Subscriber access provided by Chicago State University
Article
Highly Sensitive, Selective and Patchable Pressure Sensor Mimicking Ion Channel Engaged Sensory Organ Kyoung-Yong Chun, Young Jun Son, and Chang-Soo Han ACS Nano, Just Accepted Manuscript • Publication Date (Web): 07 Apr 2016 Downloaded from http://pubs.acs.org on April 8, 2016
Just Accepted “Just Accepted” manuscripts have been peer-reviewed and accepted for publication. They are posted online prior to technical editing, formatting for publication and author proofing. The American Chemical Society provides “Just Accepted” as a free service to the research community to expedite the dissemination of scientific material as soon as possible after acceptance. “Just Accepted” manuscripts appear in full in PDF format accompanied by an HTML abstract. “Just Accepted” manuscripts have been fully peer reviewed, but should not be considered the official version of record. They are accessible to all readers and citable by the Digital Object Identifier (DOI®). “Just Accepted” is an optional service offered to authors. Therefore, the “Just Accepted” Web site may not include all articles that will be published in the journal. After a manuscript is technically edited and formatted, it will be removed from the “Just Accepted” Web site and published as an ASAP article. Note that technical editing may introduce minor changes to the manuscript text and/or graphics which could affect content, and all legal disclaimers and ethical guidelines that apply to the journal pertain. ACS cannot be held responsible for errors or consequences arising from the use of information contained in these “Just Accepted” manuscripts.
ACS Nano is published by the American Chemical Society. 1155 Sixteenth Street N.W., Washington, DC 20036 Published by American Chemical Society. Copyright © American Chemical Society. However, no copyright claim is made to original U.S. Government works, or works produced by employees of any Commonwealth realm Crown government in the course of their duties.
Page 1 of 30
1 2 3 4 5 6 7 8 9 10 11 12 13 14 15 16 17 18 19 20 21 22 23 24 25 26 27 28 29 30 31 32 33 34 35 36 37 38 39 40 41 42 43 44 45 46 47 48 49 50 51 52 53 54 55 56 57 58 59 60
ACS Nano
Highly Sensitive and Patchable Pressure Sensors Mimicking Ion Channel-Engaged Sensory Organs
Kyoung-Yong Chun†, Young Jun Son‡, Chang-Soo Han†,‡,* †
Development Group for Creative Research Engineers of Convergence Mechanical System,
School of Mechanical Engineering, College of Engineering, Korea University, Anam-Dong, Seongbuk-Gu, Seoul 136-713, Rep. of Korea ‡
School of Mechanical Engineering, College of Engineering, Korea University, Anam-Dong,
Seongbuk-Gu, Seoul 136-713, Rep. of Korea
KEYWORDS: Bioinspired, Ion channel, Pressure response, Receptor, Nanopore, Sensor
ACS Paragon Plus Environment
1
ACS Nano
1 2 3 4 5 6 7 8 9 10 11 12 13 14 15 16 17 18 19 20 21 22 23 24 25 26 27 28 29 30 31 32 33 34 35 36 37 38 39 40 41 42 43 44 45 46 47 48 49 50 51 52 53 54 55 56 57 58 59 60
Page 2 of 30
ABSTRACT
Biological ion channels have led to much inspiration because of their unique and exquisite operational functions in living cells. Specifically, their extreme and dynamic sensing abilities can be realized by the combination of receptors and nanopores coupled together to construct an ion channel system. In the current study, we demonstrated that artificial ion channel pressure sensors inspired by nature for detecting pressure are highly sensitive and patchable. Our ion channel pressure sensors basically consisted of receptors and nanopore membranes, enabling dynamic current responses to external forces for multiple applications. The ion channel pressure sensors had a sensitivity of ~5.6 kPa-1 and a response time of ~12 ms at a frequency of 1 Hz. The power consumption was recorded as less than a few µW. Moreover, a reliability test showed stability over 10,000 loading-unloading cycles. Additionally, linear regression was performed in terms of temperature, which showed no significant variations, and there were no significant current variations with humidity. The patchable ion channel pressure sensors were then used to detect blood pressure/pulse in humans, and different signals were clearly observed for each person. Additionally, modified ion channel pressure sensors detected complex motions including pressing and folding in a high-pressure range (10–20 kPa).
