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Mutagenesis vol. 18 no. 5 pp. 439-443, September 2003
© 2003 UK Environmental Mutagen Society/Oxford University Press

Induction of kinetochore-positive and kinetochore-negative micronuclei in CHO cells by ELF magnetic fields and/or X-rays

Gui-Rong Ding1,2, Takehisa Nakahara1 and Junji Miyakoshi1,3

1Department of Radiological Technology, School of Health Sciences, Faculty of Medicine, Hirosaki University, 66-1 Hon-cho, Hirosaki 036-8564, Japan and 2Department of Radiation Medicine, Fourth Military Medical University, Xi’an 710032, China


   Abstract
Top
 Abstract
Introduction
 Materials and methods
 Results
 Discussion
 References
 
To test the genotoxic effects of extremely low frequency (ELF) magnetic fields, the induction of micronuclei by exposure to ELF magnetic fields and/or X-rays was investigated in cultured Chinese hamster ovary (CHO) cells, using the cytokinesis block method. Micronuclei derived from acentric fragments or from whole chromosomes were evaluated by immunofluorescent staining using anti-kinetochore antibodies from the serum of scleroderma (CREST syndrome) patients. A 60 Hz ELF magnetic field at 5 mT field strength was applied, either before or after 1 Gy X-ray irradiation or without additional X-ray irradiation. No statistically significant difference in the frequency of micronuclei in CHO cells was observed between a sham exposure (no exposure to an ELF magnetic field) and a 24 h ELF magnetic field exposure. Exposure to an ELF magnetic field for 24 h before X-ray irradiation or for 18 h after X-ray irradiation did not affect the frequency of X-ray-induced micronuclei. However, the number of kinetochore-positive micronuclei was significantly increased in the cells subjected to X-ray irradiation followed by ELF magnetic field exposure, but not in the cells treated with ELF magnetic field exposure before X-ray irradiation, compared with exposure to X-rays alone. The number of spontaneous kinetochore-positive and kinetochore-negative micronuclei was not affected by exposure to an ELF magnetic field alone. Our data suggest that exposure to an ELF magnetic field has no effect on the number of spontaneous and X-ray-induced micronuclei. However, ELF magnetic field exposure after but not before X-ray irradiation may somehow accelerate X-ray-induced lagging of whole chromosomes (or centric fragments) in CHO cells.


   Introduction
Top
 Abstract
 Introduction
Materials and methods
 Results
 Discussion
 References
 
Increasing interest has recently been focused on the health effects of extremely low frequency (ELF) magnetic fields produced by power lines and household electrical appliances. A possible association between ELF magnetic field exposure and cancer has been suggested, but has not been demonstrated unequivocally (Wertheimer and Leeper, 1979Go; Savitz and Loomis, 1995Go; Linet et al., 1997Go).

In order to find explanations for the possible increased cancer risk associated with ELF magnetic field exposure and to elucidate the underlying mechanisms, in vivo and in vitro studies have been performed on the genotoxic effects of ELF magnetic fields. These effects include the induction of chromosomal aberrations and sister chromatid exchange. Some papers have provided positive data linking these effects to ELF magnetic field exposure. For example, Yaguchi et al. (1999, 2000Go) showed that exposure to ELF magnetic fields could induce chromosomal aberrations or sister chromatid exchange in mouse m5S cells. Lai and Singh (1997Go) reported that a 2 h exposure of rats to a 60 Hz magnetic field (flux densities of 0.1, 0.25 and 0.5 mT) caused a dose-dependent increase in DNA strand breaks in brain cells. When HL-60 cells were exposed to a 45 mT ELF magnetic field, apoptotic cell death, characterized by cell shrinkage, nuclear fragmentation and cleavage and fragmentation of internucleosomal DNA was induced (Narita et al., 1997Go). In contrast, other literature suggests that ELF magnetic fields do not cause chromosomal aberrations or DNA damage (Rosenthal and Obe, 1989Go; Frazier et al., 1990Go; Antonopoulos et al., 1995Go; Miyakoshi et al., 2000Go). These reports have suggested that ELF magnetic fields cannot directly damage DNA and that any relationship between an increased incidence of cancer and ELF magnetic field exposure can be explained by the promotion of cellular transformation or by the action of a co-carcinogenic factor.

