Magnetic fields with frequency of 217 Hz can reduce cell apoptosis caused by electrochemotherapy

Magnetic fields with frequency of 217 Hz can reducecell apoptosis caused by electrochemotherapy

M. Mansourian1, S. Mohammad P. Firoozabadi1, Z. Shankayi1 &Z. M. Hassan2

1Department of Medical Physics, School of Medical Sciences, Tarbiat Modares University,Tehran, Iran, and 2Department of Immunology, School of Medical Sciences,Tarbiat Modares University, Tehran, Iran

Nowadays, due to the wide use of mobile phones, extensive studies have been carried out on theeffects of magnetic field (MF) on public health. In this paper, we study the effect of 217Hz MFsimilar to that generated by GSM900 mobile phones on cancer and healthy cells treated withelectric pulse and cytotoxic drug. The experiments conducted include exposure to (a) electricpulses alone (4000 square-wave electric pulses with low amplitude of 70 V/cm and frequency of5 kHz), (b) electric pulses following MF exposure, (c) electrochemotherapy (electric pulses andcytotoxic drug) alone and (d) MF exposure with subsequent electrochemotherapy. The resultsindicate that the percentage of apoptosis decreases significantly (p , 0.05) in treatment groupsusing electrochemotherapy after MF exposure compared to that in treatment groups usingelectrochemotherapy alone. We observed that 217Hz MF similar to that generated by GSM900mobile phones can incur resistance of the cells in response to electric pulses. Our findingsimplied the existence of amplitude window effect in alternations induced by extremelylow-frequency MF.

Keywords: apoptosis, bleomycin, electroporation, magnetic field therapy

Introduction

Cancer is a major problem which affects public health. There are many differenttypes of therapeutic modalities including surgery, chemotherapy, radiotherapy andimmunotherapy, but they all have limitations. For instance, in chemotherapymodality, cytotoxic nonpermeant drugs are unable to diffuse through the plasmamembrane of intact cells. Electrochemotherapy is a new therapeutic approach toenhance uptake of nonpermeant cytotoxic drugs inside the cells using electric pulses(Mir & Orlowski, 1999). In this approach, the control of electrical parameters iscritical for simultaneously obtaining cell permeabilization and cell survival (Sersaet al., 2008). Recent studies have shown that pulsed electrical fields can be used toinduce death of cells. Cell death might occur through either apoptosis or necrosis(Hengarther, 2000). Apoptosis is the process of programmed cell death which is

Correspondence: S. M. P. Firoozabadi, Department of Medical Physics, School of Medical Sciences,Tarbiat Modares University, Tehran, Iran. Tel: þ 98 21 82883821. Fax: þ 98 21 88006544.E-mail: [email protected] 16 January 2012; revised 25 May 2012; accepted 29 June 2012

Electromagnetic Biology and Medicine, 32(1): 70–78, 2013Q Informa UK LtdISSN: 1536-8378 print / 1536-8386 onlineDOI: 10.3109/15368378.2012.708693

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characterized by distinct morphological characteristics including blebbing, cellshrinkage, nuclear fragmentation, chromatin condensation and chromosomalDNA fragmentation. In contrast to necrosis, which is a form of traumatic cell deaththat results from acute cellular injury and induces inflammatory reactions, apoptosiscauses death of cells that can quickly be removed by phagocytosis before thecontents of the cell can spill out onto surrounding cells and cause damage.Therefore, apoptosis is considered as a suitable method for cancer therapy (Russo,Terrasi, & Agnese, 2006).

