Mechanism and Machine Theory 78 (2014) 131–140

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Mechanism and Machine Theory

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A novel MEMS device for the multidirectional mechanicalstimulation of single cells: Preliminary results

Francesca Antoniolli, Stefano Maggiolino, Nicola Scuor, Paolo Gallina⁎, Orfeo SbaizeroDepartment of Architecture and Engineering, University of Trieste, via A. Valerio 10, 34127 Trieste, Italy

a r t i c l e i n f o

⁎ Corresponding author.E-mail address: pgallina@units.it (P. Gallina).

http://dx.doi.org/10.1016/j.mechmachtheory.2014.03.0094-114X/© 2014 Elsevier Ltd. All rights reserved.

a b s t r a c t

Article history:Received 6 September 2011Received in revised form 19 December 2013Accepted 21 March 2014Available online 18 April 2014

In recent years, understanding cell mechanics has gained increasing importance, with significantimplications for humanhealth. Currently, different technologies have been developed to perform themechanical stimulation of living cells. However, they often show some limitations. Here we presentthe development and characterization of a novelmicroelectromechanical system (MEMS), designedto perform a multidirectional mechanical stimulation of single living cells: in this way, in vitro cellbehavior is closely simulated. The proposed device employs a new compliant spring linkage tomovea twelve-slice sectioned plate that works as a seating platform for the cell under study. The wholeplatform ismoved bymeans of four series of bimorph thermal actuators, which allow displacementsin 12directions in the x–y plane. Results show theworkability of the device under certain conditions,with important implications for a better understanding of cell mechanics and related disease.

© 2014 Elsevier Ltd. All rights reserved.

Keywords:MEMSLinkage mechanismCell stretchingSingle cellMechanical stimulation

1. Introduction

Living cells can sense mechanical forces and convert them into biological responses. Similarly, biological and biochemicalsignals are known to influence the abilities of cells to sense, generate and bear mechanical forces [1]. Studies in the mechanics ofsingle cells have rapidly evolved in the past decade with important implications for biotechnology and human health. Manysystems have been created to stretch and study the mechanical properties of single cells.

According to Bao and Sures, these can be classified into three main categories: the first is constituted by local probes, such asthe tip of an AFM, which performs the local stimulation of a single cell [2,3]; the second is represented by devices that can exertthe mechanical loading of an entire cell. This category includes optical tweezers [4,5] and microplates [6]. In the third category,the simultaneous mechanical stretching of an entire population of cells is performed [7,8]. Unfortunately these systems are oftenvery complicated and present some limitations: for example, they fail to allow the stimulation of an entire cell (such as the AFM),they cannot be used to study adherent cells [9], they exert forces only in the pN range (such as the optical tweezers), and theygive an average response on a huge number of cells (such as the stretching devices).

An alternative and novel approach is represented by MEMS, an acronym for microelectromechanical systems. MicrofabricatedMEMS have already found a niche in the biology community: they can be used to sense, stimulate, manipulate or control cells andbiomolecules [10]. In a certain sense they are superior to the technologies described above since they have suitable dimensions forsingle-cell studies, they can exert forces in the range of nN–μN [11] and they can be applied to whole and adherent cells. They canwork in a liquid environment, have biocompatible surfaces and can be easily integrated in other instruments such as fluorescencemicroscopes or spectroscopic devices, thus obtaining details on the structure and morphology of the whole cell, too. We believethat this approach is superior to current atomic force microscopy methods that cannot measure the properties of the whole celland optical trap methods that cannot be applied to cells adhered to a substrate. Using our MEMS approach, it is possible to both

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actuate and sense at a length scale comparable with single cells. Besides stress–strain data, this approach, in combination withstandard biological microscopy techniques, can give information on the structure and morphology of the whole cell.

In recent years, a MEMS device for the biaxial stimulation of living cells has been developed [12]. Such a device consists in anin-plane biaxial cell stretcher rather than out of-plane stretching, typical of the flexion of membranes (see Fig. 1). The sittingplatform which hosts the cell is split into 4 slices. When the electrostatic actuator is operated, thanks to a linkage mechanism, the2 opposite slices move far away. An in-plane MEMS actuator can easily provide a few micrometers of displacement, using onlyflexural joints. This level of displacement better compares with the dimensions of typical target cells (e.g. adult myocytes), thatcan be of the order of 50 μm [13]. The drawback of this mechanism is that a biaxial stimulation does not always represent the beststimulation to guarantee the environment of a living cell.

