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Electrochemical Behavior of MCF-7 Cells on Carbon NanotubeModified Electrode and Application in Evaluating the Effect of5-FluorouracilKun Chen, Jinhua Chen,* Manli Guo, Zhenfeng Li, Shouzhuo Yao*

State Key Laboratory of Chemo/Biosensing and Chemometrics, College of Chemistry and Chemical Engineering, Hunan University,Changsha, 410082, P.R. China*e-mail: chenjinhua@hnu.cn

Received: January 10, 2006Accepted: March 30, 2006

AbstractThe electrochemical behavior of human breast cancer cells (MCF-7) suspension on multiwalled carbon nanotube(MWCNT) modified graphite electrode was studied by using cyclic voltammetry (CV) and potentiometric strippinganalysis (PSA). Compared with bare graphite electrode, the MWCNTs-modified electrode showed electrocatalyticproperty to the oxidation of electroactive species in the cell suspension. One oxidative peak at about þ0.74 V wasobserved in the cyclic voltammogram. PSA was proved to be more sensitive than CV for investigation of theelectrochemical behavior of cells. And it was found that ultrasonication treatment of the cell suspension cansignificantly enhance the PSA signal. Factors influencing the PSA signal of cells, including deposition time, depositionpotential and stripping current, were investigated in detail and the optimum conditions were obtained. The baselinecorrected PSA signal was found to be related to the viability of cells and the technique was used for monitoring thegrowth of MCF-7 cells. The effect of anticancer drug 5-fluorouracil (5-FU) on the growth of MCF-7 cells was alsoinvestigated by PSA.

Keywords: Cyclic voltammetry, Potentiometric stripping analysis, MCF-7 cells, Cell viability, 5-Fluorouracil

DOI: 10.1002/elan.200603503

1. Introduction

Cell biological functions generally relate to cell viability,which is traditionally evaluated by morphological observa-tion under a microscope or by biological technology.Electrochemical technologies have been approved to beeffective to provide nonmorphological observation meth-ods for following cell health state and evaluating effective-ness of drugs or chemical compounds. Scanning electro-chemical microscopy (SECM) [1 – 2], electrochemical im-pedance spectroscopy (EIS) [3], electric cell-substrateimpedance sensing (ECIS) [4 – 7] and oxygen electrode[8 – 10] could provide useful information on cell health statein cell culture course and can be used to evaluate theeffectiveness of chemical compounds because the electrodebehavior of cells has positive relation with cell viability.Recently, the voltammetric behavior of living cells has

been recognized and the anodic peak current was found torelate with cell metabolic viability in the culture course,which provides a simple and inexpensive electrochemicalmethod for monitoring the cell growth and evaluating theeffect of chemicals on cells [11 – 13]. However, the anodicpeak currents in cyclic voltammograms of cells weregenerally weak. Potentiometric stripping analysis (PSA), apowerful electroanalytical technique including preconcen-tration of the analyte by electrodeposition and stripping of

the analyte at an appropriate current, has been proved to bemore sensitive than CV for studying the electrochemicalbehavior ofMCF-7 cells and has beenused to investigate thecytotoxic effect of diosgenin [14]. However, the PSA signalreported in that workwas very weak. Searching formethodsto improve the electrochemical response signal seems to beof great importance.Modification of the working electrode surface can en-

hance the sensitivity and selectivity once a judicious choiceof the modifier has been made [15]. Carbon nanotubes(CNTs) as the quintessential nanomaterial have alreadycompiled an impressive list of superlatives since theirdiscovery in 1991 [16]. Because of their unique topologicallycontrolled electronic properties, CNTs have been widelyused in electrochemical investigations, for instance, in directelectrochemistry of proteins [17], construction of electro-chemical sensors and biosensors [18 – 19], electrocatalysis[20 – 21], and electrodematerials in batteries [22]. However,according to our knowledge, the electrochemical behaviorof mammalian cells on CNTs modified electrode hasscarcely been reported and whether the chemically modi-fied electrode can enhance the electrochemical responsesignal is still unclear.In this work, the electrochemical behavior of human

breast cancer cells (MCF-7) suspension was investigated onmultiwalled carbon nanotube modified graphite electrode

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by using CV and PSA techniques. Factors influencing thePSA signal of cells, including deposition time, depositionpotential and stripping current, were optimized. The growthof cells during the culture course and the cytotoxic effect of5-fluorouracil (5-FU) was investigated by using the PSAmethod and the electrochemical resultswere comparedwithmorphological observation.