In the past, several studies have indicated that strong electric fields(.4.5 kV/cm) reduce cell survival through mild apoptosis as well as severenecrosis. On the other hand, relatively low-voltage electric fields (0.2 kV/cm)demonstrate more apoptosis and less necrosis. Thus, electrochemotherapy usinglow voltages would be suitable for targeted anticancer treatment because itdecreases undesirable side effects such as severe inflammatory reaction due tonecrosis (Matsuki, Ishikawa, Imai, & Yamaguchi, 2008). In this regard, Shankayi andothers examined the antitumor effectiveness of low-voltage amplitude electro-chemotherapy (4000 pulses of 100ms duration at 5 kHz repetition frequency with70V/cm) (Shankayi & Firoozabadi, 2011; Shankayi, Firoozabadi, & Hssan, 2010).This protocol of treatment inhibiting tumor growth using low voltage and highfrequency resulted in reduction of discomfort and pain which arise from musclecontractions during treatment. In fact, the standard electrochemotherapy protocolin clinic has used a train of high-amplitude rectangular pulses with 1Hz repetitionfrequency for treatment of patients. By this protocol, patients experience anunpleasant sensation during pulse delivery, which is mainly attributed to musclecontractions provoked by high-amplitude and low-frequency pulses (Miklavcicet al., 2005; Mir, 2006; Mir et al., 2006; Pucihar, Mir, & Miklavcic, 2002; Sersa et al.,2008). Shankayi and others observed in vivo, low-electric field and high-frequencyelectroporation by bleomycin is more effective and considerable in reducing andeliminating invasive ductal carcinoma transplanted into Balb/c mice (Shankayi &Firoozabadi, 2011; Shankayi et al., 2010).

Nowadays, due to the wide use of mobile phones, extensive studies have beencarried out on the effects of magnetic fields (MFs) generated by handsets on publichealth. Global system for mobile communications (GSM) is already one of the mostcommon technologies in mobile phone. Pulsed magnetic fields (PMFs) withfrequency of 217Hz are transmitted during time division multiple access (TDMA)mode of operation of GSM handsets. In the GSM system, the TDMAmode causes thehandset battery to be switched on during short bursts of transmission that in turnproduces current variation and generates MF. This means that the handset issurrounded by extremely low-frequency (ELF) magnetic fields. As ELF radiationfrom handsets is thought to have lower intensity than that produced by theradiofrequency (RF) component, not much attention was paid to the sole influenceof this exposure (Krewski et al., 2007; Repacholi, 2001). Therefore, studiesinvestigating biological effects of radiation emitted by mobile phones have mainlyfocused on the RF emissions from handsets (Hamblin & Wood, 2002; Perentos, Iskra,McKenzie, & Cosic, 2007). The effects of ELF magnetic field generated by mobilephones have been the subject of only some studies (Cook et al., 2005; Czyz et al.,2004; Kaviani Moghadam, Firoozabadi, & Janahmadi, 2009).

Most of the people, including cancer patients, use mobile phones that emit ELFmagnetic fields into their users. Thus, it is of interest to examine whether such an ELFmagnetic field interferes with their treatment. In the previous study, we researchedthe effect of acute exposure to 217Hz MF similar to that emitted by mobile phoneson cell apoptosis treated with chemotherapy. Our results show that 217Hz MF by

Effect of magnetic field on electrochemotherapy 71

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itself can induce apoptosis in K562 cells at intensities of 120 and 159.4mT. Moreover,such a MF led to a minor increase (insignificant) in apoptosis percentage when cellswere treated with chemotherapy drug (bleomycin) after MF exposure at 93.25mT(Mansourian, Firoozabadi, Hassan, & Shankayi, 2011).

To date, no published studies have examined the effect of 217Hz MF of mobilephones on the efficiency of cancer treatment with electrochemotherapy. Thus, thepresent study aimed to investigate whether the 217HzMFs similar to those generatedbymobile phones are capable of causing any changes in the sensitivity of cells treatedwith electric pulse and cytotoxic drug and altering apoptosis percentage of cells.

Materials and methods

CellsThe human erythroleukemia K562 cell line (this cell line is derived from a chronicmyeloid leukemia patient) was grown in RPMI-1640 medium complemented with10% fetal bovine serum (FBS), 160mg/ml L-glutamine (all from Invitrogen/Gibco,Carlsbad, CA, USA), 100 units/ml penicillin and 16mg/mg gentamicin in thesuspension culture. The cells were cultured at 37 8C in a 5% CO2 incubator at 90%humidity.