The micronucleus assay is a simple cytogenetic test that is based on the detection of small ancillary nuclei in mitotically dividing cells. A distinct advantage of this assay is that micronuclei can be generated as a consequence of both structural chromosome damage and incorrect chromosomal distribution (Lynch et al., 1993Go). Micronuclei derived from chromosome breakage and those derived from errors in chromosome distribution can be discriminated from each other by visualizing kinetochores in micronuclei (Hennig et al., 1988Go). It can be achieved by immunofluorescent staining using anti-kinetochore antibodies from the serum of scleroderma (CREST syndrome) patients (Horvathova et al., 1997Go). Recently, Simko et al. (2001Go) reported that during exposure to a 50 Hz, 1 mT magnetic field, application of benzopyrene (BP) resulted in a 1.8-fold increase in micronucleus formation in Syrian hamster embryo cells, compared with treatment with BP alone. The aim of the current study was to evaluate the genotoxic effects of ELF magnetic fields on X-ray induced micronuclei with or without kinetochores (kinetochore-positive and kinetochore-negative micronuclei) in cultured Chinese hamster ovary (CHO) cells.


   Materials and methods
Top
 Abstract
 Introduction
 Materials and methods
Results
 Discussion
 References
 
Cell cultures
CHO-K1 cells were obtained from the Japanese Cancer Research Resource Bank, Tokyo. The cells were maintained in Ham’s F-12 medium (Nikken, Osaka, Japan) supplemented with 10% fetal bovine serum (Gibco BRL) at 37°C in an atmosphere of 95% air and 5% CO2. For each experiment, a new vial of frozen cells was thawed.

Chemicals
The cytokinesis blocking reagent cytochalasin B (Nacalai Tesque Inc.) was dissolved in dimethylsulfoxide (DMSO) (Nacalai Tesque Inc.) at a concentration of 2 mg/ml and stored at –20°C. A concentration of 3 µg/ml cytochalasin B was used in the experiment. Anti-kinetochore serum was purchased from Antibodies Inc. and the fluorescein isothiocyanate (FITC)-conjugated goat anti-human IgG was bought from Sigma.

ELF magnetic field exposure system and X-ray irradiation
The exposure apparatus for a 5 mT ELF magnetic field has been described elsewhere (Miyakoshi et al., 1994Go). Briefly, the background environmental 60 Hz ELF magnetic field during the sham exposure was <0.5 µT. The atmosphere in the incubator for both units was saturated with humidified 95% air and 5% CO2. X-ray irradiation was performed using a Hitachi MBR-1520 operating at 150 kVp, 20 mA with 0.5 mm Al and 0.1 mm Cu filters and a dose rate of 0.98–1.02 Gy/min.

Exposure procedure
Approximately 4 x 105 cells were plated in 10 cm dishes, following sham exposure or exposure to an ELF magnetic field for 24 h. The cells were irradiated by X-rays (1 Gy) and, after irradiation, cytochalasin B was added to the medium at a final concentration of 3 µg/ml. The cells were then exposed to an ELF magnetic field or placed in a sham exposure incubator for 18 h, which is 1.5 times the length of their cell cycle. The cells were then harvested (Figure 1).



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  		Fig. 1. Schematic presentation of the treatment regime of the CHO cell cultures.

 
Slide preparation
Following the above treatment, the cells were detached using 0.1% trypsin and 0.02% EDTA and resuspended in Ham’s F-12 medium at a concentration of 2.5 x 104 cells/ml. An aliquot of 0.4 ml of the cell suspension was added to each tube of a cytocentrifuge (Cytospin; Shandon Southern Ltd) and spun down onto clean slides at 900 r.p.m. for 5 min. The preparations were then fixed in pre-chilled 70% ethanol for 30 min.

Immunofluorescence staining
After washing in phosphate-buffered saline (PBS) and blocking with 1% bovine serum albumin, the slides were incubated in a humidified incubator for 1 h at 37°C with CREST sera diluted to 1:50 in PBS. After three washes in PBS, the slides were incubated at 37°C for 30 min with FITC-conjugated goat anti-human IgG diluted to 1:100 in PBS. After three washes in PBS, the preparations were counterstained with propidium iodide (0.2 µg/ml) and mounted in 90% glycerol.