Here we present the design and characterisation of a novel MEMS device to perform the multidirectional mechanicalstimulation of single cells that uses bimorph thermal actuators as the engine to drive the entire structure.

The proposed device represents an upgrade of the biaxial stimulation one. It is capable of pulling single cells from 12 differentdirections pointing to the center of the device. This way stress–strain conditions come closer to those of a membrane subjected toa uniform radial force. In many biological environments, cells undergo this kind of isotropic stress state. For this reason, it isreasonable that a multidirectional mechanical stimulation device could be employed as a useful tool for studying mechanical andbiological properties of living cells.

The paper is devoted mainly to the ideation and the synthesis of the linkage mechanism and to its practical implementation.After the kinematic analysis and the design considerations, the building process is explained. Eventually, experimental results arepresented in order to validate the prototype.

2. Kinematic analysis

A schema of the device is presented in Fig. 2. The heart of the MEMS consists in the mechanism located at the center of thepicture. 12 arrow-shaped slices point to the center of the mechanism. The area where the cell to be stimulated can be located isgiven by the disc made up by the tips of the arrows.

As can be noticed, the mechanism can be divided into 12 identical slices. In order to get an insight into the kinematic behaviorof the mechanism, let us consider a single sector separately. It is useful to refer to Fig. 3a. The linkage represents a detail of thewhole mechanism of Fig. 2 (the red colored portion). Basically, one of the 12 sectors, is made up of a rigid bar (vertical bar EG inthe figure) that we refer to as the ‘arrow’ and 2 pinned–pinned beams (EF and GH in the figure). Since the arrow is 20 μmwide, it

Fig. 1. Schema of the biaxial stimulation MEMS device.

Fig. 2. Schema of the multidirectional stimulation MEMS device.

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can be assumed to be a rigid body. Since the two horizontal beams are 2 μm wide they behave as springs. Their compliantbehavior is represented by the red shape in the figure. Thanks to the fact that the beams are perpendicular to the bar they arelinked to, it can be assumed that, for small displacements, the arrow can move along a line pointing to the center of themechanism (point P).

Therefore, from a kinematic point of view, for small displacements, each one of the two springs/beams can be thought ofas a rigid link with two revolute joints at its ends. This way, the single slice sub-mechanism introduced in Fig. 3a has the samebehavior of the 4-bar linkage represented in Fig. 3b. Of course, this new kinematic model, does not take into account thestiffness of the two beams, but it is a good candidate to analyze the kinematic behavior of the whole mechanism.

In Fig. 3c a new sector is added. In order to synchronize the movement of the new arrow with the contiguous one, a rigid linkhas been introduced between points A and B. The rod AC is rigidly fixed to the initial arrow; at the same time, rod BD is rigidlyfixed to the second arrow. The two rods are connected trough the link AB. Note that, as shown in Fig. 4, the two ends A and B ofthe link have been thinned. This way, points A and B of the mechanism behave as flexural hinges [14]. Let us refer to the link AB as‘chain link’. Lengths of the links are given in Table 1.

Let us carry out the velocity analysis of the mechanism considering the vector notation introduced in Fig. 5. Consider an XYCartesian reference frame. The loop closure equations for the 4-bar linkage is

FE�! þ EG

�! − GH�! þ HF

�! ¼ 0: ð1Þ

Taking the derivative of the above relation and considering that φFE = π, φEG ¼ 32π and φHG = π, it yields

zEGφEG ¼ 0−zFEφFE þ zHGφHG ¼ 0

⇒φEG ¼ 0φFE ¼ zFE

zHGφHG:

8<:

8<: ð2Þ

Therefore, as was predicted, the arrow EG, for small displacements, does not rotate. The arrow can only translate along its axis(dot line). For the same reason, point A moves along line m (red line) and point B moves along line n. The loop closure equationsfor the triangle ABR leads to

RA�! þ AB

�! þ BR�! ¼ 0: ð3Þ

Deriving and considering that, for Eq. (2), φBR ¼ φRA ¼ 0, it yields

z R AcosφRA−zABsinφABφAB þ z B RcosφBR ¼ 0

z R AsinφRA þ zABcosφABφAB þ z B RsinφBR ¼ 0:

(ð4Þ

Fig. 3. Kinematic behavior of a single sector of the mechanism.