2. Experimental

2.1. Chemicals

Multiwalled carbon nanotubes (MWCNTs, 10 – 20 nm indiameter) were purchased from Shenzhen Nanotech PortCo., Ltd (Shenzhen, China). Prior to use, the MWCNTswere purified by refluxing in concentrated nitric acid for 8 h,followed by filtering, rinsingwith double-distilled water anddrying. 5-Fluorouracil (5-FU) was a product of Sigma.Phosphate-buffered saline (PBS) solution consisting of136.7 mM NaCl, 2.7 mM KCl, 9.7 mM Na2HPO4 and1.5 mM KH2PO4 was used in the experiments. A stocksolution of 5-FU (5.0 mM) was prepared with PBS andsterilized through filtration by using a 0.22 mm filter (What-man). All other chemicals were of analytical grade.

2.2. Apparatus

CV and PSA experiments were performed with a CHInstrument Model 660A-electrochemical analyzer (Shang-hai Chenhua Apparatus Company, China) and a conven-tional three electrode system. Graphite rod encapsulated inepoxy resin, modified with MWCNTs, was used as theworking electrode, with a saturated calomel electrode(SCE) as the reference electrode and a platinum electrodeas the auxiliary electrode. All measurements were carriedout in a 10-mL detection cell and the temperature was keptaround 37 8C. All potentials measured in this report werewith respect to SCE.

2.3. Cell Culture

MCF-7 (cell line of humanbreast cancer) cells were culturedin flasks in RPMI-1640 (Gibco) with 10% heat-inactivatednewborn calf serum, 100 IUmL–1 penicillin and 100 mgmL–1

streptomycin at 37 8C in a humidified atmosphere contain-ing 5% CO2. For investigating the effect of 5-FU, the cellswere firstly allowed to settle and grow for 24 h afterinoculation. Then fresh culture medium was supplied and5-FU solution was added. For electrochemical measure-ments, the cells cultured inRPMI-1640medium for differenttimewere gently rinsed with PBS for three or four times andthen collected through trypsinization with 0.25% trypsin-0.02% EDTA. Upon proper dilution with PBS, a cellsuspension was obtained. The viability of cells was deter-mined byTrypan blue dye exclusion test and cell densitywas

estimated with a hemocytometer. The morphology of cellsduring the culture course was observed by a culturemicroscope (Olympus CKX41).

2.4. Procedures

The graphite electrode surface (0.16 cm2) was hand-polish-ed with fine emery paper, and washed with double-distilledwater before use. The MWCNT film was constructed viacasting 12 mL 0.5 mg mL–1 MWCNT suspension in double-distilled water onto the surface of graphite electrode. Afterbeing carefully rinsed with water, the MWCNTs-modifiedelectrode was immersed in PBS and electrochemicallytreated by cyclic voltammetry in the potential range from0.0 to 1.0 V vs. SCE until a stable voltammogram wasobtained. Then the modified electrode was transferred tothe cell suspension in PBS and electrochemical measure-ments were carried out. For PSA, the derivative signal (dt/dE) was used as the analytical signal.

3. Results and Discussion

3.1. Voltammetric Behavior of MCF-7 Cells

Figure 1 shows the typical cyclic voltammograms of MCF-7cells at bare and MWCNTs-modified graphite electrodes.No redox peaks can be observed at both electrodes in thepotential range of 0.0 and 1.0 V in PBS without cells (curvesa and c). Thebackground current of theMWCNTs-modifiedelectrode is apparently larger than that of the bare graphiteelectrode, which is due to the enhanced effective surfacearea of the modified electrode. When the measurementswere performed in the presence of freshly collected MCF-7cells, an oxidative peak at about þ0.74 Vappears (curve d)at theMWCNTs-modified electrode.While at bare graphiteelectrode, the anodic current increases slightly from 0.6 V,but no obvious oxidative peak can be observed (curve c).The observed phenomena show that MWCNTs haveelectrocatalytic property to the electrochemical oxidationof electroactive species in the MCF-7 cell suspension. Nocorresponding reduction peak waves were observed in thereversal scans, which indicate a clear irreversible voltam-metric character of the cell suspension. Many previousstudies proposed that the voltammetric response of cells hadrelation with some enzymes [11, 13, 23]. But the intrinsicreason for cell voltammetric behavior still waits for furtherinvestigation.