Micronucleus/kinetochore scoring
The slides were coded and scored blind under a 400x magnification using a fluorescence microscope (Olympus). Both the PI stained binucleated cells and the FITC stained kinetochores could be identified using the same optical set-up. Only binucleated cells were scored for micronuclei. Identification of micronuclei was made according to the following criteria: (i) the micronucleus is distinctly separated from the two parental nuclei; (ii) the size of the micronucleus is smaller than 1/3 the size of the main nuclei; (iii) the presence or absence of a kinetochore signal in micronuclei was assessed; (iv) 1000 binucleated cells per treatment group were analyzed and, where possible, when a binucleated cell with a micronucleus was observed, the micronucleus was classified as either kinetochore-negative or kinetochore-positive. If there were more than two micronuclei in one binucleated cell, they were not counted. Only one scorer took part in the analysis, and three independent experiments were performed.

Statistics
A comparison of the percentages of micronuclei and kinetochore-positive micronuclei was performed by the {chi}2 test and P <= 0.05 was considered to be statistically significant.


   Results
Top
 Abstract
 Introduction
 Materials and methods
 Results
Discussion
 References
 
Representative images of kinetochore-labeled CHO cells using the anti-kinetochore antibody technique are shown in Figure 2a and b. The kinetochore appears as a yellow dot against the red nucleus. The presence of a kinetochore spot indicates the centromere region of each chromosome.



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  		Fig. 2. Cytokinesis-blocked CHO cells labeled with kinetochore antibodies. (a) Binucleated cells and a kinetochore-negative micronucleus are indicated. (b) A kinetochore-positive micronucleus is shown.

 
Figure 3 shows the number of binucleated cells that were carrying micronuclei (<=2) after exposure of the cells to magnetic fields and/or X-rays. No statistically significant difference in the frequency of binucleated cells carrying micronuclei was observed between the sham exposure and the 24 h ELF magnetic field exposure. Following X-ray irradiation, the number of binucleated cells carrying micronuclei increased significantly (P < 0.01). Exposure to an ELF magnetic field for 24 h before X-ray irradiation (designated M+X) or for 18 h after X-ray irradiation (X+M) did not affect the frequency of X-ray-induced micronuclei.



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  		Fig. 3. Percentage of micronucleated binucleated cells induced in CHO cells after exposure to an ELF magnetic field with or without X-ray irradiation. Data represent the mean ± SE of three independent experiments. M, 5 mT magnetic field; X, X-rays at 1 Gy.

 
As shown in Figure 4, among the micronuclei induced by X-ray irradiation, only a small number were kinetochore-positive (~4%). The ratio of kinetochore-positive micronucleated CHO cells increased significantly in the X+M or M+X+M (exposure to ELF magnetic field before and after X-ray irradiation) treated cells (P < 0.05), but not in the M+X treated cells, compared with treatment with X-rays alone. The frequency of spontaneous kinetochore-positive and kinetochore-negative micronuclei was not modified by exposure to an ELF magnetic field alone. The percentages of kinetochore-positive micronuclei in the cells sham treated or treated with an ELF magnetic field were ~38.4 and 39.8%, respectively.



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  		Fig. 4. Percentage of kinetochore-positive micronuclei induced in CHO cells after exposure to an ELF magnetic field with or without X-ray irradiation. Data represent the mean ± SE of three independent experiments. *P < 0.05 compared with 1 Gy treatment. M, 5 mT magnetic field; X, X-rays at 1 Gy.

 

   Discussion
Top
 Abstract
 Introduction
 Materials and methods
 Results
 Discussion
References
 
In the current study, we showed that exposure to a 5 mT ELF magnetic field alone could not induce micronuclei in CHO cells. This result agrees with most of the data available in the literature regarding EMF genotoxicity (McCann et al., 1998Go). In sham exposed cells, ~40% of the micronuclei were kinetochore-positive, which is similar to the data reported by Degrassi and Tanzarella (1998Go). Exposure to an ELF magnetic field has no effect on the number of spontaneous kinetochore-positive and kinetochore-negative micronuclei. Our data indicate that both spontaneous chromosomal aberrations and numerical changes are involved in the spontaneous production of micronuclei in CHO cells and that a 5 mT ELF magnetic field exposure alone has no effect on this process. After X-ray irradiation, most of the micronuclei were kinetochore-negative, which confirms the clastogenic properties of X-rays. However, a small excess of kinetochore-positive micronuclei was also observed, suggesting that X-rays have a slight aneugenic potential. It can also be envisaged that the kinetochore-positive micronuclei contain a centric fragment, i.e. the chromosome has been broken at the centromere and the kinetochore proteins have followed the centric fragment to the micronuclei, although kinetochore-positive micronuclei are usually considered to represent micronuclei with whole chromosomes, because the kinetochore is associated with the centromere. An increase in the frequency of X-ray induced kinetochore-positive micronuclei in X+M and M+X+M treated CHO cells, but not in M+X treated cells, was also observed in this study. The number of kinetochore-positive micronuclei in the X+M and M+X+M treated cells did not differ. The data suggest that, in CHO cells, exposure to an ELF magnetic field after, but not before, X-ray irradiation may somehow accelerate X-ray-induced lagging of whole chromosomes (or centric fragments) in CHO cells.