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In conclusion, sinceφBR ¼ π6, φRA = 0 andφAB ¼ 19

12π, replacing the angles into Eq. (4) and simplifying, the relationship betweenthe velocity of point A along line m and the velocity of point B along line n is

z R A ¼ z B R: ð5Þ

Fig. 4. Central detail of the mechanism.

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In other words, the chain link AB introduced between the two slices, causes that when the tip of the arrow EG moves along itsaxis from the center P of the mechanism of an amount δ, the tip of the contiguous arrowmoves along its axis from the same centerof the same amount δ. This way the two tips become synchronized.

The whole mechanism is made up of 12 slices (12 arrows) located around the center P, each one rotated π6 with respect to the

previous one. Each one is linked to the previous one through a chain link (see rod AB described above). Therefore, when the twoopposite and vertical arrows as well as the two opposite and horizontal arrows are pulled (by the four actuators), all the 12 tips ofthe center of the mechanism open with a radially symmetrical movement. This way the multidirectional mechanical stimulationof a single cell placed at the center of the mechanism is possible.

In order to avoid asymmetric kinematic behaviors, another chain link has been introduced between the last slice and the firstone. The drawback of this solution is that the whole mechanism becomes overconstrained. In fact, according to Grubler'sequation [15], the degrees of freedom of the mechanism are

Table 1Geomet

Link

PEEFGHGE

D:o:F ¼ l−1ð Þ � 3−r � 2 ¼ 49−1ð Þ � 3−72� 2 ¼ 0 ð6Þ

l is the number of rigid links (frame included) and r is the number of revolute joints. But, for small displacements, the

whereconstraint introduced with the aforesaid rod is redundant and inconsistent. Its effect consists only of increasing the overallstiffness of the mechanism. In any case, this increment is not enough to prevent the actuators from pulling the arrows, as wastested by FEM analysis.

3. Prototype description

Fig. 6 shows a picture of the device, taken with a microscope (Leica M3Z) provided with a photo camera (Leica DFC420),entirely supported on a 2 × 2 mmMEMS outline. At the heart of the device is a twelve-slice sectioned plate that works, if made tofunction properly by a protein such as fibronectin, as an adhesion platform for the cell being tested. Each of the twelve slices ismechanically connected to the proximal ones via the compliant spring linkage described in previous Section, designed to assurehomogeneous displacement of the platform slices in the six movement directions. In addition, four of the twelve slices are

rical parameters of the mechanism.

μm Link μm

292 EC 37114 CA 6945 BD 44

154 PD 163

Fig. 5. Kinematic schema.

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connected to four groups of eight thermal actuators, designed to move the entire platform structure. The dimensions and shape ofthe sectioned plate were designed according to the fabrication rules and minimum features available (2 μm) from themicrofabrication process used to build the MEMS device.

Concerning the actuation component, several motion principles can be employed in MEMS technology: thermal actuation,comb drive, magnetic and piezoelectric actuation. Thermal actuators have several advantages: they need low driving voltages andexhibit larger displacements and forces than electrostatic actuators. For these reasons, four sets of eight bimorph thermalactuators were designed to operate the stretcher. Bimorph actuators were preferred to V-shaped ones because of their capacity toexert higher forces, in the range of μN. Motion in bimorph actuation is given by the differential Joule heating, produced by a

Fig. 6. Picture of the mechanism.

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current flow, of a cold and a hot arm, which were respectively designed as 6-micron and 32-micron large arms. The stiffness of thestructure, the twelve slices and the springs linkage was estimated by means of finite element analysis using a commerciallyavailable software package (Femlab 3.4), assuming plane stress and stress–strain linearity conditions. Assuming for thepolysilicon a Young's modulus of 158 GPa and a Poisson's ratio of 0.22 [16], the total stiffness of a quarter of the entire platform isabout 2.44 N/m. The finite element model of the platform is shown in Fig. 7, in which a virtual force of 1 nN is applied at each ofthe main slices along the direction of motion. The value of the virtual force (1 nN) does not represent the real force acting on theMEMS in real environment conditions. Its value is used just to estimate the stiffness of the structure.

