Cell Nanomechanics Based on Dielectric Elastomer Actuator Device
The main components, principle, and technology of dielectric elastomer actuator (DEA) were reviewed to illustrate that DEA can be an effective carrier for mechanobiology research.
Comparison between DEA-based bioreactors and current commercial devices is provided, as well as the outlook of the DEA bio-applications in the future.
KeywordsDielectric elastomer actuator Mechanical stimulus Bioreactor Mechanobiology
Mechanobiology is an emerging science concern about the effects of mechanical loadings and physical forces on cell behaviors and diseases . Biological cells and tissues living in vivo environment are exposed to several mechanical stimulations such as stretching and contracting. As reported so far, mechanical loadings can be sensed by cells and then influence cellular behaviors like migration, proliferation, orientation, and gene expression [2, 3, 4, 5, 6, 7, 8, 9]. Additionally, some diseases such as atherosclerosis  and cancers  are proved to have similar relation with mechanical cues as well. For example, Kim et al.  found that mechanical effects can affect cellular remodeling and regeneration of tissue, which means the possibility of developing cell-based therapies. Besides, Park et al.  confirmed that equiaxial and uniaxial strains have different induction effects on the differentiation of mesenchymal stem cells. In a word, people are now trying to achieve better understand of cellular mechanism for the purpose of developing more effective and advanced biomedical technology.
However, studying mechanical stimulus in vitro directly remains difficult because the traditional cell culture technology cannot provide such mechanics, so the first problem need to solve is to apply mechanical stimulations to cells while cultured in vitro to mimic the true environment in vivo. As reported so far, some methods have been taken to apply mechanical loadings on cells, including hydrostatic pressure and fluid shear [14, 15, 16], other interesting devices such as biochip , wrinkled skin-on-a-chip , pneumatic stretching system , motor-driven system , piezoelectric , and optical actuation methods [22, 23]. More recently, a custom-built open-source stretch system assembled from laser-cut acrylic plates emerged . In general, such a gap between engineering and biology is attractive and even profitable; some companies have entered this market and are selling their products, which include Flexcell system [25, 26] from Bio-Equip, STB-1400  from Strex, etc. Generally, these means require complex designs and result in complicated system structures and besides high costs. In contrast, dielectric elastomer actuators (DEAs) are simpler, have advantages of highly controllable deformation, sub-millisecond response time, and optically transparent, and can be integrated with cell culture environment conveniently. Since Pelrine et al.  presented their landmark discovery about electrostatically activated elastomeric actuators in 2000, this novel technology has been used in many fields, such as energy harvesters , tactile displays , soft robotics [31, 32] and what to be emphasized here, mechanically biological cells stimulus, and the potential application as the biosensor to measure the cellular contraction force.
In this review, firstly we introduce the basic dielectric elastomer actuator technology simply, including the components and actuation mechanism of the DEA devices, and the characterization methods. Secondly, we overview the applications of DEA-based devices in the field of cellular mechanical loading, which can be divided into bio-stretching device and biosensor. Thirdly, comparisons of popular commercial methods and DEA-based devices are made. Lastly, we further provide our prospect on DEAs’ applications in the future mechanobiology research.
2 Components of the DEA Devices
DEAs are typically simple in structure and require very different materials with traditional actuators like electric motors. Briefly, the dielectric elastomer membrane (DEM) and the compliant electrodes are what demanded, the pre-stretched DEM sandwiched by electrodes [32, 33] and then fixed by rigid frames. These two main components are the key to determine the performance of DEA-based devices and combine with various pre-stretch sets to make DEA forms diversify.
2.1 Dielectric Elastomer Membrane
The DEM belongs to one subcategory of electroactive polymers (EAPs), which can respond to electrical stimulation with significant size or shape change, and has already emerged as a new actuation material . As one of the most important components of DEAs, the material properties of DEM directly determine the actuation performance of DEAs. Since the 1990s, researchers have conducted massive experiments to find proper DEM materials, such as silicones, polyurethanes, acrylics, and nitrile rubbers. Among these, silicones and acrylics are the two most commonly used materials. The most widely used acrylic DEM is 3 M VHB 4910 and 3 M VHB 4905 . Both of them are made of a mixture of aliphatic acrylate, which shows a property of high viscosity, flexibility, and tensile resistance. However, the VHB-based DEAs show serious viscoelastic nonlinearity that makes the precision tracking control challenge [36, 37, 38, 39, 40, 41].