ACS Paragon Plus Environment
2
Page 3 of 30
1 2 3 4 5 6 7 8 9 10 11 12 13 14 15 16 17 18 19 20 21 22 23 24 25 26 27 28 29 30 31 32 33 34 35 36 37 38 39 40 41 42 43 44 45 46 47 48 49 50 51 52 53 54 55 56 57 58 59 60
ACS Nano
Ion channels are necessary units to sustain life in all living cells, and continuously transport appropriate ions through cell membranes. Moreover, the vital functions of ion channels are fundamentally indispensable for sensory organ homeostasis. Basically, ion channels provide electric signals to nerves, which are generated by ion movement across the cell membrane when receptors are activated by a diverse range of environmental stimuli such as heat,1 smell,2,3 sound,4 light,5 and pressure.6,7 To date, a number of research groups have achieved artificial ion channel sensors inspired by nature.8-14 Among them however, pressure detection using artificial ion channel systems has been quite rare and progress has been limited. In the field of biology, it is well known that a change in cell membrane potential occurs in response to mechanical stimuli via mechanosensory receptors such as the deflection of hair-cell stereocilia in the cochlea, and this is known as mechanotransduction.15 In particular, stretch-activated ion channels are one of the pressure-detecting mechanosensors present in microbes, yeast, and plants that have been studied over the last several decades,16 even though their exact operative mechanism is still under investigation. In general, mechanoreceptors in human skin can be divided into two types as either the rapidly adapting type as in Meissner’s and Pacinian corpuscles or the slow adapting type as in Merkel receptors and Ruffini cylinders.17 However, many perceptions are determined by the complex networking of these four receptors, such as when one holds a bottle in their hand without crushing it. Among these mechanoreceptors, we aimed to mimic Merkel receptors, which are located in the epidermis of human skin, and respond to steady pressure from small objects. The Merkel receptor works in the frequency range of 0.3–3 Hz. Thus far, most studies on flexible or patchable pressure sensors have involved silicone or polymer-based devices including those that are transistive,18-20 capacitive,21,22 piezoelectric,23,24 piezoresistive,25-27 or optical sensing.28,29 All these system are coupled between input and output
ACS Paragon Plus Environment
3
ACS Nano
1 2 3 4 5 6 7 8 9 10 11 12 13 14 15 16 17 18 19 20 21 22 23 24 25 26 27 28 29 30 31 32 33 34 35 36 37 38 39 40 41 42 43 44 45 46 47 48 49 50 51 52 53 54 55 56 57 58 59 60
Page 4 of 30
regions generating unstable electrical properties, low insensitivity to other stimuli, high working power, and static sensation. For instance, the main concern of piezoelectric sensors is their high internal resistance, which is significantly influenced by the input impedance of the readout electronic circuit and the low sensitivity to temperature and static forces.30 In the case of capacitive sensors, the main drawbacks are the noise related to the electric field interaction and the fringe effect, which limit their feasibility in specific electronics.31 The biological ion channel systems that sense external stimuli fundamentally consist of receptors and nanopores. Thus, the hybrid design of ion channels has been very elaborately and effectively evolved. A receptor can be mechanically triggered by external stimuli and the nanopores play an electrochemical role along with pathways for ion transport, and these two elements are coupled, which strongly resembles the coupling between the receptor regions given stimuli and the pores generating signals in nature. Furthermore, ion channels have multiple important key properties. First, ion channels are passive, and thus are not stoichiometrically coupled to the consumption of energy.32 Second, there is high selectivity in the recognition of substrates by their receptors. Additionally, direct signals are obtained from the transport of ions across the membrane following an electrochemical gradient without extra amplification or electric circuitry. Ion channels also conduct ions at very fast rates (>106 ions/s) in the micro to nanoscale dimension,32 which is not associated with a large consumption of energy. Therefore, ion channels are commonly used as sensors to monitor physical parameters including acceleration, temperature, properties of acoustic waves, fluidics, and pressure. Their many functional features can deliver dynamic spatial resolution, offer flexibility, and can be integrated into diverse surfaces in addition to their short response time and low power consumption.
ACS Paragon Plus Environment
4
Page 5 of 30
1 2 3 4 5 6 7 8 9 10 11 12 13 14 15 16 17 18 19 20 21 22 23 24 25 26 27 28 29 30 31 32 33 34 35 36 37 38 39 40 41 42 43 44 45 46 47 48 49 50 51 52 53 54 55 56 57 58 59 60
ACS Nano
In the current study, we demonstrate that bioinspired ion channel pressure sensors, that include receptors and nanopores, are simply constructed by stacking structures with polymers, electrolytes, and nanopore membranes. Such assembled ion channel devices lead to highly sensitive, responsive, selective, and dynamic pressure detection. The sensitivity of our ion channel pressure sensors was ~5.6 kPa-1 with response times of ~12 ms at a frequency of 1 Hz. The stability of our sensors was evaluated by current signals over 10,000 loading/unloading cycles. Moreover, variations in sensitivity were not significant in a humidity test. In application, the patchable ion channel pressure sensor described herein could successfully detect human blood pressure/pulse, and sense complex motions like pressing and folding.