Several epidemiological studies have suggested that ELF magnetic fields produced by power lines and household electrical appliances are associated with an increased incidence of cancer. According to the NIEHS (1998Go), power line frequency magnetic fields are classified as a possible carcinogen, but it is generally accepted that direct genomic interactions with ELF electric or magnetic fields is unlikely, because of the low energy of the fields. However, exposure to magnetic fields applied vertically in the Merritt coil system for 72 h was shown to increase the formation of micronuclei in human amnion cells (Simko et al., 1998Go). Under our experimental conditions, we failed to find any significant direct effect of exposure to an ELF magnetic field alone on micronucleus induction in CHO-K1 cells, which supports the suggestion that ELF magnetic fields act as a promoter or as a co-carcinogenic factor in previously initiated cells. Several in vitro and in vivo models have been investigated to examine this hypothesis and have yielded different results (Juutilainen et al., 2000Go). Some reports have shown that the genotoxic potential of certain mutagens, including ionizing radiation, may be affected by co-exposure to an ELF magnetic field. The formation of transformed foci in C3H/10T 1/2 cells treated with phorbol ester has been reported to be enhanced after magnetic field exposure (Cain et al., 1993Go) and cells irradiated with {gamma}-rays showed increased chromosomal aberrations when they were exposed to an EMF (Hintenlang, 1993Go). However, many negative findings have also been reported. Using transformed K562 human lymphocytes, Khan et al. (1992Go) showed that, after 2.3 Gy {gamma}-ray irradiation, exposure to a 30 mT magnetic field for 1 h failed to affect the level of micronuclei, which is consistent with our data.

Recently, it has been argued that aneuploidy is a primary cause of cancer (Li et al., 1997Go; Duesberg et al., 1998Go; Duesberg, 1999Go). Aneuploidy may contribute to tumor development by causing abnormal changes in the number of genes and resultant genetic instability. Because it is generally considered that micronuclei containing kinetochore proteins are formed by lagging of whole chromosomes, the frequency of kinetochore-positive micronuclei can be used as a marker of aneuploidy induction (Eastmond and Tucker, 1989Go). Induction of lagging chromosomes has generally been attributed to a malfunction in the spindle apparatus, such as disruption of the microtubules (Eastmond and Tucker, 1989Go). However, it was also reported that kinetochores may be detached from the chromosome and might thus appear in a micronucleus together with a fragment (Sgura et al., 2001Go). By using a combined anti-kinetochore antibody and FISH staining with pancentromeric probes, Sgura et al. (2001Go) found that X-rays induce aneuploidy in primary human fibroblasts through a non-DNA damage mechanism. Since X-rays are a powerful clastogen, it is possible that chromosome fragments may also have been included in the number of lagging chromosomes scored in the current study. However, the results still indicate that, following X-ray irradiation, ELF magnetic fields can induce aneuploidy. This, in turn, provides a better understanding of a possible mechanism through which ELF magnetic fields can induce carcinogenesis.


   Acknowledgements
 
The authors thank Miss M.Yoshida for her technical assistance. This study was supported, in part, by the Research for the Future Program, Japan Society for the Promotion of Science and The Ministry of Education, Science, Sports and Culture, Japan.


   Notes
 
3To whom correspondence should be addressed. Tel: +81 172 39 5964; Fax: +81 172 33 2830; Email: miyakosh@cc.hirosaki-u.ac.jp


   References
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 Abstract
 Introduction
 Materials and methods
 Results
 Discussion
 References
 

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Received on January 22, 2003; accepted on June 26, 2003.


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