Silicone rubber, which has good elastic properties, has fast strain response speed, and can maintain constant modulus at higher temperature, is one of the commonly used matrices for the preparation of DEM materials although the deformation degree of silicone membrane is low. Because of its weak viscoelastic characteristics, the response speed of silicone film is faster and shows higher efficiency. Besides, Akbari et al.  have presented theoretical guidelines for improving the deformation actuation of silicon-based DEM by changing the pre-stretch ratios.
Actually, DEA devices used for biomedical and bioinspired systems have already been reported , such as refreshable braille displays for the blinds and bioinspired tunable lenses for the visually impaired. However, as reported by Herbert Shea and colleagues, for cell- and tissue-related applications, the DEM materials to be chosen should satisfy some special requirements : Firstly, they should be non-cytotoxic and compatible with standard cell culture protocols like sterilization and incubation; secondly, they need to be optically transparent for the convenience of integrating with the optical microscopes. After that, the selection of DEMs can be flexible since various designs and fabrications may be chosen. For example, some works used Sylgard 186 (Dow Corning) as the DEM and covered it with Silbione LSR 4305 (BlueStar Silicones) as the biocompatible membrane, which contacts the biological samples directly [44, 45]. Besides, as the alternative, other PDMS has been used as well [46, 47, 48]. In our group, ELASTOSIL Film 2030 250/100 from WACKER was used to meet the principles above.
2.2 Materials and Techniques for Electrodes
Another indispensable element for DEAs is the compliant electrode; well-designed electrodes patterning can bring the charges to the target shape and area and therefore form the desired deformation. As commonly accepted, the electrode materials should have some properties: (1) They have the ability to maintain conductivity during large strains; (2) their stiffness can be ignorable, comparing with that of DEM; (3) they have the ability to maintain good stability ; (4) they are preferably to be patternable for conducting flexible electrode designs . For applications on cells and tissues, as reported by Samuel Rosset et al. , manufacturability, miniaturization, impact on DEA performance, and the compatibility with low-voltage operation need to be taken into consideration. In this section, some widely used electrode materials are introduced.
2.2.1 Carbon-Based Electrodes
Because of the low stiffness and ability to maintain conductive at large strain [50, 51, 52], carbon-based electrodes are the most popular electrode materials for DEAs; typically, they can be divided into three main categories: carbon powder, carbon grease, and conductive rubber.
Carbon Powder Electrodes The main outstanding merit of powder-based electrodes is their less contributory to the stiffness of the DEM. Applying the loose carbon powders directly on the membrane became the solid choice in the early stage. However, the disadvantages of carbon powder are obvious: It is difficult to maintain conductivity at large strain [53, 54] and lifetime is also limited because of the detaching of conductive particles from electrodes .
Conductive Rubber Electrodes Similar but not identical to carbon grease, conductive rubbers are produced through directly mixing conductive particles with silicone. As a result, the ablation or migration of the conductive particles can be avoided, and the lifetime of the electrodes can be extended. However, the impact on the stiffness of the DEM is not negligible .
Clearly, a mask covered on the surface of the membrane can be helpful to paint the carbon material into desired shape. Pelrine et al.  have presented their work for fabricating loose carbon grease and powder-based electrodes. To improve the uniformity, Schlaak et al.  proposed the use of spray coating as presented in Fig. 1a, which is an efficient manufacture method and can be used for commercial applications. Similarly, the electrodes can be stamped on the DEM . In such case, fabricate a soft stamp into desired pattern by replication on an etched silicon negative master as shown in Fig. 1b. Besides, printing techniques can also be used to pattern electrodes as presented in Fig. 1c since the carbon-based materials can be made into conductive ink . As reported by Krebs, printing methods have been utilized to manufacture flexible devices . More advanced, high-resolution and robust compliant electrodes for silicon-based soft actuators and sensors are completed through laser ablation technology  (Fig. 1d).
2.2.2 Metallic Electrodes
2.2.3 Transparent Electrodes
Basically, the conductive materials which meet the requirements of DEA electrodes application are non-transparent. However, some works proposed several transparent electrodes that can be potentially used in optical applications. As reported, Hu et al.  have studied transparent and conductive nanotube thin films on electrical and optical properties. Kovacs et al.  found that loose carbon black with extremely thin thickness can be partly transparent when applied on adhesive acrylic membrane. Implanted palladium and gold electrodes have also been reported to be possibly present transparency with a ratio of 35 and 70%, and the value is dependent on the metal and the implanted dose . Besides, ionic hydrogel is a novel, ordinarily, and transparent material for electrodes of DEAs [66, 67]. Combining ionic hydrogel with 3D printing, people successfully fabricated electric-driven soft actuators that can achieve a maximum vertical displacement of 9.78 ± 2.52 mm at 5.44 kV .