3.2. PSA Signal of MCF-7 Cells

Potentiometric stripping analysis (PSA) has been proved tobe more suitable for studying the electrochemical behaviorof MCF-7 cells than cyclic voltammetry because theelectroactive species of interest are preconcentrated onthe working electrode [14]. Concentrations of analytes in

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solution are obtained from potential-time curves recordedat constant currents. WhatLs more, the time is the physicalparameter measured in potentiometric stripping that can bemeasured with high accuracy, precision and resolution. ThePSA signals of freshly collected MCF-7 cells on bare andMWCNTs-modified graphite electrodes are shown in Fig-ure 2. The PSA signal of cells on MWCNTs-modifiedelectrode (curve c) is significantly sharper and higher thanthat on bare graphite electrode (curves a), which indicatesthat MWCNTs accelerate the irreversible electron transferbetween cells and the electrode surface.The PSAmeasurement was repeated for many times on a

MWCNTs-modified graphite electrode in the same cellsuspension (prior to each measurement, the solution wasmagnetically stirred to avoid the aggregation of cells), andan interesting phenomenonwas observed.With the increaseofmeasurement time, thePSAsignal first decreased slightly,and then increased gradually until a plateau was reached.The probable reason is that the electroactive speciescorresponding to the PSA signal are not only exist on cell

membrane but also intracellularly existed. Under continu-ous electrostimulation andwith the increase of time, the cellpermeability changed. Due to the irreversible electrodeprocess, extracellular electroactive species were firstlyoxidized and the PSA signal faded. At the same timeintracellular electroactive species were slowly released,which provided a supplement to the diminished items,resulting in the gradual increase of PSA signal. However,the process was rather time consuming and thus ultra-sonication treatment of the freshly collected cells wasperformed prior to PSA measurement, which also cangreatly enhance cell permeability. As can be observed fromFigure 2, after ultrasonication, the PSA signals on bothelectrodes increase significantly (curves b and d).In order to investigate the effect of ultrasonication time

on the PSA signal, the cell suspension (with certain cellnumber) was put into a sonication bath and PSA measure-ment was performed at different time intervals. As shown inFigure 3, with the increase of ultrasonication time, the PSAsignal increases until a climax is obtained at 90 min. Furtherultrasonication doesnLt benefit the increase of the PSAsignal obviously. The cell suspension was observed under amicroscope prior to eachmeasurement and itwas found thatno whole cells existed when the suspension had beenultrasonicated for 90 min. So in the following experiments,in order to obtain themaximum electrochemical signals, thecell suspensions were ultrasonicated till nowhole cells couldbe observed prior to each measurement.

3.3. Electrode Behavior of Ultrasonicated MCF-7 Cells

Cyclic voltammetry is mainly used to investigate thereversibility and kinetic aspects of electrode reactions.Cyclic voltammograms at different scan rates of the ultra-sonicatedMCF-7 cells onMWCNTs-modified electrode areshown in Figure 4. With the increase of the scan rate from 2to 200 mV s–1, the anodic peak potential moves positivelyand the peak current increases. In order to evaluate thecharacteristics of the electrode redox processes, the rela-

Fig. 1. Cyclic voltammograms at bare (a, b) and MWCNTs-modified (c, d) graphite electrodes in PBS in the absence (a, c)and presence (b, d) of MCF-7 cells. Cell density, 1.8� 106 cellsmL–1; scan rate, 50 mV s–1.

Fig. 2. The baseline corrected chronopotentiograms of freshlycollected (a, c) and ultrasonicated (b, d) MCF-7 cells on baregraphite electrode (a, b) and MWCNTs-modified graphite elec-trode (c, d). Experimental conditions: deposition potential, 0.0 V;deposition time, 400 s; stripping current, 40 mA. Cell density: 1.8�106 cells mL–1.

Fig. 3. Effect of ultrasonication time on PSA peak signal. Celldensity: 5� 105 cells mL–1.