Another biological system used in our study was human lymphocytes which play acentral role in the immune responses and are well known from a biological point ofview. Human peripheral blood was taken from donors and lymphocytes wereisolated using Ficoll Hypaque (Sigma Chemical Co., Saint Louis, MO, USA) (Vissers,Jester, & Fanton, 1988). Then, the lymphocytes were resuspended in RPMI-1640medium supplemented with 10% FBS.

MF exposure systemThe 20-cm diameter coils, which included 287 turns of 0.78-mm-diameter insulatedcopper wire, were separated by 10 cm. They were connected to a 217-Hz signalgenerator (made in Bioelectromagnetic Laboratory of Tarbiat Modares University)and a homemade power signal amplifier. The MF had duty cycle of 13% andfrequency of 217Hz. Pulses were generated for 0.577ms; every 4.6ms resulted in217Hz pulses (217Hz ¼ 1/4.6ms). The shape of the pulse magnetic field wasevaluated using BioLab software (Figure 1). Flux densities of the MF were measuredusing a Tesla Meter (TES-1394; TES Electrical Electronic Corp., Thedford, Ontario,Canada).

MF exposure of cellsCells were centrifuged and resuspended in the culture medium, at a concentration of1.5 £ 106 cells/ml. Of these cells, 450 were transferred to small petri dishes. They

Figure 1. The shape of the pulse magnetic field (0.576ms pulse duration, 217Hz frequency).

72 M. Mansourian et al.

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were placed between a pair of Helmholtz coil, and PMFs were applied (Figure 2). Allexperiments were carried out at 25 8C, 5% CO2.

Cells were exposed to three different flux intensities of MF (93.25, 120 and159.4mT) for 10min (Kaviani Moghadam, Firoozabadi, Lak, & Janahmadi, 2008;Mahrour et al., 2005). These intensities are consistent with those used in otherstudies (Sage, Johansson, & Sage, 2007). All flux densities are given as root meansquares. The intensity of field measured at all points of the petri dish was the same.One minute after MF exposure, the cells were treated with chemotherapy,electroporation or electrochemotherapy in independent groups. Also, three groupsof cells were exposed to MF without any treatment. For all the treatments, onegroup was considered as the control group if it was under similar experimentalconditions compared with the other groups but without any MF exposure ortreatment.

In this research, we used low-voltage electrical pulses (4000 pulses, 100ms square-wave electric pulses of 70 V/cm amplitude with repetition frequency of 5 kHz) for thecell electropermeabilization in electroporation and electrochemotherapy treatments(Shankayi & Firoozabadi, 2011). By using a pulse generator (ECT-SBDC made inBioelectromagnetic Laboratory of Tarbiat Modares University), low-intensity pulseswere fed to the cell suspension using parallel stainless steel electrodes separated by1 cm, yielding a uniform electric field.

Electrochemotherapy of the cells was carried out by adding 0.1mM externalconcentration of bleomycin immediately after pulse application (never .60 s afterthe end of pulse application; Pavlin et al., 2005). Such a concentration of bleomycinwhich is less than standard clinical doses of drug can reduce the degree of toxicityand other side effects such as hyperpigmentation or alopecia (hair loss).

After treatment, the cells were put into six-well plates. Then, they were incubatedfor 24 h. All experiments were carried out at 25 8C and 5% CO2.

Cell apoptosis assayTreated cells (450 cells for each assay) were centrifuged for 5min at 300g and themedia were removed. Binding buffer (500ml) that contains an optimal concentrationof calcium which is required for Annexin V binding to phosphatidylserine (PS) on thecell surface, Annexin V (5ml) that is a specific PS-binding protein that can be used todetect apoptotic cells and propidium iodide solution (5ml) were added to eachsample. The samples were kept for 5min in darkness before evaluation. Afterward,the percentage of apoptosis was assessed by FACSCalibur flow cytometer (BectonDickinson, USA) using the 488 nm line of the argon ion laser (Figure 3).

