thin liquid layer; a similar possibility was previously suggested for LB deposited onto silicon nanoparticles.39 We showed that highly doped SiNWE could achieve a significantly higher electrochemical oxidation rate as compared to flat silicon electrode at similar doping levels. Nanoscale dimensions of the SiNWE enables enhanced mass transport rates that give large limiting Faradic current densities and enable SiNWEs to reach high current densities within reasonable applied voltages. We present a simple and versatile route for making these electrodes biocompatible by coating them with a supported lipid bilayer. Finally, we showed that specific permeability of protein pores incorporated in the lipid bilayer could modulate device’s electrochemical response. Our results open up a number of interesting opportunities. SiNW electrodes provide a straightforward solution to creation of microfabricated multiplexed electrode arrays for probing biological objects. Perhaps the most intriguing is the possibility of incorporating passive and active biological ion pores in these constructs and using them to create new generations of nanobioelectronic devices. Acknowledgment. A.N. acknowledges support from the Biomolecular Materials Program at the DOE Office of Basic Energy Sciences. J.M. acknowledges support from the LSP program at LLNL. J.M. and N.M. contributed equally to this 1125
work. Parts of this work were performed under the auspices of the U.S. Department of Energy by Lawrence Livermore National Laboratory under Contract DE-AC52-07NA27344. Supporting Information Available: Descriptions of materials and methods and electrochemical characterization of the flat silicon electrodes. This material is available free of charge via the Internet at http://pubs.acs.org.
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References (1) Alberts, B.; Bray, D.; Lewis, J.; Raff, M.; Roberts, K., Molecular Biology of the Cell, 3 ed.; Garland: New York, 1994. (2) Berne, R. M.; Levy, M. N.; Koeppen, B. M.; Stanton, B. A., Physiology, 5th ed.; Mosby: St Louis, MO, 2004. (3) Jordan, P. C. Fifty years of progress in ion channel research. IEEE Trans. Nanobiosci. 2005, 4 (1), 3–9. (4) Patolsky, F.; Timko, B. P.; Yu, G. H.; Fang, Y.; Greytak, A. B.; Zheng, G. F.; Lieber, C. M. Detection, stimulation, and inhibition of neuronal signals with high-density nanowire transistor arrays. Science 2006, 313 (5790), 1100–1104. (5) Patolsky, F.; Zheng, G. F.; Hayden, O.; Lakadamyali, M.; Zhuang, X. W.; Lieber, C. M. Electrical detection of single viruses. Proc. Natl. Acad. Sci. U.S.A. 2004, 101 (39), 14017–14022. (6) Patolsky, F.; Lieber, C. M. Nanowire Nanosensors. Mater. Today 2005, (04), 21–28. (7) Gupta, M.; Caniard, A.; Touceda-Varela, A.; Campopiano, D. J.; Mareque-Rivas, J. C. Nitrilotriacetic Acid-Derivatized Quantum Dots for Simple Purification and Site-Selective Fluorescent Labeling of Active Proteins in a Single Step. Bioconjugate Chem. 2008, 19 (10), 1964–1967. (8) Um, S. H.; Lee, J. B.; Park, N.; Kwon, S. Y.; Umbach, C. C.; Luo, D. Enzyme-catalysed assembly of DNA hydrogel. Nat. Mater. 