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tions of DEp� ln v and ln Ip�DEp were examined. Theequations are:

DEp¼ 0.0767þ 0.0159 ln v r¼0.9942 (1)

ln Ip¼�12.15þ 34.7968 DEp r¼ 0.9893 (2)

Where DEp (V) is the difference between the peakpotentials at a certain scan rate and 10 mV s–1, v (V/s) isthe scan rate, Ip (A) is thepeak current. FromEquation1and2, the relationship between Ip and v is:

Ip¼ 7.64� 10�5 v0.5533 (3)

Based on the experimental results and principle describedby Bard and Faulkner [24], these results show that theelectrode redox process of ultrasonicated MCF-7 cells istotally irreversible. And the number of the electronsinvolved in the rate determining step is from 2.88 to 1.81,which were calculated from RT/2bnbF¼ 0.0159 and bnbF/RT¼ 34.7968, respectively. b is the transfer coefficient andb¼ 0.5 is chosen, nb is the number of the electrons involvedin the rate determining step.

3.4. Factors Influencing the PSA Signal of MCF-7 Cells

The parameters of PSA, including deposition time, deposi-tionpotential and stripping current, were optimized in detailand the experimental results are shown in Figure 5. It can beobserved from Figure 5a that PSA signal increases withdeposition time,while it do not increasemuchwhen the timeis longer than 400 s. Therefore, a deposition time of 400 s isselected. To choose an appropriate stripping current, weexamined the influence of different stripping current (20, 40,60, 80, 100 and 200 mA) on PSA signal. As shown inFigure 5b, the PSA signal decreases with the increase ofstripping current. When the stripping current is larger than200 mA, the stripping time is so short that no obvious signalcan be found, while the PSAcurves are not smoothwhen the

stripping current is smaller than 40 mA. Therefore, although20 mA has higher PSA signal, 40 mA is selected as theoptimal stripping current. Thedepositionpotentials of�0.2,0.0, 0.2, 0.4 and 0.6 V were also investigated. As shown inFigure 5c, with the increase of deposition potential, the PSAsignal decreases and no obvious PSA signal can be observedwhen the deposition potential is applied at 0.6 V. The reasonfor the effect of deposition potential on thePSA signal is stillnot clear. On the other hand, at�0.2 V the PSA curve is notsmooth and the baseline is much higher compared with0.0 V. So during accumulation period, the applied potentialof 0.0 V is preferred.

Fig. 4. Cyclic voltammograms of ultrasonicated MCF-7 cells onMWCNTs-modified electrode at different scan rates. From a) tof), scan rate: 200, 100, 50, 10, 5 and 2 mV s–1.

Fig. 5. Influence of the experimental conditions on PSA signal ofultrasonicated cells. a) deposition time (deposition voltage, 0.0 V;stripping current, 40 mA), b) stripping current (deposition voltage,0.0 V; deposition time, 400 s); and c) deposition voltage (deposi-tion time, 400 s; stripping current, 40 mA). Cell density: 1.8� 106

cells mL–1.

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3.5. Description of Cell Growth

The ability of PSA method for monitoring the growth ofcells was tested in this work. In our experiment,MCF-7 cellswith the samedensity (1� 105 cellsmL�1)were inoculated inmany flasks and cultured under the identical condition.When the cells had been allowed to settle and grow for 24 h,fresh culturemediumwas supplied to each flask and the cellswere cultured continuously. At every time interval duringthe cell culture course, three flasks of cells were taken outand the cells were harvested for PSA measurements.Figure 6 shows the relative PSA signal of MCF-7 cells

during the culture course with no nutrient replenished. Theinitial time for PSA measurement was recorded when thefresh culture medium was added. With the increase ofculture time, the PSA signal increases gradually until amaximum value is reached, and then decreases sharply. Theinitial increase of PSA signal with the culture time is causedby the proliferation of cells. In cell culture, nutrients areimportant in maintaining cell viability. When the cells arecultured continuously in the CO2 incubator for longer timewithout any fresh nutrient replenished, the viability of cellscan undoubtedly be affected, which is confirmed by the factthat more and more cells become blue in Trypan blue dyeexclusion test and lots of cells float in the medium. So thedecrease of PSA signal in Figure 6 is related to the decreaseof cell viability. These results indicate that the baselinecorrected PSA signal can represent cell viability and be usedfor monitoring the growth of cells.