Figure 2. A schematic representation of the exposure of cells by magnetic field.


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StatisticsEach experiment was repeated three times on different days. The resultsare expressed as mean ^ SD of data obtained for independent experiments.Statistical analysis was done using independent Student’s t-test. A value of p,0.05was considered to be statistically significant.

Results

Electroporation and electrochemotherapyAnalysis of our data showed that the application of electric field strength of 70 V/cmusing 4000 electric pulses and 5 kHz repetition frequency to cells can inducesignificant apoptosis compared with control groups in both types of cells.Furthermore, electrochemotherapy with a combination of bleomycin and electricfield exhibited statistically significant difference compared with electroporation

Figure 3. An example of a flow cytometer plot in the evaluation of apoptosis percentage. Cells inlower left quadrant can be regarded as viable nonapoptotic cells, the cells in upper left quadrant arenecrotic cells. Upper right and lower right quadrants show apoptotic cells. (A) Control group,(B) electroporation group and (C) electrochemotherapy group.

Figure 4. Percentage of apoptosis in (B) K562 cell line and ( ) lymphocyte cells treated withelectroporation (EP) and electrochemotherapy (ECT). The value of the control group apoptosis wasscaled to 100 and the apoptosis of other experimental groups was computed as the percentage ofcontrol apoptosis.



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group only in K562 cells. These treatments had more effect on K562 cells than onlymphocyte cells as shown in Figure 4. Also, necrosis was not observed in any of thecell types. The value of apoptosis of the control group was scaled to 100 and theapoptosis of other experimental groups was computed as the percentage of controlapoptosis.

MF and electroporationThe next part of this study was carried out with the purpose of investigating whetherMF can change the resistance of the cells in response to electric pulses and so theefficiency of electroporation. The results shown in Figure 5 demonstrate thatelectroporation of the cells could be affected by means of MF. In lymphocyte cells,percentage of apoptosis was significantly less in groups treated with electroporationafter MF exposure at 93.25 and 120mT than in groups treated with electroporationwithout any MF exposure (p, 0.05). Similar decrease in percentage of apoptosiswas observed for K562 cell line, but it occurs only at the intensity of 120mT.

Figure 5. Percentage of apoptosis in (A) K562 cell line and (B) lymphocyte cells exposed to MFexposure and electroporation (EP): ( ) control group without any exposure; (A) groups treated withelectric pulse with no MF exposure and (B) cells exposed to MF and electric pulses. The value of thecontrol group apoptosis was scaled to 100 and the apoptosis of other experimental groups wascomputed as the percentage of control apoptosis), *p, 0.05.

Figure 6. Percentage of apoptosis in (A) K562 cell line and (B) lymphocyte cells exposed to MF withsubsequent electrochemotherapy (ECT) treatment: ( ) control group without any exposure;(A) groups treated with electrochemotherapy without MF exposure and (B) cells exposed toMF andthen to electrochemotherapy treatment. The value of the control group apoptosis was scaled to 100and the apoptosis of other experimental groups was computed as the percentage of controlapoptosis, *p, 0.05.


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MF and electrochemotherapyThe main purpose of this study was to investigate the influence of 217Hz MFs similarto that generated by GSM900 mobile phones on electrochemotherapy. Thus, weanalyzed the percentage of apoptosis in cells treated with electric pulse (amplitude of70 V/cm and frequency of 5 kHz) and bleomycin after exposure to MFs of variousintensities. As shown in Figure 6, MF exposure before the electrochemotherapy ofcells could produce alteration in cell apoptosis percentage at some of the intensities.Induced apoptosis for lymphocyte cells was significantly reduced at the intensities of93.25 and 159.4mT. A similar result was obtained for K562 cell line when the appliedintensity was 159.4mT. In this cell line, MF exposure before electrochemotherapydecreased the apoptosis percentage. Apoptosis at 159.4mT was reduced to the extentthat it was significantly fewer than apoptosis at 93.25 and 120mT. In these twointensities, apoptosis was reduced but it was not significant.