2006, 5 (10), 797–801. (9) Kam, N. W. S.; O’Connell, M.; Wisdom, J. A.; Dai, H. J. Carbon nanotubes as multifunctional biological transporters and near-infrared agents for selective cancer cell destruction. Proc. Natl. Acad. Sci. U.S.A. 2005, 102 (33), 11600–11605. (10) Heller, I.; Kong, J.; Heering, H. A.; Williams, K. A.; Lemay, S. G.; Dekker, C. Individual single-walled carbon nanotubes as nanoelectrodes for electrochemistry. Nano Lett. 2005, 5 (1), 137–142. (11) Chen, S. L.; Kucernak, A. The voltammetric response of nanometersized carbon electrodes. J. Phys. Chem. B 2002, 106 (36), 9396–9404. (12) Bertoncello, P.; Edgeworth, J. P.; Macpherson, J. V.; Unwin, P. R. Trace level cyclic voltammetry facilitated by single-walled carbon nanotube network electrodes. J. Am. Chem. Soc. 2007, 129 (36), 10982. (13) Cui, Y.; Wei, Q. Q.; Park, H. K.; Lieber, C. M. Nanowire nanosensors for highly sensitive and selective detection of biological and chemical species. Science 2001, 293 (5533), 1289–1292. (14) Zheng, G. F.; Patolsky, F.; Cui, Y.; Wang, W. U.; Lieber, C. M. Multiplexed electrical detection of cancer markers with nanowire sensor arrays. Nat. Biotechnol. 2005, 23 (10), 1294–1301. (15) Chen, R. J.; Bangsaruntip, S.; Drouvalakis, K. A.; Kam, N. W. S.; Shim, M.; Li, Y. M.; Kim, W.; Utz, P. J.; Dai, H. J. Noncovalent functionalization of carbon nanotubes for highly specific electronic biosensors. Proc. Natl. Acad. Sci. U.S.A. 2003, 100 (9), 4984–4989. (16) Favero, G.; Campanella, L.; Cavallo, S.; D’Annibale, A.; Perrella, M.; Mattei, E.; Ferri, T. Glutamate receptor incorporated in a mixed hybrid bilayer lipid membrane array, as a sensing element of a biosensor working under flowing conditions. J. Am. Chem. Soc. 2005, 127 (22), 8103–8111. (17) Favero, G.; D’Annibale, A.; Campanella, L.; Santucci, R.; Ferri, T. Membrane supported bilayer lipid membranes array: preparation, stability and ion-channel insertion. Anal. Chim. Acta 2002, 460 (1), 23–34. (18) Artyukhin, A. B.; Shestakov, A.; Harper, J.; Bakajin, O.; Stroeve, P.; Noy, A. Functional one-dimensional lipid bilayers on carbon nanotube templates. J. Am. Chem. Soc. 2005, 127 (20), 7538–7542. (19) Huang, S. C. J.; Artyukhin, A. B.; Martinez, J. A.; Sirbuly, D. J.; Wang, Y.; Ju, J. W.; Stroeve, P.; Noy, A. Formation, stability, and mobility of one-dimensional lipid Bilayers on polysilicon nanowires. Nano Lett. 2007, 7 (11), 3355–3359. (20) Zhou, X. J.; Moran-Mirabal, J. M.; Craighead, H. G.; McEuen, P. L. Supported lipid bilayer/carbon nanotube hybrids. Nat. Nanotechnol. 2007, 2 (3), 185–190. (21) Lauhon, L. J.; Gudiksen, M. S.; Wang, C. L.; Lieber, C. M. Epitaxial 1126
(26)
(27) (28)
(29)
(30)
(31)
(32)
(33) (34)
(35)
(36)
(37)
(38)
(39)
(40)
(41)
(42)
(43)
core-shell and core-multishell nanowire heterostructures. Nature 2002, 420 (6911), 57–61. Cui, Y.; Duan, X. F.; Hu, J. T.; Lieber, C. M. Doping and electrical transport in silicon nanowires. J. Phys. Chem. B 2000, 104 (22), 5213– 5216. Zhang, X. G. Electrochemistry of silicon and its oxide; Kluwer Academic/Plenum: New York, 2001. Koval, C. A.; Howard, J. N. Electron-Transfer at Semiconductor Electrode Liquid Electrolyte Interfaces. Chem. ReV. 1992, 92 (3), 411– 433. Madou, M. J.; Loo, B. H.; Frese, K. W.; Morrison, S. R. Bulk and Surface Characterization of the Silicon Electrode. Surf. Sci. 1981, 108 (1), 135–152. Krysinski, P.; Brzostowska-Smolska, M. Three-probe voltammetric characterisation of octadecanethiol self-assembled monolayer integrity on gold electrodes. J. Electroanal. Chem. 1997, 424 (1-2), 61–67. Morrison, S. R. Electrochemistry at semiconductor and oxidized metal electrodes; Plenum