As mentioned above, DEAs for cellular research need to be optically transparent. Therefore, the development of transparent electrodes can accelerate the applications of DEAs of cellular use; before that, much work is still demanded to develop such novel electrodes materials and techniques.
3 Actuation Mechanism of DEAs
Generally, for the DEA-based devices, it is noteworthy that the pre-stretch of DEM is another indispensable design parameter that can affect the performance. Obviously, pre-stretching can prevent the buckling of the dielectric elastomer when electrically activated. Secondly, pre-stretching the elastomer contributes to improve the performance of DEAs since it can increase electromechanical instability (EMI) of the membrane [28, 72, 73, 74, 75]. Additionally, equiaxial and uniaxial pre-stretch can help to generate equiaxial and uniaxial strain, respectively. Therefore, it is common to change the amplitude and ratio of pre-stretch to generate desired behaviors of DEAs.
Figure 3c, d shows the classical configuration of DEAs for cell mechanical stimulus . Usually, the rigid frame is necessary to hold pre-stretch of the DEM. Once the voltage is applied, the area with electrodes is expanded, while the remaining area is compressed. As a result, the expanded area is defined as active and can be used for stretching the cells and the compressed area is called passive and can be adopted to compress the cells.
4 Evaluation of DEAs
It is important to understand cellular environment when studying cells’ responses to the mechanical loadings, so precisely characterization of DEA devices is indispensable, that is, we need to gain the strain distribution of our target area in the DEA. Currently, finite element modeling (FEM) and image processing (machine vision and digital image correlation) techniques are widely used to calculate the strain distribution.
FEM is a non-contact way commonly used in many fields to calculate stress and strain distribution of a mechanical/structural system . To complete the FEM, some basic parameters of the materials are required such as Poisson’s ratio and elastic modulus. Constrain the model with certain boundary conditions and divide it through multiple grids, calculate the strain in every single grid, and finally generate the whole strain distribution. For example, Akbari et al.  optimize the geometric configuration of the actuator by using a simplified FEM.
Besides the strain distribution, the basic deformation–voltage responses (average strain) can be obtained through image processing as well. As reported by Rosset et al., they measured the strain of actuator using machine vision via a LabVIEW image processing to track the four corners of the electrodes . After calibration, the coordinates of these four corners that are under both actuated and non-actuated states are recorded, so that the curve of voltage induced strain can be plotted.
5 DEA-Based Devices for Cellular Research
According to the different cell amounts that the DEA-based bioreactors may apply in, they can be divided into two categories: one for single cell and the other for a small population of cells or in other word tissue engineering.
5.1 DEA-Based Bio-Stretcher/Reactor for Single Cell
5.2 DEA-Based Bioreactor for Small Population of Cells
Such a progress actually indicates the diversified future of the DEA-based bioreactor. DEAs can be applicable for different purposes and further fabricated into the bioreactor with a specific function.
5.3 DEAs Designed for the Measurement of Traction Force of Cells
6 Comparison Between Usual Commercial Bioreactors and the DEA-Based Ones
Performance parameters of different technologies and models
Uniaxial stretch 2, 4, 5, 8, 10, 12, 15, 20%
1/60, 1/30, 1/10, 1/6, 1/3, 1/2, 1 Hz
Uniaxial stretch 2, 4, 5, 8, 10, 12, 15, 20%
1/60, 1/30, 1/10, 1/6, 1/3, 1/2, 1 Hz
Uniaxial stretch 2, 4, 6, 8, 10, 12, 15, 20%
1/60, 1/10, 1/3, 1 Hz
Nikon and Olympus
Uniaxial stretch (2 switchable modes)
1/6, 1/3, 1/2, 1 Hz
Nikon and Olympus
Biaxial stretch and compression, ~ 30%
0.05, 0.2, 0.5 Hz
Nikon and Olympus
Stretch, ~ 30%
Sinusoidal, etc.; custom definable
Sinusoidal, etc.; custom definable
Uniaxial stretch ~ 38% compression ~ 12%
> 10 Hz, customer definable
In a word, DEAs can be a greater available carrier choice for cellular mechanical loading research. Therefore, we give a brief outlook of DEAs’ applications (next section) and hope to enlighten the combination of mechanobiology and DEAs.