The PolyMUMPs process was chosen to build the MEMS devices. PolyMUMPs is a commercially available program thatprovides cost-effective, proof-of-concept MEMS fabrication to industry, universities and government worldwide [17]. It is athree-layer polysilicon micromachining process designed to be as general as possible and to be capable of supporting manydifferent designs on a single silicon wafer.

The layers are: an n-type silicon wafer, a silicon nitride layer for electrical isolation, a 500-nm polysilicon film, a 2.0 μmpolysilicon layer and another polysilicon layer.

The final layer in PolyMUMPs process is a 0.5 μm gold metal layer that provides probing, electrical connections and highlyreflective mirror surfaces. Before release, the photoresist stripping has been performed by dipping the MEMS for 3 min in acetone.The release has been carried out by immersing the chip in a 49 HF bath, at room temperature, for 2 min. After release, the MEMShas been rinsed in DI water and propilic alcohol for several minutes to reduce stiction. Drying has been performed in an oven at110 °C for 10 min. For characterization and testing, the devices have been glued on a chip carrier with cyanoacrylate adhesivepaste; electrical connection to the carrier has been achieved by welding a gold wire (25 μm in diameter) by means of the ballbonding process (4124 Manual Gold ball bonder).

4. Experimental results

In order to test the efficiency of the thermal actuators, the MEMS device was actuated and characterized in three differentenvironments: in vacuum (10−6 mbar), in air and in DI water. Increasing DC voltage starting from 0 V was applied through a DCpower supply (62006P-300-8, Chroma) and current was recorded by means of a current meter (DM 102 Plus, Digimaster). Tomeasure the platform slice displacement, tests were performed: in the first case, a scanning electron microscope (JSM-7401 F,Jeol) equipped with a home-made electrical feed-through system was used; and in the second and third cases, tests were carriedout placing the MEMS device on the stage of an optical microscope (Optiphot, Nikon) equipped with a digital camera (Coolpix4500, Nikon). As a consequence, distances between opposite tips at different applied voltages were evaluated, in the first casethrough the SEM utilities, and in the second and third protocol instances by taking digital camera micrographs and measuringdistances with a commercial image processing software package (Image Pro Plus 5.0). In this way, applied voltage–current flowand applied voltage–displacement characteristics could be traced in each environment.

Fig. 7. Finite element model of the platform.

Fig. 8. Test in vacuum environment: a) null displacement; b) maximum displacement.

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Fig. 8 shows two SEM micrographs (in a high vacuum environment) of the circular platform centre when 0 V (a) and 8 V (b)are respectively applied. It can be noted that the distance between opposite tips is approximately the same in all directions, inaccordance with the initial design of the linkage apparatus. The maximum displacement was recorded with an applied potentialof 8 V and was approximately 9 μm between opposite tips. When a potential of 8.5 V was applied, burning of the thermalactuators occurred. This is because the MEMS is operated in a vacuum environment. The experiment was repeated 3 times, slowlyincreasing the applied tension (steps of 0.5 V every 10 s), until the MEMS burned. Each trial shows similar results, proving thatthe test was conducted under repeatability conditions.

Fig. 9 shows two optical micrographs of the platform operating in air when potentials of 0 V (a) and 14.5 V (b) wererespectively applied. The test was repeated twice, slowly increasing the tension (steps of 0.5 V every 10 s) from 0 to 14.5 V andwaiting 10 s in the ‘open’ configuration. After that the tension was slowly decreased until 0 V.

In DI water tests, no displacement could be recorded because water hydrolysis occurred when a potential higher than 1.5 Vwas applied.

Fig. 10 shows the current flow as a function of the applied voltage in the three different environments. As expected, in all threeenvironments the characteristic remains linear only for low applied potentials and current flows. With increasing current flow,Joule heating occurs, increasing the total resistance of the system. In addition, it can be noted that in the linear tract, the slope ofthe curves is lower for the SEM data, medium for the air data and higher for the water data. This is due to the different thermaltransfer mechanisms occurring in the three different environments. In vacuum, the only thermal transfer mechanism is radiation,so the system is subjected to more pronounced heating. In air, the thermal transfer mechanism consists of radiation andconduction. At the microscale, in fact, the heat transfer contribution through convention is negligible [18]. Lastly, the heat transfermechanism in water takes place, as in the case of air, through radiation and conduction. However, the conductivity coefficient inwater is approximately 20 times that of air [19], so the system is subjected to a more pronounced cooling in water than in air.