Discussion

Recent years have witnessed wide use of mobile phones and enormous attentionabout its effect on human health. This effect has raised concerns about publicexposure to radiation emitted from cell phones and the possible interaction betweensuch radiation and the biological effects on human tissues, particularly the brain andthe human immune system. Many research studies have indicated a link betweenelectromagnetic field (EMF) radiation and negative biological effects. For instance,Hardell, Carlberg, & Hansson Mild (2006) and Repacholi (1997) have reported risk ofdeveloping brain tumor due to the exposure to EMF radiation generated by cellphones. Also, Salford et al. (1994) have confirmed that blood–brain barrier functioncould be affected by cell phone radiation and Phillips et al. (1998) have observedDNA damage due to exposure to EMF radiation.

As it was mentioned before, cell phones are surrounded by ELF magnetic fields.These fields may affect treatment of cancer cells by electrochemotherapy. Our resultsindicate a decrease in apoptosis percentage caused by electrochemotherapyfollowing 217Hz MF exposure. These findings can clarify one of the most importantbiological effects of 217Hz MF similar to that generated by GSM900 mobile phones.Electric fields generate depolarizing and hyperpolarizing transmembrane potentialsacross the cell. They lead to the formation of pores when electrical membranebreakdown occurs (Matsuki et al., 2008). Apoptosis can be induced by electricalpulses based on change in the membrane integrity, the micropore formation and theactivation of caspase enzymes. The fact that the cells show resistance to electric pulsesuggests that 217Hz MF can modify cell membrane such that fewer pores werecreated. This modification can be applied to dielectric constant, electric resistance orconductivity of cell membrane because electroporation depends on these factors(Faurie et al., 1979).

The other important finding in the present study is the observation of the effect ofMF only at some of the intensities. In fact, we did not observe effects to continuallyincrease with increasing MF amplitude or to decrease with decreasing MFamplitude. The ELF magnetic field exposures affect the apoptosis of cells in anonmonotonic manner. This event can be described by “window effect” of MFswhich indicates targets inside biosystem respond only to the electromagnetic waveswith some discrete frequency or intensity range (Haile et al., 2008).

Although the effects of mobile phone RF fields on cancer especially on thecarcinogenesis and tumor promotion have been studied previously, the effect of ELFmagnetic field from mobile phones on cancer and its treatment has been lessregarded. In the present study, we considered 217Hz field similar to that generated



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by GSM900 mobile phones as a factor influencing cancer cell treatment. Althoughthe possibility of a link between rate of using mobile phones and modification ofcancer treatment efficiency is difficult, our results encourage further research toobtain consequences leading to guidelines for cancerous patients using mobilephones such that their treatment efficiency is not influenced. To achieve suchguidelines, it is essential that more similar studies be performed with the otherradiation intensities of mobile phones with the frequency of 217Hz. Furthermore, inaddition to 217HzMF, other ELF frequencies of mobile phones such as 8.34 and 2Hzmust be tested. Also, we propose similar experiments on the effect of 217Hz MFmobile phones on various types of cancer cells and on other treatment methods ofcancer cells in vitro and in vivo.

In conclusion, we observed that 217Hz MFs similar to that generated by GSM900mobile phones can induce apoptosis in cancer cells and incur resistance of the cellsin response to electric pulses. Our data were obtained on cells in culture and shouldbe considered as an experimental basis for prompting studies at the in vivo level.

Declaration of interest

This paper is from a M.Sc. thesis that was supported by grants from Tarbiat ModaresUniversity. The authors report no conflicts of interest. The authors alone areresponsible for the content and writing of the paper.

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Magnetic fields with frequency of 217 Hz can reduce cell apoptosis caused by electrochemotherapy

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