7 Outlook of DEAs in Cellular Mechanical Loading Research
A phenomenon of cellular and tissue behavior adjustment is strongly associated with the changes in extracellular matrix (ECM) and protein expression, which can be determined by the loading and cell type. For in vitro cellular stimulus, we can deform the cell membrane by stretching the cell adhesion substrate [95, 96]. Over the past years, people have conducted interesting researches on the load-sensitive cells, trying to discover the relations between cellular responses and different loading conditions. Although most of the published results were completed by the pneumatic and motor-driven devices, comparison suggests that DEA-based devices share the properties as well or even better, so the following applications can theoretically be the references for development of DEA-based bioreactors.
For broader fields to discuss, tumor research and rehabilitation engineering may be appropriate [106, 107, 108]. Uncontrolled proliferation of tumor causes forces interaction to the ECM and tissues nearby, which can be usually classified into shear, compress, and stretching stresses . Hofmann et al.  found that mechanical stretching increases the proliferation of cancer cells, while Helmlinger et al.  found that compressive stress inhibits the growth of tumor spheroids. Besides, cells and tissues in human’s joint undergo complex forces during our daily life, which means that rehabilitation research from athletic injury can be inspired from mechanical stimulus as well. As reported, the state of tendon and meniscus can be associated with mechanical loadings. 10%-strain dynamic compression promotes anabolic of meniscus, while strain at 20% regulates the state into catabolism , and the responses can be frequency and time dependent. More interestingly, cyclic tension strains show inhibition of inflammatory of meniscal cells . In addition, experimental results demonstrated that tendons also respond to mechanical loads, appropriate loads enhance tendons, while chronic mechanical loading may accelerate tendinopathy [112, 113].
In this section, we simply introduce several potential applications of DEA-based devices for mechanobiology research, including cellular reorientation, endocytosis, etc. Actually, much more concrete scenarios of this field are still waiting to be explored. Similar to the motor-driven devices, DEAs are at the junction of medical (biology) and engineering science; they can be designed into various mechanical loading bioreactors while maintaining cell and tissue affinity. As a promising tool, we hope that DEAs can contribute to the development of mechanobiology.
Exploring the response of cells is an exciting, evolving but challenging task which is significant for biomedicine engineering. Directly, many illnesses can be linked with the disordered cells and tissues functions, which means that it makes sense to research cellular responses under various mechanical loadings for better understanding of some diseases or even cancers. Furthermore, if we can regulate cells and tissues into the proper states or functions through mechanical stimulus, some effective and promising treatments can be developed.
In this work, we firstly provide simple introduce of DEAs, including components, actuation principle, evaluation methods, and several applications on cellular mechanical loading. Then, we compare the DEA-based bioreactors with current widely used custom-built bioreactors, showing their connections and differences, and some prominent properties of DEAs stand out. At last, we give short outlook of DEA technology in the future mechanobiology research.
In a word, although much corresponding examples are still lack, employing DEAs as the bioreactors and biosensors for cellular applications is actually opening the door of cellular mechanobiology through a novel method. As the new generation of actuators, DEAs bring some irreplaceable advantages compared to traditionally used peers like the motor-driven and pneumatic: They have simpler structure, faster response, and higher controllability. In addition, DEAs are more flexible to design and can be easily catered the request of biocompatible and combine with microscope to form an experimental system. Among these advantages, the property of rapid response makes the DEA-based devices potential to simulate some extreme conditions, such as sudden cardiac death, which is absolutely difficult to realize by some other bioreactors. Furthermore, continuous advances in material science and microfabrication technology make it feasible and promising to study cellular response of mechanical stimulus through DEA devices since they can be manufactured into micro–nanoscale, and then design into high-throughput devices that are meaningful for cellular research. What is more, because the using of powerful algorithm and image processing tools, this field can be multidisciplinary and a hot issue in the future, which means low threshold for the people to conduct this study.
Nevertheless, some challenges still remain elusive. Firstly, the drive voltage for DEAs is usually too high (several thousand volts), which makes this technique risky and limit their broad applications. Therefore, much works are still need to cut down the required voltage or electric field. As reported, for example, Shea’s group have tried to reduce the voltage by decreasing the thickness of DEM . Secondly, optimization of DEAs’ basic performance can be crucial, including larger strain, higher energy density, longer lifetime (cycles that can be tolerated, longer shelf time), and better stability, and all of these are important to determine DEAs’ further applications in both cell and tissues’ mechanobiology and other possible fields.
The authors are grateful for the financial support from the National Natural Science Foundation of China (Grant Nos. 81822024, 11761141006, and 21605102) and the National Key Research and Development Program of China (Grant No. 2017YFC1200904).
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