RESULTS AND DISCUSSION First, we considered the conceptual design of a hybrid ion channel, which was inspired by biological ion channels in nature as shown in Figure 1A (left side). A general cellular response to mechanical deformation is indicated by a change in ion permeance through the plasma cell membrane corresponding to a change in current flow, which leads to the dissipation of electrochemical energy across the cell membrane. Such organismal function is essentially for physiological processes related to touch, stress, pain, and hearing. In this natural ion channel system, when external pressure is applied, the receptor is instantly triggered, and the artificial ion channel we fabricated herein can be similarly activated by ion transport across the membrane as shown in the right side of Figure 1A. The current changes generated by this ion transport can be monitored during the pressure-on phase by applying a potential between the two reservoirs. Figure 1B presents a schematic illustration of the fabrication procedure of the ion channel pressure-sensing device. The procedure involved three main steps: (i) mounting a reservoir
ACS Paragon Plus Environment
5
ACS Nano
1 2 3 4 5 6 7 8 9 10 11 12 13 14 15 16 17 18 19 20 21 22 23 24 25 26 27 28 29 30 31 32 33 34 35 36 37 38 39 40 41 42 43 44 45 46 47 48 49 50 51 52 53 54 55 56 57 58 59 60
Page 6 of 30
including polyaniline (PANi) electrolytes onto the polyvinylidene difluoride (PVDF) supporting material, (ii) installing a polycarbonate track-etched (PCTE) nanopore membrane onto the PANi reservoir, and (iii) attaching the PVDF (receptor) after mounting another PANi reservoir onto the membrane. The final ion channel device had a symmetrical shape with a nanopore membrane in the middle of two reservoirs. A detailed fabrication procedure is provided in the experimental section. Deformation of the sensors by mechanical stimuli induced ion movement across the membrane, leading to a change in current when a potential was applied (Figure 1C). When the device was in the pressure-off state, the sensors recovered to their original shape and simultaneously the ions reflow across the membrane, causing a return to the initial current value. Figure 1D shows a typical magnified scanning electron microscopy (SEM) image of the nanopore membrane with pores ~100 nm in diameter. Pore density was 4 × 108 pores/cm2 as mentioned by the supplier. The final ion channel device is shown in Figure 1E. The device was connected to Ag/AgCl electrodes with dimension of 20 × 15 mm2. To measure the current responses of our ion channel pressure sensors in response to mechanical stimuli, an in-house system consisting of a computer-controlled stepping motor and a force sensor were used to apply a precise external pressure with a frequency up to 2 Hz while electric signals were simultaneously recorded as shown in Figure 2A (also see Supporting Information, Movie S1). Current generated across the membrane with a bias could be changed by incremental loads, which induced the ion flow. The sensitivity, S of our pressure sensor was defined as the slope of the curve S = (∆I /Ioff)/∆p, where ∆p denotes the change in the applied pressure, and ∆I and Ioff denote the relative change in current and the current without the applied pressure, respectively. The ratios of current change (∆I/Ioff) were calculated on the basis of the
ACS Paragon Plus Environment
6
Page 7 of 30
1 2 3 4 5 6 7 8 9 10 11 12 13 14 15 16 17 18 19 20 21 22 23 24 25 26 27 28 29 30 31 32 33 34 35 36 37 38 39 40 41 42 43 44 45 46 47 48 49 50 51 52 53 54 55 56 57 58 59 60
ACS Nano
measured current values, and were plotted as a function of the applied pressure as shown in Figure 2B. The applied potential was 500 mV at 0.5 Hz. All data were plotted as the averages of four or five experiments. Pressure sensing was carried out for all samples under the same conditions. The size of the pressure-triggered ion channel device was 300 mm2. In the pressureon state, the current across the ion channel sensors showed an exponential relationship between ∆I/Ioff and applied pressure p; however, an approximately linear relationship between ∆I/Ioff and p was observed in the range of 0–3.5 kPa, revealing two regions of sensitivity as S = 2.3 kPa-1 and 5.6 kPa-1 under approximately 1 kPa. These sensitivity values are higher than the typical sensitivity of 0.005–0.55 kPa-1 reported for other pressure sensors.33-37 The increased sensitivity at high pressures could have arisen from the behavior of ion movement induced by the interaction between the deformational degree of the receptors and electrolytes as well as from the properties of the receptors including stiffness and hardness, though the exact mechanism of the increased sensitivity needs to be further studied. For the concept of our device, the receptors can essentially serve as tunable triggers that determine ion movement behavior across the membranes. An important consideration for receptors is to ensure that their associated current amplitudes have specific characteristics. According to different receptor types, dynamic signal shapes can be achieved. We selected three materials with different stiffnesses as mechanosensitive receptors. In comparison to PVDF (30 µm), mica (45 µm) and willow glass (30 µm) resulted in interesting performances. For example, when we used mica as a receptor, the shape of the output current signal was similar to that of PVDF except in the low-pressure range, and the sensitivity (S = 0.47 kPa-1) was lower than that of PVDF (Supporting Information, Figure S1). In the case of willow glass (30 µm), the slope of the sensitivity was almost linear in the range of