Fig. 9. Tests in air: a) initial configuration; b) maximum displacement.

Fig. 10. Current flow as function of the applied voltage.

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Fig. 11 shows the displacement occurring at the platform opposite tips as a function of the applied voltage in vacuum and airenvironments. As expected, the system efficiency in the vacuum environment is higher than in air. This greater efficiency can beobserved, on the one hand, as higher displacement with an equally applied potential; and on the other hand, as the maximumobtainable displacement, that is about 9 μm in vacuum versus about 2 μm in air. This is due to the possibility of reaching highertemperatures when working in a vacuum environment, because of the almost complete absence of oxygen. Instead, in air, wherethe oxygen percentage is around 21, polysilicon combustion takes place at lower temperatures. Two other side effects whichcontribute to increased efficiency in a vacuum environment are represented by the higher temperature difference achievablebetween hot and cold arms, due to the only radiation contribution to heat transfer, and by the lower friction and stiction betweenmoving structures and substrate in the SEM vacuum chamber.

5. Future work

The novel MEMS device for the multidirectional mechanical stimulation of single cells described in this work is thus ready tobe used for testing with living cells. Despite the limitations encountered with thermal actuators when working in a liquidenvironment, which are aggravated when the solution is conductive such as in the case of a cell culture medium, the device asdesigned and built is suitable for performing experimental tests by covering only the central part with a microscopic drop ofmedium, where the sectioned platform is located. Liquid evaporation can be prevented by placing the entire set-up in anenvironmentally controlled chamber, with high percentage humidity. The microscopic solution drop can be placed on the deviceusing a glass capillary, previously stretched by means of a hot puller, which allows the creation of a glass micro-tip with acurvature radius of a few microns. In this way, the glass capillary, moved by means of a micromanipulator, can be used to placeboth the solution drop and the living cell. At the same time, in order to achieve a more user-friendly device, a new idea is beingdeveloped: the idea is to divide the device into two MEMS 2 × 2 mm outlines: the first, holding the cell adhesion platform,working in liquid environment; the second, in which the thermal actuators will be located, working in air. A mechanicalconnection between the two MEMS can be realized as a post-processing technique by means of a carbon fiber, which is around atenth in diameter and millimeters in length, or by means of a gold micro-wire, welded to the microstructures using a traditionalwire bonding for electrical connections.

Fig. 11. Displacement as a function of the applied voltage.

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One drawback of the presented mechanism is the size of the central hole (25 μm). It is larger than the size of some cells(e.g. spread-out mammalian cells), making it impractical to plant the cell onto the stretching plates. On the other hand, it isnot possible to reduce the size of the hole indefinitely because of geometrical and MEMS production limitations. Therefore,future upgrades of the mechanism should face this problem, finding a trade-off between production limits and applicability.However, this MEMS can work with large size cells (e.g. neurons, oocyte or cargiomyocytes) that can be placed in the centralstage without falling into the hole. Moreover, the MEMS is suitable for studying the adhesion forces between two cells. Thereare genetic mutations targeting the particular structure (desmosome) which bond to cells together, and therefore it isimportant to place on the MEMS stage two cells at the same time.

6. Conclusions

A novel MEMS device has been developed to study the mechanical properties of single cells and their response to externalmechanical stimuli. The cell seating platform was designed as a twelve-slice sectioned plate to simulate cell behavior in vivo asbest as possible by performing a multidirectional displacement. Bimorph thermal actuators were developed to move the entiresystem. The device was fabricated via a commercially available multi-user MEMS process and characterized in differentenvironments. The results, according to the theoretical principle, showed worse results when passing from vacuum to air andliquid. As expected, in all three environments the characteristic remains linear only for low applied potentials and current flows.In the linear tract, the slope of the curves is lower for the SEM data, medium for the air data and higher for the water data. Thisendorses the different thermal transfer mechanisms occurring in the three different environments. However, the system canwork properly with living cells only if the central part of the device is covered by a medium, while the thermal actuators work inair. These future experiments have important implications for a better understanding of cell mechanics and related disease.

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