Press: New York, 1980. Horrocks, B. R.; Mirkin, M. V.; Bard, A. J. Scanning Electrochemical Microscopy 0.25. Application to Investigation of the Kinetics of Heterogeneous Electron-Transfer at Semiconductor (WSe2 and Si) Electrodes. J. Phys. Chem. 1994, 98 (37), 9106–9114. Finklea, H. O.; Avery, S.; Lynch, M.; Furtsch, T. Blocking Oriented Monolayers of Alkyl Mercaptans on Gold Electrodes. Langmuir 1987, 3 (3), 409–413. Stratakis, E.; Misra, N.; Spanakis, E.; Hwang, D. J.; Grigoropoulos, C. P.; Fotakis, C.; Tzanetakis, P. Imaging dielectric properties of Si nanowire oxide with conductive atomic force microscopy complemented with femtosecond laser illumination. Nano Lett. 2008, 8 (7), 1949–1953. Faber, E. J.; de Smet, L. C. P. M.; Olthuis, W.; Zuilof, H.; Sudholter, E. J. R.; Bergveld, P.; van den Berg, A. Si-C linked organic monolayers on crystalline silicon surfaces as alternative gate insulators. ChemPhysChem 2005, 6 (10), 2153–2166. Krysinski, P.; Zebrowska, A.; Palys, B.; Lotowski, Z. Spectroscopic and electrochemical studies of bilayer lipid membranes tethered to the surface of gold. J. Electrochem. Soc. 2002, 149 (6), E189–E194. Bard, A. J.; Faulkner, L. R. Electrochemical methods: fundamentals and applications, 2nd ed.; Wiley: New York, 2001. Paddon-Row, M. N., Electron and Energy Transfer. In Stimulating Concepts in Chemistry; Vo¨gtle, F., Stoddart, J. F., Masakatsu, S., Eds.; Wiley-VCH: Weinheim, 2000; pp 267-291. Huang, S.-C. J.; Artyukhin, A. B.; Martinez, J. A.; Sirbuly, D. J.; Wang, Y.; Ju, J.-W.; Stroeve, P.; Noy, A. Formation, Stability, and Mobility of One-Dimensional Lipid Bilayers on Polysilicon Nanowires. Nano Lett. 2007, 7 (11), 3355–3359. Stroumpoulis, D.; Parra, A.; Tirrell, M. A kinetic study of vesicle fusion on silicon dioxide surfaces by ellipsometry. AIChE J. 2006, 52 (8), 2931–2937. Krysinski, P.; Moncelli, M. R.; Tadini-Buoninsegni, F. A voltammetric study of monolayers and bilayers self-assembled on metal electrodes. Electrochim. Acta 2000, 45 (12), 1885–1892. Cannes, C.; Kanoufi, F.; Bard, A. J. Cyclic voltammetry and scanning electrochemical microscopy of ferrocenemethanol at monolayer and bilayer-modified gold electrodes. J. Electroanal. Chem. 2003, 547 (1), 83–91. Roiter, Y.; Ornatska, M.; Rammohan, A. R.; Balakrishnan, J.; Heine, D. R.; Minko, S. Interaction of nanoparticles with lipid membrane. Nano Lett. 2008, 8 (3), 941–944. Gu, L. Q.; Braha, O.; Conlan, S.; Cheley, S.; Bayley, H. Stochastic sensing of organic analytes by a pore-forming protein containing a molecular adapter. Nature 1999, 398 (6729), 686–690. Song, L. Z.; Hobaugh, M. R.; Shustak, C.; Cheley, S.; Bayley, H.; Gouaux, J. E. Structure of staphylococcal alpha-hemolysin, a heptameric transmembrane pore. Science 1996, 274 (5294), 1859–1866. Glazier, S. A.; Vanderah, D. J.; Plant, A. L.; Bayley, H.; Valincius, G.; Kasianowicz, J. J. Reconstitution of the pore-forming toxin alphahemolysin in phospholipid/18-octadecyl-1-thiahexa(ethylene oxide) and phospholipid/n-octadecanethiol supported bilayer membranes. Langmuir 2000, 16 (26), 10428–10435. Bao, H. F.; Peng, Z. Q.; Wang, E. K.; Dong, S. J. Loosely packed self-assembled monolayer of N-hexadecyl-3,6-di(p-mercaptophenylacetylene)carbazole on gold and its application in biomimetic membrane research. Langmuir 2004, 20 (25), 10992–10997.
NL8036504 Nano Lett., Vol. 9, No. 3, 2009