3.6. Effect of Anticancer Drugs

5-FU is one of the most potent anticancer drugs, and itscytocidal effect is considered to be induced by inhibitingDNAsynthesis and/or bybeing incorporated intoRNA[25].In this work, 5-FU was selected as a model of anticancerdrug and its cytocidal effect on MCF-7 was investigated byusing the PSA technique. The inoculated MCF-7 cells wereallowed to settle and grow for 24 h, then fresh culture

medium was supplied and 5-FU was added. Figure 7 showsthe relative PSA signals of MCF-7 cells incubated in thepresence of 0.0, 0.5, 5.0 and 50.0 mM 5-FU for 24 and 48 h,respectively. At 24 h, the PSA signals of cells incubated inthe presence of 0.0 and 0.5 mM 5-FU are identical, whichindicates that the effect of 0.5 mM 5-FU on the viability andproliferation of cells is not obvious. Additionally, with theincrease of 5-FU concentration from 0.5 to 50.0 mM, thePSA signal decreases obviously. While at 48 h the effect of0.5 mM 5-FU on cell growth can be observed clearly and thedifference between the PSA signals of cells incubated in theabsence and in the presence of 5-FUbecomesmore striking.A control experiment was also performed to investigatewhether 5-FU in the detection solution has effect on thePSA signal of the cell suspension. No obvious change of thePSA signal has been observed after the addition of 5-FUwith a final concentration of 50.0 mM. Therefore, thedecrease of PSA signal is mainly due to the antiproliferativeeffect of 5-FU on the cells.The cytotoxic effect of 5-FU on MCF-7 cells was further

confirmed by morphological observation and the corre-sponding images of cells incubated in the presence of 0.0 and5.0 mM 5-FU for 24 h and 48 h are shown in Figure 8. It canbe observed that when incubated in the absence of 5-FU, thecells proliferate well and the number of cells increasesgradually (images b and d), which is consistent with theincrease of PSA signal shown in Figure 7 (column a). Whilethe proliferation and viability of cells is significantlyinhibited in the presence of 5.0 mM5-FU as can be observedfrom images c and e. The number of cells exposed to 5.0 mM5-FU at 24 and 48 h is much smaller than that of the cellsincubated in the absence of 5-FU, which results in smallerPSA signal (column c in Fig. 7). In the presence of 5.0 mM5-FU, the cell morphology changes at 24 h (image c) and somedead cells floating in the culturemedium can be observed at48 h (image e). Reduction of cell population and morphol-ogy change represent the positive effects of an anticancerdrug.The above results indicate that thePSAmethod can beused to evaluate the cytocidal effect of 5-FU.

Fig. 6. Growth curve of the MCF-7 cells described by therelative baseline corrected PSA signal. Cell inoculation density:1� 105 cells/mL. The initial time was recorded when the cells wereallowed to settle and grow for 24 h.

Fig. 7. Effects of a) 0.0, b) 0.5, c) 5.0, and d) 50.0 mM 5-FU onMCF-7 cells. The initial time was recorded when 5-FU was added.

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4. Conclusions

In this work, a marvelous PSA signal of ultrasonicatedhuman breast cancer cells MCF-7 can be observed atMWCNTs-modified graphite electrode. The PSA signalrelates to the viability of cells during the culture course.Additionally, the PSA method is successfully applied formonitoring the effect of 5-FU on the growth ofMCF-7 cells.The combination of PSA technique and electrode modifi-cation with nanomaterials is very helpful to the enhance-ment of electrochemical signals ofmammalian cells, which isbeneficial for the monitoring of cell growth and assessmentof chemical cytotoxicity.

5. Acknowledgements

This work was supported by the Scientific ResearchFoundation for the Returned Overseas Chinese Scholars,State Education Ministry (2001-498), the National NatureScience Foundation of China (20335020, 20275009 and20575019) and the Basic Research Special Program of theMinistry of Science and Technology of China(2003CCC00700).

Fig. 8. Microscope images of MCF-7 cells treated with 0.0 (a, b, d) and 5 mM (a, c, e) 5-FU for 0 h (a), 24 h (b, c) and 48 h (d, e). Theinitial time was recorded when the cells were allowed to settle and grow for 24 h.

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